Skip to main content
Top
Published in: European Journal of Clinical Microbiology & Infectious Diseases 1/2020

01-01-2020 | Original Article

Genotyping of methicillin-resistant Staphylococcus aureus from sepsis patients in Pakistan and detection of antibodies against staphylococcal virulence factors

Authors: Stefan Monecke, Muhammad Ali Syed, Mushtaq Ahmad Khan, Shehzad Ahmed, Sadia Tabassum, Darius Gawlik, Elke Müller, Annett Reissig, Sascha D. Braun, Ralf Ehricht

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 1/2020

Login to get access

Abstract

In order to obtain more information on the MRSA population structure in the border region of Afghanistan and Pakistan, we collected and genotyped MRSA causing bloodstream infections from a tertiary care hospital in Peshawar, Pakistan, that serves the local population as well as Afghan immigrants and refugees. Thirty-one MRSA isolates from 30 patients were included and characterized by microarray hybridisation. For 25 patients, serum samples were tested using protein microarrays in order to detect antibodies against staphylococcal virulence factors. The most conspicuous result was the high rate of PVL-positive MRSA. Twenty-two isolates (71%) harboured lukF/S-PV genes. The most common lineage was CC772-MRSA-V/VT (PVL+) to which eleven isolates were assigned. The second most common strain was, surprisingly, CC8-MRSA-[IV+ACME] (PVL+), “USA300” (9 isolates). Two isolates were tst1 positive CC22-MRSA-IV, matching the Middle Eastern “Gaza Epidemic Strain”. Another two were PVL-positive CC30-MRSA-IV. The remaining isolates belonged to, possibly locally emerging, CC1, CC5, and CC8 strains with SCC mec IV elements. Twenty-three patient sera were positive for anti-PVL-IgG antibodies. Several questions arise from the present study. It can be assumed that MRSA and high rates of PVL-positive S. aureus/MRSA are a public health issue in the Afghanistan/Pakistan border region. A possible emergence of the “USA300” clone as well as of the CC772 lineage warrants further investigation.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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(1):737CrossRef 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(1):737CrossRef
2.
go back to reference Tariq TM (2014) Bacteriologic profile and antibiogram of blood culture isolates from a children's hospital in Kabul. J Coll Physicians Surg Pak 24(6):396–399PubMed Tariq TM (2014) Bacteriologic profile and antibiogram of blood culture isolates from a children's hospital in Kabul. J Coll Physicians Surg Pak 24(6):396–399PubMed
3.
go back to reference Aro T, Kantele A (2018) High rates of meticillin-resistant Staphylococcus aureus among asylum seekers and refugees admitted to Helsinki University hospital, 2010 to 2017. Euro Surveill 23(45) Aro T, Kantele A (2018) High rates of meticillin-resistant Staphylococcus aureus among asylum seekers and refugees admitted to Helsinki University hospital, 2010 to 2017. Euro Surveill 23(45)
4.
go back to reference Murray CK, Yun HC, Griffith ME, Thompson B, Crouch HK, Monson LS, Aldous WK, Mende K, Hospenthal DR (2009) Recovery of multidrug-resistant bacteria from combat personnel evacuated from Iraq and Afghanistan at a single military treatment facility. Mil Med 174(6):598–604CrossRef Murray CK, Yun HC, Griffith ME, Thompson B, Crouch HK, Monson LS, Aldous WK, Mende K, Hospenthal DR (2009) Recovery of multidrug-resistant bacteria from combat personnel evacuated from Iraq and Afghanistan at a single military treatment facility. Mil Med 174(6):598–604CrossRef
5.
go back to reference Vento TJ, Calvano TP, Cole DW, Mende K, Rini EA, Tully CC, Landrum ML, Zera W, Guymon CH, Yu X, Beckius ML, Cheatle KA, Murray CK (2013) Staphylococcus aureus colonization of healthy military service members in the United States and Afghanistan. BMC Infect Dis 13:325CrossRef Vento TJ, Calvano TP, Cole DW, Mende K, Rini EA, Tully CC, Landrum ML, Zera W, Guymon CH, Yu X, Beckius ML, Cheatle KA, Murray CK (2013) Staphylococcus aureus colonization of healthy military service members in the United States and Afghanistan. BMC Infect Dis 13:325CrossRef
6.
go back to reference Arfat Y (2013) Genotyping of methicillin resistant Staphylococcus aureus (MRSA) from local hospital of Rawalpindi/Islamabad, Pakistan. Local Hospital of Rawalpindi/Islamabad. Quaid-i-Azam University, Islamabad, Islamabad Arfat Y (2013) Genotyping of methicillin resistant Staphylococcus aureus (MRSA) from local hospital of Rawalpindi/Islamabad, Pakistan. Local Hospital of Rawalpindi/Islamabad. Quaid-i-Azam University, Islamabad, Islamabad
7.
go back to reference Jamil B, Gawlik D, Syed MA, Shah AA, Abbasi SA, Müller E, Reißig A, Ehricht R, Monecke S (2017) Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: molecular characterisation by microarray technology. Eur J Clin Microbiol Infect Dis Jamil B, Gawlik D, Syed MA, Shah AA, Abbasi SA, Müller E, Reißig A, Ehricht R, Monecke S (2017) Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: molecular characterisation by microarray technology. Eur J Clin Microbiol Infect Dis
8.
go back to reference Khan S, Sung K, Iram S, Nawaz M, Xu J, Marasa B (2016) Draft genome sequences of two methicillin-resistant clinical Staphylococcus aureus isolates. Genome Announc 4(1) Khan S, Sung K, Iram S, Nawaz M, Xu J, Marasa B (2016) Draft genome sequences of two methicillin-resistant clinical Staphylococcus aureus isolates. Genome Announc 4(1)
9.
go back to reference Madzgalla S, Syed MA, Khan MA, Rehman SS, Muller 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):1541–1547CrossRef Madzgalla S, Syed MA, Khan MA, Rehman SS, Muller 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):1541–1547CrossRef
10.
go back to reference Monecke S, Slickers P, Gawlik D, Müller E, Reissig A, Ruppelt-Lorz A, Akpaka P, Bandt D, Bes M, Boswihi S, Coleman D, Coombs G, Dorneanu O, Gostev V, Ip M, Jamil B, Jatzwauk L, Narvaez M, Roberts R, Senok A, Shore A, Sidorenko S, Skakni L, Somily A, Syed M, Thürmer A, Udo E, Vremeră 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) Monecke S, Slickers P, Gawlik D, Müller E, Reissig A, Ruppelt-Lorz A, Akpaka P, Bandt D, Bes M, Boswihi S, Coleman D, Coombs G, Dorneanu O, Gostev V, Ip M, Jamil B, Jatzwauk L, Narvaez M, Roberts R, Senok A, Shore A, Sidorenko S, Skakni L, Somily A, Syed M, Thürmer A, Udo E, Vremeră 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)
11.
go back to reference Naeem I, Naqvi BS, Hashmi K, Gauhar S (2006) Paediatric nosocomial infections: resistance pattern of clinical isolates. Pak J Pharm Sci 19(1):52–57PubMed Naeem I, Naqvi BS, Hashmi K, Gauhar S (2006) Paediatric nosocomial infections: resistance pattern of clinical isolates. Pak J Pharm Sci 19(1):52–57PubMed
12.
go back to reference 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):330–337CrossRef 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):330–337CrossRef
13.
go back to reference 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):56–62CrossRef 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):56–62CrossRef
14.
go back to reference Wiese L, Mejer N, Schønheyder HC, Westh H, Jensen AG, Larsen AR, Skov R, Benfield T (2013) A nationwide study of comorbidity and risk of reinfection after Staphylococcus aureus bacteraemia. J Infect 67(3):199–205CrossRef Wiese L, Mejer N, Schønheyder HC, Westh H, Jensen AG, Larsen AR, Skov R, Benfield T (2013) A nationwide study of comorbidity and risk of reinfection after Staphylococcus aureus bacteraemia. J Infect 67(3):199–205CrossRef
15.
go back to reference Kupfer M, Jatzwauk L, Monecke S, Mobius J, Weusten A (2010) MRSA in a large German University hospital: male gender is a significant risk factor for MRSA acquisition. GMS Krankenhhyg Interdiszip 5(2) Kupfer M, Jatzwauk L, Monecke S, Mobius J, Weusten A (2010) MRSA in a large German University hospital: male gender is a significant risk factor for MRSA acquisition. GMS Krankenhhyg Interdiszip 5(2)
16.
go back to reference 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):e17936CrossRef 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):e17936CrossRef
17.
go back to reference 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 53:237–251CrossRef 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 53:237–251CrossRef
18.
go back to reference 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):e0162654CrossRef 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):e0162654CrossRef
19.
go back to reference Selle M, Hertlein T, Oesterreich B, Klemm T, Kloppot P, Müller E, Ehricht R, Stentzel S, Broker BM, Engelmann S, Ohlsen K (2016) Global antibody response to Staphylococcus aureus live-cell vaccination. Sci Rep 6:24754CrossRef Selle M, Hertlein T, Oesterreich B, Klemm T, Kloppot P, Müller E, Ehricht R, Stentzel S, Broker BM, Engelmann S, Ohlsen K (2016) Global antibody response to Staphylococcus aureus live-cell vaccination. Sci Rep 6:24754CrossRef
20.
go back to reference Stieber B, Monecke S, Müller E, Büchler J, Ehricht R (2015) Direct, specific and rapid detection of staphylococcal proteins and exotoxins using a multiplex antibody microarray. PLoS One 10(12):e0143246CrossRef Stieber B, Monecke S, Müller E, Büchler J, Ehricht R (2015) Direct, specific and rapid detection of staphylococcal proteins and exotoxins using a multiplex antibody microarray. PLoS One 10(12):e0143246CrossRef
21.
go back to reference Kohler C, Dunachie SJ, Müller E, Kohler A, Jenjaroen K, Teparrukkul P, Baier V, Ehricht R, Steinmetz I (2016) Rapid and sensitive multiplex detection of Burkholderia pseudomallei-specific antibodies in melioidosis patients based on a protein microarray approach. PLoS Negl Trop Dis 10(7):e0004847CrossRef Kohler C, Dunachie SJ, Müller E, Kohler A, Jenjaroen K, Teparrukkul P, Baier V, Ehricht R, Steinmetz I (2016) Rapid and sensitive multiplex detection of Burkholderia pseudomallei-specific antibodies in melioidosis patients based on a protein microarray approach. PLoS Negl Trop Dis 10(7):e0004847CrossRef
22.
go back to reference Novick RP (2003) Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49(2):93–105CrossRef Novick RP (2003) Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49(2):93–105CrossRef
23.
go back to reference Vojtov N, Ross HF, Novick RP (2002) Global repression of exotoxin synthesis by staphylococcal superantigens. Proc Natl Acad Sci U S A 99(15):10102–10107CrossRef Vojtov N, Ross HF, Novick RP (2002) Global repression of exotoxin synthesis by staphylococcal superantigens. Proc Natl Acad Sci U S A 99(15):10102–10107CrossRef
24.
go back to reference Stieber B, Monecke S, Müller E, Baier V, Coombs G, Ehricht R (2013) Development and usage of protein microarrays for the quantitative measurement of Panton-Valentine leukocidin. Mol Cell Probes Stieber B, Monecke S, Müller E, Baier V, Coombs G, Ehricht R (2013) Development and usage of protein microarrays for the quantitative measurement of Panton-Valentine leukocidin. Mol Cell Probes
25.
go back to reference McCaskill ML, Mason EO Jr, Kaplan SL, Hammerman W, Lamberth LB, Hulten KG (2007) Increase of the USA300 clone among community-acquired methicillin-susceptible Staphylococcus aureus causing invasive infections. Pediatr Infect Dis J 26(12):1122–1127CrossRef McCaskill ML, Mason EO Jr, Kaplan SL, Hammerman W, Lamberth LB, Hulten KG (2007) Increase of the USA300 clone among community-acquired methicillin-susceptible Staphylococcus aureus causing invasive infections. Pediatr Infect Dis J 26(12):1122–1127CrossRef
26.
go back to reference Miko BA, Uhlemann AC, Gelman A, Lee CJ, Hafer CA, Sullivan SB, Shi Q, Miller M, Zenilman J, Lowy FD (2012) High prevalence of colonization with Staphylococcus aureus clone USA300 at multiple body sites among sexually transmitted disease clinic patients: an unrecognized reservoir. Microbes Infect 14(12):1040–1043CrossRef Miko BA, Uhlemann AC, Gelman A, Lee CJ, Hafer CA, Sullivan SB, Shi Q, Miller M, Zenilman J, Lowy FD (2012) High prevalence of colonization with Staphylococcus aureus clone USA300 at multiple body sites among sexually transmitted disease clinic patients: an unrecognized reservoir. Microbes Infect 14(12):1040–1043CrossRef
27.
go back to reference Seybold U, Kourbatova EV, Johnson JG, Halvosa SJ, Wang YF, King MD, Ray SM, Blumberg HM (2006) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 42(5):647–656CrossRef Seybold U, Kourbatova EV, Johnson JG, Halvosa SJ, Wang YF, King MD, Ray SM, Blumberg HM (2006) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 42(5):647–656CrossRef
28.
go back to reference Weber S, Ehricht R, Slickers P, Abdel-Wareth L, Donnelly G, Pitout M, Monecke S (2010) Genetic fingerprinting of MRSA from Abu Dhabi. ECCMID, Vienna Weber S, Ehricht R, Slickers P, Abdel-Wareth L, Donnelly G, Pitout M, Monecke S (2010) Genetic fingerprinting of MRSA from Abu Dhabi. ECCMID, Vienna
29.
go back to reference 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 14:13–18CrossRef 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 14:13–18CrossRef
30.
go back to reference Uhlemann AC, Kennedy AD, Martens C, Porcella SF, Deleo FR, Lowy FD (2012) Toward an understanding of the evolution of Staphylococcus aureus strain USA300 during colonization in community households. Genome Biol Evol 4(12):1275–1285CrossRef Uhlemann AC, Kennedy AD, Martens C, Porcella SF, Deleo FR, Lowy FD (2012) Toward an understanding of the evolution of Staphylococcus aureus strain USA300 during colonization in community households. Genome Biol Evol 4(12):1275–1285CrossRef
31.
go back to reference Monecke S, Ehricht R, Slickers P, Tan HL, Coombs G (2009) The molecular epidemiology and evolution of the Panton-Valentine leukocidin-positive, methicillin-resistant Staphylococcus aureus strain USA300 in Western Australia. Clin Microbiol Infect 15(8):770–776CrossRef Monecke S, Ehricht R, Slickers P, Tan HL, Coombs G (2009) The molecular epidemiology and evolution of the Panton-Valentine leukocidin-positive, methicillin-resistant Staphylococcus aureus strain USA300 in Western Australia. Clin Microbiol Infect 15(8):770–776CrossRef
32.
go back to reference Earls MR, Shore AC, Brennan GI, Simbeck A, Schneider-Brachert W, Vremerǎ T, Dorneanu OS, Slickers P, Ehricht R, Monecke S, Coleman DC (2019) A novel multidrug-resistant PVL-negative CC1-MRSA-IV clone emerging in Ireland and Germany likely originated in South-Eastern Europe. Infect Genet Evol 69:117–126CrossRef Earls MR, Shore AC, Brennan GI, Simbeck A, Schneider-Brachert W, Vremerǎ T, Dorneanu OS, Slickers P, Ehricht R, Monecke S, Coleman DC (2019) A novel multidrug-resistant PVL-negative CC1-MRSA-IV clone emerging in Ireland and Germany likely originated in South-Eastern Europe. Infect Genet Evol 69:117–126CrossRef
33.
go back to reference 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 51:31–35CrossRef 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 51:31–35CrossRef
34.
go back to reference Monecke S, Müller E, Buechler J, Rejman J, Stieber B, Akpaka PE, Bandt D, Burris R, Coombs G, Hidalgo-Arroyo GA, Hughes P, Kearns A, Abos SM, Pichon B, Skakni L, Soderquist B, Ehricht R (2013) Rapid detection of Panton-Valentine leukocidin in Staphylococcus aureus cultures by use of a lateral flow assay based on monoclonal antibodies. J Clin Microbiol 51(2):487–495CrossRef Monecke S, Müller E, Buechler J, Rejman J, Stieber B, Akpaka PE, Bandt D, Burris R, Coombs G, Hidalgo-Arroyo GA, Hughes P, Kearns A, Abos SM, Pichon B, Skakni L, Soderquist B, Ehricht R (2013) Rapid detection of Panton-Valentine leukocidin in Staphylococcus aureus cultures by use of a lateral flow assay based on monoclonal antibodies. J Clin Microbiol 51(2):487–495CrossRef
35.
go back to reference Rasigade JP, Trouillet-Assant S, Breurec S, Antri K, Lina G, Bes M, Tristan A, Badiou C, Bernelin M, Fall C, Ramdani-Bouguessa N, Etienne J, Vandenesch F, Laurent F (2015) The levels of antibodies to Panton-Valentine leukocidin (PVL) vary with PVL prevalence along a north-to-south gradient. Eur J Clin Microbiol Infect Dis 34(5):927–933CrossRef Rasigade JP, Trouillet-Assant S, Breurec S, Antri K, Lina G, Bes M, Tristan A, Badiou C, Bernelin M, Fall C, Ramdani-Bouguessa N, Etienne J, Vandenesch F, Laurent F (2015) The levels of antibodies to Panton-Valentine leukocidin (PVL) vary with PVL prevalence along a north-to-south gradient. Eur J Clin Microbiol Infect Dis 34(5):927–933CrossRef
36.
go back to reference Ji-Young P, Jae-Seok K, Heungjeong W (2015) Prevalence of antibody to toxic shock syndrome toxin-1 in burn patients. Ann Lab Med 35(1):89–93CrossRef Ji-Young P, Jae-Seok K, Heungjeong W (2015) Prevalence of antibody to toxic shock syndrome toxin-1 in burn patients. Ann Lab Med 35(1):89–93CrossRef
37.
go back to reference Quan L, Morita R, Kawakami S (2010) Toxic shock syndrome toxin-1 (TSST-1) antibody levels in Japanese children. Burns 36(5):716–721CrossRef Quan L, Morita R, Kawakami S (2010) Toxic shock syndrome toxin-1 (TSST-1) antibody levels in Japanese children. Burns 36(5):716–721CrossRef
38.
go back to reference Parsonnet J, Goering RV, Hansmann MA, Jones MB, Ohtagaki K, Davis CC, Totsuka K (2008) Prevalence of toxic shock syndrome toxin 1 (TSST-1)-producing strains of Staphylococcus aureus and antibody to TSST-1 among healthy Japanese women. J Clin Microbiol 46(8):2731–2738CrossRef Parsonnet J, Goering RV, Hansmann MA, Jones MB, Ohtagaki K, Davis CC, Totsuka K (2008) Prevalence of toxic shock syndrome toxin 1 (TSST-1)-producing strains of Staphylococcus aureus and antibody to TSST-1 among healthy Japanese women. J Clin Microbiol 46(8):2731–2738CrossRef
39.
go back to reference 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(11):e28189CrossRef 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(11):e28189CrossRef
40.
go back to reference D'Souza N, Rodrigues C, Mehta A (2010) Molecular characterization of methicillin resistant Staphylococcus aureus (MRSA) with emergence of epidemic clones ST 22 and ST 772, in Mumbai, India. J Clin Microbiol 48(5):1806–1811CrossRef D'Souza N, Rodrigues C, Mehta A (2010) Molecular characterization of methicillin resistant Staphylococcus aureus (MRSA) with emergence of epidemic clones ST 22 and ST 772, in Mumbai, India. J Clin Microbiol 48(5):1806–1811CrossRef
Metadata
Title
Genotyping of methicillin-resistant Staphylococcus aureus from sepsis patients in Pakistan and detection of antibodies against staphylococcal virulence factors
Authors
Stefan Monecke
Muhammad Ali Syed
Mushtaq Ahmad Khan
Shehzad Ahmed
Sadia Tabassum
Darius Gawlik
Elke Müller
Annett Reissig
Sascha D. Braun
Ralf Ehricht
Publication date
01-01-2020
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 1/2020
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-019-03695-9

Other articles of this Issue 1/2020

European Journal of Clinical Microbiology & Infectious Diseases 1/2020 Go to the issue