Malaria and Nutritional Status Among Children With Severe Acute Malnutrition in Niger: A Prospective Cohort Study

Catherine E Oldenburg, Philippe J Guerin, Fatou Berthé, Rebecca F Grais, Sheila Isanaka, Catherine E Oldenburg, Philippe J Guerin, Fatou Berthé, Rebecca F Grais, Sheila Isanaka

Abstract

Background: The relationship between malaria infection and nutritional status is complex. Previous studies suggest malaria may increase the incidence and severity of malnutrition, while malnutrition may increase the risk of malaria infection. Here, we report bidirectional associations between malaria and nutritional status among children with uncomplicated severe acute malnutrition (SAM).

Methods: This study is a secondary analysis of a randomized, controlled trial for the treatment of uncomplicated SAM in Niger. Children aged 6-59 months were enrolled and followed for 12 weeks. Malaria infection was assessed using an histidine-rich protein 2 (HRP2) rapid diagnostic test at admission and at any follow-up visit with fever. We assessed the association of nutritional status at admission on malaria incidence using Cox proportional hazards regression and malaria infection at admission on nutritional recovery and weight and height gain using linear regression.

Results: Of 2399 children included in the analysis, 1327 (55.3%) were infected with malaria at admission. Malaria incidence was 12.1 cases/100 person-months among those without malaria infection at admission. Nutritional status at admission was not associated with malaria incidence. Children with malaria infection at admission and subsequently treated with an artemisinin-based combination therapy had increased weight gain (0.38 g/kg/day; 95% confidence interval [CI], 0.07 to 0.69) and reduced height gain (-0.002 mm/day; 95% CI, -0.004 to -0.0008).

Conclusions: Malaria infection was common among children treated for uncomplicated SAM. Malaria infection may impair height gain. Proper medical and nutritional management should be ensured to prevent adverse effects of malaria infection.

Clinical trials registration: NCT01613547.

Figures

Figure 1.
Figure 1.
Histogram of malaria incidence and admissions to nutrition program. Black bars indicate the number of children during each month with incident malaria infection. The gray line indicates the number of admissions to the nutritional program per month.

References

    1. World Health Organization. World Malaria Report 2017 2017:1–196.
    1. Wang H, Bhutta ZA, Coates MM et al. . Global, regional, national, and selected subnational levels of stillbirths, neonatal, infant, and under-5 mortality, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016; 388:1725–1774.
    1. Kampe EOI, Muller O, Sie A, Becher H. Seasonal and temporal trends in all-cause and malaria mortality in rural Burkina Faso, 1998–2007. Malaria J 2015; 14:1–9.
    1. Doudou MH, Mahamadou A, Ouba I et al. . A refined estimate of the malaria burden in Niger. Malar J 2012; 11:89.
    1. Burki TK. Malaria and malnutrition: Niger’s twin crises. Lancet 2013; 382:587–8.
    1. Guillebaud J, Mahamadou A, Zamanka H et al. . Epidemiology of malaria in an area of seasonal transmission in Niger and implications for the design of a seasonal malaria chemoprevention strategy. Malar J 2013; 12:379.
    1. Langendorf C, Roederer T, de Pee S et al. . Preventing acute malnutrition among young children in crises: a prospective intervention study in Niger. PLoS Med 2014; 11:e1001714.
    1. Page AL, de Rekeneire N, Sayadi S et al. . Infections in children admitted with complicated severe acute malnutrition in Niger. PLoS One 2013; 8:e68699.
    1. Ferreira ED, Alexandre MA, Salinas JL et al. . Association between anthropometry- based nutritional status and malaria: a systematic review of observational studies. Malaria Journal 2015; 14:346.
    1. Das D, Grais RF, Okiro E et al. . Complex and entangled interactions between malaria and malnutrition: a systematic review. 2017; 1.
    1. Denoeud-Ndam L, Dicko A, Baudin E et al. . Efficacy of artemether-lumefantrine in relation to drug exposure in children with and without severe acute malnutrition: an open comparative intervention study in Mali and Niger. BMC Med 2016; 14:167.
    1. Shikur B, Deressa W, Lindtjørn B. Association between malaria and malnutrition among children aged under-five years in Adami Tulu District, south-central Ethiopia: a case–control study. BMC Public Health 2016; 16:174.
    1. Sumbele IUN, Bopda OSM, Kimbi HK, Ning TR, Nkuo-Akenji T. Nutritional status of children in a malaria meso endemic area: cross sectional study on prevalence, intensity, predictors, influence on malaria parasitaemia and anaemia severity. BMC Public Health 2015; 15:1099.
    1. Gone T, Lemango F, Eliso E, Yohannes S, Yohannes T. The association between malaria and malnutrition among under-five children in Shashogo District, Southern Ethiopia: a case-control study. Infect Dis Poverty 2017; 6:9.
    1. Arinaitwe E, Gasasira A, Verret W et al. . The association between malnutrition and the incidence of malaria among young HIV-infected and -uninfected Ugandan children: a prospective study. Malar J 2012; 11:90.
    1. Deen JL, Walraven GE, von Seidlein L. Increased risk for malaria in chronically malnourished children under 5 years of age in rural Gambia. J Trop Pediatr 2002; 48:78–83.
    1. Genton B, Al-Yaman F, Ginny M, Taraika J, Alpers MP. Relation of anthropometry to malaria morbidity and immunity in Papua New Guinean children. Am J Clin Nutr 1998; 68:734–41.
    1. Fillol F, Sarr JB, Boulanger D et al. . Impact of child malnutrition on the specific anti-Plasmodium falciparum antibody response. Malar J 2009; 8:116.
    1. Tonglet R, Mahangaiko Lembo E, Zihindula PM, Wodon A, Dramaix M, Hennart P. How useful are anthropometric, clinical and dietary measurements of nutritional status as predictors of morbidity of young children in central Africa?Trop Med Int Health 1999; 4:120–30.
    1. Danquah I, Dietz E, Zanger P et al. . Reduced efficacy of intermittent preventive treatment of malaria in malnourished children. Antimicrob Agents Chemother 2009; 53:1753–9.
    1. Muller O, Garenne M, Kouyate B, Becher H. The association between protein–energy malnutrition, malaria morbidity and all-cause mortality in West African children. Trop Med Int Health 2003; 8:507–11.
    1. Nyakeriga AM, Troye-Blomberg M, Chemtai AK, Marsh K, Williams TN. Malaria and nutritional status in children living on the coast of Kenya. Am J Clin Nutr 2004; 80:1604–10.
    1. Alexandre MA, Benzecry SG, Siqueira AM et al. . The association between nutritional status and malaria in children from a rural community in the Amazonian region: a longitudinal study. PLoS Negl Trop Dis 2015; 9:e0003743.
    1. WWARN ACT Malaria Malnutrition Study Group. Assessing the impact of malnutrition on the treatment outcome of artemisinin-based combination therapy in uncomplicated P. falciparum malaria: 65th Annual Meeting of the American Society of Tropical Medicine and Hygiene, 13-17 November 2016; Atlanta, GA.
    1. Fillol F, Cournil A, Boulanger D et al. . Influence of wasting and stunting at the onset of the rainy season on subsequent malaria morbidity among rural preschool children in Senegal. Am J Trop Med Hyg 2009; 80:202–8.
    1. Hautvast JL, Tolboom JJ, Kafwembe EM et al. . Severe linear growth retardation in rural Zambian children: the influence of biological variables. Am J Clin Nutr 2000; 71:550–9.
    1. Kang H, Kreuels B, Adjei O, Krumkamp R, May J, Small DS. The causal effect of malaria on stunting: a Mendelian randomization and matching approach. Int J Epidemiol 2013; 42:1390–8.
    1. Muhangi L, Lule SA, Mpairwe H et al. . Maternal HIV infection and other factors associated with growth outcomes of HIV-uninfected infants in Entebbe, Uganda. Public Health Nutr 2013; 16:1548–57.
    1. Deen JL, Walraven GE, von Seidlein L. Increased risk for malaria in chronically malnourished children under 5 years of age in rural Gambia. J Trop Pediatr 2002; 48:78–83.
    1. Padonou G, Le Port A, Cottrell G et al. . Factors associated with growth patterns from birth to 18 months in a Beninese cohort of children. Acta Trop 2014; 135:1–9.
    1. Isanaka S, Langendorf C, Berthé F et al. . Routine amoxicillin for uncomplicated severe acute malnutrition in children. N Engl J Med 2016; 374:444–53.
    1. WHO Multicentre Growth Reference Study Group. Assessment of differences in linear growth among populations in the WHO Multicentre Growth Reference Study. Acta Paediatr 2006; 450:56–65.
    1. Ballard T, Coates J, Swindale A, Deitchler M. Household hunger scale: indicator definition and measurement guide. 2011. Washington, DC: Food and Nutrition Technical Assistance II Project, FHI 360.
    1. Arimond M, Ruel MT. Dietary diversity is associated with child nutritional status: evidence from 11 demographic and health surveys. J Nutr 2004; 134:2579–85.
    1. Grandesso F, Nabasumba C, Nyehangane D et al. . Performance and time to become negative after treatment of three malaria rapid diagnostic tests in low and high malaria transmission settings. Malaria J 2016; 15:496.
    1. Greenland S. Modeling and variable selection in epidemiologic analysis. Am J Public Health 2006; 79:340–9.
    1. Mfonkeu JB, Gouado I, Kuaté HF et al. . Biochemical markers of nutritional status and childhood malaria severity in Cameroon. Br J Nutr 2010; 104:886–92.
    1. Novelli EM, Hittner JB, Davenport GC et al. . Clinical predictors of severe malarial anaemia in a holoendemic Plasmodium falciparum transmission area. Br J Haematol 2010; 149:711–21.
    1. Maketa V, Mavoko HM, da Luz RI et al. . The relationship between Plasmodium infection, anaemia and nutritional status in asymptomatic children aged under five years living in stable transmission zones in Kinshasa, Democratic Republic of Congo. Malaria J 2015; 14:1–9.
    1. Custodio E, Descalzo MA, Villamor E et al. . Nutritional and socio-economic factors associated with Plasmodium falciparum infection in children from Equatorial Guinea: results from a nationally representative survey. Malar J 2009; 8:225.
    1. Friedman JF, Kwena AM, Mirel LB et al. . Malaria and nutritional status among pre-school children: results from cross-sectional surveys in western Kenya. Am J Trop Med Hyg 2005; 73:698–704.
    1. Lewnard JA, Berrang-Ford L, Lwasa S et al. ; Indigenous Health Adaptation to Climate Change Research Team 2013 Relative undernourishment and food insecurity associations with Plasmodium falciparum among Batwa pygmies in Uganda: evidence from a cross-sectional survey. Am J Trop Med Hyg 2014; 91:39–49.
    1. Mitangala Ndeba P, Hennart P, D’Alessandro U et al. . Protein-energy malnutrition and malaria-related morbidity in children under 59 months in the Kivu region of the Democratic Republic of the Congo. Med Trop (Mars) 2008; 68:51–7.
    1. Mathanga DP, Halliday KE, Jawati M et al. . The high burden of malaria in primary school children in Southern Malawi. Am J Trop Med Hyg 2015; 93:779–89.
    1. Müller O, Garenne M, Kouyaté B, Becher H. The association between protein-energy malnutrition, malaria morbidity and all-cause mortality in West African children. Trop Med Int Health 2003; 8:507–11.
    1. Nyakeriga AM, Troye-Blomberg M, Chemtai AK, Marsh K, Williams TN. Malaria and nutritional status in children living on the coast of Kenya. Am J Clin Nutr 2004; 80:1604–10.
    1. de Onis M, Branca F. Childhood stunting: a global perspective. Matern Child Nutr 2016; 12(Suppl 1):12–26.
    1. Mitangala PN, DAlessandro U, Donnen P et al. . Infection palustre et état nutritionnel: résultats d’une cohorte d’enfants âgés de 6 à 59 mois au Kivu en République démocratique du Congo. Revue d’Épidémiologie et de Santé Publique 2013; 61:111–20.
    1. Hendriksen IC, White LJ, Veenemans J et al. . Defining falciparum-malaria-attributable severe febrile illness in moderate-to-high transmission settings on the basis of plasma PfHRP2 concentration. J Infect Dis 2013; 207:351–61.
    1. DeBoer MD, Scharf RJ, Leite AM et al. . Systemic inflammation, growth factors, and linear growth in the setting of infection and malnutrition. Nutrition 2017; 33:248–53.
    1. Kassim OO, Ako-Anai KA, Torimiro SE, Hollowell GP, Okoye VC, Martin SK. Inhibitory factors in breastmilk, maternal and infant sera against in vitro growth of Plasmodium falciparum malaria parasite. J Trop Pediatr 2000; 46:92–6.
    1. Sinnis P, Willnow TE, Briones MR, Herz J, Nussenzweig V. Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes. J Exp Med 1996; 184:945–54.
    1. Vora N, Homsy J, Kakuru A et al. . Breastfeeding and the risk of malaria in children born to HIV-infected and uninfected mothers in rural Uganda. J Acquir Immune Defic Syndr 2010; 55:253–61.
    1. Kalanda BF, Verhoeff FH, Brabin BJ. Breast and complementary feeding practices in relation to morbidity and growth in Malawian infants. Eur J Clin Nutr 2005; 60:401–7.
    1. Doctor SM, Liu Y, Whitesell A et al. . Malaria surveillance in the Democratic Republic of the Congo: comparison of microscopy, PCR, and rapid diagnostic test. Diagn Microbiol Infect Dis 2016; 85:16–8.
    1. Wanja EW, Kuya N, Moranga C et al. . Field evaluation of diagnostic performance of malaria rapid diagnostic tests in western Kenya. Malaria J 2016; 15:456.

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