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Published in: Antimicrobial Resistance & Infection Control 1/2018

Open Access 01-12-2018 | Review

Mupirocin-resistant Staphylococcus aureus in Africa: a systematic review and meta-analysis

Authors: Adebayo O. Shittu, Mamadou Kaba, Shima M. Abdulgader, Yewande O. Ajao, Mujibat O. Abiola, Ayodele O. Olatimehin

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2018

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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.
Literature
1.
go back to reference Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339:520–32.PubMed Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339:520–32.PubMed
2.
go back to reference Levy PY, Ollivier M, Drancourt M, Raoult D, Argenson JN. Relation between nasal carriage of Staphylococcus aureus and surgical site infection in orthopedic surgery: the role of nasal contamination. A systematic literature review and meta-analysis. Orthop Traumatol Surg Res. 2013;99:645–51. https://doi.org/10.1016/j.otsr.2013.03.030.PubMed Levy PY, Ollivier M, Drancourt M, Raoult D, Argenson JN. Relation between nasal carriage of Staphylococcus aureus and surgical site infection in orthopedic surgery: the role of nasal contamination. A systematic literature review and meta-analysis. Orthop Traumatol Surg Res. 2013;99:645–51. https://​doi.​org/​10.​1016/​j.​otsr.​2013.​03.​030.PubMed
3.
10.
go back to reference Fuller AT, Mellows G, Woolford M, Banks GT, Barrow KD, Chain EB. Pseudomonic acid: an antibiotic produced by Pseudomonas fluorescens. Nature. 1971;234:416–7.PubMed Fuller AT, Mellows G, Woolford M, Banks GT, Barrow KD, Chain EB. Pseudomonic acid: an antibiotic produced by Pseudomonas fluorescens. Nature. 1971;234:416–7.PubMed
11.
go back to reference Gilbart J, Perry CR, Slocombe B. High-level mupirocin resistance in Staphylococcus aureus: evidence for two distinct isoleucyl-tRNA synthetases. Antimicrob Agents Chemother. 1993;37:32–8.PubMedPubMedCentral Gilbart J, Perry CR, Slocombe B. High-level mupirocin resistance in Staphylococcus aureus: evidence for two distinct isoleucyl-tRNA synthetases. Antimicrob Agents Chemother. 1993;37:32–8.PubMedPubMedCentral
12.
go back to reference Perl TM, Golub JE. New approaches to reduce Staphylococcus aureus nosocomial infection rates: treating S. aureus nasal carriage. Ann Pharmacother. 1998;32:S7–16. Perl TM, Golub JE. New approaches to reduce Staphylococcus aureus nosocomial infection rates: treating S. aureus nasal carriage. Ann Pharmacother. 1998;32:S7–16.
14.
go back to reference Hughes J, Stabler R, Gaunt M, Karadag T, Desai N, Betley J, Ioannou A, Aryee A, Hearn P, Marbach H, Patel A, Otter JA, Edgeworth JD, Tosas AO. Clonal variation in high- and low-level phenotypic and genotypic mupirocin resistance of MRSA isolates in south-East London. J Antimicrob Chemother. 2015;70:3191–9. https://doi.org/10.1093/jac/dkv248.PubMed Hughes J, Stabler R, Gaunt M, Karadag T, Desai N, Betley J, Ioannou A, Aryee A, Hearn P, Marbach H, Patel A, Otter JA, Edgeworth JD, Tosas AO. Clonal variation in high- and low-level phenotypic and genotypic mupirocin resistance of MRSA isolates in south-East London. J Antimicrob Chemother. 2015;70:3191–9. https://​doi.​org/​10.​1093/​jac/​dkv248.PubMed
16.
go back to reference Hayden MK, Lolans K, Haffenreffer K, Avery TR, Kleinman K, Li H, Kaganov RE, Lankiewicz J, Moody J, Septimus E, Weinstein RA, Hickok J, Jernigan J, Perlin JB, Platt R, Huang SS. Chlorhexidine and mupirocin susceptibility of methicillin-resistant Staphylococcus aureus isolates in the REDUCE-MRSA trial. J Clin Microbiol. 2016;54:2735–42.PubMedPubMedCentral Hayden MK, Lolans K, Haffenreffer K, Avery TR, Kleinman K, Li H, Kaganov RE, Lankiewicz J, Moody J, Septimus E, Weinstein RA, Hickok J, Jernigan J, Perlin JB, Platt R, Huang SS. Chlorhexidine and mupirocin susceptibility of methicillin-resistant Staphylococcus aureus isolates in the REDUCE-MRSA trial. J Clin Microbiol. 2016;54:2735–42.PubMedPubMedCentral
17.
19.
go back to reference Swenson JM, Wong B, Simor AE, Thomson RB, Ferraro MJ, Hardy DJ, Hindler J, Jorgensen J, Reller LB, Traczewski M, McDougal LK, Patel JB. Multicenter study to determine disk diffusion and broth microdilution criteria for prediction of high- and low-level mupirocin resistance in Staphylococcus aureus. J Clin Microbiol. 2010;48:2469–75. https://doi.org/10.1128/JCM.00340-10.PubMedPubMedCentral Swenson JM, Wong B, Simor AE, Thomson RB, Ferraro MJ, Hardy DJ, Hindler J, Jorgensen J, Reller LB, Traczewski M, McDougal LK, Patel JB. Multicenter study to determine disk diffusion and broth microdilution criteria for prediction of high- and low-level mupirocin resistance in Staphylococcus aureus. J Clin Microbiol. 2010;48:2469–75. https://​doi.​org/​10.​1128/​JCM.​00340-10.PubMedPubMedCentral
24.
go back to reference Cochran WG. The combination of estimates from different experiments. Biometrics. 1954;10:101–29. Cochran WG. The combination of estimates from different experiments. Biometrics. 1954;10:101–29.
27.
go back to reference Sterne JA, Sutton AJ, Ioannidis JP, Terrin N, Jones DR, Lau J, Carpenter J, Rücker G, Harbord RM, Schmid CH, Tetzlaff J, Deeks JJ, Peters J, Macaskill P, Schwarzer G, Duval S, Altman DG, Moher D, Higgins JP. Recommendations for examining and interpreting funnel plots assymettry in meta-analysis of randomised control trials. BMJ. 2011;342:1–8. https://doi.org/10.1136/bmj.d4002. Sterne JA, Sutton AJ, Ioannidis JP, Terrin N, Jones DR, Lau J, Carpenter J, Rücker G, Harbord RM, Schmid CH, Tetzlaff J, Deeks JJ, Peters J, Macaskill P, Schwarzer G, Duval S, Altman DG, Moher D, Higgins JP. Recommendations for examining and interpreting funnel plots assymettry in meta-analysis of randomised control trials. BMJ. 2011;342:1–8. https://​doi.​org/​10.​1136/​bmj.​d4002.
28.
go back to reference Salama MF. Comparative molecular analysis of community or health care associated methicillin-resistant Staphylococcus aureus. Egypt J Med Microbiol. 2006;15:371–80. Salama MF. Comparative molecular analysis of community or health care associated methicillin-resistant Staphylococcus aureus. Egypt J Med Microbiol. 2006;15:371–80.
29.
go back to reference Taher S, Roshdy H. Prevalence of Panton-Valentine Leukocidin genes among Staphylococcus aureus isolates in Mansoura University hospitals. Egypt J Med Microbiol. 2009;18:97–108. Taher S, Roshdy H. Prevalence of Panton-Valentine Leukocidin genes among Staphylococcus aureus isolates in Mansoura University hospitals. Egypt J Med Microbiol. 2009;18:97–108.
30.
go back to reference Wali I, Ouda N, El-Seidi E. Mupirocin resistance among methicillin resistant Staphylococcus aureus isolates in an Egyptian hospital. Egypt J Med Lab Sci. 2011;20:1–11. Wali I, Ouda N, El-Seidi E. Mupirocin resistance among methicillin resistant Staphylococcus aureus isolates in an Egyptian hospital. Egypt J Med Lab Sci. 2011;20:1–11.
32.
go back to reference Marais E, Aithma N, Perovic O, Oosthuyen WF, Musenge E, Dusé AG. Antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolates from South Africa. S Afr Med J. 2009;99:170–3.PubMed Marais E, Aithma N, Perovic O, Oosthuyen WF, Musenge E, Dusé AG. Antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolates from South Africa. S Afr Med J. 2009;99:170–3.PubMed
33.
go back to reference Wasserman E, Orth H, Senekal M, Harvey K. High prevalence of mupirocin resistance associated with resistance to other antimicrobial agents in Staphylococcus aureus isolated from patients in private health care, Western Cape. South Afr J Infect Dis. 2014;29:126–32. Wasserman E, Orth H, Senekal M, Harvey K. High prevalence of mupirocin resistance associated with resistance to other antimicrobial agents in Staphylococcus aureus isolated from patients in private health care, Western Cape. South Afr J Infect Dis. 2014;29:126–32.
34.
go back to reference Swe Swe K, Naidoo N, Jaglal P. Molecular epidemiology of a suspected methicillin-resistant Staphylococcus aureus outbreak in a renal unit of a central academic hospital in KwaZulu-Natal, South Africa. South Afr J Infect Dis. 2015;30:6–10. Swe Swe K, Naidoo N, Jaglal P. Molecular epidemiology of a suspected methicillin-resistant Staphylococcus aureus outbreak in a renal unit of a central academic hospital in KwaZulu-Natal, South Africa. South Afr J Infect Dis. 2015;30:6–10.
35.
go back to reference Bamaiyi PH, Aniesona AT. Prevalence and antimicrobial susceptibility patterns of bovine and ovine Staphylococcus aureus isolates in Maiduguri, Nigeria. Adv Anim Vet Sci. 2013;1:59–64. Bamaiyi PH, Aniesona AT. Prevalence and antimicrobial susceptibility patterns of bovine and ovine Staphylococcus aureus isolates in Maiduguri, Nigeria. Adv Anim Vet Sci. 2013;1:59–64.
36.
go back to reference Mai-siyama IB, Okon KO, Adamu NB, Askira UM, Isyaka TM, Adamu SG, Mohammed A. Methicillin-resistant Staphylococcus aureus (MRSA) colonization rate among ruminant animals slaughtered for human consumption and contact persons in Maiduguri, Nigeria. Afr J Microbiol Res. 2014;8:2643–9. https://doi.org/10.5897/AJMR2014.6855. Mai-siyama IB, Okon KO, Adamu NB, Askira UM, Isyaka TM, Adamu SG, Mohammed A. Methicillin-resistant Staphylococcus aureus (MRSA) colonization rate among ruminant animals slaughtered for human consumption and contact persons in Maiduguri, Nigeria. Afr J Microbiol Res. 2014;8:2643–9. https://​doi.​org/​10.​5897/​AJMR2014.​6855.
37.
go back to reference Tachbele E, Erku W, Gebre-Michael T, Ashenafi M. Cockroach-associated food-borne bacterial pathogens from some hospitals and restaurants in Addis Ababa, Ethiopia: Distribution and antibiograms. JRTPH. 2006;5:34–41. Tachbele E, Erku W, Gebre-Michael T, Ashenafi M. Cockroach-associated food-borne bacterial pathogens from some hospitals and restaurants in Addis Ababa, Ethiopia: Distribution and antibiograms. JRTPH. 2006;5:34–41.
38.
go back to reference Njage PMK, Dolci S, Jans C, Wangoh J, Lacroix C, Meile L. Phenotypic and genotypic antibiotic resistance patterns of Staphylococcus aureus from raw and spontaneously fermented camel milk. BJAST. 2013;3(3):87–98. Njage PMK, Dolci S, Jans C, Wangoh J, Lacroix C, Meile L. Phenotypic and genotypic antibiotic resistance patterns of Staphylococcus aureus from raw and spontaneously fermented camel milk. BJAST. 2013;3(3):87–98.
39.
go back to reference Rode H, Hanslo D, de Wet PM, Millar AJW, Cywes S. Efficacy of mupirocin in methicillin-resistant Staphylococcus aureus burn wound infection. Antimicrob Agents Chemother. 1989;33:1358–61.PubMedPubMedCentral Rode H, Hanslo D, de Wet PM, Millar AJW, Cywes S. Efficacy of mupirocin in methicillin-resistant Staphylococcus aureus burn wound infection. Antimicrob Agents Chemother. 1989;33:1358–61.PubMedPubMedCentral
41.
go back to reference Ben Slama K, Gharsa H, Klibi N, Jouini A, Lozano C, Gómez-Sanz E, Zarazaga M, Boudabous A, Torres C. Nasal carriage of Staphylococcus aureus in healthy humans with different levels of contact with animals in Tunisia: genetic lineages, methicillin resistance, and virulence factors. Eur J Clin Microbiol Infect Dis. 2011;30:499–508. https://doi.org/10.1007/s10096-010-1109-6.PubMed Ben Slama K, Gharsa H, Klibi N, Jouini A, Lozano C, Gómez-Sanz E, Zarazaga M, Boudabous A, Torres C. Nasal carriage of Staphylococcus aureus in healthy humans with different levels of contact with animals in Tunisia: genetic lineages, methicillin resistance, and virulence factors. Eur J Clin Microbiol Infect Dis. 2011;30:499–508. https://​doi.​org/​10.​1007/​s10096-010-1109-6.PubMed
43.
go back to reference Gharsa H, Sallem RB, Slama KB, Gomez-Sanz E, Lazano C, Jouini A, Klibi N, Zarazaga M, Boudabous A, Torres C. High diversity of genetic lineages and virulence genes in nasal Staphylococcus aureus isolates from donkeys destined to food consumption in Tunisia with predominance of the ruminant associated CC133 lineage. BMC Vet Res. 2012;8:203. https://doi.org/10.1186/1746-6148-8-203.PubMedPubMedCentral Gharsa H, Sallem RB, Slama KB, Gomez-Sanz E, Lazano C, Jouini A, Klibi N, Zarazaga M, Boudabous A, Torres C. High diversity of genetic lineages and virulence genes in nasal Staphylococcus aureus isolates from donkeys destined to food consumption in Tunisia with predominance of the ruminant associated CC133 lineage. BMC Vet Res. 2012;8:203. https://​doi.​org/​10.​1186/​1746-6148-8-203.PubMedPubMedCentral
46.
48.
go back to reference Okon KO, Basset P, Uba A, Lin J, Oyawoye B, Shittu AO, Blanc DS. Co-occurrence of predominant Panton-Valentine Leukocidin-positive sequence type (ST) 152 and multidrug-resistant ST 241 Staphylococcus aureus clones in Nigerian hospitals. J Clin Microbiol. 2009;47:3000–3. https://doi.org/10.1128/JCM.01119-09. Okon KO, Basset P, Uba A, Lin J, Oyawoye B, Shittu AO, Blanc DS. Co-occurrence of predominant Panton-Valentine Leukocidin-positive sequence type (ST) 152 and multidrug-resistant ST 241 Staphylococcus aureus clones in Nigerian hospitals. J Clin Microbiol. 2009;47:3000–3. https://​doi.​org/​10.​1128/​JCM.​01119-09.
51.
go back to reference Perovic O, Iyaloo S, Kularatne R, Lowman W, Bosman N, Wadula J, Seetharam S, Duse A, Mbelle N, Bamford C, Dawood H, Mahabeer Y, Bhola P, Abrahams S, Singh-Moodley A. Prevalence and trends of Staphylococcus aureus bacteraemia in hospitalized patients in South Africa, 2010-2012: laboratory-based surveillance mapping of antimicrobial resistance and molecular epidemiology. PLoS One. 2015;10:e0145429. https://doi.org/10.1371/journal.pone.0145429.PubMedPubMedCentral Perovic O, Iyaloo S, Kularatne R, Lowman W, Bosman N, Wadula J, Seetharam S, Duse A, Mbelle N, Bamford C, Dawood H, Mahabeer Y, Bhola P, Abrahams S, Singh-Moodley A. Prevalence and trends of Staphylococcus aureus bacteraemia in hospitalized patients in South Africa, 2010-2012: laboratory-based surveillance mapping of antimicrobial resistance and molecular epidemiology. PLoS One. 2015;10:e0145429. https://​doi.​org/​10.​1371/​journal.​pone.​0145429.PubMedPubMedCentral
53.
go back to reference Shittu A, Lin J, Kolawole D. Antimicrobial susceptibility patterns of Staphylococcus aureus and characterization of MRSA in southwestern Nigeria. Wounds. 2006;18:77–84. Shittu A, Lin J, Kolawole D. Antimicrobial susceptibility patterns of Staphylococcus aureus and characterization of MRSA in southwestern Nigeria. Wounds. 2006;18:77–84.
57.
go back to reference Ahmed MO, Elramalli AK, Amri SG, Abuzweda AR, Abouzeed YM. Isolation and screening of methicillin-resistant Staphylococcus aureus from health care workers in Libyan hospitals. EMHJ. 2012;18:37–42.PubMed Ahmed MO, Elramalli AK, Amri SG, Abuzweda AR, Abouzeed YM. Isolation and screening of methicillin-resistant Staphylococcus aureus from health care workers in Libyan hospitals. EMHJ. 2012;18:37–42.PubMed
62.
go back to reference Souly K, Ait el Kadi M, Lhmadi K, Biougnach H, Boughaidi A, Zouhdi M, Benasila S, Elyoussefi Z, Bouattar T, Zbiti N, Skalli Z, Rhou H, Ouzeddoun N, Bayahia R, Benamar L. Epidemiology and prevention of Staphylococcus aureus nasal carriage in hemodialyzed patients. Med Mal Infect. 2011;41:469–74. https://doi.org/10.1016/j.medmal.2011.05.005. Souly K, Ait el Kadi M, Lhmadi K, Biougnach H, Boughaidi A, Zouhdi M, Benasila S, Elyoussefi Z, Bouattar T, Zbiti N, Skalli Z, Rhou H, Ouzeddoun N, Bayahia R, Benamar L. Epidemiology and prevention of Staphylococcus aureus nasal carriage in hemodialyzed patients. Med Mal Infect. 2011;41:469–74. https://​doi.​org/​10.​1016/​j.​medmal.​2011.​05.​005.
65.
69.
go back to reference Ngoa UA, Schaumburg F, Adegnika AA, Kösters K, Möller T, Fernandes JF, Alabi A, Issifou S, Becker K, Grobusch MP, Kremsner PG, Lell B. Epidemiology and population structure of Staphylococcus aureus in various population groups from a rural and semi-urban area in Gabon, Central Africa. Acta Trop. 2012;124:42–7. https://doi.org/10.1016/j.actatropica.2012.06.005. Ngoa UA, Schaumburg F, Adegnika AA, Kösters K, Möller T, Fernandes JF, Alabi A, Issifou S, Becker K, Grobusch MP, Kremsner PG, Lell B. Epidemiology and population structure of Staphylococcus aureus in various population groups from a rural and semi-urban area in Gabon, Central Africa. Acta Trop. 2012;124:42–7. https://​doi.​org/​10.​1016/​j.​actatropica.​2012.​06.​005.
76.
go back to reference Clinical and Laboratory Standard Institute (CLSI). Performance standards for antimicrobial susceptibility testing: 27th edition. CLSI supplement M100. Wayne CLSI. 2017. Clinical and Laboratory Standard Institute (CLSI). Performance standards for antimicrobial susceptibility testing: 27th edition. CLSI supplement M100. Wayne CLSI. 2017.
77.
go back to reference The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 8.1, 2018. http://www.eucast.org. Accessed 28th May, 2018. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 8.1, 2018. http://​www.​eucast.​org. Accessed 28th May, 2018.
79.
go back to reference Hurdle JG, O’Neill AJ, Mody L, Chopra I, Bradley SF. In vivo transfer of high-level mupirocin resistance from Staphylococcus epidermidis to methicillin-resistant Staphylococcus aureus associated with failure of mupirocin prophylaxis. J Antimicrob Chemother. 2005;56:1166–8.PubMed Hurdle JG, O’Neill AJ, Mody L, Chopra I, Bradley SF. In vivo transfer of high-level mupirocin resistance from Staphylococcus epidermidis to methicillin-resistant Staphylococcus aureus associated with failure of mupirocin prophylaxis. J Antimicrob Chemother. 2005;56:1166–8.PubMed
Metadata
Title
Mupirocin-resistant Staphylococcus aureus in Africa: a systematic review and meta-analysis
Authors
Adebayo O. Shittu
Mamadou Kaba
Shima M. Abdulgader
Yewande O. Ajao
Mujibat O. Abiola
Ayodele O. Olatimehin
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2018
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-018-0382-5

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