Top

European Journal of Clinical Microbiology & Infectious Diseases

Published in:

01-04-2018 | Original Article

Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: molecular characterisation by microarray technology

Authors: Bushra Jamil, Darius Gawlik, Muhammad Ali Syed, Asim Ali Shah, Shahid Ahmad Abbasi, Elke Müller, Annett Reißig, Ralf Ehricht, Stefan Monecke

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 4/2018

Abstract

The prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in Pakistan is known to be high, but very few studies have described the molecular epidemiology of the different MRSA clones circulating in the country. Forty-four MRSA isolates were collected from two tertiary care hospitals of the Rawalpindi district of Pakistan. All strains were identified by a conventional phenotypic method and then subjected to genotyping by microarray hybridisation. Six clonal complexes (CCs) and 19 strains were identified. The most commonly identified strains were: (i) Panton–Valentine leucocidin (PVL)-positive CC772-MRSA-V, “Bengal Bay Clone” (ten isolates; 22.3%), (ii) ST239-MRSA [III + ccrC] (five isolates) and (iii) a CC8-MRSA-IV strain, as well as CC6-MRSA-IV (both with four isolates; 9.1% each). Several of the strains detected indicated epidemiological links to the Middle Eastern/Arabian Gulf region. Further studies are needed to type MRSA from countries with less known epidemiology and to monitor the distribution and spread of strains, as well as possible links to global travel, migration and commerce.

Available only for authorised users

Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C, Hiramatsu K (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45(5):1323–1336CrossRefPubMedPubMedCentral

Ito T, Ma XX, Takeuchi F, Okuma K, Yuzawa H, Hiramatsu K (2004) Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48(7):2637–2651CrossRefPubMedPubMedCentral

International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53(12):4961–4967CrossRef

Shore AC, Coleman DC (2013) Staphylococcal cassette chromosome mec: recent advances and new insights. Int J Med Microbiol 303(6–7):350-359. https://doi.org/10.1016/j.ijmm.2013.02.002 CrossRefPubMed

Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE (2007) The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 13(3):222–235CrossRefPubMed

Jevons MP (1961) “Celbenin”-resistant staphylococci. Br Med J 1(5219):924–925CrossRef

Pantosti A, Venditti M (2009) What is MRSA? Eur Respir J 34(5):1190–1196. https://doi.org/10.1183/09031936.00007709 CrossRefPubMed

Chambers HF, DeLeo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7:629–641CrossRefPubMedPubMedCentral

Coombs GW, Nimmo GR, Bell JM, Huygens F, O’Brien FG, Malkowski MJ, Pearson JC, Stephens AJ, Giffard PM; Australian Group for Antimicrobial Resistance (2004) Genetic diversity among community methicillin-resistant Staphylococcus aureus strains causing outpatient infections in Australia. J Clin Microbiol 42(10):4735–4743CrossRefPubMedPubMedCentral

10.

Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38(3):1008–1015PubMedPubMedCentral

11.

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(4):e17936CrossRefPubMedPubMedCentral

12.

Chua K, Laurent F, Coombs G, Grayson ML, Howden BP (2011) Antimicrobial resistance: Not community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA)! A clinician’s guide to community MRSA—its evolving antimicrobial resistance and implications for therapy. Clin Infect Dis 52(1):99–114. https://doi.org/10.1093/cid/ciq067 CrossRefPubMed

13.

Otter JA, French GL (2008) The emergence of community-associated methicillin-resistant Staphylococcus aureus at a London teaching hospital, 2000–2006. Clin Microbiol Infect 14(7):670–676CrossRefPubMed

14.

Miller LG, Perdreau-Remington F, Bayer AS, Diep B, Tan N, Bharadwa K, Tsui J, Perlroth J, Shay A, Tagudar G, Ibebuogu U, Spellberg B (2007) Clinical and epidemiologic characteristics cannot distinguish community-associated methicillin-resistant Staphylococcus aureus infection from methicillin-susceptible S. aureus infection: a prospective investigation. Clin Infect Dis 44(4):471–482CrossRefPubMed

15.

Monecke S, Jatzwauk L, Müller E, Nitschke H, Pfohl K, Slickers P, Reissig A, Ruppelt-Lorz A, Ehricht R (2016) Diversity of SCCmec elements in Staphylococcus aureus as observed in south-eastern Germany. PLoS One 11(9):e0162654. https://doi.org/10.1371/journal.pone.0162654 CrossRefPubMedPubMedCentral

16.

Akhter R, Khan K, Hasan F (2009) Isolation and antimicrobial susceptibility pattern of methicillin-resistant and methicillin sensitive Staphylococcus aureus. J Surg Pak 14(4):161–164

17.

Ajmal AN, Mir F, Aslam M, Hafeez R (2009) Nosocomial methicillin resistant Staphylococcus aureus frequency in a tertiary care hospital, Lahore, Pakistan. Biomedica 25(2):97–100

18.

Butt T, Ahmad RN, Usman M, Mahmood A (2004) Methicillin-resistant Staphylococcus aureus, Pakistan, 1996–2003. Emerg Infect Dis 10(9):1691–1692. https://doi.org/10.3201/eid1009.030844 CrossRefPubMedPubMedCentral

19.

Hafiz S, Hafiz AN, Ali L, Chughtai AS, Memon B, Ahmed A, Hussain S, Sarwar G, Mughal T, Siddiqui SJ, Awan A, Zaki K, Fareed A (2002) Methicillin resistant Staphylococcus aureus: a multicentre study. J Pak Med Assoc 52(7):312–315PubMed

20.

Perwaiz S, Barakzi Q, Farooqi BJ, Khursheed N, Sabir N (2007) Antimicrobial susceptibility pattern of clinical isolates of methicillin resistant Staphylococcus aureus. J Pak Med Assoc 57(1):2–4PubMed

21.

Hussain S, Shams R, Ahmad K, Perveen R, Riaz B (2005) Prevalence of methicillin resistant Staphylococcus aureus (MRSA) in surgical site infections in a tertiary care hospital. J Pathol 3(2):81–85

22.

Shabir S, Hardy KJ, Abbasi WS, McMurray CL, Malik SA, Wattal C, Hawkey PM (2010) Epidemiological typing of meticillin-resistant Staphylococcus aureus isolates from Pakistan and India. J Med Microbiol 59(Pt 3):330–337. https://doi.org/10.1099/jmm.0.014910-0 CrossRefPubMed

23.

Zafar A, Stone M, Ibrahim S, Parveen Z, Hasan Z, Khan E, Hasan R, Wain J, Bamford K (2011) Prevalent genotypes of meticillin-resistant Staphylococcus aureus: report from Pakistan. J Med Microbiol 60(Pt 1):56–62. https://doi.org/10.1099/jmm.0.022707-0 CrossRefPubMed

24.

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(9):1541–1547. https://doi.org/10.1007/s10096-016-2695-8 CrossRefPubMed

25.

Afroz S, Kobayashi N, Nagashima S, Alam MM, Hossain AB, Rahman MA, Islam MR, Lutfor AB, Muazzam N, Khan MA, Paul SK, Shamsuzzaman AK, Mahmud MC, Musa AK, Hossain MA (2008) Genetic characterization of Staphylococcus aureus isolates carrying Panton–Valentine leukocidin genes in Bangladesh. Jpn J Infect Dis 61(5):393–396PubMed

26.

Blomfeldt A, Larssen KW, Moghen A, Gabrielsen C, Elstrøm P, Aamot HV, Jørgensen SB (2017) Emerging multidrug-resistant Bengal Bay clone ST772-MRSA-V in Norway: molecular epidemiology 2004–2014. Eur J Clin Microbiol Infect Dis 36(10):1911–1921. https://doi.org/10.1007/s10096-017-3014-8 CrossRefPubMed

27.

Brennan GI, Shore AC, Corcoran S, Tecklenborg S, Coleman DC, O’Connell B (2012) Emergence of hospital- and community-associated Panton–Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus genotype ST772-MRSA-V in Ireland and detailed investigation of an ST772-MRSA-V cluster in a neonatal intensive care unit. J Clin Microbiol 50(3):841–847. https://doi.org/10.1128/jcm.06354-11 CrossRefPubMedPubMedCentral

28.

Ellington MJ, Ganner M, Warner M, Cookson BD, Kearns AM (2010) Polyclonal multiply antibiotic-resistant methicillin-resistant Staphylococcus aureus with Panton–Valentine leucocidin in England. J Antimicrob Chemother 65(1):46–50CrossRefPubMed

29.

Mediavilla JR, Chen L, Mathema B, Kreiswirth BN (2012) Global epidemiology of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA). Curr Opin Microbiol 15(5):588–595. https://doi.org/10.1016/j.mib.2012.08.003 CrossRefPubMed

30.

Monecke S, Baier V, Coombs GW, Slickers P, Ziegler A, Ehricht R (2013) Genome sequencing and molecular characterisation of Staphylococcus aureus ST772-MRSA-V, “Bengal Bay Clone”. BMC Res Notes 6(1):548. https://doi.org/10.1186/1756-0500-6-548 CrossRefPubMedPubMedCentral

31.

Prabhakara S, Khedkar S, Shambat SM, Srinivasan R, Basu A, Norrby-Teglund A, Seshasayee ASN, Arakere G (2013) Genome sequencing unveils a novel sea enterotoxin-carrying PVL phage in Staphylococcus aureus ST772 from India. PLoS One 8(3):e60013. https://doi.org/10.1371/journal.pone.0060013 CrossRefPubMedPubMedCentral

32.

Sanchini A, Campanile F, Monaco M, Cafiso V, Rasigade JP, Laurent F, Etienne J, Stefani S, Pantosti A (2011) DNA microarray-based characterisation of Panton–Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus from Italy. Eur J Clin Microbiol Infect Dis 30(11):1399–1408. https://doi.org/10.1007/s10096-011-1234-x CrossRefPubMed

33.

Shore AC, Tecklenborg SC, Brennan GI, Ehricht R, Monecke S, Coleman DC (2014) Panton–Valentine leukocidin-positive Staphylococcus aureus in Ireland from 2002 to 2011: 21 clones, frequent importation of clones, temporal shifts of predominant methicillin-resistant S. aureus clones, and increasing multiresistance. J Clin Microbiol 52(3):859–870. https://doi.org/10.1128/JCM.02799-13 CrossRefPubMedPubMedCentral

34.

Udo EE, Al-Lawati BAH, Al-Muharmi Z, Thukral SS (2014) Genotyping of methicillin-resistant Staphylococcus aureus in the Sultan Qaboos University Hospital, Oman reveals the dominance of Panton–Valentine leucocidin-negative ST6-IV/t304 clone. New Microbes New Infect 2(4):100–105. https://doi.org/10.1002/nmi2.47 CrossRefPubMedPubMedCentral

35.

Williamson DA, Roberts SA, Ritchie SR, Coombs GW, Fraser JD, Heffernan H (2013) Clinical and molecular epidemiology of methicillin-resistant Staphylococcus aureus in New Zealand: rapid emergence of sequence type 5 (ST5)-SCCmec-IV as the dominant community-associated MRSA clone. PLoS One 8(4):e62020. https://doi.org/10.1371/journal.pone.0062020 CrossRefPubMedPubMedCentral

36.

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 53:237–251CrossRefPubMed

37.

Scicluna EA, Shore AC, Thürmer A, Ehricht R, Slickers P, Borg MA, Coleman DC, Monecke S (2010) Characterisation of MRSA from Malta and the description of a Maltese epidemic MRSA strain. Eur J Clin Microbiol Infect Dis 29(2):163–170CrossRefPubMed

38.

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(1):146CrossRefPubMedPubMedCentral

39.

Coombs G, Pearson J, Daley D, Robinson O, Nimmo G, Turnidge JD (2013) Staphylococcus aureus Programme 2012 (SAP 2012) community survey. MRSA epidemiology and typing report. Australian Group on Antimicrobial Resistance (AGAR), Australia

40.

Holden MTG, Hsu L-Y, Kurt K, Weinert LA, Mather AE, Harris SR, Strommenger B, Layer F, Witte W, de Lencastre H, Skov R, Westh H, Žemličková H, Coombs G, Kearns AM, Hill RLR, Edgeworth J, Gould I, Gant V, Cooke J, Edwards GF, McAdam PR, Templeton KE, McCann A, Zhou Z, Castillo-Ramírez S, Feil EJ, Hudson LO, Enright MC, Balloux F, Aanensen DM, Spratt BG, Fitzgerald JR, Parkhill J, Achtman M, Bentley SD, Nübel U (2013) A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res 23(4):653–664. https://doi.org/10.1101/gr.147710.112 CrossRefPubMedPubMedCentral

41.

Robinson DA, Enright MC (2004) Evolution of Staphylococcus aureus by large chromosomal replacements. J Bacteriol 186(4):1060–1064CrossRefPubMedPubMedCentral

42.

Biber A, Abuelaish I, Rahav G, Raz M, Cohen L, Valinsky L, Taran D, Goral A, Elhamdany A, Regev-Yochay G; PICR Study Group (2012) A typical hospital-acquired methicillin-resistant Staphylococcus aureus clone is widespread in the community in the Gaza strip. PLoS One 7(8):e42864. https://doi.org/10.1371/journal.pone.0042864 CrossRefPubMedPubMedCentral

43.

Al Laham N, Mediavilla JR, Chen L, Abdelateef N, Elamreen FA, Ginocchio CC, Pierard D, Becker K, Kreiswirth BN (2015) MRSA clonal complex 22 strains harboring toxic shock syndrome toxin (TSST-1) are endemic in the primary Hospital in Gaza, Palestine. PLoS One 10(3):e0120008. https://doi.org/10.1371/journal.pone.0120008 CrossRefPubMedPubMedCentral

44.

Udo EE, Boswihi SS, Al-Sweih N (2016) High prevalence of toxic shock syndrome toxin-producing epidemic methicillin-resistant Staphylococcus aureus 15 (EMRSA-15) strains in Kuwait hospitals. New Microbes New Infect 12:24–30. https://doi.org/10.1016/j.nmni.2016.03.008 CrossRefPubMedPubMedCentral

45.

Senok A, Somily A, Raji A, Gawlik D, Al-Shahrani F, Baqi S, Boswihi S, Skakni L, Udo EE, Weber S, Ehricht R, Monecke S (2016) Diversity of methicillin-resistant Staphylococcus aureus CC22-MRSA-IV from Saudi Arabia and the Gulf region. Int J Infect Dis 51:31–35CrossRefPubMed

46.

Monecke S, Aamot HV, Stieber B, Ruppelt A, Ehricht R (2014) Characterization of PVL-positive MRSA from Norway. APMIS 122(7):580–584. https://doi.org/10.1111/apm.12181 CrossRefPubMed

47.

Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, Chantratita N, Gardete S, Tavares A, Day N, Lindsay JA, Edgeworth JD, de Lencastre H, Parkhill J, Peacock SJ, Bentley SD (2010) Evolution of MRSA during hospital transmission and intercontinental spread. Science 327(5964):469–474CrossRefPubMedPubMedCentral

48.

Chen H, Yang X, Wang Q, Zhao C, Li H, He W, Wang X, Zhang F, Wang Z, Chen M, Zhu B, Wang H (2014) Insights on evolution of virulence and resistance from the whole-genome analysis of a predominant methicillin-resistant Staphylococcus aureus clone sequence type 239 in China. Chin Sci Bull 59(11):1104–1112. https://doi.org/10.1007/s11434-014-0149-1 CrossRef

49.

Yamamoto T, Takano T, Higuchi W, Iwao Y, Singur O, Reva I, Otsuka Y, Nakayashiki T, Mori H, Reva G, Kuznetsov V, Potapov V (2012) Comparative genomics and drug resistance of a geographic variant of ST239 methicillin-resistant Staphylococcus aureus emerged in Russia. PLoS One 7(1):e29187. https://doi.org/10.1371/journal.pone.0029187 CrossRefPubMedPubMedCentral

50.

Weber S, Ehricht R, Slickers P, Abdel-Wareth L, Donnelly G, Pitout M, Monecke S (2010) Genetic fingerprinting of MRSA from Abu Dhabi. In: Proceedings of the 20th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID), Vienna, Austria, April 2010

51.

Witte W, Enright M, Schmitz FJ, Cuny C, Braulke C, Heuck D (2001) Characteristics of a new epidemic MRSA in Germany ancestral to United Kingdom EMRSA 15. Int J Med Microbiol 290(8):677–682CrossRefPubMed

Title: Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: molecular characterisation by microarray technology
Authors: Bushra Jamil
Darius Gawlik
Muhammad Ali Syed
Asim Ali Shah
Shahid Ahmad Abbasi
Elke Müller
Annett Reißig
Ralf Ehricht
Stefan Monecke
Publication date: 01-04-2018
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Clinical Microbiology & Infectious Diseases / Issue 4/2018
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI: https://doi.org/10.1007/s10096-017-3161-y

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: molecular characterisation by microarray technology

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

Prosthetic valve endocarditis caused by Propionibacterium species: a national registry-based study of 51 Swedish cases

Evaluation of the Copan Myco-TB kit for the decontamination of respiratory samples for the detection of Mycobacteria

Long-lasting cough in an adult German population: incidence, symptoms, and related pathogens

Evaluation of the use of sonication of retrieved implants for the diagnosis of prosthetic joint infection in a routine setting

Gut microbiome production of short-chain fatty acids and obesity in children

The rapid diagnosis of viral respiratory tract infections and its impact on antimicrobial stewardship programs

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page