Assessment of the aetiology of acute gastroenteritis outbreaks in infants reveals rotavirus, noroviruses and adenovirus prevalence and viral coinfections in Nsukka, Nigeria
Tóm tắt
A better understanding of the aetiology of acute gastroenteritis (AGE) outbreaks in Southeast Nigeria would help safeguarding public health. This study screened stool samples collected from infants (children < 5 years of age) attending selected hospitals in Nsukka for human enteric viruses and evaluated the seasonality of AGE based on three-year records available at selected hospitals. A total of 120 stool samples (109 from diarrhoeal-patients and 11 from non-diarrhoeal patients, as control) collected during the AGE outbreaks of January – March 2019 and January–February 2020. The samples were analysed using an immunochromatographic lateral flow assay for differential qualitative detection of rotavirus (RoV), adenovirus (AdV), and norovirus genogroups I and II (NoVI, NoVII). Three-year (2017–2019) retrospective data on the cases of AGE reported at the hospitals were also collected and analysed. The overall prevalence of acute gastroenteritis was high (75.83%), with 13.19%representing viral co-infections. Rotavirus detection rate (69.17%) was higher than that for other viral agents (15.83%). Both mono- and mixed infections were observed for RoV, AdV and NoVII, whereas NoVI was detected only in co-infection cases. Analysis of risk factors showed that acute gastroenteritis was detected more often in infants of age ˂1 year (73.53%) than in those 1 ≤ 2 years (22.55%) or > 2 years (3.92%) in age. Gender and age were not associated with the cases of co-infections (p˂0.05). The seasonality data indicated one peak of the infection occurring in January 2017 which has decreased consecutively in the subsequent two years. These results demonstrate the prevalence and co-occurrence of enteric viruses in cases of infantile diarrhoea in Nsukka. Further molecular characterization of enteric virus strains, especially noroviruses, in this region would contribute significantly to global epidemiological data.
Tài liệu tham khảo
Khalil IA, Troeger C, Blacker BF, Rao PC, Brown A, Atherly DE, Brewer TG, Engmann CM, Houpt ER, Kang G, Kotloff KL, Levine MM, Luby SP, MacLennan CA, Pan WK, Pavlinac PB, Platts-Mills JA, Qadri F, Riddle MS, Ryan ET, Shoultz DA, Steele AD, Walson JL, Sanders JW, Mokdad AH, Murray CJL, Hay SI, Reiner RC Jr. Morbidity and mortality due to shigella and enterotoxigenic Escherichia coli diarrhoea: the global burden of disease study 1990–2016. Lancet Infect Dis. 2018;18(11):1229–40. https://doi.org/10.1016/S1473-3099(18)30475-4.
Fernandez-Cassi X, Martínez-Puchol S, Silva-Sales M, Cornejo T, Bartolome R, Bofill-Mas S, Girones R. Unveiling Viruses associated with gastroenteritis using a metagenomics approach. Viruses. 2020;12(12):1432. https://doi.org/10.3390/v12121432.
Quee FA, de Hoog ML, Schuurman R, Bruijning-Verhagen P. Community burden and transmission of acute gastroenteritis caused by norovirus and rotavirus in the Netherlands (RotaFam): a prospective household-based cohort study. Lancet Infect Dis. 2020;20(5):598–606.
Bányai K, Estes MK, Martella V, Parashar UD. Viral gastroenteritis. Lancet Infect Dis. 2018;392(10142):175–86.
Stuempfig ND, Seroy J. Viral Gastroenteritis. [Updated 2020 Nov 19]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. Available from: https://www.ncbi.nlm.nih.gov/books/NBK518995/. Accessed 5 Jan 2021.
Munnink BO, van der Hoek L. Viruses Causing gastroenteritis: the known, the new and those beyond. Viruses. 2016;8(2):42. https://doi.org/10.3390/v8020042.
Altzibar JM, Zigorraga C, Rodriguez R, Leturia N, Garmendia A, Rodriguez A, Alkorta M, Arriola L. Outbreak of acute gastroenteritis caused by contamination of drinking water in a factory, the Basque country. J Water Health. 2015;13(1):168–73. https://doi.org/10.2166/wh.2014.048.
Gastañaduy AS, Bégué RE. Acute gastroenteritis viruses. Infect Dis. 2017. https://doi.org/10.1016/B978-0-7020-6285-8.00162-3.
Upfold NS, Luke GA, Knox C. Occurrence of human enteric viruses in water sources and shellfish: a focus on Africa. Food Environ Virol. 2021;13:1–31. https://doi.org/10.1007/s12560-020-09456-8.
Prüss-Ustün A, Wolf J, Bartram J, Clasen T, Cumming O, Freeman MC, Gordon B, Hunter PR, Medlicott K, Johnston R. Burden of disease from inadequate water, sanitation and hygiene for selected adverse health outcomes: an updated analysis with a focus on low- and middle-income countries. Int J Hyg Environ Health. 2019;222(5):765–77.
Nwokoro UU, Ugwa O, Onwuliri CD, Obi IF, Ngozi MO, Agunwa C. Water, sanitation and hygiene risk factors associated with diarrhoea morbidity in a rural community of Enugu, South East Nigeria. Pan Afr Med J. 2020;37:115. https://doi.org/10.11604/pamj.2020.37.115.17735.
Tate JE, Burton AH, Boschi-Pinto C, Parashar UD. World health organization-coordinated global rotavirus surveillance network global, regional, and national estimates of rotavirus mortality in children <5 years of age, 2000–2013. Clin Infect Dis. 2016;62:S96–105.
Folorunso OS, Sebolai OM. Overview of the development, impacts, and challenges of live-attenuated oral rotavirus vaccines. Vaccines. 2020;8(3):341. https://doi.org/10.3390/vaccines8030341.
Steger CL, Boudreaux CE, LaConte LE, Pease JB, Mc Donald SM. Group A Rotavirus VP1 Polymerase and VP2 core shell proteins: Intergenotypic sequence variation and in-vitro Functional compatibility. J Virol. 2019;93(2):e01642.
Chhabra P, Payne DC, Szilagyi PG, Edwards KM, Staat MA, Shirley SH, Wikswo M, Nix WA, Lu X, Parashar UD, Jan V. Etiology of viral gastroenteritis in children <5 years of age in the United States 2008–2009. J Infect Dis. 2013;208(5):790–800.
Yen C-S, Huang Y-C, Chen C-J, Shie S-S, Yang S-L, Huang C-G, Tsao K-C, Chiu C-H, Hsieh Y-C, Kuo C-Y, Huang K-Y, Lin T-Y. Detection of norovirus and rotavirus among inpatients with acute gastroenteritis in a medical center in northern Taiwan, 2013–2018. J Microbiol, Immunol Infect. 2020;53(6):955–62. https://doi.org/10.1016/j.jmii.2020.06.016.
Shah MP, Hall AJ. Norovirus illnesses in children and adolescents. Infect Dis Clin North Am. 2018;32(1):103–18. https://doi.org/10.1016/j.idc.2017.11.004.
Qui FZ, Shen XX, Li GX, Zhao L, Chen C, Duan SX, Guo JY, Zhao MC, Yan TF, Qi JJ, Wang L, Feng ZS, Ma XJ. Adenovirus associated with acute diarrhea: a case-control study. BMC Infect Dis. 2018;18(1):450. https://doi.org/10.1186/s12879-018-3340-1.
Zambruni M, Luna G, Silva M, Bausch DG, Rivera FP, Velapatino G, Campos M, Chea-Woo E, Baiocchi N, Cleary TG, Ochoa TJ. High Prevalence and increased severity of norovirus mixed infections among children 12–24 months of age living in the suburban areas of Lima. Peru J Pediatr Infect Dis Soc. 2016;5(3):337–41. https://doi.org/10.1093/jpids/piv001.
Shrestha S, Thakali O, Raya S, Shrestha L, Parajuli K, Sherchand JB. Acute gastroenteritis associated with rotavirus a among children less than 5 years of age in Nepal. BMC Infect Dis. 2019;19:456. https://doi.org/10.1186/s12879-019-4092-2.
Tagbo BN, Chukwubike CM, Ezeugwu RI, Ani EO. Adenovirus and Rotavirus associated diarrhoea in under 5 children from Enugu rural communities. South East Nigeria World J Vaccines. 2019;9:71–83.
De Graziaa S, Bonuraa F, Bonuraa C, Mangiaracinaa L, Filizzoloa C, Martellab V, Giammanco GM. Assessing the burden of viral co-infections in acute gastroenteritis in children: an eleven-year-long investigation. J Clin Virol. 2020;129: 104513.
Japhet MO, Famurewa O, Adesina OA, Opaleye OO, Wang B, Höhne M, Bock CT, Mas MA, Niendorf S. Viral gastroenteritis among children of 0–5 years in Nigeria: characterization of the first Nigerian aichivirus, recombinant noroviruses and detection of a zoonotic astrovirus. J Clin Virol. 2019;111:4–11. https://doi.org/10.1016/j.jcv.2018.12.004.
Echiegu EA, Eya OR, Ugwu SN, Ugwuishiwu B. Evaluation of effluent from the University of Nigeria, Nsukka wastewater treatment plant for irrigation purposes. Am J Environ Sci. 2016;12(2):122–30.
Chigor V, Ibangha I-A, Chigor C, Titilawo Y. Treated wastewater used in fresh produce irrigation in Nsukka Southeast Nigeria is a reservoir of enterotoxigenic and multidrug-resistant Escherichia coli. Heliyon. 2020;6:e03780. https://doi.org/10.1016/j.heliyon.2020.e03780.
Kaplon J, Théry L, Bidalot M, Grangier N, Frappier J, Serge L, Glélé A, de Rougemont A, Ambert-Balay K. Diagnostic performance of triplex norovirus / rotavirus / adenovirus triplex ICG tests. In: 39th interdisciplinary congress of anti-infectious chemotherapy (RICAI). 2019- Paris. J Clin Microbiol 2019; 59(1):e01749-20
Mokomane M, Kasvosve I, de Melo E, Pernica JM, Goldfarb DM. The global problem of childhood diarrhoeal diseases: emerging strategies in prevention and management. Ther Adv Infect Dis. 2018;5(1):29–43. https://doi.org/10.1177/2049936117744429.
Colston JM, Faruque ASG, Hossain MJ, Saha D, Kanungo S, Mandomando I, Nisar MI, Zaidi AKM, Omore R, Breiman RF, Sow SO, Roose A, Levine MM, Kotloff KL, Ahmed T, Bessong P, Bhutta Z, Mduma E, Penatero YP, Sunder SP, et al. Associations between household-level exposures and all-cause diarrhea and pathogen-specific enteric infections in children enrolled in five sentinel surveillance studies. Int J Environ Res Public Health. 2020. https://doi.org/10.3390/ijerph17218078.
Desselbeger U. Viral gastroenteritis. J Gastrointest Infect. 2017;45(11):690–4. https://doi.org/10.1016/j.mpmed.2017.08.005.
Ojobor CD, Olovo CV, Onah LO, Ike AC. Prevalence and associated factors to rotavirus infection in children less than 5 years in Enugu State. Nigeria Virus Dis. 2020;31(3):1–7. https://doi.org/10.1007/s13337-020-00614-x.
Farfán-García AE, Imdad A, Zhang C, Arias-Guerrero MY, Sánchez-Álvarez NT, Iqbal J, Hernández-Gamboa AE, Slaughter JC, Gómez-Duarte OG. Etiology of acute gastroenteritis among children less than 5 years of age in Bucaramanga, Colombia: a case-control study. PLoS Negl Trop Dis. 2020. https://doi.org/10.1371/journal.pntd.0008375.
Posovszky C, Buderus S, Classen M, Lawrenz B, Keller KM, Koletzko S. Acute infectious gastroenteritis in infancy and childhood. Deutsches Arzteblatt Int. 2020;117(37):615–24. https://doi.org/10.3238/arztebl.2020.0615.
Salami A, Fakih H, Chakkour M, Salloum L, Bahmad HF, Ghssein G. Prevalence, risk factors and seasonal variations of different Enteropathogens in Lebanese hospitalized children with acute gastroenteritis. BMC Pediatr. 2019;19:137. https://doi.org/10.1186/s12887-019-1513-8.
Muendo C, Laving A, Kumar R, Osano B, Egondi T, Njuguna P. Prevalence of rotavirus infection among children with acute diarrhoea after rotavirus vaccine introduction in Kenya, a hospital cross-sectional study. BMC Pediatr. 2018;18(1):323. https://doi.org/10.1186/s12887-018-1291-8.
Li Y, Fan X, Yu G, Wei P, Wang Y, Guo H. An acute gastroenteritis outbreak associated with breakfast contaminated with norovirus by asymptotic food handler at a kindergarten in Shenzhen China. BMC Infect Dis. 2021;21:54. https://doi.org/10.1186/s12879-021-05762-z.
Trevethan R. Sensitivity, specificity, and predictive values: foundations, pliabilities, and pitfalls in research and practice. Front Public Health. 2017;5:307. https://doi.org/10.3389/fpubh.2017.00307.
Lucero Y, Lagomarcino AJ, Espinoza M, Kawakami N, Mamani N, Huerta N, Del Canto F, Farfán M, Sawaguchi Y, George S, O’Ryan M. Norovirus compared to other relevant etiologies of acute gastroenteritis among families from a semirural county in Chile. Int J Infect Dis. 2020;101:353–60. https://doi.org/10.1016/j.ijid.2020.10.013.
El Qazoui M, Oumzil H, Baassi L, El Omari N, Sadki K, Amzazi S, Benhafid M, El Aouad R. Rotavirus and norovirus infections among acute gastroenteritis children in Morocco. BMC Infect Dis. 2014;14:300. https://doi.org/10.1186/1471-2334-14-300.
Zaraket R, Salami A, Bahmad M, El Roz A, Khalaf B, Ghssein G, Bahmad HF. Prevalence, risk factors, and clinical characteristics of rotavirus and adenovirus among Lebanese hospitalized children with acute gastroenteritis. Heliyon. 2020;6(6):e04248. https://doi.org/10.1016/j.heliyon.2020.e04248.
de Oliveira Ferreiraa CE, Rabonia SM, Pereiraa LA, Nogueiraa MB, Vidala LR, Almeidaa SM. Viral acute gastroenteritis: clinical and epidemiological features of co-infected patients. Braz J Infect Dis. 2012;16(3):267–72.
Dey SK, Sharif N, Sarkar OS, Sarkar MK, Talukder AA, Phan T, Ushijima H. Molecular epidemiology and surveillance of circulating rotavirus among children with gastroenteritis in Bangladesh during 2014–2019. PLoS ONE. 2020;15(11):e0242813. https://doi.org/10.1371/journal.pone.0242813.
Ezeonwu B, Ibeneme C, Aneke F, Oguonu T. Clinical features of acute gastroenteritis in children at university of Nigeria teaching hospital, Ituku-ozalla. Enugu Ann Med Health Sci Res. 2013;3(3):361–4. https://doi.org/10.4103/2141-9248.117948.
Agbla JM, Esona MD, Agbankpe AJ, Capo-Chichi A, Gautam R, Dougnon TV, Razack O, Bowen MD, Bankole HS. Molecular characteristics of rotavirus genotypes circulating in the south of Benin, 2016–2018. BMC Res Notes. 2020;13(1):485. https://doi.org/10.1186/s13104-020-05332-7.
Cho SR, Chae SJ, Jung S, Choi W, Han MG, Yoo CK, Lee DY. Trends in acute viral gastroenteritis among children aged ≤ 5 years through the national surveillance system in South Korea 2013–2019. J Med Virol. 2020;93(8):4875–82.
van Dongen JA, Rouers ED, Schuurman R, Bonten MJ, Bruijning-Verhagen P. Acute gastroenteritis disease burden in infants with medical risk conditions in the Netherlands. J Pediatr Infect Dis. 2020;40(4):300. https://doi.org/10.1097/INF.0000000000003002.
Louya VM, Tsague BN, Ntoumi F, Vouvoungui C, Kobawila SC. High prevalence of norovirus and rotavirus co-infection in children with acute gastroenteritis hospitalised in Brazzaville, Republic of Congo. Trop Med Int Health. 2019;24:1427–33. https://doi.org/10.1111/tmi.13317.
Tatte VS, Gopalkrishna V. Detection of different enteric viruses in children with diarrheal disease: evidence of the high frequency of mixed infections. Access Microbiol. 2019;1(2):e000010. https://doi.org/10.1099/acmi.0.000010.
Thangjui S, Sripirom N, Titichoatrattana S, Mekmullica J. Accuracy and cross-reactivity of rapid diagnostic tests for norovirus and rotavirus in a real clinical setting. Infect Chemother. 2020;52(3):360–8. https://doi.org/10.3947/ic.2020.52.3.360.
Li J, Yang Y, Liang ZC, Gao ZY, Jia L, Liu BW, Chen LJ, Wang QY. Analysis of pathogenic composition and clinical characteristics of viral acute gastroenteritis in children under five years old in Beijing. Zhonghua yu Fang yi xue za zhi [Chin J Prevent Med]. 2020;54(10):1104–10. https://doi.org/10.3760/cma.j.cn112150-20191129-00892.
Van Trang N, Vu HT, Le NT, Huang P, Jiang X, Anh DD. Association between norovirus and rotavirus infection and histo-blood group antigen types in Vietnamese children. J Clinic Microbiol. 2014;52(5):1366–74. https://doi.org/10.1128/JCM.02927-13.
Amarasiri M, Sano D. Specific interactions between human norovirus and environmental matrices: effects on the virus ecology. Viruses. 2019;11(3):224. https://doi.org/10.3390/v11030224.
Das S, Sahoo GC, Das P, Singh UK, Jaiswal AK, Singh P, Kumar R. Evaluating the impact of breastfeeding on rotavirus antigenemia and disease severity in indian children. PLoS ONE. 2016;11(2):e0146243. https://doi.org/10.1371/journal.pone.0146243.
Furuya K, Nakajima H, Sasaki Y, Urita Y. An examination of co-infection in acute gastroenteritis and histo-blood group antigens leading to viral infection susceptibility. Biomed Rep. 2016;4(3):331–4. https://doi.org/10.3892/br.2016.585.
Motayo BO, Adeniji AJ, Faneye AO. First molecular detection and VP7 (G) genotyping of group a rotavirus by semi-nested RT-PCR from sewage in Nigeria. Rev Inst Med Trop S Paulo. 2016;58:74. https://doi.org/10.1590/S1678-9946201658074.
Tang JW, Wilson P, Shetty N, Noakes CJ. Aerosol-Transmitted infections-a new consideration for public health and infection control teams. Curr Treat Options Infect Dis. 2015;7(3):176–201. https://doi.org/10.1007/s40506-015-0057-1.
Lartey BL, Quaye O, Damanka SA, Agbemabiese CA, Armachie J, Dennis FE, Enweronu-Laryea C, Armah GE. Understanding pediatric norovirus epidemiology: a decade of study among Ghanaian children. Viruses. 2020;12(11):1321. https://doi.org/10.3390/v12111321.
Leung AK, Hon KL. Paediatrics: how to manage viral gastroenteritis. Drugs Context. 2021. https://doi.org/10.7573/dic.2020-11-7.