Does vitamin A supplementation protect schoolchildren from acquiring soil-transmitted helminthiasis? A randomized controlled trial

Hesham M Al-Mekhlafi, Tengku Shahrul Anuar, Ebtesam M Al-Zabedi, Mohamed T Al-Maktari, Mohammed A K Mahdy, Abdulhamid Ahmed, Atiya A Sallam, Wan Ariffin Abdullah, Norhayati Moktar, Johari Surin, Hesham M Al-Mekhlafi, Tengku Shahrul Anuar, Ebtesam M Al-Zabedi, Mohamed T Al-Maktari, Mohammed A K Mahdy, Abdulhamid Ahmed, Atiya A Sallam, Wan Ariffin Abdullah, Norhayati Moktar, Johari Surin

Abstract

Background: Despite the intensive global efforts to control intestinal parasitic infections, the prevalence of soil-transmitted helminth (STH) infections is still very high in many developing countries particularly among children in rural areas.

Methods: A randomized, double-blind, placebo-controlled trial was conducted on 250 Aboriginal schoolchildren in Malaysia to investigate the effects of a single high-dose of vitamin A supplementation (200,000 IU) on STH reinfection. The effect of the supplement was assessed at 3 and 6 months after receiving interventions; after a complete 3-day deworming course of 400 mg/daily of albendazole tablets.

Results: Almost all children (98.6%) were infected with at least one STH species. The overall prevalence of ascariasis, trichuriasis and hookworm infection was 67.8%, 95.5% and 13.4%, respectively. Reinfection rates of Ascaris, Trichuris and hookworm were high; at 6 months, assessment reached 80% of the prevalence reported before treatment. There were no significant differences in the reinfection rates and intensities of STH between vitamin A supplemented-children and those who received placebo at 3 and 6 months (p > 0.05).

Conclusions: Vitamin A supplementation showed no protective effect against STH reinfection and this could be due to the high endemicity of STH in this community. Long-term interventions to reduce poverty will help significantly in reducing this continuing problem and there is no doubt that reducing intestinal parasitic infection would have a positive impact on the health, nutrition and education of these children.

Trial registration: This trial was registered at clinicaltrials.gov as NCT00936091.

Figures

Figure 1
Figure 1
A geographic map showing the study area (location of school and villages in Lipis district).
Figure 2
Figure 2
Flow chart of data collection and follow up.

References

    1. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37. doi: 10.1186/1756-3305-7-37.
    1. World Health Organization . Helminth Control in School-age Children. A Guide for Managers of Control Programmes. Geneva: World Health Organisation; 2011.
    1. Ahmed A, Al-Mekhlafi HM, Choy SH, Ithoi I, Al-Adhroey AH, Abdulsalam AM, Surin J. The burden of moderate-to-heavy soil-transmitted helminth infections among rural Malaysian aborigines: an urgent need for an integrated control programme. Parasit Vectors. 2011;4:242. doi: 10.1186/1756-3305-4-242.
    1. Hotez PJ, Fenwick A, Savioli L, Molyneux DH. Rescuing the bottom billion through control of neglected tropical diseases. Lancet. 2009;373:1570–1575. doi: 10.1016/S0140-6736(09)60233-6.
    1. Albonico M, Bickle Q, Ramsan M, Montresor A, Savioli L, Taylor M. Efficacy of mebendazole and levamisole alone or in combination against intestinal nematode infections after repeated targeted mebendazole treatment in Zanzibar. Bull World Health Organ. 2003;81:343–352.
    1. Olsen A, Nawiri J, Friis H. The impact of iron supplementation on reinfection with intestinal helminths and Schistosoma mansoni in western Kenya. Trans R Soc Trop Med Hyg. 2000;94:493–499. doi: 10.1016/S0035-9203(00)90063-4.
    1. Al-Mekhlafi HMS, Surin J, Atiya AS, Ariffin WAW, Mahdy AKM, Abdullah HC. Pattern and predictors of soil-transmitted helminth re-infection among aboriginal school children in rural peninsular Malaysia. Acta Trop. 2008;107:200–204. doi: 10.1016/j.actatropica.2008.05.022.
    1. Grazioso CF, Isalgue M, de Ramirez I, Ruz M, Solomons NW. The effect of zinc supplementation on parasitic reinfestation of Guatemalan schoolchildren. Am J Clin Nutr. 1993;57:673–678.
    1. Friis H, Ndhlovu P, Mduluza T, Kaondera K, Sandstrom B, Michaelsen KF, Vennervald BJ, Christensen NO. The impact of zinc supplementation on Schistosoma mansoni reinfection rate and intensities: a randomized, controlled trial among rural Zimbabwean schoolchildren. Eur J Clin Nutr. 1997;51:33–37. doi: 10.1038/sj.ejcn.1600359.
    1. Serghides L, Kain KC. Mechanism of protection induced by vitamin A in falciparum malaria. Lancet. 2002;359:1404–1406. doi: 10.1016/S0140-6736(02)08360-5.
    1. World Health Organization . Strategy Development and Monitoring for Parasitic Diseases and Vector Control Team. How to add Deworming to Vitamin A Distribution? Geneva: World Health Organization; 2004.
    1. Semba RD. The role of vitamin A and related retinoids in immune function. Nutr Rev. 1998;56:S38–S48. doi: 10.1111/j.1753-4887.1998.tb01643.x.
    1. Djakoure C, Guibourdenche J, Porquet D, Pagesy P, Peillon F, Li JY, Evain-Brion D. Vitamin A and retinoic acid stimulate within minutes Camp release and growth hormone secretion in human pituitary cells. J Clin Endocrinol Metab. 1996;81(8):3123–3126.
    1. Maden M, Gale E, Zile M. The role of Vitamin A in the development of the central nervous system. J Nutr. 1998;128:471S–475S.
    1. Hurst RJ, Else KJ. Retinoic acid signalling in gastrointestinal parasite infections: lessons from mouse models. Parasite Immunol. 2012;34(7):351–359. doi: 10.1111/j.1365-3024.2012.01364.x.
    1. Aukrust P, Muller F, Ueland T, Svardal AM, Berge RK, Froland SS. Decreased vitamin A levels in common variable immunodeficiency: vitamin A supplementation in vivo enhances immunoglobulin production and downregulates inflammatory responses. Eur J Clin Invest. 2000;30:252–259. doi: 10.1046/j.1365-2362.2000.00619.x.
    1. Hoag KA, Nashold FE, Goverman J, Hayes CE. Retinoic acid enhances the T helper 2 cell development that is essential for robust antibody responses through its action on antigen-presenting cells. J Nutr. 2002;132:3736–3739.
    1. Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science. 2005;308:1463–1465. doi: 10.1126/science.1108661.
    1. Ross AC, Gardner EM. The function of vitamin A in cellular growth and differentiation, and its roles during pregnancy and lactation. Adv Exp Med Biol. 1994;352:187–200. doi: 10.1007/978-1-4899-2575-6_15.
    1. Norhayati M, Oothuman P, Azizi O, Fatmah MS. Efficacy of single dose albendazole on the prevalence and intensity of infection of soil-transmitted helminths in Orang Asli children in Malaysia. Southeast Asian J Trop Med Public Health. 1997;28:563–569.
    1. World Health Organization . Technical Report Series: 912. Geneva: World Health Organisation; 2002. Prevention and control of intestinal parasitic infections: prevention and control of schistosomiasis and soil-transmitted helminthiasis.
    1. Jozefzoon L, Oostburg B. Detection of hookworm and hookworm-like larvae in human fecocultures in Suriname. Am J Trop Med Hygiene. 1994;51:501–505.
    1. Montresor A. Arithmetic or geometric means of eggs per gram are not appropriate indicators to estimate the impact of control measures in helminth infections. Trans R Soc Trop Med Hyg. 2007;101:773–776. doi: 10.1016/j.trstmh.2007.04.008.
    1. Albonico M, Rinaldi L, Sciascia S, Morgoglione ME, Piemonte M, Maurelli MP, Musella V, Utzinger J, Ali SM, Ame SM, Cringoli G. Comparison of three copromicroscopic methods to assess albendazole efficacy against soil-transmitted helminth infections in school-aged children on Pemba Island. Trans R Soc Trop Med Hyg. 2013;107(8):493–501. doi: 10.1093/trstmh/trt051.
    1. Wright CC, Sim J. Intention-to-treat approach to data from randomized controlled trials: a sensitivity analysis. J Clin Epidemiol. 2003;56:833–842. doi: 10.1016/S0895-4356(03)00155-0.
    1. Hollis S, Campbell F. What is meant by intention to treat analysis? Survey of published randomised controlled trials. BMJ. 1999;319:670–674. doi: 10.1136/bmj.319.7211.670.
    1. World Health Organization . Soil-Transmitted Helminthiases. Eliminating Soil-Transmitted Helminthiases as a Public Health Problem in Children: Progress Report 2001–2010 and Strategic Plan 2011–2020. Geneva: World Health Organisation; 2012.
    1. Gilgen DD, Mascie-Taylor CG, Rosetta LL. Intestinal helminth infections, anaemia and labour productivity of female tea pluckers in Bangladesh. Trop Med Int Health. 2001;6:449–457. doi: 10.1046/j.1365-3156.2001.00729.x.
    1. Ahmed A, Al-Mekhlafi H, Azam M, Ithoi I, Al-Adhroey A, Abdulsalam A, Surin J. Soil-transmitted helminthiasis: a critical but neglected factor influencing school participation of Aboriginal children in rural Malaysia. Parasitology. 2012;139:802–808. doi: 10.1017/S003118201100237X.
    1. Al-Mekhlafi MH, Azlin M, Aini UN, Shaik A, Sa’iah A, Norhayati M. Prevalence and predictors of low serum retinol and hypoalbuminaemia among children in rural Peninsular Malaysia. Trans R Soc Trop Med Hyg. 2007;101:1233–1240. doi: 10.1016/j.trstmh.2007.09.006.
    1. Ahmed A, Al-Mekhlafi HM, Al-Adhroey AH, Ithoi I, Abdulsalam AM, Surin J. The nutritional impacts of soil-transmitted helminths infections among Orang Asli schoolchildren in rural Malaysia. Parasit Vectors. 2012;5:119. doi: 10.1186/1756-3305-5-119.
    1. Nasr NA, Al-Mekhlafi HM, Ahmed A, Roslan MA, Bulgiba A. Towards an effective control programme of soil-transmitted helminth infections among Orang Asli in rural Malaysia. Part 1: Prevalence and associated key factors. Parasit Vectors. 2013;6:27. doi: 10.1186/1756-3305-6-27.
    1. Neva FA, Brown HW. Basic Clinical Parasitology. Norwalk, Conn: Appleton & Lange; 1995.
    1. Bleay C, Wilkes CP, Paterson S, Viney ME. Density-dependent immune responses against the gastrointestinal nematode Strongyloides ratti. Int J Parasitol. 2007;37:1501–1509. doi: 10.1016/j.ijpara.2007.04.023.
    1. Anderson RM, Truscott JE, Pullan RL, Brooker SJ, Hollingsworth TD. How effective is school-based deworming for the community-wide control of soil-transmitted helminths? PLoS Negl Trop Dis. 2013;7(2):e2027. doi: 10.1371/journal.pntd.0002027.
    1. Payne LG, Koski KG, Ortega-Barria E, Scott ME. Benefit of vitamin A supplementation on Ascaris reinfection is less evident in stunted children. J Nutr. 2007;137:1455–1459.
    1. Long KZ, Rosado JL, Montoya Y, de Lourdes Solano M, Hertzmark E, DuPont HL, Santos JI. Effect of vitamin A and zinc supplementation on gastrointestinal parasitic infections among Mexican children. Pediatrics. 2007;120:e846–e855. doi: 10.1542/peds.2006-2187.
    1. Lima AA, Soares AM, Lima NL, Mota RM, Maciel BL, Kvalsund MP, Barrett LJ, Fitzgerald RP, Blaner WS, Guerrant RL. Effects of vitamin A supplementation on intestinal barrier function, growth, total parasitic, and specific Giardia spp infections in Brazilian children: a prospective randomized, double-blind, placebo-controlled trial. J Pediatr Gastroenterol Nutr. 2010;50(3):309–315. doi: 10.1097/MPG.0b013e3181a96489.

Source: PubMed

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