1887

Abstract

Unlike western countries the knowledge of group A streptococcus (GAS) epidemiology in India remains patchy and incomplete. Typing is crucial for surveillance as well as in predicting the efficacy of multivalent M protein vaccine. The present study aimed to explore the types of 206 invasive and non-invasive GAS isolates from South India as well as reviewing all the published literature on GAS molecular epidemiology from India thereby generating a pan-Indian data to predict the conjectural coverage of the 30-valent M-protein vaccine in this population.

typing and superantigen (SAg) profiling of GAS along with reviewing literatures on GAS molecular epidemiology from India.

This study revealed a high diversity of types with 63, 82, 183, 85, 92, 169, 42, 44, 106, 74, 12 being frequently encountered, belonging to twenty clusters. The pan-Indian data on prevalent types further supports our study findings with 135 different types. Six clusters dominated accounting for 80 % of the GAS isolates: E3(26 %), E6(20 %), E2(11 %), E4(10 %), D4(7 %), E1(6 %). No significant association was noted between types and the nature of infection (≥0.05) while a few SAg profiles were significantly associated with certain types. Pan Indian data revealed that only 16 % of the types encountered were included in proposed 30-valent M protein based vaccine.

The coverage among the South Indian GAS isolates was 28.2 % which increased to only 46.6 % with the cross-opsonic effect, thus highlighting the importance of developing a specific multivalent vaccine including the prevalent types in India or considering the use of conserved C-repeat vaccines and non-M protein based vaccines.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001018
2019-07-01
2019-12-12
Loading full text...

Full text loading...

References

  1. Carapetis JR, Steer AC, Mulholland EK, Weber M. The global burden of group A streptococcal diseases. Lancet Infect Dis 2005;5:685–694 [CrossRef]
    [Google Scholar]
  2. Cunningham MW. Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 2000;13:470–511 [CrossRef]
    [Google Scholar]
  3. Brahmadathan NK. Molecular biology of group A Streptococcus and its implications in vaccine strategies. Indian J Med Microbiol 2017;35:176–183 [CrossRef]
    [Google Scholar]
  4. Smeesters PR, Mardulyn P, Vergison A, Leplae R, Van Melderen L. Genetic diversity of group A Streptococcus M protein: implications for typing and vaccine development. Vaccine 2008;26:5835–5842 [CrossRef]
    [Google Scholar]
  5. Beall B, Facklam R, Thompson T. Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J Clin Microbiol 1996;34:953–958
    [Google Scholar]
  6. Smeesters PR, McMillan DJ, Sriprakash KS, Georgousakis MM. Differences among group A Streptococcus epidemiological landscapes: consequences for M protein-based vaccines?. Expert Rev Vaccines 2009;8:1705–1720 [CrossRef]
    [Google Scholar]
  7. Sanderson-Smith M, De Oliveira DMP, Guglielmini J, McMillan DJ, Vu T et al. A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development. J Infect Dis 2014;210:1325–1338 [CrossRef]
    [Google Scholar]
  8. Baroux N, D’Ortenzio E, Amédéo N, Baker C, Ali Alsuwayyid B et al. The emm-cluster typing system for group A Streptococcus identifies epidemiologic similarities across the Pacific region. Clin Infect Dis 2014;59:e84–e92 [CrossRef]
    [Google Scholar]
  9. Maripuu L, Eriksson A, Norgren M. Superantigen gene profile diversity among clinical group A streptococcal isolates. FEMS Immunol Med Microbiol 2008;54:236–244 [CrossRef]
    [Google Scholar]
  10. Liu D, Hollingshead S, Swiatlo E, Lawrence ML, Austin FW. Rapid identification of Streptococcus pyogenes with PCR primers from a putative transcriptional regulator gene. Res Microbiol 2005;156:564–567 [CrossRef]
    [Google Scholar]
  11. Williamson DA, Smeesters PR, Steer AC, Morgan J, Davies M et al. Comparative M-protein analysis of Streptococcus pyogenes from pharyngitis and skin infections in New Zealand: implications for vaccine development. BMC Infect Dis 2016;16: [CrossRef]
    [Google Scholar]
  12. Dale JB, Penfound TA, Chiang EY, Walton WJ. New 30-valent M protein-based vaccine evokes cross-opsonic antibodies against non-vaccine serotypes of group A streptococci. Vaccine 2011;29:8175–8178 [CrossRef]
    [Google Scholar]
  13. Index of /pub/infectious_diseases/biotech/emmsequ/. n.d;ftp://ftp.cdc.gov/pub/infectious_diseases/biotech/tsemm/
  14. Arya DK, Sharma A, Mehta G, Dua M, Johri AK. Molecular epidemiology and virulence characteristics of prevalent group A streptococci recovered from patients in northern India. J Infect Dev Ctries 2014;8:271–281 [CrossRef]
    [Google Scholar]
  15. Balaji K, Thenmozhi R, Prajna L, Dhananjeyan G, Pandian SK. Comparative analysis of emm types, superantigen gene profiles and antibiotic resistance genes among Streptococcus pyogenes isolates from ocular infections, pharyngitis and asymptomatic children in South India. Infect Genet Evol 2013;19:105–112 [CrossRef]
    [Google Scholar]
  16. Chauhan S, Kashyap N, Kanga A, Thakur K, Sood A et al. Genetic diversity among group A streptococcus isolated from throats of healthy and symptomatic children. J Trop Pediatr 2016;62:152–157 [CrossRef]
    [Google Scholar]
  17. Dhanda V, Kumar R, Thakur JS, Chakraborti A. emm type distribution pattern of group A Streptococcus in North India: need for a new preventive approach. Indian J Med Res 2010;132:741–744
    [Google Scholar]
  18. Dhanda V, Vohra H, Kumar R. Group A Streptococcus virulence factors genes in north India & their association with emm type in pharyngitis. Indian J Med Res 2011;133:110–115
    [Google Scholar]
  19. Kumar R, Vohra H, Chakraborty A, Sharma YP, Bandhopadhya S et al. Epidemiology of group A streptococcal pharyngitis & impetigo: a cross-sectional & follow up study in a rural community of northern India. Indian. J Med Res 2009;130:765–771
    [Google Scholar]
  20. Mathur P, Bhardwaj N, Mathur K, Behera B, Gupta G et al. Clinical and molecular epidemiology of beta-hemolytic streptococcal infections in India. J Infect Dev Ctries 2014;8:297–303 [CrossRef]
    [Google Scholar]
  21. Rajkumari R, Jose JM, Brahmadathan KN. Genetic diversity and allelic variation in south Indian isolates of group A streptococci causing invasive disease. Indian J Med Microbiol 2017;35:575–579
    [Google Scholar]
  22. Sagar V, Bergmann R, Nerlich A, McMillan DJ, Nitsche Schmitz DP et al. Variability in the distribution of genes encoding virulence factors and putative extracellular proteins of Streptococcus pyogenes in India, a region with high streptococcal disease burden, and implication for development of a regional multisubunit vaccine. Clin Vaccine Immunol 2012;19:1818–1825 [CrossRef]
    [Google Scholar]
  23. Chiang-Ni C, Zheng PX, Wang SY, Tsai PJ, Chuang WJ et al. Epidemiology analysis of Streptococcus pyogenes in a hospital in Southern Taiwan by use of the updated emm cluster typing system. J Clin Microbiol 2016;54:157–162 [CrossRef]
    [Google Scholar]
  24. Steer AC, Law I, Matatolu L, Beall BW, Carapetis JR. Global emm type distribution of group A streptococci: systematic review and implications for vaccine development. Lancet Infect Dis 2009;9:611–616 [CrossRef]
    [Google Scholar]
  25. Smeesters PR, Dramaix M, Van Melderen L. The emm-type diversity does not always reflect the M protein genetic diversity--is there a case for designer vaccine against GAS. Vaccine 2010;28:883–885 [CrossRef]
    [Google Scholar]
  26. Smeesters PR, Vergison A, Campos D, de Aguiar E, Miendje Deyi VY et al. Differences between Belgian and Brazilian group A Streptococcus epidemiologic landscape. PLoS One 2006;1:e10 [CrossRef]
    [Google Scholar]
  27. Koutouzi F, Tsakris A, Chatzichristou P, Koutouzis E, Daikos GL et al. Streptococcus pyogenes emm types and Clusters during a 7-year period (2007 to 2013) in pharyngeal and Nonpharyngeal Pediatric isolates. J Clin Microbiol 2015;53:2015–2021 [CrossRef]
    [Google Scholar]
  28. Sivagnanam S, Zhou F, Lee AS, O’sullivan MVN. Epidemiology of invasive group A Streptococcus infections in Sydney, Australia. Pathology 2015;47:365–371 [CrossRef]
    [Google Scholar]
  29. Bessen DE, Carapetis JR, Beall B, Katz R, Hibble M et al. Contrasting molecular epidemiology of group A streptococci causing tropical and nontropical infections of the skin and throat. J Infect Dis 2000;182:1109–1116 [CrossRef]
    [Google Scholar]
  30. Espinosa LE, Li Z, Gomez Barreto D, Calderon Jaimes E, Rodriguez RS et al. M protein gene type distribution among group A streptococcal clinical isolates recovered in Mexico City, Mexico, from 1991 to 2000, and Durango, Mexico, from 1998 to 1999: overlap with type distribution within the United States. J Clin Microbiol 2003;41:373–378 [CrossRef]
    [Google Scholar]
  31. Tanaka D, Gyobu Y, Kodama H, Isobe J, Hosorogi S et al. emm typing of group A Streptococcus clinical isolates: identification of dominant types for throat and skin isolates. Microbiol Immunol 2002;46:419–423 [CrossRef]
    [Google Scholar]
  32. Tyrrell GJ, Lovgren M, Forwick B, Hoe NP, Musser JM et al. M types of group A streptococcal isolates submitted to the National centre for Streptococcus (Canada) from 1993 to 1999. J Clin Microbiol 2002;40:4466–4471 [CrossRef]
    [Google Scholar]
  33. Shulman ST, Tanz RR, Dale JB, Beall B, Kabat W et al. Seven-year surveillance of North American pediatric group A streptococcal pharyngitis isolates. Clin Infect Dis 2009;49:78–84 [CrossRef]
    [Google Scholar]
  34. Alfaresi MS. Group A streptococcal genotypes from throat and skin isolates in the United Arab Emirates. BMC Res Notes 2010;3:94 [CrossRef]
    [Google Scholar]
  35. Devi U, Borah PK, Malik V, Parida P, Mahanta J. M types & toxin gene profile of group A streptococci isolated from children in Dibrugarh district of Assam, India. Indian J Med Res 2016;143:659–662
    [Google Scholar]
  36. Dey N, McMillan DJ, Yarwood PJ, Joshi RM, Kumar R et al. High diversity of group A streptococcal emm types in an Indian community: the need to tailor multivalent vaccines. Clin Infect Dis 2005;40:46–51 [CrossRef]
    [Google Scholar]
  37. Menon T, Lloyd C, Malathy B, Sakota V, Jackson D et al. emm type diversity of beta-haemolytic streptococci recovered in Chennai, India. J Med Microbiol 2008;57:540–542 [CrossRef]
    [Google Scholar]
  38. Ray D, Saha S, Sinha S, Pal NK, Bhattacharya B. Molecular characterization and evaluation of the emerging antibiotic-resistant Streptococcus pyogenes from Eastern India. BMC Infect Dis 2016;16: [CrossRef]
    [Google Scholar]
  39. Sagar V, Kumar R, Ganguly NK, Chakraborti A. Comparative analysis of emm type pattern of group A Streptococcus throat and skin isolates from India and their association with closely related SIC, a streptococcal virulence factor. BMC Microbiol 2008;8:150 [CrossRef]
    [Google Scholar]
  40. Sindhulina C, Geethalakshmi S, Thenmozhivalli PR, Jose JM, Brahmadathan KN. Bacteriological and molecular studies of group A streptococcal pharyngitis in a South Indian hospital. Indian J Med Microbiol 2008;26:197 [CrossRef]
    [Google Scholar]
  41. Sagar V, Bakshi DK, Nandi S, Ganguly NK, Kumar R et al. Molecular heterogeneity among North Indian isolates of group A Streptococcus. Lett Appl Microbiol 2004;39:84–88 [CrossRef]
    [Google Scholar]
  42. Haggar A, Nerlich A, Kumar R, Abraham VJ, Brahmadathan KN et al. Clinical and microbiologic characteristics of invasive Streptococcus pyogenes infections in North and South India. J Clin Microbiol 2012;50:1626–1631 [CrossRef]
    [Google Scholar]
  43. Shulman ST, Tanz RR, Dale JB, Steer AC, Smeesters PR. Added value of the emm-cluster typing system to analyze group A Streptococcus epidemiology in high-income settings. Clin Infect Dis 2014;59:1651–1652 [CrossRef]
    [Google Scholar]
  44. Bidet P, Liguori S, Plainvert C, Bonacorsi S, Courroux C et al. Identification of group A streptococcal emm types commonly associated with invasive infections and antimicrobial resistance by the use of multiplex PCR and high-resolution melting analysis. Eur J Clin Microbiol Infect Dis 2012;31:2817–2826 [CrossRef]
    [Google Scholar]
  45. Darenberg J, Luca-Harari B, Jasir A, Sandgren A, Pettersson H et al. Molecular and clinical characteristics of invasive group A streptococcal infection in Sweden. Clin Infect Dis 2007;45:450–458 [CrossRef]
    [Google Scholar]
  46. Naseer U, Steinbakk M, Blystad H, Caugant DA. Epidemiology of invasive group A streptococcal infections in Norway 2010–2014: a retrospective cohort study. Eur J Clin Microbiol Infect Dis 2016;35:1639–1648 [CrossRef]
    [Google Scholar]
  47. Berman HF, Tartof SY, Reis JN, Reis MG, Riley LW. Distribution of superantigens in group A streptococcal isolates from Salvador, Brazil. BMC Infect Dis 2014;14:294 [CrossRef]
    [Google Scholar]
  48. Commons RJ, Smeesters PR, Proft T, Fraser JD, Robins-Browne R et al. Streptococcal superantigens: categorization and clinical associations. Trends Mol Med 2014;20:48–62 [CrossRef]
    [Google Scholar]
  49. Friães A, Pinto FR, Silva-Costa C, Ramirez M, Melo-Cristino J. Superantigen gene complement of Streptococcus pyogenes—relationship with other typing methods and short-term stability. Eur J Clin Microbiol Infect Dis 2013;32:115–125 [CrossRef]
    [Google Scholar]
  50. Rivera A, Rebollo M, Miró E, Mateo M, Navarro F et al. Superantigen gene profile, emm type and antibiotic resistance genes among group A streptococcal isolates from Barcelona, Spain. J Med Microbiol 2006;55:1115–1123 [CrossRef]
    [Google Scholar]
  51. Anand TD, Rajesh T, Rajendhran J, Gunasekaran P. Superantigen profiles of emm and emm-like typeable and nontypeable pharyngeal streptococcal isolates of South India. Ann Clin Microbiol Antimicrob 2012;11:3 [CrossRef]
    [Google Scholar]
  52. Dale JB, Penfound TA, Tamboura B, Sow SO, Nataro JP et al. Potential coverage of a multivalent M protein-based group A streptococcal vaccine. Vaccine 2013;31:1576–1581 [CrossRef]
    [Google Scholar]
  53. Engel ME, Muhamed B, Whitelaw AC, Musvosvi M, Mayosi BM et al. Group A streptococcal emm type prevalence among symptomatic children in Cape town and potential vaccine coverage. Pediatr Infect Dis J 2014;33:208–210 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001018
Loading
/content/journal/jmm/10.1099/jmm.0.001018
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error