Synergistic effects between rotavirus and coinfecting pathogens on diarrheal disease: Evidence from a community-based study in northwestern Ecuador

American Journal of Epidemiology

Volumn 176, Issue 5, 2012, Pages 387-395

  Bhavnani, Darlene ^a   Goldstick, Jason E ^a   Cevallos, William ^b   Trueba, Gabriel ^c   Eisenberg, Joseph N S ^a  

^a UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSIDAD CENTRAL DEL ECUADOR   (Ecuador)

^c UNIVERSIDAD SAN FRANCISCO DE QUITO   (Ecuador)

Author keywords

case control studies; diarrhea; Escherichia coli; Giardia; interaction; prevalence; rotavirus; synergism

Indexed keywords

CHILD HEALTH; COHORT ANALYSIS; COLIFORM BACTERIUM; DEVELOPING WORLD; DIARRHEAL DISEASE; DISEASE PREVALENCE; FLAGELLATE; INFECTIVITY; MORBIDITY; MORTALITY; PARASITE; PATHOGEN; RISK FACTOR; SYNERGISM; VIRUS;

ADOLESCENT; ADULT; AGED; ARTICLE; CASE CONTROL STUDY; CHILD; COMMUNITY ASSESSMENT; CONTROLLED STUDY; ECUADOR; ENTEROBACTERIACEAE INFECTION; ENTEROINVASIVE ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GIARDIA; GIARDIASIS; HUMAN; INFANT; INFECTION RISK; INFECTIOUS DIARRHEA; MAJOR CLINICAL STUDY; MIXED INFECTION; NEWBORN; NONHUMAN; PLESIOMONAS SHIGELLOIDES; PLESIOMONAS SHIGELLOIDES INFECTION; PRESCHOOL CHILD; PREVALENCE; ROTAVIRUS; ROTAVIRUS INFECTION; SCHOOL CHILD;

ADOLESCENT; ADULT; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; COINFECTION; DIARRHEA; ECUADOR; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GIARDIA; GIARDIASIS; HUMANS; INFANT; INFANT, NEWBORN; ODDS RATIO; PREVALENCE; ROTAVIRUS; ROTAVIRUS INFECTIONS; VIRULENCE; YOUNG ADULT;

ECUADOR;

ESCHERICHIA COLI; GIARDIA; ROTAVIRUS;

EID: 84865703838     PISSN: 00029262     EISSN: 14766256     Source Type: Journal    
DOI: 10.1093/aje/kws220     Document Type: Article

References (46)

1. Global Health Observatory. Causes of death in 2008. Geneva, Switzerland: World Health Organization; 2012. (www.who.int/gho/mortality-burden-disease/ causes-death-2008/en/index.html). (Accessed October 28, 2011).
2. O'Ryan M, Prado V, Pickering LK. A millennium update on pediatric diarrheal illness in the developing world. Semin Pediatr Infect Dis. 2005;16(2): 125-136.
3. Boschi-Pinto C, Velebit L, Shibuya K. Estimating child mortality due to diarrhoea in developing countries. Bull World Health Organ. 2008;86(9):710-717.
4. Grimprel E, Rodrigo C, Desselberger U. Rotavirus disease: impact of coinfections. Pediatr Infect Dis J. 2008; 27(1 suppl):S3-S10.
5. Hien BT, Trang do T, Scheutz F, et al. Diarrhoeagenic Escherichia coli and other causes of childhood diarrhoea: a case-control study in children living in a wastewater-use area in Hanoi, Vietnam. J Med Microbiol. 2007;56(Pt 8): 1086-1096.
6. Black RE, Lopez de Romana G, Brown KH, et al. Incidence and etiology of infantile diarrhea and major routes of transmission in Huascar, Peru. Am J Epidemiol. 1989; 129(4):785-799.
7. Albert MJ, Faruque AS, Faruque SM, et al. Case-control study of enteropathogens associated with childhood diarrhea in Dhaka, Bangladesh. J Clin Microbiol. 1999;37(11): 3458-3464.
8. Orlandi PP, Silva T, Magalhaes GF, et al. Enteropathogens associated with diarrheal disease in infants of poor urban areas of Porto Velho, Rondonia: a preliminary study. Mem Inst Oswaldo Cruz. 2001;96(5):621-625.
9. Bodhidatta L, McDaniel P, Sornsakrin S, et al. Case-control study of diarrheal disease etiology in a remote rural area in western Thailand. Am J Trop Med Hyg. 2010;83(5): 1106-1109.
10. Souza EC, Martinez MB, Taddei CR, et al. Etiologic profile of acute diarrhea in children in Sao Paulo. (In Portuguese). J Pediatr (Rio J). 2002;78(1):31-38.
11. Ochoa TJ, Ecker L, Barletta F, et al. Age-related susceptibility to infection with diarrheagenic Escherichia coli among infants from periurban areas in Lima, Peru. Clin Infect Dis. 2009;49(11):1694-1702.
12. Torres ME, Pirez MC, Schelotto F, et al. Etiology of children's diarrhea in Montevideo, Uruguay: associated pathogens and unusual isolates. J Clin Microbiol. 2001;39(6):2134-2139.
13. Tzipori SR, Makin TJ, Smith ML, et al. Clinical manifestations of diarrhea in calves infected with rotavirus and enterotoxigenic Escherichia coli. J Clin Microbiol. 1981;13(6):1011-1016.
14. Newsome PM, Coney KA. Synergistic rotavirus and Escherichia coli diarrheal infection of mice. Infect Immun. 1985;47(2):573-574.
15. Tzipori S, Chandler D, Makin T, et al. Escherichia coli and rotavirus infections in four-week-old gnotobiotic piglets fed milk or dry food. Aust Vet J. 1980;56(6): 279-284.
16. Thouless ME, DiGiacomo RF, Deeb BJ. The effect of combined rotavirus and Escherichia coli infections in rabbits. Lab Anim Sci. 1996;46(4):381-385.
17. Wray C, Dawson M, Afshar A, et al. Experimental Escherichia coli and rotavirus infection in lambs. Res Vet Sci. 1981;30(3):379-381.
18. Katouli M, Shokouhi F, Farhoudi-Moghaddam AA, et al. Occurrence of colonization factor antigens I & II in enterotoxigenic Escherichia coli associated diarrhea in Iran & correlation with severity of disease. Indian J Med Res. 1992;95:115-120.
19. Hori H, Akpedonu P, Armah G, et al. Enteric pathogens in severe forms of acute gastroenteritis in Ghanaian children. Acta Paediatr Jpn. 1996;38(6):672-676.
20. Unicomb LE, Faruque SM, Malek MA, et al. Demonstration of a lack of synergistic effect of rotavirus with other diarrheal pathogens on severity of diarrhea in children. J Clin Microbiol. 1996;34(5):1340-1342.
21. Uhnoo I, Olding-Stenkvist E, Kreuger A. Clinical features of acute gastroenteritis associated with rotavirus, enteric adenoviruses, and bacteria. Arch Dis Child. 1986;61(8): 732-738.
22. Bilenko N, Levy A, Dagan R, et al. Does co-infection with Giardia lamblia modulate the clinical characteristics of enteric infections in young children? Eur J Epidemiol. 2004;19(9):877-883.
23. Superti F, Petrone G, Pisani S, et al. Superinfection by Listeria monocytogenes of cultured human enterocyte-like cells infected with poliovirus or rotavirus. Med Microbiol Immunol. 1996;185(3):131-137.
24. Di Biase AM, Petrone G, Conte MP, et al. Infection of human enterocyte-like cells with rotavirus enhances invasiveness of Yersinia enterocolitica and Y. pseudotuberculosis. J Med Microbiol. 2000;49(10):897-904.
25. Bukholm G. Human rotavirus infection enhances invasiveness of enterobacteria in MA-104 cells. APMIS. 1988;96(12):1118-1124.
26. Eisenberg JN, Cevallos W, Ponce K, et al. Environmental change and infectious disease: how new roads affect the transmission of diarrheal pathogens in rural Ecuador. Proc Natl Acad Sci USA. 2006;103(51):19460-19465.
27. Horvitz DG, Thompson DJ. A generalization of sampling without replacement from a finite universe. J Am Stat Assoc. 1952;47(260):663-685.
28. Rothman KJ, Greenland S. Modern Epidemiology. 2nd ed. Philadelphia, PA: Lippincott-Raven Publishers; 1998.
29. Escobar JC, Bhavnani D, Trueba G, et al. Plesiomonas shigelloides infection, Ecuador, 2004-2008. Emerg Infect Dis. 2012;18(2):322-324.
30. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123-140.
31. Kinsey MD, Formal SB, Dammin GJ, et al. Fluid and electrolyte transport in rhesus monkeys challenged intracecally with Shigella flexneri 2a. Infect Immun. 1976;14(2):368-371.
32. Kandel G, Donohue-Rolfe A, Donowitz M, et al. Pathogenesis of Shigella diarrhea. XVI. Selective targetting of Shiga toxin to villus cells of rabbit jejunum explains the effect of the toxin on intestinal electrolyte transport. J Clin Invest. 1989;84(5):1509-1517.
33. Muller N, von Allmen N. Recent insights into the mucosal reactions associated with Giardia lamblia infections. Int J Parasitol. 2005;35(13):1339-1347.
34. Stecher B, Hardt WD. The role of microbiota in infectious disease. Trends Microbiol. 2008;16(3):107-114.
35. Raffatellu M, Baumler AJ. Salmonella's iron armor for battling the host and its microbiota. Gut Microbes. 2010;1(1): 70-72.
36. Hasan KZ, Pathela P, Alam K, et al. Aetiology of diarrhoea in a birth cohort of children aged 0-2 year(s) in rural Mirzapur, Bangladesh. J Health Popul Nutr. 2006;24(1): 25-35.
37. Zaki AM, DuPont HL, el Alamy MA, et al. The detection of enteropathogens in acute diarrhea in a family cohort population in rural Egypt. Am J Trop Med Hyg. 1986;35(5): 1013-1022.
38. Velazquez FR, Matson DO, Guerrero ML, et al. Serum antibody as a marker of protection against natural rotavirus infection and disease. J Infect Dis. 2000;182(6):1602-1609.
39. Brussow H, Sidoti J, Barclay D, et al. Prevalence and serotype specificity of rotavirus antibodies in different age groups of Ecuadorian infants. J Infect Dis. 1990;162(3): 615-620.
40. Anderson EJ, Weber SG. Rotavirus infection in adults. Lancet Infect Dis. 2004;4(2):91-99.
41. Endara P, Trueba G, Solberg OD, et al. Symptomatic and subclinical infection with rotavirus P[8]G9, rural Ecuador. Emerg Infect Dis. 2007;13(4):574-580.
42. Hasing ME, Trueba G, Baquero MI, et al. Rapid changes in rotaviral genotypes in Ecuador. J Med Virol. 2009;81(12): 2109-2113.
43. Gilman RH, Marquis GS, Miranda E, et al. Rapid reinfection by Giardia lamblia after treatment in a hyperendemic Third World community. Lancet. 1988;1(8581):343-345.
44. Molbak K, Wested N, Hojlyng N, et al. The etiology of early childhood diarrhea: a community study from Guinea-Bissau. J Infect Dis. 1994;169(3):581-587.
45. Baqui AH, Sack RB, Black RE, et al. Enteropathogens associated with acute and persistent diarrhea in Bangladeshi children less than 5 years of age. J Infect Dis. 1992;166(4): 792-796.
46. Urbina D, Arzuza O, Young G, et al. Rotavirus type A and other enteric pathogens in stool samples from children with acute diarrhea on the Colombian northern coast. Int Microbiol. 2003;6(1):27-32.