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/lp/springer-journals/mupirocin-resistant-staphylococcus-aureus-in-africa-a-systematic-6KRM0wCb1B
- Publisher
- Springer Journals
- Copyright
- Copyright © The Author(s). 2018
- Subject
- Biomedicine; Medical Microbiology; Drug Resistance; Infectious Diseases
- eISSN
- 2047-2994
- DOI
- 10.1186/s13756-018-0382-5
- Publisher site
- See Article on Publisher Site
Abstract
Background: Mupirocin is widely used for nasal decolonization of Staphylococcus aureus to prevent subsequent staphylococcal infection in patients and healthcare personnel. However, the prolonged and unrestricted use has led to the emergence of mupirocin-resistant (mupR) S. aureus. The aim of this systematic review was to investigate the prevalence, phenotypic and molecular characteristics, and geographic spread of mupR S. aureus in Africa. Methods: We examined five electronic databases (EBSCOhost, Google Scholar, ISI Web of Science, MEDLINE, and Scopus) for relevant English articles on screening for mupR S. aureus from various samples in Africa. In addition, we performed random effects meta-analysis of proportions to determine the pooled prevalence of mupR S. aureus in Africa. The search was conducted until 3 August 2016. Results: We identified 43 eligible studies of which 11 (26%) were obtained only through Google Scholar. Most of the eligible studies (28/43; 65%) were conducted in Nigeria (10/43; 23%), Egypt (7/43; 16%), South Africa (6/43; 14%) and Tunisia (5/43; 12%). Overall, screening for mupR S. aureus was described in only 12 of 54 (22%) African countries. The disk diffusion method was the widely used technique (67%; 29/43) for the detection of mupR S. aureus in Africa. The mupA-positive S. aureus isolates were identified in five studies conducted in Egypt (n = 2), South Africa (n = 2), and Nigeria (n = 1). Low-level resistance (LmupR) and high-level resistance (HmupR) were both reported in six human studies from South Africa (n = 3), Egypt (n = 2) and Libya (n = 1). Data on mupR-MRSA was available in 11 studies from five countries, including Egypt, Ghana, Libya, Nigeria and South Africa. The pooled prevalence (based on 11 human studies) of mupR S. aureus in Africa was 14% (95% CI =6.8 to 23.2%). The proportion of mupA-positive S. aureus in Africa ranged between 0.5 and 8%. Furthermore, the frequency of S. aureus isolates that exhibited LmupR, HmupR and mupR-MRSA in Africa were 4 and 47%, 0.5 and 38%, 5 and 50%, respectively. Conclusions: The prevalence of mupR S. aureus in Africa (14%) is worrisome and there is a need for data on administration and use of mupirocin. The disk diffusion method which is widely utilized in Africa could be an important method for the screening and identification of mupR S. aureus. Moreover, we advocate for surveillance studies with appropriate guidelines for screening mupR S. aureus in Africa. Keywords: Africa, Prevalence, Meta-analysis, Mupirocin, Staphylococcus aureus, Systematic review * Correspondence: bayo_shittu@yahoo.com Department of Microbiology, Obafemi Awolowo University, Ile-Ife, Osun State 22005, Nigeria Full list of author information is available at the end of the article © The Author(s). 2018 Open Access 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. Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 2 of 16 Background and AS) from five electronic databases (EBSCOhost, Staphylococcus aureus is a well-recognized human patho- Google Scholar, ISI Web of Science, MEDLINE, and gen that is implicated in a wide array of superficial, Scopus). The search terms for each database are re- invasive and toxigenic infections [1]. Meta-analyses of ported in Table 1. The literature search was concluded published studies have provided evidence that S. aureus on 3 August 2016. nasal carriage is an important risk factor for subsequent infection among patients with surgical site infections and Eligible article identification atopic dermatitis [2, 3]. Other high-risk groups include pa- The identification of the eligible articles was conducted tients colonized with methicillin-resistant Staphylococcus according to the guidelines for preferred reporting items aureus (MRSA) undergoing dialysis, and patients admitted for systematic reviews and meta-analyses (PRISMA) in the intensive care unit [4, 5]. Consequently, infection [23]. We defined an eligible article as a peer-reviewed prevention strategies such as nasal decolonization are publication that (i) included mupirocin in the antibiotic employed to minimize the occurrence of staphylococcal susceptibility testing of S. aureus isolates, and (ii) infection and reduce the risk of transmission in healthcare employed phenotypic ((disc diffusion, E-test, minimum settings [6, 7]. Mupirocin (2%) nasal ointment alone or in inhibitory concentration (MIC), VITEK and other auto- combination with 4% chlorhexidine (CHG) based body mated methods)), and/or molecular ((conventional or wash is considered as the main decolonization strategy for real-time polymerase chain reaction (PCR)) techniques. S. aureus carriage [8, 9]. Mupirocin is a naturally occur- International multicentre studies that included African ring antibiotic produced by Pseudomonas fluorescens that countries were also eligible for inclusion. interferes with protein synthesis by competitive inhibition of the bacterial isoleucyl-tRNA synthetase (IRS) [10, 11]. Data extraction and analysis It gained prominence in the mid-1990s for the eradication The relevant data were extracted from each of the eligible of S. aureus nasal carriage due to its effectiveness, safety articles included in this systematic review. A study that and cost [12]. analysed S. aureus isolates from another investigation but Mupirocin-resistant (mupR) S. aureus was first reported answered a different research question were both consid- in the United Kingdom in 1987 [13]. Since then, it has been ered as one study (Table 2). We performed three levels of reported in several countries worldwide [14–17]. The emer- analysis (Fig. 1). First, to understand the characteristics gence of mupR S. aureus has been associated with unre- and geographic spread of mupR S. aureus in Africa, stricted policies and use of mupirocin for long periods in studies that included mupirocin in the antibiotic suscepti- health care settings [8, 18]. Decolonization failure in pa- bility testing and employed phenotypic and/or molecular tients with S. aureus carriage is associated with high-level techniques were identified. Secondly, the prevalence of mupirocin resistance (HmupR - minimum inhibitory con- S. aureus with the mupA gene, isolates that expressed centration [MIC]: ≥512 μg/ml), while that of low-level LmupR and HmupR, and mupR-MRSA in Africa were mupirocin resistance (LmupR – MIC: 8-64 μg/ml) is still derived from each eligible study as follows: unclear [7, 19]. LmupR is mediated through point mutation MupA‐positive S: aureus (largely V588F and V631F) in the native isoleucyl-tRNA Number of MupA‐positive S: aureus isolates synthetase (ileS)gene[20]. In contrast, HmupR is mainly Total number of isolates screened with mupirocin attributed to the acquisition of plasmids with the mupA (or ileS2) gene encoding an additional IRS with no affinity for S: aureus that expressed LmupR mupirocin [11, 21]. Anotherdeterminant forHmupR is the Number of S: aureus isolates with LmupR acquisition of a plasmid-mediated mupB gene [22]. Total number of isolates screened with mupirocin There is no data summarizing reports on screening, S: aureus that expressed HmupR prevalence, characterization, and geographic spread of Number of S: aureus isolates with HmupR mupR S. aureus in Africa. This systematic review evaluated Total number of isolates screened with mupirocin published articles that assessed for mupirocin resistance in African S. aureus isolates. The findings from this systematic MupR‐MRSA review highlight the need to develop an early warning sys- Number of mupR‐MRSA isolates tem, including harmonized strategies for the prompt Total number of isolates screened with mupirocin screening and identification of mupR S. aureus in Africa. Methods Thirdly, to estimate the prevalence of mupR S. aureus in Literature search strategy humans, studies that employed at least one of the screen- The relevant English articles from human and animal in- ing methods with defined breakpoint for mupirocin resist- vestigations were retrieved by three authors (YA, SA, ance were included in the meta-analysis. The StatsDirect Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 3 of 16 Table 1 Keywords used to identify eligible studies available in five biomedical databases Database Search period Search strategy MEDLINE via PubMed 1974 - August 2016 (Staphylococcus aureus OR S. aureus) EBSCOhost via Academic Search premier, 1982 - August 2016 AND Africa-Wide information and CINAHL (Mupirocin) AND ISI Web of Science 1950 - August 2016 (Algeria OR Angola OR Benin OR Botswana OR Burkina Faso OR “Burkina Faso” OR Burkina Fasso OR Upper Volta OR “Upper Volta” OR Burundi OR Cameroon OR Cape Verde OR “Cape Verde” OR Central African Republic OR Chad OR Comoros OR “Iles Comores” OR Iles Comores OR Comoro Islands OR “Comoro Islands” OR Congo OR Democratic Republic Congo OR “Democratic Republic of the Congo” OR Zaire OR Djibouti OR Egypt OR Equatorial Guinea OR “Equatorial Guinea” OR Eritrea OR Ethiopia OR Gabon OR Gambia OR Ghana OR Guinea OR Guinea Bissau OR “Guinea Bissau” OR Ivory Coast OR “Ivory Coast” OR Cote d’Ivoire OR “Cote d’Ivoire” OR Kenya OR Lesotho OR Liberia OR Libya OR Libia OR Jamahiriya OR Jamahiryia OR Madagascar OR Malawi OR Mali OR Mauritania OR Mauritius OR Ile Maurice OR “Ile Maurice” OR Morocco OR Mozambique OR Moçambique OR Namibia OR Niger OR Nigeria OR Rwanda OR Sao Tome OR “Sao Tome” OR Senegal OR Seychelles OR Sierra Leone OR “Sierra Leone” OR Somalia OR South Africa OR “South Africa” OR Sudan OR South Sudan OR “South Sudan” OR Swaziland OR Tanzania OR Tanganyika OR Zanzibar OR Togo OR Tunisia OR Uganda OR Western Sahara OR “Western Sahara” OR Zambia OR Zimbabwe OR Africa OR Africa* OR Southern Africa OR West Africa OR Western Africa OR Eastern Africa OR East Africa OR North Africa OR Northern Africa OR Central Africa OR Sub Saharan Africa OR Subsaharan Africa OR Sub-Saharan Africa) NOT (Guinea pig* OR “Guinea pig*” OR Aspergillus niger OR “Aspergillus niger” OR Europe* OR America* OR Asia*) Scopus from SciVerse 1982 - August 2016 (Staphylococcus aureus OR S. aureus) AND (Mupirocin) AND (Africa) Google Scholar** (Staphylococcus aureus OR S. aureus) AND (Mupirocin) AND (Name of each African country) Examples (Staphylococcus aureus OR S. aureus) AND (Mupirocin) AND (Algeria) (Staphylococcus aureus OR S. aureus) AND (Mupirocin) AND (Zimbabwe) The African countries were manually selected (as recommended by Scopus database) to exclude studies from other continents **The Google Scholar search was conducted between July-September 2015 statistical software version 3.0.165 (England: StatsDir- animal sources (n = 1), and cockroaches (n = 1). Most ectLtd.2016) was utilized to assess the heterogeneity of of the eligible studies (32/43; 74%) were obtained from the eligible studies included in the meta-analysis EBSCOhost, ISI Web of Science, MEDLINE, and Scopus. (Cochran Q-test) [24], and to ascertain the inconsist- The remaining studies (11/43; 26%) were obtained ency across the studies (I2 statistic) [25]. The random only through Google Scholar and consisted of studies effects model was used to determine the pooled preva- conducted in Egypt [28–31], South Africa [32–34], lence of mupR S. aureus in Africa. The criterion for Nigeria [35, 36], Ethiopia [37] and Kenya [38]. statistical significance for heterogeneity was set at alpha = 0.05. The risk of publication bias was assessed Screening and identification of mupR S. aureus in Africa and visualized by a Funnel plot [26, 27]. Only 12 of the 54 (22%) African countries reported data on screening for mupR S. aureus (Fig. 2). The first pub- lished article indicated that mupirocin had been in use in Results Africa, at least from the late 1980s [39]. Most of these Eligible studies from electronic database search studies (28/43; 65%) were conducted in Nigeria (10/43; We identified 43 reports (Table 1)ofwhich 34 studies 23%), Egypt (7/43; 16%), South Africa (6/43; 14%) and investigated only human samples. The remaining nine Tunisia (5/43; 12%) (Fig. 2). MupR S. aureus was mainly studies assessed samples from only animals (n =5), identified through the disk diffusion method (29/43; 67%). human and environmental sources (n =2), human and The guidelines by the Clinical and Laboratory Standards Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 4 of 16 Table 2 Characteristics of the 43 eligible studies on screening for mupirocin resistance in Staphylococcus aureus from various sources in Africa Region Country Study Period Setting Sample Method for Guideline Published Number of Mupirocin resistant isolates Reference testing (year of reports for S. aureus Source Type Number Number Number Number mupA gene + resistance to publication) detection isolates (%) MRSA (%) LmupR/ LMupR/HmupR (Method) mupirocin of mupR screened HmupR S. aureus with mupirocin North Algeria 2005–2007 C & H Human Pus, venous Disk diffusion CLSI (NA) – 19 0 (0) 0 (0) –– [47] Africa catheter, tracheal VITEK-2 aspirate, punction fluid, blood, urine Egypt 2005–2006 C & H Human NA Disk diffusion NCCLS – 64 0 (0) 0 (0) –– [28] (2003) Egypt 2008–2009 C & H Human Skin and soft Disk diffusion CLSI (2007) – 386 1 (0.3) NA NA – [29] tissue, post- operative wound swab Egypt 2007–2008 C Human Pus, sputum, Broth dilution CLSI (2005) – 21 0 (0) 0 (0) –– [58] catheter, blood, urine, wound abscess Egypt 2010 H Human Sputum, blood, E-test – Kresken 86 30 (34.9) 30 (34.9) 25/5 2/3 (PCR) [30] catheter, et al., traumatic wound, (2004) urine Egypt 2012 H Human Wound discharge, Disk diffusion CLSI (2007) – 150 0 (0) 0 (0) –– [40] blood, body fluid Agar dilution aspirate, urine, faeces, sputum, nasal, throat, ear and genital swab Egypt 2012–2013 H Human Nasal swab Disk diffusion CLSI (2011) – 39 3 (7.7) 3 (3.7) NA – [31] Egypt 2013–2015 H Human Pus & Wound Agar dilution CLSI (2011) – 73 13 (17.8) 13 (17.8) 5/8 0/6 (PCR) [52] swab Libya NA H Human Skin swab Disk diffusion NA – 40 0 (0) NA –– [61] Libya 2008–2009 H Human & NA Disk diffusion BSAC – 86 13 (15.1) 13 (8.1) NA – [56] Environment (2008) Libya 2009 H Human Nasal swab Disk diffusion BSAC – 109 5 (4.6) 5 (4.6) 4/1 – [57] Agar dilution (2008) Morocco 2008- H Human Nasal swab Disk diffusion CA-SFM – 81 0 (0) 0 (0) –– [62] (2007) Tunisia 2008–2009 C Human Nasal swab Disk diffusion CLSI (2008) – 55 0 (0) 0 (0) –– [41] Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 5 of 16 Table 2 Characteristics of the 43 eligible studies on screening for mupirocin resistance in Staphylococcus aureus from various sources in Africa (Continued) Region Country Study Period Setting Sample Method for Guideline Published Number of Mupirocin resistant isolates Reference testing (year of reports for S. aureus Source Type Number Number Number Number mupA gene + resistance to publication) detection isolates (%) MRSA (%) LmupR/ LMupR/HmupR (Method) mupirocin of mupR screened HmupR S. aureus with mupirocin Tunisia 2003–2005 C Human Pus, blood, Phoenix CA-SFM – 64 NA NA –– [59] articular puncture, Automated (2006) venous catheter Microbiology System Tunisia 2013 H Human Wound abscess Disk diffusion CA-SFM – 8NA NA –– [60] (2013) Tunisia 2010 C Animal Nasal swab Disk diffusion CLSI (2010) – 73 0 (0) 0 (0) –– [42] (Sheep) Tunisia 2010 C Animal Nasal swab Disk diffusion CLSI (2010) – 50 0 (0) 0 (0) –– [43] (Donkeys) West Ghana 2011–2012 H Human Nasal swab Disk diffusion EUCAST – 105 1 (0.9) 0 (0) 0/1 – [54] Africa (2012) Ghana 2011–2012 C Human Nasal swab Disk diffusion EUCAST – 124 0 (0) 0 (0) –– [67] (2012) Ghana 2010–2013 C & H Human NA Broth EUCAST – 30 4 (13.3) 4 (13.3) 4/0 0/0 (DNA microarray) [55] microdilution (NA) Ghana 2012–2013 C Human Nasal & Wound VITEK-2 EUCAST – 91 0 (0) 0 (0) –– [68] swab (NA) Nigeria* NA NA Human NA Disk diffusion NA – 1 0 (0) 0 (0) –– [80] Nigeria* 2002–2004 H Human Wound, blood, Disk diffusion – Udo et al., 200 1 (0.5) 0 (0) 0/1 0/1 (PCR) [53] ear, eye, urine (1999) Nigeria 2006 C Human Nasal swab Disk diffusion CLSI (2005) – 101 12 (11.9) NA NA – [44] Nigeria 2007 H Human NA Disk diffusion CLSI (NA) – 96 0 (0) 0 (0) –– [48] Nigeria* NA H Human Wound swab, Disk diffusion NCCLS – 1 1 0 (0) 0/1 0/1 (PCR) [45] blood, urine, E-test (2003) endotracheal aspirate Nigeria 2009 H Human Wound, sputum, Broth DIN 58940 – 68 0 (0) 0 (0) –– [63] semen, nasal microdilution (2004) swab Nigeria 2010 H Human NA VITEK-2 –– 51 0 (0) 0 (0) –– [64] Nigeria 2009–2011 H Human Aspirate, blood, Disk diffusion CLSI (NA) – 62 0 (0) 0 (0) –– [49] ear, eye, vaginal discharge, sputum, wounds, urine, nasal swab Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 6 of 16 Table 2 Characteristics of the 43 eligible studies on screening for mupirocin resistance in Staphylococcus aureus from various sources in Africa (Continued) Region Country Study Period Setting Sample Method for Guideline Published Number of Mupirocin resistant isolates Reference testing (year of reports for S. aureus Source Type Number Number Number Number mupA gene + resistance to publication) detection isolates (%) MRSA (%) LmupR/ LMupR/HmupR (Method) mupirocin of mupR screened HmupR S. aureus with mupirocin Nigeria 2010–2011 H Human NA VITEK-2 EUCAST – 290 0 (0) 0 (0) –– [65] (NA) Nigeria 2008–2010 C Animal Faecal swab Disk diffusion – Udo et al., 107 0 (0) 0 (0) –– [66] (Bats) (1999) Nigeria 2006–2007 C & H Animal Nasal & skin swab Disk diffusion – Udo et al., 173 0 (0) 0 (0) –– [35] (Bovine) & (1999) (Ovine) Nigeria 2012 C Human Nasal swab Disk diffusion CLSI (2006) – 10 Humans 33 (37.9) NA 0/33 – [36] Animal Milk 77 Animals Central Gabon 2009 C & H Human Nasal, axillae, VITEK-2 –– 5 0 (0) 0 (0) –– [69] Africa inguinal swab São Tomé & Príncipe 2010–2012 H Human Nasal swab Disk diffusion BSAC (NA) – 55 0 (0) 0 (0) –– [70] East Ethiopia NA H & R Cockroach Cockroach Body Disk diffusion – Jorgenson 17 17 (100) NA NA – [37] Africa surface/Gut et al., (1999) Kenya 2011 H Human Nasal and axillary VITEK-2 CLSI (2012) – 86 0 (0) 0 (0) –– [71] skin swab Kenya 2011–2013 H Human Pus, blood, urine VITEK-2 CLSI (2010) – 731 0 (0) 0 (0) –– [72] Kenya NA C Animal Raw camel milk Disk diffusion CLSI (2008) – 47 0 (0) 0 (0) –– [38] (Camel) Broth microdilution South South Africa 1996 H Human Wound, urine, Disk diffusion NCCLS – 236 5 (2.1) NA NA – [46] Africa skin and blood (2000) South Africa** 2001–2003 H Human Wound, sputum, Disk diffusion – Udo et al., 227 16 (7.0) 15 (6.6) 14/2 0/2 (PCR) [50] blood (1999) South Africa 2005–2006 H Human Blood, pus & skin Disk diffusion – Udo et al., 248 123 123 117/6 – [32] wound, E-test (2006) (49.6) (49.6) cerebrospinal fluid South Africa** NA H Human Wound swab, Disk diffusion NCCLS – 16 16 (100) 14 (87.5) 14/2 0/2 (PCR) [45] blood, urine, E-test (2003) endotracheal aspirate South Africa 2013 H Human Tissue, blood, Disk diffusion CLSI (2012) – 997 277 NA 43/234 0/5 (Real time PCR) [33] cerebrospinal VITEK-2 (27.8) fluid, wound swab Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 7 of 16 Table 2 Characteristics of the 43 eligible studies on screening for mupirocin resistance in Staphylococcus aureus from various sources in Africa (Continued) Region Country Study Period Setting Sample Method for Guideline Published Number of Mupirocin resistant isolates Reference testing (year of reports for S. aureus Source Type Number Number Number Number mupA gene + resistance to publication) detection isolates (%) MRSA (%) LmupR/ LMupR/HmupR (Method) mupirocin of mupR screened HmupR S. aureus with mupirocin South Africa 2010–2012 H Human Blood Microscan CLSI (2015) – 2709 236 (8.7) 202 (7.5) NA – [51] (MIC Panel Type 33) South Africa 2009–2010 H Human & Nasal & hand VITEK-2 –– 13 4 (30.8) 4 (30.8) 0/4 – [34] Environment swab, dialysate fluid, surface swab, air samples KEY: mupR S. aureus: mupirocin resistant Staphylococcus aureus; LmupR low-level mupirocin resistance, HmupR high-level mupirocin resistance, mupA mupirocin resistance gene, MIC Minimum inhibitory concentration, BSAC British Society for Antimicrobial Chemotherapy, CA-SFM Comité de l’Antibiogramme de la Société Française de Microbiologie, CLSI Clinical and Laboratory Standards Institute, DIN 58940 Deutsches Institut für Normung DIN 58940, EUCAST European Committee on Antimicrobial Susceptibility Testing, NCCLS National Committee for Clinical Laboratory Standards, PCR Polymerase Chain Reaction; − Not determined, NA Not available, H Hospital, C Community, R Restaurant *Separate reports that analyzed the same isolates but answered different questions (considered as one single study) in Nigeria; **: Separate reports that analyzed the same isolates but answered different questions (considered as one single study) in South Africa. Reference [45] is recorded in Nigeria and South Africa, but the isolates were derived from studies in Nigeria [53] and South Africa [50], respectively Other published reports applied for the detection of mupR S. aureus in Africa 1. Jorgenson JH, Turnidge JD, Washington JA. Dilution and disc diffusion method. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, editors. Manual of Clinical Microbiology, 7th edition. American Society for Microbiology, Washington DC, 1999. p. 1526–1543. Adapted from NCCLS: National Committee for Clinical Laboratory Standards 1997. Approved Standard M2-A6; National Committee for Clinical Laboratory Standards 1999. Approved Standard M100-S9. 2. Kresken M, Hafner D, Schmitz FJ, Wichelhaus TA. Prevalence of mupirocin resistance in clinical isolates of Staphylococcus aureus and Staphylococcus epidermidis. Results of the antimicrobial resistance surveillance study of the Paul-Ehrlich Society for Chemotherapy, 2001. Int J Antimicrob Agents, 2004, 23:577–81. The widely accepted breakpoints: ≤4 mg/l (susceptible), 8–256 mg/l (low-level resistance) and ≥ 512 mg/l (high-level resistance) was utilized in this study. 3. Udo EE, Farook VS, Mokadas EM, Jacob LE, Sanyal SC. Molecular fingerprinting of mupirocin-resistant methicillin-resistant Staphylococcus aureus from a burn unit. Int J Infect Dis, 1999,3:82–7. Growth within a 14-mm zone of inhibition with the 5 μg mupirocin disk detected low-level resistance, while growth to the edge of the 200 μg mupirocin disk indicated high-level resistance. 4. Udo EE, Al-Sweih N, Mokaddas E, Johny M, Dhar R, Gomaa HH, Al-Obaid I, Rotimi VO. Antibacterial resistance and their genetic location in MRSA isolated in Kuwait hospitals, 1994–2004. BMC Infect Dis, 2006;6:168. The widely accepted breakpoints:≤4 mg/l (susceptible), 8–256 mg/l (low-level resistance) and ≥ 512 mg/l (high-level resistance) was utilized in this study. Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 8 of 16 90 articles identified through database search: 3177 articles identified through Google scholar � 33 in PubMed; � 39 in EBSCOhost; � 14 in Web of Science; � 4 in Scopus 3168 articles after duplicates removed 3168 articles screened 3120 articles excluded based on title and abstracts 3 Full-text articles excluded, with reasons: � 1 article was not written in English 48 Full-text articles assessed for eligibility � 1 study involved pilgrims from different countries though carried out in Africa � 1 study made use of X-ray 45 articles included in systematic review 2 separate articles that analyzed the same S. aureus 43 articles included in analysis of systematic review isolate but answered different questions 11 articles included in meta-analysis Fig. 1 The Preferred Reporting Items for Systematic Review and Meta-analysis flow diagram Institute (CLSI), previously known as National Committee reported in six African countries including South Africa for Clinical Laboratory Standards (NCCLS), were broadly [32–34, 46, 50, 51], Egypt [29–31, 52], Nigeria [36, 44, used in Africa (Table 2). However, a number of studies 53], Ghana [54, 55], Libya [56, 57] and Ethiopia [37] [28, 29, 31, 33, 36, 40–46] utilized the disk diffusion (Fig. 2;Table 2). The mupA-positive S. aureus was de- method with CLSI guidelines that had no zone diam- tected in five studies from Egypt [30, 52], South Africa eter breakpoint for mupirocin. Moreover, some studies [33, 50]and Nigeria[53]. LmupR and HmupR were [47–49] did not provide information on the year of both reported in six human studies conducted in South publication of the CLSI guidelines. MupR S. aureus was Africa [32, 33, 50], Egypt [30, 52]and Libya[57]. The Nigeria Egypt South Africa Tunisia Ghana Kenya Libya Algeria Ethiopia Gabon Morocco São Tomé and Príncipe Countries Fig. 2 Studies on screening for mupirocin-resistant Staphylococcus aureus in Africa Number of studies Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 9 of 16 Table 3 Prevalence of mupirocin-resistant S. aureus from various sources in Africa based on phenotypic and molecular methods Mupirocin resistance Country Source Number Phenotypic Molecular Guidelines or reports Reference positive/Total Agar Broth Disk E-test Microscan VITEK PCR Micro BSAC CLSI EUCAST Other tested (%) Dilution microdilution diffusion system array reports MupA-positive S. aureus Egypt Human 5/86 (5.8) –– – √ –– √ –– – – √ [30] Egypt Human 6/73 (8.2) √ –– – – – √ –– √ –– [52] Nigeria Human 1/200 (0.5) –– √ –– – √ –– – – √ [53] South Africa Human 2/227 (0.9) –– √ –– – √ –– – – √ [50] South Africa Human NA –– √ –– √√ –– √ –– [33] LmupR S. aureus Egypt Human 25/86 (29.1) –– – √ –– √ –– – – √ [30] Egypt Human 5/73 (6.8) √ –– – – – √ –– √ –– [52] Ghana Human 4/30 (13.3) – √ –– – – – √ –– √ – [55] Libya Human 4/109 (3.7) √ – √ –– – – – √ –– – [57] South Africa Human 14/227 (6.2) –– √ –– – – – – – – √ [50] South Africa Human 117/248 (47.2)–– √√ –– – – – – – √ [32] South Africa Human 43/997 (4.3) –– √ –– √ –– – √ –– [33] South Africa Human & Environment 4/13 (30.8) –– – – – √ –– – – – – [34] HmupR S. aureus Egypt Human 5/86 (5.8) –– – √ –– √ –– – – √ [30] Egypt Human 8/73 (11) √ –– – – – √ –– √ –– [52] Ghana Human 1/105 (1.0) –– √ –– – – – – – √ – [54] Libya Human 1/109 (0.9) √ – √ –– – – – √ –– – [57] Nigeria Human 1/200 (0.5) –– √ –– – √ –– – – √ [53] Nigeria Human 12/101 (11.9) –– √ –– – – – – √ –– [44] Nigeria Human & Animal 33/87 (37.9) –– √ –– – – – – √ –– [36] South Africa Human 2/227 (0.9) –– √ –– – √ –– – – √ [50] South Africa Human 6/248 (2.4) –– √√ –– – – – – – √ [32] South Africa Human 234/997 (23.5)–– √ –– √ –– – √ –– [33] mupR-MRSA Egypt Human 30/86 (34.9) –– – √ –– √ –– – – √ [30] Egypt Human 3/39 (7.7) –– √ –– – – – – √ –– [31] Egypt Human 13/73 (17.8) √ –– – – – √ –– √ –– [52] Ghana Human 4/30 (13.3) – √ –– – – – √ –– √ – [55] Libya Human 13/86 (15.1) –– √ –– – – – √ –– – [56] Libya Human 5/109 (4.6) √ – √ –– – – – √ –– – [57] Nigeria Human & Animal 33/87 (37.9) –– √ –– – – – – √ –– [36] South Africa Human 15/227 (6.6) –– √ –– – √ –– – – √ [50] Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 10 of 16 Table 3 Prevalence of mupirocin-resistant S. aureus from various sources in Africa based on phenotypic and molecular methods (Continued) Mupirocin resistance Country Source Number Phenotypic Molecular Guidelines or reports Reference positive/Total Agar Broth Disk E-test Microscan VITEK PCR Micro BSAC CLSI EUCAST Other tested (%) Dilution microdilution diffusion system array reports South Africa Human 123/248 (49.6)–– √√ –– – – – – – √ [32] South Africa Human 202/2709 (7.5)–– – – √ –– – – √√ – [51] South Africa Human & Environment 4/13 (30.8) –– – – – √ –– – – – – [34] KEY: BSAC British Society for Antimicrobial Chemotherapy, CLSI Clinical and Laboratory Standards Institute, EUCAST European Committee on Antimicrobial Susceptibility Testing, NA Not Available, PCR Polymerase Chain Reaction, √: test was performed. -: test was not performed The widely accepted breakpoints: ≤4 mg/l (susceptible), 8–256 mg/l (low-level resistance) and ≥ 512 mg/l (high-level resistance) was utilized in this study: Kresken M, Hafner D, Schmitz FJ, Wichelhaus TA. Prevalence of mupirocin resistance in clinical isolates of Staphylococcus aureus and Staphylococcus epidermidis. Results of the antimicrobial resistance surveillance study of the Paul-Ehrlich Society for Chemotherapy, 2001. Int J Antimicrob Agents, 2004, 23:577–81. Growth within a 14-mm zone of inhibition with the 5 μg mupirocin disk detected low-level resistance, while growth to the edge of the 200 μg mupirocin disk indicated high-level resistance according to: Udo EE, Farook VS, Mokadas EM, Jacob LE, Sanyal SC. Molecular fingerprinting of mupirocin-resistant methicillin-resistant Staphylococcus aureus from a burn unit. Int J Infect Dis, 1999,3:82–7. The widely accepted breakpoints: ≤4 mg/l (susceptible), 8–256 mg/l (low-level resistance) and ≥ 512 mg/l (high-level resistance) was utilized in this study: Udo EE, Al-Sweih N, Mokaddas E, Johny M, Dhar R, Gomaa HH, Al-Obaid I, Rotimi VO. Antibacterial resistance and their genetic location in MRSA isolated in Kuwait hospitals, 1994–2004. BMC Infect Dis, 2006;6:168 Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 11 of 16 mupR-MRSA isolates were identified in South Africa [32, West Africa 34, 50, 51], Egypt [30, 31, 52], Libya [56, 57], Ghana [55] S. aureus resistance to mupirocin was investigated in and Nigeria [36](Table 3). MupR-MRSA was not reported Nigeria [35, 36, 44, 48, 49, 53, 63–66] and Ghana [54, 55, from MRSA isolates recovered from studies conducted in 67, 68]. Only two studies from Ghana reported on mupR Egypt [28, 58], Tunisia [59, 60] and Algeria [47]. S. aureus [54, 55]. In Nigeria, three studies (including two An assessment of data on mupR S. aureus at the re- from only human sources and one from both animal and gional level is described as follows (Fig. 3). human samples, respectively) reported on S. aureus iso- lates that demonstrated HmupR [36, 44, 53]. North Africa Central Africa Seventeen eligible studies were recorded from this region, MupR S. aureus was not detected in studies conducted including Egypt [28–31, 40, 52, 58], Tunisia [41–43, 59, in Gabon [69], and São Tomé and Príncipe [70]. 60], Libya [56, 57, 61], Algeria [47] and Morocco [62]. MupR S. aureus was reported in six studies conducted in East Africa two North African countries: Egypt [29–31, 52] and Libya In this review, we identified four eligible studies con- [56, 57]. PCR detection of the mupA gene was performed ducted in Kenya [38, 71, 72] and Ethiopia [37]. A report in only two studies conducted in Egypt [30, 52]. In on the role of cockroaches as potential vectors of food- addition, one of the reports identified two mupA positive borne pathogens in Ethiopia identified 17 mupR S. aur- MRSA that exhibited LmupR [30]. MupR S. aureus was eus isolates [37]. All the S. aureus isolates (one animal not detected in Tunisia [41–43, 59, 60], Algeria [47], and and two human studies) from Kenya were susceptible to Morocco [62]. mupirocin [38, 71, 72]. Fig. 3 Geographic distribution of mupirocin-resistant (mupR) Staphylococcus aureus in Africa. Countries (in green) in which mupR S. aureus have been investigated but not reported. Countries (in red) in which mupR S. aureus have been investigated and reported Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 12 of 16 Southern Africa MupR S. aureus and co-resistance to other antibiotics The six studies reported in this geographical area were In this systematic review, two studies (conducted in Egypt from South Africa and consisted of two single centre and South Africa) showed that mupR S. aureus was asso- studies [34, 46] and four multicenter studies [32, 33, 50, ciated with multi-drug resistance [30, 33]. 51]. MupR S. aureus was identified in all the reports, while mupA-positive S. aureus isolates were noted in Molecular characterization of mupR S. aureus in Africa only two studies [33, 50]. Only three studies provided molecular data on mupR S. aureus in Africa [45, 54, 55]. A report provided evidence Prevalence of mupR S. aureus in Africa of a 35 kb (non-conjugative) and 41.1 kb (conjugative) The random-effects pooled prevalence of mupR S. aureus plasmid encoding mupA in S. aureus isolates from Nigeria in Africa is 14% (95% CI =6.8 to 23.2%). This was calcu- and South Africa [45]. It also described an MRSA clone lated based on 11 heterogeneous human studies (Figs. 4 that demonstrated LmupR in South Africa. LmupR was and 5) conducted in South Africa [32, 33, 50, 51], Ghana also identified among MRSA isolates assigned with ST36, [54, 55], Egypt [30, 52], Libya [56, 57] and Nigeria [53]. In ST88, and ST789 in Ghana [55]. A cross-sectional S. aur- Africa, the proportion of S. aureus isolates with the eus study identified a methicillin susceptible S. aureus mupA gene, and those that expressed LmupR and (MSSA) strain with HmupR from a 51-year-old hospital HmupR ranged between 0.5 and 8%, 4 and 47%, 0.5 staff in Ghana [54]. Molecular characterization indicated and 38%, respectively. The frequency of mupR-MRSA that the strain (spa type t4805) was PVL-positive. isolates ranged between 5 and 50% (Table 3). Discussion Association of MupR S. aureus with mupirocin use in This is the first systematic review on mupR S. aureus in Africa Africa and clearly showed the paucity of data on the There is no data on the use of mupirocin as an agent for continent. Nevertheless, this study indicated a high S. aureus decolonization and its association with mupR prevalence ((14% (95% CI =6.8 to 23.2)) of mupR S. aur- S. aureus in Africa. eus in Africa. These observations support the need for mupR S. aureus surveillance data to provide information MupR S. aureus and biofilm production on its epidemiology and clinical significance in Africa. It A report from Egypt noted that mupR-MRSA were mod- is noteworthy that Google Scholar was valuable in the erate to strong biofilm producers [52]. identification of several eligible studies [28–38]. We Fig. 4 Bias assessment (Funnel) plot for studies assessing rates of mupirocin-resistant Staphylococcus aureus in Africa. Random effects (DerSimonian-Laird). Pooled proportion = 0.139303 (95% CI = 0.067511 to 0.23165). Bias indicators, Begg-Mazumdar: Kendall’s tau = 0.2 P = 0.4454, Egger: bias = 4.771137 (95% CI = −2.517874 to 12.060148) P = 0.1728, Harbord: bias = 2.014783 (92.5% CI = −5.90181 to 9.931377) P = 0.6208 Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 13 of 16 Fig. 5 Pooled estimate of proportions (human studies) for mupirocin-resistant Staphylococcus aureus in Africa observed that 26% (11/43) of the eligible studies were Société Française de Microbiologie (CA-SFM) [77, 78]. identified from African journals which were not indexed The breakpoint values for the detection of LmupR and in commonly used electronic databases. Google Scholar differentiation from HmupR are not provided in these has been considered as a useful supplement with other documents(CA-SFM,CLSI, and EUCAST).Despite electronic databases for systematic review search [73] in- this limitation, the disk diffusion method in conjunc- cluding recent meta-analyses of published studies on S. tion with any of these guidelines could at least be valu- aureus in Africa [74, 75]. able for the preliminary screening and identification of The phenotypic methods for the screening and iden- HmupR S. aureus in Africa. MRSA decolonization failure tification of mupR S. aureus include disc diffusion is of clinical significance as it is often attributed to persist- (two-disc strategy: 5 μgand 200 μg), agar dilution, ence or re-colonization associated with isolates exhibiting broth micro-dilution and E-test [19]. In this study, the HmupR, while that of LmupR is not clear [7, 19, 79]. In disk diffusion method and the CLSI (formerly NCCLS) this review, the prevalence of S. aureus that exhibited guidelines were strategies mainly applied to detect mupR LmupR, HmupR and mupR-MRSA in Africa was predi- S. aureus in Africa. However, we observed certain incon- cated on a range of methods using different guidelines. sistencies [28, 29, 31, 33, 36, 40–49]. For instance, a num- We suggest that surveillance data from Africa is estab- ber of studies [28, 29, 31, 33, 36, 40–42, 44–46]applied lished on harmonized guidelines to enhance quality assur- the disk diffusion method with the CLSI guidelines that ance and comparison at the continental and global level. had no breakpoint values for mupirocin. The 2017 CLSI We noted a prevalence of mupR-MRSA ranging guidelines recommend the use of the 200 μg disk to differ- between 5 and 50% in Africa (Table 3). This is of serious entiate between HmupR and the absence of HmupR (i.e. concern. Specifically, the relationship between mupiro- no zone = HmupR; any zone = absence of HmupR) [76]. cin resistance and MRSA has important consequences The 200 μg disk with a different breakpoint (Susceptible on infection control measures and effectiveness of ≥30 mm, Resistance < 18 mm) is also endorsed for the dif- decolonization strategies [8]. MupR-MRSA could limit ferentiation between HmupR and the absence of HmupR the choices available for the control and prevention of in the latest versions (accessed 28th May, 2018) of the healthcare-associated MRSA infections (7, 8). There- European Committee for Antimicrobial Susceptibility fore, surveillance studies are important to investigate Testing (EUCAST) and Comité de l’antibiogramme de la the emergence and spread of mupirocin resistance in Shittu et al. Antimicrobial Resistance and Infection Control (2018) 7:101 Page 14 of 16 hospital settings in Africa. This is important among pa- Consent for publication Not applicable. tients at high risk of MRSA infections, including patients in the dermatology, dialysis and the Intensive Care Units. Competing interests In addition, there is the need for more data on the mo- The authors declare that there are no competing interests. lecular characterization of mupR S. aureus in Africa [45, 54, 55]. For instance, whole genome sequencing (WGS) will assist in understanding the transmission dynamics of Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in mupR S. aureus in Africa. Moreover, WGS data will allow published maps and institutional affiliations. comprehensive investigation of the genetic basis for LmupR mutation (which is largely due to V588F and Author details Department of Microbiology, Obafemi Awolowo University, Ile-Ife, Osun V631F in the native gene (ileS)) and mupB-positive S. aur- State 22005, Nigeria. Division of Medical Microbiology, Department of eus in Africa. Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, Language bias was the main limitation of this system- South Africa. Institute of Infectious Disease and Molecular Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa. atic review as we did not include studies published in French, Portuguese, Arabic and Spanish. 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Journal
Antimicrobial Resistance and Infection Control – Springer Journals
Published: Aug 15, 2018
Keywords: Africa; Prevalence; Meta-analysis; Mupirocin; Staphylococcus aureus; Systematic review