Staphylococcus aureus and Streptococcus pyogenes in the north: distinctively different
Deborah Holt A B * and Philip Giffard A BA College of Health and Human Sciences, Charles Darwin University, Darwin, NT 0811, Australia.
B Tropical and Emerging Infectious Diseases Division, Menzies School of Health Research, Charles Darwin University, Darwin, NT 0811, Australia.
Deborah Holt is a senior lecturer at Charles Darwin University and Honorary Research Fellow at the Menzies School of Health Research. She is a molecular biologist whose research focuses on the molecular epidemiology and pathogenesis of skin pathogens with importance in Indigenous communities in northern Australia. |
Phil Giffard is Head of Laboratory Science at the Menzies School of Health Research and Head of Biomedical Science in the College of Health and Human Science at Charles Darwin University. He has a long-standing research interested in microbial genotyping technology and associated bioinformatic methods. |
Microbiology Australia 43(3) 104-107 https://doi.org/10.1071/MA22034
Submitted: 28 June 2022 Accepted: 28 August 2022 Published: 20 September 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the ASM. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Staphylococcus aureus and Streptococcus pyogenes are important contributors to disease in northern Australia. Both are opportunistic pathogens, frequently carried on the skin or in the respiratory tract in the absence of disease. A large proportion of the S. aureus strains causing infection in northern Australia possess the Panton Valentine (PVL) toxin, with ST93, ST5, and ST121 being significant. PVL+ strains are associated with both community- and healthcare-associated infections, and a large proportion are methicillin-resistant S. aureus (MRSA). MRSA strains known to be healthcare associated (ST239 and ST22) are not prevalent. CC1 PVL− MRSA continue to cause infections. The diversity of S. pyogenes emm types in northern Australia is high with skin tropic and non-tropic emm types predominating. This contrasts with other parts of Australia where emm diversity is lower and rates of pharyngitis higher. The high diversity raises concerns for the likely efficacy of vaccines based on the variable region of the M protein, the nucleotide sequence of which underpins emm typing. It is likely that complex interactions occur between these two important bacterial pathogens, and other important skin pathogens in the region such as the scabies mite.
Keywords: emm typing, M protein, Panton Valentine leucocidin, PVL, pyoderma, rheumatic heart disease, skin infections, Staphylococcus aureus, Streptococcus pyogenes.
References
[1] Currie, BJ and Carapetis, JR (2000) Skin infections and infestations in Aboriginal communities in northern Australia. Australas J Dermatol 41, 139–143.| Skin infections and infestations in Aboriginal communities in northern Australia.Crossref | GoogleScholarGoogle Scholar |
[2] Turner, KME and Feil, EJ (2007) The secret life of the multilocus sequence type. Int J Antimicrob Agents 29, 129–135.
| The secret life of the multilocus sequence type.Crossref | GoogleScholarGoogle Scholar |
[3] Henderson, A and Nimmo, GR (2018) Control of healthcare- and community-associated MRSA: recent progress and persisting challenges. Br Med Bull 125, 25–41.
| Control of healthcare- and community-associated MRSA: recent progress and persisting challenges.Crossref | GoogleScholarGoogle Scholar |
[4] Coombs, GW et al.. (2014) Community-onset Staphylococcus aureus Surveillance Programme annual report, 2012. Commun Dis Intell Q Rep 38, E59–E69.
[5] Dotel, R et al.. (2019) Molecular epidemiology of methicillin-resistant Staphylococcus aureus isolates in New South Wales, Australia, 2012–2017. Infect Dis Health 24, 134–140.
| Molecular epidemiology of methicillin-resistant Staphylococcus aureus isolates in New South Wales, Australia, 2012–2017.Crossref | GoogleScholarGoogle Scholar |
[6] Coombs, GW et al.. (2020) Australian Group on Antimicrobial Resistance (AGAR) Australian Enterococcal Sepsis Outcome Programme (AESOP) Annual Report 2019. Commun Dis Intell 44, 1–12.
| Australian Group on Antimicrobial Resistance (AGAR) Australian Enterococcal Sepsis Outcome Programme (AESOP) Annual Report 2019.Crossref | GoogleScholarGoogle Scholar |
[7] Brennan, L et al.. (2013) Community-associated meticillin-resistant Staphylococcus aureus carriage in hospitalized patients in tropical northern Australia. J Hosp Infect 83, 205–211.
| Community-associated meticillin-resistant Staphylococcus aureus carriage in hospitalized patients in tropical northern Australia.Crossref | GoogleScholarGoogle Scholar |
[8] Holt, DC et al.. (2021) Longitudinal whole-genome based comparison of carriage and infection associated Staphylococcus aureus in northern Australian dialysis clinics. PLoS One 16, e0245790.
| Longitudinal whole-genome based comparison of carriage and infection associated Staphylococcus aureus in northern Australian dialysis clinics.Crossref | GoogleScholarGoogle Scholar |
[9] Tong, SYC et al.. (2015) Progressive increase in community-associated methicillin-resistant Staphylococcus aureus in Indigenous populations in northern Australia from 1993 to 2012. Epidemiol Infect 143, 1519–1523.
| Progressive increase in community-associated methicillin-resistant Staphylococcus aureus in Indigenous populations in northern Australia from 1993 to 2012.Crossref | GoogleScholarGoogle Scholar |
[10] van Hal, SJ et al.. (2018) Global scale dissemination of ST93: a divergent Staphylococcus aureus epidemic lineage that has recently emerged from remote northern Australia. Front Microbiol 9, 1453.
| Global scale dissemination of ST93: a divergent Staphylococcus aureus epidemic lineage that has recently emerged from remote northern Australia.Crossref | GoogleScholarGoogle Scholar |
[11] McGuinness, SL et al.. (2021) Clinical and molecular epidemiology of an emerging Panton-Valentine leukocidin-positive ST5 methicillin-resistant Staphylococcus aureus clone in Northern Australia. mSphere 6, e00651-20.
| Clinical and molecular epidemiology of an emerging Panton-Valentine leukocidin-positive ST5 methicillin-resistant Staphylococcus aureus clone in Northern Australia.Crossref | GoogleScholarGoogle Scholar |
[12] Tong, SYC et al.. (2009) Community-associated strains of methicillin-resistant Staphylococcus aureus and methicillin-susceptible S. aureus in indigenous Northern Australia: epidemiology and outcomes. J Infect Dis 199, 1461–1470.
| Community-associated strains of methicillin-resistant Staphylococcus aureus and methicillin-susceptible S. aureus in indigenous Northern Australia: epidemiology and outcomes.Crossref | GoogleScholarGoogle Scholar |
[13] Rao, Q et al.. (2015) Staphylococcus aureus ST121: a globally disseminated hypervirulent clone. J Med Microbiol 64, 1462–1473.
| Staphylococcus aureus ST121: a globally disseminated hypervirulent clone.Crossref | GoogleScholarGoogle Scholar |
[14] Harch, SAJ et al.. (2017) High burden of complicated skin and soft tissue infections in the Indigenous population of Central Australia due to dominant Panton Valentine leucocidin clones ST93-MRSA and CC121-MSSA. BMC Infect Dis 17, 405.
| High burden of complicated skin and soft tissue infections in the Indigenous population of Central Australia due to dominant Panton Valentine leucocidin clones ST93-MRSA and CC121-MSSA.Crossref | GoogleScholarGoogle Scholar |
[15] Coombs, GW et al.. (2004) Genetic diversity among community methicillin-resistant Staphylococcus aureus strains causing outpatient infections in Australia. J Clin Microbiol 42, 4735–4743.
| Genetic diversity among community methicillin-resistant Staphylococcus aureus strains causing outpatient infections in Australia.Crossref | GoogleScholarGoogle Scholar |
[16] Tong, SYC et al.. (2015) Novel staphylococcal species that form part of a Staphylococcus aureus-related complex: the non-pigmented Staphylococcus argenteus sp. nov. and the non-human primate-associated Staphylococcus schweitzeri sp. nov. Int J Syst Evol Microbiol 65, 15–22.
| Novel staphylococcal species that form part of a Staphylococcus aureus-related complex: the non-pigmented Staphylococcus argenteus sp. nov. and the non-human primate-associated Staphylococcus schweitzeri sp. nov.Crossref | GoogleScholarGoogle Scholar |
[17] Carapetis, JR et al.. (1996) Acute rheumatic fever and rheumatic heart disease in the top end of Australia’s Northern Territory. Med J Aust 164, 146–149.
| Acute rheumatic fever and rheumatic heart disease in the top end of Australia’s Northern Territory.Crossref | GoogleScholarGoogle Scholar |
[18] McMillan, DJ et al.. (2013) Updated model of group A Streptococcus M proteins based on a comprehensive worldwide study. Clin Microbiol Infect 19, E222–E229.
| Updated model of group A Streptococcus M proteins based on a comprehensive worldwide study.Crossref | GoogleScholarGoogle Scholar |
[19] Steer, AC et al.. (2009) Global emm type distribution of group A streptococci: systematic review and implications for vaccine development. Lancet Infect Dis 9, 611–616.
| Global emm type distribution of group A streptococci: systematic review and implications for vaccine development.Crossref | GoogleScholarGoogle Scholar |
[20] McDonald, MI et al.. (2006) Low rates of streptococcal pharyngitis and high rates of pyoderma in Australian aboriginal communities where acute rheumatic fever is hyperendemic. Clin Infect Dis 43, 683–689.
| Low rates of streptococcal pharyngitis and high rates of pyoderma in Australian aboriginal communities where acute rheumatic fever is hyperendemic.Crossref | GoogleScholarGoogle Scholar |
[21] Giffard, PM et al.. (2019) Concerns for efficacy of a 30-valent M-protein-based Streptococcus pyogenes vaccine in regions with high rates of rheumatic heart disease. PLoS Negl Trop Dis 13, e0007511.
| Concerns for efficacy of a 30-valent M-protein-based Streptococcus pyogenes vaccine in regions with high rates of rheumatic heart disease.Crossref | GoogleScholarGoogle Scholar |
[22] Bessen, DE et al.. (2000) Contrasting molecular epidemiology of group A streptococci causing tropical and nontropical infections of the skin and throat. J Infect Dis 182, 1109–1116.
| Contrasting molecular epidemiology of group A streptococci causing tropical and nontropical infections of the skin and throat.Crossref | GoogleScholarGoogle Scholar |
[23] McDonald, MI et al.. (2007) Molecular typing of Streptococcus pyogenes from remote Aboriginal communities where rheumatic fever is common and pyoderma is the predominant streptococcal infection. Epidemiol Infect 135, 1398–1405.
| Molecular typing of Streptococcus pyogenes from remote Aboriginal communities where rheumatic fever is common and pyoderma is the predominant streptococcal infection.Crossref | GoogleScholarGoogle Scholar |
[24] McDonald, MI et al.. (2008) The dynamic nature of group A streptococcal epidemiology in tropical communities with high rates of rheumatic heart disease. Epidemiol Infect 136, 529–539.
| The dynamic nature of group A streptococcal epidemiology in tropical communities with high rates of rheumatic heart disease.Crossref | GoogleScholarGoogle Scholar |
[25] Richardson, LJ et al.. (2011) Preliminary validation of a novel high-resolution melt-based typing method based on the multilocus sequence typing scheme of Streptococcus pyogenes. Clin Microbiol Infect 17, 1426–1434.
| Preliminary validation of a novel high-resolution melt-based typing method based on the multilocus sequence typing scheme of Streptococcus pyogenes.Crossref | GoogleScholarGoogle Scholar |
[26] McGregor, KF et al.. (2004) Group A streptococci from a remote community have novel multilocus genotypes but share emm types and housekeeping alleles with isolates from worldwide sources. J Infect Dis 189, 717–723.
| Group A streptococci from a remote community have novel multilocus genotypes but share emm types and housekeeping alleles with isolates from worldwide sources.Crossref | GoogleScholarGoogle Scholar |
[27] Towers, RJ et al.. (2013) Extensive diversity of Streptococcus pyogenes in a remote human population reflects global-scale transmission rather than localised diversification. PLoS One 8, e73851.
| Extensive diversity of Streptococcus pyogenes in a remote human population reflects global-scale transmission rather than localised diversification.Crossref | GoogleScholarGoogle Scholar |
[28] Williamson, DA et al.. (2015) M-Protein analysis of Streptococcus pyogenes isolates associated with acute rheumatic fever in New Zealand. J Clin Microbiol 53, 3618–3620.
| M-Protein analysis of Streptococcus pyogenes isolates associated with acute rheumatic fever in New Zealand.Crossref | GoogleScholarGoogle Scholar |
[29] Good, MF et al.. (2015) Strategic development of the conserved region of the M protein and other candidates as vaccines to prevent infection with group A streptococci. Expert Rev Vaccines 14, 1459–1470.
| Strategic development of the conserved region of the M protein and other candidates as vaccines to prevent infection with group A streptococci.Crossref | GoogleScholarGoogle Scholar |
[30] Sanderson-Smith, M et al.. (2014) A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development. J Infect Dis 210, 1325–1338.
| A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development.Crossref | GoogleScholarGoogle Scholar |
[31] Valery, PC et al.. (2008) Skin infections among Indigenous Australians in an urban setting in far North Queensland. Epidemiol Infect 136, 1103–1108.
| Skin infections among Indigenous Australians in an urban setting in far North Queensland.Crossref | GoogleScholarGoogle Scholar |
[32] Bowen, AC et al.. (2014) The microbiology of impetigo in indigenous children: associations between Streptococcus pyogenes, Staphylococcus aureus, scabies, and nasal carriage. BMC Infect Dis 14, 727.
| The microbiology of impetigo in indigenous children: associations between Streptococcus pyogenes, Staphylococcus aureus, scabies, and nasal carriage.Crossref | GoogleScholarGoogle Scholar |