Fecal Contamination in Child Play Spaces and on Child Hands Are Associated with Subsequent Adverse Child Developmental Outcomes in Rural Democratic Republic of the Congo: REDUCE Prospective Cohort Study

Christine Marie George Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Christine Marie George in
Current site
Google Scholar
PubMed
Close
,
Alves Birindwa Food for the Hungry, Nutrition, Washington, District of Columbia;

Search for other papers by Alves Birindwa in
Current site
Google Scholar
PubMed
Close
,
Sara Beck Department of Civil Engineering, University of British Columbia, Vancouver, British Columbia, Canada;

Search for other papers by Sara Beck in
Current site
Google Scholar
PubMed
Close
,
Timothy R. Julian Eawag, Swiss Federal Institute of Aquatic Science and Technology, Duebendorf, Switzerland;

Search for other papers by Timothy R. Julian in
Current site
Google Scholar
PubMed
Close
,
Jennifer Kuhl Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Jennifer Kuhl in
Current site
Google Scholar
PubMed
Close
,
Camille Williams Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Camille Williams in
Current site
Google Scholar
PubMed
Close
,
Nicole Coglianese Food for the Hungry, Nutrition, Washington, District of Columbia;

Search for other papers by Nicole Coglianese in
Current site
Google Scholar
PubMed
Close
,
Elizabeth D. Thomas Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Elizabeth D. Thomas in
Current site
Google Scholar
PubMed
Close
,
Sarah Bauler Food for the Hungry, Nutrition, Washington, District of Columbia;

Search for other papers by Sarah Bauler in
Current site
Google Scholar
PubMed
Close
,
Ruthly François Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Ruthly François in
Current site
Google Scholar
PubMed
Close
,
Angela Ng Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Angela Ng in
Current site
Google Scholar
PubMed
Close
,
Amani Sanvura Presence Food for the Hungry, Nutrition, Washington, District of Columbia;

Search for other papers by Amani Sanvura Presence in
Current site
Google Scholar
PubMed
Close
,
Bisimwa Rusanga Jean Claude Food for the Hungry, Nutrition, Washington, District of Columbia;

Search for other papers by Bisimwa Rusanga Jean Claude in
Current site
Google Scholar
PubMed
Close
,
Fahmida Tofail International Centre for Diarrhoeal Disease Research, Child Development Unit, Dhaka, Bangladesh

Search for other papers by Fahmida Tofail in
Current site
Google Scholar
PubMed
Close
,
Jamie Perin Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Jamie Perin in
Current site
Google Scholar
PubMed
Close
,
Patrick Mirindi Food for the Hungry, Nutrition, Washington, District of Columbia;

Search for other papers by Patrick Mirindi in
Current site
Google Scholar
PubMed
Close
, and
Lucien Bisimwa Cirhuza Food for the Hungry, Nutrition, Washington, District of Columbia;

Search for other papers by Lucien Bisimwa Cirhuza in
Current site
Google Scholar
PubMed
Close
Restricted access

ABSTRACT.

The objective of the Reducing Enteropathy, Undernutrition, and Contamination in the Environment (REDUCE) program is to identify exposure pathways to fecal pathogens that are significant contributors to morbidity among young children in the Democratic Republic of the Congo (DRC), and on developing and evaluating scalable interventions to reduce fecal contamination from these pathways. This prospective cohort study of 270 children under 5 years of age was conducted in rural South Kivu, DRC, to investigate the association between Escherichia coli in hand rinse, soil, food, object, surface, stored water, and water source samples and child developmental outcomes. Child developmental outcomes were assessed by communication, fine motor, gross motor, personal social, problem-solving, and combined scores measured by the Extended Ages and Stages Questionnaire (EASQ) at a 6-month follow-up. Children having E. coli present in the soil in their play spaces had significantly lower combined EASQ z scores (coefficient: −0.38 (95% CI: −0.73, −0.03)). E. coli on children’s hands was associated with lower communication EASQ z scores (−0.37 (95% CI: −0.0.10, −0.01), and E. coli in stored drinking water was associated with lower gross motor EASQ z scores (−0.40 (95% CI: −0.68, −0.12). In the REDUCE cohort study, E. coli in soil in child play spaces, on children’s hands, and in stored drinking water was associated with lower developmental outcome scores (communication, gross motor, fine motor, and problem-solving skills). These results suggest the need for interventions to reduce fecal contamination in the household environment to protect the cognitive development of susceptible pediatric populations in rural DRC.

    • Supplemental Materials (PDF 23 KB)

Author Notes

Address correspondence to Christine Marie George, Associate Professor, Department of International Health, Program in Global Disease Epidemiology and Control, Johns Hopkins Bloomberg School of Public Health, 615 N. Wolfe St., Rm. E5535, Baltimore, MD 21205-2103. E-mail: cmgeorge@jhu.edu

Authors’ addresses: Christine Marie George, Jennifer Kuhl, Camille Williams, Elizabeth Thomas, Ruthly François, Angela Ng, and Jamie Perin, Department of International Health, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, E-mails: cgeorg19@jhu.edu, jennifer.m.kuhl@gmail.com, cwill302@jhmi.edu, liz.thomas@jhu.edu, ruthlyfrancois@gmail.com, angelang1201@gmail.com, and jperin@jhu.edu. Alves Birindwa, Nicole Coglianese, Sarah Bauler, Amani Sanvura Presence, Bisimwa Rusanga Jean Claude, Patrick Mirindi, and Lucien Bisimwa Cirhuza, Food for the Hungry, Nutrition, Washington, DC, E-mails: namuneshaalves4@gmail.com, nicole.coglianese@gmail.com, sarahbauler@gmail.com, presencesanvura@gmail.com, jcbisrus@gmail.com, patrick.mirindi@gmail.com, and lucienbis86@gmail.com. Sara Beck, Department of Civil Engineering, University of British Columbia, Vancouver, BC, Canada, E-mail: saraebeck1@gmail.com. Timothy Julian, Department of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (Eawag), Dübendorf, Switzerland, E-mail: tim.julian@eawag.ch. Fahmida Tofail, International Centre for Diarrhoeal Disease Research Bangladesh, Child Development Unit, Dhaka, Bangladesh, E-mail: ftofail@icddrb.org.

  • 1.

    Black MM , Walker SP , Fernald LC , Andersen CT , DiGirolamo AM , Lu C , McCoy DC , Fink G , Shawar YR , Shiffman J , 2017. Advancing early childhood development: from science to scale 1: early childhood development coming of age: science through the life course. Lancet 389: 77.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

     GBD Diarrhoeal Diseases Collaborators, 2017. Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infect Dis 17: 909948.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Checkley W , Gilman RH , Epstein LD , Suarez M , Diaz JF , Cabrera L , Black RE , Sterling CR , 1997. Asymptomatic and symptomatic cryptosporidiosis: their acute effect on weight gain in Peruvian children. Am J Epidemiol 145: 156163.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Lee G , Pan W , Yori PP , Olortegui MP , Tilley D , Gregory M , Oberhelman R , Burga R , Chavez CB , Kosek M , 2013. Symptomatic and asymptomatic Campylobacter infections associated with reduced growth in Peruvian children. PLoS Negl Trop Dis 7: e2036.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Lee G , Paredes Olortegui M , Penataro Yori P , Black RE , Caulfield L , Banda Chavez C , Hall E , Pan WK , Meza R , Kosek M , 2014. Effects of Shigella-, Campylobacter- and ETEC-associated diarrhea on childhood growth. Pediatr Infect Dis J 33: 10041009.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    George CM et al.2018. Enteric infections in young children are associated with environmental enteropathy and impaired growth. TM & IH 23: 2633.

  • 7.

    Guerrant RL , Oriá RB , Moore SR , Oriá MO , Lima AA , 2008. Malnutrition as an enteric infectious disease with long-term effects on child development. Nutr Rev 66: 487505.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Prado EL , Dewey KG , 2014. Nutrition and brain development in early life. Nutr Rev 72: 267284.

  • 9.

    Berkman DS , Lescano AG , Gilman RH , Lopez SL , Black MM , 2002. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 359: 564571.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Walker SP , Chang SM , Powell CA , Simonoff E , Grantham-McGregor SM , 2007. Early childhood stunting is associated with poor psychological functioning in late adolescence and effects are reduced by psychosocial stimulation. J Nutr 137: 24642469.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Pavlakis AE , Noble K , Pavlakis SG , Ali N , Frank Y , 2015. Brain imaging and electrophysiology biomarkers: is there a role in poverty and education outcome research? Pediatr Neurol 52: 383388.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Stewart CP et al.2018. Effects of water quality, sanitation, handwashing, and nutritional interventions on child development in rural Kenya (WASH Benefits Kenya): a cluster-randomised controlled trial. Lancet Child Adolesc Health 2: 269280.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Tofail F et al.2018. Effect of water quality, sanitation, hand washing, and nutritional interventions on child development in rural Bangladesh (WASH Benefits Bangladesh): a cluster-randomised controlled trial. Lancet Child Adolesc Health 2: 255268.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Dearden KA , Brennan AT , Behrman JR , Schott W , Crookston BT , Humphries DL , Penny ME , Fernald LC , 2017. Does household access to improved water and sanitation in infancy and childhood predict better vocabulary test performance in Ethiopian, Indian, Peruvian and Vietnamese cohort studies? BMJ Open 7: e013201.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Bowen A , Agboatwalla M , Luby S , Tobery T , Ayers T , Hoekstra RM , 2012. Association between intensive handwashing promotion and child development in Karachi, Pakistan: a cluster randomized controlled trial. Arch Pediatr Adolesc Med 166: 10371044.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Gladstone MJ et al.2019. Independent and combined effects of improved water, sanitation, and hygiene (WASH) and improved complementary feeding on early neurodevelopment among children born to HIV-negative mothers in rural Zimbabwe: substudy of a cluster-randomized trial. PLoS Med 16: e1002766.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Humphrey JH et al.2019. Independent and combined effects of improved water, sanitation, and hygiene, and improved complementary feeding, on child stunting and anaemia in rural Zimbabwe: a cluster-randomised trial. Lancet Glob Health 7: e132e147.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Julian TR , Islam MA , Pickering AJ , Roy S , Fuhrmeister ER , Ercumen A , Harris A , Bishai J , Schwab KJ , 2015. Genotypic and phenotypic characterization of Escherichia coli isolates from feces, hands, and soils in rural Bangladesh via the Colilert Quanti-Tray System. Appl Environ Microbiol 81: 17351743.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

     American Public Health Association, 2012. Standard Methods for the Examination of Water and Waste Water. Washington, DC: Association APH.

    • PubMed
    • Export Citation
  • 20.

    George CM et al.2021. Child hand contamination is associated with subsequent pediatric diarrhea in rural Democratic Republic of the Congo (REDUCE Program). TM & IH 26: 102110.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Fernald LC , Kariger P , Hidrobo M , Gertler PJ , 2012. Socioeconomic gradients in child development in very young children: Evidence from India, Indonesia, Peru, and Senegal. Proc Natl Acad Sci USA 109 (Suppl 2): 1727317280.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Wijnhoven TM , de Onis M , Onyango AW , Wang T , Bjoerneboe GE , Bhandari N , Lartey A , al Rashidi B , 2004. Assessment of gross motor development in the WHO Multicentre Growth Reference Study. Food Nutr Bull 25 (Suppl): S37S45.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Fernald LC , Kariger P , Engle P , Raikes A , 2009. Examining early child development in low-income countries: a toolkit for the assessment of children in the first five years of life. Washington, DC: The World Bank.

    • PubMed
    • Export Citation
  • 24.

    Fernald LC , Kariger P , Hidrobo M , Gertler PJ , 2012. Socioeconomic gradients in child development in very young children: evidence from India, Indonesia, Peru, and Senegal. Proc Natl Acad Sci USA 109 (Suppl 2): 17273–17280.

    • PubMed
    • Export Citation
  • 25.

    Ngure FM et al.2013. Formative research on hygiene behaviors and geophagy among infants and young children and implications of exposure to fecal bacteria. Am J Trop Med Hyg 3: 3.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    George CM et al.2015. Geophagy is associated with environmental enteropathy and stunting in children in rural Bangladesh. Am J Trop Med Hyg 92: 1117.

  • 27.

    Guerrant DI , Moore SR , Lima AA , Patrick PD , Schorling JB , Guerrant RL , 1999. Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am J Trop Med Hyg 61: 707713.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Hossain MI , Haque R , Mondal D , Mahfuz M , Ahmed AS , Islam MM , Guerrant RL , Petri WA Jr , Ahmed T , 2016. Undernutrition, vitamin A and iron deficiency are associated with impaired intestinal mucosal permeability in young Bangladeshi children assessed by lactulose/Mannitol test. PLoS One 11: e0164447.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Kwong LH , Ercumen A , Pickering AJ , Arsenault JE , Islam M , Parvez SM , Unicomb L , Rahman M , Davis J , Luby SP , 2020. Ingestion of fecal bacteria along multiple pathways by young children in rural Bangladesh participating in a cluster-randomized trial of water, sanitation, and hygiene interventions (WASH Benefits). Environ Sci Technol 54: 1382813838.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Kwong LH , Ercumen A , Pickering AJ , Unicomb L , Davis J , Leckie JO , Luby SP , 2021. Soil ingestion among young children in rural Bangladesh. J Expo Sci Environ Epidemiol. 31: 82–93.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Black K , Shalat SL , Freeman NC , Jimenez M , Donnelly KC , Calvin JA , 2005. Children’s mouthing and food-handling behavior in an agricultural community on the US/Mexico border. J Expo Anal Environ Epidemiol 15: 244251.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Chandna J et al.2020. Effects of improved complementary feeding and improved water, sanitation and hygiene on early child development among HIV-exposed children: substudy of a cluster randomised trial in rural Zimbabwe. BMJ Glob Health 5: e001718.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Reid B , Seu R , Orgle J , Roy K , Pongolani C , Chileshe M , Fundira D , Stoltzfus R , 2018. A community-designed play-yard intervention to prevent microbial ingestion: A baby water, sanitation, and hygiene pilot study in rural Zambia. Am J Trop Med Hyg 99: 513525.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Mbuya MN et al.2015. Design of an intervention to minimize ingestion of fecal microbes by young children in rural Zimbabwe. Nephrol Dial Transplant 61 (Suppl 7): S703S709.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Biswas SK et al.2021. Formative research for the design of a baby water, sanitation, and hygiene mobile health program in Bangladesh (CHoBI7 Mobile Health Program). Am J Trop Med Hyg. 104: 357.

    • PubMed
    • Export Citation
  • 36.

    Kuhl J et al.2021. Formative research for the development of baby water, sanitation, and hygiene interventions for young children in the Democratic Republic of the Congo (REDUCE program). BMC Public Health 21: 427.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    George CM , Vignola E , Ricca J , Davis T , Perin J , Tam Y , Perry H , 2015. Evaluation of the effectiveness of care groups in expanding population coverage of Key child survival interventions and reducing under-5 mortality: a comparative analysis using the lives saved tool (LiST). BMC Public Health 15: 835.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 1550 664 86
Full Text Views 114 36 1
PDF Downloads 104 15 1
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save