• 1.

    Prost A, 1986. The burden of blindness in adult males in the savanna villages of West Africa exposed to onchocerciasis. Trans R Soc Trop Med Hyg 80: 525527.

    • Search Google Scholar
    • Export Citation
  • 2.

    World Health Organization Expert Committee, 1995. Onchocerciasis and Its Control. Report no. 852. Geneva, Switzerland: World Health Organization.

  • 3.

    Murdoch ME, Asuzu MC, Hagan M, Makunde WH, Ngoumou P, Ogbuagu KF, Okello D, Ozoh G, Remme J, 2002. Onchocerciasis: the clinical and epidemiological burden of skin disease in Africa. Ann Trop Med Parasitol 96: 283296.

    • Search Google Scholar
    • Export Citation
  • 4.

    Mathers CD, Ezzati M, Lopez AD, 2007. Measuring the burden of neglected tropical diseases: the global burden of disease framework. PLoS Negl Trop Dis 1: e114.

    • Search Google Scholar
    • Export Citation
  • 5.

    Sauerbrey M, 2008. The Onchocerciasis Elimination Program for the Americas (OEPA). Ann Trop Med Parasitol 102 (Suppl 1 ):2529.

  • 6.

    Greene BM et al.., 1985. Comparison of ivermectin and diethylcarbamazine in the treatment of onchocerciasis. N Engl J Med 313: 133138.

  • 7.

    White AT, Newland HS, Taylor HR, Erttmann KD, Keyvan-Larijani E, Nara A, Aziz MA, D’Anna SA, Williams PN, Greene BM, 1987. Controlled trail and dose finding study of ivermectin for the treatment of onchocerciasis. J Infect Dis 156: 463470.

    • Search Google Scholar
    • Export Citation
  • 8.

    Remme J, Baker RHA, DeSole G, Dadzie KY, Walsh JF, Adams MA, Alley ES, Avissey HSK, 1989. A community trial of ivermectin in the onchocerciasis focus of Asubende, Ghana. I. Effect on the microfilarial reservoir and the transmission of Onchocerca volvulus. Tropenmed Parasitol 40: 367374.

    • Search Google Scholar
    • Export Citation
  • 9.

    Cupp EW, Bernardo MJ, Kiszewski AE, Collins RC, Taylor HR, Aziz MA, Greene BM, 1986. The effects of ivermectin on transmission of Onchocerca volvulus. Science 231: 740742.

    • Search Google Scholar
    • Export Citation
  • 10.

    Cupp EW, Ochoa AO, Collins RC, Ramberg FR, Zea G, 1989. The effect of multiple ivermectin treatments on infection of Simulium ochraceum with Onchocerca volvulus. Am J Trop Med Hyg 40: 501506.

    • Search Google Scholar
    • Export Citation
  • 11.

    Trpis M, Childs JE, Fryauff DJ, Greene BM, Williams PN, Munoz BE, Pacque MC, Taylor HR, 1990. Effect of mass treatment of a human population with ivermectin on transmission of Onchocerca volvulus by Simulium yahense in Liberia, West Africa. Am J Trop Med Hyg 42: 148156.

    • Search Google Scholar
    • Export Citation
  • 12.

    Colatrella B, 2008. The Mectizan Donation Program: 20 years of successful collaboration: a retrospective. Ann Trop Med Parasitol 102 (Suppl 1 ):711.

    • Search Google Scholar
    • Export Citation
  • 13.

    Carter TC, 2015. Onchocerciasis Elimination Program for the Americas. Available at: http://www.cartercenter.org/health/river_blindness/oepa.html. Accessed May 7, 2015.

  • 14.

    Diawara L et al.., 2009. Feasibility of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: first evidence from studies in Mali and Senegal. PLOS Neg Tropl Dis 3: e497.

    • Search Google Scholar
    • Export Citation
  • 15.

    Zarroug IM et al.., 2016. The first confirmed elimination of an onchocerciasis focus in Africa: Abu Hamed, Sudan. Am J Trop Med Hyg 27: 10371040.

    • Search Google Scholar
    • Export Citation
  • 16.

    Lakwo TL et al.., 2013. The disappearance of onchocerciasis from the Itwara focus, western Uganda after elimination of the vector Simulium neavei and 19 years of annual ivermectin treatments. Acta Trop 126: 218221.

    • Search Google Scholar
    • Export Citation
  • 17.

    Katabarwa M et al.., 2014. Transmission of Onchocerca volvulus by Simulium neavei in Mount Elgon focus of eastern Uganda has been interrupted. Am J Trop Med Hyg 90: 11591166.

    • Search Google Scholar
    • Export Citation
  • 18.

    Lakwo TL et al.., 2015. Successful interruption of the transmission of Onchocerca volvulus in Mpamba-Nkusi focus, Kibaale District, mid-western Uganda. East Afr Med J 92: 401407.

    • Search Google Scholar
    • Export Citation
  • 19.

    Katabarwa MN et al.., 2016. The imaramagambo onchocerciasis focus in southwestern Uganda: interruption of transmission after disappearance of the vector Simulium neavei and its associated freshwater crabs. Am J Trop Med Hyg 95: 417425.

    • Search Google Scholar
    • Export Citation
  • 20.

    Lakwo T et al.., 2017. Interruption of the transmission of Onchocerca volvulus in the Kashoya-Kitomi focus, western Uganda by long-term ivermectin treatment and elimination of the vector Simulium neavei by larviciding. Acta Trop 167: 128136.

    • Search Google Scholar
    • Export Citation
  • 21.

    World Health Organization, 2016. Guidelines for Stopping Mass Drug Administration and Verifying Elimination of Human Onchocerciasis: Criteria and Procedures. Document no. WHO/HTM/NTD/PCT/2016.1. Geneva, Switzerland: WHO.

  • 22.

    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: 14141417.

    • Search Google Scholar
    • Export Citation
  • 23.

    Gopal H, Hassan HK, Rodríguez-Pérez MA, Toé LD, Lustigman S, Unnasch TR, 2012. Oligonucleotide based magnetic bead capture of Onchocerca volvulus DNA for PCR pool screening of vector black flies. PLOS Neg Trop Dis 6: e1712.

    • Search Google Scholar
    • Export Citation
  • 24.

    Walsh JF, Davies JB, LeBerre R, Garms R, 1978. Standardization of criteria for assessing the effects of Simulium control in onchocerciasis control programmes. Trans R Soc Trop Med Hyg 72: 675676.

    • Search Google Scholar
    • Export Citation
  • 25.

    Davies JB, Seketeli A, Walsh JF, Barro T, Sawadogo R, 1981. Studies on biting Simulium damnosum s.l. at a breeding site in the Onchocerciasis Control Programme area during and after an interruption of insecticidal treatments. Tropenmed Parasitol 32: 1724.

    • Search Google Scholar
    • Export Citation
  • 26.

    Porter CH, Collins RC, 1988. Seasonality of adult black flies and Onchocerca volvulus transmission in Guatemala. Am J Trop Med Hyg 38: 153167.

    • Search Google Scholar
    • Export Citation
  • 27.

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

  • 28.

    Cupp EW, Sauerbrey M, Richards F, 2011. Elimination of human onchocerciasis: history of progress and current feasibility using ivermectin (Mectizan®) monotherapy. Acta Trop 120 (Suppl 1 ):S100S108.

    • Search Google Scholar
    • Export Citation
  • 29.

    Rodríguez-Pérez MA et al.., 2013. Development of a novel trap for the collection of black flies of the Simulium ochraceum complex. PLoS One 8: e76814.

    • Search Google Scholar
    • Export Citation
  • 30.

    Toé LD et al.., 2014. Optimization of the Esperanza Window Trap for the collection of the African onchocerciasis vector Simulium damnosum sensu lato. Acta Trop 137: 3943.

    • Search Google Scholar
    • Export Citation
  • 31.

    Rodríguez-Pérez MA, Adeleke MA, Rodríguez-Luna IC, Cupp EW, Unnasch TR, 2014. Evaluation of a community-based trapping program to collect Simulium ochraceum sensu lato for verification of onchocerciasis elimination. PLOS Neg Trop Dis 8: e3249.

    • Search Google Scholar
    • Export Citation
  • 32.

    Vajime C, Quillevere D, 1978. The distribution of the Simulium damnosum complex in West Africa with particular reference to the onchocerciasis control programme area. Tropenmed Parasitol 29: 473481.

    • Search Google Scholar
    • Export Citation
  • 33.

    Jacob BG, Novak RJ, Toe L, Sanfo M, Griffith DA, Lakwo TL, Habomugisha P, Katabarwa MN, Unnasch TR, 2013. Validation of a remote sensing model to identify Simulium damnosum s.l. breeding sites in sub-Saharan Africa. PLOS Neg Trop Dis 7: e2342.

    • Search Google Scholar
    • Export Citation
  • 34.

    Young RM et al.., 2015. Identification of human semiochemicals attractive to the major vectors of onchocerciasis. PLOS Neg Trop Dis 9: e3450.

  • 35.

    Raybould JN, White GB, 1979. The distribution, bionomics and control of onchocerciasis vectors (Diptera: Simuliidae) in eastern Africa and the Yemen. Tropenmed Parasitol 30: 505547.

    • Search Google Scholar
    • Export Citation
  • 36.

    Ndyomugyenyi R, 1998. The burden of onchocerciasis in Uganda. Ann Trop Med Parasitol 92 (Suppl 1 ):S133S137.

  • 37.

    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: 203210.

    • Search Google Scholar
    • Export Citation
  • 38.

    Katabarwa M et al.., 2012. Transmission of onchocerciasis in Wadelai focus of northwestern Uganda has been interrupted and the disease eliminated. J Parasitol Res 2012: 748540.

    • Search Google Scholar
    • Export Citation
  • 39.

    Basanez MG, Collins RC, Porter CH, Little MP, Brandling-Bennett D, 2002. Transmission intensity and the patterns of Onchocerca volvulus infection in human communities. Am J Trop Med Hyg 67: 669679.

    • Search Google Scholar
    • Export Citation
  • 40.

    Lamberton PH et al.., 2015. Onchocerciasis transmission in Ghana: persistence under different control strategies and the role of the simuliid vectors. PLoS Negl Trop Dis 9: e0003688.

    • Search Google Scholar
    • Export Citation
  • 41.

    Basanez MG, Walker M, Turner HC, Coffeng LE, de Vlas SJ, Stolk WA, 2016. River blindness: mathematical models for control and elimination. Adv Parasitol 94: 247341.

    • Search Google Scholar
    • Export Citation
  • 42.

    AG B, 2016. BG Sweetscent Saftey Data Sheet. Regensburg, Germany: Biogents AG.

  • 43.

    Mukabana WR, Takken W, Coe R, Knols BG, 2002. Host-specific cues cause differential attractiveness of Kenyan men to the African malaria vector Anopheles gambiae. Malar J 1: 17.

    • Search Google Scholar
    • Export Citation
  • 44.

    Mukabana WR, Takken W, Killeen GF, Knols BG, 2004. Allomonal effect of breath contributes to differential attractiveness of humans to the African malaria vector Anopheles gambiae. Malar J 3: 1.

    • Search Google Scholar
    • Export Citation
  • 45.

    Higazi TB, Boakye DA, Wilson MD, Mahmoud BM, Baraka OZ, Mukhtar MM, Unnasch TR, 2000. Cytotaxonomic and molecular analysis of Simulium (Edwardsellum) damnosum Theobald sensu lato from Abu Hamed, Sudan. J Med Entomol 37: 547553.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 
 
 

 

 

 

 

 

 

Evaluation of Community-Directed Operation of Black Fly Traps for Entomological Surveillance of Onchocerca volvulus Transmission in the Madi-Mid North Focus of Onchocerciasis in Northern Uganda

View More View Less
  • 1 Nwoya District Local Government, Nwoya, Uganda;
  • | 2 Department of Biostatistics, School of Public Health, University of Alabama at Birmingham, Birmingham, Alabama;
  • | 3 Vector Control Division, Ministry of Health, Kampala, Uganda;
  • | 4 The Carter Center, Uganda Office, Kampala, Uganda;
  • | 5 Global Health Infectious Disease Research, College of Public Health, University of South Florida, Tampa, Florida

Entomological measures of transmission are important metrics specified by the World Health Organization to document the suppression and interruption of transmission of Onchocerca volvulus, the causative agent of onchocerciasis. These metrics require testing of large numbers of vector black flies. Black fly collection has relied on human landing collections, which are inefficient and potentially hazardous. As the focus of the international community has shifted from onchocerciasis control to elimination, replacement of human landing collections has become a priority. The Esperanza window trap (EWT) has shown promise as an alternative method for collection of Simulium damnosum s.l., the primary vector of O. volvulus in Africa. Here, we report the results of a community-based trial of the EWT in northern Uganda. Traps operated by residents were compared with human landing collections in two communities over 5 months. Three traps, when operated by a single village resident, collected over four times as many S. damnosum as did the two-men collection team. No significant differences were noted among the bait formulations. The results suggest that EWTs may be effectively operated by community residents and that the trap represents a viable alternative to human landing collections for entomological surveillance of O. volvulus transmission.

Author Notes

Address correspondence to Thomas R. Unnasch, Global Health Infectious Disease Research Program, 3720 Spectrum Boulevard, Tampa, FL 33620. E-mail tunnasch@health.usf.edu

Financial support: This work was supported by grants from the Task Force for Global Health and the National Institute of Allergy and Infectious Diseases (Project no. 1R01AI123245) to Thomson Lakwo and Thomas R. Unnasch.

Authors’ addresses: Denis Loum, Nwoya District Local Government Health Department, Gulu, Uganda, E-mail: loumdenis2@gmail.com. Charles R. Katholi, Department of Biostatistics, School of Public Health, University of Alabama at Birmingham, Birmingham, AL, E-mail: ckatholi@uab.edu. Thomson Lakwo and Edridah M. Tukahebwa, Vector Control Division, Ministry of Health, Kampala, Uganda, E-mails: tlakwo@gmail.com and edmuheki@gmail.com. Peace Habomugisha, The Carter Center, Uganda Office, Kampala, Uganda, E-mail: peace.habomugisha@cartercenter.org. Thomas R. Unnasch, Global Health Infectious Disease Program, Tampa, FL, E-mail: tunnasch@health.usf.edu.

Save