Skip to main content

Advertisement

Log in

Coinfection in acute gastroenteritis predicts a more severe clinical course in children

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

The objectives of this study were to determine the incidence of enteric pathogens causing acute gastroenteritis (AGE) among hospitalized children in a large Italian hospital, to measure the incidence of coinfections, and to compare the clinical characteristics of those infected with one versus multiple agents. A prospective study was conducted from March 2010 to April 2011 at the Bambino Gesù Pediatric Hospital in Rome, Italy. All patients between 1 month and 16 years of age admitted to the Pediatric Department with a diagnosis of AGE were eligible for enrollment. Two stool samples for each patient were tested for gastrointestinal pathogens. We summarized the clinical severity of episodes, describing the duration of diarrhea, duration and frequency of vomiting, fever, and severity of dehydration. All the patients underwent medical evaluation with estimation of dehydration. One or more etiological agents were detected in 151 out of 232 patients (65.1 %), while we did not detect any etiological agent in 81 (34.9 %). Rotavirus was detected in 96 (63.6 %), adenovirus in 17 (11.2 %), norovirus in 7 (4.6 %), toxin-producing Clostridium difficile in 23 (15.2 %), Salmonella spp. in 15 (9.9 %, B group in 12/15 and D group in 3/15), C. perfringens in 12 (7.9 %), Campylobacter spp. in 6 (4 %), and verotoxigenic Escherichia coli (VTEC) in 2 (1.3 %). In 27 children out of 151 (17.9 %), we found evidence of coinfection. Coinfection with rotavirus and toxin-producing C. difficile was the most common (63 %). Children with coinfection had a more severe clinical presentation and had a higher probability to be severely dehydrated, independently of age and living community type.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Kosek M, Bern C, Guerrant RL (2003) The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81:197–204

    PubMed  Google Scholar 

  2. Parashar UD, Gibson CJ, Bresee JS, Glass RI (2006) Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12:304–306

    Article  PubMed  Google Scholar 

  3. Marie-Cardine A, Gourlain K, Mouterde O, Castignolles N, Hellot MF, Mallet E, Buffet-Janvresse C (2002) Epidemiology of acute viral gastroenteritis in children hospitalized in Rouen, France. Clin Infect Dis 34:1170–1178

    Article  PubMed  Google Scholar 

  4. Román E, Wilhelmi I, Colomina J, Villar J, Cilleruelo ML, Nebreda V, Del Alamo M, Sánchez-Fauquier A (2003) Acute viral gastroenteritis: proportion and clinical relevance of multiple infections in Spanish children. J Med Microbiol 52:435–440

    Article  PubMed  Google Scholar 

  5. Levidiotou S, Gartzonika C, Papaventsis D, Christaki C, Priavali E, Zotos N, Kapsali E, Vrioni G (2009) Viral agents of acute gastroenteritis in hospitalized children in Greece. Clin Microbiol Infect 15:596–598

    Article  PubMed  CAS  Google Scholar 

  6. Guerrero ML, Noel JS, Mitchell DK, Calva JJ, Morrow AL, Martínez J, Rosales G, Velázquez FR, Monroe SS, Glass RI, Pickering LK, Ruiz-Palacios GM (1998) A prospective study of astrovirus diarrhea of infancy in Mexico City. Pediatr Infect Dis J 17:723–727

    Article  PubMed  CAS  Google Scholar 

  7. Simpson R, Aliyu S, Iturriza-Gómara M, Desselberger U, Gray J (2003) Infantile viral gastroenteritis: on the way to closing the diagnostic gap. J Med Virol 70:258–262

    Article  PubMed  CAS  Google Scholar 

  8. Tran A, Talmud D, Lejeune B, Jovenin N, Renois F, Payan C, Leveque N, Andreoletti L (2010) Prevalence of rotavirus, adenovirus, norovirus, and astrovirus infections and coinfections among hospitalized children in northern France. J Clin Microbiol 48:1943–1946

    Article  PubMed  Google Scholar 

  9. Dionisi AM, Filetici E, Ocwzarek S, Arena S, Benedetti I, Lucarelli C, Luzzi I, Scavia G, Minelli F, Ciaravino G, Marziano ML, Caprioli A (2011) Enter-net international surveillance network. Report 2007–2009. Not Ist Super Sanitá 24:3–10

    Google Scholar 

  10. Ruggeri FM, Delogu R, Petouchoff T, Tcheremenskaia O, De Petris S, Fiore L; RotaNet-Italy Study Group (2011) Molecular characterization of rotavirus strains from children with diarrhea in Italy, 2007–2009. J Med Virol 83:1657–1668

    Article  PubMed  CAS  Google Scholar 

  11. Scavia G, Baldinelli F, Busani L, Caprioli A (2012) The burden of self-reported acute gastrointestinal illness in Italy: a retrospective survey, 2008–2009. Epidemiol Infect 140:1193–1206

    Article  PubMed  CAS  Google Scholar 

  12. Medici MC, Tummolo F, Albonetti V, Abelli LA, Chezzi C, Calderaro A (2012) Molecular detection and epidemiology of astrovirus, bocavirus, and sapovirus in Italian children admitted to hospital with acute gastroenteritis, 2008–2009. J Med Virol 84:643–650

    Article  PubMed  Google Scholar 

  13. Guarino A, Albano F, Ashkenazi S, Gendrel D, Hoekstra JH, Shamir R, Szajewska H; European Society for Paediatric Gastroenterology, Hepatology, and Nutrition; European Society for Paediatric Infectious Diseases (2008) European Society for Paediatric Gastroenterology, Hepatology, and Nutrition/European Society for Paediatric Infectious Diseases evidence-based guidelines for the management of acute gastroenteritis in children in Europe. J Pediatr Gastroenterol Nutr 46:S81–S122

    Article  PubMed  Google Scholar 

  14. Gorelick MH, Shaw KN, Murphy KO (1997) Validity and reliability of clinical signs in the diagnosis of dehydration in children. Pediatrics 99:E6

    Article  PubMed  CAS  Google Scholar 

  15. Giaquinto C, van Damme P; REVEAL Study Group (2010) Age distribution of paediatric rotavirus gastroenteritis cases in Europe: the REVEAL study. Scand J Infect Dis 42:142–147

    Article  PubMed  Google Scholar 

  16. Forster J, Guarino A, Parez N, Moraga F, Román E, Mory O, Tozzi AE, de Aguileta AL, Wahn U, Graham C, Berner R, Ninan T, Barberousse C, Meyer N, Soriano-Gabarró M; and the Rotavirus Study Group (2009) Hospital-based surveillance to estimate the burden of rotavirus gastroenteritis among European children younger than 5 years of age. Pediatrics 123:e393–e400

    Article  PubMed  Google Scholar 

  17. Finamore E, Vitiello M, Kampanaraki A, Rao M, Galdiero M, Galdiero E, Bevilacqua P, Gallo MA, Galdiero M (2011) G2 as an emerging rotavirus strain in pediatric gastroenteritis in southern Italy. Infection 39:113–119

    Article  PubMed  CAS  Google Scholar 

  18. Rosenfeldt V, Vesikari T, Pang XL, Zeng SQ, Tvede M, Paerregaard A (2005) Viral etiology and incidence of acute gastroenteritis in young children attending day-care centers. Pediatr Infect Dis J 24:962–965

    Article  PubMed  Google Scholar 

  19. Nitiema LW, Nordgren J, Ouermi D, Dianou D, Traore AS, Svensson L, Simpore J (2011) Burden of rotavirus and other enteropathogens among children with diarrhea in Burkina Faso. Int J Infect Dis 15:e646–e652

    Article  PubMed  Google Scholar 

  20. Rosenfeldt V, Vesikari T, Pang XL, Zeng SQ, Tvede M, Paerregaard A (2005) Viral etiology and incidence of acute gastroenteritis in young children attending day-care centers. Pediatr Infect Dis J 24:962–965

    Article  PubMed  Google Scholar 

  21. Junquera CG, de Baranda CS, Mialdea OG, Serrano EB, Sánchez-Fauquier A (2009) Prevalence and clinical characteristics of norovirus gastroenteritis among hospitalized children in Spain. Pediatr Infect Dis J 28:604–607

    Article  PubMed  Google Scholar 

  22. Gonzalez-Galan V, Sánchez-Fauqier A, Obando I, Montero V, Fernandez M, Torres MJ, Neth O, Aznar-Martin J (2011) High prevalence of community-acquired norovirus gastroenteritis among hospitalized children: a prospective study. Clin Microbiol Infect 17:1895–1899

    Article  PubMed  CAS  Google Scholar 

  23. Yori PP, Schwab K, Gilman RH, Nappier S, Portocarrero DV, Black RE, Olortegui MP, Hall ER, Moe C, Leon J, Cama VA, Kosek M (2009) Norovirus highly prevalent cause of endemic acute diarrhea in children in the Peruvian Amazon. Pediatric Infect Dis J 28:844–847

    Article  Google Scholar 

  24. Giaquinto C, Jackson AE, Vesikari T (2012) Report of the second European expert meeting on rotavirus vaccination. Vaccine 30:2237–2244

    Article  PubMed  Google Scholar 

  25. Enoch DA, Butler MJ, Pai S, Aliyu SH, Karas JA (2011) Clostridium difficile in children: colonisation and disease. J Infect 63:105–113

    Article  PubMed  Google Scholar 

  26. Benson L, Song X, Campos J, Singh N (2007) Changing epidemiology of Clostridium difficile-associated disease in children. Infect Control Hosp Epidemiol 28:1233–1235

    Article  PubMed  Google Scholar 

  27. Zilberberg MD, Shorr AF, Kollef MH (2008) Increase in Clostridium difficile-related hospitalizations among infants in the United States, 2000–2005. Pediatr Infect Dis J 27:1111–1113

    Article  PubMed  Google Scholar 

  28. Bagci S, Eis-Hübinger AM, Franz AR, Bierbaum G, Heep A, Schildgen O, Bartmann P, Kupfer B, Mueller A (2008) Detection of astrovirus in premature infants with necrotizing enterocolitis. Pediatr Infect Dis J 27:347–350

    Article  PubMed  Google Scholar 

  29. Hunter CJ, Upperman JS, Ford HR, Camerini V (2008) Understanding the susceptibility of the premature infant to necrotizing enterocolitis (NEC). Pediatr Res 63:117–123

    Article  PubMed  Google Scholar 

  30. Kim J, Shaklee JF, Smathers S, Prasad P, Asti L, Zoltanski J, Dul M, Nerandzic M, Coffin SE, Toltzis P, Zaoutis T (2012) Risk factors and outcomes associated with severe Clostridium difficile infection in children. Pediatr Infect Dis J 31:134–138

    Article  PubMed  Google Scholar 

  31. Lukkarinen H, Eerola E, Ruohola A, Vainionpää R, Jalava J, Kotila S, Ruuskanen O (2009) Clostridium difficile ribotype 027-associated disease in children with norovirus infection. Pediatr Infect Dis J 28:847–848

    Article  PubMed  Google Scholar 

  32. Koh H, Baek SY, Shin JI, Chung KS, Jee YM (2008) Coinfection of viral agents in Korean children with acute watery diarrhea. J Korean Med Sci 23:937–940

    Article  PubMed  Google Scholar 

  33. Di Biase AM, Petrone G, Conte MP, Seganti L, Ammendolia MG, Tinari A, Iosi F, Marchetti M, Superti F (2000) Infection of human enterocyte-like cells with rotavirus enhances invasiveness of Yersinia enterocolitica and Y. pseudotuberculosis. J Med Microbiol 49:897–904

    PubMed  Google Scholar 

  34. Taylor MB, Marx FE, Grabow WO (1997) Rotavirus, astrovirus and adenovirus associated with an outbreak of gastroenteritis in a South African child care centre. Epidemiol Infect 119:227–230

    Article  PubMed  CAS  Google Scholar 

  35. Smith CK, McNeal MM, Meyer NR, Haase S, Dekker CL (2011) Rotavirus shedding in premature infants following first immunization. Vaccine 29:8141–8146

    Article  PubMed  CAS  Google Scholar 

  36. Wilhelmi I, Colomina J, Martín-Rodrigo D, Roman E, Sánchez-Fauquier A (2001) New immunochromatographic method for rapid detection of rotaviruses in stool samples compared with standard enzyme immunoassay and latex agglutination techniques. Eur J Clin Microbiol Infect Dis 20:741–743

    Article  PubMed  CAS  Google Scholar 

  37. Ouermi D, Karou D, Ilboudo D, Nadembega WMC, Pietra V, Belem A, Simpore J, Kabre G, Pignatelli S, Sawadogo L (2007) Prevalence of rotavirus, adenovirus and enteric parasites among pediatric patients attending Saint Camille Medical Centre in Ouagadougou. Pak J Biol Sci 10:4266–4270

    Article  Google Scholar 

  38. Viehoff R, Van Beers D, De Foor M, Col D, Venuti M, Paulart F, Leclipteux Th (1998) Comparison of a rapid immunochromatographic diagnostic test for Adenovirus detection. In: Proceedings of the 1998 European Society for Clinical Virology meeting: Progress in Clinical Virology IV, Hamburg, Germany, August/September 1998

  39. Battaglioli G, Nazarian EJ, Lamson D, Musser KA, St George K (2012) Evaluation of the RIDAQuick norovirus immunochromatographic test kit. J Clin Virol 53:262–264

    Article  PubMed  CAS  Google Scholar 

Download references

Competing interests

The authors declare that they have no competing interests.

Author contributions

All authors read and approved the final manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Valentini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valentini, D., Vittucci, A.C., Grandin, A. et al. Coinfection in acute gastroenteritis predicts a more severe clinical course in children. Eur J Clin Microbiol Infect Dis 32, 909–915 (2013). https://doi.org/10.1007/s10096-013-1825-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-013-1825-9

Keywords

Navigation