Enteric viral pathogens and child growth among under-five children: findings from South Asia and sub-Saharan Africa.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
15 Jun 2024
15 Jun 2024
Historique:
received:
17
01
2024
accepted:
07
06
2024
medline:
16
6
2024
pubmed:
16
6
2024
entrez:
15
6
2024
Statut:
epublish
Résumé
Enteric viral pathogens are associated with a significant burden of childhood morbidity and mortality. We investigated the relationship between viral pathogens and child growth among under-5 children. We analyzed data from 5572/22,567 children enrolled in the Global Enteric Multicenter Study across seven study sites (2007-2011). Multiple linear regression was used to examine the association between the viral pathogens and changes of length/height-for-age (HAZ), weight-for-age (WAZ), and weight-for-length/height (WHZ) z-scores, stratified by diarrheal symptoms and adjusted for potential covariates. Rotavirus (18.51%) and norovirus (7.33%) were the most prevalent enteric viral pathogens among symptomatic and asymptomatic under-5 children, respectively. Infection with individual enteric viral pathogens hurts child growth in asymptomatic children. However, the relationship with HAZ was less clear and statistically non-significant. On the other hand, the combined viral pathogens demonstrated a strong negative influence on child growth [WAZ: β coef.: - 0.10 (95%, CI - 0.15, - 0.05); P < 0.001 and WHZ: β: - 0.12 (95% CI - 0.17, - 0.07); P < 0.001] among asymptomatic children. Infection with any viral pathogen was associated with growth shortfalls [HAZ: β: - 0.05 (95% CI - 0.09, 0.00); P = 0.03 and WAZ: β: - 0.11 (95% CI - 0.16, - 0.07); P < 0.001 and WHZ: β: - 0.13 (95% CI - 0.18, - 0.09); P < 0.001], though the relationship with HAZ was less evident and became statistically non-significant in older children. Notably, among symptomatic children with moderate-to-severe diarrhea, individual enteric viral pathogens, as well as the combined effects of these pathogens [WHZ: β: 0.07; (95% CI 0.01, 0.14); P = 0.03] and the presence of any virus [HAZ: β: 0.09 (95% CI 0.05, 0.13) & WAZ: β: 0.08 (95% CI 0.03, 0.12); P < 0.001], exhibited positive effects on child growth. While previous studies hypothesized that several viral pathogens had a conflicting controversial role in child growth, we find clear indications that enteric viral pathogens are associated with growth shortfalls, specifically among asymptomatic children. These findings highlight the need for preventive strategies targeting children with enteric viral pathogens, which could address the consequences of growth faltering.
Identifiants
pubmed: 38879558
doi: 10.1038/s41598-024-64374-0
pii: 10.1038/s41598-024-64374-0
doi:
Types de publication
Journal Article
Multicenter Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
13871Subventions
Organisme : Bill & Melinda Gates Foundation
ID : INV-002050
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
WHO. Diarrhoeal disease. https://www.who.int/news-room/fact-sheets/detail/diarrhoeal-disease (2017).
Troeger, C. et al. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of diarrhoea in 195 countries: A systematic analysis for the Global Burden of Disease Study 2016. Lancet. Infect. Dis. 18, 1211–1228 (2018).
doi: 10.1016/S1473-3099(18)30362-1
Hartman, R. M. et al. Risk factors for mortality among children younger than age 5 years with severe diarrhea in low- and middle-income countries: Findings from the world health organization-coordinated global rotavirus and pediatric diarrhea surveillance networks. Clin. Infect. Dis. 76, e1047–e1053. https://doi.org/10.1093/cid/ciac561 (2022).
doi: 10.1093/cid/ciac561
pmcid: 9907489
Rogawski, E. T. & Guerrant, R. L. The burden of enteropathy and “subclinical” infections. Pediatr. Clin. N. Am. 64, 815–836. https://doi.org/10.1016/j.pcl.2017.03.003 (2017).
doi: 10.1016/j.pcl.2017.03.003
Musa, T. H., Musa, H. H., Ali, E. A. & Musa, N. E. Prevalence of malnutrition among children under five years old in Khartoum State Sudan. Pol. Ann. Med. 21, 1–7 (2014).
doi: 10.1016/j.poamed.2014.01.001
Wong, H. J., Moy, F. M. & Nair, S. Risk factors of malnutrition among preschool children in Terengganu, Malaysia: A case control study. BMC Public Health 14, 1–10 (2014).
doi: 10.1186/1471-2458-14-S3-S1
Checkley, W. et al. Multi-country analysis of the effects of diarrhoea on childhood stunting. Int. J. Epidemiol. 37, 816–830 (2008).
doi: 10.1093/ije/dyn099
pubmed: 18567626
pmcid: 2734063
Black, R. E., Brown, K. H. & Becker, S. Effects of diarrhea associated with specific enteropathogens on the growth of children in rural Bangladesh. Pediatrics 73, 799–805 (1984).
doi: 10.1542/peds.73.6.799
pubmed: 6374599
Qadri, F. et al. Mucosal and systemic immune responses in patients with diarrhea due to CS6-expressing enterotoxigenic Escherichia coli. Infect. Immun. 75, 2269–2274 (2007).
doi: 10.1128/IAI.01856-06
pubmed: 17296752
pmcid: 1865745
Bernard-Raichon, L. & Cadwell, K. Immunomodulation by enteric viruses. Annu. Rev. Virol. 10, 477–502 (2023).
doi: 10.1146/annurev-virology-111821-112317
pubmed: 37380186
Kotloff, K. L. et al. The Global Enteric Multicenter Study (GEMS) of diarrheal disease in infants and young children in developing countries: Epidemiologic and clinical methods of the case/control study. Clin. Infect. Dis. 55, S232–S245 (2012).
doi: 10.1093/cid/cis753
pubmed: 23169936
pmcid: 3502307
Nitiema, L. W. et al. Burden of rotavirus and other enteropathogens among children with diarrhea in Burkina Faso. Int. J. Infect. Dis. 15, e646–e652 (2011).
doi: 10.1016/j.ijid.2011.05.009
pubmed: 21763172
Chissaque, A. et al. Rotavirus A infection in children under five years old with a double health problem: Undernutrition and diarrhoea–a cross-sectional study in four provinces of Mozambique. BMC Infect. Dis. 21, 1–13 (2021).
doi: 10.1186/s12879-020-05718-9
Rogawski, E. T. et al. Use of quantitative molecular diagnostic methods to investigate the effect of enteropathogen infections on linear growth in children in low-resource settings: Longitudinal analysis of results from the MAL-ED cohort study. Lancet Glob. Health 6, e1319–e1328 (2018).
doi: 10.1016/S2214-109X(18)30351-6
pubmed: 30287125
pmcid: 6227248
Troeger, H. et al. Structural and functional changes of the duodenum in human norovirus infection. Gut 58, 1070–1077 (2009).
doi: 10.1136/gut.2008.160150
pubmed: 19036950
Budge, S., Parker, A. H., Hutchings, P. T. & Garbutt, C. Environmental enteric dysfunction and child stunting. Nutr. Rev. 77, 240–253 (2019).
doi: 10.1093/nutrit/nuy068
pubmed: 30753710
pmcid: 6394759
Semba, R. D. et al. Child stunting is associated with low circulating essential amino acids. EBioMedicine 6, 246–252 (2016).
doi: 10.1016/j.ebiom.2016.02.030
pubmed: 27211567
pmcid: 4856740
Nuss, E. T. & Tanumihardjo, S. A. Quality protein maize for Africa: Closing the protein inadequacy gap in vulnerable populations. Adv. Nutr. 2, 217–224 (2011).
doi: 10.3945/an.110.000182
pubmed: 22332054
pmcid: 3090170
Liu, Y. et al. Gut-muscle axis and sepsis-induced myopathy: The potential role of gut microbiota. Biomed. Pharmacother. 163, 114837 (2023).
doi: 10.1016/j.biopha.2023.114837
pubmed: 37156115
Sturgeon, J. P. et al. Inflammation: the driver of poor outcomes among children with severe acute malnutrition?. Nutr. Rev. 81(12), 1636–1652 (2023).
doi: 10.1093/nutrit/nuad030
pubmed: 36977352
pmcid: 10639108
Stephanie, A. B. et al. Antibiotic use attributable to specific aetiologies of diarrhoea in children under 2 years of age in low-resource settings: A secondary analysis of the MAL-ED birth cohort. BMJ Open 12, e058740. https://doi.org/10.1136/bmjopen-2021-058740 (2022).
doi: 10.1136/bmjopen-2021-058740
Ternhag, A., Asikainen, T., Giesecke, J. & Ekdahl, K. A meta-analysis on the effects of antibiotic treatment on duration of symptoms caused by infection with Campylobacter species. Clin. Infect. Dis. 44, 696–700 (2007).
doi: 10.1086/509924
pubmed: 17278062
Das, R., Haque, M. A., Chisti, M. J., Faruque, A. S. G. & Ahmed, T. Associated factors, post infection child growth, and household cost of invasive enteritis among under 5 children in Bangladesh. Sci. Rep. 11, 12738. https://doi.org/10.1038/s41598-021-92132-z (2021).
doi: 10.1038/s41598-021-92132-z
pubmed: 34140589
pmcid: 8211821
Nakawesi, J. S., Wobudeya, E., Ndeezi, G., Mworozi, E. A. & Tumwine, J. K. Prevalence and factors associated with rotavirus infection among children admitted with acute diarrhea in Uganda. BMC Pediatr. 10, 1–5 (2010).
doi: 10.1186/1471-2431-10-69
Koyuncu, A., Simuyandi, M., Bosomprah, S. & Chilengi, R. Nutritional status, environmental enteric dysfunction, and prevalence of rotavirus diarrhoea among children in Zambia. PLoS One 15, e0240258 (2020).
doi: 10.1371/journal.pone.0240258
pubmed: 33007035
pmcid: 7531814
Das, S. K. et al. Long-term impact of changing childhood malnutrition on rotavirus diarrhoea: Two decades of adjusted association with climate and socio-demographic factors from urban Bangladesh. PLoS One 12, e0179418 (2017).
doi: 10.1371/journal.pone.0179418
pubmed: 28877163
pmcid: 5587254
Raheem, A., Liang, L., Zhang, G. & Cui, S. Modulatory effects of probiotics during pathogenic infections with emphasis on immune regulation. Front. Immunol. 12, 616713 (2021).
doi: 10.3389/fimmu.2021.616713
pubmed: 33897683
pmcid: 8060567
Jeong, H. S., Jeong, A. & Cheon, D. S. Epidemiology of astrovirus infection in children. Korean J. Pediatr. 55, 77–82. https://doi.org/10.3345/kjp.2012.55.3.77 (2012).
doi: 10.3345/kjp.2012.55.3.77
pubmed: 22474461
pmcid: 3315622
Kotloff, K. L. et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): A prospective, case-control study. Lancet 382, 209–222 (2013).
doi: 10.1016/S0140-6736(13)60844-2
pubmed: 23680352
Das, R. et al. Symptomatic and asymptomatic enteric protozoan parasitic infection and their association with subsequent growth parameters in under five children in South Asia and sub-Saharan Africa. PLoS Neglect. Trop. Dis. 17, e0011687. https://doi.org/10.1371/journal.pntd.0011687 (2023).
doi: 10.1371/journal.pntd.0011687
Panchalingam, S. et al. Diagnostic microbiologic methods in the GEMS-1 case/control study. Clin. Infect. Dis. 55, S294–S302 (2012).
doi: 10.1093/cid/cis754
pubmed: 23169941
pmcid: 3502308
Filmer, D. & Pritchett, L. H. Estimating wealth effects without expenditure data—or tears: An application to educational enrollments in states of India. Demography 38, 115–132 (2001).
pubmed: 11227840
Shrestha, N. Factor analysis as a tool for survey analysis. Am. J. Appl. Math. Stat. 9, 4–11 (2021).
doi: 10.12691/ajams-9-1-2
Vatcheva, K. P., Lee, M., McCormick, J. B. & Rahbar, M. H. Multicollinearity in regression analyses conducted in epidemiologic studies. Epidemiology https://doi.org/10.4172/2161-1165.1000227 (2016).
doi: 10.4172/2161-1165.1000227
pubmed: 27274911