Efficacy of integrated school based de-worming and prompt malaria treatment on helminths -Plasmodium falciparum co-infections: A 33 months follow up study

BMC International Health and Human Rights

Takafira Mduluza⁸  Nirbhay Kumar²  Francisca Mutapi⁵  Vivian Chadukura⁷  Gibson Hlerema⁷  James Mudzori³  Kimberly C Brouwer⁴  Munyaradzi P Mapingure⁸  Godfrey Makware¹  Noah H Paul⁸  Davison Sangweme²  Sekesai Mtapuri-Zinyowera⁶  Nicholas Midzi⁷ 

[1] Central Statistical Office, PO Box CY 342, Causeway, Harare, Zimbabwe;Johns Hopkins Bloomberg School of Public Health, Department of Molecular Microbiology and Immunology, Baltimore, Maryland, USA;National Microbiology Reference Laboratory, P.O. Box ST749, Southerton, Zimbabwe;University of California, San Diego, Division of International Health & Cross Cultural Medicine, Department of Family and Preventive Medicine, San Diego, California USA;University of Edinburgh, Institute for Immunology and Infection Research, Edinburgh, UK;College of Health Sciences, Department of Medical Microbiology, P.0 Box A178, Avondale, Harare, Zimbabwe;National Institute of Health Research, Box CY 573, Causeway Harare, Zimbabwe;University of Zimbabwe, Department of Biochemistry, P.O Box MP167, Mount Pleasant, Harare, Zimbabwe

关键词: deworming;    STHs;    schistosomiasis;    malaria;    co-infection;   

Others  :  856609
DOI  :  10.1186/1472-698X-11-9

 received in 2011-04-19, accepted in 2011-06-22,  发布年份 2011

【 摘 要 】

Background

The geographical congruency in distribution of helminths and Plasmodium falciparum makes polyparasitism a common phenomenon in Sub Saharan Africa. The devastating effects of helminths-Plasmodium co-infections on primary school health have raised global interest for integrated control. However little is known on the feasibility, timing and efficacy of integrated helminths-Plasmodium control strategies. A study was conducted in Zimbabwe to evaluate the efficacy of repeated combined school based antihelminthic and prompt malaria treatment.

Methods

A cohort of primary schoolchildren (5-17 years) received combined Praziquantel, albendazole treatment at baseline, and again during 6, 12 and 33 months follow up surveys and sustained prompt malaria treatment. Sustained prompt malaria treatment was carried out throughout the study period. Children's infection status with helminths, Plasmodium and helminths-Plasmodium co-infections was determined by parasitological examinations at baseline and at each treatment point. The prevalence of S. haematobium, S. mansoni, STH, malaria, helminths-Plasmodium co-infections and helminths infection intensities before and after treatment were analysed.

Results

Longitudinal data showed that two rounds of combined Praziquantel and albendazole treatment for schistosomiasis and STHs at 6 monthly intervals and sustained prompt malaria treatment significantly reduced the overall prevalence of S. haematobium, S. mansoni, hookworms and P. falciparum infection in primary schoolchildren by 73.5%, 70.8%, 67.3% and 58.8% respectively (p < 0.001, p < 0.001, p < 0.001, p < 0.001 respectively). More importantly, the prevalence of STH + schistosomes, P. f + schistosomes, and P. f + STHs + schistosomes co-infections were reduced by 68.0%, 84.2%, and 90.7%, respectively. The absence of anti-helminthic treatment between the 12 mth and 33 mth follow-up surveys resulted in the sharp increase in STHs + schistosomes co-infection from 3.3% at 12 months follow up survey to 10.7%, slightly more than the baseline level (10.3%) while other co-infection combinations remained significantly low. The overall prevalence of heavy S. haematobium, S. mansoni and hookworms infection intensities were significantly reduced from: 17.9-22.4% to 2.6-5.1%, 1.6-3.3% to 0.0% and 0.0-0.7% to 0.0% respectively.

Conclusion

Biannual Integrated school based antihelminthic and sustained prompt malaria treatment has a potential to reduce the burden of helminths-plasmodium co-infections in primary school children. In areas of stable malaria transmission, active case finding is recommended to track and treat asymptomatic malaria cases as these may sustain transmission in the community.

【 授权许可】

   
2011 Midzi et al; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]World Health Organization: The prevention and control of schistosomiasis and soil transmitted helminthiasis. Report of a WHO Expert Committee. Geneva, WHO Technical Report Series No.912 2002.
• [2]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(12):547-551.
• [3]Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S: Hookworm infection. N Engl J Med 2004, 351(8):799-807.
• [4]World Health Organization: World malaria report. WHO; 2009.
• [5]Taylor P, Makura O: Prevalence and distribution of schistosomiasis in Zimbabwe. Ann Trop Med Parasitol 1985, 79(3):287-99.
• [6]Chandiwana SK, Taylor P, De V, Clarke V: Prevalence and intensity of schistosomiasis in two rural areas in Zimbabwe and their relationship to village location and snail infection rates. Ann Trop Med Prasitol 1988, 82(2):163-173.
• [7]Chimbari MJ, Chirundu D: Prevalence and intensity of the schistosomiasis situation along the Zimbabwean urban and peri-urban shoreline of Lake Kariba. Cent Afr J Med 2003, 49(1-2):8-12.
• [8]Midzi N, Sangweme D, Zinyowera S, Mapingure MP, Brouwer KC, Munatsi A, Mutapi F, Mudzore J, Kumar N, Woelk G, Mduluza T: The burden of polyparasitism among primary school children in rural and farming areas in Zimbabwe. Trans R Soc Trop Med Hyg 2008, 102:1039-1045.
• [9]Zimbabwe National Health Profile Ministry of Health and Child Welfare, Harare, Zimbabwe; 2008.
• [10]Macdonald F, Goldsmid JM: Intestinal helminth infections in the Burma Valley area of Rhodesia. Cent Afr J Med 1973, 19(6):113-115.
• [11]Chandiwana SK, Kambaza A, Mutetwa SM: A study of nutritional status, parasitic infection and haematology in a farm worker community in Zimbabwe. Cent Afr J Trop Med 1984, 30(9):172-175.
• [12]Chandiwana SK, Bradley M, Chombo F: Hookworm and round worm infections in farm - worker communities in the large-scale agricultural sector in Zimbabwe. J Trop Med Hyg 1989, 92(5):338-3344.
• [13]Taylor P, Mutambu SL: A review of the malaria situation in Zimbabwe with special reference to the period 1972-1981. Trans R Soc Trop Med Hyg 1986, 80:12-19.
• [14]Brooker S, Clements ACA, Hotez PJ, Hay SI, Tatem AJ, Bundy DAP, Snow R: The co-distribution of Plasmodium falciparum and hookworm among African school children. Mal J 2006, 5:99. BioMed Central Full Text
• [15]Raso G, Luginbüh A, Adjoua CA, Tian-Bi NT, Silué KD, Matthys B, Vounatsou P, Wang Y, Dumas ME, Holmes E, Singer BH, Tanner M, N'Goran EK, Utzinger J: Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Côte d'Ivoire. Int J Epi 2004, 33:1092-1102.
• [16]Hotez JP, Molyneux DH, Fenwick A, Ottesen E, Sachs SE, Sachs JD: Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDs, Tuberculosis and Malaria. PLoS Medicine 2006, 3(5):001-009.
• [17]Le Hesran JY, Akiana J, Ndiaya JM, Dia M, Konate L: Severe malaria attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal. Trans R Soc Trop Med Hyg 2004, 98:397-399.
• [18]Graham Al, Lamb TJ, Read AF, Allen JE: Malaria-filaria co-infection in mice makes malarial disease more severe unless filarial infection achieves patency. JID 2005, 191:410-421.
• [19]Legesse M, Erko B, Balcha F: Increased parasitaemia and delayed parasite clearance in Schistosoma mansoni and Plasmodium berghei co-infected mice. Acta Tropica 2004, 91:161-166.
• [20]Spiegel A, Tall A, Raphenon G, Trape JF, Druilhe : Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 2003, 97:198-199.
• [21]Briand V, Watier I, Le Hesran JV, Garcia A, Cot M: Coinfection with Plasmodium falciparum and Schistosoma haematobium: Protective effect of schistosomiasis on malaria in Senegalese children? Am J Trop Med Hyg 2005, 72(6):702-707.
• [22]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):194-198.
• [23]Lyke K, Dicko A, Dabo A, Sangare L, Kone A, Coulibaly D, Guindo A, Traore K, Daou M, Diarra I, Sztein MB, Plowe CV, Doumbo OK: Association of Schistosoma haematobium infection with protection against acute Plasmodium falciparum malaria in Malian children. Am J Trop Med Hyg 2005, 73(6):1124-1130.
• [24]Druilhe P, Adama Tall A, Sokhna C: Worms can worsen malaria: towards a new means to roll back malaria? Trends Parasitol 2005, 21(8):359-362.
• [25]Stoltzfus RJ, Chwaya HM, Tielsch JM, Schulze KJ, Albonico M, Salvioli L: Epidemiology of iron deficiency anaemia in Zanzibari schoolchildren: the importance of hookworms. Am J Clin Nutr 1997, 65:153-9.
• [26]Olsen A, Kabarateine NB, Ndyomugyenyi R, Brooker S: Epidemiology of helminths infections and their relationship to clinical malaria in South West-Uganda. Trans R Soc Trop Med & Hyg 2005, 99:18-24.
• [27]Nkuo-Akenji TK, Chi PC, Cho JF, Ndamukong KKJ, Sumbele I: Malaria and helminth co-infection in children living in a malaria endemic setting of mount Cameroon and predictors of anemia. J Parasitol 2006, 92(6):1191-1195.
• [28]Midzi N, Mtapuri-Zinyowera S, Sangwemec D, Chirehwa MT, Mapingure MP, Mudzori J, Hlerema G, Mutapi F, Kumar N, Mduluza T: Consequences of polyparasitism on anaemia among primary school children in Zimbabwe. Acta Tropica 2010.
• [29]Nokes C, Bundy DAP: Compliance and absenteeism in school children: implications for helminth control. Trans R Soc Trop Med Hyg 1993, 87:148-152.
• [30]Brooker S, Guyatt H, Omumbo J, Shretta R, Drake L, Ouma J: Situation Analysis of Malaria in School-aged Children in Kenya - What Can Be Done? Parasitology Today 2000, 16(5):183-185.
• [31]Stephenson LS, Latham MC, Adams EJ, Kinoti SN, Pertet A: Weight gain of Kenyan school children infected with hookworm, Trichuris trichiura and Ascaris lumbricoides is improved following once- or twice yearly treatment with albendazole. J Nutr 1993, 123:656-665.
• [32]Nokes C, Cooper ES, Robinson BA, Bundy DAP: Geohelminth infection and academic assessment in Jamaican children. Trans R Soc Trop Med Hyg 1991, 85:272-273.
• [33]Nokes C, Mcgarvey ST, Shiue I, Wu G, Wu H, Bundy DAP, Olds GR: Evidence for an improvement in cognitive function following treatment of Schistosoma japonicum infection in Chinese primary schoolchildren. Am J Trop Med Hyg 1999, 60(4):556-565.
• [34]Partnership for Child Development: Heavy schistosomiasis associated with poor short-term memory and slower reaction times in Tanzanian schoolchildren. Trop Med Int Health 2002, 7(2):104-117.
• [35]Ndamba J, Makaza N, Munjoma M, Gomo E, Kaondera KC: The physical fitness and work performance of agricultural workers infected with Schistosoma mansoni in Zimbabwe. Ann Trop Med Parasitol 1993, 87(6):553-61.
• [36]Molyneux DH, Hotez PJ, Fenwick A: "Rapid-impact interventions": How a policy of integrated control for Africa's neglected tropical diseases could benefit the poor. PLoS Med 2005, 2:e336.
• [37]Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW, Hotez PJ: Epidemiology of Plasmodium-helminths co-infection in Africa: Population at risk, potential impact on anaemia, and prospects for combining control. Am J Trop Med Hyg 2007, 77(suppl 6):88-98.
• [38]World Health Organization: Preventive chemotherapy in human helminthiasis, coordinated use of antihelminthic drugs in control interventions: a manual for health professionals and programme managers. Geneva: WHO; 2006.
• [39]Brooker S, Clarke S, Snow RW, Bundy DAP: Malaria in African schoolchildren: Options for control. Trans R Soc Trop Med Hyg 2008, 102:304-305.
• [40]Utzinger J, Raso G, Brooker S, De Savigny D, Tanner M, Ornbejerg N, Singer BH, N'goran EK: Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution. Parasitol 2009, 136:1859-1874.
• [41]Hall A, Horton S: New advice from CCo8. Deworming. Copenhagen Consensus Centre Best practice paper. Copenhagen Business School. Solbjerg Plads3.2000 Frederiksberg. Denmark 2009.
• [42]Mutapi F, Ndhlovu PD, Hagan P, Woolhouse ME: Anti-schistosome antibody responses in children co-infected with malaria. Parasite Immunol 2000, 22:341-348.
• [43]Chandiwana SK, Taylor P, Clarke V: Prevalence and intensity of schistosomiasis in two rural areas in Zimbabwe and their relationship to village location and snail infection rates. Ann Trop Med Parasitol 1988, 82(2):163-173.
• [44]Mott KE, Baltes R, Bambagha J, Baldassini B: Field studies of a reusable polyamide filter for detection of Schistosma haematobium eggs by urine filtration. Tropen medlizin and Parasitologie 1982, 3:227-228.
• [45]Doehring E, Feldmeier H, Daffalla AA: Day-to-day variation and circadian rhythm of eggs excretion in urinary schistosomiasis in the Sudan. Ann Trop Med and Parastol 1983, 77:587-594.
• [46]Cheesbrough M: Formal ether concentration technique. District Laboratory Practice in Tropical Countries Part 1: Tropical Health Technology, Cambridge PE15 OTT UK 1998, 197-199.
• [47]Katz N, Chaves A, Pellegrino J: A simple device for quantitative stool thick-smear technique in Schistosoma mansoni. Revisita do instituto de Medicina Tropical de Sao Paulo 1972, 14:397-400.
• [48]EDLIZ: Essential drugs list and Standard Treatment Guidelines for Zimbabwe. Harare, Zimbabwe 4th edition. 2000.
• [49]Ezeamama AE, Friedman JF, Olveda RM, Acosta LP, Kurtis JD, Mor V, McGarvey ST: Functional significance of low-intensity polyparasite helminth infections in anaemia. JID 2008, 192(12):2160-2170.
• [50]Ezeamama AE, McGarvey ST, Acosta LP, Zierler S, Manalo DL, Wu HW, Kurtis JD, Mor V, Olveda RM, Friedman JF: The synergistic effect of concomitant schistosomiasis hookworm and Trichuris infections on children's anaemia burden. PLoS Negl Trop Dis 2008, 2(6):e245. 18523547 (P, S, G, E, B, D).
• [51]WHA (54.19): Communicable diseases. World Health Assembly Resolution 2001.
• [52]Raso G, Vounatsou P, Singer BH, Goran EKN, Tanner M, Utzinger J: An integrated approach for risk profiling and spatial prediction of Schistosoma mansoni-hookworm co-infection. PNAS 2006, 103(18):6934-6939.
• [53]Toure S, Zhang Y, Bosque-Oliva E, Ky C, Ouedraogo A, Koukounari A, Gabrielli AF, Sellin B, Webster JP, Fenwick A: Two-year impact of single praziquantel treatment on infection in the national control programme on schistosomiasis in Burkina Faso. Bull World Health Organ 2008, 86:780-787.
• [54]Knopp S, Mohammed KA, Rollinson D, Stothard JR, Khamis IS, Utzinger J, Marti H: Changing Patterns of Soil-Transmitted Helminthiases in Zanzibar in the Context of National Helminth Control Programs. Am J Trop Med Hyg 2009, 81(6):1071-1078.
• [55]Woolhouse MEJ, Watts CH, Chandiwana SK: Heterogeneities in transmission rates and the epidemiology of schistosome infection. Proc R Soc Lond B 1991, 245:109-114.
• [56]Chandiwana SK, Woolhouse MEJ: Heterogeneities in water contact patterns and the epidemiology of Schistosoma haematobium. Parastol 1991, 103:363-370.
• [57]Woohouse MEJ, Etard JF, Dietz K, Ndhlovhu PD, Chandiwana SK: Heterogeneities in schistosome transmission dynamics and control. Parasitol 1998, 117:475-482.
• [58]McGregor IA: Immunology of malarial infection and its possible consequences. Br Med Bull 1972, 28:22-27.
• [59]Grobusch MP, Egan E, Gosling RD, Newman RD: Intermittent preventive therapy for malaria: progress and future directions. Curr Opin Infect Dis 2007, 20:613-620.
• [60]Menendez C, Schellenberg D, Macete E, Aide P, Kahigwa E, Sanz S, Aponte JJ, Sacarlal J, Mshinda H, Tanner M, Alonso PL: Varying efficacy of intermittent preventive treatment for malaria in infants in two similar trials: public health implications. Mal J 2007, 6:132. BioMed Central Full Text