Lymphatic filariasis in Luangwa District, South-East Zambia

Sheila Tamara Shawa1, E. T. Mwase1, Erik Helmer Pedersen2, Paul E. Simonsen2
1Department of Paraclinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia
2Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Thorvaldsensvej 57, 1871, Frederiksberg C, Denmark

Tóm tắt

Abstract Background Past case reports and recent data from LF mapping surveys indicate that LF occurs in Zambia, but no studies have been carried out to document its epidemiology and health implications. The present study assessed infection, disease, transmission and human perception aspects of LF in an endemic area of Luangwa District, South-East Zambia, as a background for planning and implementation of control. Methods Two neighbouring rural communities were registered and a questionnaire survey undertaken. Clinical examination, and sampling of blood for circulating filarial antigens (CFA; marker of adult worm infection) and antibodies to Bm14 antigen (marker of exposure to transmission), were carried out during the daytime. Blood from CFA positive individuals was examined for microfilariae (mf) at night. Vector surveys were carried out in selected households, using light traps. Results 985 individuals aged ≥ 1 year were registered. The CFA prevalence increased with age from 1.2% in age group 1–14 years to 20.6% in age group 50+ years (overall 8.6%). Wuchereria bancrofti mf were identified in 10.9% of CFA positive individuals (corresponding to a community prevalence of 0.9%). Prevalence and intensity of Bm14 antibodies were much higher in individuals ≥ 30 years than in younger individuals (57.2 vs. 19.3%; 0.594 vs. 0.241 OD-values). Elephantiasis and hydrocele were well known clinical manifestations in the area, but only one case of hydrocele was detected in the study population. Identified potential vectors were Anopheles funestus and An. gambiae. Conclusion The study confirmed that LF was endemic in the study communities, but infection and disease prevalence was low. Several indications, including a marked recent decline in CFA prevalence, suggest that transmission in the area is on the decrease, perhaps because of intensive application of malaria control measures targeting the Anopheles vectors. It is recommended that mass drug administration is initiated to accelerate this positive trend of decline in LF transmission in the area.

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Tài liệu tham khảo

Hotez PJ, Kamath A: Neglected tropical diseases in Sub-Saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis. 2009, 3: e412-10.1371/journal.pntd.0000412.

Ngwira BMM, Jabu CH, Kanyongoloka H, Mponda M, Crampin AC, Branson K, Alexender NDE, Fine PEM: Lymphatic filariasis in the Karonga district of Northern Malawi: a prevalence survey. Ann Trop Med Parasitol. 2002, 96: 137-144. 10.1179/0003498302125000411.

Ngwira BMM, Tambala P, Perez AM, Bowie C, Molyneux DH: The geographical distribution of lymphatic filariasis infection in Malawi. Filaria J. 2007, 6: 12-10.1186/1475-2883-6-12.

Nielsen NO, Makaula P, Nyakuipa D, Bloch P, Nyasulu Y, Simonsen PE: Lymphatic filariasis in lower Shire, Southern Malawi. Trans R Soc Trop Med Hyg. 2002, 96: 133-138. 10.1016/S0035-9203(02)90279-8.

Manhenje I, Galan-Puchades MT, Fuentes MV: Socio-environmental variables and transmission risk of lymphatic filariasis in central and northern Mozambique. Geospat Hlth. 2013, 7: 391-398.

Sasa M: Human filariasis: A global survey of epidemiology and control. 1976, University of Tokyo Press

Hawking F: The distribution of human filariasis throughout the World part III. Africa. Trop Dis Bull. 1977, 74: 649-679.

Fujita K, ODA T, Tsukidate S, Mori A, Ueda M, Kurokawa K: Preliminary report on human filariasis in Mozambique, East Africa. Trop Med. 1985, 27: 83-91.

Kelly-Hope LA, Thomas BC, Bockerie MJ, Molyneux DH: Lymphatic filariasis in the Democratic Republic of Congo; micro-stratification overlap mapping (MOM) as a prerequisite for control and surveillance. Parasit Vectors. 2011, 4: 178-10.1186/1756-3305-4-178.

Buckley JJC: A helminthological survey in Northern Rhodesia. J Helminthol. 1946, 21: 111-174. 10.1017/S0022149X00032041.

Barclay R: Filariasis in Luangwa basin. Med J Zambia. 1971, 5: 201-203.

Hira PR: Bancroftian filariasis in Zambia. Ann Trop Med Parasitol. 1975, 69: 521-522.

Hira PR: Bancroftian filariasis: an autochthonous case in Zambia. Med J Zambia. 1976, 10: 160-163.

Hira PR: Wuchereria bancrofti: the staining of the microfilarial sheath in giemsa and haematoxylin for diagnosis. Med J Zambia. 1977, 11: 93-96.

Kaile T: Filariasis presenting as pyrexia of unknown origin in a young Zambian adult: a case report. Zambian J Med Health Sci. 1998, 2: 2-3.

Matondo AS, Lungu AG: Lymphatic filariasis in a Zambian woman: a case report. Zambian J Med Health Sci. 1998, 2: 55-56.

Mwase ET, Stensgaard AS, Msakashalo-Senkwe M, Mubila L, Mwansa J, Songolo P, Shawa ST, Simonsen PE: Mapping the geographical distribution of lymphatic filariasis in Zambia. PLoS Negl Trop Dis. In press

Weil GJ, Lammie PJ, Weiss N: The ICT filariasis test: a rapid-format antigen test for diagnosis of bancroftian filariasis. Parasitol Today. 1997, 13: 401-404. 10.1016/S0169-4758(97)01130-7.

Weil GJ, Ramzy RMR: Diagnostic tools for filariasis elimination programs. Trends Parasitol. 2006, 23: 2-

Tisch DJ, Bockarie MJ, Dimber Z, Kiniboro B, Tarongka N, Hazlett FE, Kastens W, Alpers MP, Kuzura JW: Mass drug administration trail to eliminate lymphatic filariasis in Papua New Guinea: changes in microfilaraemia, filarial antigen, and Bm14 antibody after cessation. Am J Trop Med Hyg. 2008, 78: 289-293.

Estambale BBA, Simonsen PE, Knight R, Bwayo JJ: Bancroftian filariasis in Kwale District of Kenya. I. clinical and parasitological survey in an endemic community. Ann Trop Med Parasitol. 1994, 88: 145-151.

Meyrowitsch DW, Simonsen PE, Makunde WH: Bancroftian filariasis: analysis of infection and disease in five endemic communities of north-eastern Tanzania. Ann Trop Med Parasitol. 1995, 89: 653-663.

McMahon JE, Marshall TF, Vaughan JP, Abaru DE: Bancroftian filariasis: a comparison of microfilariae counting techniques using counting chamber standard slide and membrane (nuclepore) filtration. Ann Trop Med Hyg. 1979, 73: 457-464.

Rwegoshora RT, Pedersen EM, Mukoko DA, Meyrowitsch DW, Masese N, Malecela–Lazaro MN, Ouma JH, Michael E, Simonsen PE: Bancroftian filariasis: patterns of vector abundance and transmission in two east African communities with different levels of endemicity. Ann Trop Med Parasitol. 2005, 99: 253-265. 10.1179/136485905X29675.

Joseph HM, Melrose W: Applicacility of the filter paper technique for detection of antifilarial IgG4 antibodies using the Bm14 filariasis CELISA. J Parasitol Res. 2010, Article ID 594687

Weil GJ, Curtis KC, Fischer PU, Won KY, Lammie PJ, Joseph H, Melrose WD, Brattig NW: A multicentre evaluation of a new antibody test kit for lymphatic filariasis employing recombinant Brugia malayi antigen Bm-14. Acta Trop. 2011, 120s: s19-s22.

Onapa AW, Simonsen PE, Pedersen EM, Okelle DO: Lymphatic filariasis in Uganda: baseline investigations in Lira, Soroti and Katawi districts. Trans R Soc Trop Med Hyg. 2001, 95: 161-167. 10.1016/S0035-9203(01)90145-2.

Simonsen PE, Meyrowitsch DW, Jaoko WG, Malecela MN, Mukoko D, Pedersen EM, Ouma JH, Rwegoshora RT, Masese N, Magnussen P, Estambale BBA, Micheal E: Bancroftian filariasis infection, disease, and specific antibody response patterns in a high and a low endemicity community in East Africa. Am J Trop Med Hyg. 2002, 66: 550-559.

Joseph H, Maiava F, Naseri T, Silva U, Lammie P, Melrose W: Epidemiological assessment of continuing transmission of lymphatic filariasis in Samoa. Ann Trop Med Parasitol. 2011, 105: 567-578. 10.1179/2047773211Y.0000000008.

Roberts CJ, Whitehall J, Gelfand M: W. bancrofti in Kenyemba area. Cent Afr J Med. 1973, 19: 13-14.

Davey G, Tekola F, Newport MJ: Podoconiosis: non-infectious geochemical elephantiasis. Trans R Soc Trop Med Hyg. 2007, 101: 1175-1180. 10.1016/j.trstmh.2007.08.013.

Parker M, Allen T: Will mass drug administration eliminate lymphatic filariasis? Evidence from northern coastal Tanzania. J Biosoc Sci. 2013, 45: 517-545. 10.1017/S0021932012000466.

Kent RJ: The mosquitoes of Macha, Zambia. 2006, The John Hopkins Malaria Research Institute,http://www.jhsph.edu/malaria,

Kent RJ, Thuma PE, Mrakurva S, Norris DE: Seasonality, blood feeding behaviour, and transmission of Plasmodium falciparum by Anopheles arabiensis after an extended draught in southern Zambia. Am J Trop Med Hyg. 2007, 76: 267-274.

Fornadel CM, Norris LC, Glass GE, Norris DE: Analysis of Anopheles arabiensis blood feeding behaviour in southern Zambia during the two years after introduction of insecticide-treated bed nets. Am J Trop Med Hyg. 2010, 84: 848-853.

Seyoum A, Sikaala CH, Canda J, Chinula D, Ntamatungiro AJ, Hawela M, Miller JM, Russell TL, Briet OJT, Killeen G: Human exposure to anopheline mosquitoes occurs primarily indoors, even for users of insecticide-treated nets in Luangwa Valley, South-east Zambia. Parasit Vectors. 2012, 5: 101-10.1186/1756-3305-5-101.

Sikaala CH, Killeen GF, Chanda J, Chinula D, Miller JM, Rusell TL, Seyoum A: Evalutaion of alternative mosquito sampling methods for malaria vectors in lowland South-East Zambia. Parasit Vectors. 2013, 6: 91-10.1186/1756-3305-6-91.

Bockarie MJ, Pedersen EM, White GB, Micheal E: Role of vector control in the global program to eliminate lymphatic filariasis. Ann Rev Entomol. 2009, 54: 469-487. 10.1146/annurev.ento.54.110807.090626.

Merelo-Lobo RA, McCall PJ, Perez MA, Spiers AA, Mzilahowa T, Ngwire B, Molyneux DH, Donelly MJ: Identification of the vectors of lymphatic filariasis in the Lower Shire Valley, southern Malawi. Trans R Soc Trop Med Hyg. 2003, 97: 299-301. 10.1016/S0035-9203(03)90149-0.

Kent RJ, Mrakurva S, Hamapumbu H, Norris DE: Recognition of a novel melanotic mutant in a field population of Culex pipiens quinquefasciatus in southern Zambia. J Am Mosq Contr Assoc. 2007, 23: 71-75. 10.2987/8756-971X(2007)23[71:ROANMM]2.0.CO;2.

Chizema-Kawesha E, Miller JM, Steketee RW, Mukonka VM, Mukuka C, Mohamed AD, Miti SK, Campbell CC: Scaling up malaria control in Zambia: Progress and impact 2005–2008. Am J Trop Med Hyg. 2010, 83: 480-488. 10.4269/ajtmh.2010.10-0035.

Larsen DA, Keating J, Miller J, Bennett A, Changufu C, Katebe C, Eisele TP: Barriers to insecticide-treated mosquito net possession 2 years after a mass free distribution campaign in Luangwa District Zambia. PloS One. 2010, 5: e13129-10.1371/journal.pone.0013129.

Kelly-Hope LA, Molyneux DH, Bockarie MJ: Can malaria vector control accelerate the interruption of lymphatic filariasis transmission in Africa; capturing a window of opportunity?. Parasit Vectors. 2013, 6: 39-10.1186/1756-3305-6-39.

Chanda E, Masaninga F, Coleman M, Sikaal C, Katebe C, MacDonald M, Baboo KS, Govere J, Manga L: Integrated vector management: the Zambian experience. Malaria J. 2008, 7: 164-10.1186/1475-2875-7-164.

Chanda E, Hemingway J, Kleinschmidt I, Rehman AM, Phiri FN, Coetzer S, Mthembu D, Shinondo CJ, Chizema-Kawesha E, Kamuliwo M, Mukonka V, Baboo KS, Coleman M: Insecticide resistance and the future of malaria control in Zambia. PLoS One. 2011, 6: e24336-10.1371/journal.pone.0024336.

Webber RH: The natural decline of Wuchereria bancrofti infection in a vector control situation in the Solomon Islands. Trans R Soc Trop Med Hyg. 1977, 71: 396-400. 10.1016/0035-9203(77)90037-2.

Njenga SM, Mwandawiro CS, Wamae CN, Mukoko DA, Omar AA, Shimada M, Bockarie MJ, Molyneux DH: Sustained reduction in prevalence of lymphatic filariasis infection in spite of missed rounds of mass drug administration in an area under mosquito nets for malaria control. Parasit Vectors. 2011, 4: 90-10.1186/1756-3305-4-90.