Invasive streptococcal group A infection in children: а review of the literature and a clinical case of the toxic shock syndrome and complicated community-acquired pneumonia in a child with lung malformation

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Abstract

Streptococcal group A  infection (SGAI) remains an important cause of morbidity and mortality in children. In the recent years, the spread of new highly virulent strains of Streptococcus pyogenes, capable of producing cytolysins and pyrogenic exotoxins (superantigens) has led to an increase in the number of severe forms of diseases with high mortality rates. Invasive infection can occur as necrotizing fasciitis, myositis, sepsis, toxic shock syndrome, scarlet fever, meningitis, myocarditis, and pneumonia. A variety of symptoms in patients with tonsillitis without purulent depositions or after a blunt trauma of soft tissues, such as vomiting, diarrhea, and abdominal pain, can mimic other diseases. The toxic shock syndrome with circulatory collapse, hypotension, acute renal failure, and coagulopathy may develop rapidly and be fatal if not recognized on time or if treated inadequately. Time-sensitive combined antimicrobial therapy and adequate fluid administration, before the bacteriological results are obtained, are important components of any successful treatment. The review describes the current epidemiological situation, diagnostic criteria and treatment strategies for invasive SGAI with an emphasis on the toxic shock syndrome. We present our own observation of SGAI in a 5-year-old child with tonsillitis without purulent depositions, with abdominal pain, typical erythematous rash with desquamation at typical time intervals, and a toxic shock syndrome and pneumonia complicated by pleuritis and pneumohydorotorax. The complications and duration of pneumonia were related to lung malformation (adenomatous cystic type 1 malformation of the lungs), which was newly detected at the time of the disease.

Conclusion: Due to global spread of SGAI, doctors should be alert to its severe manifestations.

About the authors

E. R. Meskina

Moscow Regional Research and Clinical Institute (MONIKI)

Author for correspondence.
Email: meskinaelena@rambler.ru

Elena R. Meskina – MD, PhD, Head of Сhildren's Infectious Disease Department.

61/2 Shchepkina ul., Moscow, 129110, tel.: +7 (916) 121 61 72

Russian Federation

M. K. Khadisova

Moscow Regional Research and Clinical Institute (MONIKI)

Email: murzabekova.marina.1979@mail.ru

Marima K. Khadisova – MD, PhD, Research Fellow, Сhildren's Infectious Disease Department.

61/2 Shchepkina ul., Moscow, 129110, tel.: +7 (926) 264 93 30

Russian Federation

References

  1. Покровский ВИ, Брико НИ, Клейменов ДА. Распространенность и клинико-эпидемиологическая характеристика заболеваний, вызываемых стрептококками группы А в России. Терапевтический архив. 2009;81(11): 5–9.
  2. Stevens DL, Bryant AE. Severe Group A Streptococcal Infections. In: Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: Basic Biology to Clinical Manifestations [Internet]. Oklahoma City (OK): University of Oklahoma Health Sciences Center; 2016. Available from: https://www.ncbi.nlm.nih.gov/books/ NBK333425/ (Accessed 20 January 2018).
  3. Краснова ЕИ. Стрептококковая инфекция. Клинико-диагностические и лечебно-профилактические аспекты. Новосибирск: Сибмедиздат НГМУ; 2015. 160 с.
  4. Chang K, Frankovich J, Cooperstock M, Cunningham MW, Latimer ME, Murphy TK, Pasternack M, Thienemann M, Williams K, Walter J, Swedo SE; PANS Collaborative Consortium. Clinical evaluation of youth with pediatric acute-onset neuropsychiatric syndrome (PANS): recommendations from the 2013 PANS Consensus Conference. J Child Adolesc Psychopharmacol. 2015;25(1): 3–13. doi: 10.1089/cap.2014.0084.
  5. Shaikh N, Leonard E, Martin JM. Prevalence of streptococcal pharyngitis and streptococcal carriage in children: a meta-analysis. Pediatrics. 2010;126(3):e557–64. doi: 10.1542/peds.20092648.
  6. Otlu B, Karakurt C, Bayındır Y, Kayabaş Ü, Yakupoğulları Y, Gözükara Bağ H. Carriage of Streptococcus pyogenes in primary school children: M-protein types, pyrogenic toxin genes, and investigation of the clonal relationships between the isolates. Mikrobiyol Bul. 2015;49(3): 301–13. doi: 10.5578/mb.9311.
  7. Centers for Disease Control and Prevention. 2015. Active Bacterial Core Surveillance Report, Emerging Infections Program Network, Group A Streptococcus, 2015 [Internet]. Available from: https://www.cdc.gov/abcs/reports-findings/survreports/gas15.html (Accessed 20 January 2018).
  8. Ross A, Shoff HW. Toxic Shock Syndrome [Updated 2017 Oct 6]. In: StatPearls [Internet]. Treasure Island (FL): Stat Pearls Publishing; 2017. Available from: https://www.ncbi.nlm.nih.gov/books/NBK459345/(Accessed 20 January 2018).
  9. Efstratiou A, Lamagni T. Epidemiology of Streptococcus pyogenes. 2016 Feb 10 [Updated 2017 Apr 3]. In: Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: Basic Biology to Clinical Manifestations [Internet]. Oklahoma City (OK): University of Oklahoma Health Sciences Center; 2016. Available from: https://www.ncbi.nlm.nih.gov/books/ NBK343616/ (Accessed 20 January 2018).
  10. Loubinoux J, Plainvert C, Collobert G, Touak G, Bouvet A, Poyart C; CNR-Strep Network. Adult invasive and noninvasive infections due to Streptococcus dysgalactiae subsp. equisimilis in France from 2006 to 2010. J Clin Microbiol. 2013;51(8): 2724–7. doi: 10.1128/JCM.0126213.
  11. Oppegaard O, Mylvaganam H, Kittang BR. Beta-haemolytic group A, C and G streptococcal infections in Western Norway: a 15-year retrospective survey. Clin Microbiol Infect. 2015;21(2): 171–8. doi: 10.1016/j.cmi.2014.08.019.
  12. Spaulding AR, Salgado-Pabón W, Kohler PL, Horswill AR, Leung DY, Schlievert PM. Staphylococcal and streptococcal superantigen exotoxins. Clin Microbiol Rev. 2013;26(3): 422–47. doi: 10.1128/CMR.00104-12.
  13. Lamagni TL, Darenberg J, Luca-Harari B, Siljander T, Efstratiou A, Henriques-Normark B, Vuopio-Varkila J, Bouvet A, Creti R, Ekelund K, Koliou M, Reinert RR, Stathi A, Strakova L, Ungureanu V, Schalén C; Strep-EURO Study Group, Jasir A. Epidemiology of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol. 2008;46(7): 2359–67. doi: 10.1128/JCM.0042208.
  14. Darenberg J, Henriques-Normark B, Lepp T, Tegmark-Wisell K, Tegnell A, Widgren K. Increased incidence of invasive group A streptococcal infections in Sweden, January 2012 – February 2013. Euro Surveill. 2013;18(14): 20443. doi: 10.2807/1560-7917.ES2013.18.14.20443.
  15. Imöhl M, Fitzner C, Perniciaro S, van der Linden M. Epidemiology and distribution of 10 superantigens among invasive Streptococcus pyogenes disease in Germany from 2009 to 2014. PLoS One. 2017;12(7):e0180757. doi: 10.1371/journal.pone.0180757.
  16. Seale AC, Davies MR, Anampiu K, Morpeth SC, Nyongesa S, Mwarumba S, Smeesters PR, Efstratiou A, Karugutu R, Mturi N, Williams TN, Scott JA, Kariuki S, Dougan G, Berkley JA. Invasive Group A Streptococcus Infection among Children, Rural Kenya. Emerg Infect Dis. 2016;22(2): 224–32. doi: 10.3201/eid2202.151358.
  17. Nasser W, Beres SB, Olsen RJ, Dean MA, Rice KA, Long SW, Kristinsson KG, Gottfredsson M, Vuopio J, Raisanen K, Caugant DA, Steinbakk M, Low DE, McGeer A, Darenberg J, Henriques-Normark B, Van Beneden CA, Hoffmann S, Musser JM. Evolutionary pathway to increased virulence and epidemic group A Streptococcus disease derived from 3,615 genome sequences. Proc Natl Acad Sci U S A. 2014;111(17):E1768– 76. doi: 10.1073/pnas.1403138111.
  18. Zhu L, Olsen RJ, Nasser W, de la Riva Morales I, Musser JM. Trading capsule for increased cytotoxin production: contribution to virulence of a newly emerged clade of emm89 Streptococcus pyogenes. MBio. 2015;6(5):e01378–15. doi: 10.1128/mBio.01378-15.
  19. Zhu L, Olsen RJ, Nasser W, Beres SB, Vuopio J, Kristinsson KG, Gottfredsson M, Porter AR, DeLeo FR, Musser JM. A molecular trigger for intercontinental epidemics of group A Streptococcus. J Clin Invest. 2015;125(9): 3545–59. doi: 10.1172/JCI82478.
  20. Proft T, Fraser JD. Streptococcal Superantigens: Biological properties and potential role in disease. In: Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: Basic Biology to Clinical Manifestations [Internet]. Oklahoma City (OK): University of Oklahoma Health Sciences Center; 2016. Available from: https://www.ncbi.nlm.nih.gov/books/NBK333435/ (Accessed 20 January 2018).
  21. Ramachandran G, Tulapurkar ME, Harris KM, Arad G, Shirvan A, Shemesh R, Detolla LJ, Benazzi C, Opal SM, Kaempfer R, Cross AS. A peptide antagonist of CD28 signaling attenuates toxic shock and necrotizing soft-tissue infection induced by Streptococcus pyogenes. J Infect Dis. 2013;207(12): 1869–77. doi: 10.1093/infdis/jit104.
  22. Shaler CR, Choi J, Rudak PT, Memarnejadian A, Szabo PA, Tun-Abraham ME, Rossjohn J, Corbett AJ, McCluskey J, McCormick JK, Lantz O, Hernandez-Alejandro R, Haeryfar SMM. MAIT cells launch a rapid, robust and distinct hyperinflammatory response to bacterial superantigens and quickly acquire an anergic phenotype that impedes their cognate antimicrobial function: Defining a novel mechanism of superantigen-induced immunopathology and immunosuppression. PLoS Biol. 2017;15(6):e2001930. doi: 10.1371/journal.pbio.2001930.
  23. Us D. Viral superantigens. Mikrobiyol Bul. 2016;50(3): 491–504. doi: 10.5578/mb.24250.
  24. Streptococcal Toxic Shock Syndrome (STSS) (Streptococcus pyogenes) 2010 Case Definition CSTE Position Statement(s) Centers for Disease Control and Prevention. National Notifiable Diseases Surveillance System (NNDSS) [Internet]. Available from: https://wwwn.cdc.gov/nndss/conditions/streptococcal-toxic-shock-syndrome/case-definition/2010/(Accessed 27 January 2018).
  25. Nuwayhid ZB, Aronoff DM, Mulla ZD. Blunt trauma as a risk factor for group A streptococcal necrotizing fasciitis. Ann Epidemiol. 2007;17(11): 878–81. doi: 10.1016/j.annepidem.2007.05.011.
  26. Bryant AE, Bayer CR, Aldape MJ, Stevens DL. The roles of injury and nonsteroidal anti-inflammatory drugs in the development and outcomes of severe group A streptococcal soft tissue infections. Curr Opin Infect Dis. 2015;28(3): 231–9. doi: 10.1097/QCO.0000000000000160.
  27. Kerr DL, Loraas EK, Links AC, Brogan TV, Schmale GA. Toxic shock in children with bone and joint infections: a review of seven years of patients admitted to one intensive care unit. J Child Orthop. 2017;11(5): 387–92. doi: 10.1302/1863-2548.11.170058.
  28. Tapiainen T, Launonen S, Renko M, Saxen H, Salo E, Korppi M, Kainulainen L, Heiskanen-Kosma T, Lindholm L, Vuopio J, Huotari T, Rusanen J, Uhari M. Invasive Group A Streptococcal Infections in Children: A Nationwide Survey in Finland. Pediatr Infect Dis J. 2016;35(2): 123–8. doi: 10.1097/INF.0000000000000945.
  29. Stone K, Tackley E, Weir S. BET 2: NSAIs and chickenpox. Emerg Med J. 2018;35(1): 66–8. doi: 10.1136/emermed-2017-207366.2.
  30. Schlievert PM, Bohach GA. Staphylococcal and streptococcal superantigens: an update. In Kotb M, Fraser JD, editors. Superantigens: molecular basis for their role in human diseases. Washington: ASM Press; 2007. p. 21–36.
  31. Agyeman PKA, Schlapbach LJ, Giannoni E, Stocker M, Posfay-Barbe KM, Heininger U, Schindler M, Korten I, Konetzny G, Niederer-Loher A, Kahlert CR, Donas A, Leone A, Hasters P, Relly C, Baer W, Kuehni CE, Aebi C, Berger C. Epidemiology of blood culture-proven bacterial sepsis in children in Switzerland: a population-based cohort study. Lancet Child Adolesc Health. 2017;1(2): 124–33. doi: 10.1016/S2352-4642(17)30010-X.
  32. Lin JC, Spinella PC, Fitzgerald JC, Tucci M, Bush JL, Nadkarni VM, Thomas NJ, Weiss SL; Sepsis Prevalence, Outcomes, and Therapy Study Investigators. New or progressive multiple organ dysfunction syndrome in pediatric severe sepsis: a sepsis phenotype with higher morbidity and mortality. Pediatr Crit Care Med. 2017;18(1): 8–16. doi: 10.1097/PCC.0000000000000978.
  33. Tilahun AY, Holz M, Wu TT, David CS, Rajagopalan G. Interferon gamma-dependent intestinal pathology contributes to the lethality in bacterial superantigen-induced toxic shock syndrome. PLoS One. 2011;6(2):e16764. doi: 10.1371/journal.pone.0016764.
  34. Tilahun AY, Marietta EV, Wu TT, Patel R, David CS, Rajagopalan G. Human leukocyte antigen class II transgenic mouse model unmasks the significant extrahepatic pathology in toxic shock syndrome. Am J Pathol. 2011;178(6): 2760–73. doi: 10.1016/j.ajpath.2011.02.033.
  35. Stevens DL, Shelly M, Stiller R, Villasenor-Sierra A, Bryant AE. Acute reversible cardiomyopathy in patients with streptococcal toxic shock syndrome. In: Proceedings of the XVII Lancefield International Symposium on Streptococci and Streptococcal Diseases. Porto Heli, Greece, June 2008. Porto Heli: FEMS; 2008. p. 179.
  36. Li Z, Bryant AE, Hamilton SM, Bayer CR, Ma Y, Stevens DL. Do cardiomyocytes mount an immune response to Group A Streptococcus? Cytokine. 2011;54(3): 258–65. doi: 10.1016/j.cyto.2011.02.009.
  37. Kotb M, Norrby-Teglund A, McGeer A, El-Sherbini H, Dorak MT, Khurshid A, Green K, Peeples J, Wade J, Thomson G, Schwartz B, Low DE. An immunogenetic and molecular basis for differences in outcomes of invasive group A streptococcal infections. Nat Med. 2002;8(12): 1398– 404. doi: 10.1038/nm800.
  38. Stevens DL, Bisno AL, Chambers HF, Dellinger EP, Goldstein EJ, Gorbach SL, Hirschmann JV, Kaplan SL, Montoya JG, Wade JC. Practice guidelines for the diagnosis and management of skin and soft tissue infections: 2014 update by the infectious diseases society of America. Clin Infect Dis. 2014;59(2): 147–59. doi: 10.1093/cid/ciu296.
  39. Rhodes A, Evans LE, Alhazzani W, Levy MM, Antonelli M, Ferrer R, Kumar A, Sevransky JE, Sprung CL, Nunnally ME, Rochwerg B, Rubenfeld GD, Angus DC, Annane D, Beale RJ, Bellinghan GJ, Bernard GR, Chiche JD, Coopersmith C, De Backer DP, French CJ, Fujishima S, Gerlach H, Hidalgo JL, Hollenberg SM, Jones AE, Karnad DR, Kleinpell RM, Koh Y, Lisboa TC, Machado FR, Marini JJ, Marshall JC, Mazuski JE, McIntyre LA, McLean AS, Mehta S, Moreno RP, Myburgh J, Navalesi P, Nishida O, Osborn TM, Perner A, Plunkett CM, Ranieri M, Schorr CA, Seckel MA, Seymour CW, Shieh L, Shukri KA, Simpson SQ, Singer M, Thompson BT, Townsend SR, Van der Poll T, Vincent JL, Wiersinga WJ, Zimmerman JL, Dellinger RP. Surviving Sepsis Campaign: International Guidelines for Management of Sepsis and Septic Shock: 2016. Intensive Care Med. 2017;43(3): 304–77. doi: 10.1007/s00134-0174683-6.
  40. Kissoon N. Understanding fluid administration approaches in children with co-morbidities and septic shock. Crit Care. 2017;21(1): 204. doi: 10.1186/s13054-017-1741-y.
  41. Davis AL, Carcillo JA, Aneja RK, Deymann AJ, Lin JC, Nguyen TC, Okhuysen-Cawley RS, Relvas MS, Rozenfeld RA, Skippen PW, Stojadinovic BJ, Williams EA, Yeh TS, Balamuth F, Brierley J, de Caen AR, Cheifetz IM, Choong K, Conway E Jr, Cornell T, Doctor A, Dugas MA, Feldman JD, Fitzgerald JC, Flori HR, Fortenberry JD, Graciano AL, Greenwald BM, Hall MW, Han YY, Hernan LJ, Irazuzta JE, Iselin E, van der Jagt EW, Jeffries HE, Kache S, Katyal C, Kissoon NT, Kon AA, Kutko MC, MacLaren G, Maul T, Mehta R, Odetola F, Parbuoni K, Paul R, Peters MJ, Ranjit S, Reuter-Rice KE, Schnitzler EJ, Scott HF, Torres A Jr, Weingarten-Abrams J, Weiss SL, Zimmerman JJ, Zuckerberg AL. American College of Critical Care Medicine Clinical Practice Parameters for Hemodynamic Support of Pediatric and Neonatal Septic Shock. Crit Care Med. 2017;45(6): 1061–93. doi: 10.1097/CCM.0000000000002425.
  42. Workman JK, Ames SG, Reeder RW, Korgenski EK, Masotti SM, Bratton SL, Larsen GY. Treatment of Pediatric Septic Shock With the Surviving Sepsis Campaign Guidelines and PICU Patient Outcomes. Pediatr Crit Care Med. 2016;17(10):e451–8. doi: 10.1097/PCC.0000000000000906.
  43. Zadroga R, Williams DN, Gottschall R, Hanson K, Nordberg V, Deike M, Kuskowski M, Carlson L, Nicolau DP, Sutherland C, Hansen GT. Comparison of 2 blood culture media shows significant differences in bacterial recovery for patients on antimicrobial therapy. Clin Infect Dis. 2013;56(6): 790–7. doi: 10.1093/cid/cis1021.
  44. Cardoso T, Carneiro AH, Ribeiro O, Teixeira-Pinto A, Costa-Pereira A. Reducing mortality in severe sepsis with the implementation of a core 6-hour bundle: results from the Portuguese community-acquired sepsis study (SACiUCI study). Crit Care. 2010;14(3):R83. doi: 10.1186/cc9008.
  45. Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, Bellomo R, Bernard GR, Chiche JD, Coopersmith CM, Hotchkiss RS, Levy MM, Marshall JC, Martin GS, Opal SM, Rubenfeld GD, van der Poll T, Vincent JL, Angus DC. The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315(8): 801–10. doi: 10.1001/jama.2016.0287.
  46. Discussion and Recommendations for the Application of Procalcitonin to the Evaluation and Management of Suspected Lower Respiratory Tract Infections and Sepsis Gaithersburg, Maryland FDA Executive Summary. Prepared for the November 10, 2016 meeting of the Microbiology Devices Panel of the Medical Devices Advisory Committee [Internet]. Available from: https://www.fda.gov/downloads/AdvisoryCommittees/CommitteesMeetingMaterials/MedicalDevices/MedicalDevicesAdvisoryCommittee/MicrobiologyDevicesPanel/UCM528156.pdf (Accessed 22 February 2018).
  47. Российское респираторное общество. Межрегиональное педиатрическое респираторное общество. Федерация педиатров стран СНГ. Московское общество детских врачей. Внебольничная пневмония у детей. Клинические рекомендации. М.: Оригинал-макет; 2015. 64 с.
  48. Tamayo E, Montes M, Vicente D, Pérez-Trallero E. Streptococcus pyogenes pneumonia in adults: clinical presentation and molecular characterization of isolates 2006–2015. PLoS One. 2016;11(3):e0152640. doi: 10.1371/journal.pone.0152640.
  49. Herrera AL, Huber VC, Chaussee MS. The association between invasive group A streptococcal diseases and viral respiratory tract infections. Front Microbiol. 2016;7:342. doi: 10.3389/fmicb.2016.00342.
  50. Erlichman I, Breuer O, Shoseyov D, Cohen-Cymberknoh M, Koplewitz B, Averbuch D, Erlichman M, Picard E, Kerem E. Complicated community acquired pneumonia in childhood: different types, clinical course, and outcome. Pediatr Pulmonol. 2017;52(2): 247–54. doi: 10.1002/ppul.23523.
  51. Birch C, Gowardman J. Streptococcus pyogenes: a forgotten cause of severe community-acquired pneumonia. Anaesth Intensive Care. 2000;28(1): 87–90.

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