Transmission of Onchocerca volvulus Continues in Nyagak-Bondo Focus of Northwestern Uganda after 18 Years of a Single Dose of Annual Treatment with Ivermectin

Moses N. Katabarwa The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Tom Lakwo The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Peace Habomugisha The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Stella Agunyo The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Edson Byamukama The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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David Oguttu The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Ephraim Tukesiga The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Dickson Unoba The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Patrick Dramuke The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Ambrose Onapa The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Edridah M. Tukahebwa The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Dennis Lwamafa The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Frank Walsh The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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Thomas R. Unnasch The Carter Center, Atlanta, Georgia; Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Health Services, Kabarole District, FortPortal, Uganda; Health Services, Nebbi District, Nebbi, Uganda; Health Services, Zombo District, Zombo, Uganda; ENVISION, ENVISION/RTI International, Kampala, Uganda; National Disease Control, Ministry of Health, Kampala, Uganda; Entomology, Lythan St. Anne's, Lancashire, United Kingdom; Global Health, University of South Florida, Tampa, Florida

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The objective of the study was to determine whether annual ivermectin treatment in the Nyagak-Bondo onchocerciasis focus could safely be withdrawn. Baseline skin snip microfilariae (mf) and nodule prevalence data from six communities were compared with data collected in the 2011 follow-up in seven communities. Follow-up mf data in 607 adults and 145 children were compared with baseline (300 adults and 58 children). Flies collected in 2011were dissected, and poolscreen analysis was applied to ascertain transmission. Nodule prevalence in adults dropped from 81.7% to 11.0% (P < 0.0001), and mf prevalence dropped from 97.0% to 23.2% (P < 0.0001). In children, mf prevalence decreased from 79.3% to 14.1% (P < 0.0001). Parous and infection rates of 401 flies that were dissected were 52.9% and 1.5%, respectively, whereas the infective rate on flies examination by polymerase chain reaction (PCR) was 1.92% and annual transmission potential was 26.9. Stopping ivermectin treatment may result in onchocerciasis recrudescence.

Author Notes

* Address correspondence to Moses N. Katabarwa, The Carter Center, One Copenhill, 453 Freedom Parkway Atlanta, GA 30307. E-mail: mkataba@emory.edu

Authors' addresses: Moses N. Katabarwa, The Carter Center, Atlanta, GA, E-mail: mkataba@emory.edu. Tom Lakwo, David Oguttu, and Edridah M. Tukahebwa, Vector Control Division, Ministry of Health, Kampala, Uganda, E-mails: tlakwo@gmail.com, dguttu@gmail.com, and edmuheki@gmail.com. Peace Habomugisha, Stella Agunyo, and Edson Byamukama, Health Programs, The Carter Center, Kampala, Uganda, E-mails: provia5@hotmail.com, agunyoegunyu@gmail.com, and edson.navs@gmail.com. Ephraim Tukesiga, Health Services, Kabarole District, FortPortal, Uganda, E-mail: ephraim.tukesiga@gmail.com. Dickson Unoba, Health Services, Nebbi District, Nebbi, Uganda, E-mail: unoba2@gmail.com. Patrick Dramuke, Health Services, Zombo District, Zombo, Uganda, E-mail: dramuke.patrick@gmail.com. Ambrose Onapa, ENVISION, RTI International, Kampala, Uganda, E-mail: kwibale1@yahoo.co.uk. Dennis Lwamafa, National Disease Control, Ministry of Health, Kampala, Uganda, E-mail: lwamafa@yahoo.co.uk. Frank Walsh, Entomology, Lythan St. Anne's, Lancashire, UK, E-mail: frank@walsh.me.uk. Thomas R. Unnasch, Global Health, University of South Florida, Tampa, FL, E-mail: tunnasch@health.usf.edu.

  • 1.

    Enk CD, Gardlo K, Ruzicka T, BenEzra D, 2003. Onchocerciasis. Hautarzt 54: 513–517.

  • 2.

    Taylor HR, Pacque M, Munoz B, Greene BM, 1990. Impact of mass treatment of onchocerciasis with ivermectin on the transmission of infection. Science 250: 116–118.

  • 3.

    Borsboom GJ, Boatin BA, Nagelkerke NJ, Agoua H, Akpoboua KL, Alley EW, Bissan Y, Renz A, Yameogo L, Remme JH, Habbema JD, 2003. Impact of vermectin on onchocerciasis transmission: assessing the empirical evidence that repeated ivermectin mass treatments may lead to elimination/eradication in West-Africa. Filaria J 2: 8.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    World Health Organisation, 1991. Report of the World Health Organization: Strategies for Ivermectin Distribution through Primary Health Care System. Geneva: World Health Organization.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Noma M, Nwoke BE, Nutall I, Tambala PA, Enyong P, Namsenmo A, Remme J, Amazigo UV, Kale OO, Sékétéli A, 2002. Rapid epidemiological mapping of onchocerciasis (REMO): its application by the African Programme for Onchocerciasis Control (APOC). Ann Trop Med Parasitol 96 (Suppl 1): S29–S39.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Katabarwa M, Eyamba A, Habomugisha P, Lakwo T, Ekobo S, Kamgno J, Kuete T, Ndyomugyenyi R, Onapa A, Salifou M, Ntep M, Richards FO, 2008. After a decade of annual dose mass ivermectin treatment in Cameroon and Uganda, onchocerciasis transmission continues. Trop Med Int Health 13: 1196–1203.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Amazigo UV, Brieger WR, Katabarwa M, Akogun O, Ntep M, Boatin B, N'Doyo J, Noma M, Sékétéli A, 2002. The challenges of community-directed treatment with ivermectin (CDTI) within the African Programme for Onchocerciasis Control (APOC). Ann Trop Med Parasitol 96 (Suppl 1): S41–S58.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Sékétéli A, Adeoye G, Eyamba A, Nnoruka E, Drameh P, Amazigo UV, Noma M, Agboton F, Aholou Y, Kale OO, Dadzie KY, 2002. The achievements and challenges of the African Programme for Onchocerciasis Control (APOC). Ann Trop Med Parasitol 96 (Suppl 1): S15–S28.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Brieger WR, Okeibunor JC, Abiose AO, Ndyomugyenyi R, Kisoka W, Wanji S, Elhassan E, Amazigo UV, 2007. Feasibility of measuring compliance to annual ivermectin treatment in the African Programme for Onchocerciasis Control. Trop Med Int Health 12: 260–268.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Diawara L, Traoré MO, Badji A, Bissan Y, Doumbia K, Goita SF, Konaté L, Mounkoro K, Sarr MD, Seck AF, Toé L, Tourée S, Remme JH, 2009. Feasibility of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: first evidence from studies in Mali and Senegal. PLoS Negl Trop Dis 3: e497.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Katabarwa MN, Eyamba A, Nwane P, Enyong P, Yaya S, Baldiagaï J, Madi TK, Yougouda A, Andze GO, Richards FO, 2011. Seventeen years of annual distribution of ivermectin has not interrupted onchocerciasis transmission in North Region, Cameroon. Am J Trop Med Hyg 85: 1041–1049.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Nelson GS, 1958. Onchocerciasis in the West Nile District of Uganda. Trans R Soc Trop Med Hyg 52: 368–376.

  • 13.

    Hopkins DR, Richards FO, Katabarwa M, 2005. Whither onchocerciasis control in Africa. Am J Trop Med Hyg 72: 1–2.

  • 14.

    Katabarwa M, Onapa AW, Nakileza B, 1999. Rapid epidemiological mapping of onchocerciasis in areas of Uganda where Simulium neavei is the vector. East Afr Med J 76: 440–446.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Albiez EJ, Buttner DW, Duke BO, 1988. Diagnosis and extirpation of nodules in human onchocerciasis. Trop Med Parasitol 39 (Suppl 4): 331–346.

  • 16.

    Ngoumou P, Walsh JF, Mace JM, 1994. A rapid mapping technique for the prevalence and distribution of onchocerciasis: a Cameroon case study. Ann Trop Med Parasitol 88: 463–474.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Prost A, Prod’hon J, 1978. Le diagnostique parasitologique de l’onchocercose. Revue critique des methods en usage. Medicine Tropicale 38: 519–532.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Schulz-Key H, 1978. A simple technique to assess the total number of Onchocerca volvulus microfilariae in skin snips. Tropenmed Parasitol 29: 51–54.

  • 19.

    World Health Organization, 1995. Onchocerciasis and Its Control. Report of a WHO Expert Committee on Onchocerciasis Control. Technical Report Series 852. Geneva: World Health Organization.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Garms R, Lakwo TL, Ndyomugyenyi R, Kipp W, Rubaale T, Tukesiga E, Katamanywa J, Post RJ, Amazigo UV, 2009. The elimination of the vector Simulium neavei from the Itwara onchocerciasis focus in Uganda by ground larviciding. Acta Trop 111: 203–210.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Garms R, Cheke RA, 1985. Infections with Onchocerca volvulus in different members of the Simulium damnosum complex in Togo and Benin. Zeitschrift für Angewandte Zoologie 72: 479–495.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Jacobi CA, Enyong P, Renz A, 2010. Individual exposure to Simulium bites and intensity of Onchocerca volvulus infection. Parasit Vectors 3: 53.

  • 23.

    Toé L, Back C, Adjami AG, Tang JM, Unnasch TR, 1997. Onchocerca volvulus: comparison of field collection methods for the preservation of parasite and vector samples for PCR analysis. Bull World Health Organ 75: 443–447.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Yamèogo L, Toè L, Hougard JM, Boatin BA, Unnasch TR, 1999. Pool screen polymerase chain reaction for estimating the prevalence of Onchocerca volvulus infection in Simulium damnosum sensu lato: results of a field trial in an area subject to successful vector control. Am J Trop Med Hyg 60: 124–128.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Rodríguez-Pérez MA, Danis-Lozano R, Rodríguez MH, Unnasch TR, Bradley JE, 1999. Detection of Onchocerca volvulus infection in Simulium ochraceum sensu lato: comparison of a PCR assay and fly dissection in a Mexican hypoendemic community. Parasitology 119: 613–619.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Richards FO Jr, Miri ES, Katabarwa M, Eyamba A, Sauerbrey M, Zea-Flores G, Korve K, Mathai W, Homeida MA, Mueller I, Hilyer E, Hopkins DR, 2001. The Carter Center's assistance to river blindness control programs: establishing treatment objectives and goals for monitoring ivermectin delivery systems on two continents. Am J Trop Med Hyg 65: 108–114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Katholi CR, Toe L, Merriweather A, Unnasch TR, 1995. Determining the prevalence of Onchocerca volvulus infection in vector populations by polymerase chain reaction screening of pools of black flies. J Infect Dis 172: 1414–1417.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Bottomley C, Isham V, Collins RC, Basáñez MG, 2008. Rates of microfilarial production by Onchocerca volvulus are not cumulatively reduced by multiple ivermectin treatments. Parasitology 135: 1571–1581.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Raybould JN, White GB, 1979. The distribution, bionomics and control of onchocerciasis vectors (Diptera: Simuliidae) in Eastern Africa and the Yemen. Tropenmed Parasitol 30: 505–547.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Katabarwa MN, Walsh F, Habomugisha P, Lakwo TL, Agunyo S, Oguttu DW, Unnasch TR, Unoba D, Byamukama E, Tukesiga E, Ndyomugyenyi R, Richards FO, 2012. Transmission of onchocerciasis in Wadelai focus of northwestern Uganda has been interrupted and the disease eliminated. J Parasitol Res 2012: 748540. doi:10.1155/2012/748540 [Epub 2012 Aug 26].

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Boatin BA, Toé L, Alley ES, Nagelkerke NJ, Borsboom G, Habbema JD, 2002. Detection of Onchocerca volvulus infection in low prevalence areas: a comparison of three diagnostic methods. Parasitology 125: 545–552.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Duerr HP, Eichner M, 2010. Epidemiology and control of onchocerciasis: the threshold biting rate of savannah onchocerciasis in Africa. Int J Parasitol 40: 641–650.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    World Health Organization, 2001. Certification of elimination of human onchocerciasis: criteria and procedures. Criteria for Certification of Interruption of Transmission/Elimination of Human Onchocerciasis. Geneva: World Health Organization.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Fischer P, Yocha J, Rubaale T, Garms R, 1997. PCR and DNA hybridization indicate the absence of animal filariae from vectors of Onchocerca volvulus in Uganda. J Parasitol 83: 1030–1034.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Unnasch TR, Meredith SEO, 1996. The use of degenerate primers in conjunction with strain and species oligonucleotides to classify Onchocerca volvulus. Clapp JP, ed. Species Diagnostic Protocols: PCR and Other Nucleic Acid Methods. Totowa, NJ: Humana Press, 293–303.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Fischer P, Rubaale T, Meredith SEO, Büttner DW, 1996. Sensitivity of a polymerase chain reaction-based assay to detect Onchocerca volvulus DNA in skin biopsies. Parasitol Res 82: 395–401.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Osei-Atweneboana MY, Eng JK, Boakye DA, Gyapong JO, Prichard RK, 2007. Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: a two-phase epidemiological study. Lancet 369: 2021–2029.

    • PubMed
    • Search Google Scholar
    • Export Citation
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