{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T19:47:52Z","timestamp":1788983272620,"version":"build-2803163510"},"reference-count":41,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2021,1,28]],"date-time":"2021-01-28T00:00:00Z","timestamp":1611792000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"icddr,b core fund","award":["N\/A"],"award-info":[{"award-number":["N\/A"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Non-typhoidal Salmonella (NTS) is one of the less focused on infections and is often associated with faulty child nutrition in the developing world. This study aimed to evaluate the association of NTS infection with growth faltering among children under the age of five. We analyzed data from 378 fecal NTS positive children with both moderate-to-severe diarrhea (MSD) and asymptomatic infection from the seven countries of South Asia and sub-Saharan Africa during enrolment and on day 60 follow up in the Global Enteric Multicenter Study (GEMS) for the period of December 2007 to March 2011. Children not associated with fecal NTS (n = 1134) were randomly selected from the same dataset (1:3 ratio) as a comparison group. The association between an explanatory variable and the outcome variable was longitudinally tested using generalized estimating equations (GEE), where the dependent variables were height-for-age (HAZ), weight-for-age (WAZ), and weight-for-height (WHZ) z-score, and the independent variable was the presence of fecal NTS. The GEE multivariable model identified a negative association between fecal NTS and WAZ (coefficient: \u22120.19; 95% CI (confidence interval): \u22120.33, \u22120.04, and p value = 0.010), WHZ (coef: \u22120.19; 95% CI: \u22120.34, \u22120.05, and p value = 0.007), and HAZ (coef: \u22120.13; 95% CI: \u22120.27, \u22120.01, and p value = 0.073) after adjusting for age, gender, diarrhea, breastfeeding status, mothers\u2019 education, number of children under the age of five, household size by the number of people regularly sleep at the home, handwashing practice, source of drinking water, wealth index, presence of co-pathogens, comorbidity, and study sites. In the GEMS, where children were followed during 50\u201390 days of enrolment, the presence of fecal NTS harmed the child\u2019s anthropometric outcomes. Minimizing potential exposure to NTS is needed to curb worsening child undernutrition.<\/jats:p>","DOI":"10.3390\/nu13020392","type":"journal-article","created":{"date-parts":[[2021,1,28]],"date-time":"2021-01-28T01:22:23Z","timestamp":1611796943000},"page":"392","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Association between Non-Typhoidal Salmonella Infection and Growth in Children under 5 Years of Age: Analyzing Data from the Global Enteric Multicenter Study"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7499-7278","authenticated-orcid":false,"given":"Rina","family":"Das","sequence":"first","affiliation":[{"name":"Nutrition and Clinical Services Division, icddr,b, Dhaka 1212, Bangladesh"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3452-8367","authenticated-orcid":false,"given":"Md. Ahshanul","family":"Haque","sequence":"additional","affiliation":[{"name":"Nutrition and Clinical Services Division, icddr,b, Dhaka 1212, Bangladesh"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohammod Jobayer","family":"Chisti","sequence":"additional","affiliation":[{"name":"Nutrition and Clinical Services Division, icddr,b, Dhaka 1212, Bangladesh"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abu Sayed Golam","family":"Faruque","sequence":"additional","affiliation":[{"name":"Nutrition and Clinical Services Division, icddr,b, Dhaka 1212, Bangladesh"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tahmeed","family":"Ahmed","sequence":"additional","affiliation":[{"name":"Nutrition and Clinical Services Division, icddr,b, Dhaka 1212, Bangladesh"},{"name":"James P. Grant School of Public Health, BRAC University, Dhaka 1212, Bangladesh"},{"name":"Department of Global Health, University of Washington, Seattle, WA 98104, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Kariuki, S., Mbae, C., Van Puyvelde, S., Onsare, R., Kavai, S., Wairimu, C., Ngetich, R., Clemens, J., and Dougan, G. (2020). High relatedness of invasive multi-drug resistant non-typhoidal Salmonella genotypes among patients and asymptomatic carriers in endemic informal settlements in Kenya. PLoS Negl. Trop. Dis., 14.","DOI":"10.1371\/journal.pntd.0008440"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1086\/650733","article-title":"The global burden of nontyphoidal Salmonella gastroenteritis","volume":"50","author":"Majowicz","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1016\/S0140-6736(12)60034-8","article-title":"Global malaria mortality between 1980 and 2010: A systematic analysis","volume":"379","author":"Murray","year":"2012","journal-title":"Lancet"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2197","DOI":"10.1016\/S0140-6736(12)61689-4","article-title":"Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: A systematic analysis for the Global Burden of Disease Study 2010","volume":"380","author":"Murray","year":"2012","journal-title":"Lancet"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1177\/000992280404300906","article-title":"Risk factors for development of nontyphoid Salmonella bacteremia","volume":"43","author":"Wysoki","year":"2004","journal-title":"Clin. Pediatr."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2489","DOI":"10.1016\/S0140-6736(11)61752-2","article-title":"Invasive non-typhoidal salmonella disease: An emerging and neglected tropical disease in Africa","volume":"379","author":"Feasey","year":"2012","journal-title":"Lancet"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.1099\/jmm.0.022319-0","article-title":"Molecular characterization of antimicrobial resistance in non-typhoidal salmonellae associated with systemic manifestations from India","volume":"59","author":"Menezes","year":"2010","journal-title":"J. Med. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Jabeen, K., Zafar, A., Irfan, S., Khan, E., Mehraj, V., and Hasan, R. (2010). Increase in isolation of extended spectrum beta lactamase producing multidrug resistant non typhoidal Salmonellae in Pakistan. BMC Infect. Dis., 10.","DOI":"10.1186\/1471-2334-10-101"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.trstmh.2008.09.009","article-title":"Distribution trends of Salmonella serovars in India (2001\u20132005)","volume":"103","author":"Kumar","year":"2009","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.trstmh.2011.10.004","article-title":"The decline of typhoid and the rise of non-typhoid salmonellae and fungal infections in a changing HIV landscape: Bloodstream infection trends over 15 years in southern Vietnam","volume":"106","author":"Nga","year":"2012","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1016\/j.trstmh.2008.01.019","article-title":"Bacteraemia due to non-typhoidal Salmonella in Thailand: Clinical and microbiological analysis","volume":"102","author":"Kiratisin","year":"2008","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1086\/318457","article-title":"Nontyphoidal salmonellosis","volume":"32","author":"Acheson","year":"2001","journal-title":"Clin. Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1016\/j.bpg.2012.11.003","article-title":"Nutritional consequences of chronic diarrhoea","volume":"26","author":"Gorospe","year":"2012","journal-title":"Best Pract. Res. Clin. Gastroenterol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Shahunja, K.M., Leung, D.T., Ahmed, T., Bardhan, P.K., Ahmed, D., Qadri, F., Ryan, E.T., and Chisti, M.J. (2015). Factors Associated with Non-typhoidal Salmonella Bacteremia versus Typhoidal Salmonella Bacteremia in Patients Presenting for Care in an Urban Diarrheal Disease Hospital in Bangladesh. PLoS Negl. Trop. Dis., 9.","DOI":"10.1371\/journal.pntd.0004066"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1097\/01.inf.0000202066.02212.ff","article-title":"Salmonella bacteremia in Kenyan children","volume":"25","author":"Brent","year":"2006","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1056\/NEJMoa040275","article-title":"Bacteremia among children admitted to a rural hospital in Kenya","volume":"352","author":"Berkley","year":"2005","journal-title":"N. Engl. J. Med."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"S225","DOI":"10.1093\/cid\/cis787","article-title":"Some epidemiologic, clinical, microbiologic, and organizational assumptions that influenced the design and performance of the Global Enteric Multicenter Study (GEMS)","volume":"55","author":"Farag","year":"2012","journal-title":"Clin. Infect. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"S232","DOI":"10.1093\/cid\/cis753","article-title":"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","volume":"55","author":"Kotloff","year":"2012","journal-title":"Clin. Infect. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"S215","DOI":"10.1093\/cid\/cis761","article-title":"The Global Enteric Multicenter Study (GEMS): Impetus, rationale, and genesis","volume":"55","author":"Levine","year":"2012","journal-title":"Clin. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/S0140-6736(13)60844-2","article-title":"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","volume":"382","author":"Kotloff","year":"2013","journal-title":"Lancet"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1093\/cid\/ciu468","article-title":"Shigella isolates from the global enteric multicenter study inform vaccine development","volume":"59","author":"Livio","year":"2014","journal-title":"Clin. Infect. Dis."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"S246","DOI":"10.1093\/cid\/cis788","article-title":"Statistical methods in the Global Enteric Multicenter Study (GEMS)","volume":"55","author":"Blackwelder","year":"2012","journal-title":"Clin. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Sow, S.O., Muhsen, K., Nasrin, D., Blackwelder, W.C., Wu, Y., Farag, T.H., Panchalingam, S., Sur, D., Zaidi, A.K.M., and Faruque, A.S.G. (2016). The Burden of Cryptosporidium Diarrheal Disease among Children <24 Months of Age in Moderate\/High Mortality Regions of Sub-Saharan Africa and South Asia, Utilizing Data from the Global Enteric Multicenter Study (GEMS). PLoS Negl. Trop. Dis., 10.","DOI":"10.1371\/journal.pntd.0004729"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"S294","DOI":"10.1093\/cid\/cis754","article-title":"Diagnostic microbiologic methods in the GEMS-1 case\/control study","volume":"55","author":"Panchalingam","year":"2012","journal-title":"Clin. Infect. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"242","DOI":"10.3201\/eid2101.140795","article-title":"Microbiota That Affect Risk for Shigellosis in Children in Low-Income Countries","volume":"21","author":"Lindsay","year":"2015","journal-title":"Emerg. Infect. Dis. J."},{"key":"ref_26","unstructured":"Cogill, B. (2003). Anthropometric Indicators Measurement Guide, Food and Nutrition Technical Assistance Project, Academy for Educational Development."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"381","DOI":"10.4103\/0256-4947.67076","article-title":"Prevalence of malnutrition in Saudi children: A community-based study","volume":"30","author":"Foster","year":"2010","journal-title":"Ann. Saudi Med."},{"key":"ref_28","unstructured":"World Health Organization (2006). WHO Child Growth Standards: Length\/Height-for-Age, Weight-for-Age, Weight-for-Length, Weight -for-Height and Body Mass Index-for-Age: Methods and Development, World Health Organization."},{"key":"ref_29","unstructured":"World Health Organization (2012). WHO Child Growth Standards, SAS Macro, version 3.2.2, World Health Organization."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1057","DOI":"10.1093\/ije\/20.4.1057","article-title":"Methodological issues in diarrhoeal diseases epidemiology: Definition of diarrhoeal episodes","volume":"20","author":"Baqui","year":"1991","journal-title":"Int. J. Epidemiol."},{"key":"ref_31","first-page":"115","article-title":"Estimating wealth effects without expenditure data\u2014Or tears: An application to educational enrollments in states of India","volume":"38","author":"Filmer","year":"2001","journal-title":"Demography"},{"key":"ref_32","unstructured":"Diggle, P., Liang, K.-Y., and Zeger, S.L. (1994). Longitudinal Data Analysis, Oxford University Press."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e025439","DOI":"10.1136\/bmjopen-2018-025439","article-title":"Relative contributions of the correlates of stunting in explaining the mean length-for-age z-score difference between 24-month-old stunted and non-stunted children living in a slum of Dhaka, Bangladesh: Results from a decomposition analysis","volume":"9","author":"Das","year":"2019","journal-title":"BMJ Open"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1467","DOI":"10.1111\/j.1365-3156.2009.02399.x","article-title":"Invasive non-typhoidal Salmonella in Mozambican children","volume":"14","author":"Mandomando","year":"2009","journal-title":"Trop. Med. Int. Health"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1097\/MD.0b013e31828a01f9","article-title":"Inherited IL-12p40 Deficiency: Genetic, Immunologic, and Clinical Features of 49 Patients From 30 Kindreds: Erratum","volume":"92","author":"Prando","year":"2013","journal-title":"Medicine"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"579","DOI":"10.3390\/nu5020579","article-title":"Effect of malnutrition on the expression of cytokines involved in Th1 cell differentiation","volume":"5","author":"Miliar","year":"2013","journal-title":"Nutrients"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/S0016-5085(19)32926-9","article-title":"Pathophysiology of Salmonella Diarrhea in the Rhesus Monkey: Intestinal Transport, Morphological and Bacteriological Studies","volume":"67","author":"Rout","year":"1974","journal-title":"Gastroenterology"},{"key":"ref_38","first-page":"423","article-title":"Abdominal ultrasonographic findings in typhoid fever: A comparison between typhoid patients and those with non-typhoidal Salmonella and Campylobacter jejuni enterocolitis","volume":"43","author":"Kobayashi","year":"2012","journal-title":"Southeast Asian J. Trop. Med. Public Health"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1017\/S0031182005007353","article-title":"Asymptomatic giardiasis and growth in young children; a longitudinal study in Salvador, Brazil","volume":"131","author":"Prado","year":"2005","journal-title":"Parasitology"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1093\/tropej\/50.2.90","article-title":"Effect of Giardia infection on growth and psychomotor development of children aged 0\u20135 years","volume":"50","author":"Simsek","year":"2004","journal-title":"J. Trop. Pediatr."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"17124","DOI":"10.1038\/s41598-019-53533-3","article-title":"Determinants of Campylobacter infection and association with growth and enteric inflammation in children under 2 years of age in low-resource settings","volume":"9","author":"Haque","year":"2019","journal-title":"Sci. Rep."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/13\/2\/392\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:16:22Z","timestamp":1760159782000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/13\/2\/392"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,28]]},"references-count":41,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["nu13020392"],"URL":"https:\/\/doi.org\/10.3390\/nu13020392","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,28]]}}}