A meta-analysis on the prevalence of resistance of Staphylococcus aureus to different antibiotics in Nigeria

Christian Kelechi Ezeh; Chibuzor Nwadibe Eze; Marie Esther Uju Dibua; Stephen Chijioke Emencheta

doi:10.1186/s13756-023-01243-x

A meta-analysis on the prevalence of resistance of Staphylococcus aureus to different antibiotics in Nigeria

Ezeh, Christian Kelechi; Eze, Chibuzor Nwadibe; Dibua, Marie Esther Uju; Emencheta, Stephen Chijioke 2023-04-25 00:00:00 Background Rapid emergence of multidrug resistant Staphylococcus aureus has resulted to difficulty in treatment of infections caused by such strains. The aim of this meta-analysis study was to determine the pooled prevalence of resistance of S. aureus to different antibiotics in Nigeria. Methods Literature search for studies was done using Google scholar, PubMed, Science direct, and African Journal Online. The prevalence of S. aureus resistance to different antibiotics was evaluated using the meta-analysis propor - tion command in MedCalc software version 20.0 adopting a rand effect model. I statistic and Egger test in MedCalc was used to evaluate the heterogeneity and the presence of publication bias among studies respectively. Results A total of 40, 682 studies were retrieved through the database search of which 98 studies met the study inclusion criteria. Prevalence of resistance of S. aureus to different antibiotics ranges from 13 to 82%. Results showed a very high degree of resistance to penicillin G (82% [95% confidence interval (CI) 61%, 0.96%]), cloxacillin (77% [95% CI 64%, 88%]), amoxacillin (74% [95% CI 66%, 81%]), cefuroxime (69% [95% CI 51%, 85%]), ampicillin (68% [95% CI 53%, 81%]). Moderately resistance to erythromycin (47% [95% CI 40%, 53%]), chloramphenicol (47% [95% CI 37%, 56%]), methicillin (46% [95% CI 37%, 56%]), ofloxacin (24% [95% CI 18%, 31%]) and rifampicin 24% [95% CI 6%, 48%]). Low resistance was observed in vancomycin 13% (95% CI 7%, 21%). For each individual meta-analysis, high heterogeneity was observed with I range (79.36–98.60%) at p-values ≤ 0.01). Egger’s tests for regression intercept in funnel plots indicated no evidence of publication bias. Conclusion This meta-analysis study established that S. aureus in Nigeria has developed resistance to commonly used antibiotics such as the beta-lactam class antibiotics, sulphonamides, tetracyclines, chloramphenicol, and vanco- mycin. Hence it is imperative to develop programs to promote rational use of antimicrobial agents, infection preven- tion and control to reduce the incidence of antimicrobial resistance. Keywords Antibiotic resistance, Meta-analysis, Nigeria, Staphylococcus aureus Background Staphylococcus aureus (S. aureus) is well adapted to vari- ous environments due to their metabolic versatility and *Correspondence: pharmic resistance ability. S. aureus colonize the skin Christian Kelechi Ezeh ezechristian.kelechi@gmail.com and nasopharyngeal membranes as normal microbiota Department of Microbiology, University of Nigeria, Nsukka, Enugu State, in healthy individuals [1]. However, they cause myriad of Nigeria detrimental infections when they invade the internal tis- Department of Pharmaceutical Microbiology, University of Nigeria, Nsukka, Enugu State, Nigeria sues or enter the bloodstream. S. aureus is an important © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 2 of 22 pathogen involved in both hospital-acquired and com- using the appropriate studies that rely solely on S. aureus munity-acquired infections and causes many infectious from the title. The prevalence of resistance of S. aureus to diseases ranging from mild skin and soft tissue infec- various routinely used antibiotics in Nigeria is a country tions, bones and joint infections, infective endocarditis, wide study as it covers studies from the six geo-political cardiovascular disorders, osteomyelitis, bacteremia, and regions of Nigeria. Meta-analysis was adopted because it fatal pneumonia in both healthy and individuals with is a quantitative study of pooled prevalence of resistance underlying diseases [2]. The high incidence of both com - of S. aureus to routinely use antibiotics in Nigeria. munity and nosocomial staphylococcal infections coin- cide with the emergence of multidrug resistant S. aureus which renders antibiotic treatments ineffective [3]. Search strategy S. aureus has become resistant to various antibiotics Electronic search engines including Google scholar, Pub- over the past years especially to the beta-lactam class Med, ScienceDirect, and African Journal Online (AJOL) of antibiotics [4]. Emergence of methicillin resistant were used to search for available studies from 23rd March S. aureus (MRSA) and vancomycin resistant S. aureus to May 2022. Relevant key words such as Staphylococcus, (VRSA) constitutes a serious global public health prob- antibiotic resistance, antibacterial resistance, antimicro- lem. Currently, VRSA and MRSA strains are classified bial resistance, drug resistance, drug susceptibility, Nige- as very potent and dangerous agents that can potentially ria were used during the search. These key words were cause devastating damage worldwide in the absence of used in different combinations (Staphylococcus OR S. effective treatment options [5]. aureus AND antibiotic resistance OR antibacterial resist- Various mechanisms of resistance utilized by S. aureus ance OR antimicrobial resistance OR drug resistance include: production of beta-lactamase enzymes to deac- AND Nigeria) in various electronic databases using the tivate beta-lactam antibiotics, efflux pump for extruding Boolean operators. The reference lists of included articles antibiotics such as tetracyclines [6], reduced accumula- were also check to identify studies relevant to the current tion of macrolides antibiotics [7], production of aminogly- study. cosides modifying enzymes to inactivate aminoglycoside antibiotics, alteration of DNA gyrase and topoisomerase IV expression of floroquinolones antibiotics, and expression of Inclusion and exclusion criteria Mec genes which alters penicillin binding proteins [8]. The titles of search results of all retrieved articles were In Nigeria, the prevalence of multi-drug resistant path- screened independently by two authors with the aim of ogens continue to be on the increase due to several fac- including studies that address the research question. The tors such as drug misuse, self medication, lack of trained articles were inserted into Zotero version 5.0.95.1 refer- medical personnel, and poverty. As the world battles encing application which helped in detecting duplicate the persistent rise in antimicrobial resistance (AMR), it articles. The title of the study which solely focused on is pertinent that adequate data and information about prevalence of antimicrobial resistance of S. aureus was AMR is known which can serve as the basic foundation grouped as eligible for inclusion. S. aureus resistance for setting out effective interventions to contain the cri - in any state in Nigeria and studies only done in Nigeria sis of AMR. From the literature, no prior meta-analysis represented in the title is the first criteria for inclusion. has been done on S. aureus resistance to different anti - However, studies that focused on many microbial strains biotics routinely use in Nigeria. Due to the various infec- antimicrobial resistance were excluded. tions caused by S. aureus, it is pertinent to determine In general, retrieved studies selected from predefined the pooled prevalence of resistance of S. aureus to vari- criteria were screened further using the inclusion cri- ous routinely used antibiotics in Nigeria. This will help teria: studies that were research articles and used cross in improving treatment options and enlighten the popu- sectional design, studies that used human samples, stud- lace on the menace and the possible cause of treatment ies that conducted antimicrobial susceptibility tests using failures due to the increasing rise of multidrug resistant the Clinical Laboratory Standard Institute (CLSI) guide- strains. The aim of this meta-analysis was to determine lines, studies written in English language and studies with the pooled prevalence of S. aureus resistance to various full text. routinely used antibiotics in Nigeria. Exclusion criteria in this meta-analysis include: studies conducted on non-human samples, studies with isolates below 20, duplicate studies, studies that did not conduct Methods antimicrobial susceptibility tests using the Clinical Labo- Study design ratory Standard Institute (CLSI) guidelines studies not Meta-analysis was adopted to evaluate the prevalence of written in English, and review articles. S. aureus of resistance to various antibiotics in Nigeria E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 3 of 22 Data extraction the study is considered as having no significant influence Relevant data such as name of author (s) and publica- on the overall estimate and vice versa. tion year, study design, study place, clinical sample size, isolate source, total number of Staphylococcus aureus Results isolates tested in each research article, and total No. of Characteristics of included studies isolates resistant each antibiotics. In situations where the Studies search record from electronic databases yielded proportion of susceptible isolates was reported, then the 40, 682 of which 35, 400, 2, 180, 1,706, and 1396 were No. of resistant Staphylococcus aureus isolates was cal- from Google scholar, AJOL, PubMed, and Science Direct, culated by subtracting the percentage susceptibility from respectively. Articles from Google Scholar gave 35,400 100 and then dividing the result by 100 and multiplying results comprising of many studies irrelevant or that does to the total number of isolates. However, in situation not fit to the study aim; hence, they were screened ran - where the proportion of the resistant isolates was given, domly from titles alone. Screening of the titles reduced then the No. of resistant Staphylococcus aureus isolates the number of eligible articles to 134 for full text assess- was calculated by dividing the proportion of the resistant ment. After going through the full texts, 36 articles were isolates by 100 and multiply with the total number of iso- excluded (reported small number of isolates and iso- lates. The formula is given as thus: lates not from human samples). Thus, 98 studies met the number of resistant isolates Prevalence of resistance(%) = × 100 (1) total number of isolates To ascertain the reporting of all relevant information inclusion criteria of the study (Fig. 1). in this meta-analysis, we followed the Preferred report- About 46, 640 S. aureus isolates were tested against ing Items for Systematic Review and Meta-analysis different antibiotics and 23,048 isolates were resistant to (PRISMA) [9] (Additional file 1: S1) guidelines. various antibiotics. Isolates sources include: nasal, blood, vaginal, ear, wound, urine, throat, pimples, hand, and mixed samples were collected from both symptomatic patients [61] and asymptomatic people [37]. Eighty six Statistical analysis procedures studies used primary data while twelve used records from In this meta-analysis, statistical analyses were performed hospitals. The characteristics of each study included is using MedCalc statistical software version 20.0.1. The summarized Table 1. pooled prevalence of antibiotic resistance of S. aureus was evaluated using the meta-analysis proportion com- Heterogeneity survey and publication bias mand in MedCalc. A total of 23 separate meta-analyses The included studies were conducted in the six geo-polit - were carried out to evaluate the pooled prevalence of S. ical zones of Nigeria; a total of 98 studies comprising of aureus resistance to 23 different antibiotics. Between 6 26 from South South, 23 South West, 20 South East, 18 and 77 studies were included in the 23 different meta- North West, 8 North Central and 3 North East. Quality analyses. I statistic command in MedCalc was used to assessment (risk of bias) was done in line with the follow- evaluate the heterogeneity among the included stud- ing criteria: studies which used CLSI guideline for anti- ies. Random effect and fixed effect are two models used biotic resistant assessment, studies that used more than to estimate pooled prevalence in meta-analysis. In this 20 S. aureus isolates and studies that used adequate sam- study, due to the characteristically high heterogeneity of ple representative of the region where testing was done. the included studies, the random effect model was used Agar diffusion based method was used to determine the for meta-analysis at 95% CIs. Egger test was employed for resistance level of S. aureus isolates in all included stud- assessing the presence of publication bias [10]. ies. High heterogeneity was observed for each of the The Freeman-Tukey double arcsine transformation was meta-analyses performed with I ranging from 79.36 used to ensure studies which report proportions near or to 98.60%; at p-values ≤ 0.01). This is due to vast differ - at 0 and 1 were not being excluded. In addition, studies ence in sample sizes; some studies used 20 isolates while that report unusually high prevalence of resistance when some used 400 isolates which impacted on the resistance compared to others, a sensitivity analysis was perform profile of each antibiotic. Also, number of clinical sam - by removing the studies. If the point estimate of pooled ples and recovered S. aureus isolates differ in all studies prevalence after removing a study that reported unusu- and these disparities resulted in high heterogeneity. More ally high prevalence of resistance lies within the 95% CI studies were conducted in the Southern (South South, of the overall pooled estimate for all studies combined, Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 4 of 22 Fig. 1 PRISMA flowchart for the selection and screening of eligible studies E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 5 of 22 Table 1 Characteristics of included studies Reference Study Study place Data type Setting and sample Sample size No of Antibiotics used source recovered isolates [11] Akortha and Iken- South south (Benin) Primary, Hospital: Nasal 52 20 CPR, TET, CHL, ERY, AMP, ebomeli, 2010 OFL [12] Idris et al., 2018 Northwest (Kano) Primary Hospital: Blood 195 MET, CPR, TET, ERY, GEN, CLIN, CEF [13] Stanley et al., 2013 Southsouth (Portha- Primary Hospital: Vaginal 265 74 MET, CPR, TET, ERY, AMP, court) swab GEN [14] Odu and Okonkwo, Southsouth (Portha- Primary Urban:Nasal 100 32 MET, CIPRO, TET, ERY, 2012 court) AMP, GEN, CLIN, CXC, COT, STR [15] Isibor and Otabor, Southsouth (Edo) Primary Urban: Nasal 100 32 AMO, CTR, CRX [16] Nworie, 2013 Southeast (Ebonyi) Primary Urban: Nasal 87 20 VAN, CPR, TET, ERY, AMP, OFL, GEN, COT, CTR [17] Egbuobi et al., 2014 Southeast (Imo) Primary Hospital: Different 200 76 MET clinical samples [18] Olowo-Okere et al., Northwest Primary Hospital: Wound 38 20 CPR, ERY, AMO, GEN, 2017 NOR [19] Olorode et al. 2021 Southsouth (Bayelsa) Primary Hospital: Different 250 25 MET, CPR, CHLERY, AMP, clinical samples AMO, GEN, RIF, STR, NOR [20] Onanuga and Southsouth (Bayelsa) Primary Hospital: Urine 200 46 VAN, CPR, TET, CHL, Awhowho, 2012 AMP, OFL, GEN, COT, AUG, CRX, CEF [21] Ayodeji and Omoniyi, Southwest (Ogun) Primary Hospital; Different 107 107 VAN, CPR, TET, ERY, AMP, 2009 clinical samples AMO, GEN, CXC, COT, STR, CAZ, PEN [22] Onanuga and Nortwest (Kaduna) Primary Urban: Urine 150 54 VAN, MET, CPR, AMP, Onaolapo, 2008 OFL, GEN, CLIN [23] Chigbu and Ezeronye, Southeast (Abia) Primary Hospital: Ear and 70 38 CPR, TET, CHL, ERY, AMP, 2003 nasal AMO, GEN, RIF, CXC, PEN [24] Enabule et al., 2007 Southsouth Primary Hospital: Urine 80 CPR, TET, ERY, AMP, GEN [25] Yah et al., 2009 Southsouth (Benin) Primary Hospital: Wound 153 86 CPR, TET, CHL, ERY, GENCXC, COT [26] Onwubiko and Saidiq, Northwest (Kano) Secondary Hospital: Different 150 CPR, TET, ERY, AMP, 2011 clinical samples AMO, OFL, GENCXC, STR, PEN, CAZ [27] Onanuga and Teme- SOuthsouth Primary Urban: Nasal 120 40 VAN, CPR, CHL, ERY, die, 2011 AMP, AMO, OFL, AUG, CRX, CEF [28] Onanuga et al., 2005 Northcentral (Abuja) Primary Hospital: Urine 150 60 VAN, MET, CPR, AMP, OFL, GEN, CLIN [29] Akanbi and Mbe, Northcentral (Abuja) Primary Hospital: Different 214 VAN, MET, ERY, AMP, 2013 clinical samples OFL, GEN [30] Terry et al., 2011 Nortwest Secondary Hospital: Different 194 MET, TET, CHL, ERY, clinical samples AMP, GEN, STR, CAZ, PEN, CTR [31] Iroha et al., 2012 Southeast (Ebonyi) Primary Hospital: Nasal 105 VAN, CPR, ERY, CLIN, CXC, COT, PEN [32] Eke et al., 2012 Southsouth (Edo) Primary Urban: Nasal and ear 100 39 MET, CPR, TET, AMP, PEN [33] Ekundayo and Southeast (Abia) Primary Hospital: Different 100 113 TET, CHL, ERY, AMP, Ndubuisi, 2015 clinical samples GEN, CXC, COT, AUG, STR, PEN [34] Obasuyi and Akerele, Southsouth (Edo) Secondary Hospital: Different 75 MET 2015 clinical samples Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 6 of 22 Table 1 (continued) Reference Study Study place Data type Setting and sample Sample size No of Antibiotics used source recovered isolates [35] Akerele et al., 2015 Southsouth (Edo) Primary Urban: Nasal 200 99 MET, CPR, ERY, AMP, AMO, GEN, STR, CTR [36] Badger-Emeka et al., Southeast 9Enugu) Primary Hospital: Wound 34 34 VAN, MET, TET, CHL, ERY, 2014 AMO, OFL, GEN, CXC, COT, AUG, STR [37] Ayeni et al., 2015 Southsouth (Bayelsa) Secondary Urban: Nasal 185 185 ERY, AMP, PEN, CTR, NOR [38] Torimino et al., 2012 Southwest (Oyo) Primary Urban: Different clini- 50 40 CPR, TET, CHL, ERY, cal samples AMO, OFL, GENCXC, COT, STR, CTR [39] Bale et al., 2019 Southwest (Kwara) Primary Urban: Nasal 113 42 TET, ERY, OFL, CXC, AUG, CTR, CTR [40] Adesoji et al., 2019 Nortwest (Katsina) Primary Urban: Different clini- 120 120 ERY, OFL, GEN, CXC, cal samples AUG, CAZ, CRX, CTR [41] Ariom et al., 2011 Southeast (Ebonyi) Primary Hospital: Different 709 84 MET, CPR, TET, GEN, clinical samples CAZ, PN [42] Ajani et al., 2020 Southwest (Ogun) Primary Urban: Nasal 200 20 MET [43] Olonrunfemi et al., Northcentral Primary Urban: Urine 217 73 MET [44] Onanuga et al., 2021 Northeast Primary Urban: Nasal 262 46 TET, ERY, AMO, GENCOT [45] Ramalan et al., 2020 Northcentral Primary Hospital: Urine 202 62 CPR, CHL, ERY, AMP, (Nasarawa) AMO, GEN, STR [46] Udobi et al., 2013 Northwest (Kaduna) Primary Hospital: Skin and 217 69 CPR, AMO, GEN, CTR wound [47] Obasola et al., 2010 Southwest (Oyo) Primary Urban: Different clini- 50 50 TET, CHL, ERY, AMO, cal samples GENCXC, COT, AUG [48] Moses et al., 2017 Southsouth (Uyo) Primary Hospital: Nasal 130 41 VAN, CPR, TET, ERY, GENCLIN, CEF [49] Nsofor et al., 2015 Southeast (Imo) Primary Urban: Nasal 270 152 TET, CHL, ERY, GEN [50] Adetayo et al., 2014 Southwest (Oyo) Primary Hospital: Different 150 66 VAN clinical samples [51] Ejikeugwu et al., 2018 Southeast (Ebonyi) Secondary Hospital: Different 39 ERY, GEN, CLIN, CXC, clinical samples CEF [52] Anucha et al., 2021 Southeast (Anambra) Primary Hospital: Urine 236 62 VAN, TET, ERY, AMO, OFL, GEN, CRX [53] Agwu et al., 2010 Southsouth (Edo) Primary Hospital: Wound 220 66 VAN, RIF, CRX, CTR [54] Adesida et al., 2016 Southwest (Lagos) Primary Urban: Nasal 230 50 ERY, AMO, OFL, GEN, CXC, CAZ, CRX, CTR [55] Mofolorunsho et al., Northcentral (Kogi) Primary Hospital: Different 100 22 CPR, TET, ERY, AMO, 2015 clinical samples OFL, GEN, COT, STR [56] Osiyemi et al., 2018 Southwest (Ogun) primary Hospital: Different 338 161 VAN, CPR, TET, ERY, OFL, clinical samples GEN, COT, AUG, CAZ, CEF, CTR [57] Ibe et al., 2014 Southeast (Abia) Primary Hospital: Different 84 69 MET clinical samples [58] Onaolapo et al., 2016 Northwest(Kaduna) Primary Hospital: Wound and 65 22 VAN, CPR, ERY, AMP, skin AMO, CLIN, CEF, CTR [59] Ugwu et al., 2016 Southsouth (Delta) Primary Urban: Nasal 300 218 MET [60] Tula et al., 2016 Northeast Primary Hospital: Different 100 45 CPR, AMO, OFL, GEN, clinical samples CXC, CAZ, CRX, CTR [61] Anyanwu et al., 2013 Northwest (Kaduna) Primary Hospital: Skin 400 69 VAN, CHL, CAZ, CTR [62] Onyeagwara et al., Southsouth (Edo) Primary Hospital: Nasal 50 25 CPR, ERY, AMP, AMO, 2014 GENSTR, CAZ [63] Ngwai and Bakare, Northcentral Primary Urban: Urine 300 60 CHL, TET, ERY, AMO, 2012 (Nasarawa) GENCXC, STR E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 7 of 22 Table 1 (continued) Reference Study Study place Data type Setting and sample Sample size No of Antibiotics used source recovered isolates [64] Umar et al., 2015 Nortwest (Kaduna) Primary Hospital: Skin and 40 34 CPR, CHL, ERY, AMO, nasal GEN, RIF, STR [65] Obajuluwa et al., 2015 Northwest (Kaduna) Primary Hospital: Wound and 100 39 VAN, CPR, ERY, AMP, skin AMO, GENCEF, CTR [66] Iduh et al., 2015 Southsouth Primary Hospital: Wound 300 64 TET, AMP, GEN, STR [67] Ibanga et al., 2020 Southsouth (Akwa- Primary Hospital Different 100 28 TET, CHL, ERY, AMO, Ibom) clinical samples GEN, STR [68] Emeakaroha et al., Southeast (Imo) Primary Urban: Nasal and 54 28 CHL, ERY, AMO, AMP, 2017 throat COT, CRX, PEN [69] Bisi-Johnson et al., Southwest (Oyo) Primary Hospital: Different 86 97 TET, CHL, AMP, AMO, 2005 clinical samples GENCXC, STR, PEN [70] Ayepola et al., 2015 Southwest (Lagos) Secondary Hospital:Nasal ` 217 TET, GEN, PEN [71] Odogwu et al., 2019 Northcentral (Abuja) Primary Hospital: Different 360 55 CPR, ERY, AMP, GEN, RIF, clinical samples CLIN, STR, TRIM [72] Adeiza et al., 2020 Northwest (Sokoto) Primary Hospital: Nasal 378 33 TET, CHL, ERY, GEN, CLIN, CAZ, CEF, TRIM [73] Ismail et al., 2015 Northeast (Borno) Primary Urban: Different clini- 110 42 CPR, CHL, ERY, AMO, cal samples GEN, RIF, STR, NOR [74] Ibrahim et al., 2018 Northwest (Kano) Primary Hospital: Wound 150 71 CPR, TET, ERY, GEN, and ear CLIN, CEF, TRIM, CTR [75] Olowe et al., 2013 Southwest (Ekiti) Primary Hospital: Different 208 VAN, MET, TET, ERY, clinical samples GEN, PEN, CEF [76] Oche et al., 2021 Northwest (Kano) Primary Hospital: Different 140 26 MET, CPR, TET, ERY, AM, clinical samples GEN, CEF, TRIM, NOR [77] Onelum et al., 2015 Southwest (oyo) Primary Hospital: Different 246 102 MET, CHL, GEN, CLIN, clinical samples CAZ, CEF [78] Akinduti et al., 2021 Southwest (Ogun) Primary Hospital: Different 256 68 VAN, CPR, TET, ERY, clinical samples AMO, OFL, GEN, CAZ, CRX, TRIM [79] Oladipo et al., 2019 Southwest (Osun) Primary Hospital: Different 25 MET, CPR, ERY, AMO, clinical samples GEN, OFL, CXC, CEF, CRX [80] Ogefere et al., 2020 Southsouth (Edo) Secondary Urban: Different clini- 556 MET cal samples [81] Motayo et al., 2012 Southwest (Ogun) Hospital: Different 50 MET, TET, CHL, ERY, clinical samples AMO, GEN, CTR [82] Onyeka et al., 2021 Southsouth (Rivers) Primary Urban: 150 78 ERY, OFL, GENCXC, AUG, CAZ, CRX, CTR [83] Ugwu et al., 2009 Southeast (Enugu) Primary Nasal 100 53 TET, CHL, AMO, GEN, COT, AUG [84] Nsofor et al., 2016 Southeast (Abia) Primary Hospital: Different 424 104 CPR, TET, CHL, ERY, AMP, clinical samples CAZ, PEN [85] Mbim et al., 2017 Southsouth (Cross Primary Hospital: Nasal 150 42 MET, CPR, CHL, ERY, river) AMO, GEN, RIF, CEF, NOR [86] Ogbolu et al., 2015 Southwest (Osun) Secondary Hospital: Different 116 VAN, TET, ERY, GEN, CAZ clinical samples [87] Osinupebi et al., 2018 Southwest (Ogun) Primary Hospital: Different 338 161 VAN, CPR, TET, ERY, OFL, clinical samples GEN, COT, AUG, CAZ, CEF, CTR [88] Ajoke et al., 2012 Northcntral (Plateau) Primary Urban: Nasal 200 98 TET, ERY, AMP, AMO, GEN [89] Onyebueke et al., Southeast (Enugu) Primary Hospital: Urine 818 89 CPR, ERY, AMO, GEN, 2019 STR, NOR Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 8 of 22 Table 1 (continued) Reference Study Study place Data type Setting and sample Sample size No of Antibiotics used source recovered isolates [90] Adetutu et al., 2017 Southwest (Ota) Primary Urban: Pimple 20 20 TET, CHL, ERY, GEN, CXC, COT, AUG, STR [91] Bale et al., 2021 Southwest (Kwara) Primary Hospital: Urine 856 56 MET, CPR, TET, CHL, ERY, AMO, OFL, GEN, AUG, CEF, CTR [92] Nmema, 2017 Southwest (Ondo) Primary Urban: Skin and nasal 80 34 ERY, GEN, CXC, AUG, CAZ, CRX, CTR [93] Ike et al., 2016 Southeast (Anambra) Primary Hospital: Nasal and 261 142 MET hand [94] Ugwu et al., 2015 Southeast (Anambra) Primary Hospital: Nasal 100 68 CPR, ERY, AMP, AMO, OFL, GEN, COT, STR, CTR [95] Emeka- Nwabunnia Southeast (Imo) Primary Urban:Different clini- 59 VAN et al., 2015 cal samples [96] Alli et al., 2012 Southwest (Osun) Secondary hospital: different 116 VAN, TET, ERY, AMO, samples GEN, CAZ [97] Sadauki et al., 2022 Northwest (Kano) Primary Hospital: Blood 214 40 MET, CPR, GEN, PEN, CTR [98] O’ Malley et al., 2015 Southwest (lagos) Primary Hospital: Different 73 38 TET, ERY, GEN clinical samples [99] Emeka- Nwabunnia Southeast (Anambra) Primary Hospital: Different 83 25 MET et al., 2019 clinical samples [100] Ako-Nai et al., 2005 Southwest (Osun) Primary Urban: Different clini- 112 CPR, TET, CHL, ERY, GEN cal samples [101] Frank-Peterside and Southsouth (Rivers) Primary Hospital: Different 50 VAN, MET Mukoro, 2010 clinical samples [102] Yahaya et al., 2022 Northwest (Kano) Primary Hospital: Different 200 31 CPR, CHL, ERY, CLIN, clinical samples COT, CEF [103] Onanuga et al., 2019 Southsouth (Bayelsa) Primary Urban: Nasal 390 47 CPR, TET, ERY, AMO, GEN, COT [104] Ogini and Olayinka, Southwest (Oyo) Primary Urban: Nasal 700 223 CPR, TET, ERY, AMO, 2021 GEN [105] Nwankwo et al., 2010 Northwest (Kano) Secondary Hospital: Different 185 MET, CPR, AMO, OFL, clinical samples GEN, CAZ, CTR [106] Olufunmiso et al., Southwest (Ogun) Primary Hospital: Different 200 200 ERY, OFL, GEN, COT, 2017 clinical samples AUG, CAZ, CRX, CTR [107] Olajide et al., 2012 Northwest (Kano) Secondary Hospital: Different 100 ERY, AMO.CRX, NOR clinical samples VAN Vancomycin; MET Meticilin; CPR Ciprofloxacin; TET Tetracycline; COT Cotrimoxazole; CHL Chloramphenicol; ERY Erythromycin; PEN Penicillin; CLIN Clindmycin; AMO Amoxicillin; AMP Ampicillin; GEN Gentamycin; CTR Ceftriaxone; AUG Amoxicillin/clavulanic acid; CAZ Ceftazidime; CRX Cefuroxime; CXC Cloxacillin; NOR Norfloxacillin; RIF Rifampicin; STR Streptomycin; OFL Ofloxacin; TRIM Trimethroprim; CEF Cefoxitin South West, and South East) part of Nigeria giving rise test rule which state that ‘P-value less than 0.05 indicates to high heterogeneity. Studies were done in different hos - the presence of publication bias’. pitals within these regions with different prevalence esti - mates. Random sampling was used in most of the studies Prevalence of S. aureus resistance to different antimicrobial and different clinical samples were collected. More than agents one clinical sample per patient was collected in 51 stud- In this meta-analysis, the pooled prevalence of S. aureus ies while one clinical sample was collected per patient in resistance to twenty-three different antibiotics and the 47 studies. Egger’s test for a regression intercept gave a number of studies included in each meta-analysis is sum- p-value range of 0.06 to 0.99, indicating no evidence of marized in Table 2. Prevalence of resistance of S. aureus to publication bias (Additional file 2: S2) following Eggers’ E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 9 of 22 Table 2 Pooled prevalence of S. aureus resistance to different antibiotics in Nigeria Antibiotics No. of studies Total No. of No. of resistant Pooled AMR prevalence I (P‑ value) isolates isolates (95% CI) (P ≤ 0.01) Vancomycin 29 2546 340 0.13 (0.7, 0.21) 96.60 Methicilin 30 3109 1445 0.46 (0.37, 0.56) 96.71 Ciprofloxacin 44 2739 838 0.31 (0.24, 0.38) 93.85 Tetracycline 43 3359 2170 0.65 (0.56, 0.76) 96.03 Cotrimoxazole 21 1293 855 0.66 (0.55, 0.76) 93.91 Chloramphenicol 32 2015 943 0.47 (0.37, 0.56) 95.03 Erythromycin 66 4969 2325 0.47 (0.40, 0.53) 95.31 Penicillin 15 1709 1396 0.82 (0.61, 0.96) 98.97 Clindamycin 12 787 275 0.35 (0.23, 0.49) 93.26 Amoxicillin 40 2167 1614 0.74 (0.66, 0.81) 94.64 Ampicillin 28 2074 1408 0.68 (0.53, 0.81) 97.91 Gentamycin 77 5470 1701 0.31 (0.25, 0.37) 95.90 Ceftriaxone 25 2144 943 0.44 (0.34, 0.54) 95.64 Amoxicillin/clavulanic acid 20 1665 1032 0.62 (0.50, 0.73) 95.76 Ceftazidim 24 2179 1329 0.61 (0.46, 0.75) 98.01 Cefuroxime 17 1035 714 0.69 (0.51, 0.85) 97.23 Cloxacillin 22 1565 1205 0.77 (0.64, 0.88) 97.13 Norfloxacillin 9 491 162 0.33 (0.17, 0.52) 95.27 Rifampicin 7 302 72 0.24 (0.06, 0.48) 95.19 Streptomycin 20 1287 579 0.45 (0.34, 0.57) 94.08 Ofloxacin 25 2058 494 0.24 (0.18, 0.31) 91.63 Trimethoprim 6 291 160 0.55 (0.35, 0.74) 91.99 Cefoxitine 21 1791 770 0.43 (0.31, 0.56) 96.61 Prevalence of resistance of S. aureus to beta‑lactams each antibiotic based on pharmacological classification is antibiotics given below for antibiotics routinely used in Nigeria. Estimation of the pooled prevalence of S. aureus resist- ance to penicillin antibiotics (penicillin G, methicillin, Prevalence of resistance S. aureus to rifamycins amoxicillin, cloxacillin, ampicillin, and amoxacilin/calu- (rifampicins) vanic acid are here presented. Resistance to penicillin G, Seven studies involving the prevalence of resistance amoxicillin, cloxacillin, ampicillin, and augmentin were to rifampicin was analyzed. The pooled prevalence of estimated based on 15, 40, 22, 28 and 20 studies respec- resistance of S. aureus to rifampicin in Nigeria is 24% tively. Pooled prevalence resistance rates were highest (95% confidence interval [CI] 6%, 48%). The forest plot in penicillin G at 82% (95% CI 61%, 96%). Resistance to (rifampicin) is presented in Fig. 2. cloxacillin [77% (95% CI 64%, 88%)], to amoxicillin [74% (95% CI 66%, 81%)], to ampicillin [68% (95% CI 53%, Prevalence of resistance of S. aureus to glycopeptides 81%)] and to amoxacilin/caluvanic [62% (95% CI 50%, (vancomycin) 73%)]. However, resistance rate was moderate for methi- The pooled prevalence of S. aureus resistance to van - cillin [46% (95% CI 37%, 56%)]. Forest plots for antibiot- comycin is 13% (95% CI 7%, 21%) and the forest plot is ics (methicillin and penicillin G) resistance are shown in presented in Fig. 3. Sensitivity results after exclusion of Fig. 4 and 5, respectively while the forest plots for amoxi- four studies [20, 22, 27, 36] that reported high prevalence cillin, ampicillin, amoxicillin/clavulanic acid and cloxa- of S. aureus resistant to vancomycin is 7% (95% CI 3.3%, cillin resistance are presented in Additional file 3: S3, 12%). Hence, there was significant decrease in poled prevalence. Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 10 of 22 Rifampicin at 95% CI Olorode et al, 2021 Chigbu & Ezeronye, 2003 Agwu et al, 2010 Umar et al, 2015 Odogwu et al, 2019 Ismail et al, 2015 Mbim et al, 2017 Total (random effects) 0.00.2 0.40.6 0.8 Proportion (24%) Po oled prevalence 0.24 (0.06, 0.48) I = 95.19 ( P ≤ 0.01) Fig. 2 Forest plot of the prevalence of S. aureus resistance to rifampicin Prevalence of resistance of S. aureus to floroquinolones Additional file 4: S4, Additional file 5: S5 and Additional Three antibiotics (ciprofloxacin, ofloxacin, and nor- file 6: S6 respectively. floxacilin) from floroquinolones were included in the Higher prevalence of resistance among cephalosporin study. For ciprofloxacin, 44 studies were used to esti- antibiotic was observed in cefuroxime 69% (95% CI 51%, mate the pooled resistance, 25 were used for ofloxacin 85%) followed by ceftazidime 61% (95% CI 46%, 75%). and 9 studies were used for norfloxacilin. The pooled Resistance to ceftriaxone is 44% (95% CI 34%, 54%) and prevalence of resistance of S. aureus to ciprofloxa- to cefoxitine is 43% (95% CI 31%, 546%). The forest plot cin [31% (95% CI 24%, 38%)], ofloxacin [24% (95% CI for ceftriaxone resistance is presented in Fig. 6 while the 18%, 31%)], and to norfloxacillin [33% (95% CI 17%, forest plots for cefuroxime and cefoxitine resistance are 52%)]. The forest plot for ofloxacin resistance is pre- presented respectively in Additional file 7: S7 and Addi- sented in Fig. 7 while the forest plot for ciprofloxacin tional file 8: S8. E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 11 of 22 Vancomycin at 95% CI Nworie et al, 2013 Onanuga & Awhowho, 2012 Ayodeji & Omoniy i, 2009 Onanuga &Temedie, 2011 Onanuga et al, 2005 Akanbi & Mbe, 2013 Iroha et al, 2012 Badger-Emeka et al, 2014 Moses et al, 2017 Anucha et al, 2021 Agwu et al. 2016 Osiy emi et al, 2018 Onaolapo et al, 2016 Any anwu et al, 2013 Obajuluwa et al, 2015 Olowe et al, 2013 Akinduti et al, 2021 Ogbolu et al, 2015 Osinupebi et al, 2018 Emeka-Nwabunnia, 2015 Alli et al, 2012 Frank-Peterside & Mukoro, 2010 Ogini & Olay inka, 2021 Onanuga & Onaolapo, 2008 Yah, 2007 Onwubiko & Sadiq, 2011 Terry et al. 2011 Ayeni et al. 2015 Olorunfemi et al. 2020 Total (f ixed effects) Total (random ef fects) 0.00.2 0.40.6 0.81.0 Proportion (13%) Pooled prev alence 0.13 (0.7, 0.21) I = 96.60% (p 0.01) Fig. 3 Forest plot of the prevalence of S. aureus resistance to vancomycin and norfloxacilin included in Additional file 9: S9 and [31% (95% CI 25%, 37%)]. The forest plot for chloram - Additional file 10: S10. phenicol resistance is presented in Fig. 8 while the forest plots for tetracycline, erythromycin, gentamycin, strep- Prevalence of resistance of S. aureus to protein synthesis tomycin, and clindamycin resistance are presented in inhibitors Additional file 11: S11, Additional file 12: S12, Additional Tetracycline a reversible protein synthesis inhibitor file 13: S13, Additional file 14: S14, and Additional file 15: showed the highest resistance rate [65% 995% CI 56%, S15 respectively. 76%)] followed by erythromycin (macrolides) [47% (95% CI 40%, 53%)] and chloramphenicol [47% (95% CI 37%, Prevalence of resistance of S. aureus to antimetabolites 56%)], respectively. Aminoglycosides (gentamycin and High resistance was observed among the antimetabolites streptomycin) and lincosamides (clindamycin) showed antibiotics. Pooled prevalence of S. aureus resistance to relatively lower level of resistance. The pooled prevalence cotrimoxazole was found to be 66% (95% CI 55%, 76%) of resistance to streptomycin [45% (95% CI 34%, 57%)], to and to trimethoprim is 55% (95% CI 35%, 74%). The for - clindamycin [35% (95% CI 23%, 49%)] and to gentamycin est plot for cotrimoxazole resistance is presented in Fig. 9 Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 12 of 22 Meth icilin at 95 % CI Id ris et al, 2018 Odu & Oknok wo , 2012 Eg buob i et al, 2 014 Olorod e et al, 202 1 On an ug a & On ao lapo , 2008 On an ug a & Temedie, 2011 Ak an bi & Mb e 2013 Terry et al, 2011 Ek e et al, 2012 Ob asuy i & Ak erele, 2015 Ak erele et al, 2015 Badger-Emek a et al, 201 4 Ario m et al, 201 9 Ajan i et al, 2020 Olorunfemi et al, 2020 Ad etay o et al, 2014 ib e et al, 201 5 ug wu et al 2016 Olowe et al, 2013 Oche et al, 2020 On elum et al, 2015 Olad ipo et al, 201 9 Og efere et al, 2020 Mo tayo et al, 2 012 Mb im et al, 2017 Bale et al, 2021 Ik e et al, 2 016 Sadauk i et al, 202 2 Frank-Petersid e & Muko ro, 2 010 Nwank wo et al, 2010 To tal (random effects) 0.00 .2 0.40 .6 0.81 .0 Pro portion (4 6%) Po oled prev alen ce 0.46 (0 .37, 0.56) I = 96.71 % (P ≤ 0.01 ) Fig. 4 Forest plot of the prevalence of S. aureus resistance to methicillin while the forest plot for trimethoprim is presented in ampicillin, cefuroxime, amoxacilin, cloxacillin, and penci- Additional file 16: S16. lin G. Comparison of the prevalence of S. aureus resistance Discussion to different antibiotics Antimicrobial resistance continues to be on the rise The trend of prevalence of S. aureus resistance to differ - which constitutes a serious public health problem glob- ent antibiotics addressed in this meta-analysis is shown ally. Many microbes have developed resistance to many in Fig. 10. From observation, the prevalence of resist- different antimicrobial agents over time. This meta- ance of S. aureus to the different antibiotics in this study analysis estimated the pooled prevalence of resistance ranges from 13 (vancomycin) to 82% (penicillin G). of Staphylococcus aureus to 23 different antibiotics rou - The order of resistance in increasing order based on tinely used in Nigeria. Ninety eight studies [98] were the pooled prevalence of S.aureus resistance to differ - included in this meta-analysis study with variation in the ent antibiotics was observed to be vancomycin, ofloxacin, number of studies included in each meta-analysis which rifampicin, ciprofloxacilin, gentamycin, norfloxacillin, clin - ranged from 6 to 77. In general, the 98 studies evaluated damycin, cefoxitine, ceftriaxone, streptomycin, methicillin, the rate of S. aureus resistance to different antibiotics chloramphenicol, erythromycin, trimethoprim, ceftazidim, based on 46,640 isolates of which 23, 048 were resist- amoxicillin-clavulanic acid, tetracycline, cotrimoxazole, ant to various antibiotics. Prevalence of resistance of S. E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 13 of 22 Penicillin at 95% CI Ayodeji & Omoniyi, 2009 Chigbu & Ezeronye, 2003 Onanuga et al, 2021 Terry et al, 2011 Iroha et al, 2012 Eke et al, 2012 Ekundayo & Ndubuisi, 2015 Ayeni et al, 2015 Ariom et al, 2019 Emeakaroha et al, 2017 Bisi-Johnson et al, 2005 Ayepola et al, 2015 Olowe et al, 2013 Oche et al, 2021 Sadauki et al, 2022 Total (random effects) 0.00.2 0.40.6 0.81.0 Proportion (82%) Pooled prevalence 0.82 (0.61, 0.96) I = 98.97 ( P≤ 0.01) Fig. 5 Forest plot of the prevalence of S. aureus resistance to penicillin G aureus to different antibiotics ranges from 13 to 82%. vaginal swab) were collected from both symptomatic Results from the meta-analysis showed that resistance patients [61] and asymptomatic people [37]. of S. aureus to routinely used antibiotics in Nigeria was High heterogeneity was observed for each of the meta- alarmingly high. From the studies, it was found that 82% analyses performed with I ranging from 79.36 to 98.90% S. aureus were resistant to penicillin G. However, it was at p-values ≤ 0.01). This is because many studies used observed from the studies that 24% of S. aureus were varying number of isolates/sample sizes. Some stud- resistant to ofloxacin and rifampicin. In general, clini - ies used 20 isolates while some used 400 isolates which cal samples (nasal, urine, wound, pimple, ear, blood, and impacted on the resistance profile of each antibiotic. This Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 14 of 22 Ceftriaxone at 95% CI Onwubiko & Sadiq, 2011 Terry et al, 2011 Akerele et al, 2015 Torimino et al, 2012 Bale et al, 2019 Adesoji et al, 2019 Udobi et al, 2013 Agwu et al, 2010 Adesida et al, 2016 Osiyemi et al, 2018 Onaolapo et al, 2016 Tula et al, 2016 Anyanwu et al, 2013 Onyeagwara et al, 2014 Obajuluwa et al, 2015 Ibrahim et al, 2018 Motayo t al, 2012 Onyeka et al, 2021 Osinupebi et al, 2018 Bale et al, 2021 Nmema, 2017 Ugwu et al, 2015 Frank-Peterside & Mukoro, 2010 Nwankwo et al, 2010 Olufunmiso et al, 2017 Total (random effects) 0.00.2 0.40.6 0.81.0 Proportion (44%) Pooled prevalence 0.44 (0.34, 0.54) I = 95.64 (P≤ 0.01) Fig. 6 Forest plot of the prevalence of S. aureus resistance to ceftriaxone can better be illustrated in the prevalence of resistance of antibiotics and publication bias was not found. Egger S. aureus to vancomycin. Sensitivity test was carried out test is use to estimate asymmetry of data using funnel to by removing studies that reported very high prevalence plots. p-value less than 0.05 using Egger criteria indicate of S. aureus to vancomycin and the overall pooled preva- no presence of publication bias even though erythro- lence reduced from 13 to 7%. This showed the degree mycin had p-value of 0.017 which is below 0.05. This is of heterogeneity among studies. Possible cause of het- because a p-value of 0.017 for the Egger test means that erogeneity is due to different number of clinical samples the results found have a 1.7% chance to occur when there and number of isolates recovered which were subjected is no ’small sample bias. to antibiotic sensitivity tests. Also random sampling of The pooled prevalence of S. aureus resistance to Beta- clinical samples can also be the possible cause. Publica- lactams class of antibiotics was extremely high espe- tion bias was evaluated for all meta-analysis of the 23 cially for penicillins. S. aureus showed highest resistance E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 15 of 22 Ofloxacin at 95% CI Akortha & Ikenebomeli , 2010 Nworie, 2013 Onanuga & Awhowho, 2012 Onanuga & Onaolapo, 2008 Onwubiko & Sadiq, 2011 Onwubiko & Temedie, 2011 Akanbi & Mbe, 2013 Badger-Emeka, 2014 Torimo et al, 2012 Bale et al, 2019 Adesoji et al, 2019 Anucha et al, 2021 Adesida et al, 2016 Mofolorunsho et al, 2015 Osiyemi et al, 2018 Tula et al, 2016 Akinduti et al, 2019 Oladipo et al, 2019 Onyeka et al, 2021 Osinupebi et al, 2018 Ajoke et al, 2012 Bale et al, 2021 Ugwu et al, 2015 Nwankwo et al, 2010 Olufunmiso et al, 2017 Total (random effects) 0.00.2 0.40.6 0.81.0 Proportion (24%) Po oled prevalence 0.24 (0.18, 0.31) I = 91.63 (P≤ 0.01) Fig. 7 Forest plot of the prevalence of S. aureus resistance to ofloxacin to penicillin G (82%) and 69% resistance to cefuroxime However, S. aureus resistance to amoxicillin and ampi- (cephalosporin). The pooled estimate of S. aureus resist - cillin is relatively high from our results. Lower rate of ance to penicillin G is comparable with the reported esti- resistance was observed among beta-lactamase-resistant mation of worldwide resistance of 90–95% [108]. This is antibiotics (methicillin, ceftriaxone, cefoxitine). Also, not surprising due to the fact that penicillin G is the first lower rate of resistance to clindamycin might be attrib- antibiotic to be discovered. Bacteria are able to develop uted to infrequent use of the antibiotic. Amoxicillin- resistance to antibiotics due to selective pressure from clavulanic acid was developed as a combination of an antibiotics. Selective pressure from penicillin led to the antibiotic (amoxicillin) and non-antibiotic (clavulanic production of beta-lactamase to conuter the effect of acid). Clavulanic acid inhibit beta-lactamase enzyme beta-lactam antibiotics. Consequently, semi-synthetic which prolong the antibacterial activity of amoxicil- beta-lactam antibiotics such as ampicillin, Amoxicil- lin component; however, results from the meta-analysis lin/clavulanic acid and amoxicillin with different side showed high resistance of S. aureus to amoxicillin/clavu- chains were developed to counter such bacteria strains. lanic acid. Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 16 of 22 Chloramphenicol at 95 % CI Akortha & Ikenebomeli, 2010 Olorede et al, 2021 Onanuga & Awhowho, 2012 Chigbu & Ezeronye, 2003 Yah et al, 2009 Onwubiko & Sadiq, 2011 Onanuga & Temedie, 2011 Terry et al, 2011 Ekundayo & Ndubuisi, 2015 Badger-Emeka et al, 2014 Torimino et al, 2012 Ramalan et al, 2020 Obasola et al, 2010 Anyanwu et al, 2013 Ngwai & Bakare, 2012 Umar et al, 2015 Ibanga et al, 2020 Emeakaroha et al, 2017 Bisi-Johnson et al, 2005 Adeiza et al, 2020 Ismail et al, 2015 Onelum et al, 2015 Motayo et al, 2012 Ugwu et al, 2009 Nsofor et al, 2019 Mbim et al, 2017 Adetutu et al, 2017 Bale et al, 2021 Ako-Nai et al, 2005 Yahaya et al, 2022 Nsofor et al, 2015 Olajide et al, 1012 Total (random effects) 0.00.2 0.40.6 0.81.0 Proportion (47 %) Pooled prevalence 0.47 (0.37, 0.56) I = 95.03 ( P ≤ 0.01) Fig. 8 Forest plot of the prevalence of S. aureus resistance to chloramphenicol Another semi-synthetic penicillin resistant antibiotic 2014. Which depicted MRSA prevalence ranged 33–95% called methicillin was developed which is resistant to in Africa. Similarly, the pooled estimate of 46% in our hydrolysis of beta-lactamase was developed. The term study is also in agreement with the pooled prevalence Methicillin Resistant Staphylococcus aurues (MRSA) is estimate of MRSA in continents such as North America, synonymous with multi-drug resistance (MDR) because Asia, and Europe which ranges from 23.1 to 47.4% [109]. MRSA are invariably resistant to different antibiotics. The high pooled prevalence in our study might be due Acquisition of mec A gene that encodes penicillin binding to certain factors and variables such as the inclusion of nosocomial and community acquired infections in the protein confers resistance to S. aureu [109]. The pooled original studies analyzed. Generally, nosocomial infec prevalence of S. aureus to methicillin (46% [95% CI 37%, - 56%]) in Nigeria is similar to 2014 global surveillance tion causing pathogens are believed to possess higher reports of the world health organization (WHO) [110] resistance rate due to prolonged and higher exposure to E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 17 of 22 Cotrimoxazole at 95% CI Odu & Okonkwo, 2012 Nworie, 2013 Onanuga & Awhowho, 2012 Iroha et al, 2012 Ekunday o & Ndubuisi, 2015 adger-Emeka, 2014 Torimino et al, 2012 Onanuga et al, 2021 Obasola et al, 2010 M ofolorunsho et al, 2015 Osiy emi et al, 2018 Emekaroha et al, 2017 Ugwu et al, 2009 Osinup ebi et al, 2018 adetutu et al, 2017 Ugwu et al, 2015 ako-Nai et al, 2005 Onanuga et al, 2019 Yahaya et al, 2022 Chigbu & Ezerony e, 2003 Ramalan et al, 2020 Total (random effects) 0.0 0.2 0.4 0.6 0.8 1.0 Prop ortion (66%) Pooled prevalence 0.66 (0.55, 0.76) I = 93.91 (P≤ 0.01) Fig. 9 Forest plot of the prevalence of S. aureus resistance to cotrimoxazole different antimicrobial agents and exchange of genetic studies [20, 22, 28, 36] reported a very high prevalence materials. Thus, there is greater transmission of resistant of VRSA; however, sensitivity analysis showed that they genes through various means within the hospital settings had high significant influence on the overall pooled [111]. The implication of infections cause by MRSA is dif - prevalence estimate. Removing the three studies reduces ficulty in treatment which often requires alternative anti - the pooled prevalence of S. aureus resistance to vanco- microbial agents which are most times very expensive. mycin from 13 to 7%. Analyzing studies that depicted The pooled prevalence of S. aureus resistance to van - high prevalence of resistance of S. aureus to vancomy- comycin (13% at 95% CI [0.7%, 21%]) in this meta-anal- cin showed that the same author conducted and pub- ysis is high and a cause for concern when compared to lished the three studies in peer reviewed journals. Urine global prevalence estimate [4]. The prevalence of vanco - samples were mainly used for S. aureus isolation by the mycin resistant S. aureus (VRSA) in Africa was reported author in the three studies of which [20, 22] were from to be 2.5% [4]. This is quite low when compared to the symptomatic urinary tract infection patients who visited result from this study which is very high (13%). With the hospitals and [27] from healthy volunteers. Urinary this increased resistance, the use of vancomycin to treat tract infection is a common infection and a reason for MRSA is becoming problematic and poses serious health antibioticl use; consequently, resistant microbial strains challenge. The rise in VRSA might be due to the indis - have emerged. This reason might be attributed to the criminate use of vancomycin in Nigeria. By the way, Four high prevalence of S. aureus resistant to vancomycin in Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 18 of 22 percentage % Antibiotics Fig. 10 Comparison of the prevalence of S. aureus resistance to different antibiotics in Nigeria the three studies. Exposure to resistant strains especially expression of Mec genes which alters penicillin binding in hospital settings might have resulted in the increased proteins. From the results and mechanism of resistance resistance to vancomycin in the three studies [112, 113]. of S. aureus, it can be said that S. aureus found in Nigeria This is because in Nigeria, expired or waste antibiotics are highly resistant to the beta-lactam class of antibiotics. are not properly discharged. This could result in selective The pooled prevalence of S. aureus resistance to the pressure on inhabitant microorganisms which results in floroquinolones class of antibiotics such as ciprofloxa - development of various resistant mechanisms. cin, ofloxacin, and norfloxacin was lower especially for Generally, the global pattern of antimicrobial resistance ciprofloxacin which is commonly used within Nigeria. varies among different geographical locations and socio - However, high pooled prevalence of S. aureus resistance economic level [114, 115]. Variations in studies can be to antimetabolites class of antibiotics (cotrimoxazole and attributed to design, time, and population involved. Het- trimethoprim) was observed. erogeneity tests at p ≤ 0.01 showed significant variation From the meta-analysis, S. aureus mediated infection among included studies in this meta-analysis. Therefore, in Nigeria can be treated using vancomycin, floroqui - it is reasonable to assert that the study population might nolones, and aminoglycosides. MRSA has been a concern be infected with the same strains of S. aureus within the in Nigeria especially with the incidence of VRSA. Newer same location at a specified period. This is because most alternative antibiotics such as linezolid, telavancin, cef- of the studies were conducted within a specified period taroline, tigecycline and daptomycin are rarely used in of time and area. Nigeria. Various factors such as lack of infection preven- Mechanisms of resistance of S. aureus include: produc- tion which lead to reoccurrence of infection, inappro- tion of beta-lactamase enzymes to deactivate beta-lactam priate use of antibiotics, poor hospital facilities, lack of sensitive antibiotics, efflux pump for extruding antibi - routine susceptibility test before antibiotic administra- otics such as tetracyclines [6], reduced accumulation of tion, and self medication contributes to the rapid emer- macrolides antibiotics [7], production of aminoglyco- gence and re-emergence of AMR. Tackling this factors, side modifying enzymes to inactivate aminoglycosides will go a long way in the fight against the continue rise of antibiotics, alteration of DNA gyrase and topoisomer- MDR pathogens in general. ase IV expression for floroquinolones antibiotics, and Prevalence of resistance (%) Vancomycin Ofloxacin Rifampicin Ciprofloxacin Gentamycin Norfloxacillin Clindamycin Cefoxitine Ceftriaxone Streptomycin Methicillin Chloramphenicol Erythromycin Trimethoprim Ceftazidime amoxicillin/clavulanic acid Tetracycline Cotrimoxazole Ampicillin Cefuroxime Amoxicillin Cloxacillin Penicillin E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 19 of 22 Study limitations Supplementary Information Most of the included studies share similar characteristics. The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s13756- 023- 01243-x. The search was limited to only titles that deal with antibi - otic resistance. Selection was done randomly especially in Additional file 1: S1. PRISMA 2009 Checklist Google Scholar with had 35, 400 studies results from the Additional file 2: S2. Egger’s test of publication bias search. The meta-analysis was done once for each anti - Additional file 3: S3. Forest plot of the prevalence of S. aureus resistance to biotics and sub-grouping to reduce high heterogeneity amoxicllin and publication bias was not done due to too many meta- Additional file 4: S4. Forest plot of the prevalence of S. aureus resistance analysis already done. The included studies used in-vitro to ampicillin antimicrobial assays which has limitations such as dif- Additional file 5: S5. Forest plot of the prevalence of S. aureus resistance to ficulties in interpreting data, variability of testing media augmentin (differences in cation content, acidic or alkaline), and dif - Additional file 6: S6. Forest plot of the prevalence of S. aureus resistance to ficulty in knowing the pharmacokinetics of an antibiotic cloxacillin or post effect of an antibiotic (a situation where bacteria Additional file 7: S7. Forest plot of the prevalence of S. aureus resistance to cefuroxime growth is inhibited even when the antibiotic concentra- Additional file 8: S8. Forest plot of the prevalence of S. aureus resistance to tion falls below the MIC). Most of the studies were done cefoxitine in teaching hospitals and tertiary institutions in big cit- Additional file 9: S9. Forest plot of the prevalence of S. aureus resistance to ies; hence both symptomatic and asymptomatic individu- ciprofloxacin als are involved. For symptomatic individuals, most of Additional file 10: S10. Forest plot of the prevalence of S. aureus resistance the studies were done in teaching hospitals were patients to norfloxacin with chronic and recurrent infections are treated; resist- Additional file 11: S11. Forest plot of the prevalence of S. aureus resistance ance level could be overestimated. to tetracycline Additional file 12: S12. Forest plot of the prevalence of S. aureus resistance to erythromycin Conclusion Additional file 13: S13. Forest plot of the prevalence of S. aureus resistance to gentamycin The results of this meta-analysis showed that S. aureus Additional file 14: S14. Forest plot of the prevalence of S. aureus resistance is resistant to many routinely used antibiotics in Nige- to streptomycin ria. It is highly resistant to beta-lactams, tetracyclines, Additional file 15: S15. Forest plot of the prevalence of S. aureus resistance and antimetabolites antibiotics. Resistance of S. aureus to clindamycin to vancomycin remains a serious health problem due to Additional file 16: S16. Forest plot of the prevalence of S. aureus resistance limited treatment options. There is a lot of variation in to trimethoprim resistance estimates between studies. High heterogene- ity was observed in each meta-analysis for each antibiotic Acknowledgements which was attributed to various factors such as differ - Not applicable ent clinical sample and recovered isolates sizes, random Author contributions sampling and method used for resistance investigation. CKE, CNE and UMED conceptualized the research idea. CKE and SCE con- Hence it is imperative to develop programs to promote ducted literature search, selection and data extraction. CKE performed the rational use of antimicrobial agents, infection prevention statistical analyses. CKE prepared the draft manuscript. All authors revised, edited and approved the final manuscript. and control to reduce the incidence of AMR. In addition, furthers researches focusing on identifying the dynam- Funding ics promoting microbial resistance, infectious microbial No funding was received. strains and molecular/genetic basis of resistance should Availability of data and materials be encouraged. The data supporting the conclusions of this article are included within the article and its supporting information. Abbreviations Declarations AMR Antimicrobial resistance CLSI Clinical Laboratory Standard Institute Ethics approval and consent to participate CI Confidence interval Not applicable. MRSA Methicillin resistant Staphylococcus aureus S. aureus Staphylococcus aureus VRSA Vancomycin resistant Staphylococcus aureus Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 20 of 22 Consent for publication 19. Olorode OA, Ogba OM, Nanighe SO. Molecular detection of methicil- Not applicable. lin resistance genes (Mec A; Pvl) in methicillin resistant Staphylococcus aureus isolates from Federal Medical Centre, Yenagoa, Bayelsa State, Competing interests Nigeria. J Curr Med Res Opin. 2021;4(10):1035–41. The authors declare that they have no competing interests. 20. Onanuga A, Awhowho GO. Antimicrobial resistance of Staphylococcus aureus strains from patients with urinary tract infections in Yenagoa, Nigeria. J Pharm Bioallied Sci. 2012;4(3):226–30. Received: 11 August 2022 Accepted: 14 April 2023 21. Ayodeji AA, Omoniyi AK. Multi-drug resistant Staphylococcus aureus in clinical cases in Ile-Ife, Southwest Nigeria. Int J Med Med Sci. 2009;1(3):68–72. 22. Onanuga A, Onaolapo AJ. Antimicrobial Susceptibility of Community- associated Staphylococcus aureus Isolates from Healthy Women in Zaria, Nigeria. Trop J Pharm Res. 2008;7(1):929–34. References 23. Chigbu C, Ezeronye OU. Antibiotic resistant Staphylococcus aureus in 1. Rasigade JP, Vandenesch F. Vandenesch, Staphylococcus aureus: a patho- Abia State of Nigeria. Afr J Biotechnol. 2013;2(10):374–8. gen with still unresolved issues. Infect Genet Evol. 2014;21:510–4. 24. Yah SC, Enabule OI, Eggafona NO. The screening of multidrug resistance 2. Bamigboye BT, Olowe OA, Taiwo SS. Phenotypic and molecular iden- (MDR) susceptibilities of Staphyloccocus aureus and Staphyloccocus epi- tification of vancomycin resistance in clinical Staphylococcus aureus dermidis to methicillin and vancomycin in teaching hospitals in Nigeria. isolates in Osogbo, Nigeria. Eur J Microbiol Immunol. 2018;8:25–30. Int J Biol Chem Sci. 2007;2(4):257–61. 3. McGuinness WA, Malachowa N, DeLeo FR. Vancomycin resistance in 25. Yah SC, Yusuf EO, Haruna T. Patterns of antibiotics susceptibility of Staphylococcus aureus. Yale J Biol Med. 2017;90(2):269–681. isolates and plasmid analysis of Staphylococcus from surgical site infec- 4. Shariati A, Dadashi M, Moghadam MT. Global prevalence and distribu- tions in Nigeria. Sudan JMS. 2009;3(4):810–8. tion of vancomycin resistant, vancomycin intermediate and hetero- 26. Onwubiko NE, Sadiq NM. Antibiotic sensitivity pattern of Staphylococ- geneously vancomycin intermediate Staphylococcus aureus clinical cus aureus from clinical isolates in a tertiary health institution in Kano, isolates: a systematic review and meta-analysis. Sci Rep. 2020;10:12689. Northwestern Nigeria. Pan Afr Med J. 2011;8(4):1–7. 5. Khan A, Wilson B, Gould IM. Current and future treatment options for 27. Onanuga A, Temedie TC. Nasal carriage of multi-drug resistant Staphylo- community-associated MRSA infection. Expert Opin Pharmacother. coccus aureus in healthy inhabitants of Amassoma in Niger delta region 2018;19(5):457–70. of Nigeria. Afr Health Sci. 2011;11(2):176–81. 6. Sompolinsky D, Zaidenzaig Y, Ziegler-Schlomowitz R, Abramova N. 28. Onanuga A, Avosuahi RO, Onaolapo JA. Prevalence and susceptibility Mechanism of tetracycline resistance in Staphylococcus aureus. J Gen pattern of methicillinresistant Staphylococcus aureus isolates among Microbiol. 1970;62(3):351–62. healthy women in Zaria. Nigeria Afr J Biotechnol. 2005;4(11):1321–4. 7. Yamagishi S, Nakajima Y, Inoue M, Oka Y. Decrease in accumulation of 29. Akanbi RO, Mbe JU. Occurrence of methicillin and vancomycin resistant macrolide antibiotics as a mechanism of resistance in Staphylococcus Staphylococcus aureus in University of Abuja teaching hospital, Abuja, aureus. Jpn J Microbiol. 1971;15(1):39–52. Nigeria. Afr J Clin Exp Microbiol. 2013;14(1):10–3. 8. Li XF, Fan XJ, Guo XJ, Feng P, Lu XJ, Gao YY, et al. A study on the mecha- 30. Alli OAT, Ogbolu DO, Akorele E, Onemu OM, Okanlawon BM. Distribu- nism of drug resistance in Staphylococcus aureus. Sichuan Da Xue Xue tion of mecA gene amongst Staphylococcus aureus isolates from Bao Yi Xue Ban. 2006;37(3):365–8. Southwestern Nigeria. Afr J Biomed Res. 2011;14:9–14. 9. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items 31. Iroha IR, Okoye E, Osigwe CA, Moses IB, Ejikeugwu CP, Nwakaeze AE. for systematic reviews and meta-analyses: the PRISMA statement. PloS Isolation, Phenotypic characterization and prevalence of ESBL-produc- Med. 2009;151:264–9. ing Escherichia coli and Klebsiella species from orthopedic wounds 10. Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis in National Orthopedic Hospital Enugu (NOHE), South East Nigeria. J detected by a simple, graphical test. BMJ. 1997;315(7109):629–34. Pharm Care Health Syst. 2017;4(4):1000184. 11. Akortha EE, Ikenebomeh MJ. Nasal colonization of symptomatic 32. Eke S, Abdulkadiri S, Okoro CJ, Ekoh SN, Mbachi NG. The prevalence and pneumonia patients in University of Benin Teaching Hospital, Benin resistivity pattern of Staphylococcus aureus Isolates from apparently City, Nigeria by multiple antibiotic resistant Staphylococcus aureus. Afr J healthy university students in Ekpoma, Edo, Nigeria. Int J Basic Appl Microbiol Res. 2010;4(11):1071–5. Innov Res. 2012;1(4):183–7. 12. Idris MA, Kumurya AS, Mohammed Y. Detection of methicillin-resistant 33. Ekundayo EO, Ndubuisi RN. In-vitro antimicrobial susceptibility pattern staphylococcus aureus among bacterial isolated from children aged of Staphylococcus aureus isolates in Umuahia, Abia state, Nigeria. Afr J 0–5 years with septicaemia in Kano, north western, Nigeria. FUDMA J Clin Exp Microbiol. 2015;16(3):62–6. Microbiol. 2018;1(1):51–7. 34. Obasuyi O, Akerele JO. High incidence of multidrug-resistant strains of 13. Stanley CN, Ugboma HAA, Ibezim EC, Attama AA. Prevalence and anti- methicillinresistant Staphylococcus aureus isolated from clinical samples biotic susceptibility of Staphylococcus aureus and other staphylococcal in Benin-city, Nigeria. Afr J Clin Exp Microbiol. 2015;16(3):124–7. infections in pregnant women attending antenatal clinic in a tertiary 35. Akerele JO, Obasuyi O, Omede D. Prevalence of methicillin-resistant hospital in port Harcourt, Nigeria. Infect Dis Ther. 2013;2(1):1–6. Staphylococcus aureus among healthy residents of Ekosodin commu- 14. Odu NN, Okonko IO. Nasal carriage and antibiotics susceptibility of nity in Benin-City, Nigeria. Trop J Pharm Res. 2015;14(8):1495–9. Staphylococcus aureus in healthy students of University of Port Harcourt, 36. Badger-Emeka LI, Emeka PM, Dibua UME. Plasmid profile of multi Rivers State, Nigeria. N Y Sci J. 2012;5(7):56–63. antibiotic resistant Staphylococcus aureus isolated from diabetic 15. Isibor JO, Otabor E. Asymptomatic carriage of plasmid-mediated wounds from patients at Nsukka, South astern, Nigeria. Afr J Biotectnol. multidrugresistant Staphylococcus aureus in nasal tracts of persons in a 2014;13(43):4148–54. semi-urban area of Nigeria. Am J life Sci. 2014;2(4):200–4. 37. Ayeni FA, Gbarabon T, Andersen C, Nørskov-Lauritsen N. Comparison 16. Nworie A. Nasal carriage of methicillin resistant Staphylococcus aureus of identification and antimicrobial resistance pattern of Staphylococcus amongst meat sellers in Abakaliki Metropolis, Ebonyi State, Nigeria. aureus isolated from Amassoma, Bayelsa state, Nigeria. Afr Health Sci. Microbiol Res Int. 2013;1(3):48–53. 2015;15(4):1282–8. 17. Egbuobi RC, Wachuku CK, Dike-Ndudim JN, Ogamaka AI, Okorie HM, 38. Torimiro N, Torimiro SEA. Antibiotic resistance profile in community- Nwagbaraocha MA, et al. Evaluation of antibacterial profile of methicil- associated Staphylococcus aureus strains isolated from a Nigerian peri- lin resistant Staphylococcus aureus (MRSA) isolated from hospitals in urban community. Afr J Biotechnol. 2012;11(94):16071–6. Imo state, Nigeria. Int J Med Med Sci. 2014;6(2):69–74. 39. Bale M, Babatunde SK, Adedayo MR, Ajiboye AE, Ajao AT. Characteriza- 18. Olowo-Okere A, Atana RF, Abass A, Shuaibu AS, Yahya UH, Tanko N. tion of methicillin-resistant Staphylococcus aureus isolates from appar- Incidence and antibiotic susceptibility profile of Staphylococcus aureus ently healthy individuals in Malete, Kwara state, Nigeria. Afr J Clin Exp isolates from wounds of patients at specialist hospital, Sokoto, Nigeria. J Microbiol. 2019;20(1):17–24. Med Bacteriol. 2017;6(4):44–50. E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 21 of 22 40. Adesoji AT, Onuh JT, Bagu J, Itohan SA. Prevalence and antibiogram 59. Ugwu MC, Anie CO, Ibezim EC, Esimone CO. Antimicrobial evaluation study of Staphylococcus aureus isolated from clinical and selected of methicillin-resistant Staphylococcus aureus nasal carriage amongst drinking water of Dutsin-Ma, Katsina state, Nigeria. Afr Health Sci. healthy students in Agbor, Delta State, Nigeria. Arch Clin Microbiol. 2019;19(1):1385–92. 2016;7(2):13. 41. Ariom TO, Iroha TR, Moses IB, Iroha CS, Ude UT, Kalu AC. Detection and 60. Tula MY, Okoro AJ, Okojie RO, Iyoha O. Antimicrobial susceptibility phenotypic characterization of methicillin-resistant Staphylococcus pattern and plasmid-mediated antibacterial resistance in Staphylococ- aureus from clinical and community samples in Abakaliki, Ebonyi State, cus aureus and coagulase-negative staphylococci. Highl Med Res J. Nigeria. Afr Health Sci. 2019;19(2):2026–36. 2016;16(2):80–6. 42. Ajani TA, Elikwu CJ, Nwadike V, Babatunde T, Anaedobe CG, Shonekan 61. Anyanwu NC, Abdullahi IO, Ameh JB, Ella EE. Molecular detection of O, et al. Nasal carriage of methicillin resistant Staphylococcus aureus PVL, msrA genes and antibiotic susceptibility pattern of staphylococcus among medical students of a private institution in Ilishan-Remo, Ogun aureus from skin and soft tissue infections in Zaria, Nigeria. Sci J Micro- State, Nigeria. Afr J Clin Exp Microbiol. 2020;21(4):311–7. biol. 2013;2(2):43–52. 43. Olorunfemi PO, Onaolapo JA, Ibrahim YKE. Prevalence and antibiotic 62. Onyeagwara N, Obasuy O, Ottih I, Akerele JO. Nasal carriage of susceptibility of community acquired methicillin resistant Staphylococ- methicillin-resistant Staphylococcus aureus among hospitalized cus aureus from healthy students of University of Jos. J Pharm Bioresour. otorhinolaryngological patients in Benin City of Nigeria. Arch Int Surg. 2020;17(2):131–41. 2014;4(2):99–103. 44. Onanuga A, Adamu OJ, Odetoyin B, Hamza JA. Nasal carriage of multi- 63. Ngwai YB, Bakare OR. Asymptomatic bacteriuria and antimicrobial drug resistant panton valentine leukocidin positive Staphylococcus susceptibility of Staphylococcus aureus from university students in Keffi, aureus in healthy individuals of Tudun-Wada, Gombe State, Nigeria. Afr Nigeria. Int J Microbiol Bioinform. 2012;2(1):6–8. J Infect Dis. 2021;15(1):24–33. 64. Umar M, Abdulkarim IM, Yaya A, Bello HI, Yusuf G, Mathias ML. Bio- 45. Ramalan AS, Joseph FN, Owoseni MC, Ya’aba Y, Chuku A. Prevalence and chemical characterization and antibiotic susceptibility profile of Staphy - antibiotic resistance profile of Staphylococcus aureus and Escherichia lococcus aureus isolated from patients attending Barau Dikko Specialist coli among patients attending urology Clinic of Dalhatu Araf specialist Hospital, Kaduna State, Nigeria. Int J Novel Res Life Sci. 2015;2(6):1–9. hospital (dash) Lafia, Nasarawa state, Nigeria. Bayero J Pure Appl Sci. 65. Obajuluwa AF, Olayinka BO, Adeshina JA, Afolabi-Balogun NB. Plasmid 2020;13(1):80–9. profile of Staphylococcus aureus from orthopaedic patients in Ahmadu 46. Udobi CE, Obajuluwa AF, Onaolapo AJ. Prevalence and Antibiotic Bello University Teaching Hospital Zaria, Nigeria. Afr J Microbiol Res. resistance pattern of methicillin-resistant Staphylococcus aureus from an 2015;9(33):1941–6. Orthopaedic Hospital in Nigeria. BioMed Res Int. 2013;4. 66. Iduh UM, Chollom CS, Nuhu A, Spencer THI, Nura MB, Ashcroft OF, et al. 47. Obasola EF, Ezeamagu CO, Oyelade AA, Adeniyi AO. Comparative study Nosocomial infections in post-operative wounds due to Staphylococ- of antibiotic resistance of Staphylococcus species isolated from clinical cus aureus and Pseudomonas aeruginosa in Benue State Nigeria. Afr J and environmental samples. AU J Tech. 2010;13(3):165–9. Microbiol Res. 2015;9(36):1989–96. 48. Moses AE, Ohagim IP, Inyang UC. Nasal methicillin-resistant Staphy- 67. Ibanga IA, Akan OD, Iyanga FZ, Mantu EC, Asuquo M. Multi-drug resist- lococcus aureus carriage in pre and post-operative patients in a ance pattern of Staphylococcus aureus from pediatric ward, General tertiary health facility in Uyo, South-south, Nigeria. World J Pharm Res. Hospital, Ikot-Ekpaw, Mkpat Enin LGA, Akwa-Ibom State, Nigeria. Arch 2017;6(5):160–71. Clin Microbiol. 2020;11(105):1–4. 49. Nsofor CA, Nwokenkwo VN, Nwaokpa C. Nasal carriage of Staphylo- 68. Emeakaroha MC, Nkwocha IG, Adieze NC, Adieze IE. Antimicrobial sus- coccus aureus among apparently Healthy School Children in Owerri ceptibility pattern of Staphylococcus aureus, and their nasal and throat Metropolis, Nigeria. Basic Res J Microbiol. 2015;2(3):34–8. carriage among food handlers at the Federal University of Technology, 50. Adetayo TO, Deji-Agboola AM, Popoola MY, Atoyebi TJ, Egberongbe KJ. Owerri Nigeria. Int J Biomol Biomed. 2017;6(3):1–7. Prevalence of methicillin resistant Staphylococcus aureus from clinical 69. Bisi-Johnson MA, Kolawole DO, Shittu OA. Epidemiological analysis of specimens in Ibadan, Nigeria. Int J Eng Sci. 2014;3(9):1–11. clinical isolates of Staphylococcus aureus in IIe-Ife, Nigeria. Pak J Bio Sci. 51. Ejikeugwu C, Nwezeagu FJ, Edeh C, Eze P. Detection of constitutive and 2005;8(7):1016–20. inducible-clindamycin-resistance in clinical isolates of Staphylococcus 70. Ayepola OO, Nurudeen AO, Egwari LO, Becke K, Schaumburg F. Molecu- aureus from a Federal Teaching Hospital in Abakaliki, Nigeria. J Bacteriol lar characterization and antimicrobial susceptibility of Staphylococcus Infect Dis. 2018;2(1):31–4. aureus isolates from clinical infection and asymptomatic carriers in 52. Anucha JC, Morikwe UC, Ikegbunam MN, Ezejiegu CK, Ugwu MC. Age Southwest Nigeria. PLoS ONE. 2015;10(9): e0137531. and gender- based antibiotic susceptibility patterns of Staphylococcus 71. Odogwu DA, Kadarko PS, Muazu JS, Bassey BE, Abimiku RH, Nkene IH, aureus among HIV patients in some selected hospitals in Anambra et al. Antimicrobial resistance profile and molecular detection of MecA Central, Nigeria. Gen Mol Med. 2021;3(2):1–5. gene in methicillin resistant Staphylococcus aureus from patients in 53. Agwu E, Ihongbe J, Inyang N. Prevalence of quinolone-susceptible selected general hospitals in Abuja municipal, Nigeria. GSC Biol Pharm Pseudomonas aeruginosa and Staphylococcus aureus in delayed-healing Sci. 2019;7(3):93–106. diabetic foot ulcers in Ekpoma, Nigeria. Cell Tis Prod. 2010;22(4):100–5. 72. Adeiza SS, Onaolapo JA, Olayinka BO. Prevalence, risk-factors, and 54. Adesida AS, Okeyide AO, Abioye A, Omolopo I, Egwuatu TO, Amisu antimicrobial susceptibility profile of methicillin-resistant Staphylococ- KO, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus cus aureus (MRSA) obtained from nares of patients and staff of Sokoto among elderly people in Lagos, Nigeria. Avicenna J Clin Microb Infect. state-owned hospitals in Nigeria. GMS Hyg Infect Control. 2020;15:1–17. 2016;3(4):e39272. 73. Ismail HY, Bello HS, Mustafa A, Adamu A. Multidrug resistance pattern 55. Mofolorunsho CK, Ocheni M, Omatola CO, Agieni AG. Staphylococ- of Staphylococcus aureus isolates in Maiduguri metropolis. Sci Rev. cus aureus prevalence and antibiotic susceptibility profile in Anyigba, 2015;1(2):16–20. North-Central Nigeria. Am J Infect Dis. 2015;11(4):93–7. 74. Ibrahim S, Adam SA, Alero AA, Umar S. Prevalence and antibiotic sensi- 56. Osiyemi JA, Osinupebi OA, Akinduti PA, Ejilude O, Makanjuola tivity pattern of Staphylococcus aureus Isolated from wound and otitis SO, Sunmola NO, et al. Antibiotic resistance profile of methicillin- media among patients attending Aminu Kano Teaching Hospital, Kano, resistant Staphylococcus aureus in Abeokuta, Nigeria. J Adv Microbiol. Nigeria. Microbiol Res J Int. 2018;25(2):1–9. 2018;9(2):1–9. 75. Olowe OA, Kukoyi OO, Taiwo SS, Ojurongbe O, Opaleye OO, Bolaji OS, 57. Ibe C, Onyeagba RA, Ugochukwu SC. Antibiotic resistance patterns and et al. Phenotypic and molecular characteristics of methicillin-resistant plasmid profiles of methicillin resistant Staphylococcus aureus isolates Staphylococcus aureus isolates from Ekiti State, Nigeria. Infect Drug Res. from human samples. Br Microbiol Res J. 2014;4(2):185–94. 2013;6:87–92. 58. Onaolapo JA, Olayinka BO, Adeshina GO, Igwe JC, Obajuluwa AF. 76. Oche AD, Oyegoke PI, Akpudo MO, Olayinka BO. Antibiotics resist- Antimicrobial susceptibility pattern of Staphylococcus aureus isolates ance pattern of Staphylococcus aureus isolated from in-patients of an from orthopaedic patients in Abuth Zaria. J Food Indust Microbiol. Orthopaedic Hospital in North-Western Nigeria. Int J Epidemiol Res. 2016;2(1):1–6. 2021;8(4):160–6. Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 22 of 22 77. Onelum B, Odetoyin B, Onipede A, Oyelese A. The role of methicillin- genome of Staphylococcus aureus from hospitals in South Western resistant Staphylococcus aureus in clinical infections in Obafemi Nigeria. Indian J Med Microbiol. 2012;30(2):159–64. Awolowo University Teaching Hospitals Complex, Ile-Ife, South Western 97. Sadauki AH, Olorukooba AA, Balogun MS, Dalhat MM, Waziri H, Nigeria. J Microbiol Exp. 2015;2(2):00041. Abdulaziz MM, et al. Nasal carriage of meticillin-resistant Staphylococcus 78. Akindut AP, Osiyemi JA, Banjo TT, Ejilude O, El-Ashke M, Adeyemi AG, aureus among children living with HIV attending infectious diseases et al. Clonal diversity and spatial dissemination of multi-antibiotics clinics in Kano. Nigeria Infect Prev Pract. 2022;4:1–8. resistant Staphylococcus aureus pathotypes in Southwest Nigeria. PLoS 98. O’Malley SM, Emele FE, Nwaokorie FO, Idika N, Umeizudike AK, Emeka- ONE. 2021;16(2):e0247013. Nwabunnia I, et al. Molecular typing of antibiotic-resistant Staphylococ- 79. Oladipo AO, Oladipo OG, Bezuidenhout CC. Multi-drug resistance traits cus aureus in Nigeria. J Infect Public Health. 2015;8:187–93. of methicillin-resistant Staphylococcus aureus and other Staphylococ- 99. Emeka-Nwabunnia I, Ejigeme K, Oguoma OI. Antibiotic resistance cal species from clinical and environmental sources. J Water Health. pattern of methicillin-resistant Staphylococcus aureus isolated from chil- 2019;17(6):932–43. dren under the age of five years in Anambra State. Niger J Biotechnol. 80. Ogefere HO, Umaru G, Ibadin EE, Omoregie R. Prevalence of methicillin- 2019;36(1):213–21. resistant staphylococci among apparently healthy students attend- 100. Ako-Nai AK, Adeyemi FM, Aboderin OA, Kassim OO. Antibiotic resist- ing a tertiary institution in Benin City, Nigeria. Niger J Basic Appl Sci. ance profile of staphylococci from clinical sources recovered from 2019;27(1):114–21. infants. Afr J Biotechnol. 2015;4(6):816–22. 81. Motayo BO, Akinduti PA, Okerentugba PO, Innocent-Adiele HC, Onoh 101. Frank-Peterside N, Mukoro M. The current susceptibility pattern of CC, Nwanze JC, et al. Methicillin resistance and beta-lactamase produc- methicillin resistant Staphylococcus aureus to antibiotics in Port Har- tion in Staphylococcus aureus isolated from different clinical samples in court. Global J Pure Appl Sci. 2010;16(4):375–9. Abeokuta, Nigeria. Acad Arena. 2012;4(6):25–8. 102. Yahaya H, Ahmad AS, Ibrahim A, Abdullahi AS. Phenotypic Detection of 82. Onyeka FI, Nwobodo DC, Umenne IC, Atada EE, Ojukwu CA, Aniekwe Macrolide, Lincosamide and Streptogramin B resistance among Staphy- MA, et al. Antibiotic resistance pattern of Staphylococcus aureus isolated lococcus aureus clinical isolates in A Northern Nigeria Tertiary Hospital. from nostrils of healthy undergraduates of Madonna University Elele Alq J Med App Sci. 2022;5(1):193–8. Campus, Rivers State, Nigeria. Microbes Infect Dis. 2021;2(2):280–5. 103. Onanuga A, Eboh DD, Okou GT. Antibiogram and virulence character- 83. Ugwu CM, Odimegwu DC, Ibezim EC, Esimone CO. Antibiotic Resist- istics of multi-drug resistant Staphylococcus aureus from nasal cavity of ance patterns of Staphylococcus aureus isolated from nostrils of healthy healthy students of Niger Delta University, Amassoma, Bayelsa State, human subjects in a Southeastern Nigeria Locality. Maced J Med Sci. Nigeria. J Clin Diagn Res. 2019;13(7):24–9. 2009;2(4):294–300. 104. Oginni IO, Olayinka AA. Distribution and antibiotics resistance pattern 84. Nsofor CA, Nwokenkwo VN, Ohale CU. Prevalence and antibiotic sus- of community-acquired methicillin-resistance Staphylococcus aureus in ceptibility pattern of Staphylococcus aureus isolated from various clini- Southwestern Nigeria. Adv Exp Med Biol. 2022;1369:81–91. cal specimens in South East Nigeria. MOJ Cell Sci Rep. 2016;3(2):00054. 105. Nwankwo EOK, Sale A, Magagi A, Ihesiulor G. Methicillin resistant S. 85. Mbim EN, Mboto CI, Edet UO, Umego CF, George UE, Temidayo L. aureus (MRSA) and their antibiotic sensitivity pattern in Kano, Nigera. Comparative evaluation of methicillin-resistant Staphylococcus aureus Afr J Clin Exp Microbiol. 2010;11(1):129–36. (MRSA) isolates from hospital and community settings in Nigeria. J Adv 106. Olufunmiso C, Tolulope I, Roger C. Multidrug and vancomycin resist- Microbiol. 2017;4(4):1–9. ance among clinical isolates of Staphylococcus aureus from different 86. Ogbolu DO, Alli TOA, Bello LA, Ibrahim AO. Emergence of vancomycin teaching hospitals in Nigeria. Afr Health Sci. 2017;17(3):798–806. intermediate Staphylococcus aureus ( VISA) in clinical isolates of methicil- 107. Olajide RA, Ameh JA, Simon MK. Antibiotic resistance and susceptibil- lin resistant S. aureus from South Western Region of Nigeria. Int J Trop ity pattern/profile of Staphylococcus aureus and Klebsiella species to Dis Health. 2015;10(4):1–5. popularly—used and readily available antibiotics in Zaria, Nigeria. J 87. Osinupebi OA, Osiyemi JA, Deji-Agboola AM, Akinduti PA, Ejilude O, Phytother Pharm. 2012;1:16–21. Makanjuola SO, et al. Prevalence of methicillin-resistant Staphylococcus 108. Hemaiswarya S, Kruthiventi AK, Doble M. Synergism between natural aureus in Abeokuta, Nigeria. South Asian J Res Microbiol. 2018;1(1):1–8. products and antibiotics against infectious diseases. Phytomedicine. 88. Ajoke OI, Okeke OI, Odeyemi OA, Okwori AEJ. Prevalence of methicillin- 2008;15(8):639–52. resistant Staphylococcus aureus from healthy community individuals 109. Li S, Li J, Qiao Y, Ning X, Zeng T, Shen X. Prevalence and invasiveness volunteers in Jos south, Nigeria. J Microbiol Biotechnol Food Sci. of community-acquired methicillin-resistant Staphylococcus aureus: a 2012;1(6):1389–405. metaanalysis. Indian J Pathol Microbiol. 2014;57(3):418–22. 89. Onyebueke EA, Onyemelukwe NF, Oladeji DS. Antibiotic susceptibility 110. WHO. Antimicrobial resistance: global report ton surveillance. 2014. pattern of Staphylococcus species implicated in urinary tract infection 111. Struelens MJ. The epidemiology of antimicrobial resistance in in Enugu state Nigeria. Pharm OnLine. 2019;1:166–76. hospital acquired infections: problems and possible solutions. BMJ. 90. Adetutu AA, Oritsewehinmi B, Khiwili OM, Moradeke AO, Odochi AS, 1998;317(7159):652–4. Adeola OE. Studies on Staphylococcus aureus isolated from pimples. Pak 112. Guta M, Aragaw K, Merid Y. Bacteria from infected surgical wounds and J Biol Sci. 2017;20:350–4. their antimicrobial resistance in Hawassa University referral teaching 91. Bale MI, Babatunde SK, Awe S. prevalence of methicillin resistant hospital, southern Ethiopia. Afr J Microbiol Res. 2014;8(11):1118–24. Staphylococcus aureus bacteriuria among pregnant women attend- 113. Dessalegn L, Shimelis T, Tadesse E, Gebre-selassie S. Aerobic bacterial ing secondary health hospitals in LLorin, Nigeria. J Adv Microbiol. isolates from post-surgical wound and their antimicrobial suscep- 2021;21(9):2456–7116. tibility pattern: a hospital based cross-sectional study. J Med Res. 92. Nmema EE. Risk factors for infection of Staphylococcus aureus: nasal car- 2014;3(2):18–23. riage, skin carriage and multi-antibiotic resistance in healthy individuals. 114. DACA. Antimicrobials use, resistance and containment baseline survey: Br J Med Med Res. 2017;21(9):1–8. syntheses of findings. In: 2009th ed. Addis Ababa; 2009. 93. Ike B, Ugwu MC, Ikegbunam MN, Nwobodo D, Ejikeugwu C, Gugu 115. Falagas ME, Karageorgopoulos DE, Leptidis J, Korbila IP. MRSA in T, et al. Prevalence, antibiogram and molecular characterization of Africa: filling the global map of antimicrobial resistance. PLoS ONE. comunity-acquired methicillin-resistant Staphylococcus aureus in AWKA, 2013;8(7):e68024. Anambra Nigeria. Open Microbiol J. 2016;10:211–21. 94. Ugwu MC, Mokwe NM, Ejikeugwu P, Enemor EC, Eze CO, Ugwu BC, et al. Publisher’s Note Antibiogram of Staphylococcus aureus from healthy school pupils in Springer Nature remains neutral with regard to jurisdictional claims in pub- Agulu, Southeastern Nigeria. Int J Res Pharm Biosci. 2015;2(4):5–9. lished maps and institutional affiliations. 95. Emeka-Nwabunnia I, Chiegboka NA, Udensi UJ, Nwaokorie FO. Vancomycin-resistant Staphylococcus aureus isolates from HIV positive patients in Imo State, Nigeria. Sci J Public Health. 2015;3(5):1–7. 96. Alli OAT, Ogbolu DO, Mustapha JO, Akinbami R, Ajayi AO. The non- association of Panton-valentine leukocidin and mecA genes in the http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance and Infection Control Springer Journals http://www.deepdyve.com/lp/springer-journals/a-meta-analysis-on-the-prevalence-of-resistance-of-staphylococcus-1MDBp7Kjh4

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References (176)

M. Guta., K. Aragaw, Y. Merid (2014)
Bacteria from infected surgical wounds and their antimicrobial resistance in Hawassa University Referral Teaching Hospital, Southern Ethiopia
African Journal of Microbiology Research, 8
Oyetunji Ajoke, I. Okeke, O. Odeyemi, A. Okwori (2012)
PREVALENCE OF METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS FROM HEALTHY COMMUNITY INDIVIDUALS VOLUNTEERS IN JOS SOUTH, NIGERIA
The Journal of Microbiology, Biotechnology and Food Sciences, 1
MA Idris, AS Kumurya, Y Mohammed (2018)
Detection of methicillin-resistant staphylococcus aureus among bacterial isolated from children aged 0?5 years with septicaemia in Kano, north western, Nigeria
FUDMA J Microbiol, 1
A. Onanuga, T. Temedie (2011)
Nasal carriage of multi-drug resistant Staphylococcus aureus in healthy inhabitants of Amassoma in Niger delta region of Nigeria.
African health sciences, 11 2
BO Motayo, PA Akinduti, PO Okerentugba, HC Innocent-Adiele, CC Onoh, JC Nwanze (2012)
Methicillin resistance and beta-lactamase production in Staphylococcus aureus isolated from different clinical samples in Abeokuta, Nigeria
Acad Arena, 4
J. Akerele, O. Obasuyi, D. Omede (2015)
Prevalence of Methicillin-Resistant Staphylococcus aureus among Healthy Residents of Ekosodin Community in Benin-City, Nigeria
Tropical Journal of Pharmaceutical Research, 14
Odogwu Angel, Parom Kadarko, Jodi Muazu, B. Bassey, Abimiku Helma, Nkene Haruna, Ngwai Boyi (2019)
Antimicrobial resistance profile and molecular detection of MecA gene in methicillin resistant Staphylococcus aureus from patients in selected general hospitals in Abuja municipal, Nigeria
GSC Biological and Pharmaceutical Sciences
Chijioke Nsofor, Vivian Nwokenkwo, Christian Ohale (2016)
Prevalence and antibiotic susceptibility pattern of staphylococcus aureus isolated from various clinical specimens in south east Nigeria
, 3
S. Adeiza, J. Onaolapo, B. Olayinka (2020)
Prevalence, risk-factors, and antimicrobial susceptibility profile of methicillin-resistant Staphylococcus aureus (MRSA) obtained from nares of patients and staff of Sokoto state-owned hospitals in Nigeria
GMS Hygiene and Infection Control, 15
S Eke (2012)
183
Int J Basic Appl Innov Res, 1
Ugwu Mc, Mokwe Nm, Ejikeugwu Pc, Enemor Ec, Eze Co, U. Bc, Gugu Th (2015)
Antibiogram of Staphylococcus Aureus from Healthy School Pupils in Agulu, Southeastern Nigeria
SC Yah, OI Enabule, NO Eggafona (2007)
The screening of multidrug resistance (MDR) susceptibilities of Staphyloccocus aureus and Staphyloccocus epidermidis to methicillin and vancomycin in teaching hospitals in Nigeria
Int J Biol Chem Sci, 2
OA Olorode (2021)
1035
J Curr Med Res Opin, 4
NN Odu (2012)
56
N Y Sci J, 5
S. Adesida, Abiola Okeyide, A. Abioye, I. Omolopo, T. Egwuatu, K. Amisu, A. Coker (2016)
Nasal Carriage of Methicillin-resistant Staphylococcus aureus among Elderly People in Lagos, Nigeria
Avicenna Journal of Clinical Microbiology and Infection, 3
D. Moher, A. Liberati, J. Tetzlaff, D. Altman (2010)
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
International journal of surgery, 8 5
EO Ekundayo (2015)
62
Afr J Clin Exp Microbiol, 16
A. Ako-Nai, F. Adeyemi, O. Aboderin, O. Kassim (2005)
Antibiotic resistance profile of staphylococci from clinical sources recovered from infants.
African Journal of Biotechnology, 4
J. Onaolapo, B. Olayinka, G. Adeshina, Igwe Jc, A. Obajuluwa (2016)
Antimicrobial Susceptibility Pattern of Staphylococcus aureus Isolatesfrom Orthopaedic Patients in Abuth, Zaria
, 2
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations
D Sompolinsky (1970)
351
J Gen Microbiol, 62
D Moher, A Liberati, J Tetzlaff, DG Altman (2009)
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement
PloS Med, 151
OA Olorode, OM Ogba, SO Nanighe (2021)
Molecular detection of methicillin resistance genes (Mec A; Pvl) in methicillin resistant Staphylococcus aureus isolates from Federal Medical Centre, Yenagoa, Bayelsa State, Nigeria
J Curr Med Res Opin, 4
A Onanuga (2012)
226
J Pharm Bioallied Sci, 4
CN Stanley (2013)
1
Infect Dis Ther, 2
TO Ariom (2019)
2026
Afr Health Sci, 19
J. Isibor, E. Otabor (2014)
Asymptomatic Carriage of Plasmid-Mediated Multidrug-Resistant Staphylococcus aureus in Nasal Tracts of Persons in a Semi-Urban Area of Nigeria
American Journal of Life Sciences, 2
O. Obasuyi, J. Akerele (2015)
High incidence of multidrug-resistant strains of methicill inresistant Staphylococcus aureus isolated from clinical samples in Benin-City, Nigeria
African Journal of Clinical and Experimental Microbiology, 16
AA Ayodeji (2009)
68
Int J Med Med Sci, 1
J. Rasigade, F. Vandenesch (2014)
Staphylococcus aureus: a pathogen with still unresolved issues.
Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases, 21
MA Idris (2018)
51
FUDMA J Microbiol, 1
U. Iduh, C. Chollom, A. Nuhu, T. Spencer, M. Nura, O. Ashcroft, N. Faruku (2015)
Nosocomial infections in post-operative wounds due to Staphylococcus aureus and Pseudomonas aeruginosa in Benue State Nigeria
African Journal of Microbiology Research, 9
A. Nworie, A. So, Ibiam Ga, Egwu Ih, I. Odoh, Oti-wilberforce R.O, U. Eze, Obi Ia (2013)
Nasal carriage of methicillin resistant Staphylococcus aureus amongst meat sellers in Abakaliki Metropolis, Ebonyi State, Nigeria
, 1
M Bale (2019)
17
Afr J Clin Exp Microbiol, 20
Ezera Agwu, J. Ihongbe, N. Inyang (2010)
Prevalence of Quinolone-susceptible Pseudomonas aeruginosa and Staphylococcus aureus in Delayed-healing Diabetic Foot Ulcers in Ekpoma, Nigeria .
Wounds : a compendium of clinical research and practice, 22 4
A. Sadauki, A. Olorukooba, Muhammad Balogun, M. Dalhat, H. Waziri, M. Abdulaziz, C. Umeokonkwo, F. Hassan-Hanga, K. Sabitu (2022)
Nasal carriage of meticillin-resistant Staphylococcus aureus among children living with HIV attending Infectious Diseases Clinics in Kano, Nigeria
Infection Prevention in Practice, 4
Lopiso Dessalegn, T. Shimelis, Endale Tadesse, S. Gebre-selassie (2014)
Aerobic bacterial isolates from post-surgical wound and their antimicrobial susceptibility pattern : a hospital based cross-sectional study
C. Mofolorunsho, M. Ocheni, C. Omatola, A. Agieni (2015)
Staphylococcus aureus Prevalence and Antibiotic Susceptibility Profile in Anyigba, North-Central Nigeria
American Journal of Infectious Diseases, 11
A Onanuga (2021)
24
Afr J Infect Dis, 15
I. Ibanga, O. Akan, F. Uyanga, E. Mantu, M. Asuquo (2020)
Multi-Drug Resistance Pattern of Staphylococcus aureus from Pediatric ward, General Hospital, Ikot-Ekpaw, Mkpat Enin LGA, Akwa-Ibom State, Nigeria
Archives of Clinical Microbiology, 11
MY Tula, AJ Okoro, RO Okojie, O Iyoha (2016)
Antimicrobial susceptibility pattern and plasmid-mediated antibacterial resistance in Staphylococcus aureus and coagulase-negative staphylococci
Highl Med Res J, 16
Adesoji T, Onuh P, Bagu J, Itohan A (2019)
Prevalence and antibiogram study of Staphylococcus aureus isolated from clinical and selected drinking water of Dutsin-Ma, Katsina state, Nigeria
African Health Sciences, 19
Olugbenga Olowe, Olayinka Kukoyi, Samuel Taiwo, O. Ojurongbe, O. Opaleye, Oloyede Bolaji, Abiodun Adegoke, O. Makanjuola, D. Ogbolu, Oyebode Terry, Alli
Infection and Drug Resistance Dovepress Phenotypic and Molecular Characteristics of Methicillin-resistant Staphylococcus Aureus Isolates from Ekiti State, Nigeria
P. Olorunfemi, J. Onaolapo, Y. Ibrahim (2021)
Prevalence and antibiotic susceptibility of community acquired methicillin resistant Staphylococcus aureus from healthy students of University of Jos
Journal of Pharmacy & Bioresources, 17
A. Onanuga, Ocholi Adamu, B. Odetoyin, J. Hamza (2020)
NASAL CARRIAGE OF MULTI-DRUG RESISTANT PANTON VALENTINE LEUKOCIDIN POSITIVE STAPHYLOCOCCUS AUREUS IN HEALTHY INDIVIDUALS OF TUDUN-WADA, GOMBE STATE, NIGERIA
African Journal of Infectious Diseases, 15
E. Ekundayo, Rn Ndubuisi (2015)
In-vitro antimicrobial susceptibility pattern of Staphylococcus aureus isolates in Umuahia, Abia state, Nigeria
African Journal of Clinical and Experimental Microbiology, 16
E Agwu, J Ihongbe, N Inyang (2010)
Prevalence of quinolone-susceptible Pseudomonas aeruginosa and Staphylococcus aureus in delayed-healing diabetic foot ulcers in Ekpoma, Nigeria
Cell Tis Prod, 22
D. Sompolinsky, Y. Zaidenzaig, R. Ziegler-Schlomowitz, N. Abramova (1970)
Mechanism of tetracycline resistance in Staphylococcus aureus.
Journal of general microbiology, 62 3
F. Ayeni, Tombari Gbarabon, C. Andersen, N. Nørskov-Lauritsen (2016)
Comparison of identification and antimicrobial resistance pattern of Staphylococcus aureus isolated from Amassoma, Bayelsa state, Nigeria.
African health sciences, 15 4
C. Udobi, A. Obajuluwa, J. Onaolapo (2013)
Prevalence and Antibiotic Resistance Pattern of Methicillin-Resistant Staphylococcus aureus from an Orthopaedic Hospital in Nigeria
BioMed Research International, 2013
O Obasuyi (2015)
124
Afr J Clin Exp Microbiol, 16
N. Onyeagwara, O. Obasuyi, I. Ottih, J. Akerele (2014)
Nasal carriage of methicillin-resistant Staphylococcus aureus among hospitalized otorhinolaryngological patients in Benin City of Nigeria
Archives of International Surgery, 4
(2022)
Phenotypic Detection of Macrolide, Lincosamide and Streptogramin B resistance among Staphylococcus aureus clinical isolates in A Northern Nigeria Tertiary Hospital
AS Ramalan (2020)
80
Bayero J Pure Appl Sci, 13
A Shariati (2020)
12689
Sci Rep, 10
B. Akanbi, J. Mbe (2012)
Occurrence of Methicillin and Vancomycin Resistant Staphylococcus aureus in University of Abuja Teaching Hospital, Abuja, Nigeria
African Journal of Clinical and Experimental Microbiology, 14
Ajayi Adetutu, Bibi Oritsewehinmi, Oniha Ikhiwili, Atolagbe Moradeke, Anosike Odochi, Onibokun Adeola (2017)
Studies on Staphylococcus aureus Isolated from Pimples.
Pakistan journal of biological sciences : PJBS, 20 7
Will McGuinness, Natalia Małachowa, F. DeLeo (2017)
Vancomycin Resistance in Staphylococcus aureus 
The Yale Journal of Biology and Medicine, 90
Michael Okpara (2003)
Antibiotic resistant Staphylococcus aureus in Abia State of Nigeria
N. Frank-Peterside, M. Mukoro (2010)
The current susceptibility pattern of methicillin resistant Staphylococcus aureus to antibiotics in Port Harcourt
Global Journal of Pure and Applied Sciences, 16
C Chigbu (2013)
374
Afr J Biotechnol, 2
H. Ogefere, G. Umaru, Ephraim Ibadin, R. Omoregie (2020)
Prevalence Of Methicillin-Resistant Staphylococci Among Apparently Healthy Students Attending A Tertiary Institution In Benin City, Nigeria
Nigerian Journal of Basic and Applied Sciences, 27
(2012)
Antibiotic resistance and susceptibility pattern/profile of Staphylococcus aureus and Klebsiella species to popularly—used and readily available antibiotics in Zaria, Nigeria
T. Alli, O.A, Ogbolu (2011)
Distribution of mecA gene amongst Staphylococcus aureus isolates from Southwestern Nigeria
M Egger (1997)
629
BMJ, 315
Franklin Onyeka, D. Nwobodo, Ignatus Umenne, Emmanuel Atada, Chibundu Ojukwu, Maureen Aniekwe, J. Philomena, Joseph Ikem (2020)
Antibiotic Resistance Pattern of Staphylococcus aureus Isolated from Nostrils of Healthy Undergraduates of Madonna University Elele Campus, Rivers State, Nigeria.
M. Bale, S. Babatunde, M. Adedayo, A. Ajiboye, A. Ajao (2018)
Characterization of methicillin-resistant Staphylococcus aureus isolates from apparently healthy individuals in Malete, Kwara state, Nigeria
African Journal of Clinical and Experimental Microbiology
D. Oche, P. Oyegoke, M. Akpudo, B. Olayinka (2021)
Antibiotics Resistance Pattern of Staphylococcus aureus Isolated From In-patients of an Orthopaedic Hospital in North-Western Nigeria
International Journal of Epidemiologic Research
Iroha Ir, E. Okoye, Osigwe Ca, Moses Ib, C. Ejikeugwu, Nwakaeze Ae (2017)
Isolation, Phenotypic Characterization and Prevalence of ESBL-Producing Escherichia Coli and Klebsiella Species from Orthopedic Wounds in National Orthopedic Hospital Enugu (NOHE), South East Nigeria
Journal of Pharmaceutical Care & Health Systems, 2017
I. Emeka-Nwabunnia, K. Ejigeme, O. Oguoma (2019)
Antibiotic resistance pattern of methicillin-resistant Staphylococcus aureus isolated from children under the age of five Years in Anambra State
Nigerian Journal of Biotechnology
D Moher (2009)
264
PloS Med, 151
EE Akortha (2010)
1071
Afr J Microbiol Res, 4
A. Oladipo, O. Oladipo, C. Bezuidenhout (2019)
Multi-drug resistance traits of methicillin-resistant Staphylococcus aureus and other Staphylococcal species from clinical and environmental sources.
Journal of water and health, 17 6
A Onanuga (2005)
1321
Nigeria Afr J Biotechnol, 4
F. Villiers, F. Huygens, A. Rensburg (1989)
Methicillin resistance and beta-lactamase production in Staphylococcus aureus.
South African medical journal = Suid-Afrikaanse tydskrif vir geneeskunde, 75 5
IR Iroha (2017)
1000184
J Pharm Care Health Syst, 4
AH Sadauki, AA Olorukooba, MS Balogun, MM Dalhat, H Waziri, MM Abdulaziz (2022)
Nasal carriage of meticillin-resistant Staphylococcus aureus among children living with HIV attending infectious diseases clinics in Kano
Nigeria Infect Prev Pract, 4
PO Olorunfemi (2020)
131
J Pharm Bioresour, 17
JP Rasigade, F Vandenesch (2014)
Vandenesch, Staphylococcus aureus: a pathogen with still unresolved issues
Infect Genet Evol, 21
O. Fagade, C. Ezeamagu, A. Oyelade, A. Ogunjobi (2010)
Comparative study of antibiotic resistance of Staphylococcus species isolated from clinical and environmental samples.
AU Journal of Technology, 13
A Olowo-Okere (2017)
44
J Med Bacteriol, 6
(2014)
Antimicrobial resistance: global report ton surveillance
Xiao-fang Li, Xin-jian Fan, Xiao-jing Guo, P. Feng, X. Lü, Yan-yu Gao, Y. Xiong, Rujia Yu, Xiaozheng Ding (2006)
[A study on the mechanism of drug resistance in Staphylococcus aureus].
Sichuan da xue xue bao. Yi xue ban = Journal of Sichuan University. Medical science edition, 37 3
S. Hemaiswarya, A. Kruthiventi, M. Doble (2008)
Synergism between natural products and antibiotics against infectious diseases.
Phytomedicine : international journal of phytotherapy and phytopharmacology, 15 8
A. Onanuga, A. Oyi, J. Onaolapo (2005)
Prevalence and susceptibility pattern of methicillinresistant Staphylococcus aureus isolates among healthy women in Zaria, Nigeria
African Journal of Biotechnology, 4
S. Eke, S. Abdulkadiri, C. Okoro, S. Ekoh, Ng Mbachi (2012)
The prevalence and resistivity pattern of Staphylococcus Aureus isolates from apparently healthy University students in Ekpoma, Edo, Nigeria
, 1
JO Isibor (2014)
200
Am J life Sci, 2
OA Olowe, OO Kukoyi, SS Taiwo, O Ojurongbe, OO Opaleye, OS Bolaji (2013)
Phenotypic and molecular characteristics of methicillin-resistant Staphylococcus aureus isolates from Ekiti State, Nigeria
Infect Drug Res, 6
I. Emeka-Nwabunnia, N. Chiegboka, U. Udensi, F. Nwaokorie (2015)
Vancomycin-Resistant Staphylococcus aureus Isolates from HIV Positive Patients in Imo State, Nigeria
Science Journal of Public Health, 3
M. Ugwu, D. Odimegwu, E. Ibezim, C. Esimone (2009)
Antibiotic Resistance Patterns of Staphylococcus aureus Isolated from Nostrils of Healthy Human Subjects in a Southeastern Nigeria Locality
Macedonian Journal of Medical Sciences, 2
I. Oginni, A. Olayinka (2021)
Distribution and Antibiotics Resistance Pattern of Community-Acquired Methicillin-Resistance Staphylococcus aureus in Southwestern Nigeria.
Advances in experimental medicine and biology
YB Ngwai, OR Bakare (2012)
Asymptomatic bacteriuria and antimicrobial susceptibility of Staphylococcus aureus from university students in Keffi, Nigeria
Int J Microbiol Bioinform, 2
A. Moses (2017)
NASAL METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS CARRIAGE IN PRE AND POST-OPERATIVE PATIENTS IN A TERTIARY HEALTH FACILITY IN UYO, SOUTH-SOUTH, NIGERIA
World journal of pharmaceutical research
SC Yah, EO Yusuf, T Haruna (2009)
Patterns of antibiotics susceptibility of isolates and plasmid analysis of Staphylococcus from surgical site infections in Nigeria
Sudan JMS, 3
MI Bale, SK Babatunde, S Awe (2021)
prevalence of methicillin resistant Staphylococcus aureus bacteriuria among pregnant women attending secondary health hospitals in LLorin, Nigeria
J Adv Microbiol, 21
A Onanuga, RO Avosuahi, JA Onaolapo (2005)
Prevalence and susceptibility pattern of methicillinresistant Staphylococcus aureus isolates among healthy women in Zaria
Nigeria Afr J Biotechnol, 4
O. Olufunmiso, Ikpehae Tolulope, C. Roger (2017)
Multidrug and vancomycin resistance among clinical isolates of Staphylococcus aureus from different teaching hospitals in Nigeria
African Health Sciences, 17
T. Ajani, C. Elikwu, V. Nwadike, T. Babatunde, C. Anaedobe, O. Shonekan, C. Okangba, A. Omeonu, B. Faluyi, T. Thompson, E. Ebeigbe, B. Eze, M. Ajani, K. Perelade, M. Amoran, P. Okisor, T. Worancha, J. Ayoade, E. Agbeniga, C. Emmanuel, C. Coker (2020)
Nasal carriage of methicillin resistant Staphylococcus aureus among medical students of a private institution in Ilishan-Remo, Ogun State, Nigeria
African Journal of Clinical and Experimental Microbiology, 21
SC Yah (2009)
810
Sudan JMS, 3
E. Mbim, C. Mboto, U. Edet, C. Umego, U. George, I. Temidayo (2017)
Comparative Evaluation of Methicillin-resistant Staphylococcus aureus (MRSA) Isolates from Hospital and Community Settings in Nigeria
, 4
N Torimiro, SEA Torimiro (2012)
Antibiotic resistance profile in community-associated Staphylococcus aureus strains isolated from a Nigerian peri-urban community
Afr J Biotechnol, 11
M. Falagas, D. Karageorgopoulos, John Leptidis, I. Korbila (2013)
MRSA in Africa: Filling the Global Map of Antimicrobial Resistance
PLoS ONE, 8
C. Ibe, R. Onyeagba, S. Ugochukwu (2014)
Antibiotic Resistance Patterns and Plasmid Profiles of Methicillin Resistant Staphylococcus aureus Isolates from Human Samples.
British microbiology research journal, 4
S. Yah, I. Enabulele, N. Eghafona (2008)
The screening of multi-drug resistance (MDR) susceptibilities of Staphylococcus aureus and Staphylococcus epidermidis to methicillin and vancomycin in teaching hospitals in Nigeria
Sudan journal of medical sciences, 2
Ejikeugwu Chika, N. Joseph, E. Chijioke, E. Peter (2018)
Detection of constitutive- and inducible-clindamycin-resistance in clinical isolates of Staphylococcus aureus from a Federal Teaching Hospital in Abakaliki, Nigeria
, 2
RC Egbuobi (2014)
69
Int J Med Med Sci, 6
RO Akanbi (2013)
10
Afr J Clin Exp Microbiol, 14
BT Bamigboye (2018)
25
Eur J Microbiol Immunol, 8
Shipeng Li, Juan Li, Yanhong Qiao, X. Ning, Ting Zeng, Xu-zhuang Shen (2014)
Prevalence and invasiveness of community-acquired methicillin-resistant Staphylococcus aureus: a meta-analysis.
Indian journal of pathology & microbiology, 57 3
OAT Alli (2011)
9
Afr J Biomed Res, 14
Nneoma Anyanwu, I. Abdullahi, J. Ameh, Elijah Ella (2013)
Molecular detection of PVL, msrA genes and antibiotic susceptibility pattern of staphylococcus aureus from skin and soft tissue infections in Zaria, Nigeria
, 2
M. Egger, G. Smith, Martin Schneider, C. Minder (1997)
Bias in meta-analysis detected by a simple, graphical test
BMJ, 315
Umar (2015)
Biochemical Characterization and Antibiotic Susceptibility Profile of Staphylococcus Aureus Isolated From Patients Attending Barau Dikko Specialist Hospital, Kaduna State, Nigeria
A Khan (2018)
457
Expert Opin Pharmacother, 19
TA Ajani (2020)
311
Afr J Clin Exp Microbiol, 21
Emeakaroha, M. Chioma, Nkwocha, Ihuoma Gertrude, Adieze, Nchekwube Chibuzo, Ifechukwu (2017)
Antimicrobial susceptibility pattern of Staphylococcus aureus, and their nasal and throat carriage among food handlers at the Federal University of Technology, Owerri Nigeria
(2015)
The role of methicillinresistant Staphylococcus aureus in clinical infections in Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, South Western Nigeria
M. Tula, Azuka Okoro, R. Okojie, O. Iyoha (2016)
Complex partial seizure, disruptive behaviours and the Nigerian Legal System
Highland Medical Research Journal, 16
S Yamagishi, Y Nakajima, M Inoue, Y Oka (1971)
Decrease in accumulation of macrolide antibiotics as a mechanism of resistance in Staphylococcus aureus
Jpn J Microbiol, 15
S. Yamagishi, Y. Nakajima, M. Inoue, Y. Oka (1971)
Decrease in accumulation of macrolide antibiotics as a mechanism of resistance in Staphylococcus aureus.
Japanese journal of microbiology, 15 1
R. Egbuobi, C. Wachuku, J. Dike-Ndudim, I. Ogamaka, H. Okorie, M. Nwagbaraocha, J. Amadi, L. Egbuobi, J. Ereh (2014)
Evaluation of antibacterial profile of methicillin resistant Staphylococcus aureus (MRSA) isolated from hospitals in Imo state, Nigeria
International Journal of Medicine and Medical Sciences, 6
A Nworie (2013)
48
Microbiol Res Int, 1
EA Onyebueke, NF Onyemelukwe, DS Oladeji (2019)
Antibiotic susceptibility pattern of Staphylococcus species implicated in urinary tract infection in Enugu state Nigeria
Pharm OnLine, 1
Josephine Anucha, U. Morikwe, M. Ikegbunam, C. Ezejiegu, M. Ugwu (2021)
Age and Gender- Based Antibiotic Susceptibility Patterns of Staphylococcus aureus among HIV Patients in Some Selected Hospitals in Anambra Central, Nigeria
Genetics & Molecular Medicine
M. Struelens (1998)
The epidemiology of antimicrobial resistance in hospital acquired infections: problems and possible solutions
BMJ, 317
FA Ayeni (2015)
1282
Afr Health Sci, 15
O. Osinupebi, J. Osiyemi, A. Deji-Agboola, P. Akinduti, O. Ejilude, S. Makanjuola, N. Sunmola, E. Osiyemi (2018)
Prevalence of Methicillin-resistant Staphylococcus aureus in Abeokuta, Nigeria
H. Ismail, H. Bello, A. Mustafa, A. Adamu (2015)
Multidrug Resistance Pattern of Staphylococcus Aureus Isolates in Maiduguri Metropolis
, 1
T. Ariom, I. Iroha, I. Moses, C. Iroha, UI Ude, A. Kalu (2019)
Detection and phenotypic characterization of methicillin-resistant Staphylococcus aureus from clinical and community samples in Abakaliki, Ebonyi State, Nigeria
African Health Sciences, 19
.. M.A.Bisi-Johnson, .. D.O.Kolawole, .. A.O.Shittu (2005)
Epidemiological Analysis of Clinical Isolates of Staphylococcus aureus in Ile-Ife, Nigeria
Pakistan Journal of Biological Sciences, 8
E. Nwankwo, Magaji Nasiru (2011)
Antibiotic sensitivity pattern of Staphylococcus aureus from clinical isolates in a tertiary health institution in Kano, Northwestern Nigeria
The Pan African Medical Journal, 8
A. Shariati, M. Dadashi, M. Moghadam, A. Belkum, Somayeh Yaslianifard, D. Darban-Sarokhalil (2020)
Global prevalence and distribution of vancomycin resistant, vancomycin intermediate and heterogeneously vancomycin intermediate Staphylococcus aureus clinical isolates: a systematic review and meta-analysis
Scientific Reports, 10
Blessing Ike, M. Ugwu, M. Ikegbunam, D. Nwobodo, C. Ejikeugwu, T. Gugu, C. Esimone (2016)
Prevalence, Antibiogram and Molecular Characterization of Comunity-Acquired Methicillin-Resistant Staphylococcus Aureus in AWKA, Anambra Nigeria
The Open Microbiology Journal, 10
O. Ayepola, N. Olasupo, L. Egwari, K. Becker, F. Schaumburg (2015)
Molecular Characterization and Antimicrobial Susceptibility of Staphylococcus aureus Isolates from Clinical Infection and Asymptomatic Carriers in Southwest Nigeria
PLoS ONE, 10
H. Togt (2003)
Publisher's Note
J. Netw. Comput. Appl., 26
JO Akerele (2015)
1495
Trop J Pharm Res, 14
B. Nwankwo, S. Abdulhadi, A. Magagi, G. Ihesiulor (2009)
Methicillin resistant S. aureus (MRSA) and their antibiotic sensitivity pattern in Kano, Nigeria.
African Journal of Clinical and Experimental Microbiology, 11
N Torimiro (2012)
16071
Afr J Biotechnol, 11
E. Nmema (2017)
Risk Factors for Infection of Staphylococcus aureus: Nasal Carriage, Skin Carriage and Multi-antibiotic Resistance in Healthy Individuals
British journal of medicine and medical research, 21
AT Adesoji (2019)
1385
Afr Health Sci, 19
B. Bamigboye, O. Olowe, S. Taiwo (2018)
Phenotypic and Molecular Identification of Vancomycin Resistance in Clinical Staphylococcus Aureus Isolates in Osogbo, Nigeria
European Journal of Microbiology & Immunology, 8
K. Perrett, T. Nolan, J. McVernon (2013)
A Licensed Combined Haemophilus influenzae Type b-Serogroups C and Y Meningococcal Conjugate Vaccine
Infectious Diseases and Therapy, 2
WA McGuinness (2017)
269
Yale J Biol Med, 90
A. Akinduti, J. Osiyemi, T. Banjo, O. Ejilude, M. El-Ashker, A. Adeyemi, Y. Obafemi, P. Isibor (2021)
Clonal diversity and spatial dissemination of multi-antibiotics resistant Staphylococcus aureus pathotypes in Southwest Nigeria
PLoS ONE, 16
A. Onanuga, Godwin Awhowho (2012)
Antimicrobial resistance of Staphylococcus aureus strains from patients with urinary tract infections in Yenagoa, Nigeria
Journal of Pharmacy & Bioallied Sciences, 4
S Yamagishi (1971)
39
Jpn J Microbiol, 15
SC Yah (2007)
257
Int J Biol Chem Sci, 2
A. Khan, B. Wilson, Ian Gould (2018)
Current and future treatment options for community-associated MRSA infection
Expert Opinion on Pharmacotherapy, 19
A. Onanuga, J. Onaolapo (2008)
Antimicrobial Susceptibility of Community-associated Staphylococcus aureus Isolates from Healthy Women in Zaria, Nigeria
Tropical Journal of Pharmaceutical Research, 7
Akortha, M. Ikenebomeh (2010)
Nasal colonization of symptomatic pneumonia patients in University of Benin Teaching Hospital, Benin City, Nigeria by multiple antibiotic resistant Staphylococcus aureus
African Journal of Microbiology Research, 4
D. Ogbolu, O. Alli, L. Bello, A. Ibrahim (2015)
Emergence of Vancomycin Intermediate Staphylococcus aureus (VISA) in Clinical Isolates of Methicillin Resistant S. aureus from South Western Region of Nigeria
International Journal of Tropical Disease & Health, 10
AS Ramalan, FN Joseph, MC Owoseni, Y Ya’aba, A Chuku (2020)
Prevalence and antibiotic resistance profile of Staphylococcus aureus and Escherichia coli among patients attending urology Clinic of Dalhatu Araf specialist hospital (dash) Lafia, Nasarawa state, Nigeria
Bayero J Pure Appl Sci, 13
S. Ibrahim, Abubakar Adam, A. Aliero, S. Umar (2018)
Prevalence and Antibiotic Sensitivity Pattern of Staphylococcus aureus Isolated from Wound and Otitis Media among Patients Attending Aminu Kano Teaching Hospital, Kano, Nigeria
Microbiology Research Journal International
Odu Nn, Okonko Io (2012)
Nasal carriage and antibiotics susceptibility of Staphylococcus aureus in healthy students of University of Port Harcourt, Rivers State, Nigeria
XF Li (2006)
365
Sichuan Da Xue Xue Bao Yi Xue Ban, 37
L. Badger-Emeka, P. Emeka, U. Dibua (2014)
Plasmid profile of multi antibiotic resistant staphylococcus aureus isolated from diabetic wounds from patients at Nsukka, South-eastern, Nigeria
African Journal of Biotechnology, 13
A. Deji-Agboola, M. Popoola, T. Atoyebi, K. Egberongbe (2014)
Prevalence Of Methicillin Resistant Staphylococcus Aureus From Clinical Specimens In Ibadan , Nigeria
A Onanuga (2008)
929
Trop J Pharm Res, 7
NE Onwubiko (2011)
1
Pan Afr Med J, 8
O. Alli, D. Ogbolu, J. Mustapha, R. Akinbami, A. Ajayi (2012)
The non-association of Panton-Valentine leukocidin and mecA genes in the genome of Staphylococcus aureus from hospitals in South Western Nigeria.
Indian journal of medical microbiology, 30 2
LI Badger-Emeka, PM Emeka, UME Dibua (2014)
Plasmid profile of multi antibiotic resistant Staphylococcus aureus isolated from diabetic wounds from patients at Nsukka, South astern, Nigeria
Afr J Biotectnol, 13
A. Olowo-Okere, R. Atata, Agboola Abass, A. Shuaibu, Ungokore Yahya, N. Tanko (2017)
Incidence and Antibiotic Susceptibility Profile of Staphylococcus aureus Isolates from Wounds of Patients at Specialist Hospital, Sokoto, Nigeria
Journal of Medical Bacteriology, 6
A. Onanuga, Darlington Eboh, Gloria Okou (2019)
Antibiogram and Virulence Characteristics of Multi-drug Resistant Staphylococcus aureus from Nasal Cavity of Healthy Students of Niger Delta University, Amassoma, Bayelsa State, Nigeria
JOURNAL OF CLINICAL AND DIAGNOSTIC RESEARCH
A. Obajuluwa, B. Olayinka, G. Adeshina, J. Onaolapo, N. Afolabi-Balogun (2015)
Plasmid profile of Staphylococcus aureus from orthopaedic patients in Ahmadu Bello University Teaching Hospital Zaria, Nigeria
African Journal of Microbiology Research, 9
Inyang U.C (2017)
NASAL METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS CARRIAGE IN PRE AND POST-OPERATIVE PATIENTS IN A TERTIARY HEALTH FACILITY IN UYO, SOUTH-SOUTH, NIGERIA
S. O’Malley, F. Emele, F. Nwaokorie, N. Idika, A Umeizudike, I. Emeka-Nwabunnia, B. Hanson, R. Nair, S. Wardyn, T. Smith (2015)
Molecular typing of antibiotic-resistant Staphylococcus aureus in Nigeria.
Journal of infection and public health, 8 2
J. Osiyemi, O. Osinupebi, P. Akinduti, O. Ejilude, S. Makanjuola, N. Sunmola, E. Osiyemi (2018)
Antibiotic Resistance Profile of Methicillin-Resistant Staphylococcus aureus in Abeokuta, Nigeria
, 9
JP Rasigade (2014)
510
Infect Genet Evol, 21
M. Ugwu, A. Co, Ibezim Ec, C. Esimone (2016)
Antimicrobial Evaluation of Methicillin-Resistant Staphylococcus AureusNasal Carriage amongst Healthy Students in Agbor, Delta State, Nigeria
Archives of Clinical Microbiology, 7
Chijioke Nsofor (2015)
Nasal Carriage of Staphylococcus Aureus among Apparently Healthy School Children in Owerri Metropolis, Nigeria
, 2
S. Yah, E. Yusuf, T. Haruna (2009)
Patterns of antibiotics susceptibility of isolates and plasmid analysis of Staphylococcus from surgical site infections in Nigeria.
International Journal of Biological and Chemical Sciences, 3
A Onanuga (2011)
176
Afr Health Sci, 11
LI Badger-Emeka (2014)
4148
Afr J Biotectnol, 13
Adegoke, A. Ayodeji, Komolafe, A. Omoniyi (2009)
Multi-drug resistant Staphylococcus aureus in clinical cases in Ile-Ife, Southwest Nigeria
International Journal of Medicine and Medical Sciences, 1
Stanley, U. Haa, Ibezim (2014)
Prevalence and Antibiotic Susceptibility of Staphylococcus Aureus and Other Staphylococcal Infections in Pregnant Women Attending Antenatal Clinic in a Tertiary Hospital in Port Harcourt, Nigeria
(2009)
use, resistance and containment baseline survey: syntheses of findings

Publisher: Springer Journals
Copyright: Copyright © The Author(s) 2023
eISSN: 2047-2994
DOI: 10.1186/s13756-023-01243-x
Publisher site: See Article on Publisher Site

Abstract

Background Rapid emergence of multidrug resistant Staphylococcus aureus has resulted to difficulty in treatment of infections caused by such strains. The aim of this meta-analysis study was to determine the pooled prevalence of resistance of S. aureus to different antibiotics in Nigeria. Methods Literature search for studies was done using Google scholar, PubMed, Science direct, and African Journal Online. The prevalence of S. aureus resistance to different antibiotics was evaluated using the meta-analysis propor - tion command in MedCalc software version 20.0 adopting a rand effect model. I statistic and Egger test in MedCalc was used to evaluate the heterogeneity and the presence of publication bias among studies respectively. Results A total of 40, 682 studies were retrieved through the database search of which 98 studies met the study inclusion criteria. Prevalence of resistance of S. aureus to different antibiotics ranges from 13 to 82%. Results showed a very high degree of resistance to penicillin G (82% [95% confidence interval (CI) 61%, 0.96%]), cloxacillin (77% [95% CI 64%, 88%]), amoxacillin (74% [95% CI 66%, 81%]), cefuroxime (69% [95% CI 51%, 85%]), ampicillin (68% [95% CI 53%, 81%]). Moderately resistance to erythromycin (47% [95% CI 40%, 53%]), chloramphenicol (47% [95% CI 37%, 56%]), methicillin (46% [95% CI 37%, 56%]), ofloxacin (24% [95% CI 18%, 31%]) and rifampicin 24% [95% CI 6%, 48%]). Low resistance was observed in vancomycin 13% (95% CI 7%, 21%). For each individual meta-analysis, high heterogeneity was observed with I range (79.36–98.60%) at p-values ≤ 0.01). Egger’s tests for regression intercept in funnel plots indicated no evidence of publication bias. Conclusion This meta-analysis study established that S. aureus in Nigeria has developed resistance to commonly used antibiotics such as the beta-lactam class antibiotics, sulphonamides, tetracyclines, chloramphenicol, and vanco- mycin. Hence it is imperative to develop programs to promote rational use of antimicrobial agents, infection preven- tion and control to reduce the incidence of antimicrobial resistance. Keywords Antibiotic resistance, Meta-analysis, Nigeria, Staphylococcus aureus Background Staphylococcus aureus (S. aureus) is well adapted to vari- ous environments due to their metabolic versatility and *Correspondence: pharmic resistance ability. S. aureus colonize the skin Christian Kelechi Ezeh ezechristian.kelechi@gmail.com and nasopharyngeal membranes as normal microbiota Department of Microbiology, University of Nigeria, Nsukka, Enugu State, in healthy individuals [1]. However, they cause myriad of Nigeria detrimental infections when they invade the internal tis- Department of Pharmaceutical Microbiology, University of Nigeria, Nsukka, Enugu State, Nigeria sues or enter the bloodstream. S. aureus is an important © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 2 of 22 pathogen involved in both hospital-acquired and com- using the appropriate studies that rely solely on S. aureus munity-acquired infections and causes many infectious from the title. The prevalence of resistance of S. aureus to diseases ranging from mild skin and soft tissue infec- various routinely used antibiotics in Nigeria is a country tions, bones and joint infections, infective endocarditis, wide study as it covers studies from the six geo-political cardiovascular disorders, osteomyelitis, bacteremia, and regions of Nigeria. Meta-analysis was adopted because it fatal pneumonia in both healthy and individuals with is a quantitative study of pooled prevalence of resistance underlying diseases [2]. The high incidence of both com - of S. aureus to routinely use antibiotics in Nigeria. munity and nosocomial staphylococcal infections coin- cide with the emergence of multidrug resistant S. aureus which renders antibiotic treatments ineffective [3]. Search strategy S. aureus has become resistant to various antibiotics Electronic search engines including Google scholar, Pub- over the past years especially to the beta-lactam class Med, ScienceDirect, and African Journal Online (AJOL) of antibiotics [4]. Emergence of methicillin resistant were used to search for available studies from 23rd March S. aureus (MRSA) and vancomycin resistant S. aureus to May 2022. Relevant key words such as Staphylococcus, (VRSA) constitutes a serious global public health prob- antibiotic resistance, antibacterial resistance, antimicro- lem. Currently, VRSA and MRSA strains are classified bial resistance, drug resistance, drug susceptibility, Nige- as very potent and dangerous agents that can potentially ria were used during the search. These key words were cause devastating damage worldwide in the absence of used in different combinations (Staphylococcus OR S. effective treatment options [5]. aureus AND antibiotic resistance OR antibacterial resist- Various mechanisms of resistance utilized by S. aureus ance OR antimicrobial resistance OR drug resistance include: production of beta-lactamase enzymes to deac- AND Nigeria) in various electronic databases using the tivate beta-lactam antibiotics, efflux pump for extruding Boolean operators. The reference lists of included articles antibiotics such as tetracyclines [6], reduced accumula- were also check to identify studies relevant to the current tion of macrolides antibiotics [7], production of aminogly- study. cosides modifying enzymes to inactivate aminoglycoside antibiotics, alteration of DNA gyrase and topoisomerase IV expression of floroquinolones antibiotics, and expression of Inclusion and exclusion criteria Mec genes which alters penicillin binding proteins [8]. The titles of search results of all retrieved articles were In Nigeria, the prevalence of multi-drug resistant path- screened independently by two authors with the aim of ogens continue to be on the increase due to several fac- including studies that address the research question. The tors such as drug misuse, self medication, lack of trained articles were inserted into Zotero version 5.0.95.1 refer- medical personnel, and poverty. As the world battles encing application which helped in detecting duplicate the persistent rise in antimicrobial resistance (AMR), it articles. The title of the study which solely focused on is pertinent that adequate data and information about prevalence of antimicrobial resistance of S. aureus was AMR is known which can serve as the basic foundation grouped as eligible for inclusion. S. aureus resistance for setting out effective interventions to contain the cri - in any state in Nigeria and studies only done in Nigeria sis of AMR. From the literature, no prior meta-analysis represented in the title is the first criteria for inclusion. has been done on S. aureus resistance to different anti - However, studies that focused on many microbial strains biotics routinely use in Nigeria. Due to the various infec- antimicrobial resistance were excluded. tions caused by S. aureus, it is pertinent to determine In general, retrieved studies selected from predefined the pooled prevalence of resistance of S. aureus to vari- criteria were screened further using the inclusion cri- ous routinely used antibiotics in Nigeria. This will help teria: studies that were research articles and used cross in improving treatment options and enlighten the popu- sectional design, studies that used human samples, stud- lace on the menace and the possible cause of treatment ies that conducted antimicrobial susceptibility tests using failures due to the increasing rise of multidrug resistant the Clinical Laboratory Standard Institute (CLSI) guide- strains. The aim of this meta-analysis was to determine lines, studies written in English language and studies with the pooled prevalence of S. aureus resistance to various full text. routinely used antibiotics in Nigeria. Exclusion criteria in this meta-analysis include: studies conducted on non-human samples, studies with isolates below 20, duplicate studies, studies that did not conduct Methods antimicrobial susceptibility tests using the Clinical Labo- Study design ratory Standard Institute (CLSI) guidelines studies not Meta-analysis was adopted to evaluate the prevalence of written in English, and review articles. S. aureus of resistance to various antibiotics in Nigeria E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 3 of 22 Data extraction the study is considered as having no significant influence Relevant data such as name of author (s) and publica- on the overall estimate and vice versa. tion year, study design, study place, clinical sample size, isolate source, total number of Staphylococcus aureus Results isolates tested in each research article, and total No. of Characteristics of included studies isolates resistant each antibiotics. In situations where the Studies search record from electronic databases yielded proportion of susceptible isolates was reported, then the 40, 682 of which 35, 400, 2, 180, 1,706, and 1396 were No. of resistant Staphylococcus aureus isolates was cal- from Google scholar, AJOL, PubMed, and Science Direct, culated by subtracting the percentage susceptibility from respectively. Articles from Google Scholar gave 35,400 100 and then dividing the result by 100 and multiplying results comprising of many studies irrelevant or that does to the total number of isolates. However, in situation not fit to the study aim; hence, they were screened ran - where the proportion of the resistant isolates was given, domly from titles alone. Screening of the titles reduced then the No. of resistant Staphylococcus aureus isolates the number of eligible articles to 134 for full text assess- was calculated by dividing the proportion of the resistant ment. After going through the full texts, 36 articles were isolates by 100 and multiply with the total number of iso- excluded (reported small number of isolates and iso- lates. The formula is given as thus: lates not from human samples). Thus, 98 studies met the number of resistant isolates Prevalence of resistance(%) = × 100 (1) total number of isolates To ascertain the reporting of all relevant information inclusion criteria of the study (Fig. 1). in this meta-analysis, we followed the Preferred report- About 46, 640 S. aureus isolates were tested against ing Items for Systematic Review and Meta-analysis different antibiotics and 23,048 isolates were resistant to (PRISMA) [9] (Additional file 1: S1) guidelines. various antibiotics. Isolates sources include: nasal, blood, vaginal, ear, wound, urine, throat, pimples, hand, and mixed samples were collected from both symptomatic patients [61] and asymptomatic people [37]. Eighty six Statistical analysis procedures studies used primary data while twelve used records from In this meta-analysis, statistical analyses were performed hospitals. The characteristics of each study included is using MedCalc statistical software version 20.0.1. The summarized Table 1. pooled prevalence of antibiotic resistance of S. aureus was evaluated using the meta-analysis proportion com- Heterogeneity survey and publication bias mand in MedCalc. A total of 23 separate meta-analyses The included studies were conducted in the six geo-polit - were carried out to evaluate the pooled prevalence of S. ical zones of Nigeria; a total of 98 studies comprising of aureus resistance to 23 different antibiotics. Between 6 26 from South South, 23 South West, 20 South East, 18 and 77 studies were included in the 23 different meta- North West, 8 North Central and 3 North East. Quality analyses. I statistic command in MedCalc was used to assessment (risk of bias) was done in line with the follow- evaluate the heterogeneity among the included stud- ing criteria: studies which used CLSI guideline for anti- ies. Random effect and fixed effect are two models used biotic resistant assessment, studies that used more than to estimate pooled prevalence in meta-analysis. In this 20 S. aureus isolates and studies that used adequate sam- study, due to the characteristically high heterogeneity of ple representative of the region where testing was done. the included studies, the random effect model was used Agar diffusion based method was used to determine the for meta-analysis at 95% CIs. Egger test was employed for resistance level of S. aureus isolates in all included stud- assessing the presence of publication bias [10]. ies. High heterogeneity was observed for each of the The Freeman-Tukey double arcsine transformation was meta-analyses performed with I ranging from 79.36 used to ensure studies which report proportions near or to 98.60%; at p-values ≤ 0.01). This is due to vast differ - at 0 and 1 were not being excluded. In addition, studies ence in sample sizes; some studies used 20 isolates while that report unusually high prevalence of resistance when some used 400 isolates which impacted on the resistance compared to others, a sensitivity analysis was perform profile of each antibiotic. Also, number of clinical sam - by removing the studies. If the point estimate of pooled ples and recovered S. aureus isolates differ in all studies prevalence after removing a study that reported unusu- and these disparities resulted in high heterogeneity. More ally high prevalence of resistance lies within the 95% CI studies were conducted in the Southern (South South, of the overall pooled estimate for all studies combined, Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 4 of 22 Fig. 1 PRISMA flowchart for the selection and screening of eligible studies E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 5 of 22 Table 1 Characteristics of included studies Reference Study Study place Data type Setting and sample Sample size No of Antibiotics used source recovered isolates [11] Akortha and Iken- South south (Benin) Primary, Hospital: Nasal 52 20 CPR, TET, CHL, ERY, AMP, ebomeli, 2010 OFL [12] Idris et al., 2018 Northwest (Kano) Primary Hospital: Blood 195 MET, CPR, TET, ERY, GEN, CLIN, CEF [13] Stanley et al., 2013 Southsouth (Portha- Primary Hospital: Vaginal 265 74 MET, CPR, TET, ERY, AMP, court) swab GEN [14] Odu and Okonkwo, Southsouth (Portha- Primary Urban:Nasal 100 32 MET, CIPRO, TET, ERY, 2012 court) AMP, GEN, CLIN, CXC, COT, STR [15] Isibor and Otabor, Southsouth (Edo) Primary Urban: Nasal 100 32 AMO, CTR, CRX [16] Nworie, 2013 Southeast (Ebonyi) Primary Urban: Nasal 87 20 VAN, CPR, TET, ERY, AMP, OFL, GEN, COT, CTR [17] Egbuobi et al., 2014 Southeast (Imo) Primary Hospital: Different 200 76 MET clinical samples [18] Olowo-Okere et al., Northwest Primary Hospital: Wound 38 20 CPR, ERY, AMO, GEN, 2017 NOR [19] Olorode et al. 2021 Southsouth (Bayelsa) Primary Hospital: Different 250 25 MET, CPR, CHLERY, AMP, clinical samples AMO, GEN, RIF, STR, NOR [20] Onanuga and Southsouth (Bayelsa) Primary Hospital: Urine 200 46 VAN, CPR, TET, CHL, Awhowho, 2012 AMP, OFL, GEN, COT, AUG, CRX, CEF [21] Ayodeji and Omoniyi, Southwest (Ogun) Primary Hospital; Different 107 107 VAN, CPR, TET, ERY, AMP, 2009 clinical samples AMO, GEN, CXC, COT, STR, CAZ, PEN [22] Onanuga and Nortwest (Kaduna) Primary Urban: Urine 150 54 VAN, MET, CPR, AMP, Onaolapo, 2008 OFL, GEN, CLIN [23] Chigbu and Ezeronye, Southeast (Abia) Primary Hospital: Ear and 70 38 CPR, TET, CHL, ERY, AMP, 2003 nasal AMO, GEN, RIF, CXC, PEN [24] Enabule et al., 2007 Southsouth Primary Hospital: Urine 80 CPR, TET, ERY, AMP, GEN [25] Yah et al., 2009 Southsouth (Benin) Primary Hospital: Wound 153 86 CPR, TET, CHL, ERY, GENCXC, COT [26] Onwubiko and Saidiq, Northwest (Kano) Secondary Hospital: Different 150 CPR, TET, ERY, AMP, 2011 clinical samples AMO, OFL, GENCXC, STR, PEN, CAZ [27] Onanuga and Teme- SOuthsouth Primary Urban: Nasal 120 40 VAN, CPR, CHL, ERY, die, 2011 AMP, AMO, OFL, AUG, CRX, CEF [28] Onanuga et al., 2005 Northcentral (Abuja) Primary Hospital: Urine 150 60 VAN, MET, CPR, AMP, OFL, GEN, CLIN [29] Akanbi and Mbe, Northcentral (Abuja) Primary Hospital: Different 214 VAN, MET, ERY, AMP, 2013 clinical samples OFL, GEN [30] Terry et al., 2011 Nortwest Secondary Hospital: Different 194 MET, TET, CHL, ERY, clinical samples AMP, GEN, STR, CAZ, PEN, CTR [31] Iroha et al., 2012 Southeast (Ebonyi) Primary Hospital: Nasal 105 VAN, CPR, ERY, CLIN, CXC, COT, PEN [32] Eke et al., 2012 Southsouth (Edo) Primary Urban: Nasal and ear 100 39 MET, CPR, TET, AMP, PEN [33] Ekundayo and Southeast (Abia) Primary Hospital: Different 100 113 TET, CHL, ERY, AMP, Ndubuisi, 2015 clinical samples GEN, CXC, COT, AUG, STR, PEN [34] Obasuyi and Akerele, Southsouth (Edo) Secondary Hospital: Different 75 MET 2015 clinical samples Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 6 of 22 Table 1 (continued) Reference Study Study place Data type Setting and sample Sample size No of Antibiotics used source recovered isolates [35] Akerele et al., 2015 Southsouth (Edo) Primary Urban: Nasal 200 99 MET, CPR, ERY, AMP, AMO, GEN, STR, CTR [36] Badger-Emeka et al., Southeast 9Enugu) Primary Hospital: Wound 34 34 VAN, MET, TET, CHL, ERY, 2014 AMO, OFL, GEN, CXC, COT, AUG, STR [37] Ayeni et al., 2015 Southsouth (Bayelsa) Secondary Urban: Nasal 185 185 ERY, AMP, PEN, CTR, NOR [38] Torimino et al., 2012 Southwest (Oyo) Primary Urban: Different clini- 50 40 CPR, TET, CHL, ERY, cal samples AMO, OFL, GENCXC, COT, STR, CTR [39] Bale et al., 2019 Southwest (Kwara) Primary Urban: Nasal 113 42 TET, ERY, OFL, CXC, AUG, CTR, CTR [40] Adesoji et al., 2019 Nortwest (Katsina) Primary Urban: Different clini- 120 120 ERY, OFL, GEN, CXC, cal samples AUG, CAZ, CRX, CTR [41] Ariom et al., 2011 Southeast (Ebonyi) Primary Hospital: Different 709 84 MET, CPR, TET, GEN, clinical samples CAZ, PN [42] Ajani et al., 2020 Southwest (Ogun) Primary Urban: Nasal 200 20 MET [43] Olonrunfemi et al., Northcentral Primary Urban: Urine 217 73 MET [44] Onanuga et al., 2021 Northeast Primary Urban: Nasal 262 46 TET, ERY, AMO, GENCOT [45] Ramalan et al., 2020 Northcentral Primary Hospital: Urine 202 62 CPR, CHL, ERY, AMP, (Nasarawa) AMO, GEN, STR [46] Udobi et al., 2013 Northwest (Kaduna) Primary Hospital: Skin and 217 69 CPR, AMO, GEN, CTR wound [47] Obasola et al., 2010 Southwest (Oyo) Primary Urban: Different clini- 50 50 TET, CHL, ERY, AMO, cal samples GENCXC, COT, AUG [48] Moses et al., 2017 Southsouth (Uyo) Primary Hospital: Nasal 130 41 VAN, CPR, TET, ERY, GENCLIN, CEF [49] Nsofor et al., 2015 Southeast (Imo) Primary Urban: Nasal 270 152 TET, CHL, ERY, GEN [50] Adetayo et al., 2014 Southwest (Oyo) Primary Hospital: Different 150 66 VAN clinical samples [51] Ejikeugwu et al., 2018 Southeast (Ebonyi) Secondary Hospital: Different 39 ERY, GEN, CLIN, CXC, clinical samples CEF [52] Anucha et al., 2021 Southeast (Anambra) Primary Hospital: Urine 236 62 VAN, TET, ERY, AMO, OFL, GEN, CRX [53] Agwu et al., 2010 Southsouth (Edo) Primary Hospital: Wound 220 66 VAN, RIF, CRX, CTR [54] Adesida et al., 2016 Southwest (Lagos) Primary Urban: Nasal 230 50 ERY, AMO, OFL, GEN, CXC, CAZ, CRX, CTR [55] Mofolorunsho et al., Northcentral (Kogi) Primary Hospital: Different 100 22 CPR, TET, ERY, AMO, 2015 clinical samples OFL, GEN, COT, STR [56] Osiyemi et al., 2018 Southwest (Ogun) primary Hospital: Different 338 161 VAN, CPR, TET, ERY, OFL, clinical samples GEN, COT, AUG, CAZ, CEF, CTR [57] Ibe et al., 2014 Southeast (Abia) Primary Hospital: Different 84 69 MET clinical samples [58] Onaolapo et al., 2016 Northwest(Kaduna) Primary Hospital: Wound and 65 22 VAN, CPR, ERY, AMP, skin AMO, CLIN, CEF, CTR [59] Ugwu et al., 2016 Southsouth (Delta) Primary Urban: Nasal 300 218 MET [60] Tula et al., 2016 Northeast Primary Hospital: Different 100 45 CPR, AMO, OFL, GEN, clinical samples CXC, CAZ, CRX, CTR [61] Anyanwu et al., 2013 Northwest (Kaduna) Primary Hospital: Skin 400 69 VAN, CHL, CAZ, CTR [62] Onyeagwara et al., Southsouth (Edo) Primary Hospital: Nasal 50 25 CPR, ERY, AMP, AMO, 2014 GENSTR, CAZ [63] Ngwai and Bakare, Northcentral Primary Urban: Urine 300 60 CHL, TET, ERY, AMO, 2012 (Nasarawa) GENCXC, STR E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 7 of 22 Table 1 (continued) Reference Study Study place Data type Setting and sample Sample size No of Antibiotics used source recovered isolates [64] Umar et al., 2015 Nortwest (Kaduna) Primary Hospital: Skin and 40 34 CPR, CHL, ERY, AMO, nasal GEN, RIF, STR [65] Obajuluwa et al., 2015 Northwest (Kaduna) Primary Hospital: Wound and 100 39 VAN, CPR, ERY, AMP, skin AMO, GENCEF, CTR [66] Iduh et al., 2015 Southsouth Primary Hospital: Wound 300 64 TET, AMP, GEN, STR [67] Ibanga et al., 2020 Southsouth (Akwa- Primary Hospital Different 100 28 TET, CHL, ERY, AMO, Ibom) clinical samples GEN, STR [68] Emeakaroha et al., Southeast (Imo) Primary Urban: Nasal and 54 28 CHL, ERY, AMO, AMP, 2017 throat COT, CRX, PEN [69] Bisi-Johnson et al., Southwest (Oyo) Primary Hospital: Different 86 97 TET, CHL, AMP, AMO, 2005 clinical samples GENCXC, STR, PEN [70] Ayepola et al., 2015 Southwest (Lagos) Secondary Hospital:Nasal ` 217 TET, GEN, PEN [71] Odogwu et al., 2019 Northcentral (Abuja) Primary Hospital: Different 360 55 CPR, ERY, AMP, GEN, RIF, clinical samples CLIN, STR, TRIM [72] Adeiza et al., 2020 Northwest (Sokoto) Primary Hospital: Nasal 378 33 TET, CHL, ERY, GEN, CLIN, CAZ, CEF, TRIM [73] Ismail et al., 2015 Northeast (Borno) Primary Urban: Different clini- 110 42 CPR, CHL, ERY, AMO, cal samples GEN, RIF, STR, NOR [74] Ibrahim et al., 2018 Northwest (Kano) Primary Hospital: Wound 150 71 CPR, TET, ERY, GEN, and ear CLIN, CEF, TRIM, CTR [75] Olowe et al., 2013 Southwest (Ekiti) Primary Hospital: Different 208 VAN, MET, TET, ERY, clinical samples GEN, PEN, CEF [76] Oche et al., 2021 Northwest (Kano) Primary Hospital: Different 140 26 MET, CPR, TET, ERY, AM, clinical samples GEN, CEF, TRIM, NOR [77] Onelum et al., 2015 Southwest (oyo) Primary Hospital: Different 246 102 MET, CHL, GEN, CLIN, clinical samples CAZ, CEF [78] Akinduti et al., 2021 Southwest (Ogun) Primary Hospital: Different 256 68 VAN, CPR, TET, ERY, clinical samples AMO, OFL, GEN, CAZ, CRX, TRIM [79] Oladipo et al., 2019 Southwest (Osun) Primary Hospital: Different 25 MET, CPR, ERY, AMO, clinical samples GEN, OFL, CXC, CEF, CRX [80] Ogefere et al., 2020 Southsouth (Edo) Secondary Urban: Different clini- 556 MET cal samples [81] Motayo et al., 2012 Southwest (Ogun) Hospital: Different 50 MET, TET, CHL, ERY, clinical samples AMO, GEN, CTR [82] Onyeka et al., 2021 Southsouth (Rivers) Primary Urban: 150 78 ERY, OFL, GENCXC, AUG, CAZ, CRX, CTR [83] Ugwu et al., 2009 Southeast (Enugu) Primary Nasal 100 53 TET, CHL, AMO, GEN, COT, AUG [84] Nsofor et al., 2016 Southeast (Abia) Primary Hospital: Different 424 104 CPR, TET, CHL, ERY, AMP, clinical samples CAZ, PEN [85] Mbim et al., 2017 Southsouth (Cross Primary Hospital: Nasal 150 42 MET, CPR, CHL, ERY, river) AMO, GEN, RIF, CEF, NOR [86] Ogbolu et al., 2015 Southwest (Osun) Secondary Hospital: Different 116 VAN, TET, ERY, GEN, CAZ clinical samples [87] Osinupebi et al., 2018 Southwest (Ogun) Primary Hospital: Different 338 161 VAN, CPR, TET, ERY, OFL, clinical samples GEN, COT, AUG, CAZ, CEF, CTR [88] Ajoke et al., 2012 Northcntral (Plateau) Primary Urban: Nasal 200 98 TET, ERY, AMP, AMO, GEN [89] Onyebueke et al., Southeast (Enugu) Primary Hospital: Urine 818 89 CPR, ERY, AMO, GEN, 2019 STR, NOR Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 8 of 22 Table 1 (continued) Reference Study Study place Data type Setting and sample Sample size No of Antibiotics used source recovered isolates [90] Adetutu et al., 2017 Southwest (Ota) Primary Urban: Pimple 20 20 TET, CHL, ERY, GEN, CXC, COT, AUG, STR [91] Bale et al., 2021 Southwest (Kwara) Primary Hospital: Urine 856 56 MET, CPR, TET, CHL, ERY, AMO, OFL, GEN, AUG, CEF, CTR [92] Nmema, 2017 Southwest (Ondo) Primary Urban: Skin and nasal 80 34 ERY, GEN, CXC, AUG, CAZ, CRX, CTR [93] Ike et al., 2016 Southeast (Anambra) Primary Hospital: Nasal and 261 142 MET hand [94] Ugwu et al., 2015 Southeast (Anambra) Primary Hospital: Nasal 100 68 CPR, ERY, AMP, AMO, OFL, GEN, COT, STR, CTR [95] Emeka- Nwabunnia Southeast (Imo) Primary Urban:Different clini- 59 VAN et al., 2015 cal samples [96] Alli et al., 2012 Southwest (Osun) Secondary hospital: different 116 VAN, TET, ERY, AMO, samples GEN, CAZ [97] Sadauki et al., 2022 Northwest (Kano) Primary Hospital: Blood 214 40 MET, CPR, GEN, PEN, CTR [98] O’ Malley et al., 2015 Southwest (lagos) Primary Hospital: Different 73 38 TET, ERY, GEN clinical samples [99] Emeka- Nwabunnia Southeast (Anambra) Primary Hospital: Different 83 25 MET et al., 2019 clinical samples [100] Ako-Nai et al., 2005 Southwest (Osun) Primary Urban: Different clini- 112 CPR, TET, CHL, ERY, GEN cal samples [101] Frank-Peterside and Southsouth (Rivers) Primary Hospital: Different 50 VAN, MET Mukoro, 2010 clinical samples [102] Yahaya et al., 2022 Northwest (Kano) Primary Hospital: Different 200 31 CPR, CHL, ERY, CLIN, clinical samples COT, CEF [103] Onanuga et al., 2019 Southsouth (Bayelsa) Primary Urban: Nasal 390 47 CPR, TET, ERY, AMO, GEN, COT [104] Ogini and Olayinka, Southwest (Oyo) Primary Urban: Nasal 700 223 CPR, TET, ERY, AMO, 2021 GEN [105] Nwankwo et al., 2010 Northwest (Kano) Secondary Hospital: Different 185 MET, CPR, AMO, OFL, clinical samples GEN, CAZ, CTR [106] Olufunmiso et al., Southwest (Ogun) Primary Hospital: Different 200 200 ERY, OFL, GEN, COT, 2017 clinical samples AUG, CAZ, CRX, CTR [107] Olajide et al., 2012 Northwest (Kano) Secondary Hospital: Different 100 ERY, AMO.CRX, NOR clinical samples VAN Vancomycin; MET Meticilin; CPR Ciprofloxacin; TET Tetracycline; COT Cotrimoxazole; CHL Chloramphenicol; ERY Erythromycin; PEN Penicillin; CLIN Clindmycin; AMO Amoxicillin; AMP Ampicillin; GEN Gentamycin; CTR Ceftriaxone; AUG Amoxicillin/clavulanic acid; CAZ Ceftazidime; CRX Cefuroxime; CXC Cloxacillin; NOR Norfloxacillin; RIF Rifampicin; STR Streptomycin; OFL Ofloxacin; TRIM Trimethroprim; CEF Cefoxitin South West, and South East) part of Nigeria giving rise test rule which state that ‘P-value less than 0.05 indicates to high heterogeneity. Studies were done in different hos - the presence of publication bias’. pitals within these regions with different prevalence esti - mates. Random sampling was used in most of the studies Prevalence of S. aureus resistance to different antimicrobial and different clinical samples were collected. More than agents one clinical sample per patient was collected in 51 stud- In this meta-analysis, the pooled prevalence of S. aureus ies while one clinical sample was collected per patient in resistance to twenty-three different antibiotics and the 47 studies. Egger’s test for a regression intercept gave a number of studies included in each meta-analysis is sum- p-value range of 0.06 to 0.99, indicating no evidence of marized in Table 2. Prevalence of resistance of S. aureus to publication bias (Additional file 2: S2) following Eggers’ E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 9 of 22 Table 2 Pooled prevalence of S. aureus resistance to different antibiotics in Nigeria Antibiotics No. of studies Total No. of No. of resistant Pooled AMR prevalence I (P‑ value) isolates isolates (95% CI) (P ≤ 0.01) Vancomycin 29 2546 340 0.13 (0.7, 0.21) 96.60 Methicilin 30 3109 1445 0.46 (0.37, 0.56) 96.71 Ciprofloxacin 44 2739 838 0.31 (0.24, 0.38) 93.85 Tetracycline 43 3359 2170 0.65 (0.56, 0.76) 96.03 Cotrimoxazole 21 1293 855 0.66 (0.55, 0.76) 93.91 Chloramphenicol 32 2015 943 0.47 (0.37, 0.56) 95.03 Erythromycin 66 4969 2325 0.47 (0.40, 0.53) 95.31 Penicillin 15 1709 1396 0.82 (0.61, 0.96) 98.97 Clindamycin 12 787 275 0.35 (0.23, 0.49) 93.26 Amoxicillin 40 2167 1614 0.74 (0.66, 0.81) 94.64 Ampicillin 28 2074 1408 0.68 (0.53, 0.81) 97.91 Gentamycin 77 5470 1701 0.31 (0.25, 0.37) 95.90 Ceftriaxone 25 2144 943 0.44 (0.34, 0.54) 95.64 Amoxicillin/clavulanic acid 20 1665 1032 0.62 (0.50, 0.73) 95.76 Ceftazidim 24 2179 1329 0.61 (0.46, 0.75) 98.01 Cefuroxime 17 1035 714 0.69 (0.51, 0.85) 97.23 Cloxacillin 22 1565 1205 0.77 (0.64, 0.88) 97.13 Norfloxacillin 9 491 162 0.33 (0.17, 0.52) 95.27 Rifampicin 7 302 72 0.24 (0.06, 0.48) 95.19 Streptomycin 20 1287 579 0.45 (0.34, 0.57) 94.08 Ofloxacin 25 2058 494 0.24 (0.18, 0.31) 91.63 Trimethoprim 6 291 160 0.55 (0.35, 0.74) 91.99 Cefoxitine 21 1791 770 0.43 (0.31, 0.56) 96.61 Prevalence of resistance of S. aureus to beta‑lactams each antibiotic based on pharmacological classification is antibiotics given below for antibiotics routinely used in Nigeria. Estimation of the pooled prevalence of S. aureus resist- ance to penicillin antibiotics (penicillin G, methicillin, Prevalence of resistance S. aureus to rifamycins amoxicillin, cloxacillin, ampicillin, and amoxacilin/calu- (rifampicins) vanic acid are here presented. Resistance to penicillin G, Seven studies involving the prevalence of resistance amoxicillin, cloxacillin, ampicillin, and augmentin were to rifampicin was analyzed. The pooled prevalence of estimated based on 15, 40, 22, 28 and 20 studies respec- resistance of S. aureus to rifampicin in Nigeria is 24% tively. Pooled prevalence resistance rates were highest (95% confidence interval [CI] 6%, 48%). The forest plot in penicillin G at 82% (95% CI 61%, 96%). Resistance to (rifampicin) is presented in Fig. 2. cloxacillin [77% (95% CI 64%, 88%)], to amoxicillin [74% (95% CI 66%, 81%)], to ampicillin [68% (95% CI 53%, Prevalence of resistance of S. aureus to glycopeptides 81%)] and to amoxacilin/caluvanic [62% (95% CI 50%, (vancomycin) 73%)]. However, resistance rate was moderate for methi- The pooled prevalence of S. aureus resistance to van - cillin [46% (95% CI 37%, 56%)]. Forest plots for antibiot- comycin is 13% (95% CI 7%, 21%) and the forest plot is ics (methicillin and penicillin G) resistance are shown in presented in Fig. 3. Sensitivity results after exclusion of Fig. 4 and 5, respectively while the forest plots for amoxi- four studies [20, 22, 27, 36] that reported high prevalence cillin, ampicillin, amoxicillin/clavulanic acid and cloxa- of S. aureus resistant to vancomycin is 7% (95% CI 3.3%, cillin resistance are presented in Additional file 3: S3, 12%). Hence, there was significant decrease in poled prevalence. Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 10 of 22 Rifampicin at 95% CI Olorode et al, 2021 Chigbu & Ezeronye, 2003 Agwu et al, 2010 Umar et al, 2015 Odogwu et al, 2019 Ismail et al, 2015 Mbim et al, 2017 Total (random effects) 0.00.2 0.40.6 0.8 Proportion (24%) Po oled prevalence 0.24 (0.06, 0.48) I = 95.19 ( P ≤ 0.01) Fig. 2 Forest plot of the prevalence of S. aureus resistance to rifampicin Prevalence of resistance of S. aureus to floroquinolones Additional file 4: S4, Additional file 5: S5 and Additional Three antibiotics (ciprofloxacin, ofloxacin, and nor- file 6: S6 respectively. floxacilin) from floroquinolones were included in the Higher prevalence of resistance among cephalosporin study. For ciprofloxacin, 44 studies were used to esti- antibiotic was observed in cefuroxime 69% (95% CI 51%, mate the pooled resistance, 25 were used for ofloxacin 85%) followed by ceftazidime 61% (95% CI 46%, 75%). and 9 studies were used for norfloxacilin. The pooled Resistance to ceftriaxone is 44% (95% CI 34%, 54%) and prevalence of resistance of S. aureus to ciprofloxa- to cefoxitine is 43% (95% CI 31%, 546%). The forest plot cin [31% (95% CI 24%, 38%)], ofloxacin [24% (95% CI for ceftriaxone resistance is presented in Fig. 6 while the 18%, 31%)], and to norfloxacillin [33% (95% CI 17%, forest plots for cefuroxime and cefoxitine resistance are 52%)]. The forest plot for ofloxacin resistance is pre- presented respectively in Additional file 7: S7 and Addi- sented in Fig. 7 while the forest plot for ciprofloxacin tional file 8: S8. E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 11 of 22 Vancomycin at 95% CI Nworie et al, 2013 Onanuga & Awhowho, 2012 Ayodeji & Omoniy i, 2009 Onanuga &Temedie, 2011 Onanuga et al, 2005 Akanbi & Mbe, 2013 Iroha et al, 2012 Badger-Emeka et al, 2014 Moses et al, 2017 Anucha et al, 2021 Agwu et al. 2016 Osiy emi et al, 2018 Onaolapo et al, 2016 Any anwu et al, 2013 Obajuluwa et al, 2015 Olowe et al, 2013 Akinduti et al, 2021 Ogbolu et al, 2015 Osinupebi et al, 2018 Emeka-Nwabunnia, 2015 Alli et al, 2012 Frank-Peterside & Mukoro, 2010 Ogini & Olay inka, 2021 Onanuga & Onaolapo, 2008 Yah, 2007 Onwubiko & Sadiq, 2011 Terry et al. 2011 Ayeni et al. 2015 Olorunfemi et al. 2020 Total (f ixed effects) Total (random ef fects) 0.00.2 0.40.6 0.81.0 Proportion (13%) Pooled prev alence 0.13 (0.7, 0.21) I = 96.60% (p 0.01) Fig. 3 Forest plot of the prevalence of S. aureus resistance to vancomycin and norfloxacilin included in Additional file 9: S9 and [31% (95% CI 25%, 37%)]. The forest plot for chloram - Additional file 10: S10. phenicol resistance is presented in Fig. 8 while the forest plots for tetracycline, erythromycin, gentamycin, strep- Prevalence of resistance of S. aureus to protein synthesis tomycin, and clindamycin resistance are presented in inhibitors Additional file 11: S11, Additional file 12: S12, Additional Tetracycline a reversible protein synthesis inhibitor file 13: S13, Additional file 14: S14, and Additional file 15: showed the highest resistance rate [65% 995% CI 56%, S15 respectively. 76%)] followed by erythromycin (macrolides) [47% (95% CI 40%, 53%)] and chloramphenicol [47% (95% CI 37%, Prevalence of resistance of S. aureus to antimetabolites 56%)], respectively. Aminoglycosides (gentamycin and High resistance was observed among the antimetabolites streptomycin) and lincosamides (clindamycin) showed antibiotics. Pooled prevalence of S. aureus resistance to relatively lower level of resistance. The pooled prevalence cotrimoxazole was found to be 66% (95% CI 55%, 76%) of resistance to streptomycin [45% (95% CI 34%, 57%)], to and to trimethoprim is 55% (95% CI 35%, 74%). The for - clindamycin [35% (95% CI 23%, 49%)] and to gentamycin est plot for cotrimoxazole resistance is presented in Fig. 9 Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 12 of 22 Meth icilin at 95 % CI Id ris et al, 2018 Odu & Oknok wo , 2012 Eg buob i et al, 2 014 Olorod e et al, 202 1 On an ug a & On ao lapo , 2008 On an ug a & Temedie, 2011 Ak an bi & Mb e 2013 Terry et al, 2011 Ek e et al, 2012 Ob asuy i & Ak erele, 2015 Ak erele et al, 2015 Badger-Emek a et al, 201 4 Ario m et al, 201 9 Ajan i et al, 2020 Olorunfemi et al, 2020 Ad etay o et al, 2014 ib e et al, 201 5 ug wu et al 2016 Olowe et al, 2013 Oche et al, 2020 On elum et al, 2015 Olad ipo et al, 201 9 Og efere et al, 2020 Mo tayo et al, 2 012 Mb im et al, 2017 Bale et al, 2021 Ik e et al, 2 016 Sadauk i et al, 202 2 Frank-Petersid e & Muko ro, 2 010 Nwank wo et al, 2010 To tal (random effects) 0.00 .2 0.40 .6 0.81 .0 Pro portion (4 6%) Po oled prev alen ce 0.46 (0 .37, 0.56) I = 96.71 % (P ≤ 0.01 ) Fig. 4 Forest plot of the prevalence of S. aureus resistance to methicillin while the forest plot for trimethoprim is presented in ampicillin, cefuroxime, amoxacilin, cloxacillin, and penci- Additional file 16: S16. lin G. Comparison of the prevalence of S. aureus resistance Discussion to different antibiotics Antimicrobial resistance continues to be on the rise The trend of prevalence of S. aureus resistance to differ - which constitutes a serious public health problem glob- ent antibiotics addressed in this meta-analysis is shown ally. Many microbes have developed resistance to many in Fig. 10. From observation, the prevalence of resist- different antimicrobial agents over time. This meta- ance of S. aureus to the different antibiotics in this study analysis estimated the pooled prevalence of resistance ranges from 13 (vancomycin) to 82% (penicillin G). of Staphylococcus aureus to 23 different antibiotics rou - The order of resistance in increasing order based on tinely used in Nigeria. Ninety eight studies [98] were the pooled prevalence of S.aureus resistance to differ - included in this meta-analysis study with variation in the ent antibiotics was observed to be vancomycin, ofloxacin, number of studies included in each meta-analysis which rifampicin, ciprofloxacilin, gentamycin, norfloxacillin, clin - ranged from 6 to 77. In general, the 98 studies evaluated damycin, cefoxitine, ceftriaxone, streptomycin, methicillin, the rate of S. aureus resistance to different antibiotics chloramphenicol, erythromycin, trimethoprim, ceftazidim, based on 46,640 isolates of which 23, 048 were resist- amoxicillin-clavulanic acid, tetracycline, cotrimoxazole, ant to various antibiotics. Prevalence of resistance of S. E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 13 of 22 Penicillin at 95% CI Ayodeji & Omoniyi, 2009 Chigbu & Ezeronye, 2003 Onanuga et al, 2021 Terry et al, 2011 Iroha et al, 2012 Eke et al, 2012 Ekundayo & Ndubuisi, 2015 Ayeni et al, 2015 Ariom et al, 2019 Emeakaroha et al, 2017 Bisi-Johnson et al, 2005 Ayepola et al, 2015 Olowe et al, 2013 Oche et al, 2021 Sadauki et al, 2022 Total (random effects) 0.00.2 0.40.6 0.81.0 Proportion (82%) Pooled prevalence 0.82 (0.61, 0.96) I = 98.97 ( P≤ 0.01) Fig. 5 Forest plot of the prevalence of S. aureus resistance to penicillin G aureus to different antibiotics ranges from 13 to 82%. vaginal swab) were collected from both symptomatic Results from the meta-analysis showed that resistance patients [61] and asymptomatic people [37]. of S. aureus to routinely used antibiotics in Nigeria was High heterogeneity was observed for each of the meta- alarmingly high. From the studies, it was found that 82% analyses performed with I ranging from 79.36 to 98.90% S. aureus were resistant to penicillin G. However, it was at p-values ≤ 0.01). This is because many studies used observed from the studies that 24% of S. aureus were varying number of isolates/sample sizes. Some stud- resistant to ofloxacin and rifampicin. In general, clini - ies used 20 isolates while some used 400 isolates which cal samples (nasal, urine, wound, pimple, ear, blood, and impacted on the resistance profile of each antibiotic. This Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 14 of 22 Ceftriaxone at 95% CI Onwubiko & Sadiq, 2011 Terry et al, 2011 Akerele et al, 2015 Torimino et al, 2012 Bale et al, 2019 Adesoji et al, 2019 Udobi et al, 2013 Agwu et al, 2010 Adesida et al, 2016 Osiyemi et al, 2018 Onaolapo et al, 2016 Tula et al, 2016 Anyanwu et al, 2013 Onyeagwara et al, 2014 Obajuluwa et al, 2015 Ibrahim et al, 2018 Motayo t al, 2012 Onyeka et al, 2021 Osinupebi et al, 2018 Bale et al, 2021 Nmema, 2017 Ugwu et al, 2015 Frank-Peterside & Mukoro, 2010 Nwankwo et al, 2010 Olufunmiso et al, 2017 Total (random effects) 0.00.2 0.40.6 0.81.0 Proportion (44%) Pooled prevalence 0.44 (0.34, 0.54) I = 95.64 (P≤ 0.01) Fig. 6 Forest plot of the prevalence of S. aureus resistance to ceftriaxone can better be illustrated in the prevalence of resistance of antibiotics and publication bias was not found. Egger S. aureus to vancomycin. Sensitivity test was carried out test is use to estimate asymmetry of data using funnel to by removing studies that reported very high prevalence plots. p-value less than 0.05 using Egger criteria indicate of S. aureus to vancomycin and the overall pooled preva- no presence of publication bias even though erythro- lence reduced from 13 to 7%. This showed the degree mycin had p-value of 0.017 which is below 0.05. This is of heterogeneity among studies. Possible cause of het- because a p-value of 0.017 for the Egger test means that erogeneity is due to different number of clinical samples the results found have a 1.7% chance to occur when there and number of isolates recovered which were subjected is no ’small sample bias. to antibiotic sensitivity tests. Also random sampling of The pooled prevalence of S. aureus resistance to Beta- clinical samples can also be the possible cause. Publica- lactams class of antibiotics was extremely high espe- tion bias was evaluated for all meta-analysis of the 23 cially for penicillins. S. aureus showed highest resistance E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 15 of 22 Ofloxacin at 95% CI Akortha & Ikenebomeli , 2010 Nworie, 2013 Onanuga & Awhowho, 2012 Onanuga & Onaolapo, 2008 Onwubiko & Sadiq, 2011 Onwubiko & Temedie, 2011 Akanbi & Mbe, 2013 Badger-Emeka, 2014 Torimo et al, 2012 Bale et al, 2019 Adesoji et al, 2019 Anucha et al, 2021 Adesida et al, 2016 Mofolorunsho et al, 2015 Osiyemi et al, 2018 Tula et al, 2016 Akinduti et al, 2019 Oladipo et al, 2019 Onyeka et al, 2021 Osinupebi et al, 2018 Ajoke et al, 2012 Bale et al, 2021 Ugwu et al, 2015 Nwankwo et al, 2010 Olufunmiso et al, 2017 Total (random effects) 0.00.2 0.40.6 0.81.0 Proportion (24%) Po oled prevalence 0.24 (0.18, 0.31) I = 91.63 (P≤ 0.01) Fig. 7 Forest plot of the prevalence of S. aureus resistance to ofloxacin to penicillin G (82%) and 69% resistance to cefuroxime However, S. aureus resistance to amoxicillin and ampi- (cephalosporin). The pooled estimate of S. aureus resist - cillin is relatively high from our results. Lower rate of ance to penicillin G is comparable with the reported esti- resistance was observed among beta-lactamase-resistant mation of worldwide resistance of 90–95% [108]. This is antibiotics (methicillin, ceftriaxone, cefoxitine). Also, not surprising due to the fact that penicillin G is the first lower rate of resistance to clindamycin might be attrib- antibiotic to be discovered. Bacteria are able to develop uted to infrequent use of the antibiotic. Amoxicillin- resistance to antibiotics due to selective pressure from clavulanic acid was developed as a combination of an antibiotics. Selective pressure from penicillin led to the antibiotic (amoxicillin) and non-antibiotic (clavulanic production of beta-lactamase to conuter the effect of acid). Clavulanic acid inhibit beta-lactamase enzyme beta-lactam antibiotics. Consequently, semi-synthetic which prolong the antibacterial activity of amoxicil- beta-lactam antibiotics such as ampicillin, Amoxicil- lin component; however, results from the meta-analysis lin/clavulanic acid and amoxicillin with different side showed high resistance of S. aureus to amoxicillin/clavu- chains were developed to counter such bacteria strains. lanic acid. Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 16 of 22 Chloramphenicol at 95 % CI Akortha & Ikenebomeli, 2010 Olorede et al, 2021 Onanuga & Awhowho, 2012 Chigbu & Ezeronye, 2003 Yah et al, 2009 Onwubiko & Sadiq, 2011 Onanuga & Temedie, 2011 Terry et al, 2011 Ekundayo & Ndubuisi, 2015 Badger-Emeka et al, 2014 Torimino et al, 2012 Ramalan et al, 2020 Obasola et al, 2010 Anyanwu et al, 2013 Ngwai & Bakare, 2012 Umar et al, 2015 Ibanga et al, 2020 Emeakaroha et al, 2017 Bisi-Johnson et al, 2005 Adeiza et al, 2020 Ismail et al, 2015 Onelum et al, 2015 Motayo et al, 2012 Ugwu et al, 2009 Nsofor et al, 2019 Mbim et al, 2017 Adetutu et al, 2017 Bale et al, 2021 Ako-Nai et al, 2005 Yahaya et al, 2022 Nsofor et al, 2015 Olajide et al, 1012 Total (random effects) 0.00.2 0.40.6 0.81.0 Proportion (47 %) Pooled prevalence 0.47 (0.37, 0.56) I = 95.03 ( P ≤ 0.01) Fig. 8 Forest plot of the prevalence of S. aureus resistance to chloramphenicol Another semi-synthetic penicillin resistant antibiotic 2014. Which depicted MRSA prevalence ranged 33–95% called methicillin was developed which is resistant to in Africa. Similarly, the pooled estimate of 46% in our hydrolysis of beta-lactamase was developed. The term study is also in agreement with the pooled prevalence Methicillin Resistant Staphylococcus aurues (MRSA) is estimate of MRSA in continents such as North America, synonymous with multi-drug resistance (MDR) because Asia, and Europe which ranges from 23.1 to 47.4% [109]. MRSA are invariably resistant to different antibiotics. The high pooled prevalence in our study might be due Acquisition of mec A gene that encodes penicillin binding to certain factors and variables such as the inclusion of nosocomial and community acquired infections in the protein confers resistance to S. aureu [109]. The pooled original studies analyzed. Generally, nosocomial infec prevalence of S. aureus to methicillin (46% [95% CI 37%, - 56%]) in Nigeria is similar to 2014 global surveillance tion causing pathogens are believed to possess higher reports of the world health organization (WHO) [110] resistance rate due to prolonged and higher exposure to E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 17 of 22 Cotrimoxazole at 95% CI Odu & Okonkwo, 2012 Nworie, 2013 Onanuga & Awhowho, 2012 Iroha et al, 2012 Ekunday o & Ndubuisi, 2015 adger-Emeka, 2014 Torimino et al, 2012 Onanuga et al, 2021 Obasola et al, 2010 M ofolorunsho et al, 2015 Osiy emi et al, 2018 Emekaroha et al, 2017 Ugwu et al, 2009 Osinup ebi et al, 2018 adetutu et al, 2017 Ugwu et al, 2015 ako-Nai et al, 2005 Onanuga et al, 2019 Yahaya et al, 2022 Chigbu & Ezerony e, 2003 Ramalan et al, 2020 Total (random effects) 0.0 0.2 0.4 0.6 0.8 1.0 Prop ortion (66%) Pooled prevalence 0.66 (0.55, 0.76) I = 93.91 (P≤ 0.01) Fig. 9 Forest plot of the prevalence of S. aureus resistance to cotrimoxazole different antimicrobial agents and exchange of genetic studies [20, 22, 28, 36] reported a very high prevalence materials. Thus, there is greater transmission of resistant of VRSA; however, sensitivity analysis showed that they genes through various means within the hospital settings had high significant influence on the overall pooled [111]. The implication of infections cause by MRSA is dif - prevalence estimate. Removing the three studies reduces ficulty in treatment which often requires alternative anti - the pooled prevalence of S. aureus resistance to vanco- microbial agents which are most times very expensive. mycin from 13 to 7%. Analyzing studies that depicted The pooled prevalence of S. aureus resistance to van - high prevalence of resistance of S. aureus to vancomy- comycin (13% at 95% CI [0.7%, 21%]) in this meta-anal- cin showed that the same author conducted and pub- ysis is high and a cause for concern when compared to lished the three studies in peer reviewed journals. Urine global prevalence estimate [4]. The prevalence of vanco - samples were mainly used for S. aureus isolation by the mycin resistant S. aureus (VRSA) in Africa was reported author in the three studies of which [20, 22] were from to be 2.5% [4]. This is quite low when compared to the symptomatic urinary tract infection patients who visited result from this study which is very high (13%). With the hospitals and [27] from healthy volunteers. Urinary this increased resistance, the use of vancomycin to treat tract infection is a common infection and a reason for MRSA is becoming problematic and poses serious health antibioticl use; consequently, resistant microbial strains challenge. The rise in VRSA might be due to the indis - have emerged. This reason might be attributed to the criminate use of vancomycin in Nigeria. By the way, Four high prevalence of S. aureus resistant to vancomycin in Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 18 of 22 percentage % Antibiotics Fig. 10 Comparison of the prevalence of S. aureus resistance to different antibiotics in Nigeria the three studies. Exposure to resistant strains especially expression of Mec genes which alters penicillin binding in hospital settings might have resulted in the increased proteins. From the results and mechanism of resistance resistance to vancomycin in the three studies [112, 113]. of S. aureus, it can be said that S. aureus found in Nigeria This is because in Nigeria, expired or waste antibiotics are highly resistant to the beta-lactam class of antibiotics. are not properly discharged. This could result in selective The pooled prevalence of S. aureus resistance to the pressure on inhabitant microorganisms which results in floroquinolones class of antibiotics such as ciprofloxa - development of various resistant mechanisms. cin, ofloxacin, and norfloxacin was lower especially for Generally, the global pattern of antimicrobial resistance ciprofloxacin which is commonly used within Nigeria. varies among different geographical locations and socio - However, high pooled prevalence of S. aureus resistance economic level [114, 115]. Variations in studies can be to antimetabolites class of antibiotics (cotrimoxazole and attributed to design, time, and population involved. Het- trimethoprim) was observed. erogeneity tests at p ≤ 0.01 showed significant variation From the meta-analysis, S. aureus mediated infection among included studies in this meta-analysis. Therefore, in Nigeria can be treated using vancomycin, floroqui - it is reasonable to assert that the study population might nolones, and aminoglycosides. MRSA has been a concern be infected with the same strains of S. aureus within the in Nigeria especially with the incidence of VRSA. Newer same location at a specified period. This is because most alternative antibiotics such as linezolid, telavancin, cef- of the studies were conducted within a specified period taroline, tigecycline and daptomycin are rarely used in of time and area. Nigeria. Various factors such as lack of infection preven- Mechanisms of resistance of S. aureus include: produc- tion which lead to reoccurrence of infection, inappro- tion of beta-lactamase enzymes to deactivate beta-lactam priate use of antibiotics, poor hospital facilities, lack of sensitive antibiotics, efflux pump for extruding antibi - routine susceptibility test before antibiotic administra- otics such as tetracyclines [6], reduced accumulation of tion, and self medication contributes to the rapid emer- macrolides antibiotics [7], production of aminoglyco- gence and re-emergence of AMR. Tackling this factors, side modifying enzymes to inactivate aminoglycosides will go a long way in the fight against the continue rise of antibiotics, alteration of DNA gyrase and topoisomer- MDR pathogens in general. ase IV expression for floroquinolones antibiotics, and Prevalence of resistance (%) Vancomycin Ofloxacin Rifampicin Ciprofloxacin Gentamycin Norfloxacillin Clindamycin Cefoxitine Ceftriaxone Streptomycin Methicillin Chloramphenicol Erythromycin Trimethoprim Ceftazidime amoxicillin/clavulanic acid Tetracycline Cotrimoxazole Ampicillin Cefuroxime Amoxicillin Cloxacillin Penicillin E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 19 of 22 Study limitations Supplementary Information Most of the included studies share similar characteristics. The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s13756- 023- 01243-x. The search was limited to only titles that deal with antibi - otic resistance. Selection was done randomly especially in Additional file 1: S1. PRISMA 2009 Checklist Google Scholar with had 35, 400 studies results from the Additional file 2: S2. Egger’s test of publication bias search. The meta-analysis was done once for each anti - Additional file 3: S3. Forest plot of the prevalence of S. aureus resistance to biotics and sub-grouping to reduce high heterogeneity amoxicllin and publication bias was not done due to too many meta- Additional file 4: S4. Forest plot of the prevalence of S. aureus resistance analysis already done. The included studies used in-vitro to ampicillin antimicrobial assays which has limitations such as dif- Additional file 5: S5. Forest plot of the prevalence of S. aureus resistance to ficulties in interpreting data, variability of testing media augmentin (differences in cation content, acidic or alkaline), and dif - Additional file 6: S6. Forest plot of the prevalence of S. aureus resistance to ficulty in knowing the pharmacokinetics of an antibiotic cloxacillin or post effect of an antibiotic (a situation where bacteria Additional file 7: S7. Forest plot of the prevalence of S. aureus resistance to cefuroxime growth is inhibited even when the antibiotic concentra- Additional file 8: S8. Forest plot of the prevalence of S. aureus resistance to tion falls below the MIC). Most of the studies were done cefoxitine in teaching hospitals and tertiary institutions in big cit- Additional file 9: S9. Forest plot of the prevalence of S. aureus resistance to ies; hence both symptomatic and asymptomatic individu- ciprofloxacin als are involved. For symptomatic individuals, most of Additional file 10: S10. Forest plot of the prevalence of S. aureus resistance the studies were done in teaching hospitals were patients to norfloxacin with chronic and recurrent infections are treated; resist- Additional file 11: S11. Forest plot of the prevalence of S. aureus resistance ance level could be overestimated. to tetracycline Additional file 12: S12. Forest plot of the prevalence of S. aureus resistance to erythromycin Conclusion Additional file 13: S13. Forest plot of the prevalence of S. aureus resistance to gentamycin The results of this meta-analysis showed that S. aureus Additional file 14: S14. Forest plot of the prevalence of S. aureus resistance is resistant to many routinely used antibiotics in Nige- to streptomycin ria. It is highly resistant to beta-lactams, tetracyclines, Additional file 15: S15. Forest plot of the prevalence of S. aureus resistance and antimetabolites antibiotics. Resistance of S. aureus to clindamycin to vancomycin remains a serious health problem due to Additional file 16: S16. Forest plot of the prevalence of S. aureus resistance limited treatment options. There is a lot of variation in to trimethoprim resistance estimates between studies. High heterogene- ity was observed in each meta-analysis for each antibiotic Acknowledgements which was attributed to various factors such as differ - Not applicable ent clinical sample and recovered isolates sizes, random Author contributions sampling and method used for resistance investigation. CKE, CNE and UMED conceptualized the research idea. CKE and SCE con- Hence it is imperative to develop programs to promote ducted literature search, selection and data extraction. CKE performed the rational use of antimicrobial agents, infection prevention statistical analyses. CKE prepared the draft manuscript. All authors revised, edited and approved the final manuscript. and control to reduce the incidence of AMR. In addition, furthers researches focusing on identifying the dynam- Funding ics promoting microbial resistance, infectious microbial No funding was received. strains and molecular/genetic basis of resistance should Availability of data and materials be encouraged. The data supporting the conclusions of this article are included within the article and its supporting information. Abbreviations Declarations AMR Antimicrobial resistance CLSI Clinical Laboratory Standard Institute Ethics approval and consent to participate CI Confidence interval Not applicable. MRSA Methicillin resistant Staphylococcus aureus S. aureus Staphylococcus aureus VRSA Vancomycin resistant Staphylococcus aureus Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 20 of 22 Consent for publication 19. Olorode OA, Ogba OM, Nanighe SO. Molecular detection of methicil- Not applicable. lin resistance genes (Mec A; Pvl) in methicillin resistant Staphylococcus aureus isolates from Federal Medical Centre, Yenagoa, Bayelsa State, Competing interests Nigeria. J Curr Med Res Opin. 2021;4(10):1035–41. The authors declare that they have no competing interests. 20. Onanuga A, Awhowho GO. Antimicrobial resistance of Staphylococcus aureus strains from patients with urinary tract infections in Yenagoa, Nigeria. J Pharm Bioallied Sci. 2012;4(3):226–30. Received: 11 August 2022 Accepted: 14 April 2023 21. Ayodeji AA, Omoniyi AK. Multi-drug resistant Staphylococcus aureus in clinical cases in Ile-Ife, Southwest Nigeria. Int J Med Med Sci. 2009;1(3):68–72. 22. Onanuga A, Onaolapo AJ. Antimicrobial Susceptibility of Community- associated Staphylococcus aureus Isolates from Healthy Women in Zaria, Nigeria. Trop J Pharm Res. 2008;7(1):929–34. References 23. Chigbu C, Ezeronye OU. Antibiotic resistant Staphylococcus aureus in 1. Rasigade JP, Vandenesch F. Vandenesch, Staphylococcus aureus: a patho- Abia State of Nigeria. Afr J Biotechnol. 2013;2(10):374–8. gen with still unresolved issues. Infect Genet Evol. 2014;21:510–4. 24. Yah SC, Enabule OI, Eggafona NO. The screening of multidrug resistance 2. Bamigboye BT, Olowe OA, Taiwo SS. Phenotypic and molecular iden- (MDR) susceptibilities of Staphyloccocus aureus and Staphyloccocus epi- tification of vancomycin resistance in clinical Staphylococcus aureus dermidis to methicillin and vancomycin in teaching hospitals in Nigeria. isolates in Osogbo, Nigeria. Eur J Microbiol Immunol. 2018;8:25–30. Int J Biol Chem Sci. 2007;2(4):257–61. 3. McGuinness WA, Malachowa N, DeLeo FR. Vancomycin resistance in 25. Yah SC, Yusuf EO, Haruna T. Patterns of antibiotics susceptibility of Staphylococcus aureus. Yale J Biol Med. 2017;90(2):269–681. isolates and plasmid analysis of Staphylococcus from surgical site infec- 4. Shariati A, Dadashi M, Moghadam MT. Global prevalence and distribu- tions in Nigeria. Sudan JMS. 2009;3(4):810–8. tion of vancomycin resistant, vancomycin intermediate and hetero- 26. Onwubiko NE, Sadiq NM. Antibiotic sensitivity pattern of Staphylococ- geneously vancomycin intermediate Staphylococcus aureus clinical cus aureus from clinical isolates in a tertiary health institution in Kano, isolates: a systematic review and meta-analysis. Sci Rep. 2020;10:12689. Northwestern Nigeria. Pan Afr Med J. 2011;8(4):1–7. 5. Khan A, Wilson B, Gould IM. Current and future treatment options for 27. Onanuga A, Temedie TC. Nasal carriage of multi-drug resistant Staphylo- community-associated MRSA infection. Expert Opin Pharmacother. coccus aureus in healthy inhabitants of Amassoma in Niger delta region 2018;19(5):457–70. of Nigeria. Afr Health Sci. 2011;11(2):176–81. 6. Sompolinsky D, Zaidenzaig Y, Ziegler-Schlomowitz R, Abramova N. 28. Onanuga A, Avosuahi RO, Onaolapo JA. Prevalence and susceptibility Mechanism of tetracycline resistance in Staphylococcus aureus. J Gen pattern of methicillinresistant Staphylococcus aureus isolates among Microbiol. 1970;62(3):351–62. healthy women in Zaria. Nigeria Afr J Biotechnol. 2005;4(11):1321–4. 7. Yamagishi S, Nakajima Y, Inoue M, Oka Y. Decrease in accumulation of 29. Akanbi RO, Mbe JU. Occurrence of methicillin and vancomycin resistant macrolide antibiotics as a mechanism of resistance in Staphylococcus Staphylococcus aureus in University of Abuja teaching hospital, Abuja, aureus. Jpn J Microbiol. 1971;15(1):39–52. Nigeria. Afr J Clin Exp Microbiol. 2013;14(1):10–3. 8. Li XF, Fan XJ, Guo XJ, Feng P, Lu XJ, Gao YY, et al. A study on the mecha- 30. Alli OAT, Ogbolu DO, Akorele E, Onemu OM, Okanlawon BM. Distribu- nism of drug resistance in Staphylococcus aureus. Sichuan Da Xue Xue tion of mecA gene amongst Staphylococcus aureus isolates from Bao Yi Xue Ban. 2006;37(3):365–8. Southwestern Nigeria. Afr J Biomed Res. 2011;14:9–14. 9. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items 31. Iroha IR, Okoye E, Osigwe CA, Moses IB, Ejikeugwu CP, Nwakaeze AE. for systematic reviews and meta-analyses: the PRISMA statement. PloS Isolation, Phenotypic characterization and prevalence of ESBL-produc- Med. 2009;151:264–9. ing Escherichia coli and Klebsiella species from orthopedic wounds 10. Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis in National Orthopedic Hospital Enugu (NOHE), South East Nigeria. J detected by a simple, graphical test. BMJ. 1997;315(7109):629–34. Pharm Care Health Syst. 2017;4(4):1000184. 11. Akortha EE, Ikenebomeh MJ. Nasal colonization of symptomatic 32. Eke S, Abdulkadiri S, Okoro CJ, Ekoh SN, Mbachi NG. The prevalence and pneumonia patients in University of Benin Teaching Hospital, Benin resistivity pattern of Staphylococcus aureus Isolates from apparently City, Nigeria by multiple antibiotic resistant Staphylococcus aureus. Afr J healthy university students in Ekpoma, Edo, Nigeria. Int J Basic Appl Microbiol Res. 2010;4(11):1071–5. Innov Res. 2012;1(4):183–7. 12. Idris MA, Kumurya AS, Mohammed Y. Detection of methicillin-resistant 33. Ekundayo EO, Ndubuisi RN. In-vitro antimicrobial susceptibility pattern staphylococcus aureus among bacterial isolated from children aged of Staphylococcus aureus isolates in Umuahia, Abia state, Nigeria. Afr J 0–5 years with septicaemia in Kano, north western, Nigeria. FUDMA J Clin Exp Microbiol. 2015;16(3):62–6. Microbiol. 2018;1(1):51–7. 34. Obasuyi O, Akerele JO. High incidence of multidrug-resistant strains of 13. Stanley CN, Ugboma HAA, Ibezim EC, Attama AA. Prevalence and anti- methicillinresistant Staphylococcus aureus isolated from clinical samples biotic susceptibility of Staphylococcus aureus and other staphylococcal in Benin-city, Nigeria. Afr J Clin Exp Microbiol. 2015;16(3):124–7. infections in pregnant women attending antenatal clinic in a tertiary 35. Akerele JO, Obasuyi O, Omede D. Prevalence of methicillin-resistant hospital in port Harcourt, Nigeria. Infect Dis Ther. 2013;2(1):1–6. Staphylococcus aureus among healthy residents of Ekosodin commu- 14. Odu NN, Okonko IO. Nasal carriage and antibiotics susceptibility of nity in Benin-City, Nigeria. Trop J Pharm Res. 2015;14(8):1495–9. Staphylococcus aureus in healthy students of University of Port Harcourt, 36. Badger-Emeka LI, Emeka PM, Dibua UME. Plasmid profile of multi Rivers State, Nigeria. N Y Sci J. 2012;5(7):56–63. antibiotic resistant Staphylococcus aureus isolated from diabetic 15. Isibor JO, Otabor E. Asymptomatic carriage of plasmid-mediated wounds from patients at Nsukka, South astern, Nigeria. Afr J Biotectnol. multidrugresistant Staphylococcus aureus in nasal tracts of persons in a 2014;13(43):4148–54. semi-urban area of Nigeria. Am J life Sci. 2014;2(4):200–4. 37. Ayeni FA, Gbarabon T, Andersen C, Nørskov-Lauritsen N. Comparison 16. Nworie A. Nasal carriage of methicillin resistant Staphylococcus aureus of identification and antimicrobial resistance pattern of Staphylococcus amongst meat sellers in Abakaliki Metropolis, Ebonyi State, Nigeria. aureus isolated from Amassoma, Bayelsa state, Nigeria. Afr Health Sci. Microbiol Res Int. 2013;1(3):48–53. 2015;15(4):1282–8. 17. Egbuobi RC, Wachuku CK, Dike-Ndudim JN, Ogamaka AI, Okorie HM, 38. Torimiro N, Torimiro SEA. Antibiotic resistance profile in community- Nwagbaraocha MA, et al. Evaluation of antibacterial profile of methicil- associated Staphylococcus aureus strains isolated from a Nigerian peri- lin resistant Staphylococcus aureus (MRSA) isolated from hospitals in urban community. Afr J Biotechnol. 2012;11(94):16071–6. Imo state, Nigeria. Int J Med Med Sci. 2014;6(2):69–74. 39. Bale M, Babatunde SK, Adedayo MR, Ajiboye AE, Ajao AT. Characteriza- 18. Olowo-Okere A, Atana RF, Abass A, Shuaibu AS, Yahya UH, Tanko N. tion of methicillin-resistant Staphylococcus aureus isolates from appar- Incidence and antibiotic susceptibility profile of Staphylococcus aureus ently healthy individuals in Malete, Kwara state, Nigeria. Afr J Clin Exp isolates from wounds of patients at specialist hospital, Sokoto, Nigeria. J Microbiol. 2019;20(1):17–24. Med Bacteriol. 2017;6(4):44–50. E zeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 21 of 22 40. Adesoji AT, Onuh JT, Bagu J, Itohan SA. Prevalence and antibiogram 59. Ugwu MC, Anie CO, Ibezim EC, Esimone CO. Antimicrobial evaluation study of Staphylococcus aureus isolated from clinical and selected of methicillin-resistant Staphylococcus aureus nasal carriage amongst drinking water of Dutsin-Ma, Katsina state, Nigeria. Afr Health Sci. healthy students in Agbor, Delta State, Nigeria. Arch Clin Microbiol. 2019;19(1):1385–92. 2016;7(2):13. 41. Ariom TO, Iroha TR, Moses IB, Iroha CS, Ude UT, Kalu AC. Detection and 60. Tula MY, Okoro AJ, Okojie RO, Iyoha O. Antimicrobial susceptibility phenotypic characterization of methicillin-resistant Staphylococcus pattern and plasmid-mediated antibacterial resistance in Staphylococ- aureus from clinical and community samples in Abakaliki, Ebonyi State, cus aureus and coagulase-negative staphylococci. Highl Med Res J. Nigeria. Afr Health Sci. 2019;19(2):2026–36. 2016;16(2):80–6. 42. Ajani TA, Elikwu CJ, Nwadike V, Babatunde T, Anaedobe CG, Shonekan 61. Anyanwu NC, Abdullahi IO, Ameh JB, Ella EE. Molecular detection of O, et al. Nasal carriage of methicillin resistant Staphylococcus aureus PVL, msrA genes and antibiotic susceptibility pattern of staphylococcus among medical students of a private institution in Ilishan-Remo, Ogun aureus from skin and soft tissue infections in Zaria, Nigeria. Sci J Micro- State, Nigeria. Afr J Clin Exp Microbiol. 2020;21(4):311–7. biol. 2013;2(2):43–52. 43. Olorunfemi PO, Onaolapo JA, Ibrahim YKE. Prevalence and antibiotic 62. Onyeagwara N, Obasuy O, Ottih I, Akerele JO. Nasal carriage of susceptibility of community acquired methicillin resistant Staphylococ- methicillin-resistant Staphylococcus aureus among hospitalized cus aureus from healthy students of University of Jos. J Pharm Bioresour. otorhinolaryngological patients in Benin City of Nigeria. Arch Int Surg. 2020;17(2):131–41. 2014;4(2):99–103. 44. Onanuga A, Adamu OJ, Odetoyin B, Hamza JA. Nasal carriage of multi- 63. Ngwai YB, Bakare OR. Asymptomatic bacteriuria and antimicrobial drug resistant panton valentine leukocidin positive Staphylococcus susceptibility of Staphylococcus aureus from university students in Keffi, aureus in healthy individuals of Tudun-Wada, Gombe State, Nigeria. Afr Nigeria. Int J Microbiol Bioinform. 2012;2(1):6–8. J Infect Dis. 2021;15(1):24–33. 64. Umar M, Abdulkarim IM, Yaya A, Bello HI, Yusuf G, Mathias ML. Bio- 45. Ramalan AS, Joseph FN, Owoseni MC, Ya’aba Y, Chuku A. Prevalence and chemical characterization and antibiotic susceptibility profile of Staphy - antibiotic resistance profile of Staphylococcus aureus and Escherichia lococcus aureus isolated from patients attending Barau Dikko Specialist coli among patients attending urology Clinic of Dalhatu Araf specialist Hospital, Kaduna State, Nigeria. Int J Novel Res Life Sci. 2015;2(6):1–9. hospital (dash) Lafia, Nasarawa state, Nigeria. Bayero J Pure Appl Sci. 65. Obajuluwa AF, Olayinka BO, Adeshina JA, Afolabi-Balogun NB. Plasmid 2020;13(1):80–9. profile of Staphylococcus aureus from orthopaedic patients in Ahmadu 46. Udobi CE, Obajuluwa AF, Onaolapo AJ. Prevalence and Antibiotic Bello University Teaching Hospital Zaria, Nigeria. Afr J Microbiol Res. resistance pattern of methicillin-resistant Staphylococcus aureus from an 2015;9(33):1941–6. Orthopaedic Hospital in Nigeria. BioMed Res Int. 2013;4. 66. Iduh UM, Chollom CS, Nuhu A, Spencer THI, Nura MB, Ashcroft OF, et al. 47. Obasola EF, Ezeamagu CO, Oyelade AA, Adeniyi AO. Comparative study Nosocomial infections in post-operative wounds due to Staphylococ- of antibiotic resistance of Staphylococcus species isolated from clinical cus aureus and Pseudomonas aeruginosa in Benue State Nigeria. Afr J and environmental samples. AU J Tech. 2010;13(3):165–9. Microbiol Res. 2015;9(36):1989–96. 48. Moses AE, Ohagim IP, Inyang UC. Nasal methicillin-resistant Staphy- 67. Ibanga IA, Akan OD, Iyanga FZ, Mantu EC, Asuquo M. Multi-drug resist- lococcus aureus carriage in pre and post-operative patients in a ance pattern of Staphylococcus aureus from pediatric ward, General tertiary health facility in Uyo, South-south, Nigeria. World J Pharm Res. Hospital, Ikot-Ekpaw, Mkpat Enin LGA, Akwa-Ibom State, Nigeria. Arch 2017;6(5):160–71. Clin Microbiol. 2020;11(105):1–4. 49. Nsofor CA, Nwokenkwo VN, Nwaokpa C. Nasal carriage of Staphylo- 68. Emeakaroha MC, Nkwocha IG, Adieze NC, Adieze IE. Antimicrobial sus- coccus aureus among apparently Healthy School Children in Owerri ceptibility pattern of Staphylococcus aureus, and their nasal and throat Metropolis, Nigeria. Basic Res J Microbiol. 2015;2(3):34–8. carriage among food handlers at the Federal University of Technology, 50. Adetayo TO, Deji-Agboola AM, Popoola MY, Atoyebi TJ, Egberongbe KJ. Owerri Nigeria. Int J Biomol Biomed. 2017;6(3):1–7. Prevalence of methicillin resistant Staphylococcus aureus from clinical 69. Bisi-Johnson MA, Kolawole DO, Shittu OA. Epidemiological analysis of specimens in Ibadan, Nigeria. Int J Eng Sci. 2014;3(9):1–11. clinical isolates of Staphylococcus aureus in IIe-Ife, Nigeria. Pak J Bio Sci. 51. Ejikeugwu C, Nwezeagu FJ, Edeh C, Eze P. Detection of constitutive and 2005;8(7):1016–20. inducible-clindamycin-resistance in clinical isolates of Staphylococcus 70. Ayepola OO, Nurudeen AO, Egwari LO, Becke K, Schaumburg F. Molecu- aureus from a Federal Teaching Hospital in Abakaliki, Nigeria. J Bacteriol lar characterization and antimicrobial susceptibility of Staphylococcus Infect Dis. 2018;2(1):31–4. aureus isolates from clinical infection and asymptomatic carriers in 52. Anucha JC, Morikwe UC, Ikegbunam MN, Ezejiegu CK, Ugwu MC. Age Southwest Nigeria. PLoS ONE. 2015;10(9): e0137531. and gender- based antibiotic susceptibility patterns of Staphylococcus 71. Odogwu DA, Kadarko PS, Muazu JS, Bassey BE, Abimiku RH, Nkene IH, aureus among HIV patients in some selected hospitals in Anambra et al. Antimicrobial resistance profile and molecular detection of MecA Central, Nigeria. Gen Mol Med. 2021;3(2):1–5. gene in methicillin resistant Staphylococcus aureus from patients in 53. Agwu E, Ihongbe J, Inyang N. Prevalence of quinolone-susceptible selected general hospitals in Abuja municipal, Nigeria. GSC Biol Pharm Pseudomonas aeruginosa and Staphylococcus aureus in delayed-healing Sci. 2019;7(3):93–106. diabetic foot ulcers in Ekpoma, Nigeria. Cell Tis Prod. 2010;22(4):100–5. 72. Adeiza SS, Onaolapo JA, Olayinka BO. Prevalence, risk-factors, and 54. Adesida AS, Okeyide AO, Abioye A, Omolopo I, Egwuatu TO, Amisu antimicrobial susceptibility profile of methicillin-resistant Staphylococ- KO, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus cus aureus (MRSA) obtained from nares of patients and staff of Sokoto among elderly people in Lagos, Nigeria. Avicenna J Clin Microb Infect. state-owned hospitals in Nigeria. GMS Hyg Infect Control. 2020;15:1–17. 2016;3(4):e39272. 73. Ismail HY, Bello HS, Mustafa A, Adamu A. Multidrug resistance pattern 55. Mofolorunsho CK, Ocheni M, Omatola CO, Agieni AG. Staphylococ- of Staphylococcus aureus isolates in Maiduguri metropolis. Sci Rev. cus aureus prevalence and antibiotic susceptibility profile in Anyigba, 2015;1(2):16–20. North-Central Nigeria. Am J Infect Dis. 2015;11(4):93–7. 74. Ibrahim S, Adam SA, Alero AA, Umar S. Prevalence and antibiotic sensi- 56. Osiyemi JA, Osinupebi OA, Akinduti PA, Ejilude O, Makanjuola tivity pattern of Staphylococcus aureus Isolated from wound and otitis SO, Sunmola NO, et al. Antibiotic resistance profile of methicillin- media among patients attending Aminu Kano Teaching Hospital, Kano, resistant Staphylococcus aureus in Abeokuta, Nigeria. J Adv Microbiol. Nigeria. Microbiol Res J Int. 2018;25(2):1–9. 2018;9(2):1–9. 75. Olowe OA, Kukoyi OO, Taiwo SS, Ojurongbe O, Opaleye OO, Bolaji OS, 57. Ibe C, Onyeagba RA, Ugochukwu SC. Antibiotic resistance patterns and et al. Phenotypic and molecular characteristics of methicillin-resistant plasmid profiles of methicillin resistant Staphylococcus aureus isolates Staphylococcus aureus isolates from Ekiti State, Nigeria. Infect Drug Res. from human samples. Br Microbiol Res J. 2014;4(2):185–94. 2013;6:87–92. 58. Onaolapo JA, Olayinka BO, Adeshina GO, Igwe JC, Obajuluwa AF. 76. Oche AD, Oyegoke PI, Akpudo MO, Olayinka BO. Antibiotics resist- Antimicrobial susceptibility pattern of Staphylococcus aureus isolates ance pattern of Staphylococcus aureus isolated from in-patients of an from orthopaedic patients in Abuth Zaria. J Food Indust Microbiol. Orthopaedic Hospital in North-Western Nigeria. Int J Epidemiol Res. 2016;2(1):1–6. 2021;8(4):160–6. Ezeh et al. Antimicrobial Resistance & Infection Control (2023) 12:40 Page 22 of 22 77. Onelum B, Odetoyin B, Onipede A, Oyelese A. The role of methicillin- genome of Staphylococcus aureus from hospitals in South Western resistant Staphylococcus aureus in clinical infections in Obafemi Nigeria. Indian J Med Microbiol. 2012;30(2):159–64. Awolowo University Teaching Hospitals Complex, Ile-Ife, South Western 97. Sadauki AH, Olorukooba AA, Balogun MS, Dalhat MM, Waziri H, Nigeria. J Microbiol Exp. 2015;2(2):00041. Abdulaziz MM, et al. Nasal carriage of meticillin-resistant Staphylococcus 78. Akindut AP, Osiyemi JA, Banjo TT, Ejilude O, El-Ashke M, Adeyemi AG, aureus among children living with HIV attending infectious diseases et al. Clonal diversity and spatial dissemination of multi-antibiotics clinics in Kano. Nigeria Infect Prev Pract. 2022;4:1–8. resistant Staphylococcus aureus pathotypes in Southwest Nigeria. PLoS 98. O’Malley SM, Emele FE, Nwaokorie FO, Idika N, Umeizudike AK, Emeka- ONE. 2021;16(2):e0247013. Nwabunnia I, et al. Molecular typing of antibiotic-resistant Staphylococ- 79. Oladipo AO, Oladipo OG, Bezuidenhout CC. Multi-drug resistance traits cus aureus in Nigeria. J Infect Public Health. 2015;8:187–93. of methicillin-resistant Staphylococcus aureus and other Staphylococ- 99. Emeka-Nwabunnia I, Ejigeme K, Oguoma OI. Antibiotic resistance cal species from clinical and environmental sources. J Water Health. pattern of methicillin-resistant Staphylococcus aureus isolated from chil- 2019;17(6):932–43. dren under the age of five years in Anambra State. Niger J Biotechnol. 80. Ogefere HO, Umaru G, Ibadin EE, Omoregie R. Prevalence of methicillin- 2019;36(1):213–21. resistant staphylococci among apparently healthy students attend- 100. Ako-Nai AK, Adeyemi FM, Aboderin OA, Kassim OO. Antibiotic resist- ing a tertiary institution in Benin City, Nigeria. Niger J Basic Appl Sci. ance profile of staphylococci from clinical sources recovered from 2019;27(1):114–21. infants. Afr J Biotechnol. 2015;4(6):816–22. 81. Motayo BO, Akinduti PA, Okerentugba PO, Innocent-Adiele HC, Onoh 101. Frank-Peterside N, Mukoro M. The current susceptibility pattern of CC, Nwanze JC, et al. Methicillin resistance and beta-lactamase produc- methicillin resistant Staphylococcus aureus to antibiotics in Port Har- tion in Staphylococcus aureus isolated from different clinical samples in court. Global J Pure Appl Sci. 2010;16(4):375–9. Abeokuta, Nigeria. Acad Arena. 2012;4(6):25–8. 102. Yahaya H, Ahmad AS, Ibrahim A, Abdullahi AS. Phenotypic Detection of 82. Onyeka FI, Nwobodo DC, Umenne IC, Atada EE, Ojukwu CA, Aniekwe Macrolide, Lincosamide and Streptogramin B resistance among Staphy- MA, et al. Antibiotic resistance pattern of Staphylococcus aureus isolated lococcus aureus clinical isolates in A Northern Nigeria Tertiary Hospital. from nostrils of healthy undergraduates of Madonna University Elele Alq J Med App Sci. 2022;5(1):193–8. Campus, Rivers State, Nigeria. Microbes Infect Dis. 2021;2(2):280–5. 103. Onanuga A, Eboh DD, Okou GT. Antibiogram and virulence character- 83. Ugwu CM, Odimegwu DC, Ibezim EC, Esimone CO. Antibiotic Resist- istics of multi-drug resistant Staphylococcus aureus from nasal cavity of ance patterns of Staphylococcus aureus isolated from nostrils of healthy healthy students of Niger Delta University, Amassoma, Bayelsa State, human subjects in a Southeastern Nigeria Locality. Maced J Med Sci. Nigeria. J Clin Diagn Res. 2019;13(7):24–9. 2009;2(4):294–300. 104. Oginni IO, Olayinka AA. Distribution and antibiotics resistance pattern 84. Nsofor CA, Nwokenkwo VN, Ohale CU. Prevalence and antibiotic sus- of community-acquired methicillin-resistance Staphylococcus aureus in ceptibility pattern of Staphylococcus aureus isolated from various clini- Southwestern Nigeria. Adv Exp Med Biol. 2022;1369:81–91. cal specimens in South East Nigeria. MOJ Cell Sci Rep. 2016;3(2):00054. 105. Nwankwo EOK, Sale A, Magagi A, Ihesiulor G. Methicillin resistant S. 85. Mbim EN, Mboto CI, Edet UO, Umego CF, George UE, Temidayo L. aureus (MRSA) and their antibiotic sensitivity pattern in Kano, Nigera. Comparative evaluation of methicillin-resistant Staphylococcus aureus Afr J Clin Exp Microbiol. 2010;11(1):129–36. (MRSA) isolates from hospital and community settings in Nigeria. J Adv 106. Olufunmiso C, Tolulope I, Roger C. Multidrug and vancomycin resist- Microbiol. 2017;4(4):1–9. ance among clinical isolates of Staphylococcus aureus from different 86. Ogbolu DO, Alli TOA, Bello LA, Ibrahim AO. Emergence of vancomycin teaching hospitals in Nigeria. Afr Health Sci. 2017;17(3):798–806. intermediate Staphylococcus aureus ( VISA) in clinical isolates of methicil- 107. Olajide RA, Ameh JA, Simon MK. Antibiotic resistance and susceptibil- lin resistant S. aureus from South Western Region of Nigeria. Int J Trop ity pattern/profile of Staphylococcus aureus and Klebsiella species to Dis Health. 2015;10(4):1–5. popularly—used and readily available antibiotics in Zaria, Nigeria. J 87. Osinupebi OA, Osiyemi JA, Deji-Agboola AM, Akinduti PA, Ejilude O, Phytother Pharm. 2012;1:16–21. Makanjuola SO, et al. Prevalence of methicillin-resistant Staphylococcus 108. Hemaiswarya S, Kruthiventi AK, Doble M. Synergism between natural aureus in Abeokuta, Nigeria. South Asian J Res Microbiol. 2018;1(1):1–8. products and antibiotics against infectious diseases. Phytomedicine. 88. Ajoke OI, Okeke OI, Odeyemi OA, Okwori AEJ. Prevalence of methicillin- 2008;15(8):639–52. resistant Staphylococcus aureus from healthy community individuals 109. Li S, Li J, Qiao Y, Ning X, Zeng T, Shen X. Prevalence and invasiveness volunteers in Jos south, Nigeria. J Microbiol Biotechnol Food Sci. of community-acquired methicillin-resistant Staphylococcus aureus: a 2012;1(6):1389–405. metaanalysis. Indian J Pathol Microbiol. 2014;57(3):418–22. 89. Onyebueke EA, Onyemelukwe NF, Oladeji DS. Antibiotic susceptibility 110. WHO. Antimicrobial resistance: global report ton surveillance. 2014. pattern of Staphylococcus species implicated in urinary tract infection 111. Struelens MJ. The epidemiology of antimicrobial resistance in in Enugu state Nigeria. Pharm OnLine. 2019;1:166–76. hospital acquired infections: problems and possible solutions. BMJ. 90. Adetutu AA, Oritsewehinmi B, Khiwili OM, Moradeke AO, Odochi AS, 1998;317(7159):652–4. Adeola OE. Studies on Staphylococcus aureus isolated from pimples. Pak 112. Guta M, Aragaw K, Merid Y. Bacteria from infected surgical wounds and J Biol Sci. 2017;20:350–4. their antimicrobial resistance in Hawassa University referral teaching 91. Bale MI, Babatunde SK, Awe S. prevalence of methicillin resistant hospital, southern Ethiopia. Afr J Microbiol Res. 2014;8(11):1118–24. Staphylococcus aureus bacteriuria among pregnant women attend- 113. Dessalegn L, Shimelis T, Tadesse E, Gebre-selassie S. Aerobic bacterial ing secondary health hospitals in LLorin, Nigeria. J Adv Microbiol. isolates from post-surgical wound and their antimicrobial suscep- 2021;21(9):2456–7116. tibility pattern: a hospital based cross-sectional study. J Med Res. 92. Nmema EE. Risk factors for infection of Staphylococcus aureus: nasal car- 2014;3(2):18–23. riage, skin carriage and multi-antibiotic resistance in healthy individuals. 114. DACA. Antimicrobials use, resistance and containment baseline survey: Br J Med Med Res. 2017;21(9):1–8. syntheses of findings. In: 2009th ed. Addis Ababa; 2009. 93. Ike B, Ugwu MC, Ikegbunam MN, Nwobodo D, Ejikeugwu C, Gugu 115. Falagas ME, Karageorgopoulos DE, Leptidis J, Korbila IP. MRSA in T, et al. Prevalence, antibiogram and molecular characterization of Africa: filling the global map of antimicrobial resistance. PLoS ONE. comunity-acquired methicillin-resistant Staphylococcus aureus in AWKA, 2013;8(7):e68024. Anambra Nigeria. Open Microbiol J. 2016;10:211–21. 94. Ugwu MC, Mokwe NM, Ejikeugwu P, Enemor EC, Eze CO, Ugwu BC, et al. Publisher’s Note Antibiogram of Staphylococcus aureus from healthy school pupils in Springer Nature remains neutral with regard to jurisdictional claims in pub- Agulu, Southeastern Nigeria. Int J Res Pharm Biosci. 2015;2(4):5–9. lished maps and institutional affiliations. 95. Emeka-Nwabunnia I, Chiegboka NA, Udensi UJ, Nwaokorie FO. Vancomycin-resistant Staphylococcus aureus isolates from HIV positive patients in Imo State, Nigeria. Sci J Public Health. 2015;3(5):1–7. 96. Alli OAT, Ogbolu DO, Mustapha JO, Akinbami R, Ajayi AO. The non- association of Panton-valentine leukocidin and mecA genes in the

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Antimicrobial Resistance and Infection Control – Springer Journals

Published: Apr 25, 2023

Keywords: Antibiotic resistance; Meta-analysis; Nigeria; Staphylococcus aureus

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A meta-analysis on the prevalence of resistance of Staphylococcus aureus to different antibiotics in Nigeria

A meta-analysis on the prevalence of resistance of Staphylococcus aureus to different antibiotics in Nigeria

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A meta-analysis on the prevalence of resistance of Staphylococcus aureus to different antibiotics in Nigeria

A meta-analysis on the prevalence of resistance of Staphylococcus aureus to different antibiotics in Nigeria

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