Onchocerciasis-Associated Epilepsy with Head Nodding Seizures—Nodding Syndrome: A Case Series of 15 Patients from Western Uganda, 1994

Christoph Kaiser Basic Health Services Kabarole and Bundibugyo Districts, Fort Portal, Uganda; Vector Control Unit, Ministry of Health, Fort Portal, Uganda; Department of Public Health Sciences, University of Alberta, Edmonton, Canada

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George Asaba Basic Health Services Kabarole and Bundibugyo Districts, Fort Portal, Uganda; Vector Control Unit, Ministry of Health, Fort Portal, Uganda; Department of Public Health Sciences, University of Alberta, Edmonton, Canada

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Tom Rubaale Basic Health Services Kabarole and Bundibugyo Districts, Fort Portal, Uganda; Vector Control Unit, Ministry of Health, Fort Portal, Uganda; Department of Public Health Sciences, University of Alberta, Edmonton, Canada

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Ephraim Tukesiga Basic Health Services Kabarole and Bundibugyo Districts, Fort Portal, Uganda; Vector Control Unit, Ministry of Health, Fort Portal, Uganda; Department of Public Health Sciences, University of Alberta, Edmonton, Canada

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Walter Kipp Basic Health Services Kabarole and Bundibugyo Districts, Fort Portal, Uganda; Vector Control Unit, Ministry of Health, Fort Portal, Uganda; Department of Public Health Sciences, University of Alberta, Edmonton, Canada

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Nodding syndrome (NS) is an encephalopathy characterized by the core symptom of epileptic head nodding seizures, affecting children at the age between 3 and 18 years in distinct areas of tropical Africa. A consistent correlation with onchocerciasis was found, but so far, the causation of NS has not been fully clarified. With a systematic analysis of features of a cohort of epilepsy patients examined in the Itwara onchocerciasis focus of western Uganda in 1994, we provide evidence that NS actually occurred in this area at this time, and we demonstrate a correlation between prevalence of NS and that of onchocerciasis in different villages. Following the elimination of onchocerciasis by community-directed treatment with ivermectin and ground larviciding, our data provide a baseline to examine the question whether NS will disappear once its putative cause has been removed.

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Author Notes

Address correspondence to Christoph Kaiser, Practice for Child and Adolescent Health, Balzenbergstr. 73, Baden-Baden 76530, Germany. E-mail: drchkaiser@web.de

Authors’ addresses: Christoph Kaiser, Practice for Child and Adolescent Health, Baden-Baden, Germany, E-mail: drchkaiser@web.de. George Asaba and Tom Rubaale, District Health Department, Kabarole District Local Government, Fort Portal, Uganda, E-mails: asaba_george@yahoo.com and trubaale@gmail.com. Walter Kipp, Department of Public Health Sciences, University of Alberta, Edmonton, Canada, E-mail: walter.kipp@ualberta.ca. Ephraim Tukesiga, Vector Control Unit, Ministry of Health, Fort Portal, Uganda, E-mail: ephraim.tukesiga@gmail.com.

  • 1.

    Ovuga E, Kipp W, Mungherera M, Kasoro S, 1992. Epilepsy and retarded growth in a hyperendemic focus of onchocerciasis in rural western Uganda. East Afr Med J 69: 554556.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Kipp W, Kasoro S, Burnham G, 1994. Onchocerciasis and epilepsy in Uganda. Lancet 343: 183184.

  • 3.

    Kaiser C, Kipp W, Asaba G, Mugisa C, Kabagambe G, Rating D, Leichsenring L, 1996. The prevalence of epilepsy follows the distribution of onchocerciasis in a west Ugandan focus. Bull World Health Organ 74: 361367.

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

    Kaiser C, Benninger C, Asaba G, Mugisa C, Kabagambe G, Kipp W, Rating D, 2000. Clinical and electro-clinical classification of epileptic seizures in west Uganda. Bull Soc Pathol Exot 93: 255259.

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

    Kaiser C, Rubaale T, Tukesiga E, Kipp W, Asaba G, 2015. Case report: nodding syndrome, western Uganda, 1994. Am J Trop Med Hyg 93: 198202.

  • 6.

    Aall-Jilek LM, 1965. Epilepsy in the Wapagoro tribe in Tanganyika. Acta Psychiatr Scand 41: 5786.

  • 7.

    Lacey M, 2003. Nodding disease: mystery of southern Sudan. Lancet Neurol 2: 714.

  • 8.

    Spencer PS et al. 2013. Nodding syndrome in Mundri county, South Sudan: environmental, nutritional and infectious factors. Afr Health Sci 13: 183204.

  • 9.

    Idro R et al. 2014. Nodding syndrome in Ugandan children–clinical features, brain imaging and complications: a case series. BMJ Open 3: e002540.

  • 10.

    Foltz JL et al. 2013. An epidemiologic investigation of potential risk factors for nodding syndrome in Kitgum District, Uganda. PLoS One 8: e66419.

  • 11.

    Van Bemmel K, Derluyn I, Stroeken K, 2014. Nodding syndrome or disease? On the conceptualization of an illness-in-the-making. Ethn Health 19: 100118.

  • 12.

    Winkler AS et al. 2015. The head nodding syndrome—clinical classification and possible causes. Epilepsia 49: 20082015.

  • 13.

    Dowell SF et al. 2013. Nodding syndrome. Emerg Infect Dis 19: 13741384.

  • 14.

    World Health Organisation, 2012. International Scientific Meeting on Nodding Syndrome, Kampala, Uganda. Available at: http://www.who.int/neglected_diseases/diseases/Nodding_syndrom_Kampala_Report_2012.pdf. Accessed April 10, 2018.

    • PubMed
    • Export Citation
  • 15.

    Fischer P, Kipp W, Bamuhiga J, Binta-Kahwa J, Kiefer A, Büttner DW, 1993. Parasitological and clinical characterization of Simulium neavei-transmitted onchocerciasis in western Uganda. Trop Med Parasitol 44: 311321.

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

    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
  • 17.

    Kaiser C, 1998. Introducing Anti-Epileptic Treatment into Primary Health Care: A Case Study in an Area of High Epilepsy Prevalence in Kabarole District, West Uganda. MSc Thesis, Institute of Tropical Hygiene and Public Health, University of Heidelberg, Heidelberg, Germany.

    • PubMed
    • Export Citation
  • 18.

    Kaiser C, Asaba G, Leichsenring M, Kabagambe G, 1998. High incidence of epilepsy related to onchocerciasis in west Uganda. Epilepsy Res 30: 247251.

  • 19.

    Kaiser C, Asaba G, Mugisa C, Kipp W, Kasoro S, Rubaale T, Kabagambe G, 1998. Antiepileptic drug treatment in rural Africa: involving the community. Trop Doct 28: 7377.

  • 20.

    Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL, 2002. 2000 CDC growth charts for the United States: methods and development. Vital Health Stat 11: 1190.

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

    Marshall WA, Tanner JM, 1969. Variations in pattern of pubertal changes in girls. Arch Dis Child 235: 291303.

  • 22.

    Marshall WA, Tanner JM, 1970. Variations in the pattern of pubertal changes in boys. Arch Dis Child 239: 1323.

  • 23.

    Abreu AP, Kaiser UB, 2016. Pubertal development and regulation. Lancet Diabetes Endocrinol 4: 254264.

  • 24.

    Iyengar PJ et al. Centers for Disease Control and Prevention (CDC), 2014. Prevalence of nodding syndrome–Uganda 2012–2013. MMWR Morb Mortal Wkly Rep 63: 603606.

  • 25.

    Schmutzhard E, Winkler AS, 2016. Nodding syndrome–a critical note and a plea to join forces. Trop Med Int Health 20: 201204.

  • 26.

    Burnham G, 2003. The right word. Lancet 361: 456.

  • 27.

    Van Bemmel K, Van der Weegen K, 2017. Universal classifications, national approaches and specific situations: a comparative study on the conceptualization of nodding syndrome in Uganda and Tanzania. Anthropol Med 30: 120.

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

    Jilek WG, Jilek-Aall LM, 1970. The problem of epilepsy in rural Africa: ‘Kifafa’ in a Tanzanian tribe. Transcult Psychiatry 7: 4348.

  • 29.

    Tumwine JK, Vandemaele K, Chungong S, Richer M, Anker M, Ayana Y, Opoka ML, Klaucke DN, Quarello A, Spencer PS, 2012. Clinical and epidemiologic characteristics of nodding syndrome in Mundri county, southern Sudan. Afr Health Sci 12: 242248.

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

    Anonymous, 2009. Nodding Disease or “River Epilepsy.” Integrated Regional Information Network (IRIN), Kitgum. Press release 10 August 2009. Available at: http://www.irinnews.org/report/85646/uganda-nodding-disease-or-river-epilepsy. Accessed April 10, 2018.

    • PubMed
    • Export Citation
  • 31.

    Kitara DL, Oh J, Mwaka AD, 2013. Nodding syndrome in Uganda—a disease cluster: an epidemiological dilemma. Pac J Med Sci 11: 2133.

  • 32.

    Colebunders R et al. 2016. Nodding syndrome and epilepsy in onchocerciasis endemic regions: comparing preliminary observations from South Sudan and the Democratic Republic of the Congo with data from Uganda. BMC Res Notes 9: 182.

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

    Spencer PS et al. other Members of the Oregon-Uganda Nodding Syndrome Research Team, 2016. Environmental, dietary and case-control study of nodding syndrome in Uganda: a post-measles brain disorder triggered by malnutrition? J Neurol Sci 369: 191203.

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

    Mpagi J, Katamanywa J, Garms R, 2001. Dispersal range of Simulium neavei in an onchocerciasis focus of western Uganda. Med Vet Entomol 14: 9599.

  • 35.

    Pion SDS et al. 2009. Epilepsy in onchocerciasis endemic areas: systematic review and meta-analysis of population-based surveys. PLoS Negl Trop Dis 3: e461.

  • 36.

    Levick B et al. 2017. High prevalence of epilepsy in onchocerciasis endemic regions in the Democratic Republic of the Congo. PLoS Negl Trop Dis 11: e0005732.

  • 37.

    Ngugi AK et al. SEEDS Group, 2013. Prevalence of active convulsive epilepsy in sub-Saharan Africa and associated risk factors: cross-sectional and case-control studies. Lancet Neurol 12: 253263.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Boussinesq M, Pion SD, Demanga-Ngangue, Kamgno J, 2002. Relationship between onchocerciasis and epilepsy: a matched case-control study in the Mbam Valley, Republic of Cameroon. Trans R Soc Trop Med Hyg 96: 537541.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Colebunders R et al. 2016. Prevalence of river epilepsy in the Orientale Province in the Democratic Republic of the Congo. PLoS Negl Trop Dis 10: e0004478.

  • 40.

    Kaiser C, Pion SDS, Boussinesq M, 2013. Case-control studies on the relationship between onchocerciasis and epilepsy: systematic review and meta-analysis. PLoS Negl Trop Dis 7: e2147.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    König R et al. 2010. The role of Onchocerca volvulus in the development of epilepsy in a rural area of Tanzania. Parasitology 137: 15591568.

  • 42.

    Sejvar JJ et al. 2013. Clinical, neurological, and electrophysiological features of nodding syndrome in Kitgum, Uganda: an observational case series. Lancet Neurol 12: 166174.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Johnson TP et al. 2017. Nodding syndrome may be an autoimmune reaction to the parasitic worm Onchocerca volvulus. Sci Transl Med 9: eaaf6953.

  • 44.

    Spencer PS, Schmutzhard E, Winkler AS, 2017. Nodding syndrome in the spotlight–placing recent findings in perspective. Trends Parasitol 33: 490492.

  • 45.

    Kakooza-Mwesige A, 2017. Unravelling the mysterious onchocerciasis-nodding syndrome link: new developments and future challenges. Ann Transl Med 5: 486.

  • 46.

    Kaiser C, Pion SDS, 2017. River blindness goes beyond the eye: autoimmune antibodies, cross-reactive with Onchocerca volvulus antigen, detected in brain of patients with nodding syndrome. Ann Transl Med 5: 459.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Kaiser C, Asaba G, Kasoro S, Rubaale T, Kabagambe G, Mbabazi M, 2007. Mortality from epilepsy in an onchocerciasis-endemic area in west Uganda. Trans R Soc Trop Med Hyg 101: 4855.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Kipp W, Burnham G, Bamuhiiga J, Leichsenring M, 1996. The Nakalanga syndrome in Kabarole district, western Uganda. Am J Trop Med Hyg 54: 8083.

  • 49.

    Föger K, Gora-Stahlberg G, Sejvar J, Ovuga E, Jilek-Aall L, Schmutzhard E, Kaiser C, Winkler AS, 2017. Nakalanga syndrome: clinical characteristics, potential causes, and its relationship with recently described nodding syndrome. PLoS Negl Trop Dis 11: e0005201.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Colebunders R, Suykerbuyk P, Jacob ST, van Oijen M, 2017. Nodding syndrome, other forms of epilepsy, and the Nakalanga syndrome most likely directly or indirectly caused by Onchocerca volvulus. J Neurol Sci 372: 439440.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Chesnais CB, Njamnshi AK, Zoung-Kanyi Bissek A-C, Tatah GY, Nana-Djeunga HC, Kamgno J, Colebunders R, Boussinesq M, 2018. First evidence by a cohort study in Cameroon that onchocerciasis does induce epilepsy [Abstract at the first International Workshop on Onchocerciasis-Associated Epilepsy, Antwerp, Belgium, 2017]. Infect Dis Poverty 7: 23. Available at: https://www.uantwerpen.be/en/conferences/oae-2017/. Accessed May 23, 2018.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    Coffeng LE et al. 2013. African programme for onchocerciasis control 1995–2015: model-estimated health impact and cost. PLoS Negl Trop Dis 7: e2032.

  • 53.

    Katabarwa MN et al. 2018. After 70 years of fighting an age-old scourge, onchocerciasis in Uganda, the end is in sight. Int Health 10 (Suppl 1): 7988.

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