Assessing the Impact of Animal Husbandry and Capture on Anemia among Women and Children in Low- and Middle-Income Countries: A Systematic Review

Nathalie J Lambrecht, Mark L Wilson, Andrew D Jones, Nathalie J Lambrecht, Mark L Wilson, Andrew D Jones

Abstract

Animal husbandry and capture (AHC) may mitigate anemia among women and children by supplying a source of micronutrient-rich animal source foods (ASF), yet may concurrently increase exposure to anemia-inducing pathogens such as Plasmodium spp., helminths, and enteropathogens. We conducted a systematic literature review to assess the relation between AHC and anemia among women of reproductive age, school-aged children, and children aged <5 y in low- and middle-income countries (LMICs). We used a 2-stage screening process, in which 1 reviewer searched 4 databases (PubMed, Web of Science, EMBASE, and Global Health) with predetermined search terms for relevant articles. Two reviewers then independently screened studies using a priori exclusion criteria, yielding a total of 23 articles included in the final review. We evaluated evidence from observational studies assessing animal-dependent livelihoods and livestock ownership, and interventions that promoted livestock and fish production. We found little consistency in anemia outcomes across the several AHC exposures and population groups. Poultry production interventions had modest benefits on anemia among women and children, although whether these improvements were a result of increased ASF consumption, or a result of the combined treatment study design could not be determined. Observational studies identified chicken ownership, and no other livestock species, as a risk factor for anemia among young children. However, there was limited evidence to evaluate pathways underlying these associations. Studies tended to rely on self-reported fever and diarrhea to assess illness, and no study directly assessed linkages between AHC, pathogen burden, and anemia. Thus, there is insufficient evidence to conclude whether AHC improves or worsens anemia among women and children in LMICs. Given the current interest in promoting animal production among low-income households, future studies with robust measures of livestock ownership, ASF consumption, pathogen burden, and anemia status are needed to understand the nuances of this complex and potentially contradictory relation.

Keywords: anemia; animal husbandry; animal source food consumption; children; fish production; infectious disease; livestock ownership; women; zoonotic disease.

© 2019 American Society for Nutrition.

Figures

FIGURE 1
FIGURE 1
Simplified conceptual framework of the main pathways connecting animal husbandry and capture (AHC) with anemia among women of reproductive age, school-aged children, and children aged

FIGURE 2

Preferred Reporting Items for Systematic…

FIGURE 2

Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram. AHC, animal…

FIGURE 2
Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram. AHC, animal husbandry and capture; Hb, hemoglobin.
FIGURE 2
FIGURE 2
Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram. AHC, animal husbandry and capture; Hb, hemoglobin.

References

    1. Herrero M, Grace D, Njuki J, Johnson N, Enahoro D, Silvestri S, Rufino MC. The roles of livestock in developing countries. Animal. 2013;7(s1):3–18.
    1. HLPE. Sustainable fisheries and aquaculture for food security and nutrition. A report by the High Level Panel of Experts on Food Security and Nutrition of the Committee on World Food Security. Rome; 2014.
    1. Randolph TF, Schelling E, Grace D, Nicholson CF, Leroy JL, Cole DC, Demment MW, Omore A, Zinsstag J, Ruel M. Invited review: role of livestock in human nutrition and health for poverty reduction in developing countries. J Anim Sci. 2007;85:2788–800.
    1. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet. 2008;371:243–60.
    1. Anchang KY, Avery L, Pertiwiningrum A. A commentary on occupational infectious diseases due to agricultural practices in Sub-Saharan Africa. Biomass Bioenergy. 2014;70:99–111.
    1. Grace D, Mutua F, Ochungo P, Kruska R, Jones K, Brierley L, Lapar L, Said M, Herrero M, Phuc P, et al. .. Mapping of poverty and likely zoonoses hotspots. Zoonoses Project 4. Report to the UK Department for International Development. Nairobi; 2012.
    1. World Health Organization. The control of neglected zoonotic diseases: a route to poverty alleviation. Report of a joint WHO/DFID-AHP meeting, 20 and 21 September 2005. Geneva; 2006.
    1. World Health Organization. The Global Prevalence of Anaemia in 2011. Geneva; 2015.
    1. Balarajan Y, Ramakrishnan U, Özaltin E, Shankar AH, Subramanian S. Anaemia in low-income and middle-income countries. Lancet. 2011;378:2123–35.
    1. Thurnham DI, Northrop-Clewes CA. Infection and the etiology of anemia. In: Kraemer K, Zimmermann MB, Nutritional Anemia. Basel: Sight and Life Press; 2007. pp. 231–56.
    1. Neumann C, Harris DM, Rogers LM. Contribution of animal source foods in improving diet quality and function in children in the developing world. Nutr Res. 2002;22:193–220.
    1. Donnelly B, Berrang-Ford L, Ross NA, Michel P. A systematic, realist review of zooprophylaxis for malaria control. Malar J. 2015;14:313.
    1. Portugal S, Drakesmith H, Mota MM. Superinfection in malaria: Plasmodium shows its iron will. EMBO Rep. 2011;12:1233–42.
    1. Béné C, Arthur R, Norbury H, Allison EH, Beveridge M, Bush S, Campling L, Leschen W, Little D, Squires D, et al. .. Contribution of fisheries and aquaculture to food security and poverty reduction: assessing the current evidence. World Dev. 2016;79:177–96.
    1. Friedman JF, Kanzaria HK, McGarvey ST. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol. 2005;21:386–92.
    1. Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S. Hookworm infection. N Engl J Med. 2004;351:799–807.
    1. Moore CE, Elwin K, Phot N, Seng C, Mao S, Suy K, Kumar V, Nader J, Bousfield R, Perera S, et al. .. Molecular characterization of Cryptosporidium species and Giardia duodenalis from symptomatic Cambodian children. PLoS Negl Trop Dis. 2016;10:e0004822.
    1. Vasco K, Graham JP, Trueba G. Detection of zoonotic enteropathogens in children and domestic animals in a semirural community in Ecuador. Appl Environ Microbiol. 2016;82:4218–24.
    1. Soares MP, Weiss G. The iron age of host–microbe interactions. EMBO Rep. 2015;16:1482–500.
    1. Berti PR, Krasevec J, FitzGerald S. A review of the effectiveness of agriculture interventions in improving nutrition outcomes. Public Health Nutr. 2004;7:599–609.
    1. Leroy JL, Frongillo EA. Can interventions to promote animal production ameliorate undernutrition?. J Nutr. 2007;137:2311–6.
    1. Masset E, Haddad L, Cornelius A, Isaza-Castro J. Effectiveness of agricultural interventions that aim to improve nutritional status of children: systematic review. BMJ. 2012;344:d8222.
    1. Webb Girard A, Self JL, McAuliffe C, Olude O. The effects of household food production strategies on the health and nutrition outcomes of women and young children: a systematic review. Paediatr Perinat Epidemiol. 2012;26(s1):205–22.
    1. Gates B. Why I Would Raise Chickens[Internet]. gatesnotes 2016. Available from:
    1. Headey D, Nguyen P, Kim S, Rawat R, Ruel M, Menon P. Is exposure to animal feces harmful to child nutrition and health outcomes? A multicountry observational analysis. Am J Trop Med Hyg. 2017;96:961–9.
    1. Kaur M, Graham JP, Eisenberg JN. Livestock ownership among rural households and child morbidity and mortality: an analysis of Demographic Health Survey data from 30 Sub-Saharan African countries (2005–2015). Am J Trop Med Hyg. 2017;96:741–8.
    1. Zambrano LD, Levy K, Menezes NP, Freeman MC. Human diarrhea infections associated with domestic animal husbandry: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg. 2014;108:313–25.
    1. Moher D, Liberati A, Tetzlaff J, Altman DG; The PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.
    1. World Health Organization. Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Vitamin and Mineral Nutrition Information System; Geneva; 2011.
    1. The World Bank. World Bank Country and Lending Groups[Internet]. [Cited 21 Aug, 2017]. Available from: .
    1. Guyatt GH, Oxman AD, Schünemann HJ, Tugwell P, Knottnerus A. GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology. J Clin Epidemiol. 2011;64:380–2.
    1. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014;11:e1001620.
    1. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP; STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007;4:e296.
    1. NIH National Heart Lung and Blood Institute. Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies[Internet]. 2014; [cited 9 Jul. 2017]. Available from: .
    1. Higgins JP, Altman DG. Assessing risk of bias in included studies. In: Higgins JP, Green S, Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series. The Cochrane Collaboration; 2008. pp. 187–241.
    1. Adongo AO, Shell-Duncan B, Tuitoek JP. Effect of settlement on nutrition and health status of pastoral Gabra women of reproductive age in Kalacha Location, Marsabit County, Kenya. Public Health Nutr. 2012;16:1622–30.
    1. Agyepong IA, Wellington EK, Abbey MA. A comparative study of clinical and sociocultural aspects of anaemia among adolescent girls in rural Ghana. Acta Trop. 1997;65:123–38.
    1. Ahenkorah B, Nsiah K, Baffoe P. Sociodemographic and obstetric characteristics of anaemic pregnant women attending antenatal clinic in Bolgatanga Regional Hospital. Scientifica (Cairo). 2016;2016:4687342.
    1. Bechir M, Schelling E, Hamit MA, Tanner M, Zinsstag J. Parasitic infections, anemia and malnutrition among rural settled and mobile pastoralist mothers and their children in Chad. Ecohealth. 2012;9:122–31.
    1. Custodio E, Descalzo MA, Roche J, Sánchez I, Molina L, Lwanga M, Bernis C, Villamor E, Baylin A. Nutritional status and its correlates in Equatorial Guinean preschool children: results from a nationally representative survey. Food Nutr Bull. 2008;29:49–58.
    1. Dalsin MF. Livestock-owning households of Kazakstan part 2: food patterns and health—seasonal and regional analysis. Ecol Food Nutr. 2002;41:345–71.
    1. Flores-Martinez A, Zanello G, Shankar B, Poole N. Reducing anemia prevalence in Afghanistan: socioeconomic correlates and the particular role of agricultural assets. PLoS One. 2016;11:e0156878.
    1. Hillenbrand EP, Waid JL. Adapting food-based strategies to improve the nutrition of the landless: a review of HKI's Homestead Food Production program in Bangladesh. Thompson B, Amoroso L, Improving Diets and Nutrition: Food-based Approaches. FAO; 2014.
    1. Iannotti LL, Delnatus JR, Odom AR, Eaton JC, Griggs JJ, Brown S, Wolff PB. Determinants of anemia and hemoglobin concentration in Haitian school-aged children. Am J Trop Med Hyg. 2015;93:1092–8.
    1. Jankowska MM, Lopez-Carr D, Funk C, Husak GJ, Chafe ZA. Climate change and human health: spatial modeling of water availability, malnutrition, and livelihoods in Mali, Africa. Appl Geogr. 2012;33:4–15.
    1. Jones AD, Colecraft E, Awuah R, Boatemaa S, Lambrecht NJ, Adjorlolo LK, Wilson ML. Livestock ownership is associated with higher odds of anaemia among preschool-aged children, but not women of reproductive age in Ghana. Matern Child Nutr. 2018;14(3):e12604.
    1. Keverenge-Ettyang GA, van Marken Lichtenbelt W, Esamai F, Saris W. Maternal nutritional status in pastoral versus farming communities of West Pokot, Kenya: differences in iron and vitamin A status and body composition. Food Nutr Bull. 2006;27:228–35.
    1. Kumar N, Quisumbing AR. Access, adoption, and diffusion: understanding the long-term impacts of improved vegetable and fish technologies in Bangladesh. IFPRI Discussion Paper 00995 2010.
    1. Miller EM. Maternal hemoglobin depletion in a settled northern Kenyan pastoral population. Am J Hum Biol. 2010;22:768–74.
    1. Nathan MA, Fratkin EM, Roth EA. Sedentism and child health among Rendille pastoralists of northern Kenya. Soc Sci Med. 1996;43:503–15.
    1. Olney DK, Talukder A, Iannotti LL, Ruel MT, Quinn V. Assessing impact and impact pathways of a homestead food production program on household and child nutrition in Cambodia. Food Nutr Bull. 2009;30:355–69.
    1. Olney DK, Pedehombga A, Ruel MT, Dillon A. A 2-year integrated agriculture and nutrition and health behavior change communication program targeted to women in Burkina Faso reduces anemia, wasting, and diarrhea in children 3–12.9 months of age at baseline: a cluster-randomized controlled trial. J Nutr. 2015;145:1317–24.
    1. Osei AK, Pandey P, Spiro D, Adhikari D, Haselow N, De Morais C, Davis D. Adding multiple micronutrient powders to a homestead food production programme yields marginally significant benefit on anaemia reduction among young children in Nepal. Matern Child Nutr. 2015;11(s4):188–202.
    1. Osei A, Pandey P, Nielsen J, Pries A, Spiro D, Davis D, Quinn V, Haselow N. Combining home garden, poultry, and nutrition education program targeted to families with young children improved anemia among children and anemia and underweight among nonpregnant women in Nepal. Food Nutr Bull. 2017;38:49–64.
    1. Schipani S, van der Haar F, Sinawat S, Maleevong K. Dietary intake and nutritional status of young children in families practicing mixed home gardening in northeast Thailand. Food Nutr Bull. 2002;23:175–80.
    1. Smitasiri S, Dhanamitta S. Sustaining behavior change to enhance micronutrient status: community- and women-based interventions in Thailand. ICRW/OMNI Research Report Series No. 2 1999.
    1. Talukder A, Osei AK, Haselow NJ, Kroeun H, Uddin A, Quinn V. Contribution of homestead food production to improved household food security and nutrition status—lessons learned from Bangladesh, Cambodia, Nepal and the Philippines. Thompson B, Amoroso L, Improving Diets and Nutrition: Food-based Approaches. FAO; 2014.
    1. Wang Z, Patterson CM, Oldenburg B. Implications of diet and nutrition for growth and prevalence of anaemia in rural preschool-aged children in Shandong Province, China. Asia Pac J Clin Nutr. 2000;9:87–92.
    1. Sadler K, Kerven C, Calo M, Manske M, Catley A. The fat and the lean: review of production and use of milk by pastoralists. Pastoralism. 2010;1:291–324.
    1. Fratkin E, Roth EA, Nathan MA. Pastoral sedentarization and its effects on children's diet, health, and growth among Rendille of northern Kenya. Hum Ecol. 2004;32:531–59.
    1. Fujita M, Roth EA, Nathan MA, Fratkin E. Sedentism, seasonality, and economic status: a multivariate analysis of maternal dietary and health statuses between pastoral and agricultural Ariaal and Rendille communities in northern Kenya. Am J Phys Anthropol. 2004;123:277–91.
    1. Iannotti L, Lesorogol C. Animal milk sustains micronutrient nutrition and child anthropometry among pastoralists in Samburu, Kenya. Am J Phys Anthropol. 2014;155:66–76.
    1. Ziegler EE. Consumption of cow's milk as a cause of iron deficiency in infants and toddlers. Nutr Rev. 2011;69(s1):S37–42.
    1. Penakalapati G, Swarthout J, Delahoy MJ, McAliley L, Wodnik B, Levy K, Freeman MC. Exposure to animal feces and human health: a systematic review and proposed research priorities. Environ Sci Technol. 2017;51:11537–52.
    1. Luby SP, Rahman M, Arnold BF, Unicomb L, Ashraf S, Winch PJ, Stewart CP, Begum F, Hussain F, Benjamin-Chung J, et al. .. Effects of water quality, sanitation, handwashing, and nutritional interventions on diarrhoea and child growth in rural Bangladesh: a cluster randomised controlled trial. Lancet Glob Health. 2018;6:e302–15.
    1. Null C, Stewart CP, Pickering AJ, Dentz HN, Arnold BF, Arnold CD, Benjamin-Chung J, Clasen T, Dewey KG, Fernald LCH, et al. .. Effects of water quality, sanitation, handwashing, and nutritional interventions on diarrhoea and child growth in rural Kenya: a cluster-randomised controlled trial. Lancet Glob Health. 2018;6:e316–29.
    1. Schmidt WP, Arnold BF, Boisson S, Genser B, Luby SP, Barreto ML, Clasen T, Cairncross S. Epidemiological methods in diarrhoea studies—an update. Int J Epidemiol. 2011;40:1678–92.
    1. McCormick BJJ, Lang DR. Diarrheal disease and enteric infections in LMIC communities: how big is the problem?. Trop Dis Travel Med Vaccines. 2016;2:11.
    1. Wong JT, de Bruyn J, Bagnol B, Grieve H, Li M, Pym R, Alders RG. Small-scale poultry and food security in resource-poor settings: a review. Glob Food Sec. 2017;15:43–52.
    1. Headey D, Hirvonen K. Is exposure to poultry harmful to child nutrition? An observational analysis for rural Ethiopia. PLoS One. 2016;11:e0160590.
    1. Ercumen A, Pickering AJ, Kwong LH, Arnold BF, Parvez SM, Alam M, Sen D, Islam S, Kullmann C, Chase C, et al. .. Animal feces contribute to domestic fecal contamination: evidence from E. coli measured in water, hands, food, flies, and soil in Bangladesh. Environ Sci Technol. 2017;51:8725–34.
    1. Ngure FM, Humphrey JH, Mbuya MNN, Majo F, Mutasa K, Govha M, Mazarura E, Chasekwa B, Prendergast AJ, Curtis V, et al. .. Formative research on hygiene behaviors and geophagy among infants and young children and implications of exposure to fecal bacteria. Am J Trop Med Hyg. 2013;89:709–16.
    1. Marquis GS, Ventura G, Gilman RH, Porras E, Miranda E, Carbajal L, Pentafiel M. Fecal contamination of shanty town toddlers in households with non-corralled poultry, Lima, Peru. Am J Public Health. 1990;80:146–9.
    1. Oberhelman RA, Gilman RH, Sheen P, Cordova J, Zimic M, Cabrera L, Meza R, Perez J. An intervention-control study of corralling of free-ranging chickens to control Campylobacter infections among children in a Peruvian periurban shantytown. Am J Trop Med Hyg. 2006;74:1054–9.
    1. MAL-ED Network Investigators. Relationship between growth and illness, enteropathogens and dietary intakes in the first 2 years of life: findings from the MAL-ED birth cohort study. BMJ Glob Health. 2017;2:e000370.
    1. Syed S, Ali A, Duggan C. Environmental enteric dysfunction in children. J Pediatr Gastroenterol Nutr. 2016;63:6–14.
    1. Owino V, Ahmed T, Freemark M, Kelly P, Loy A, Manary M, Loechl C. Environmental enteric dysfunction and growth failure/stunting in global child health. Pediatrics. 2016;138:e20160641.
    1. Watanabe K, Petri WA. Environmental enteropathy: elusive but significant subclinical abnormalities in developing countries. EBioMedicine. 2016;10:25–32.
    1. Michels K, Nemeth E, Ganz T, Mehrad B. Hepcidin and host defense against infectious diseases. PLoS Pathog. 2015;11:e1004998.
    1. Dumas SE, Lungu L, Mulambya N, Daka W, McDonald E, Steubing E, Lewis T, Backel K, Jange J, Lucio-Martinez B, et al. .. Sustainable smallholder poultry interventions to promote food security and social, agricultural, and ecological resilience in the Luangwa Valley, Zambia. Food Secur. 2016;8:507–20.
    1. Dumas SE, Maranga A, Mbullo P, Collins S, Wekesa P, Onono M, Young SL. “Men are in front at eating time, but not when it comes to rearing the chicken”: unpacking the gendered benefits and costs of livestock ownership in Kenya. Food Nutr Bull. 2018;39:3–27.
    1. Harris-Fry HA, Paudel P, Shrestha N, Harrisson T, Beard BJ, Jha S, Shrestha BP, Manandhar DS, Costello AM, Cortina-Borja M, et al. .. Status and determinants of intra-household food allocation in rural Nepal. Eur J Clin Nutr. 2018; doi: 10.1038/s41430-017-0063-0. [Epub ahead of print].
    1. Stoltzfus RJ, Klemm R. Research, policy, and programmatic considerations from the Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) project. Am J Clin Nutr. 2017;106(s1):428S–34S.
    1. Food and Agriculture Organization of the United Nations (FAO). Synthesis—Livestock and the Sustainable Development Goals: Global Agenda for Sustainable Livestock[Internet]. Available from: .
    1. Dalsin MF. Livestock-owning households of Kazakstan part 1: food resources—seasonal and regional analysis. Ecol Food Nutr. 2002;41:301–43.
    1. InterAction. Best Practices & Innovations (BPI) Initiative: Agriculture & Rural Livelihoods. Improved Poultry Program, Helen Keller International, Best Practice Award for Livestock Production. 2010.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever