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Blackfly Ecology and Onchocerca Volvulus Transmission in Three Formerly Hyperendemic Foci in Uganda, Tanzania and Cameroon

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Blackfly Ecology and Onchocerca Volvulus Transmission in Three Formerly Hyperendemic Foci in Uganda, Tanzania and Cameroon Blackfly ecology and Blackfly ecology andOnchocerca volvulus transmission in three formerly hyperendemic foci in Uganda, Tanzania and Cameroon Onchocerca volvulus Thesis for the degree of Doctor in Biomedical Sciences at the University of Antwerp, to be defended by transmission in three formerly hyperendemic foci in Uganda, Tanzania and Cameroon transmission in three formerly hyperendemic foci Uganda, Tanzania Adam Hendy Adam Hendy Supervisors Prof. Dr. Jean-Claude Dujardin Prof. Dr. Dirk Berkvens Faculty of Pharmaceutical, Biomedical and Veterinary Sciences Department of Biomedical Sciences Antwerp 2018 Faculty of Pharmaceutical, Biomedical and Veterinary Sciences Department of Biomedical Sciences Blackfly ecology and Onchocerca volvulus transmission in three formerly hyperendemic foci in Uganda, Tanzania and Cameroon Kriebelmug ecologie en Onchocerca volvulus transmissie in drie voorheen hyperendemische gebieden in Oeganda, Tanzania en Kameroen Thesis for the degree of Doctor in Biomedical Sciences at the University of Antwerp, to be defended by Adam Hendy Promotors: Prof. Dr. Jean-Claude Dujardin Prof. Dr. Dirk Berkvens Antwerp, 2018 Doctoral committee Promotors Prof. Dr. Jean-Claude Dujardin University of Antwerp; Institute of Tropical Medicine, Antwerp Prof. Dr. Dirk Berkvens Institute of Tropical Medicine, Antwerp Chair Prof. Dr. Louis Maes University of Antwerp Members Prof. Dr. Guy Caljon University of Antwerp Prof. Dr. Herwig Leirs University of Antwerp External jury members Prof. Dr. Thomas Unnasch University of South Florida Prof. Dr. Lisette van Lieshout Leiden University Medical Center Cover picture – Mahenge resident, accompanying research-team, taking an interest in immature blackfly stages present on decaying vegetation in a local river. Photograph by Adam Hendy, Tanzania, 2015. The research described in this thesis was primarily funded by an Institute of Tropical Medicine, Antwerp, and Flemish Interuniversity Council South Initiative (VLIR-UOS) "Structural Research Funding" (SOFI) grant. 2 Table of Contents Summary 5 List of acronyms 9 Chapter 1. Introduction 11 Chapter 2. Esperanza Window Traps for the collection of anthropophilic 49 blackflies (Diptera: Simuliidae) in Uganda and Tanzania Chapter 3. Transmission of Onchocerca spp. by human and cattle biting 79 blackflies in northern Uganda Chapter 4. The blackfly vectors and transmission of Onchocerca volvulus in 107 Mahenge, south eastern Tanzania Chapter 5. Onchocerca volvulus transmission in Région du Centre, Cameroon, 131 following 16 years of annual CDTI Chapter 6. Discussion 157 Supplementary information 168 Curriculum vitae 174 Acknowledgements 177 3 4 Summary Human onchocerciasis or ‘river blindness’ is a chronic and debilitating disease caused by repeated infection with Onchocerca volvulus, a parasitic filarial worm transmitted blackflies (Diptera: Simuliidae). Around 99% of an estimated 25.7 million infections occur in sub- Saharan Africa. Current interventions mainly rely on mass drug administration through annual community directed treatment with ivermectin (CDTI) to control the disease. The drug only temporarily sterilises adult parasites and must therefore be taken for the reproductive lifespan of the worms (12 - 15 years) in order to suppress transmission. The World Health Organization (WHO) currently aims to eliminate onchocerciasis by 2025, but it is not known whether this can be achieved through annual CDTI alone. This thesis aimed to provide a detailed study of the blackfly vectors and O. volvulus transmission in three formerly hyperendemic foci in Uganda, Tanzania and Cameroon, under long-term control either with annual CDTI, or vector control in combination with biannual CDTI. An evaluation of Esperanza Window Traps (EWTs) for the collection of human biting (anthropophilic) blackflies was conducted in Uganda and Tanzania (Chapter 2). Blackfly collections are necessary to evaluate the progress of CDTI-based programmes towards eliminating the disease, but current methods rely on the use of human bait which presents ethical problems due to risk of exposure to vector-borne pathogens. Results showed that EWTs collected numbers of Simulium damnosum s.l. (the main vector of O. volvulus in sub- Saharan Africa) comparable with vector collectors in northern Uganda, but performed poorly in Tanzania. Breeding site surveys and adult blackfly collections were also carried out in all three study countries between 2014 and 2017 (Chapters 3 – 5). Anthropophilic Simulium damnosum s.str. and Simulium bovis were collected in low numbers in northern Uganda where onchocerciasis control through biannual CDTI and vector control has been taking place since 2012. Onchocerca volvulus was not detected in any of the human biting S. damnosum s.l. (133 flies) or S. bovis (602 flies) screened for infection, although the bovine parasites Onchocerca ochengi and Onchocerca sp. ‘Siisa’ were present. Anthropophilic blackflies collected in Tanzania included ‘Nkusi J’ and Simulium kilibanum cytoforms of the S. damnosum complex, and also Simulium nyasalandicum. ‘Nkusi J’ appeared to be the predominant cytoform, and out of 12,452 S. damnosum s.l. pool screened, an estimated 0.57% (95% CI 0.43% – 0.74%) carried infective L3 stage O. volvulus larvae. Infection rates in blackflies appeared similar to pre-control levels, despite annual CDTI commencing in 1997. In Cameroon, a new chromosomal variant of Simulium squamosum E was found breeding along the lower Mbam River. Despite CDTI having taken place annually since 2000, 5 dissection of 9,281 out of 93,563 blackflies collected on human bait showed that high rates of O. volvulus transmission were still occurring at riverside sites. Whereas blackfly collections in northern Uganda were insufficient to demonstrate interruption of O. volvulus transmission according to WHO guidelines, the results are encouraging for the use of integrated approaches to control onchocerciasis. In Tanzania and Cameroon, where control has relied upon CDTI alone, O. volvulus transmission is continuing at unacceptable levels despite >15 years of annual ivermectin treatment. 6 Samenvatting Onchocerciasis of rivierblindheid is een chronisch slopende ziekte veroorzaakt door infecties met de parasitaire nematode, Onchocerca volvulus, overgedragen door kriebelmuggen (Diptera: Simuliidae). Het merendeel (99%) van de geschatte 25.7 miljoen infecties vinden plaats in sub-Saharische landen in Afrika. Controle van deze ziekte verloopt momenteel via jaarlijks georganiseerde behandelingen met ivermectin (community directed treatment with ivermectin, CDTI), een geneesmiddel dat door sterilisatie van de volwassen worm de voortplanting tegengaat. Deze onderbreking van de transmissie is echter tijdelijk en het medicijn moet genomen worden gedurende de volledige reproductieve levensduur van de wormen (12-15 jaar). De Wereldgezondheidsorganisatie (WHO) streeft momenteel naar het elimineren van onchocerciasis tegen 2025. Het blijft nog de vraag of dit zal bereikt worden met de jaarlijkse toedieningen via CDTI. Dit proefschrift heeft tot doel een gedetailleerde studie weer te geven van zowel de vectoren, Simuliidae, als de transmissie van O. volvulus in drie voormalig hyper endemische gebieden die reeds onder langdurige controle staan door jaarlijkse toedieningen van ivermectin of tweejaarlijkse toedieningen van het geneesmiddel in combinatie met vectorbestrijding. In Uganda en Tanzania werden Esperanza Window Traps (EWTs) geëvalueerd voor het verzamelen van bijtende, antropofiele kriebelmuggen (Hoofdstuk 2). Deze collecties zijn nodig om de progressie na te gaan van het ingrijpen via CDTI, gericht op de eliminatie van de Simuliidae. Momenteel wordt nog steeds menselijk lokaas gebruikt (vrijwilligers), met alle ethische implicaties tot gevolg. Resultaten tonen aan dat de aantallen van Simulium damnosum s.l. (de belangrijkste vector van O. volvulus), gecollecteerd met de EWTs, vergelijkbaar zijn met de vectorcollecties op vrijwilligers in het noord Uganda, maar dat resultaat is echter niet waarneembaar in Tanzania. Tussen 2014 en 2017 werden drie landen opgenomen in de studiegroep voor onderzoek van broedplaatsen en collecties van volwassen Simuliidae: Uganda (Mid North; Hoofdstuk 3), zuidoost Tanzania (Mahenge; Hoofdstuk 4) en centraal Kameroen (Bafia Health District; Hoofdstuk 5). Mensen bijtende Simulium damnosum s.str. en de dierlijke variant Simulium bovis werden in kleine aantallen gevangen in noord Uganda, waar onchocerciasis onder controle wordt gehouden door tweejaarlijkse toediening van CDTI én vector controle plaatsvindt sinds 2012. Onchocerca volvulus werd bovendien niet aangetroffen in de antropofiele S. damnosum s.l. (133 exemplaren) of de zoöfiele S. bovis (602 exemplaren). Na screening voor andere infecties werden echter wel runderparasieten Onchocerca ochengi en Onchocerca sp. ‘Siisa’ aangetroffen. Antropofiele kriebelmuggen verzameld in Tanzania bevatten 'Nkusi J' en Simulium kilibanum cytovormen van het S. damnosum complex, evenals Simulium 7 nyasalandicum. 'Nkusi J' bleek de overheersende cytovorm te zijn. Uit een pool van 12.452 S. damnosum s.l. screenings, bevatte een geschatte 0,57% (95% CI 0,43% - 0,74%) de infectueuze L3-fase van de O. volvulus larven. De infectie graden blijken hiermee vergelijkbaar met de niveaus vóór de bestrijding, en dit ondanks de jaarlijkse toedieningen via CDTI, reeds gestart in 1997. In Kameroen werd een nieuwe chromosomale variant van Simulium squamosum E aangetroffen op een broedplaats langs het lagere gelegen deel van de
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