Etiology of acute gastroenteritis in children requiring hospitalization in the Netherlands

  • I. H. M. Friesema
  • R. F. de Boer
  • E. Duizer
  • L. M. Kortbeek
  • D. W. Notermans
  • O. F. Norbruis
  • D. D. L. Bezemer
  • H. van Heerbeek
  • R. N. J. van Andel
  • J. G. van Enk
  • P. L. A. Fraaij
  • M. P. G. Koopmans
  • A. M. D. Kooistra-Smid
  • Y. T. H. P. van Duynhoven
Article

Abstract

Infectious gastroenteritis causes a considerable burden of disease worldwide. Costs due to gastroenteritis are dominated by the hospitalized cases. Effective control of gastroenteritis should be targeted at the diseases with the highest burden and costs. For that, an accurate understanding of the relative importance of the different bacterial, viral, and parasitic pathogens is needed. The objective of the present study was to determine the incidence and etiology of gastroenteritis requiring hospital admission in the Netherlands. Six hospitals enrolled patients admitted with gastroenteritis for approximately one year over the period May 2008 to November 2009. Participants provided questionnaires and a fecal sample, and the hospital filled out a clinical questionnaire. In total, 143 children hospitalized for gastroenteritis and 64 matched controls were included in the study. Overall incidence of gastroenteritis requiring hospitalization was estimated at 2.92 per 1,000 children aged 0–17 years per year, with the highest incidence in children under the age of 5 years. The full diagnostic panel of pathogens could be studied in fecal samples of 96 cases. One or more pathogens were found in 98% of these cases. Co-infections were observed relatively often (40%). Viruses were detected in 82% of the samples, with rotavirus being most common (56%), bacteria in 32% and parasites in 10%. The present study emphasizes the importance of viral pathogens, especially rotavirus, in hospitalizations of children with gastroenteritis. Policies to reduce (costs of) hospitalizations due to gastroenteritis should therefore be first targeted at rotavirus.

Notes

Acknowledgement

The authors would like to thank the staff of the hospitals for inclusion of the patients in the present study. We thank Hein Sprong, Max Heck and Ed Kuijper for the subtyping of Cryptosporidium and G. lamblia, Salmonella, and C. difficile, respectively. We are grateful to Carolien de Jager for her assistance in the preparation and during the execution of the study. Finally the authors thank Wilfrid van Pelt for his help in calculating the incidence figures and for critically reading the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    de Wit MA, Koopmans MP, Kortbeek LM, Wannet WJ, Vinjé J, van Leusden F et al (2001) Sensor, a population-based cohort study on gastroenteritis in the Netherlands: incidence and etiology. Am J Epidemiol 154:666–674PubMedCrossRefGoogle Scholar
  2. 2.
    de Wit MA, Kortbeek LM, Koopmans MP, de Jager CJ, Wannet WJ, Bartelds AI et al (2001) A comparison of gastroenteritis in a general practice-based study and a community-based study. Epidemiol Infect 127:389–397PubMedGoogle Scholar
  3. 3.
    van den Brandhof WE, De Wit GA, de Wit MA, van Duynhoven YT (2004) Costs of gastroenteritis in the Netherlands. Epidemiol Infect 132:211–221PubMedCrossRefGoogle Scholar
  4. 4.
    Levidiotou S, Gartzonika C, Papaventsis D, Christaki C, Priavali E, Zotos N et al (2009) Viral agents of acute gastroenteritis in hospitalized children in Greece. Clin Microbiol Infect 15:596–598PubMedCrossRefGoogle Scholar
  5. 5.
    Klein EJ, Boster DR, Stapp JR, Wells JG, Qin X, Clausen CR et al (2006) Diarrhea etiology in a Children’s Hospital Emergency Department: a prospective cohort study. Clin Infect Dis 43:807–813PubMedCrossRefGoogle Scholar
  6. 6.
    Barnes GL, Uren E, Stevens KB, Bishop RF (1998) Etiology of acute gastroenteritis in hospitalized children in Melbourne, Australia, from April 1980 to March 1993. J Clin Microbiol 36:133–138PubMedGoogle Scholar
  7. 7.
    Lorrot M, Bon F, El Hajje MJ, Aho S, Wolfer M, Giraudon H et al (2011) Epidemiology and clinical features of gastroenteritis in hospitalised children: prospective survey during a 2-year period in a Parisian hospital, France. Eur J Clin Microbiol Infect Dis 30(3):361–368. doi: 10.1007/s10096-010-1094-9 Google Scholar
  8. 8.
    de Wit MA, Koopmans MP, Kortbeek LM, van Leeuwen NJ, Bartelds AI, van Duynhoven YT (2001) Gastroenteritis in sentinel general practices, the Netherlands. Emerg Infect Dis 7:82–91PubMedCrossRefGoogle Scholar
  9. 9.
    Cerquetti M, Luzzi I, Caprioli A, Sebastianelli A, Mastrantonio P (1995) Role of Clostridium difficile in childhood diarrhea. Pediatr Infect Dis J 14:598–603PubMedCrossRefGoogle Scholar
  10. 10.
    McFarland LV, Brandmarker SA, Guandalini S (2000) Pediatric Clostridium difficile: A phantom menace or clinical reality? J Paediatr Gastroenterol Nutr 31:220–231CrossRefGoogle Scholar
  11. 11.
    Tullus K, Aronsson B, Marcus S, Mollby R (1989) Intestinal colonization with Clostridium difficile in infants up to 18 months of age. Eur J Clin Microbiol Infect Dis 8:390–393PubMedCrossRefGoogle Scholar
  12. 12.
    de Boer RF, Ott A, Kesztyus B, Kooistra-Smid AM (2010) Improved detection of five major gastro-intestinal pathogens using a molecular screening approach. J Clin Microbiol 48:4140–4146PubMedCrossRefGoogle Scholar
  13. 13.
    Schuurman T, de Boer RF, van Zanten E, van Slochteren KR, Scheper HR, Dijk-Alberts BG et al (2007) Feasibility of a molecular screening method for detection of Salmonella enterica and Campylobacter jejuni in a routine community-based clinical microbiology laboratory. J Clin Microbiol 45:3692–3700PubMedCrossRefGoogle Scholar
  14. 14.
    Van Duynhoven YTHP, Friesema IHM, Schuurman T, Roovers A, Van Zwet AA, Sabbe LJM et al (2008) Prevalence, characterization and clinical profiles of Shiga toxin-producing Escherichia coli in the Netherlands. Clin Microbiol Infect 14:437–445PubMedCrossRefGoogle Scholar
  15. 15.
    de Boer RF, Wijma J, Schuurman T, Moedt BG, Dijk-Alberts BG, Ott A et al (2010) Evaluation of a rapid molecular screening approach for the detection of toxigenic Clostridium difficile in general and subsequent identification of the tcdC < DELTA > 117 mutation in human stools. J Microbiol Methods 83:59–65PubMedCrossRefGoogle Scholar
  16. 16.
    Svraka S, Van Der Veer B, Duizer E, Dekkers J, Koopmans M, Vennema H (2009) Novel approach for detection of enteric viruses to enable syndrome surveillance of acute viral gastroenteritis. J Clin Microbiol 47:1674–1679PubMedCrossRefGoogle Scholar
  17. 17.
    Noel JS, Lee TW, Kurtz JB, Glass RI, Monroe SS (1995) Typing of human astroviruses from clinical isolates by enzyme immunoassay and nucleotide sequencing. J Clin Microbiol 33:797–801PubMedGoogle Scholar
  18. 18.
    Siebenga JJ, Vennema H, Duizer E, Koopmans MP (2007) Gastroenteritis caused by norovirus GGII.4, the Netherlands, 1994-2005. Emerg Infect Dis 13:144–146PubMedGoogle Scholar
  19. 19.
    Fischer TK, Gentsch JR (2004) Rotavirus typing methods and algorithms. Rev Med Virol 14:71–82PubMedCrossRefGoogle Scholar
  20. 20.
    Mank TG (1999) De winst van het parasitologisch onderzoek van gefixeerde ontlasting [in Dutch]. Ned Tijdschr Klin Chem 24:52–55Google Scholar
  21. 21.
    Mank TG, Zaat JO, Deelder AM, van Eijk JT, Polderman AM (1997) Sensitivity of microscopy versus enzyme immunoassay in the laboratory diagnosis of giardiasis. Eur J Clin Microbiol Infect Dis 16:615–619PubMedCrossRefGoogle Scholar
  22. 22.
    Verweij JJ, Blange RA, Templeton K, Schinkel J, Brienen EA, van Rooyen MA et al (2004) Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol 42:1220–1223PubMedCrossRefGoogle Scholar
  23. 23.
    Verweij JJ, Mulder B, Poell B, van Middelkoop D, Brienen EA, van Lieshout L (2007) Real-time PCR for the detection of Dientamoeba fragilis in fecal samples. Mol Cell Probes 21:400–404PubMedCrossRefGoogle Scholar
  24. 24.
    Lazzeroni LG, Schenker N, Taylor JMG (1990) Robustness of multiple-imputation techniques to model misspecification. Proc Surv Res Methods Sec:260-265Google Scholar
  25. 25.
    Boshuizen HC, Viet AL, Picavet HSJ, Botterweck A, van Loon AJM (2006) Non-response in a survey of cardiovascular risk factors in the Dutch population: determinants and resulting biases. Public Health 120:297–308PubMedCrossRefGoogle Scholar
  26. 26.
    Colomba C, De Grazia S, Giammanco GM, Saporito L, Scarlata F, Titone L et al (2006) Viral gastroenteritis in children hospitalised in Sicily, Italy. Eur J Clin Microbiol Infect Dis 25:570–575PubMedCrossRefGoogle Scholar
  27. 27.
    Boga JA, Melon S, Nicieza I, De Diego I, Villar M, Parra F et al (2004) Etiology of sporadic cases of pediatric acute gastroenteritis in Asturias, Spain, and genotyping and characterization of norovirus strains involved. J Clin Microbiol 42:2668–2674PubMedCrossRefGoogle Scholar
  28. 28.
    Kirkwood CD, Clark R, Bogdanovic-Sakran N, Bishop RF (2005) A 5-year study of the prevalence and genetic diversity of human caliciviruses associated with sporadic cases of acute gastroenteritis in young children admitted to hospital in Melbourne, Australia (1998–2002). J Med Virol 77:96–101PubMedCrossRefGoogle Scholar
  29. 29.
    Sanchez-Fauquier A, Montero V, Moreno S, Sole M, Colomina J, Iturriza-Gomara M et al (2006) Human rotavirus G9 and G3 as major cause of diarrhea in hospitalized children, Spain. Emerg Infect Dis 12:1536–1541PubMedCrossRefGoogle Scholar
  30. 30.
    Podkolzin AT, Fenske EB, Yu Abramycheva N, Shipulin GA, Sagalova OI, Mazepa VN et al (2009) Hospital-based surveillance of rotavirus and other viral agents of diarrhea in children and adults in Russia, 2005–2007. J Infect Dis 200:S228–S233PubMedCrossRefGoogle Scholar
  31. 31.
    Zomer TP, van Duynhoven YTHP, Mangen MJJ, van der Maas NAT, Vennema H, Boot H et al (2008) Assessing the introduction of universal rotavirus vaccination in the Netherlands. Vaccine 26:3757–3764PubMedCrossRefGoogle Scholar
  32. 32.
    Mangen MJ, van Duynhoven YT, Vennema H, van Pelt W, Havelaar AH, de Melker HE (2010) Is it cost-effective to introduce rotavirus vaccination in the Dutch national immunization program? Vaccine 28:2624–2635PubMedCrossRefGoogle Scholar
  33. 33.
    Banyai K, Kisfali P, Bogdan A, Martella V, Melegh B, Erdman D et al (2009) Adenovirus gastroenteritis in Hungary, 2003-2006. Eur J Clin Microbiol Infect Dis 28:997–999PubMedCrossRefGoogle Scholar
  34. 34.
    Verma H, Chitambar SD, Varanasi G (2009) Identification and characterization of enteric adenoviruses in infants and children hospitalized for acute gastroenteritis. J Med Virol 81:60–64PubMedCrossRefGoogle Scholar
  35. 35.
    Doorduyn Y, Van Den Brandhof WE, Van Duynhoven YT, Wannet WJ, Van Pelt W (2006) Risk factors for Salmonella Enteritidis and Typhimurium (DT104 and non-DT104) infections in The Netherlands: predominant roles for raw eggs in Enteritidis and sandboxes in Typhimurium infections. Epidemiol Infect 134:617–626PubMedCrossRefGoogle Scholar
  36. 36.
    Doorduyn Y, Van Den Brandhof WE, van Duynhoven YT, Breukink BJ, Wagenaar JA, van Pelt W (2010) Risk factors for indigenous Campylobacter jejuni and Campylobacter coli infections in The Netherlands: a case-control study. Epidemiol Infect 138:1391–1404PubMedCrossRefGoogle Scholar
  37. 37.
    de Wit MA, Koopmans MP, Kortbeek LM, van Leeuwen NJ, Vinjé J, van Duynhoven YT (2001) Etiology of gastroenteritis in sentinel general practices in the Netherlands. Clin Infect Dis 33:280–288PubMedCrossRefGoogle Scholar
  38. 38.
    Nataro JP, Mai V, Johnson J, Blackwelder WC, Heimer R, Tirrell S et al (2006) Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin Infect Dis 43:402–407PubMedCrossRefGoogle Scholar
  39. 39.
    Nguyen RN, Taylor LS, Tauschek M, Robins-Browne RM (2006) Atypical enteropathogenic Escherichia coli infection and prolonged diarrhea in children. Emerg Infect Dis 12:597–603PubMedCrossRefGoogle Scholar
  40. 40.
    Afset JE, Bevanger L, Romundstad P, Bergh K (2004) Association of atypical enteropathogenic Escherichia coli (EPEC) with prolonged diarrhoea. J Med Microbiol 53:1137–1144PubMedCrossRefGoogle Scholar
  41. 41.
    Afset JE, Bruant G, Brousseau R, Harel J, Anderssen E, Bevanger L et al (2006) Identification of virulence genes linked with diarrhea due to atypical enteropathogenic Escherichia coli by DNA microarray analysis and PCR. J Clin Microbiol 44:3703–3711PubMedCrossRefGoogle Scholar
  42. 42.
    Caprioli A, Pezzella C, Morelli R, Giammanco A, Arista S, Crotti D et al (1996) Enteropathogens associated with childhood diarrhea in Italy. The Italian Study Group on Gastrointestinal Infections. Pediatr Infect Dis J 15:876–883PubMedCrossRefGoogle Scholar
  43. 43.
    Wielinga PR, de Vries A, van der Goot TH, Mank T, Mars MH, Kortbeek LM et al (2008) Molecular epidemiology of Cryptosporidium in humans and cattle in the Netherlands. Int J Parasitol 38:809–817PubMedCrossRefGoogle Scholar
  44. 44.
    Lake IR, Harrison FC, Chalmers RM, Bentham G, Nichols G, Hunter PR et al (2007) Case-control study of environmental and social factors influencing cryptosporidiosis. Eur J Epidemiol 22:805–811PubMedCrossRefGoogle Scholar
  45. 45.
    Sprong H, Cacciò SM, van der Giessen JWB, on behalf of the ZOOPNET Network and Partners (2009) Identification of zoonotic genotypes of Giardia duodenalis. PLoS Negl Trop Dis 3:e558. doi: 10.1371/journal.pntd.0000558 PubMedCrossRefGoogle Scholar
  46. 46.
    Helms M, Simonsen J, Molbak K (2006) Foodborne bacterial infection and hospitalization: a registry-based study. Clin Infect Dis 42:498–506PubMedCrossRefGoogle Scholar
  47. 47.
    Cumberland P, Sethi D, Roderick PJ, Wheeler JG, Cowden JM, Roberts JA et al (2003) The infectious intestinal disease study of England: a prospective evaluation of symptoms and health care use after an acute episode. Epidemiol Infect 130:453–460PubMedGoogle Scholar
  48. 48.
    Weinstein M (2006) Seizures and encephalopathy as the presenting sign of viral gastroenteritis. Pediatr Emerg Care 22:579–581PubMedCrossRefGoogle Scholar
  49. 49.
    Chen SY, Tsai CN, Lai MW, Chen CY, Lin K, Lin TY et al (2009) Norovirus infection as a cause of diarrhea-associated benign infantile seizures. Clin Infect Dis 48:849–855PubMedCrossRefGoogle Scholar
  50. 50.
    Jusot JF, Vanhems P, Benzait F, Berthelot P, Patural H, Teyssier G et al (2003) Reported measures of hygiene and incidence rates for hospital-acquired diarrhea in 31 French pediatric wards: is there any relationship? Infect Control Hosp Epidemiol 24:520–525PubMedCrossRefGoogle Scholar
  51. 51.
    Ethelberg S, Olesen B, Neimann J, Schiellerup P, Helms M, Jensen C et al (2006) Risk factors for diarrhea among children in an industrialized country. Epidemiology 17:24–30PubMedCrossRefGoogle Scholar
  52. 52.
    de Wit MA, Koopmans MP, van Duynhoven YT (2003) Risk factors for norovirus, Sapporo-like virus, and group A rotavirus gastroenteritis. Emerg Infect Dis 9:1563–1570PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • I. H. M. Friesema
    • 1
  • R. F. de Boer
    • 2
  • E. Duizer
    • 1
  • L. M. Kortbeek
    • 1
  • D. W. Notermans
    • 1
  • O. F. Norbruis
    • 3
  • D. D. L. Bezemer
    • 4
  • H. van Heerbeek
    • 5
  • R. N. J. van Andel
    • 6
  • J. G. van Enk
    • 7
  • P. L. A. Fraaij
    • 8
  • M. P. G. Koopmans
    • 1
    • 8
  • A. M. D. Kooistra-Smid
    • 2
  • Y. T. H. P. van Duynhoven
    • 1
  1. 1.National Institute for Public Health and the Environment (RIVM)Centre for Infectious Disease ControlBilthovenThe Netherlands
  2. 2.Department of Research & DevelopmentLaboratory for Infectious DiseasesGroningenThe Netherlands
  3. 3.Department of PediatricsIsala HospitalZwolleThe Netherlands
  4. 4.Department of PediatricsMaasstad HospitalRotterdamThe Netherlands
  5. 5.Department of PediatricsCatharina HospitalEindhovenThe Netherlands
  6. 6.Department of PediatricsOnze Lieve Vrouwe GasthuisAmsterdamThe Netherlands
  7. 7.Department of PediatricsGelderse Vallei HospitalEdeThe Netherlands
  8. 8.Department of VirologyErasmus MC-Sophia Children’s HospitalRotterdamThe Netherlands

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