Diagnosis of viral gastroenteritis in children: interpretation of real-time PCR results and relation to clinical symptoms

European Journal of Clinical Microbiology and Infectious Diseases

Volumn 33, Issue 10, 2014, Pages 1663-1673

  Corcoran, M S ^a   van Well, G T J ^a,b   van Loo, I H M ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN VP1; PROTEIN VP4; PROTEIN VP7; ROTAVIRUS VACCINE;

ABDOMINAL CRAMP; ABDOMINAL PAIN; ADENOVIRUS INFECTION; ASTROVIRUS INFECTION; CALICIVIRUS INFECTION; CHILD; DEHYDRATION; DIARRHEA; DISEASE SEVERITY; FEVER; GENETIC VARIABILITY; GENOTYPE; HEADACHE; HUMAN; MIXED INFECTION; MYALGIA; NOROVIRUS INFECTION; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; ROTAVIRUS INFECTION; SAPOVIRUS; SAPOVIRUS INFECTION; SCORING SYSTEM; SEASONAL VARIATION; SEROTYPE; SPRING; SYMPTOM; VERNER MORRISON SYNDROME; VIRAL GASTROENTERITIS; VIRUS LOAD; VIRUS PARTICLE; VIRUS SHEDDING; VOMITING; WINTER; ADOLESCENT; CLASSIFICATION; FECES; GASTROENTERITIS; GENETICS; INFANT; ISOLATION AND PURIFICATION; MOLECULAR DIAGNOSIS; NEWBORN; PATHOLOGY; PRESCHOOL CHILD; PROCEDURES; STATISTICAL ANALYSIS; VIROLOGY; VIRUS; VIRUS DISEASES;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; DATA INTERPRETATION, STATISTICAL; FECES; GASTROENTERITIS; HUMANS; INFANT; INFANT, NEWBORN; MOLECULAR DIAGNOSTIC TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; VIRAL LOAD; VIRUS DISEASES; VIRUS SHEDDING; VIRUSES;

EID: 84911007368     PISSN: 09349723     EISSN: 14354373     Source Type: Journal    
DOI: 10.1007/s10096-014-2135-6     Document Type: Review

References (72)

1. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani DG, Jha P, Campbell H, Walker CF, Cibulskis R, Eisele T, Liu L, Mathers C; Child Health Epidemiology Reference Group of WHO and UNICEF (2010) Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 375:1969–1987
2. Friesema IHM, Lugnér AK, van Duynhoven YTHP; GEops Working Group (2012) Costs of gastroenteritis in the Netherlands, with special attention for severe cases. Eur J Clin Microbiol Infect Dis 31:1895–1900
3. 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(2):258–262
4. 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(3):280–288
5. Amar CF, East CL, Gray J, Iturriza-Gomara M, Maclure EA, McLauchlin J (2007) Detection by PCR of eight groups of enteric pathogens in 4,627 faecal samples: re-examination of the English case–control Infectious Intestinal Disease Study (1993–1996). Eur J Clin Microbiol Infect Dis 26(5):311–323
6. Wolffs PF, Bruggeman CA, van Well GT, van Loo IH (2011) Replacing traditional diagnostics of fecal viral pathogens by a comprehensive panel of real-time PCRs. J Clin Microbiol 49(5):1926–1931
7. van Maarseveen NM, Wessels E, de Brouwer CS, Vossen AC, Claas EC (2010) Diagnosis of viral gastroenteritis by simultaneous detection of Adenovirus group F, Astrovirus, Rotavirus group A, Norovirus genogroups I and II, and Sapovirus in two internally controlled multiplex real-time PCR assays. J Clin Virol 49(3):205–210
8. Logan C, O’Leary JJ, O’Sullivan N (2006) Real-time reverse transcription-PCR for detection of rotavirus and adenovirus as causative agents of acute viral gastroenteritis in children. J Clin Microbiol 44(9):3189–3195
9. Zhang S, Chen TH, Wang J, Dong C, Pan J, Moe C, Chen W, Yang L, Wang X, Tang H, Li X, Liu P (2011) Symptomatic and asymptomatic infections of rotavirus, norovirus, and adenovirus among hospitalized children in Xi’an, China. J Med Virol 83(8):1476–1484. doi:10.1002/jmv.22108
10. Olesen B, Neimann J, Böttiger B, Ethelberg S, Schiellerup P, Jensen C, Helms M, Scheutz F, Olsen KE, Krogfelt K, Petersen E, Mølbak K, Gerner-Smidt P (2005) Etiology of diarrhea in young children in Denmark: a case–control study. J Clin Microbiol 43(8):3636–3641
11. Ruuska T, Vesikari T (1990) Rotavirus disease in Finnish children: use of numerical scores for clinical severity of diarrhoeal episodes. Scand J Infect Dis 22(3):259–267
12. Clark HF, Borian FE, Bell LM, Modesto K, Gouvea V, Plotkin SA (1988) Protective effect of WC3 vaccine against rotavirus diarrhea in infants during a predominantly serotype 1 rotavirus season. J Infect Dis 158(3):570–587
13. Iturriza Gómara M, Simpson R, Perault AM, Redpath C, Lorgelly P, Joshi D, Mugford M, Hughes CA, Dalrymple J, Desselberger U, Gray J (2008) Structured surveillance of infantile gastroenteritis in East Anglia, UK: incidence of infection with common viral gastroenteric pathogens. Epidemiol Infect 136(1):23–33
14. Witsø E, Palacios G, Cinek O, Stene LC, Grinde B, Janowitz D, Lipkin WI, Rønningen KS (2006) High prevalence of human enterovirus a infections in natural circulation of human enteroviruses. J Clin Microbiol 44(11):4095–4100
15. Benschop K, Thomas X, Serpenti C, Molenkamp R, Wolthers K (2008) High prevalence of human Parechovirus (HPeV) genotypes in the Amsterdam region and identification of specific HPeV variants by direct genotyping of stool samples. J Clin Microbiol 46(12):3965–3970
16. Walter JE, Mitchell DK (2003) Astrovirus infection in children. Curr Opin Infect Dis 16(3):247–253. doi:10.1097/01.qco.0000073775.11390.60
17. Ferreira MS, Xavier Mda P, Tinga AC, Rose TL, Fumian TM, Fialho AM, de Assis RM, Carvalho Costa FA, de Oliveira SA, Leite JP, Miagostovich MP (2012) Assessment of gastroenteric viruses frequency in a children’s day care center in Rio De Janeiro, Brazil: a fifteen year study (1994–2008). PLoS One 7(3):e33754. doi:10.1371/journal.pone.0033754
18. Phillips G, Lopman B, Rodrigues LC, Tam CC (2010) Asymptomatic rotavirus infections in England: prevalence, characteristics, and risk factors. Am J Epidemiol 171(9):1023–1030
19. Parashar UD, Bresee JS, Glass RI (2003) The global burden of diarrhoeal disease in children. Bull World Health Organ 81(4):236
20. Hillis SD, Miranda CM, McCann M, Bender D, Weigle K (1992) Day care center attendance and diarrheal morbidity in Colombia. Pediatrics 90(4):582–588
21. Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI (2003) Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9:565–572
22. Wiegering V, Kaiser J, Tappe D, Weissbrich B, Morbach H, Girschick HJ (2011) Gastroenteritis in childhood: a retrospective study of 650 hospitalized pediatric patients. Int J Infect Dis 15(6):e401–e407
23. Sowmyanarayanan TV, Ramani S, Sarkar R, Arumugam R, Warier JP, Moses PD, Simon A, Agarwal I, Bose A, Arora R, Kang G (2012) Severity of rotavirus gastroenteritis in Indian children requiring hospitalization. Vaccine 30(Suppl 1):A167–A172
24. González GG, Liprandi F, Ludert JE (2011) Molecular epidemiology of enteric viruses in children with sporadic gastroenteritis in Valencia, Venezuela. J Med Virol 83:1972–1982
25. Cunliffe NA, Booth JA, Elliot C, Lowe SJ, Sopwith W, Kitchin N, Nakagomi O, Nakagomi T, Hart CA, Regan M (2010) Healthcare-associated viral gastroenteritis among children in a large pediatric hospital, United Kingdom. Emerg Infect Dis 16(1):55–62
26. Pang XL, Honma S, Nakata S, Vesikari T (2000) Human caliciviruses in acute gastroenteritis of young children in the community. J Infect Dis 181(Suppl 2):S288–S294
27. Parashar UD, Gibson CJ, Bresee JS, Glass RI (2006) Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12(2):304–306
28. Abugalia M, Cuevas L, Kirby A, Dove W, Nakagomi O, Nakagomi T, Kara M, Gweder R, Smeo M, Cunliffe N (2011) Clinical features and molecular epidemiology of rotavirus and norovirus infections in Libyan children. J Med Virol 83(10):1849–1856. doi:10.1002/jmv.22141
29. Glass RI, Kilgore PE, Holman RC, Jin S, Smith JC, Woods PA, Clarke MJ, Ho MS, Gentsch JR (1996) The epidemiology of rotavirus diarrhea in the United States: surveillance and estimates of disease burden. J Infect Dis 174(Suppl 1):S5–S11
30. Greenberg HB, Estes MK (2009) Rotaviruses: from pathogenesis to vaccination. Gastroenterology 136(6):1939–1951
31. Rimoldi SG, Stefani F, Pagani C, Chenal LL, Zanchetta N, Di Bartolo I, Lombardi A, Ruggeri FM, Di Lillo D, Zuccotti GV, Gismondo MR (2011) Epidemiological and clinical characteristics of pediatric gastroenteritis associated with new viral agents. Arch Virol 156:1583–1589
32. 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(11):962–965
33. Richardson S, Grimwood K, Gorrell R, Palombo E, Barnes G, Bishop R (1998) Extended excretion of rotavirus after severe diarrhoea in young children. Lancet 351(9119):1844–1848
34. Vesikari T, Karvonen A, Prymula R, Schuster V, Tejedor JC, Cohen R, Meurice F, Han HH, Damaso S, Bouckenooghe A (2007) Efficacy of human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in European infants: randomised, double-blind controlled study. Lancet 370:1757–1763
35. Linhares AC, Velazquez FR, Perez-Schael I, Saez-Llorens X, Abate H, Espinoza F, Lopez P, Macias-Parra M, Ortega-Barria E, Rivera-Medina DM, Rivera L, Pavia-Ruz N, Nunez E, Damaso S, Ruiz-Palacios GM, De Vos B, O’Ryan M, Gillard P, Bouckenooghe A; Human Rotavirus Vaccine Study Group (2008) Efficacy and safety of an oral live attenuated human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in Latin American infants: a randomised, double-blind, placebo-controlled phase III study. Lancet 371:1181–1189
36. Sáfadi MA, Berezin EN, Munford V, Almeida FJ, de Moraes JC, Pinheiro CF, Racz ML (2010) Hospital-based surveillance to evaluate the impact of rotavirus vaccination in São Paulo, Brazil. Pediatr Infect Dis J 29(11):1019–1022. doi:10.1097/INF.0b013e3181e7886a
37. 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(14):2624–2635
38. Mitui MT, Bozdayi G, Dalgic B, Bostanci I, Nishizono A, Ahmed K (2009) Molecular characterization of a human group C rotavirus detected first in Turkey. Virus Genes 39(2):157–164. doi:10.1007/s11262-009-0420-8
39. Jiang B, Dennehy PH, Spangenberger S, Gentsch JR, Glass RI (1995) First detection of group C rotavirus in fecal specimens of children with diarrhea in the United States. J Infect Dis 172(1):45–50
40. Banerjee I, Ramani S, Primrose B, Moses P, Iturriza-Gomara M, Gray JJ, Jaffar S, Monica B, Muliyil JP, Brown DW, Estes MK, Kang G (2006) Comparative study of the epidemiology of rotavirus in children from a community-based birth cohort and a hospital in South India. J Clin Microbiol 44(7):2468–2474
41. Aupiais C, de Rougemont A, Menager C, Vallet C, Brasme JF, Kaplon J, Pothier P, Gendrel D (2009) Severity of acute gastroenteritis in infants infected by G1 or G9 rotaviruses. J Clin Virol 46:282–285
42. Ogilvie I, Khoury H, El Khoury AC, Goetghebeur MM (2011) Burden of rotavirus gastroenteritis in the pediatric population in Central and Eastern Europe: serotype distribution and burden of illness. Hum Vaccin 7(5):523–533
43. Santos N, Hoshino Y (2005) Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 15(1):29–56. doi:10.1002/rmv.448
44. Antunes H, Afonso A, Iturriza M, Martinho I, Ribeiro C, Rocha S, Magalhães C, Carvalho L, Branca F, Gray J (2009) G2P[4] the most prevalent rotavirus genotype in 2007 winter season in an European non-vaccinated population. J Clin Virol 45:76–78
45. Payne DC, Vinjé J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, Hall CB, Chappell J, Bernstein DI, Curns AT, Wikswo M, Shirley SH, Hall AJ, Lopman B, Parashar UD (2013) Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med 368(12):1121–1130. doi:10.1056/NEJMsa1206589
46. Glass RI, Parashar UD, Estes MK (2009) Norovirus gastroenteritis. N Engl J Med 361(18):1776–1785
47. Moreno-Espinosa S, Farkas T, Jiang X (2004) Human caliciviruses and pediatric gastroenteritis. Semin Pediatric Infect Dis 15:237–245
48. Puustinen L, Blazevic V, Huhti L, Szakal ED, Halkosalo A, Salminen M, Vesikari T (2012) Norovirus genotypes in endemic acute gastroenteritis of infants and children in Finland between 1994 and 2007. Epidemiol Infect 140(2):268–275
49. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinjé J, Parashar UD (2008) Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14(8):1224–1231
50. Murata T, Katsushima N, Mizuta K, Muraki Y, Hongo S, Matsuzaki Y (2007) Prolonged norovirus shedding in infants
51. O’Ryan ML, Lucero Y, Prado V, Santolaya ME, Rabello M, Solis Y, Berríos D, O’Ryan-Soriano MA, Cortés H, Mamani N (2009) Symptomatic and asymptomatic rotavirus and norovirus infections during infancy in a Chilean birth cohort. Pediatr Infect Dis J 28(10):879–884
52. Barreira DM, Ferreira MS, Fumian TM, Checon R, de Sadovsky AD, Leite JP, Miagostovich MP, Spano LC (2010) Viral load and genotypes of noroviruses in symptomatic and asymptomatic children in Southeastern Brazil. J Clin Virol 47(1):60–64
53. Zeng M, Xu X, Zhu C, Chen J, Zhu Q, Lin S, Jie Y, Shu X; Chinese Pediatric Study Group of Norovirus Diarrhea (2012) Clinical and molecular epidemiology of norovirus infection in childhood diarrhea in China. J Med Virol 84(1):145–151. doi:10.1002/jmv.22248
54. Monica B, Ramani S, Banerjee I, Primrose B, Iturriza-Gomara M, Gallimore CI, Brown DW, Fathima M, Moses PD, Gray JJ, Kang G (2007) Human caliciviruses in symptomatic and asymptomatic infections in children in Vellore, South India. J Med Virol 79(5):544–551
55. Zeng M, Gong Z, Zhang Y, Zhu Q, Wang X (2011) Prevalence and genetic diversity of norovirus in outpatient children with acute diarrhea in Shanghai, China. Jpn J Infect Dis 64(5):417–422
56. Akihara S, Phan TG, Nguyen TA, Hansman G, Okitsu S, Ushijima H (2005) Existence of multiple outbreaks of viral gastroenteritis among infants in a day care center in Japan. Arch Virol 150(10):2061–2075
57. Kirkwood CD, Streitberg R (2008) Calicivirus shedding in children after recovery from diarrhoeal disease. J Clin Virol 43(3):346–348
58. Feeney SA, Armstrong VJ, Mitchell SJ, Crawford L, McCaughey C, Coyle PV (2011) Development and clinical validation of multiplex TaqMan® assays for rapid diagnosis of viral gastroenteritis. J Med Virol 83:1650–1656
59. Lynch JP 3rd, Fishbein M, Echavarria M (2011) Adenovirus. Semin Respir Crit Care Med 32:494–511
60. Uhnoo I, Wadell G, Svensson L, Johansson ME (1984) Importance of enteric adenoviruses 40 and 41 in acute gastroenteritis in infants and young children. J Clin Microbiol 20:365–372
61. 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(9):1170–1178
62. Guix S, Caballero S, Villena C, Bartolomé R, Latorre C, Rabella N, Simó M, Bosch A, Pintó RM (2002) Molecular epidemiology of astrovirus infection in Barcelona, Spain. J Clin Microbiol 40:133–139
63. Rodriguez-Baez N, O’Brien R, Qiu SQ, Bass DM (2002) Astrovirus, adenovirus, and rotavirus in hospitalized children: prevalence and association with gastroenteritis. J Pediatr Gastroenterol Nutr 35:64–68
64. de Wit MA, Koopmans MP, Kortbeek LM, Wannet WJ, Vinjé J, van Leusden F, Bartelds AI, van Duynhoven YT (2001) Sensor, a population-based cohort study on gastroenteritis in the Netherlands: incidence and etiology. Am J Epidemiol 154(7):666–674
65. Lyman WH, Walsh JF, Kotch JB, Weber DJ, Gunn E, Vinjé J (2009) Prospective study of etiologic agents of acute gastroenteritis outbreaks in child care centers. J Pediatr 154(2):253–257
66. Gidudu J, Sack DA, Pina M, Hudson MJ, Kohl KS, Bishop P, Chatterjee A, Chiappini E, Compingbutra A, da Costa C, Fernandopulle R, Fischer TK, Haber P, Masana W, de Menezes MR, Kang G, Khuri-Bulos N, Killion LA, Nair C, Poerschke G, Rath B, Salazar-Lindo E, Setse R, Wenger P, Wong VC, Zaman K; Brighton Collaboration Diarrhea Working Group (2011) Diarrhea: case definition and guidelines for collection, analysis, and presentation of immunization safety data. Vaccine 29(5):1053–1071
67. Givon-Lavi N, Greenberg D, Dagan R (2008) Comparison between two severity scoring scales commonly used in the evaluation of rotavirus gastroenteritis in children. Vaccine 26:5798–5801
68. Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T, Clemens SC, Cheuvart B, Espinoza F, Gillard P, Innis BL, Cervantes Y, Linhares AC, López P, Macías-Parra M, Ortega-Barría E, Richardson V, Rivera-Medina DM, Rivera L, Salinas B, Pavía-Ruz N, Salmerón J, Rüttimann R, Tinoco JC, Rubio P, Nuñez E, Guerrero ML, Yarzábal JP, Damaso S, Tornieporth N, Sáez-Llorens X, Vergara RF, Vesikari T, Bouckenooghe A, Clemens R, De Vos B, O’Ryan M; Human Rotavirus Vaccine Study Group (2006) Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 354(1):11–22
69. Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, Dallas MJ, Heyse JF, Goveia MG, Black SB, Shinefield HR, Christie CD, Ylitalo S, Itzler RF, Coia ML, Onorato MT, Adeyi BA, Marshall GS, Gothefors L, Campens D, Karvonen A, Watt JP, O’Brien KL, DiNubile MJ, Clark HF, Boslego JW, Offit PA, Heaton PM; Rotavirus Efficacy and Safety Trial (REST) Study Team (2006) Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 354(1):23–33
70. Kang G, Iturriza-Gomara M, Wheeler JG, Crystal P, Monica B, Ramani S, Primrose B, Moses PD, Gallimore CI, Brown DW, Gray J (2004) Quantitation of group A rotavirus by real-time reverse-transcription-polymerase chain reaction: correlation with clinical severity in children in South India. J Med Virol 73(1):118–122
71. Phillips G, Lopman B, Tam CC, Iturriza-Gomara M, Brown D, Gray J (2009) Diagnosing rotavirus A associated IID: Using ELISA to identify a cut-off for real time RT-PCR. J Clin Virol 44(3):242–245
72. Phillips G, Lopman B, Tam CC, Iturriza-Gomara M, Brown D, Gray J (2009) Diagnosing norovirus-associated infectious intestinal disease using viral load. BMC Infect Dis 9:63