The impact of anthelmintic treatment intervention on malaria infection and anaemia in school and preschool children in Magu district, Tanzania: An open label randomised intervention trial

BMC Infectious Diseases

Volumn 15, Issue 1, 2015, Pages

  Kinung'hi, Safari M ^a   Magnussen, Pascal ^b   Kishamawe, Coleman ^a   Todd, Jim ^c   Vennervald, Birgitte J ^b  

^a NATIONAL INSTITUTE OF MEDICAL RESEARCH   (Tanzania)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

Anaemia; Anthelmintic intervention; Magu district; Malaria infection; School children

Indexed keywords

ALBENDAZOLE; PRAZIQUANTEL; ANTHELMINTIC AGENT;

ADOLESCENT; ANEMIA; ARTICLE; CHILD; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; FECES ANALYSIS; FEMALE; HOOKWORM; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALARIA; MALE; PATIENT MONITORING; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL; SCHISTOSOMA; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMA MANSONI; SCHOOL CHILD; SINGLE DRUG DOSE; SOIL ANALYSIS; TANZANIA; TRICHURIS TRICHIURA; URINALYSIS; ANIMAL; HELMINTHIASIS; HOOKWORM INFECTIONS; ISOLATION AND PURIFICATION; MALARIA, FALCIPARUM; PREVALENCE; SCHOOL; STATISTICS AND NUMERICAL DATA;

ALBENDAZOLE; ANCYLOSTOMATOIDEA; ANEMIA; ANIMALS; ANTHELMINTICS; CHILD; CHILD, PRESCHOOL; FEMALE; HELMINTHIASIS; HOOKWORM INFECTIONS; HUMANS; MALARIA; MALARIA, FALCIPARUM; MALE; PRAZIQUANTEL; PREVALENCE; SCHISTOSOMA; SCHOOLS; TANZANIA;

EID: 84926615716     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/s12879-015-0864-5     Document Type: Article

References (57)

1. Chitsulo L, Engels D, Montressor A, Savioli L. The global status of schistosmiasis and its control. Acta Trop. 2000;77(1):41-51.
2. WHO. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. In: Report of WHO Expert Committee. Geneva: WHO; 2002. p. 1-24.
3. De Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L. Soil transmitted helminth infections: updating the global picture. Trends Parasitol. 2003;19:547-51.
4. Utzinger J, Keiser J. Schistosomiasis and soil transmitted helminthiasis: common drugs for treatment and control. Expert Opin Pharmacotger. 2004;5:263-85.
5. Kinung'hi SM, Magnussen P, Kaatano GM, Kishamawe C, Vennervald BJ. Malaria and helminth Co-infections in school and preschool children: a cross-sectional study in Magu District, North-Western Tanzania. PLoS One. 2014;9(1):e86510.
6. Lwambo NJS, Siza JE, Brooker S, Bundy DAP, Guyatt H. Patterns of concurrent hookworm infections and schistosomiasis in school children in Tanzania. Trans Roy Soc Trop Med Hyg. 1999;93:497-502.
7. Magnussen P, Ndawi B, Sheshe AK, Byskov J, Mbwana K. The Impact of a school health programme on the prevalence and morbidity of urinary schistosomiasis in Mwera Division, Pangani District, Tanzania. Trans R Soc Trop Med Hyg. 2001;95(1):58-64.
8. Magnussen P, Ndawi B, Sheshe AK, Byskov J, Mbwana K. Prevalence and morbidity of urinary schistosomiasis among school children in the Mwera Division of Pangani district, Tanazania. Ann Trop Med Parasitol. 2002;96(8):843-8.
9. Stephenson LS, Latham MC, Ottesen EA. Malnutrition and parasitic helminth infections. Parasitology. 2000;121(Suppl):S23-38.
10. Hotez PJ, Brooker S, Bethony JM. Current concepts: hookworm infection. N Engl J Med. 2004;351(8):799-808.
11. Menendez C, Kahigwa E, Hirt R, Vounatsou P, Aponte JJ, Font F, et al. Randomized placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet. 1997;350:844-50.
12. Lengeler C. Insecticide-treated nets for malaria control: real gains. Bull World Health Organ. 2004;82(2):85-91.
13. Otten M, Aregawi M, Were W, Karema K, Medin A, Bekele W, et al. Initial evidence of reduction of malaria cases and dealhs in Rwanda and Ethiopia due to rapid scale- up of malaria prevention and treatment. Malar J. 2009;8:14.
14. Mashauri FM, Kinung'hi SM, Kaatano GM, Magesa SM, Kishamawe C, Mwanga JR, et al. Impact of indoor residual spraying of lambda-cyhalothrin on malaria prevalence and anemia in an Epidemic-Prone District of Muleba, North-Western Tanzania. Am J Trop Med Hyg. 2013;88(5):841-9.
15. WHO. Preventive chemotherapy in human helminthiasis. Coordinated use of antihelmintic drugs in control interventions. A manual for health professionals and programme managers. Geneva: World Health Organization; 2006. p. 1-62.
16. Tschikuka JG, Scott ME, Gray-Donald K, Kalumba ON. Multiple infection with plasmodium and helminths in communities of low and relatively high socio-economic status. Ann Trop Med Parasitol. 1996;90(3):277-93.
17. Spiegel A, Tall A, Raphenon G, Trape JF, Druilhe P. Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Trans Roy Soc Trop Med Hyg. 2003;97:198-9.
18. Sokhna C, Le Hesran JY, Mbaye PA, Akiana J, Camara P, Diop M, et al. Increased malaria attacks among children presenting concomitant infections by S. mamsoni in Senegal. Malar J. 2004;3:43.
19. Le Hesran JY, Akiana J, Ndiaye EHM, Dia M, Senghor P, Konate L. Severe malaria attach is associeted with high prevalence of ascaris lumbricoides infection among children in rural Senegal. Trans Roy Soc Trop Med Hyg. 2004;98:397-9.
20. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE. Helminth parasites-masters of regulation. Immunol Rev. 2004;201:89-116.
21. Bentwich Z, Kalinkovich A, Weisman Z, Borkow G, Beyers N. Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunol Today. 1999;20:485-7.
22. Gallagher M, Malhotra I, Mungai PL, Wamachi AN, Kioko JM, Ouma JH, et al. The effects of maternal helminth and malaria infections on mother-to-child HIV transmission. AIDS. 2005;19(16):1849-955.
23. Shapiro AE, Tukahebwa EM, Kasten J, Clerk S, Magnussen P. Epidemiology of helminth infections and their relationship to clinical malaria in Southwest Uganda. Trans Roy Soc Trop Med Hyg. 2005;99:18-24.
24. Dreyfuss ML, Stoltzfus RJ, Shrestha JB, Pradhan EK, Leclerg SC, Khatri SK, et al. Hookworms, malaria and vitamin A deficiency contributes to anaemia and iron deficiency among pregnant women of Nepal. J Nutr. 2000;130:2527-36.
25. Ezeamama AE, Friedman JF, Acosta LP, Bellinger DC, Langdon GC, Manalo DL, et al. Helminth infection and cognitive impairment among Filipino children. Am J Trop Med Hyg. 2005;72(5):540-8.
26. Ezeamama AE, McGarvey ST, Acosta LP, Zierler S, Manalo DL, Wu HW, et al. The synergistic effect of concomitant schistosomiasis, hookworm, and trichuris infections on children's anemia burden. PLoS Negl Trop Dis. 2008;2(6):e245.
27. Tohon ZB, Mainassara HB, Garba A, Mahamane AE, Bosque-Oliva E, Ibrahim M, et al. Controlling schistosomiasis: significant decrease of anaemia in Nigerian schoolchildren. PLoS Negl Trop Dis. 2008;2(5):e241.
28. Kirwan P, Asaolu SO, Molloy SF, Abiona TC, Jackson AL, Holland CV. Patterns of soil-transmitted helminth infection and impact of four-monthly albendazole treatments in preschool children from semi-urban communities in Nigeria: a double-blind placebo-controlled randomised trial. BMC Infect Dis. 2009;9:20.
29. Kirwan P, Jackson AL, Asaolu SO, Molloy SF, Abiona TC, Bruce MC, et al. Impact of repeated four-monthly anthelmintic treatment on Plasmodium infection in preschool children: a double-blind placebo-controlled randomized trial. BMC Infect Dis. 2010;10:277.
30. Nacher M. Interactions between worms and malaria: good worms or bad worms? Malar J. 2011;10:259.
31. Vekemans J, Mash K, Greenwood B, Leach A, Kabore W, Soulanoudjingar S. Assessment of severe malaria in a multicenter, phase III, RTS, S/AS01 malaria candidate vaccine trial: case definition, standardization of data collection and patient care. Malar J. 2011;10:221.
32. Anstey NM, Price RN. Improving case definitions for severe malaria. PLoS Med. 2007;4(8):e267.
33. Tukahebwa EM, Vennervald BJ, Nuwaha F, Kabatereine NB, Magnussen P. Comparative efficacy of one versus two doses of praziquantel on cure rate of Schistosoma mansoni infection and re-infection in Mayuge District, Uganda. Trans R Soc Trop Med Hyg. 2013;107(6):397-404.
34. Webster BL, Diaw OT, Seye MM, Faye DS, Stothard JR, Sousa-Figueiredo JC, et al. Praziquantel treatment of school children from single and mixed infection foci of intestinal and urogenital schistosomiasis along the Senegal River Basin: monitoring treatment success and re-infection patterns. Acta Trop. 2013;128(2):292-302.
35. Garba A, Lamine MS, Barkiré N, Djibo A, Sofo B, Gouvras AN, et al. Efficacy and safety of two closely spaced doses of praziquantel against Schistosoma haematobium and S. mansoni and re-infection patterns in school-aged children in Niger. Acta Trop. 2013;128(2):334-44.
36. Moher D, Schulz KF, Altman DG. The CONSORT statement: revised recommendations for improving the quality of reports of parallel group randomized trials. BMC Med Res Methodol. 2001;1(2):1471-2288.
37. Schulz KF, Altman DG, Moher D, The CONSORT Group. CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. Trials. 2010;11:32.
38. Helmby H, Kullberg M, Troye-Blomberg M. Altered immune responses in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections. Infect Immun. 1998;66(11):5167-74.
39. Nacher M, Singhasivanon P, Yimsamran S, Manibunyong W, Thanyavanich N, Wuthisen P, et al. Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J Parasitol. 2002;88(1):55-8.
40. Druilhe P, Tall A, Sokhna C. Worms can worsen malaria. Towards a new means to roll back malaria? Trends Parasitol. 2005;21:359-62.
41. Fenton A. Dances with worms: the ecological and evolutionary impacts of deworming on coinfecting pathogens. Parasitology. 2013;140:1119-32.
42. Wiria AE, Hamid F, Wammes LJ, Kaisar MMM, May L. The effect of three-monthly albendazole treatment on malarial parasitemia and allergy: a household-based cluster-randomized, double-blind, placebo-controlled trial. PLoS One. 2013;8(3):e57899.
43. Waknine-Grinberg JH, Gold D, Ohayon A, Flescher E, Heyfets A, Doenhoff MJ, et al. Schistosoma mansoni infection reduces the incidence of murine cerebral Malaria. Malar J. 2010;9:1186.
44. Beasley NM, Tomkins AM, Hall A, Kihamia CM, Lorri W. The impact of population level deworming on the haemoglobin levels of school children in Tanga, Tanzania. Trop Med Intl Health. 1999;4:744-50.
45. Crump JA, Morrissey AB, Nicholson WL, Massung RF, Stoddard RA. Etiology of severe Non-malaria febrile illness in Northern Tanzania: a prospective cohort study. PLoS Negl Trop Dis. 2013;7(7):e2324.
46. Crump JA, Ramadhani HO, Morrissey AB, Saganda W, Mwako MS. Invasive bacterial and fungal infections among hospitalized HIV-infected and HIV-uninfected adults and adolescents in Northern Tanzania. Clin Infect Dis. 2011;52:341-8.
47. Crump JA, Ramadhani HO, Morrissey AB, Msuya LJ, Yang LY. Invasive bacterial and fungal infections among hospitalized HIV-infected and HIV-uninfected children and infants in northern Tanzania. Trop Med Int Health. 2011;16:830-7.
48. Mwangi TW, Bethony JM, Brooker S. Malaria and helminth interactions in humans: an epidemiological viewpoint. Ann Trop Med Parasitol. 2006;100(7):551-70.
49. Murray J, Murray A, Murray M, Murray C. The biological suppression of malaria: an ecological and nutritional interrelationship of the host and two parasites. Am J Clin Nutr. 1978;31:1363-6.
50. Brutus L, Watier L, Briand V, Hanitrasoamampionona V, Razanatsoarilala H, Cot M. Parasitic co-infections: does Ascaris lumbricoides protect against Plasmodium falciparum infection? Am J Trop Med Hyg. 2006;75(2):194-8.
51. Brutus L, Watier L, Briand V, Hanitrasoamampionona V, Razanatsoarilala H, Cot M. Confirmation of the protective effect of Ascaris lumbricoides on Plasmodium falciparum infection: results of a randomized trial in Madagascar. Am J Trop Med Hyg. 2007;77(6):1091-5.
52. Carneiro IA, Smith T, Lusingu JP, Malima R, Utzinger J, Drakeley CJ. Modeling the relationship between the population prevalence of Plasmodium falciparum malaria and anemia. Am J Trop Med Hyg. 2006;75(2 Suppl):82-9.
53. Enhardt S, Burchard GD, Mantel C, Cramer JP, Kaiser S. Malaria, anaemia and malnutrition in African school children. Defining intervention strategies. J Inf Dis. 2006;194:108-14.
54. Koukounari A, Fenwick A, Whawell S, Kabatereine NB, Kazibwe F, Tukahebwa EM, et al. Morbidity indicators of schistosomma mansoni: relationship between infection and anaemia in Ugandan school children before and after praziquantel and albedazole chemotherapy. Am J Trop Med Hyg. 2006;75(2):278-86.
55. Deribew K, Zinaye T, Petro B. Urinary schistosomiasis and malaria associated anemia in Ethiopia. Asian Pac J Trop Biomed. 2013;3(4):307-10.
56. Schellenberg D, Menendez C, Kahigwa E, Aponte J, Vidal J, Tanner M, et al. Intermittent treatment for malaria and anaemia control at time of routine vaccination in Tanzanian infants: a randomized placebo controlled trial. Lancet. 2001;357:1471-7.
57. Shulman CE, Dorman EK, Kutts F, Kawuondo K, Bulmer JN, Peshu N, et al. Intermittent sulphadoxine-pyrimethamine to prevent severe anaemia secondary to malaria in pregnancy: a randomised placebo controllled trial. Lancet. 1999;353:632-6.