Serosurveillance to Monitor Onchocerciasis Elimination: The Ugandan Experience

David Oguttu Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by David Oguttu in
Current site
Google Scholar
PubMed
Close
,
Edson Byamukama Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Edson Byamukama in
Current site
Google Scholar
PubMed
Close
,
Charles R. Katholi Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Charles R. Katholi in
Current site
Google Scholar
PubMed
Close
,
Peace Habomugisha Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Peace Habomugisha in
Current site
Google Scholar
PubMed
Close
,
Christine Nahabwe Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Christine Nahabwe in
Current site
Google Scholar
PubMed
Close
,
Monica Ngabirano Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Monica Ngabirano in
Current site
Google Scholar
PubMed
Close
,
Hassan K. Hassan Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Hassan K. Hassan in
Current site
Google Scholar
PubMed
Close
,
Thomson Lakwo Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Thomson Lakwo in
Current site
Google Scholar
PubMed
Close
,
Moses Katabarwa Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Moses Katabarwa in
Current site
Google Scholar
PubMed
Close
,
Frank O. Richards Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Frank O. Richards in
Current site
Google Scholar
PubMed
Close
, and
Thomas R. Unnasch Vector Control Division, Ministry of Health, Kampala, Uganda; The Carter Center, Kampala, Uganda; Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama; Department of Global Health, University of South Florida, Tampa, Florida; The Carter Center, Atlanta, Georgia

Search for other papers by Thomas R. Unnasch in
Current site
Google Scholar
PubMed
Close
Restricted access

Uganda is the only African country whose onchocerciasis elimination program uses a two-pronged approach of vector control and mass drug distribution. The Ugandan program relies heavily upon the use of serosurveys of children to monitor progress toward elimination. The program has tested over 39,000 individuals from 11 foci for Onchocerca volvulus exposure, using the Ov16 ELISA test. The data show that the Ov16 ELISA is a useful operational tool to monitor onchocerciasis transmission interruption in Africa at the World Health Organization (WHO) recommended threshold of < 0.1% in children. The Ugandan experience has also resulted in a re-examination of the statistical methods used to estimate the boundary of the upper 95% confidence interval for the WHO prevalence threshold when all samples tested are negative. This has resulted in the development of Bayesian and hypergeometric statistical methods that reduce the number of individuals who must be tested to meet the WHO criterion.

Author Notes

* Address correspondence to Thomas R. Unnasch, Global Health Infectious Disease Research, Department of Global Health, University of South Florida, 3720 Spectrum Blvd., Suite 304, Tampa, FL 33612. E-mail: tunnasch@health.usf.edu

Financial support: John Moores provided critical financial support for establishing the Uganda onchocerciasis molecular laboratory and launching the 2007 elimination field activities.

Authors' addresses: David Oguttu, Vector Control Division, Ministry of Health, Kampala, Uganda, E-mail: dguttu@gmail.com. Edson Byamukama and Peace Habomugisha, The Carter Center Uganda, Kampala, Uganda, E-mails: edson.navs@gmail.com and provia5@hotmail.com. Charles R. Katholi, Department of Biostatistics, School of Public Health, University of Alabama at Birmingham, Birmingham, AL, E-mail: ckatholi@uab.edu. Christine Nahabwe, Monica Ngabirano, and Thomson Lakwo, Vector Control Division, Ministry of Health, Kampala, Uganda, E-mails: ch.nahabwe@gmail.com, ngabiranomonica@ymail.com, and tlakwo@gmail.com. Hassan K. Hassan and Thomas R. Unnasch, Global Health Infectious Disease Research, Department of Global Health, University of South Florida, Tampa, FL, E-mails: hhassan@health.usf.edu and tunnasch@health.usf.edu. Moses Katabarwa and Frank O. Richards, Emory University and The Carter Center, Atlanta, GA, E-mails: mkataba@emory.edu and frich01@emory.edu.

  • 1.

    Thylefors B, 1978. Ocular Onchocerciasis. Bull World Health Organ 56: 6372.

  • 2.

    African Programme for Onchocerciasis Control, 2005. Final communiqué of the 11th session of the Joint Action Forum (JAF) of APOC, Paris, France, 6–9 December 2005. Ouagadougou, Burkina Faso: APOC.

    • PubMed
    • Export Citation
  • 3.

    Winthrop KL, Furtado JM, Silva JC, Resnikoff S, Lansingh VC, 2011. River blindness: an old disease on the brink of elimination and control. J Glob Infect Dis 3: 151155.

  • 4.

    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.

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

    Dadzie Y, Neira M, Hopkins D, 2003. Final report of the conference on the eradicability of onchocerciasis. Filaria J 2: 2.

  • 6.

    Diawara L, Traore MO, Badji A, Bissan Y, Doumbia K, Goita SF, Konate L, Mounkoro K, Sarr MD, Seck AF, Toe L, Touree 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 Neg Trop Dis 3: e497.

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

    Tekle AH, Elhassan E, Isiyaku S, Amazigo UV, Bush S, Noma M, Cousens S, Abiose A, Remme JH, 2012. Impact of long-term treatment of onchocerciasis with ivermectin in Kaduna State, Nigeria: first evidence of the potential for elimination in the operational area of the African Programme for Onchocerciasis Control. Parasit Vect 5: 28.

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

    Traore MO, Sarr MD, Badji A, Bissan Y, Diawara L, Doumbia K, Goita SF, Konate L, Mounkoro K, Seck AF, Toe L, Toure S, Remme JH, 2012. Proof-of-principle of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: final results of a study in Mali and Senegal. PLOS Neg Trop Dis 6: e1825.

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

    Katabarwa M, Walsh F, Habomugisha P, Lakwo T, Agunyo S, Oguttu D, 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.

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

    Higazi TB, Zarroug IMA, Mohamed HA, ElMubark WA, Deran TC, Aziz N, Katabarwa M, Hassan HK, Unnasch TR, Mackenzie CD, Richards F, Hashim K, 2013. Interruption of onchocerciasis transmission in the Abu Hamed Focus, Sudan. Am J Trop Med Hyg 89: 5157.

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

    African Programme for Onchocerciasis Control, 2009. Informal Consultation on elimination of Onchocerciasis Transmission with Current Tools in Africa “Shrinking the Map.” Ouagadougou, Burkina Faso: African Programme for Onchocerciasis Control.

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

    Mackenzie CD, Homeida MM, Hopkins AD, Lawrence JC, 2012. Elimination of onchocerciasis from Africa: possible? Trends Parasitol 28: 1622.

  • 13.

    World Health Organization, 2001. Criteria for Certification of Interruption of Transmission/Elimination of Human Onchocerciasis. WHO report WHO/CDS/CPE/CEE/2001.18a. Geneva: World Health Organization.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Steel RGD, Torrie JH, Dickey DA, 1997. Principles and Procedures of Statistics: A Biometrical Approach. New York: McGraw-Hill.

  • 15.

    Ndyomugyenyi R, Lakwo T, Habomugisha P, Male B, 2007. Progress towards the elimination of onchocerciasis as a public-health problem in Uganda: opportunities, challenges and the way forward. Ann Trop Med Parasitol 101: 323333.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Kruger A, Nurmi V, Yocha J, Kipp W, Rubaale T, Garms R, 1999. The Simulium damnosum complex in western Uganda and its role as a vector of Onchocerca volvulus. Trop Med Int Health 4: 819826.

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

    Lakwo TL, 2004. Preliminary studies on the biting activity and transmission of Onchocerca volvulus by Simulium neavei (Diptera: Simuliidae) in Kashoya-Kitomi focus, Western Uganda. East Afr Med J 81: 244247.

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

    Brown AW, 1962. A survey of Simulium control in Africa. Bull World Health Organ 27: 511527.

  • 19.

    Walsh JF, 1990. Review of vector control prior to the OCP. Acta Leiden 59: 6178.

  • 20.

    Ndyomugyenyi R, Tukesiga E, Buttner DW, Garms R, 2004. The impact of ivermectin treatment alone and when in parallel with Simulium neavei elimination on onchocerciasis in Uganda. Trop Med Int Health 9: 882886.

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

    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.

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

    Lakwo TL, Garms R, Rubaale T, Katabarwa M, Walsh F, Habomugisha P, Oguttu D, Unnasch T, Namanya H, Tukesiga E, Katamanywa J, Bamuhiiga J, Byamukama E, Agunyo S, Richards F, 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Lindblade KA, Arana B, Zea-Flores G, Rizzo N, Porter CH, Dominguez A, Cruz-Ortiz N, Unnasch TR, Punkosdy GA, Richards J, Sauerbrey M, Castro J, Catu E, Oliva O, Richards FO Jr, 2007. Elimination of Onchocerca volvulus transmission in the Santa Rosa focus of Guatemala. Am J Trop Med Hyg 77: 334341.

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

    Gonzalez RJ, Cruz-Ortiz N, Rizzo N, Richards J, Zea-Flores G, Dominguez A, Sauerbrey M, Catu E, Oliva O, Richards FO, Lindblade KA, 2009. Successful interruption of transmission of Onchocerca volvulus in the Escuintla-Guatemala focus, Guatemala. PLoS Negl Trop Dis 3: e404.

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

    Katholi C, 2010. Poolscreen v2.0. Available at: http://www.soph.uab.edu/bst/poolscreen. Accessed June 14, 2012.

  • 26.

    Hajek J, 1960. Limiting distributions in simple random sampling from a finite population. Publ Math Inst Hung Acad 5: 361374.

  • 27.

    Lehmann EL, 1975. Nonparametrics: Statistical Methods Based on Ranks. Oakland, CA: Holden-Day.

  • 28.

    Agresti A, Coull BA, 1998. Approximation is better than “exact” for interval estimation of binomial proportions. Am Stat 52: 119126.

  • 29.

    Wilson EB, 1927. Probabilistic inference, the law of succession, and statistical inference. J Am Stat Assoc 22: 209212.

  • 30.

    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.

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

    Gu W, Unnasch TR, Katholi CR, Lampman R, Novak RJ, 2008. Fundamental issues in mosquito surveillance for arboviral transmission. Trans R Soc Trop Med Hyg 102: 817822.

  • 32.

    Rodríguez-Pérez MA, Lilley BG, Domínguez-Vázquez A, Segura-Arenas R, Lizarazo-Ortega C, Mendoza-Herrera A, Reyes-Villanueva F, Unnasch TR, 2004. Polymerase chain reaction monitoring of transmission of Onchocerca volvulus in two endemic states in Mexico. Am J Trop Med Hyg 70: 3845.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 600 545 48
Full Text Views 449 20 1
PDF Downloads 131 14 1
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save