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.
Similar content being viewed by others
References
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
Parashar UD, Gibson CJ, Bresee JS, Glass RI (2006) Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12:304–306
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
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
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
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
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
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
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
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
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
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
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
Gorelick MH, Shaw KN, Murphy KO (1997) Validity and reliability of clinical signs in the diagnosis of dehydration in children. Pediatrics 99:E6
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
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
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
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
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
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
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
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
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
Giaquinto C, Jackson AE, Vesikari T (2012) Report of the second European expert meeting on rotavirus vaccination. Vaccine 30:2237–2244
Enoch DA, Butler MJ, Pai S, Aliyu SH, Karas JA (2011) Clostridium difficile in children: colonisation and disease. J Infect 63:105–113
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
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
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
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
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
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
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
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
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
Smith CK, McNeal MM, Meyer NR, Haase S, Dekker CL (2011) Rotavirus shedding in premature infants following first immunization. Vaccine 29:8141–8146
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
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
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
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
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
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10096-013-1825-9