• View in gallery

    Summary of the selection process and reasons for study exclusion.

  • View in gallery

    Global distribution of emm types associated with acute post-streptococcal glomerulonephritis.

  • 1.

    Oliveira D, 1997. Poststreptococcal glomerulonephritis: getting to know an old enemy. Clin Exp Immunol 107: 810.

  • 2.

    Rodriguez-Iturbe B, Musser JM, 2008. The current state of poststreptococcal glomerulonephritis. J Am Soc Nephrol 19: 18551864.

  • 3.

    Carapetis JR, Steer AC, Mulholland EK, Weber M, 2005. The global burden of group A streptococcal diseases. Lancet Infect Dis 5: 685694.

  • 4.

    Bailie RS, Runcie MJ, 2001. Household infrastructure in aboriginal communities and the implications for health improvement. Med J Aust 175: 363366.

    • Search Google Scholar
    • Export Citation
  • 5.

    Bailie J, Schierhout G, Laycock A, Kelaher M, Percival N, O’Donoghue L, McNeair T, Bailie R, 2015. Determinants of access to chronic illness care: a mixed-methods evaluation of a national multifaceted chronic disease package for Indigenous Australians. BMJ Open 5: e008103.

    • Search Google Scholar
    • Export Citation
  • 6.

    Jackson SJ, Steer AC, Campbell H, 2011. Systematic review: estimation of global burden of non‐suppurative sequelae of upper respiratory tract infection: rheumatic fever and post‐streptococcal glomerulonephritis. Trop Med Int Health 16: 211.

    • Search Google Scholar
    • Export Citation
  • 7.

    Dillon H, Derrick C, Dillon M, 1974. M-antigens common to pyoderma and acute glomerulonephritis. J Infect Dis 130: 257267.

  • 8.

    Poon-King T, Svartman M, Mohammed I, Potter E, Achong J, Cox R, Earle D, 1973. Epidemic acute nephritis with reappearance of M-type 55 streptococci in Trinidad. Lancet 301: 475479.

    • Search Google Scholar
    • Export Citation
  • 9.

    Steer AC, Law I, Matatolu L, Beall BW, Carapetis JR, 2009. Global emm type distribution of group A streptococci: systematic review and implications for vaccine development. Lancet Infect Dis 9: 611616.

    • Search Google Scholar
    • Export Citation
  • 10.

    WHO, 2017. Executive Board 141st Session, Geneva, 1 June 2017: Resolutions and Decisions, Annexes, Summary Records. Geneva, Switzerland: World Health Organisation.

    • Search Google Scholar
    • Export Citation
  • 11.

    Kanjanabuch T, Kittikowit W, Eiam-Ong S, 2009. An update on acute postinfectious glomerulonephritis worldwide. Nat Rev Nephrol 5: 259269.

  • 12.

    Marshall CS, Cheng AC, Markey PG, Towers RJ, Richardson LJ, Fagan PK, Scott L, Krause VL, Currie BJ, 2011. Acute post-streptococcal glomerulonephritis in the Northern Territory of Australia: a review of 16 years data and comparison with the literature. Am J Trop Med Hyg 85: 703710.

    • Search Google Scholar
    • Export Citation
  • 13.

    Speers DJ, Levy A, Gichamo A, Eastwood A, Leung MJ, 2017. M protein gene (emm type) analysis of group A Streptococcus isolates recovered during an acute glomerulonephritis outbreak in northern Western Australia. Pathology 49: 765769.

    • Search Google Scholar
    • Export Citation
  • 14.

    Hoy WE, White AV, Dowling A, Sharma SK, Bloomfield H, Tipiloura BT, Swanson CE, Mathews JD, McCredie DA, 2012. Post-streptococcal glomerulonephritis is a strong risk factor for chronic kidney disease in later life. Kidney Int 81: 10261032.

    • Search Google Scholar
    • Export Citation
  • 15.

    Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D, 2009. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6: e1000100.

    • Search Google Scholar
    • Export Citation
  • 16.

    Anthony B, Kaplan E, Chapman SS, Quie P, Wannamaker L, 1967. Epidemic acute nephritis with reappearance of type-49 Streptococcus. Lancet 290: 787790.

    • Search Google Scholar
    • Export Citation
  • 17.

    Facklam R 1999. emm typing and validation of provisional M types for group A streptococci. Emerg Infect Dis 5: 247253.

  • 18.

    Simpson EH, 1949. Measurement of diversity. Nature 163: 688.

  • 19.

    Grundmann H, Hori S, Tanner G, 2001. Determining confidence intervals when measuring genetic diversity and the discriminatory abilities of typing methods for microorganisms. J Clin Microbiol 39: 41904192.

    • Search Google Scholar
    • Export Citation
  • 20.

    Anthony BF, Perlman LV, Wannamaker LW, 1967. Skin infections and acute nephritis in American Indian children. Pediatrics 39: 263279.

  • 21.

    Tayeb SH, Nasr EM, Attallah AS, 1978. Streptococcal impetigo and acute glomerulonephritis in children in Cairo. Br J Dermatol 98: 53.

  • 22.

    Rodríguez-Iturbe B, Rubio L, García R, 1981. Attack rate of poststreptococcal nephritis in families: a prospective study. Lancet 317: 401403.

    • Search Google Scholar
    • Export Citation
  • 23.

    Majeed H, Yousof A, Rotta J, Havlickpva H, Bahar G, Bahbahani K, 1992. Group A streptococcal strains in Kuwait: a nine-year prospective study of prevalence and associations. Pediatr Infect Dis J 11: 295299.

    • Search Google Scholar
    • Export Citation
  • 24.

    Gaworzewska E, Colman G, 1988. Changes in the pattern of infection caused by Streptococcus pyogenes. Epidemiol Infect 100: 257269.

  • 25.

    Reid H, Bassett D, Gaworzewska E, Colman G, Poon-King T, 1990. Streptococcal serotypes newly associated with epidemic post-streptococcal acute glomerulonephritis. J Med Microbiol 32: 111114.

    • Search Google Scholar
    • Export Citation
  • 26.

    Tewodros W, Kronvall G, 2005. M protein gene (emm type) analysis of group A beta-hemolytic streptococci from Ethiopia reveals unique patterns. J Clin Microbiol 43: 43694376.

    • Search Google Scholar
    • Export Citation
  • 27.

    Mori K, Ito Y, Kamikawaji N, Sasazuki T, 1997. Elevated IgG titer against the C region of streptococcal M protein and its immunodeterminants in patients with poststreptococcal acute glomerulonephritis. J Pediatr 131: 293299.

    • Search Google Scholar
    • Export Citation
  • 28.

    Masayuma T 1996. Outbreak of acute glomerulonephritis in children: observed association with the T1 subtype of group A streptococcal infection in northern Kyushu, Japan. Pediatr Int 38: 128131.

    • Search Google Scholar
    • Export Citation
  • 29.

    Zheng MH 2009. Genetic analysis of group A Streptococcus isolates recovered during acute glomerulonephritis outbreaks in Guizhou province of China. J Clin Microbiol 47: 715720.

    • Search Google Scholar
    • Export Citation
  • 30.

    Berríos X, Lagomarsino E, Solar E, Sandoval G, Guzmán B, Riedel I, 2004. Post-streptococcal acute glomerulonephritis in Chile—20 years of experience. Pediatr Nephrol 19: 306312.

    • Search Google Scholar
    • Export Citation
  • 31.

    Dale JB, Penfound TA, Chiang EY, Walton WJ, 2011. New 30-valent M protein-based vaccine evokes cross-opsonic antibodies against non-vaccine serotypes of group A streptococci. Vaccine 29: 81758178.

    • Search Google Scholar
    • Export Citation
  • 32.

    Dale JB, Penfound TA, Tamboura B, Sow SO, Nataro JP, Tapia M, Kotloff KL, 2013. Potential coverage of a multivalent M protein-based group A streptococcal vaccine. Vaccine 31: 15761581.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

Systematic Review of Group A Streptococcal emm Types Associated with Acute Post-Streptococcal Glomerulonephritis

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  • 1 Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Victoria, Australia;
  • 2 Doherty Department at the Peter Doherty Institute for Infection and Immunity, University of Melbourne, Victoria, Australia;
  • 3 Victorian Infectious Diseases Reference Laboratory Epidemiology Unit, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Victoria, Australia;
  • 4 Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Victoria, Australia;
  • 5 Tropical Diseases Research Group, Murdoch Children’s Research Institute, Melbourne, Victoria, Australia;
  • 6 Victorian Infectious Disease Service, The Royal Melbourne Hospital, Peter Doherty Institute for Infection and Immunity, Doherty Department University of Melbourne, Victoria, Australia;
  • 7 Menzies School of Health Research, Darwin, Australia

Acute post-streptococcal glomerulonephritis (APSGN) is a postinfectious immune-mediated kidney disease associated with group A Streptococcus (GAS). The prevalence of APSGN varies within and between countries and is influenced by socioeconomic, host, and bacterial factors. The disease is more prevalent in developing countries and resource-poor settings of developed countries, such as the Indigenous populations residing in tropical Australia. The M-protein is a universally present GAS surface antigen that is the focus of molecular typing and vaccine research. Early reports suggested that some M-proteins (emm types) are more likely to cause APSGN than others. Here, we present the first systematic review of the global distribution of APSGN-associated GAS emm types. There were 46 emm types among the 676 cases described in 15 reviewed articles. Only 43% APSGN cases would have had theoretical coverage from the experimental M protein-based GAS vaccine. Vaccine coverage was higher in regions such as North America (97%) and the United Kingdom (98%) than Africa (67%) and Australia (38%). Variable vaccine coverage against APSGN- associated emm types highlights the need for further research into this disease, particularly in settings of poverty, where APSGN prevalence is higher. Three GAS emm types (emm49, emm60, and emm55) consistently occur in APSGN cases around the world. Future studies would therefore benefit from examining the genomic epidemiology of these emm types to unravel potential markers of APSGN.

INTRODUCTION

Streptococcus pyogenes, also known as Group A Streptococcus (GAS) or Streptococcus A, causes a wide spectrum of disease ranging from pharyngitis and impetigo to severe invasive disease and postinfectious sequelae such as rheumatic heart disease and acute post-streptococcal glomerulonephritis (APSGN). Acute post-streptococcal glomerulonephritis is a postinfectious immune-mediated kidney disease, where GAS antigens are purportedly deposited on the glomerular membrane and subsequently induce glomerulonephritis.1 Echoing the prevalence of other GAS diseases such as impetigo and rheumatic heart disease, the estimated prevalence of APSGN is higher in countries with a low Human Development Index (HDI) (9.3–28.5 cases per 100,000 people)2,3 than in high HDI countries (0.3–2 cases per 100,000 people).3 Acute post-streptococcal glomerulonephritis can also occur in resource-poor settings within high HDI countries. For example, the prevalence of APSGN among Indigenous Australians in the tropical north of the country, where poor housing infrastructure4 and reduced access to health care5 are common, is the highest in the world (239 per 100,000 people), even though Australia is classified as a high HDI country.6 This indicates that APSGN prevalence varies both within and between countries and is influenced by socioeconomic and possibly genetic host factors.2

In addition to investigating the host factors contributing to APSGN, researchers have also sought to identify bacterial factors that may lead to the development of this disease. The M-protein is a universally present surface antigen among GAS that has been the focus of most typing and vaccine research because of its reliable presence, molecular diversity, and immunogenicity. Early reports of APSGN outbreaks found that certain M-proteins (emm types) were overrepresented among APSGN cases, suggesting that some M-proteins are more “nephritogenic,” that is, more likely to cause APSGN, than others.7,8 However, just as APSGN incidence varies with the development index of a country, so too does the diversity of emm types within a country.9 Studies which examine the relationship between the emm type and APSGN within a single geographic region will therefore be confounded by the emm type diversity within that region. Whereas in 2018 the 71st World Health Assembly adopted a resolution calling for greater action on GAS-associated rheumatic heart disease,10 APSGN has not received the same attention despite continued outbreaks in geographical regions where rates of rheumatic heart disease are also elevated.1113 Research into APSGN also trails significantly behind research into acute rheumatic fever (ARF), another GAS sequela. A review of population-based studies identified 38 articles documenting the incidence of ARF compared with just 11 studies of APSGN, despite similar estimates of the global prevalence of each disease (471,000 cases per year in ARF and 472,000 cases of APSGN).3 Given APSGN is a leading risk factor for the development of chronic kidney disease, particularly in resource-poor settings,14 a deeper understanding of the molecular mechanisms and clinical epidemiology of GAS-associated APSGN is required so that effective preventative measures can be developed. We therefore conducted the first systematic review to examine the global distribution of APSGN-associated GAS emm types.

METHODS

A literature search was conducted based on the PRISMA guidelines for conducting reviews.15 The PubMed and Web of Science databases were searched using the terms: (pyogenes OR streptococc*) AND (*nephritis OR ((renal OR kidney) AND (disease)) OR nephropathy) AND (emm OR M). An English language limit was placed on the search. No date limits were used. The abstract and full text screening process are summarized in Figure 1. Abstracts that did not mention the aforementioned search terms were excluded. Full texts were excluded if they were review articles that did not contain primary data, contained overlapping data with previous studies, did not separate APSGN cases from other diseases in their dataset, or did not give numbers for each emm type in their dataset. Articles that did not provide an acceptable clinical definition of APSGN and studies that did not clearly differentiate APSGN cases from APSGN contacts were also excluded. An APSGN case was defined as having at least two of the following clinical signs: hematuria, hypertension, and facial or peripheral edema; laboratory evidence of hematuria and/or proteinuria; evidence of streptococcal infection by serology or culture; and a reduced complement C3 level.12,16 Studies that described patients with at least one of the aforementioned clinical signs as well as positive streptococcal culture and histopathological evidence of glomerulonephritis were also included in the review.16 Screening of abstracts and full texts and tabulation of data were performed by a single investigator (K. A. W.). As there is very good concordance between M-protein serotyping and emm gene sequencing results,17 both methods of emm typing were included in the review. emm subtypes (e.g., emm55.3) were reported in some newer studies that had used sequence typing; these were regrouped into their broader parent emm types (e.g., emm55) to align with older studies that used M-protein serotyping (https://www.cdc.gov/streplab/assigning.html). The emm type of isolates listed as “sequence type” was inferred using the CDC emm database (https://www.cdc.gov/streplab/types-emm103-124.html). As previously described,9 the geographic origin of studies was classified based on regions described in the United Nations Populations Prospects 2017 documentation (https://esa.un.org/unpd/wpp/Download/Standard/Population/). The Simpson’s index of diversity was used to calculate emm variation among APSGN cases per region.18 The diversity index was calculated as a percentage, which indicated the likelihood that two random isolates from the same geographic area would be a different emm type; higher percentages indicated higher levels of emm type diversity in a particular region.9 CIs were calculated for diversity indices.19 As a conservative approach, 95% CIs that did not overlap were considered to be significantly different at the 5% significance level. To indicate whether emm types were under- or overrepresented in APSGN cases, we evaluated the equivalent to a “residual” in a χ2 test [(observed frequency − expected frequency)/observed frequency]. The relative frequencies of each emm type observed in APSGN cases were compared with the expected frequency of emm types in each region, based on data from a large review of emm types associated with all diseases.9 Formal hypothesis testing was not performed because of the small number of APSGN cases in some geographic regions and because of the nonrandom way in which data were collected.

Figure 1.
Figure 1.

Summary of the selection process and reasons for study exclusion.

Citation: The American Journal of Tropical Medicine and Hygiene 100, 5; 10.4269/ajtmh.18-0827

RESULTS AND DISCUSSION

A total of 15 articles (from a starting set of 186 records) were included in the final review, encompassing studies from 12 countries in six regions around the world (Figure 1). A total of 676 APSGN cases were included in the review, originating from the United Kingdom (n = 47), the United States (n = 117), Latin America and the Caribbean (n = 322), Asia (n = 109), Africa (n = 60), and Australia (n = 21). Forty-six emm types were present among the 676 APSGN-associated GAS isolates (Table 1). The average number of confirmed APSGN cases reported in each study with emm typing performed was 43 (range 3–264).

Table 1

emm types of group A Streptococcus isolated from patients with acute post-streptococcal glomerulonephritis

Table 1

Most studies featured data collected over several years, with data collected during the periods of 1964–1969 (n = 3),7,16,20 1970–1979 (n = 3),8,21,22 1980–1989 (n = 3),2325 1990–1999 (n = 3),2628 and 2000–2009 (n = 1).29 Two studies collected data over more than a 10-year period: one study from Chile collected data between 1980 and 199930 and a second study from Australia featured data from 1991 to 2008.12 Seven of the 15 studies featured longitudinally collected data and did not mention an outbreak.7,2024,26 Six studies specifically defined their case collection as one or two outbreaks,8,16,25,2729 and all but one25 of these reports attributed the outbreaks to a single emm type. The two studies that collected data over more than a 10-year period contained both small outbreaks and sporadic cases.12,30 Several methods of emm typing were reported in the studies, including diffusion or precipitation M-protein serotyping (n = 11) and emm gene sequencing (n = 3). Two studies used both serotyping and precipitation methods of emm typing.7,21 One study did not specify the method of emm typing used.27 Most studies included APSGN cases that were M non-typeable.

The most common APSGN-associated GAS emm types were 55, 49, 2, 12, 60, 1, and 73. These seven emm types accounted for 85% of the reported APSGN cases. The majority (88%) of emm55 cases came from a single large outbreak of APSGN in 429 patients in Trinidad in 1971, 264 of whom had emm55 isolated from their skin or throat.8 The large Trinidad outbreak met our inclusion criteria for this review, but its inclusion admittedly skewed the data such that emm55 was greatly overrepresented. Excluding this outbreak, emm55 still accounted for 37 (9%) remaining APSGN cases. Although emm55 was the most common APSGN-associated emm type, emm49 was the most widely dispersed, being reported in five of six regions. emm49 was overrepresented among APSGN cases in the United Kingdom and North America (44/161 [27%] cases) compared with emm49 among all diseases from the United Kingdom and the United States (306/24,055 [1.3%] cases).9 emm60 was also overrepresented in APSGN cases, with its observed frequency in the United States and the United Kingdom (14/161 [8.7%] cases) being higher than its expected frequency among all GAS infections (48/24,055 [0.2%] cases).9 emm1, the most commonly reported emm type across all GAS studies (18% of all samples, n = 30,081),9 accounted for only 5% of APSGN-associated samples worldwide.

Figure 2 shows the distribution of APSGN-associated emm types around the world. Calculation of the Simpson’s diversity index showed that emm type diversity varied across geographic regions: emm type diversity was higher in Australia (88%; CI = 87–88%), the United Kingdom (87%; CI = 83–91%), and Asia (85%; 81–90%) compared with North America (69%; CI = 64–74%) and Latin America (22%; CI = 16–29%). The low diversity seen in Latin America was largely influenced by the large emm55 APSGN outbreak of 1971, which accounted for 82% of APSGN cases from this region.8 This is similar to the findings of the review by Steer et al.,9 which found higher emm type diversity among GAS disease of all types in the Pacific and Africa and lower diversity in the United Kingdom and North America.

Figure 2.
Figure 2.

Global distribution of emm types associated with acute post-streptococcal glomerulonephritis.

Citation: The American Journal of Tropical Medicine and Hygiene 100, 5; 10.4269/ajtmh.18-0827

Overall, 294 of 676 (43%) APSGN cases would have had theoretical protective coverage from the experimental 30-valent M-protein–based GAS vaccine,31 although this would increase to 352/676 (52%) if non-vaccinal M-proteins with demonstrated protection by cross-opsonization were considered.31,32 Because of the absence of emm55 in the 30-valent vaccine, only 11% of Latin American and Caribbean APSGN cases would have been covered. In Australia and Africa, 24% and 42% of cases would have been covered, respectively, increasing to 38% and 67% if non-vaccinal M-proteins with demonstrated protection by cross-opsonization were considered.31,32 This is in contrast to North America, Asia, and the United Kingdom, where 84–97%, 80–98%, and 93–98% of cases, respectively, would have had theoretical protection from the M-proteins and cross-protection demonstrated by the experimental 30-valent GAS vaccine.31,32 A similar pattern of vaccine coverage was seen in the review of emm types associated with all diseases, which found higher vaccine coverage in high-income countries such as the United Kingdom and the United States and lower coverage in Africa and the Pacific.9 It is noteworthy that fewer APSGN cases were protected by the extended coverage of the 30-valent vaccine (52%) than the proportion of all GAS cases that would have had theoretical coverage by the narrower 26-valent vaccine (69.7%).9

Despite the strict inclusion criteria we imposed in this review, our report is limited by heterogeneity among the studies we examined. Studies varied in their design, sample size, typing methods, and whether GAS was isolated from the nose or throat of APSGN patients. The results would therefore be affected by bias, most notably in the inclusion of large outbreaks that skewed some of the data such as the overrepresentation of emm55 among APSGN cases from Latin America and the Caribbean.8 Data on the site of isolation were not included in this review because some studies did not describe the site from which GAS was isolated. A study from Australia13 and another from Ethiopia26 noted that APSGN cases were more commonly associated with skin disease than pharyngitis; future investigations into the relationship between the GAS emm type, underlying disease, and APSGN are therefore indicated. We compared the observed proportions of APSGN-related emm types with expected proportions from previous reports of all GAS diseases,9 but the studies we examined were not necessarily representative of the broader population from which they came. General trends were observed in APSGN data that nevertheless mirrored the trends found in worldwide emm type diversity and vaccine coverage, indicating that comparison of our dataset with the broader dataset from a previous review9 was useful for assessing when the emm type frequency among APSGN cases diverged from the expected frequency for each region.

We observed a higher than expected occurrence of emm49 and emm60 among APSGN cases in particular regions and the underrepresentation of emm1 compared with its predominance as a cause of invasive disease. Monitoring of these nephritogenic emm types in susceptible populations such as Indigenous Australians in the tropical north is recommended for APSGN disease management. Future studies would benefit from examining the molecular epidemiology of emm49, emm60, and emm55 to determine if the M-proteins themselves are particularly nephritogenic or whether emm acts as a marker for other characteristics of these lineages that have led to their apparent overrepresentation in APSGN cases around the world.

Acknowledgments:

We thank Anusha Sarilla for her assistance in data curation and Seamus O’Reilly for his ongoing support in reviewing this manuscript.

REFERENCES

  • 1.

    Oliveira D, 1997. Poststreptococcal glomerulonephritis: getting to know an old enemy. Clin Exp Immunol 107: 810.

  • 2.

    Rodriguez-Iturbe B, Musser JM, 2008. The current state of poststreptococcal glomerulonephritis. J Am Soc Nephrol 19: 18551864.

  • 3.

    Carapetis JR, Steer AC, Mulholland EK, Weber M, 2005. The global burden of group A streptococcal diseases. Lancet Infect Dis 5: 685694.

  • 4.

    Bailie RS, Runcie MJ, 2001. Household infrastructure in aboriginal communities and the implications for health improvement. Med J Aust 175: 363366.

    • Search Google Scholar
    • Export Citation
  • 5.

    Bailie J, Schierhout G, Laycock A, Kelaher M, Percival N, O’Donoghue L, McNeair T, Bailie R, 2015. Determinants of access to chronic illness care: a mixed-methods evaluation of a national multifaceted chronic disease package for Indigenous Australians. BMJ Open 5: e008103.

    • Search Google Scholar
    • Export Citation
  • 6.

    Jackson SJ, Steer AC, Campbell H, 2011. Systematic review: estimation of global burden of non‐suppurative sequelae of upper respiratory tract infection: rheumatic fever and post‐streptococcal glomerulonephritis. Trop Med Int Health 16: 211.

    • Search Google Scholar
    • Export Citation
  • 7.

    Dillon H, Derrick C, Dillon M, 1974. M-antigens common to pyoderma and acute glomerulonephritis. J Infect Dis 130: 257267.

  • 8.

    Poon-King T, Svartman M, Mohammed I, Potter E, Achong J, Cox R, Earle D, 1973. Epidemic acute nephritis with reappearance of M-type 55 streptococci in Trinidad. Lancet 301: 475479.

    • Search Google Scholar
    • Export Citation
  • 9.

    Steer AC, Law I, Matatolu L, Beall BW, Carapetis JR, 2009. Global emm type distribution of group A streptococci: systematic review and implications for vaccine development. Lancet Infect Dis 9: 611616.

    • Search Google Scholar
    • Export Citation
  • 10.

    WHO, 2017. Executive Board 141st Session, Geneva, 1 June 2017: Resolutions and Decisions, Annexes, Summary Records. Geneva, Switzerland: World Health Organisation.

    • Search Google Scholar
    • Export Citation
  • 11.

    Kanjanabuch T, Kittikowit W, Eiam-Ong S, 2009. An update on acute postinfectious glomerulonephritis worldwide. Nat Rev Nephrol 5: 259269.

  • 12.

    Marshall CS, Cheng AC, Markey PG, Towers RJ, Richardson LJ, Fagan PK, Scott L, Krause VL, Currie BJ, 2011. Acute post-streptococcal glomerulonephritis in the Northern Territory of Australia: a review of 16 years data and comparison with the literature. Am J Trop Med Hyg 85: 703710.

    • Search Google Scholar
    • Export Citation
  • 13.

    Speers DJ, Levy A, Gichamo A, Eastwood A, Leung MJ, 2017. M protein gene (emm type) analysis of group A Streptococcus isolates recovered during an acute glomerulonephritis outbreak in northern Western Australia. Pathology 49: 765769.

    • Search Google Scholar
    • Export Citation
  • 14.

    Hoy WE, White AV, Dowling A, Sharma SK, Bloomfield H, Tipiloura BT, Swanson CE, Mathews JD, McCredie DA, 2012. Post-streptococcal glomerulonephritis is a strong risk factor for chronic kidney disease in later life. Kidney Int 81: 10261032.

    • Search Google Scholar
    • Export Citation
  • 15.

    Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D, 2009. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6: e1000100.

    • Search Google Scholar
    • Export Citation
  • 16.

    Anthony B, Kaplan E, Chapman SS, Quie P, Wannamaker L, 1967. Epidemic acute nephritis with reappearance of type-49 Streptococcus. Lancet 290: 787790.

    • Search Google Scholar
    • Export Citation
  • 17.

    Facklam R 1999. emm typing and validation of provisional M types for group A streptococci. Emerg Infect Dis 5: 247253.

  • 18.

    Simpson EH, 1949. Measurement of diversity. Nature 163: 688.

  • 19.

    Grundmann H, Hori S, Tanner G, 2001. Determining confidence intervals when measuring genetic diversity and the discriminatory abilities of typing methods for microorganisms. J Clin Microbiol 39: 41904192.

    • Search Google Scholar
    • Export Citation
  • 20.

    Anthony BF, Perlman LV, Wannamaker LW, 1967. Skin infections and acute nephritis in American Indian children. Pediatrics 39: 263279.

  • 21.

    Tayeb SH, Nasr EM, Attallah AS, 1978. Streptococcal impetigo and acute glomerulonephritis in children in Cairo. Br J Dermatol 98: 53.

  • 22.

    Rodríguez-Iturbe B, Rubio L, García R, 1981. Attack rate of poststreptococcal nephritis in families: a prospective study. Lancet 317: 401403.

    • Search Google Scholar
    • Export Citation
  • 23.

    Majeed H, Yousof A, Rotta J, Havlickpva H, Bahar G, Bahbahani K, 1992. Group A streptococcal strains in Kuwait: a nine-year prospective study of prevalence and associations. Pediatr Infect Dis J 11: 295299.

    • Search Google Scholar
    • Export Citation
  • 24.

    Gaworzewska E, Colman G, 1988. Changes in the pattern of infection caused by Streptococcus pyogenes. Epidemiol Infect 100: 257269.

  • 25.

    Reid H, Bassett D, Gaworzewska E, Colman G, Poon-King T, 1990. Streptococcal serotypes newly associated with epidemic post-streptococcal acute glomerulonephritis. J Med Microbiol 32: 111114.

    • Search Google Scholar
    • Export Citation
  • 26.

    Tewodros W, Kronvall G, 2005. M protein gene (emm type) analysis of group A beta-hemolytic streptococci from Ethiopia reveals unique patterns. J Clin Microbiol 43: 43694376.

    • Search Google Scholar
    • Export Citation
  • 27.

    Mori K, Ito Y, Kamikawaji N, Sasazuki T, 1997. Elevated IgG titer against the C region of streptococcal M protein and its immunodeterminants in patients with poststreptococcal acute glomerulonephritis. J Pediatr 131: 293299.

    • Search Google Scholar
    • Export Citation
  • 28.

    Masayuma T 1996. Outbreak of acute glomerulonephritis in children: observed association with the T1 subtype of group A streptococcal infection in northern Kyushu, Japan. Pediatr Int 38: 128131.

    • Search Google Scholar
    • Export Citation
  • 29.

    Zheng MH 2009. Genetic analysis of group A Streptococcus isolates recovered during acute glomerulonephritis outbreaks in Guizhou province of China. J Clin Microbiol 47: 715720.

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Author Notes

Address correspondence to Mark R. Davies, Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne, 792 Elizabeth Street, Melbourne, Victoria, 3000, Australia. E-mail: mark.davies1@unimelb.edu.au

Financial support: This work was supported by Australian National Health and Medical Research Council (NHMRC) project grants (#1098319 and #1130455). S. Y. C. T. is supported by a NHMRC Career Development Fellowship (#1145033).

Authors’ addresses: Kate A. Worthing, Liam McIntyre, and Mark R. Davies, Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Victoria, Australia, E-mails: kate.worthing@unimelb.edu.au, liam.mcintyre@unimelb.edu.au, and mark.davies1@unimelb.edu.au. Jake A. Lacey, Department of Doherty at the Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Victoria, Australia, E-mail: jake.lacey@unimelb.edu.au. David J. Price, Victorian Infectious Diseases Reference Laboratory Epidemiology Unit, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Victoria, Australia, and University of Melbourne, Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, Melbourne, Victoria, Australia, E-mail: david.price1@unimelb.edu.au. Andrew C. Steer, Murdoch Children’s Research Institute, Tropical Diseases Research Group, Melbourne, Victoria, Australia, E-mail: andrew.steer@rch.org.au. Steven Y. C. Tong, The Peter Doherty Institute for Infection and Immunity, Victorian Infectious Disease Service, The Royal Melbourne Hospital, and Doherty Department University of Melbourne, Melbourne, Victoria, Australia, and Menzies School of Health Research, Darwin, Australia, E-mail: steven.tong@mh.org.au.

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