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Prevalence of methicillin-resistant Staphylococcus aureus carriage on admission among patients attending regional hospitals in Dar es Salaam, Tanzania

Prevalence of methicillin-resistant Staphylococcus aureus carriage on admission among patients... Background: Methicillin-resistant Staphylococcus aureus (MRSA) is a major pathogen responsible for hospital and community acquired infection. Colonization with MRSA is associated with a high risk of developing infection. This study aimed to determine the rate of MRSA carriage on admission and the associated risk factors among patients attending regional hospitals, in Dar es Salaam, Tanzania. Results: A total of 258 patients were included in this study. Nasal swabs were collected on admission to the hospi- tal and after 48 h of hospital stay for detection of MRSA. Of 258 patients enrolled, 89 (34.5%) were colonized with S. aureus and out them 22 (24.7%) were carriers of MRSA, giving an overall MRSA nasal carriage rate of 8.5% (22/258). One patient acquired MRSA while admitted in the hospital. Most of the S. aureus isolates 85 (95.5%) were resistant to penicillin. Resistance to gentamycin, ciprofloxacin, kanamycin, linezolid and mupirocin were 14.6, 11.2, 11.2, 3.4 and 1.1%, respectively. The prevalence of inducible clindamycin resistance, constitutive clindamycin resistance, MS phe- notype (resistance to erythromycin alone), and multidrug resistance was 21.3, 3.4, 12.4, and 16.9%, respectively. We observed a statistically significant association between MRSA and multiple drugs resistance among S. aureus isolates (p = 0.001). Of the risk factors investigated none were statistically significant associated with MRSA. Conclusion: There is a high prevalence of MRSA among patients on admission at the two municipal hospitals in Dar es Salaam. The high prevalence of MRSA and the increased rates of resistance to commonly used antimicrobials among MRSA isolates call for attention to the importance of including the screening of MRSA in our hospitals setting in order to prevent further spread of MRSA strains to other patients and to the communities. Control and prevention strategies should be emphasized including decolonization. Keywords: MRSA nasal carriage, Infection, Antibiotic resistance rates of MRSA infections in the community settings, Background which are referred to as Community acquired MRSA [1, Methicillin-resistant Staphylococcus aureus (MRSA) is 2]. MRSA remains a major pathogen in nosocomial infec- an important cause of hospital-acquired infection lead- tions in developing countries [3]. Carriage of antimicro- ing to a high morbidity and mortality among patients bial-resistant strain like MRSA puts an individual at high worldwide. Recent studies have also reported increasing risk of developing infection [4]. The rate of developing infection following MRSA colonization is reported to be approximately 30% [4, 5]. Of concern is the high mortal- *Correspondence: agricolaj@muhas.ac.tz; agricolaj@yahoo.com Department of Microbiology and Immunology, Muhimbili University ity associated with MRSA infections. Infection due to S. of Health and Allied Sciences, Dar Es Salaam, Tanzania aureus ranges from mild to moderate skin and soft tissue Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Joachim et al. BMC Res Notes (2017) 10:417 Page 2 of 7 infections to invasive life-threatening systemic infections [30]. These studies used clinical specimens from hospital - [6]. ized patients who presented with symptoms and/or signs Carriage rates or infections with MRSA vary by geo- of infection. In Tanzania, no study has been conducted graphical location, type of health care facility, and the on MRSA screening among patients at the time of admis- specific population being studied. Studies have reported sion to hospitals. The current study was undertaken to prevalence of MRSA carriage on admission ranging investigate the rate of MRSA carriage on admission and from 2.6 to 8% with higher prevalence reported among the associated risk factors among patients attending the elderly patients [7–11]. Reports have shown that approxi- Amana and Mwananyamala regional hospitals in Dar es mately 80–95% of MRSA carriages are asymptomatic Salaam, Tanzania. [12]. However, harboring of MRSA strains during the time of hospital admission may have negative conse- Methods quences not only on patients’ management but also affect Study design and sampling procedures the implementation of infection control measures in the This was a hospital based cross-sectional study conducted hospital especially where resources are limited [3]. One at two regional hospitals, Mwananyamala and Amana of the consequences of admitted patients who are carry- in Dar es Salaam, Tanzania. Using Kish–Leslie formula ing MRSA is the increase in the risk of transmitting the and a reported prevalence of MRSA of 23% at MNH, Dar pathogen to other patients and health workers [13, 14]. es Salaam Tanzania by Moyo et  al. [30], a minimum sam- Populations at risk of acquiring MRSA infection include ple size of 283 was targeted. However, were able to enroll people with underlying chronic infections [15–17]. Such 258 patients. All eligible patients admitted at emergency conditions may result in severe complications and fatal department or medical ward between March and August consequences, especially if multiple antibiotic resist- 2015 were recruited in the study after obtained an informed ant strains are involved. Other reported risk factors for consent. Children below 5  years of age and patients who MRSA acquisition include prolonged hospitalization, were using antibiotic at the time of recruitment or within visiting an outpatient clinic, patients with a skin or soft- 2 weeks were excluded. Structured questionnaire was used tissue infection, working in health care facilities as well to collect social demographic information including age, as history of antibiotic use [17–20]. However, the risk sex, level of education and residence. Risk factors associ- factors for MRSA colonization at the time of hospital ated with MRSA including current and previous medical admission among patients are not well known. Identify- history and use of antibiotic in the past 3 months were also ing MRSA colonization at admission could target a high- collected. Furthermore, patients who stayed in the hospi- risk population that may benefit from interventions to tal for 48  h or more following admission were requested decrease the risk for developing MRSA infection. to provide a second set of nasal specimen. These were the Studies have shown that strategies to screen for colo- same patients whom we collected nasal samples on admis- nized patients at admission and decolonize them may sion and were more likely to have serious illness compared lead to the reduction of the transmission rate of MRSA to other patients. A total of 20 patients were available for [21, 22]. Elimination of MRSA carriage through the appli- second sample collection. cation of decolonization agents, such as nasal mupirocin and chlorhexidine soap has been reported elsewhere [14]. Sample collection and transportation Development of resistance to antimicrobial agents Well-trained health personnel collected nasal specimens among staphylococci is an increasing problem world- from both anterior nares of each patient using a sterile wide [23]. The increasing rate of MRSA multiple-drug cotton wool swab on admission. Second set of nasal swab resistant strains, which limits the therapeutic options was collected 48–72 h after admission. Nasal swabs were available for the management of MRSA related infec- placed in Stuart transport media and transported to the tions, has become a serious concern worldwide. Several microbiology and immunology laboratory at Muhimbili studies have reported the use of macrolide-lincosamide- University of Health and Allied Sciences (MUHAS) and streptogramin B (MLS ) in the treatment of staphylococ- processed within 24 h of collection. cal infections, where clindamycin is used as alternative treatment. However risks of treatment failure due MLS Laboratory procedures inducible resistance are reported to frequently increase Nasal swabs were inoculated into mannitol salt agar plates [24–26]. (OXOID, Basingstoke, United Kingdom) for S. aureus Previous studies conducted in Tanzania at Muhimbili isolation. The plates were incubated at 37  °C and exam - national hospital (MNH) and Bugando medical center ined for growth after 24–48 h. Isolates were identified as have documented an increasing prevalence of hospital- S. aureus based on colonial morphology, gram staining, acquired MRSA; 0.4% [27], 8% [28], 16.3% [29] and 23% catalase test, coagulase test and DNase test positive. The Joachim et al. BMC Res Notes (2017) 10:417 Page 3 of 7 antimicrobial susceptibility testing was carried out using Nasal carriage of S. aureus, MRSA, and antibiotic Kirby–Bauer’s disc diffusion method according to clinical susceptibility patterns and laboratory standards institute (CLSI) 2015 guidelines A total of 89/258 (34.5%) S. aureus were isolated from the [31]. The following standard antibiotic disks (OXOID UK) samples collected on admission to the hospital. Of the 89 were used; penicillin G (10  U), kanamycin (30  µg), gen- isolates, 22 (24.7%) were MRSA while 67 (75.3%) were tamicin (10 µg), erythromycin (15 µg), clindamycin (2 µg), methicillin susceptible S. aureus (MSSA) making the over- ciprofloxacin (5  µg), linezolid (30  µg) and mupirocin all prevalence of MRSA among all patients to be 22/258 (5  µg). A standard inoculum was prepared by direct col- (8.5%). Only 20 patients were available for second samples ony suspension in saline and compared with 0.5 McFar- collection due to the fact that most of the patients were land standard turbidity and inoculated on Muller Hinton discharged from the hospital before 48  h of admission. agar plate (OXOID UK). Plates were incubated at 35 °C for Of the 20 samples collected, four had S. aureus isolated, 18–24  h. Results were interpreted according to the CLSI and two out of these had MRSA carriage. One patient had guidelines [31]. MRSA detection was done using cefoxitin MRSA on admission while the second one was MRSA discs (OXOID UK) according to CLSI 2015 guidelines. All negative on admission. Table  1 shows the characteristics isolates resistant to cefoxitin were considered as MRSA. of the patients at admission to the hospital, according An inhibition zone of 21 mm or less around cefoxitin disc to their MRSA status (positive or negative). Of the total indicated MRSA [31]. S. aureus ATCC 25923 was used for number of patients colonized with MRSA, more than half quality control. 12 (54.5%) were male, half 11(50%) were aged 18–30 years In addition clindamycin inducible resistance was also and 13 (59.1%) had informal or primary education level. tested by D test as per CLSI guidelines [31]. Briefly, Most of patients who tested MRSA positive 21 (95.5%) erythromycin (15  μg) disk was placed at a distance of had no history of previous hospital admission and 18 15–26  mm (edge to edge) from clindamycin (2  μg) disk on a Mueller–Hinton agar plate. After overnight incuba- Table 1 Characteristics of  study participants with  and tion, plates were examined for the formation of flattened without MRSA zone of inhibition adjacent to the erythromycin disk. For- mation of D-shape with erythromycin indicated a posi- Characteristic MRSA positive MRSA negative tive clindamycin inducible resistant (iMLS ). Resistance N = 22 N = 236 to both clindamycin and erythromycin was recorded as n (%) n (%) constitutive resistance ( cMLS ) and MS phenotype if the Age group in years isolate was resistant to erythromycin only [31]. 7–17 3 (13.6) 21 (8.9) Data analysis 18–30 11 (50) 91 (38.6) Data obtained were analysed using statistical program 31–60 7 (31.8) 102 (43.2) for social sciences (SPSS) version 17.0. Chi square test or >60 1 (4.5) 22 (9.3) Fisher’s exact test was used where applicable to compare Sex the proportions of categorical independent and depend- Male 12 (54.5) 96 (40.7) ent variables. Univariate and multivariate analysis were Female 10 (45.5) 140 (59.3) performed to determine the risk factors associated with Education attained nasal S. aureus and MRSA colonization. A p value of Primary education and below 13 (59.1) 120 (50.8) <0.05 was considered as statistically significant. Secondary education and above 9 (40.9) 116 (49.2) History of antibiotic use Results Yes 4 (18.2) 33 (14.0) A total of 258 patients were enrolled during the study No 18 (81.8) 203 (86.0) period. Of these, 150 (58.1%) were females. The mean History of hospitalisation age was 34 years, ranging from 10 to 80 years. Half of the Yes 1 (4.5) 19 (8.1) patients 129 (50%) were from Kinondoni, 97 (38%) from No 21 (95.5) 217 (91.9) Ilala and 32 (12%) from Temeke districts. Majority of the History of attending OPC patients 133 (51.6%) had informal or attained primary Yes 4 (18.2) 56 (23.7) education. Of 258 patients, 20 (7.8%) had history of pre- No 18 (81.8) 180 (76.3) vious hospitalization while 60 (23%) had attended outpa- Type of illness on admission tient clinic prior to the current admission. Thirty-seven Chronic illness 5 (22.7) 39 (16.5) (14.3%) patients had received antibiotics within the past Acute illness 17 (77.3) 197 (83.5) 3 months. OPC outpatient clinic Joachim et al. BMC Res Notes (2017) 10:417 Page 4 of 7 (81.8%) had neither history of attending outpatient clinic 0.81–5.72]. The use of antibiotic within the past 3 months nor use of antibiotic in the past 3  months. A higher fre- appears to influence the risk of MRSA carriage (OR 1.36 quency of MRSA was detected among patients diagnosed [95% CI 0.43–4.20]) whereas as history of previous hospi- with acute illness 17 (77.3%) on admission compared to talization or attending outpatient clinic did not influence patients with chronic illness 5 (22.7%) Table 1. the rate of MRSA colonization (OR, 0.71 [95% CI 0.07– Most of the S. aureus isolates 85 (95.5%) were resist- 6.45] and 0.88 [95% CI 0.25–3.10]), respectively (Table 4). ant to penicillin. Resistance to gentamycin, ciprofloxacin, kanamycin and linezolid were 14.6, 11.2, 11.2 and 3.4%, Discussion respectively. Only one (1.1%) isolate that was MSSA was The present study determined the rate of MRSA car - found to be resistant to mupirocin. Antimicrobial resist- riage on admission among patients attending hospitals ance pattern of MRSA and MSSA are summarized in in Dar es Salaam. The overall prevalence of MRSA car - Table 2. We found higher rates of resistance to gentamy- riage among all patients investigated in this study was cin, ciprofloxacin and kanamycin among MRSA isolates 8.5%. These findings are consistent with reports from compared to MSSA isolates, (p = 0.00). other studies [7, 8, 11]. We observed a high proportion The prevalence of iMLS, cMLS , MS phenotype, and of MRSA (24.7%) among patients who were colonized B B MDR was 21.3, 3.4, 12.4, and 16.9%, respectively. There with S. aureus. The prevalence reported here is compa - was a statistically significant association between MRSA rable with reports from previous studies conducted in and multiple drugs resistance (MDR) among S. aureus Tanzania [30] but higher than the prevalence reported isolates (p = 0.001) (Table 3). by Mshana et  al. who found a prevalence of 16.2% [29]. The higher prevalence in our study could be due to dif - Factors associated with MRSA carriage ferences in the populations studied. While this study was Chronic illness increases the risk of MRSA colonization looking for MRSA carriage among admitted patients the two times compared to acute illness (odd ratio OR, 1.96 other study [29] searched for MRSA from clinical iso- [95% CI 0.52–7.31]). Male patients are more likely to be lates. Differences observed could also be due to different MRSA carrier than females with an odds ratio 2.15 [95% CI geographical locations of these studies. Our study was conducted in Dar es Salaam, which is considered to be more overcrowded/overpopulated city; this might have Table 2 Antimicrobial resistance pattern among  MRSA increased the risk of transmission. and MSSA isolates Previous study has demonstrated that the risk of acquir- ing MRSA increase with the length of hospital stay [32]. Antimicrobial drug MRSA MSSA p value In this study we also aimed to assess the risk of acquiring n = 22 (%) n = 67 (%) MRSA for those who were initially free of the organism at Penicillin NA 63 (94) the time of admission but acquired the same while in the Ceftriaxone NA 0 hospital. Twenty patients were available for second sam- Gentamycin 10 (45.5) 3 (4.5) 0.00 ples collection, 48 h after admission. One patient who was Ciprofloxacin 8 (36.4) 2 (3) 0.00 MRSA negative at the time of admission was MRSA posi- Kanamycin 8 (36.4) 2 (3) 0.00 tive after 48 h of staying in the hospital indicating that the Linezolid 2 (9.1) 1 (1.5) 0.23 organism was acquired while in the hospital. Mupirocin 0 (0) 1 (1.5) The antimicrobial resistance pattern reported in this MRSA methicillin-resistant Staphylococcus aureus, MSSA methicillin-susceptible S. study shows that MRSA isolates were resistant to most aureus, NA not applicable commonly used antibiotics. Resistance to gentamycin, ciprofloxacin and kanamycin were significantly higher among MRSA isolates compared to MSSA. Low resist- Table 3 Prevalence of  different antimicrobial resistance ance towards Linezolid (3.4%) indicates that this antibi- type among MRSA and MSSA isolates otic might be an option for empirical therapy of MRSA Resistance Overall MRSA N = 22 MSSA N = 67 p value infections at our hospitals. All MRSA isolates were sen- type N = 89 sitive to mupirocin with only one MSSA isolate (1.1%) n (%) n (%) n (%) demonstrating resistance. Various rates of mupirocin resistance among MRSA isolates have been described in iMLS 19 (21.3) 7 (31.8) 12 (17.9) 0.22 hospitalized patients ranging from 0 to 65% [33–37]. Our cMLS 3 (3.4) 2 (9.1) 1 (1.5) 0.14 results indicate that mupirocin is still suitable for decolo- MS pheno- 11 (12.4) 6 (27.3) 5 (7.5) 0.02 type nization as well as treatment of staphylococcal skin infec- MDR 19 (21.3) 16 (72.7) 3 (4.5%) 0.001 tion in our settings. Joachim et al. BMC Res Notes (2017) 10:417 Page 5 of 7 Table 4 Univariate and multivariate association between MRSA carriage and risk factors Characteristic N = 258 MRSA positive Univariate Multivariate n (%) p value; OR (95%) p value; OR (95%) Age group in years 7–17 24 3 (12.5) 0.29; 3.2 (0.37–40.5) 0.25; 4.1 (0.36–47.6) 18–30 102 11 (10.8) 0.178; 4.6 (0.49–44.5) 0.126; 6.1 (0.60–63.6) 31–60 109 7 (3.6) 0.99; 1.5 (−0.57–3.70) 0.88; 1.2 (0.11–12.7) >60 23 1 (4.3) 1 1 Sex Male 108 12 (11.1) 0.124; 2.15 (0.81–5.72) 0.104; 2.3 (0.84–6.42) Female 150 10 (6.7) 1 1 Education attained Primary education and below 133 13 (9.8) 0.46; 1.39 (0.57–3.39) 0.36; 1.6 (0.57–4.46) Secondary education and above 125 9 (7.2) 1 1 History of antibiotic use Yes 37 4 (11.0) 0.59; 1.36 (0.43–4.2) 0.38; 1.72 (0.5–5.8) No 221 18 (8.0) 1 1 History of hospitalisation Yes 20 1 (5.0) 0.76; 0.715 (0.079–6.45) 0.66; 0.60 (0.63–5.85) No 238 21 (8.8) 1 1 History of attending OPC Yes 60 4 (6.7) 0.84; 0.88 (0.25–3.1) 0.92; 0.94 (0.26–3.33) No 198 18 (9.1) 1 1 Type of illness on admission Chronic illness 44 5 (11.4) 0.314; 1.96 (0.52–7.31) 0.41; 1.74 (0.46–6.57) Acute illness 214 17 (7.9) 1 OPC outpatient clinic The use of macrolide-lincosamide-streptogramin B acquiring the pathogen. Previous studies have reported (MLSB) antibiotics in the treatment of both methicillin exposure to antibiotic is associated with risk of MRSA susceptible and resistant staphylococcal infections with colonization [18, 38]. Our findings showed a trend of clindamycin being used as alternative treatment has been but non-significantly higher MRSA among patients with reported [24]. In the current study we observed high previous exposure to antibiotics. This could be due to prevalence of iMLSB in both MRSA and MSSA isolates. our small sample size. Alternatively, there is a possibility Similar observations have been reported by other stud- that some of the patients may have not recalled properly ies conducted in and outside our settings [23, 26, 29, 30]. the information on antibiotic use for the past 3  months The high prevalence of iMLSB is an indication of possible and even for those who reported some could not men- therapeutic failure when using clindamycin in S. aureus tion the name of antibiotic or type of drug used thus infection. Notably therapeutic failures caused by mac- underestimating the role of this factor as risk for MRSA rolide-lincosamide-streptogramin B inducible resistance acquisition. Furthermore, our findings differ from the are being more commonly reported [26]. A limitation of findings of other studies, which have reported history of this study is lack of molecular confirmation and charac - previous hospitalization to be associated with increased terization of MRSA strains due to financial constraints risk of MRSA carriage [18, 38]. The lack of association making is difficult to determine the circulating MRSA may be due to the small number of patients with such genotypes. risk in the population investigated resulting into lack of In the current study we found patients with chronic ill- power to identify such associations, and this is another ness had twofold increase in the risk of acquiring MRSA limitation of our study. Studies conducted elsewhere compared to patients with acute illness. Similar findings have strongly suggested that males have a higher risk of have been reported earlier [16, 17]. This can be due to MRSA carriage [39, 40]. In this study, we observed that the fact that most of the patients with chronic disease the risk of acquiring MRSA strain were twice higher in visit hospital often and thus increasing the chance of male than in the female patients. This could be attributed Joachim et al. BMC Res Notes (2017) 10:417 Page 6 of 7 findings of this study was also sought from the participants/guardian in man- by gender differences in behavior practices and hygiene ner that will not disclose any direct personal information. such as hand washing and use of soap or playing contact sports and occupation, which may influence MRSA colo - Funding This work was supported financially by the Swedish International Develop - nization. Other risk factors associated with MRSA colo- ment Cooperation Agency (Sida) supported core funds at MUHAS. nization have been reported elsewhere [9, 11, 41] but we found no association with age or level of education. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub- Conclusion lished maps and institutional affiliations. We report a high prevalence of MRSA among patients Received: 7 December 2016 Accepted: 21 July 2017 on admission at the two municipal hospitals in Dar es Salaam, Tanzania. The high prevalence of MRSA and the increased rates of resistance to commonly used antimi- crobials among MRSA isolates call for attention to the importance of including the screening of MRSA in our References 1. Layton MC, Hierholzer WJ, Patterson JE. The evolving epidemiology of hospitals setting in order to prevent further spread of methicillin-resistant Staphylococcus aureus at a university hospital. Infect MRSA strains to other patients and to the communities. Control Hosp Epidemiol. 1995;16:12–7. Control and prevention strategies should be emphasized 2. Shiv-Sekhar C, Pallab R, Arun A, Anindita D, Meera S. 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Prevalence of methicillin-resistant Staphylococcus aureus carriage on admission among patients attending regional hospitals in Dar es Salaam, Tanzania

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Springer Journals
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2017 The Author(s)
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1756-0500
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10.1186/s13104-017-2668-8
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Abstract

Background: Methicillin-resistant Staphylococcus aureus (MRSA) is a major pathogen responsible for hospital and community acquired infection. Colonization with MRSA is associated with a high risk of developing infection. This study aimed to determine the rate of MRSA carriage on admission and the associated risk factors among patients attending regional hospitals, in Dar es Salaam, Tanzania. Results: A total of 258 patients were included in this study. Nasal swabs were collected on admission to the hospi- tal and after 48 h of hospital stay for detection of MRSA. Of 258 patients enrolled, 89 (34.5%) were colonized with S. aureus and out them 22 (24.7%) were carriers of MRSA, giving an overall MRSA nasal carriage rate of 8.5% (22/258). One patient acquired MRSA while admitted in the hospital. Most of the S. aureus isolates 85 (95.5%) were resistant to penicillin. Resistance to gentamycin, ciprofloxacin, kanamycin, linezolid and mupirocin were 14.6, 11.2, 11.2, 3.4 and 1.1%, respectively. The prevalence of inducible clindamycin resistance, constitutive clindamycin resistance, MS phe- notype (resistance to erythromycin alone), and multidrug resistance was 21.3, 3.4, 12.4, and 16.9%, respectively. We observed a statistically significant association between MRSA and multiple drugs resistance among S. aureus isolates (p = 0.001). Of the risk factors investigated none were statistically significant associated with MRSA. Conclusion: There is a high prevalence of MRSA among patients on admission at the two municipal hospitals in Dar es Salaam. The high prevalence of MRSA and the increased rates of resistance to commonly used antimicrobials among MRSA isolates call for attention to the importance of including the screening of MRSA in our hospitals setting in order to prevent further spread of MRSA strains to other patients and to the communities. Control and prevention strategies should be emphasized including decolonization. Keywords: MRSA nasal carriage, Infection, Antibiotic resistance rates of MRSA infections in the community settings, Background which are referred to as Community acquired MRSA [1, Methicillin-resistant Staphylococcus aureus (MRSA) is 2]. MRSA remains a major pathogen in nosocomial infec- an important cause of hospital-acquired infection lead- tions in developing countries [3]. Carriage of antimicro- ing to a high morbidity and mortality among patients bial-resistant strain like MRSA puts an individual at high worldwide. Recent studies have also reported increasing risk of developing infection [4]. The rate of developing infection following MRSA colonization is reported to be approximately 30% [4, 5]. Of concern is the high mortal- *Correspondence: agricolaj@muhas.ac.tz; agricolaj@yahoo.com Department of Microbiology and Immunology, Muhimbili University ity associated with MRSA infections. Infection due to S. of Health and Allied Sciences, Dar Es Salaam, Tanzania aureus ranges from mild to moderate skin and soft tissue Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Joachim et al. BMC Res Notes (2017) 10:417 Page 2 of 7 infections to invasive life-threatening systemic infections [30]. These studies used clinical specimens from hospital - [6]. ized patients who presented with symptoms and/or signs Carriage rates or infections with MRSA vary by geo- of infection. In Tanzania, no study has been conducted graphical location, type of health care facility, and the on MRSA screening among patients at the time of admis- specific population being studied. Studies have reported sion to hospitals. The current study was undertaken to prevalence of MRSA carriage on admission ranging investigate the rate of MRSA carriage on admission and from 2.6 to 8% with higher prevalence reported among the associated risk factors among patients attending the elderly patients [7–11]. Reports have shown that approxi- Amana and Mwananyamala regional hospitals in Dar es mately 80–95% of MRSA carriages are asymptomatic Salaam, Tanzania. [12]. However, harboring of MRSA strains during the time of hospital admission may have negative conse- Methods quences not only on patients’ management but also affect Study design and sampling procedures the implementation of infection control measures in the This was a hospital based cross-sectional study conducted hospital especially where resources are limited [3]. One at two regional hospitals, Mwananyamala and Amana of the consequences of admitted patients who are carry- in Dar es Salaam, Tanzania. Using Kish–Leslie formula ing MRSA is the increase in the risk of transmitting the and a reported prevalence of MRSA of 23% at MNH, Dar pathogen to other patients and health workers [13, 14]. es Salaam Tanzania by Moyo et  al. [30], a minimum sam- Populations at risk of acquiring MRSA infection include ple size of 283 was targeted. However, were able to enroll people with underlying chronic infections [15–17]. Such 258 patients. All eligible patients admitted at emergency conditions may result in severe complications and fatal department or medical ward between March and August consequences, especially if multiple antibiotic resist- 2015 were recruited in the study after obtained an informed ant strains are involved. Other reported risk factors for consent. Children below 5  years of age and patients who MRSA acquisition include prolonged hospitalization, were using antibiotic at the time of recruitment or within visiting an outpatient clinic, patients with a skin or soft- 2 weeks were excluded. Structured questionnaire was used tissue infection, working in health care facilities as well to collect social demographic information including age, as history of antibiotic use [17–20]. However, the risk sex, level of education and residence. Risk factors associ- factors for MRSA colonization at the time of hospital ated with MRSA including current and previous medical admission among patients are not well known. Identify- history and use of antibiotic in the past 3 months were also ing MRSA colonization at admission could target a high- collected. Furthermore, patients who stayed in the hospi- risk population that may benefit from interventions to tal for 48  h or more following admission were requested decrease the risk for developing MRSA infection. to provide a second set of nasal specimen. These were the Studies have shown that strategies to screen for colo- same patients whom we collected nasal samples on admis- nized patients at admission and decolonize them may sion and were more likely to have serious illness compared lead to the reduction of the transmission rate of MRSA to other patients. A total of 20 patients were available for [21, 22]. Elimination of MRSA carriage through the appli- second sample collection. cation of decolonization agents, such as nasal mupirocin and chlorhexidine soap has been reported elsewhere [14]. Sample collection and transportation Development of resistance to antimicrobial agents Well-trained health personnel collected nasal specimens among staphylococci is an increasing problem world- from both anterior nares of each patient using a sterile wide [23]. The increasing rate of MRSA multiple-drug cotton wool swab on admission. Second set of nasal swab resistant strains, which limits the therapeutic options was collected 48–72 h after admission. Nasal swabs were available for the management of MRSA related infec- placed in Stuart transport media and transported to the tions, has become a serious concern worldwide. Several microbiology and immunology laboratory at Muhimbili studies have reported the use of macrolide-lincosamide- University of Health and Allied Sciences (MUHAS) and streptogramin B (MLS ) in the treatment of staphylococ- processed within 24 h of collection. cal infections, where clindamycin is used as alternative treatment. However risks of treatment failure due MLS Laboratory procedures inducible resistance are reported to frequently increase Nasal swabs were inoculated into mannitol salt agar plates [24–26]. (OXOID, Basingstoke, United Kingdom) for S. aureus Previous studies conducted in Tanzania at Muhimbili isolation. The plates were incubated at 37  °C and exam - national hospital (MNH) and Bugando medical center ined for growth after 24–48 h. Isolates were identified as have documented an increasing prevalence of hospital- S. aureus based on colonial morphology, gram staining, acquired MRSA; 0.4% [27], 8% [28], 16.3% [29] and 23% catalase test, coagulase test and DNase test positive. The Joachim et al. BMC Res Notes (2017) 10:417 Page 3 of 7 antimicrobial susceptibility testing was carried out using Nasal carriage of S. aureus, MRSA, and antibiotic Kirby–Bauer’s disc diffusion method according to clinical susceptibility patterns and laboratory standards institute (CLSI) 2015 guidelines A total of 89/258 (34.5%) S. aureus were isolated from the [31]. The following standard antibiotic disks (OXOID UK) samples collected on admission to the hospital. Of the 89 were used; penicillin G (10  U), kanamycin (30  µg), gen- isolates, 22 (24.7%) were MRSA while 67 (75.3%) were tamicin (10 µg), erythromycin (15 µg), clindamycin (2 µg), methicillin susceptible S. aureus (MSSA) making the over- ciprofloxacin (5  µg), linezolid (30  µg) and mupirocin all prevalence of MRSA among all patients to be 22/258 (5  µg). A standard inoculum was prepared by direct col- (8.5%). Only 20 patients were available for second samples ony suspension in saline and compared with 0.5 McFar- collection due to the fact that most of the patients were land standard turbidity and inoculated on Muller Hinton discharged from the hospital before 48  h of admission. agar plate (OXOID UK). Plates were incubated at 35 °C for Of the 20 samples collected, four had S. aureus isolated, 18–24  h. Results were interpreted according to the CLSI and two out of these had MRSA carriage. One patient had guidelines [31]. MRSA detection was done using cefoxitin MRSA on admission while the second one was MRSA discs (OXOID UK) according to CLSI 2015 guidelines. All negative on admission. Table  1 shows the characteristics isolates resistant to cefoxitin were considered as MRSA. of the patients at admission to the hospital, according An inhibition zone of 21 mm or less around cefoxitin disc to their MRSA status (positive or negative). Of the total indicated MRSA [31]. S. aureus ATCC 25923 was used for number of patients colonized with MRSA, more than half quality control. 12 (54.5%) were male, half 11(50%) were aged 18–30 years In addition clindamycin inducible resistance was also and 13 (59.1%) had informal or primary education level. tested by D test as per CLSI guidelines [31]. Briefly, Most of patients who tested MRSA positive 21 (95.5%) erythromycin (15  μg) disk was placed at a distance of had no history of previous hospital admission and 18 15–26  mm (edge to edge) from clindamycin (2  μg) disk on a Mueller–Hinton agar plate. After overnight incuba- Table 1 Characteristics of  study participants with  and tion, plates were examined for the formation of flattened without MRSA zone of inhibition adjacent to the erythromycin disk. For- mation of D-shape with erythromycin indicated a posi- Characteristic MRSA positive MRSA negative tive clindamycin inducible resistant (iMLS ). Resistance N = 22 N = 236 to both clindamycin and erythromycin was recorded as n (%) n (%) constitutive resistance ( cMLS ) and MS phenotype if the Age group in years isolate was resistant to erythromycin only [31]. 7–17 3 (13.6) 21 (8.9) Data analysis 18–30 11 (50) 91 (38.6) Data obtained were analysed using statistical program 31–60 7 (31.8) 102 (43.2) for social sciences (SPSS) version 17.0. Chi square test or >60 1 (4.5) 22 (9.3) Fisher’s exact test was used where applicable to compare Sex the proportions of categorical independent and depend- Male 12 (54.5) 96 (40.7) ent variables. Univariate and multivariate analysis were Female 10 (45.5) 140 (59.3) performed to determine the risk factors associated with Education attained nasal S. aureus and MRSA colonization. A p value of Primary education and below 13 (59.1) 120 (50.8) <0.05 was considered as statistically significant. Secondary education and above 9 (40.9) 116 (49.2) History of antibiotic use Results Yes 4 (18.2) 33 (14.0) A total of 258 patients were enrolled during the study No 18 (81.8) 203 (86.0) period. Of these, 150 (58.1%) were females. The mean History of hospitalisation age was 34 years, ranging from 10 to 80 years. Half of the Yes 1 (4.5) 19 (8.1) patients 129 (50%) were from Kinondoni, 97 (38%) from No 21 (95.5) 217 (91.9) Ilala and 32 (12%) from Temeke districts. Majority of the History of attending OPC patients 133 (51.6%) had informal or attained primary Yes 4 (18.2) 56 (23.7) education. Of 258 patients, 20 (7.8%) had history of pre- No 18 (81.8) 180 (76.3) vious hospitalization while 60 (23%) had attended outpa- Type of illness on admission tient clinic prior to the current admission. Thirty-seven Chronic illness 5 (22.7) 39 (16.5) (14.3%) patients had received antibiotics within the past Acute illness 17 (77.3) 197 (83.5) 3 months. OPC outpatient clinic Joachim et al. BMC Res Notes (2017) 10:417 Page 4 of 7 (81.8%) had neither history of attending outpatient clinic 0.81–5.72]. The use of antibiotic within the past 3 months nor use of antibiotic in the past 3  months. A higher fre- appears to influence the risk of MRSA carriage (OR 1.36 quency of MRSA was detected among patients diagnosed [95% CI 0.43–4.20]) whereas as history of previous hospi- with acute illness 17 (77.3%) on admission compared to talization or attending outpatient clinic did not influence patients with chronic illness 5 (22.7%) Table 1. the rate of MRSA colonization (OR, 0.71 [95% CI 0.07– Most of the S. aureus isolates 85 (95.5%) were resist- 6.45] and 0.88 [95% CI 0.25–3.10]), respectively (Table 4). ant to penicillin. Resistance to gentamycin, ciprofloxacin, kanamycin and linezolid were 14.6, 11.2, 11.2 and 3.4%, Discussion respectively. Only one (1.1%) isolate that was MSSA was The present study determined the rate of MRSA car - found to be resistant to mupirocin. Antimicrobial resist- riage on admission among patients attending hospitals ance pattern of MRSA and MSSA are summarized in in Dar es Salaam. The overall prevalence of MRSA car - Table 2. We found higher rates of resistance to gentamy- riage among all patients investigated in this study was cin, ciprofloxacin and kanamycin among MRSA isolates 8.5%. These findings are consistent with reports from compared to MSSA isolates, (p = 0.00). other studies [7, 8, 11]. We observed a high proportion The prevalence of iMLS, cMLS , MS phenotype, and of MRSA (24.7%) among patients who were colonized B B MDR was 21.3, 3.4, 12.4, and 16.9%, respectively. There with S. aureus. The prevalence reported here is compa - was a statistically significant association between MRSA rable with reports from previous studies conducted in and multiple drugs resistance (MDR) among S. aureus Tanzania [30] but higher than the prevalence reported isolates (p = 0.001) (Table 3). by Mshana et  al. who found a prevalence of 16.2% [29]. The higher prevalence in our study could be due to dif - Factors associated with MRSA carriage ferences in the populations studied. While this study was Chronic illness increases the risk of MRSA colonization looking for MRSA carriage among admitted patients the two times compared to acute illness (odd ratio OR, 1.96 other study [29] searched for MRSA from clinical iso- [95% CI 0.52–7.31]). Male patients are more likely to be lates. Differences observed could also be due to different MRSA carrier than females with an odds ratio 2.15 [95% CI geographical locations of these studies. Our study was conducted in Dar es Salaam, which is considered to be more overcrowded/overpopulated city; this might have Table 2 Antimicrobial resistance pattern among  MRSA increased the risk of transmission. and MSSA isolates Previous study has demonstrated that the risk of acquir- ing MRSA increase with the length of hospital stay [32]. Antimicrobial drug MRSA MSSA p value In this study we also aimed to assess the risk of acquiring n = 22 (%) n = 67 (%) MRSA for those who were initially free of the organism at Penicillin NA 63 (94) the time of admission but acquired the same while in the Ceftriaxone NA 0 hospital. Twenty patients were available for second sam- Gentamycin 10 (45.5) 3 (4.5) 0.00 ples collection, 48 h after admission. One patient who was Ciprofloxacin 8 (36.4) 2 (3) 0.00 MRSA negative at the time of admission was MRSA posi- Kanamycin 8 (36.4) 2 (3) 0.00 tive after 48 h of staying in the hospital indicating that the Linezolid 2 (9.1) 1 (1.5) 0.23 organism was acquired while in the hospital. Mupirocin 0 (0) 1 (1.5) The antimicrobial resistance pattern reported in this MRSA methicillin-resistant Staphylococcus aureus, MSSA methicillin-susceptible S. study shows that MRSA isolates were resistant to most aureus, NA not applicable commonly used antibiotics. Resistance to gentamycin, ciprofloxacin and kanamycin were significantly higher among MRSA isolates compared to MSSA. Low resist- Table 3 Prevalence of  different antimicrobial resistance ance towards Linezolid (3.4%) indicates that this antibi- type among MRSA and MSSA isolates otic might be an option for empirical therapy of MRSA Resistance Overall MRSA N = 22 MSSA N = 67 p value infections at our hospitals. All MRSA isolates were sen- type N = 89 sitive to mupirocin with only one MSSA isolate (1.1%) n (%) n (%) n (%) demonstrating resistance. Various rates of mupirocin resistance among MRSA isolates have been described in iMLS 19 (21.3) 7 (31.8) 12 (17.9) 0.22 hospitalized patients ranging from 0 to 65% [33–37]. Our cMLS 3 (3.4) 2 (9.1) 1 (1.5) 0.14 results indicate that mupirocin is still suitable for decolo- MS pheno- 11 (12.4) 6 (27.3) 5 (7.5) 0.02 type nization as well as treatment of staphylococcal skin infec- MDR 19 (21.3) 16 (72.7) 3 (4.5%) 0.001 tion in our settings. Joachim et al. BMC Res Notes (2017) 10:417 Page 5 of 7 Table 4 Univariate and multivariate association between MRSA carriage and risk factors Characteristic N = 258 MRSA positive Univariate Multivariate n (%) p value; OR (95%) p value; OR (95%) Age group in years 7–17 24 3 (12.5) 0.29; 3.2 (0.37–40.5) 0.25; 4.1 (0.36–47.6) 18–30 102 11 (10.8) 0.178; 4.6 (0.49–44.5) 0.126; 6.1 (0.60–63.6) 31–60 109 7 (3.6) 0.99; 1.5 (−0.57–3.70) 0.88; 1.2 (0.11–12.7) >60 23 1 (4.3) 1 1 Sex Male 108 12 (11.1) 0.124; 2.15 (0.81–5.72) 0.104; 2.3 (0.84–6.42) Female 150 10 (6.7) 1 1 Education attained Primary education and below 133 13 (9.8) 0.46; 1.39 (0.57–3.39) 0.36; 1.6 (0.57–4.46) Secondary education and above 125 9 (7.2) 1 1 History of antibiotic use Yes 37 4 (11.0) 0.59; 1.36 (0.43–4.2) 0.38; 1.72 (0.5–5.8) No 221 18 (8.0) 1 1 History of hospitalisation Yes 20 1 (5.0) 0.76; 0.715 (0.079–6.45) 0.66; 0.60 (0.63–5.85) No 238 21 (8.8) 1 1 History of attending OPC Yes 60 4 (6.7) 0.84; 0.88 (0.25–3.1) 0.92; 0.94 (0.26–3.33) No 198 18 (9.1) 1 1 Type of illness on admission Chronic illness 44 5 (11.4) 0.314; 1.96 (0.52–7.31) 0.41; 1.74 (0.46–6.57) Acute illness 214 17 (7.9) 1 OPC outpatient clinic The use of macrolide-lincosamide-streptogramin B acquiring the pathogen. Previous studies have reported (MLSB) antibiotics in the treatment of both methicillin exposure to antibiotic is associated with risk of MRSA susceptible and resistant staphylococcal infections with colonization [18, 38]. Our findings showed a trend of clindamycin being used as alternative treatment has been but non-significantly higher MRSA among patients with reported [24]. In the current study we observed high previous exposure to antibiotics. This could be due to prevalence of iMLSB in both MRSA and MSSA isolates. our small sample size. Alternatively, there is a possibility Similar observations have been reported by other stud- that some of the patients may have not recalled properly ies conducted in and outside our settings [23, 26, 29, 30]. the information on antibiotic use for the past 3  months The high prevalence of iMLSB is an indication of possible and even for those who reported some could not men- therapeutic failure when using clindamycin in S. aureus tion the name of antibiotic or type of drug used thus infection. Notably therapeutic failures caused by mac- underestimating the role of this factor as risk for MRSA rolide-lincosamide-streptogramin B inducible resistance acquisition. Furthermore, our findings differ from the are being more commonly reported [26]. A limitation of findings of other studies, which have reported history of this study is lack of molecular confirmation and charac - previous hospitalization to be associated with increased terization of MRSA strains due to financial constraints risk of MRSA carriage [18, 38]. The lack of association making is difficult to determine the circulating MRSA may be due to the small number of patients with such genotypes. risk in the population investigated resulting into lack of In the current study we found patients with chronic ill- power to identify such associations, and this is another ness had twofold increase in the risk of acquiring MRSA limitation of our study. Studies conducted elsewhere compared to patients with acute illness. Similar findings have strongly suggested that males have a higher risk of have been reported earlier [16, 17]. This can be due to MRSA carriage [39, 40]. In this study, we observed that the fact that most of the patients with chronic disease the risk of acquiring MRSA strain were twice higher in visit hospital often and thus increasing the chance of male than in the female patients. This could be attributed Joachim et al. BMC Res Notes (2017) 10:417 Page 6 of 7 findings of this study was also sought from the participants/guardian in man- by gender differences in behavior practices and hygiene ner that will not disclose any direct personal information. such as hand washing and use of soap or playing contact sports and occupation, which may influence MRSA colo - Funding This work was supported financially by the Swedish International Develop - nization. Other risk factors associated with MRSA colo- ment Cooperation Agency (Sida) supported core funds at MUHAS. nization have been reported elsewhere [9, 11, 41] but we found no association with age or level of education. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub- Conclusion lished maps and institutional affiliations. We report a high prevalence of MRSA among patients Received: 7 December 2016 Accepted: 21 July 2017 on admission at the two municipal hospitals in Dar es Salaam, Tanzania. The high prevalence of MRSA and the increased rates of resistance to commonly used antimi- crobials among MRSA isolates call for attention to the importance of including the screening of MRSA in our References 1. Layton MC, Hierholzer WJ, Patterson JE. The evolving epidemiology of hospitals setting in order to prevent further spread of methicillin-resistant Staphylococcus aureus at a university hospital. Infect MRSA strains to other patients and to the communities. Control Hosp Epidemiol. 1995;16:12–7. Control and prevention strategies should be emphasized 2. Shiv-Sekhar C, Pallab R, Arun A, Anindita D, Meera S. 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Journal

BMC Research NotesSpringer Journals

Published: Dec 1, 2017

Keywords: biomedicine, general; medicine/public health, general; life sciences, general

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