Antibiotic resistance profile and molecular characterization of Staphylococcus aureus strains isolated in hospitals in Kabul, Afghanistan.


Journal

European journal of clinical microbiology & infectious diseases : official publication of the European Society of Clinical Microbiology
ISSN: 1435-4373
Titre abrégé: Eur J Clin Microbiol Infect Dis
Pays: Germany
ID NLM: 8804297

Informations de publication

Date de publication:
May 2021
Historique:
received: 03 08 2020
accepted: 14 12 2020
pubmed: 4 1 2021
medline: 21 8 2021
entrez: 3 1 2021
Statut: ppublish

Résumé

The aim of this study was to investigate the molecular features and the antibiotic resistance profile of 98 clinical Staphylococcus aureus isolates collected during 6 months in two hospitals of Kabul, Afghanistan. For all isolates, antimicrobial resistance patterns were determined by the disc diffusion method (including methicillin resistance which was detected using cefoxitin). The presence of the mecA/mecC genes was detected by PCR. Strains were then extensively characterized using microarray analysis. Of the 98 S. aureus isolates, methicillin-resistant S. aureus (MRSA) prevalence was high at 66.3%. Antibiotic susceptibility testing also revealed a high resistance rate to penicillin (100%), erythromycin (66.3%), ciprofloxacin (55.1%), and cotrimoxazole (40.8%). Resistance to tobramycin was detected in 25.5%, to gentamicin in 16.3%, to chloramphenicol in 34.7%, and to doxycycline in 23.5% of the isolates. All the MRSA isolates were mecA-positive and none of them harbored mecC. Isolates were grouped into twelve clonal complexes and twenty-seven distinct clones. The most frequently detected clones were the Southwest Pacific clone (CC30-MRSA-IV PVL+) (21/65 MRSA, 32.3%), the CC22-MRSA-IV TSST-1+ clone (11/65 MRSA, 16.9%), and the Bengal Bay clone (ST772-MRSA-V PVL+) (11/65 MRSA, 16.9%). The PVL genes were found in 59.2% (46/65 MRSA and 12/33 methicillin-susceptible S. aureus, MSSA) and tst1 gene in 16.3% of isolates. This molecular study highlights the high prevalence of MRSA and the large genetic diversity of the S. aureus isolates circulating and detected in two hospitals of Kabul, with the presence of multiple virulence and antibiotic resistance genes.

Identifiants

pubmed: 33389264
doi: 10.1007/s10096-020-04130-0
pii: 10.1007/s10096-020-04130-0
doi:

Substances chimiques

Anti-Bacterial Agents 0
Virulence Factors 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1029-1038

Références

Rasigade J-P, Vandenesch F (2014) Staphylococcus aureus: a pathogen with still unresolved issues. Infect Genet Evol 21:510–514. https://doi.org/10.1016/j.meegid.2013.08.018
doi: 10.1016/j.meegid.2013.08.018 pubmed: 23994773
Zhang S, Sun X, Chang W, Dai Y, Ma X (2015) Systematic review and meta-analysis of the epidemiology of vancomycin-intermediate and heterogeneous vancomycin-intermediate Staphylococcus aureus isolates. PLoS One 10:e0136082. https://doi.org/10.1371/journal.pone.0136082
doi: 10.1371/journal.pone.0136082 pubmed: 26287490 pmcid: 4546009
Cong Y, Yang S, Rao X (2020) Vancomycin resistant Staphylococcus aureus infections: a review of case updating and clinical features. J Adv Res 21:169–176. https://doi.org/10.1016/j.jare.2019.10.005
doi: 10.1016/j.jare.2019.10.005 pubmed: 32071785
Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, Chow H, Ip M, Jatzwauk L, Jonas D, Kadlec K, Kearns A, Laurent F, O’Brien FG, Pearson J, Ruppelt A, Schwarz S, Scicluna E, Slickers P, Tan H-L, Weber S, Ehricht R (2011) A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One 6:e17936. https://doi.org/10.1371/journal.pone.0017936
doi: 10.1371/journal.pone.0017936 pubmed: 21494333 pmcid: 3071808
Calfee DP (2017) Trends in community versus health care-acquired methicillin-resistant Staphylococcus aureus infections. Curr Infect Dis Rep 19:48. https://doi.org/10.1007/s11908-017-0605-6
doi: 10.1007/s11908-017-0605-6 pubmed: 29101576
Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29:1128–1132. https://doi.org/10.1086/313461
doi: 10.1086/313461 pubmed: 10524952
Chen C-J, Huang Y-C (2014) New epidemiology of Staphylococcus aureus infection in Asia. Clin Microbiol Infect 20:605–623. https://doi.org/10.1111/1469-0691.12705
doi: 10.1111/1469-0691.12705 pubmed: 24888414
Bukhari SZ, Ahmed S, Zia N (2011) Antimicrobial susceptibility pattern of Staphylococcus aureus on clinical isolates and efficacy of laboratory tests to diagnose MRSA: a multi-centre study. J Ayub Med Coll Abbottabad 23:139–142
pubmed: 22830169
Indian Network for Surveillance of Antimicrobial Resistance (INSAR) group, India (2013) Methicillin resistant Staphylococcus aureus (MRSA) in India: prevalence & susceptibility pattern. Indian J Med Res 137:363–369
Mendes RE, Mendoza M, Banga Singh KK, Castanheira M, Bell JM, Turnidge JD, Lin SSF, Jones RN (2013) Regional resistance surveillance program results for 12 Asia-Pacific nations (2011). Antimicrob Agents Chemother 57:5721–5726. https://doi.org/10.1128/AAC.01121-13
doi: 10.1128/AAC.01121-13 pubmed: 23959306 pmcid: 3811293
Dadashi M, Nasiri MJ, Fallah F, Owlia P, Hajikhani B, Emaneini M, Mirpour M (2018) Methicillin-resistant Staphylococcus aureus (MRSA) in Iran: a systematic review and meta-analysis. J Glob Antimicrob Resist 12:96–103. https://doi.org/10.1016/j.jgar.2017.09.006
doi: 10.1016/j.jgar.2017.09.006 pubmed: 28941791
Shekarabi M, Hajikhani B, Salimi Chirani A, Fazeli M, Goudarzi M (2017) Molecular characterization of vancomycin-resistant Staphylococcus aureus strains isolated from clinical samples: a three year study in Tehran, Iran. PLoS One 12:e0183607. https://doi.org/10.1371/journal.pone.0183607
doi: 10.1371/journal.pone.0183607 pubmed: 28854219 pmcid: 5576738
Naimi HM, Rasekh H, Noori AZ, Bahaduri MA (2017) Determination of antimicrobial susceptibility patterns in Staphylococcus aureus strains recovered from patients at two main health facilities in Kabul, Afghanistan. BMC Infect Dis 17:737. https://doi.org/10.1186/s12879-017-2844-4
doi: 10.1186/s12879-017-2844-4 pubmed: 29187146 pmcid: 5707873
Green T, Zafar O, Zahir S, Jumahir A, Aisha N Afghanistan Medicine Use Study: a survey of 28 health facilities in 5 provinces | Management Sciences for Health. msh.org/resources/afghanistan-medicine-use-study-a-survey-of-28-health-facilities-in-5-provinces . Accessed 15 Jul 2020
Bajis S, Van den Bergh R, De Bruycker M, Mahama G, Van Overloop C, Satyanarayana S, Bernardo RS, Esmati S, Reid AJ (2014) Antibiotic use in a district hospital in Kabul, Afghanistan: are we overprescribing? Public Health Action 4:259–264. https://doi.org/10.5588/pha.14.0068
doi: 10.5588/pha.14.0068 pubmed: 26400706 pmcid: 4533508
Société Française de Microbiologie (2017) Comité de l’Antibiogramme de la Société Française de Microbiologie CASFM / EUCAST
Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S (1991) Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 29:2240–2244
doi: 10.1128/JCM.29.10.2240-2244.1991
Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G, Laurent F, Teale C, Skov R, Larsen AR (2012) Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA(LGA251). Clin Microbiol Infect 18:395–400. https://doi.org/10.1111/j.1469-0691.2011.03715.x
doi: 10.1111/j.1469-0691.2011.03715.x pubmed: 22429460
Lina G, Boutite F, Tristan A, Bes M, Etienne J, Vandenesch F (2003) Bacterial competition for human nasal cavity colonization: role of Staphylococcal agr alleles. Appl Environ Microbiol 69:18–23. https://doi.org/10.1128/aem.69.1.18-23.2003
doi: 10.1128/aem.69.1.18-23.2003 pubmed: 152380 pmcid: 152380
Monecke S, Slickers P, Ehricht R (2008) Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol 53:237–251. https://doi.org/10.1111/j.1574-695X.2008.00426.x
doi: 10.1111/j.1574-695X.2008.00426.x pubmed: 18507678
Ullah A, Qasim M, Rahman H, Khan J, Haroon M, Muhammad N, Khan A, Muhammad N (2016) High frequency of methicillin-resistant Staphylococcus aureus in Peshawar Region of Pakistan. SpringerPlus 5:600. https://doi.org/10.1186/s40064-016-2277-3
doi: 10.1186/s40064-016-2277-3 pubmed: 27247896 pmcid: 4864768
Ghasemian A, Mirzaee M (2016) Methicillin-resistant Staphylococcus aureus (MRSA) strains and the staphylococcal cassette chromosome mec types in Iran. Infect Epidemiol Med 2:31–34 https://iem.modares.ac.ir/article-4-10977-en.pdf
doi: 10.18869/modares.iem.2.3.31
Baddour MM, Abuelkheir MM, Fatani AJ (2006) Trends in antibiotic susceptibility patterns and epidemiology of MRSA isolates from several hospitals in Riyadh, Saudi Arabia. Ann Clin Microbiol Antimicrob 5:30. https://doi.org/10.1186/1476-0711-5-30
doi: 10.1186/1476-0711-5-30 pubmed: 17140452 pmcid: 1713249
Eksi F, Gayyurhan ED, Bayram A, Karsligil T (2011) Determination of antimicrobial susceptibility patterns and inducible clindamycin resistance in Staphylococcus aureus strains recovered from southeastern Turkey. J Microbiol Immunol Infect 44:57–62. https://doi.org/10.1016/j.jmii.2011.01.011
doi: 10.1016/j.jmii.2011.01.011 pubmed: 21531354
Senok A, Ehricht R, Monecke S, Al-Saedan R, Somily A (2016) Molecular characterization of methicillin-resistant Staphylococcus aureus in nosocomial infections in a tertiary-care facility: emergence of new clonal complexes in Saudi Arabia. New Microbes New Infect 14:13–18. https://doi.org/10.1016/j.nmni.2016.07.009
doi: 10.1016/j.nmni.2016.07.009 pubmed: 27621823 pmcid: 5009225
Monecke S, Skakni L, Hasan R, Ruppelt A, Ghazal SS, Hakawi A, Slickers P, Ehricht R (2012) Characterisation of MRSA strains isolated from patients in a hospital in Riyadh, Kingdom of Saudi Arabia. BMC Microbiol 12:146. https://doi.org/10.1186/1471-2180-12-146
doi: 10.1186/1471-2180-12-146 pubmed: 22823982 pmcid: 3464608
Goudarzi M, Bahramian M, Satarzadeh Tabrizi M, Udo EE, Figueiredo AMS, Fazeli M, Goudarzi H (2017) Genetic diversity of methicillin resistant Staphylococcus aureus strains isolated from burn patients in Iran: ST239-SCCmec III/t037 emerges as the major clone. Microb Pathog 105:1–7. https://doi.org/10.1016/j.micpath.2017.02.004
doi: 10.1016/j.micpath.2017.02.004 pubmed: 28179118
Enany S, Higuchi W, Okubo T, Takano T, Enany M, Yamamoto T (2007) Brain abscess caused by Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus in Egypt, April 2007. Euro Surveill 12:E070927.2. https://doi.org/10.2807/esw.12.39.03274-en
doi: 10.2807/esw.12.39.03274-en pubmed: 17991379
Afroz S, Kobayashi N, Nagashima S, Alam MM, Hossain ABMB, Rahman MA, Islam MR, Lutfor AB, Muazzam N, Khan MAH, Paul SK, Shamsuzzaman AKM, Mahmud MC, Musa AKM, Hossain MA (2008) Genetic characterization of Staphylococcus aureus isolates carrying Panton-Valentine leukocidin genes in Bangladesh. Jpn J Infect Dis 61:393–396
pubmed: 18806351
D’Souza N, Rodrigues C, Mehta A (2010) Molecular characterization of methicillin-resistant Staphylococcus aureus with emergence of epidemic clones of sequence type (ST) 22 and ST 772 in Mumbai, India. J Clin Microbiol 48:1806–1811. https://doi.org/10.1128/JCM.01867-09
doi: 10.1128/JCM.01867-09 pubmed: 20351212 pmcid: 2863868
Jamil B, Gawlik D, Syed MA, Shah AA, Abbasi SA, Müller E, Reißig A, Ehricht R, Monecke S (2018) Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: molecular characterisation by microarray technology. Eur J Clin Microbiol Infect Dis 37:691–700. https://doi.org/10.1007/s10096-017-3161-y
doi: 10.1007/s10096-017-3161-y pubmed: 29238933
Madzgalla S, Syed MA, Khan MA, Rehman SS, Müller E, Reissig A, Ehricht R, Monecke S (2016) Molecular characterization of Staphylococcus aureus isolates causing skin and soft tissue infections in patients from Malakand, Pakistan. Eur J Clin Microbiol Infect Dis 35:1541–1547. https://doi.org/10.1007/s10096-016-2695-8
doi: 10.1007/s10096-016-2695-8 pubmed: 27262852
Pokhrel RH, Aung MS, Thapa B, Chaudhary R, Mishra SK, Kawaguchiya M, Urushibara N, Kobayashi N (2016) Detection of ST772 Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus (Bengal Bay clone) and ST22 S. aureus isolates with a genetic variant of elastin binding protein in Nepal. New Microbes New Infect 11:20–27. https://doi.org/10.1016/j.nmni.2016.02.001
doi: 10.1016/j.nmni.2016.02.001 pubmed: 27014464 pmcid: 4789347
Centers for Disease Control and Prevention (1999) Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus - Minnesota and North Dakota, 1997-1999. JAMA 282:1123–1125
Bouchiat C, Curtis S, Spiliopoulou I, Bes M, Cocuzza C, Codita I, Dupieux C, Giormezis N, Kearns A, Laurent F, Molinos S, Musumeci R, Prat C, Saadatian-Elahi M, Tacconelli E, Tristan A, Schulte B, Vandenesch F, ESCMID Study Group on Staphylococci and Staphylococcal Infections (ESGS) (2017) MRSA infections among patients in the emergency department: a European multicentre study. J Antimicrob Chemother 72:372–375. https://doi.org/10.1093/jac/dkw431
doi: 10.1093/jac/dkw431 pubmed: 27798212
Frisch MB, Castillo-Ramírez S, Petit RA, Farley MM, Ray SM, Albrecht VS, Limbago BM, Hernandez J, See I, Satola SW, Read TD (2018) Invasive methicillin-resistant Staphylococcus aureus USA500 strains from the U.S. Emerging Infections Program constitute three geographically distinct lineages. mSphere 3(3):e00571–e00517. https://doi.org/10.1128/mSphere.00571-17
doi: 10.1128/mSphere.00571-17 pubmed: 29720528 pmcid: 5932375
Albrecht N, Jatzwauk L, Slickers P, Ehricht R, Monecke S (2011) Clonal replacement of epidemic methicillin-resistant Staphylococcus aureus strains in a German university hospital over a period of eleven years. PLoS One 6:e28189. https://doi.org/10.1371/journal.pone.0028189
doi: 10.1371/journal.pone.0028189 pubmed: 22140542 pmcid: 3227659
Monecke S, Slickers P, Gawlik D, Müller E, Reissig A, Ruppelt-Lorz A, Akpaka PE, Bandt D, Bes M, Boswihi SS, Coleman DC, Coombs GW, Dorneanu OS, Gostev VV, Ip M, Jamil B, Jatzwauk L, Narvaez M, Roberts R, Senok A, Shore AC, Sidorenko SV, Skakni L, Somily AM, Syed MA, Thürmer A, Udo EE, Vremerǎ T, Zurita J, Ehricht R (2018) Molecular typing of ST239-MRSA-III from diverse geographic locations and the evolution of the SCCmec III element during its intercontinental spread. Front Microbiol 9:1436. https://doi.org/10.3389/fmicb.2018.01436
doi: 10.3389/fmicb.2018.01436 pubmed: 30087657 pmcid: 6066798
Oksuz L, Dupieux C, Tristan A, Bes M, Etienne J, Gurler N (2013) The high diversity of MRSA clones detected in a university hospital in Istanbul. Int J Med Sci 10:1740–1745. https://doi.org/10.7150/ijms.6438
doi: 10.7150/ijms.6438 pubmed: 24151444 pmcid: 3804798
Shahini Shams Abadi M, Nikokar I, Hoseini Alfatemi SM, Malekzadegan Y, Azizi A, Sedigh Ebrahim-Saraie H (2017) Epidemiology of Panton-Valentine leukocidin harbouring Staphylococcus aureus in cutaneous infections from Iran: a systematic review and meta-analysis. Infez Med 25:217–223
pubmed: 28956538
Karmakar A, Jana D, Dutta K, Dua P, Ghosh C (2018) Prevalence of Panton-Valentine leukocidin gene among community acquired Staphylococcus aureus: a real-time PCR study. J Pathog 2018:4518541. https://doi.org/10.1155/2018/4518541
doi: 10.1155/2018/4518541 pubmed: 30245888 pmcid: 6139182

Auteurs

Haji Mohammad Naimi (HM)

Department of Microbiology, Faculty of Pharmacy, Kabul University, Kabul, Afghanistan.
CIRI - Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard Lyon 1, CNRS UMR5308, ENS de Lyon, Lyon, France.

Camille André (C)

CIRI - Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard Lyon 1, CNRS UMR5308, ENS de Lyon, Lyon, France.
Laboratoire de Bactériologie, Institut des Agents Infectieux, Hôpital de la Croix-Rousse, 103 Grande Rue de la Croix-Rousse, 69004, Lyon, France.

Michèle Bes (M)

CIRI - Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard Lyon 1, CNRS UMR5308, ENS de Lyon, Lyon, France.
Centre National de Référence des Staphylocoques, Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France.
Laboratoire de Bactériologie, Institut des Agents Infectieux, Hôpital de la Croix-Rousse, 103 Grande Rue de la Croix-Rousse, 69004, Lyon, France.

Anne Tristan (A)

CIRI - Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard Lyon 1, CNRS UMR5308, ENS de Lyon, Lyon, France.
Centre National de Référence des Staphylocoques, Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France.
Laboratoire de Bactériologie, Institut des Agents Infectieux, Hôpital de la Croix-Rousse, 103 Grande Rue de la Croix-Rousse, 69004, Lyon, France.

Claude-Alexandre Gustave (CA)

CIRI - Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard Lyon 1, CNRS UMR5308, ENS de Lyon, Lyon, France.
Centre National de Référence des Staphylocoques, Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France.
Laboratoire de Bactériologie, Institut des Agents Infectieux, Hôpital de la Croix-Rousse, 103 Grande Rue de la Croix-Rousse, 69004, Lyon, France.

François Vandenesch (F)

CIRI - Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard Lyon 1, CNRS UMR5308, ENS de Lyon, Lyon, France.
Centre National de Référence des Staphylocoques, Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France.
Laboratoire de Bactériologie, Institut des Agents Infectieux, Hôpital de la Croix-Rousse, 103 Grande Rue de la Croix-Rousse, 69004, Lyon, France.

Qand Agha Nazari (QA)

Department of Microbiology, Faculty of Pharmacy, Kabul University, Kabul, Afghanistan.

Frédéric Laurent (F)

CIRI - Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard Lyon 1, CNRS UMR5308, ENS de Lyon, Lyon, France.
Centre National de Référence des Staphylocoques, Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France.
Laboratoire de Bactériologie, Institut des Agents Infectieux, Hôpital de la Croix-Rousse, 103 Grande Rue de la Croix-Rousse, 69004, Lyon, France.

Céline Dupieux (C)

CIRI - Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard Lyon 1, CNRS UMR5308, ENS de Lyon, Lyon, France. celine.dupieux-chabert@chu-lyon.fr.
Centre National de Référence des Staphylocoques, Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France. celine.dupieux-chabert@chu-lyon.fr.
Laboratoire de Bactériologie, Institut des Agents Infectieux, Hôpital de la Croix-Rousse, 103 Grande Rue de la Croix-Rousse, 69004, Lyon, France. celine.dupieux-chabert@chu-lyon.fr.

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