Persistent transmission of onchocerciasis in Kwanware-Ottou focus in Wenchi health district, Ghana.


Journal

BMC infectious diseases
ISSN: 1471-2334
Titre abrégé: BMC Infect Dis
Pays: England
ID NLM: 100968551

Informations de publication

Date de publication:
14 Oct 2024
Historique:
received: 02 10 2023
accepted: 09 10 2024
medline: 15 10 2024
pubmed: 15 10 2024
entrez: 14 10 2024
Statut: epublish

Résumé

This study examined onchocerciasis transmission in Kwanware and Ottou in the Wenchi Health District of Ghana, where persistent onchocercal microfilariae (mf) levels have been reported since 2012. This study was conducted from 2019 to 2021 and involved the following: (i) reviewing past records of ivermectin mass drug administration (MDA); (ii) conducting a treatment coverage evaluation survey (CES); (iii) conducting key informant interviews; (iv) prospecting blackfly breeding sites; (v) collecting and dissecting blackflies; and (vi) conducting parasitological and serological surveys. (i) The review indicated ongoing MDA treatment for the past 27 years, with a reported coverage of over 65% in the last 17 yearly rounds; (ii) estimated treatment coverage by the CES in 2019 was 71.3%, with most of those not taking medicine stating that they were not offered; (iii) however, the key informant interviews revealed insufficiencies in reaching a significant number of people for treatment due to remote settlement, mobility, transport logistical issues, failure to register some people for treatment, leading to a false impression of good coverage, and a short distribution time; (iv) the most productive breeding was found within 5 km of Kwanware-Ottou; and (v) blackfly daily biting rates were highest in Kwanware and Ottou, with 199 and 160 bites per day, respectively. Infection in blackflies was found only in Kwanware and Ottou, with infectivity rates of 5.9‰ (per 1000) and 6.7‰, respectively. (vi) The mf prevalence in Ottou and Kwanware, respectively, was 40.0% and 30.0% among adults aged ≥ 20 years, and the anti-(Onchocerca volvulus) Ov16 IgG4 antibodies seroprevalence rates were 8.3% and 13.3% among children aged 5-9 years. These values were reduced to undetectable levels at a radius of 10 km from Ottou. This study confirms that active onchocerciasis transmission centres on Kwanware/Ottou and is confined to a 10 km radius despite 27 yearly treatment rounds. The main contributing factors are suboptimal coverage and high biting rates. Identifying and targeting such a focus with a combination of interventions will be cost-effective in accelerating onchocerciasis elimination in Ghana.

Sections du résumé

BACKGROUND BACKGROUND
This study examined onchocerciasis transmission in Kwanware and Ottou in the Wenchi Health District of Ghana, where persistent onchocercal microfilariae (mf) levels have been reported since 2012.
METHODS METHODS
This study was conducted from 2019 to 2021 and involved the following: (i) reviewing past records of ivermectin mass drug administration (MDA); (ii) conducting a treatment coverage evaluation survey (CES); (iii) conducting key informant interviews; (iv) prospecting blackfly breeding sites; (v) collecting and dissecting blackflies; and (vi) conducting parasitological and serological surveys.
RESULTS RESULTS
(i) The review indicated ongoing MDA treatment for the past 27 years, with a reported coverage of over 65% in the last 17 yearly rounds; (ii) estimated treatment coverage by the CES in 2019 was 71.3%, with most of those not taking medicine stating that they were not offered; (iii) however, the key informant interviews revealed insufficiencies in reaching a significant number of people for treatment due to remote settlement, mobility, transport logistical issues, failure to register some people for treatment, leading to a false impression of good coverage, and a short distribution time; (iv) the most productive breeding was found within 5 km of Kwanware-Ottou; and (v) blackfly daily biting rates were highest in Kwanware and Ottou, with 199 and 160 bites per day, respectively. Infection in blackflies was found only in Kwanware and Ottou, with infectivity rates of 5.9‰ (per 1000) and 6.7‰, respectively. (vi) The mf prevalence in Ottou and Kwanware, respectively, was 40.0% and 30.0% among adults aged ≥ 20 years, and the anti-(Onchocerca volvulus) Ov16 IgG4 antibodies seroprevalence rates were 8.3% and 13.3% among children aged 5-9 years. These values were reduced to undetectable levels at a radius of 10 km from Ottou.
CONCLUSIONS CONCLUSIONS
This study confirms that active onchocerciasis transmission centres on Kwanware/Ottou and is confined to a 10 km radius despite 27 yearly treatment rounds. The main contributing factors are suboptimal coverage and high biting rates. Identifying and targeting such a focus with a combination of interventions will be cost-effective in accelerating onchocerciasis elimination in Ghana.

Identifiants

pubmed: 39402497
doi: 10.1186/s12879-024-10071-2
pii: 10.1186/s12879-024-10071-2
doi:

Substances chimiques

Ivermectin 70288-86-7

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1156

Informations de copyright

© 2024. The Author(s).

Références

Burnham G, Onchocerciasis. Lancet. 1998;351(9112):1341–6.
doi: 10.1016/S0140-6736(97)12450-3 pubmed: 9643811
Nelson G. Human onchocerciasis: notes on the history, the parasite, and the life cycle. Ann Trop Med Parasitol. 1991;85(1):83–95.
doi: 10.1080/00034983.1991.11812534 pubmed: 1888224
Nelson GS, Onchocerciasis. Adv Parasitol. 1970;8:173–224.
doi: 10.1016/S0065-308X(08)60254-7 pubmed: 4997515
Brattig NW, Cheke RA, Garms R. Onchocerciasis (river blindness) - more than a century of research and control. Acta Trop. 2021;218:105677.
doi: 10.1016/j.actatropica.2020.105677 pubmed: 32857984
WHO. Elimination of human onchocerciasis: progress report, 2020–Élimination De L’onchocercose humaine: rapport de situation, 2020. Wkly Epidemiol Rec. 2021;96(46):557–67.
WHO. Elimination of human onchocerciasis: progress report, 2021–Élimination De L’onchocercose humaine: rapport de situation, 2021. Wkly Epidemiol Rec. 2022;97(46):591–8.
WHO. Ending the neglect to attain the sustainable development goals: a road map for neglected tropical diseases 2021–2030. 2020.
Traore MO, Sarr MD, Badji A, Bissan Y, Diawara L, Doumbia K, et al. Proof-of-principle of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: final results of a study in Mali and Senegal. PLoS Negl Trop Dis. 2012;6(9):e1825.
doi: 10.1371/journal.pntd.0001825 pubmed: 23029586 pmcid: 3441490
WHO. Onchocerciasis: elimination is feasible. Wkly Epidemiol Rec. 2009;84(37):382–4.
Diawara L, Traoré MO, Badji A, Bissan Y, Doumbia K, Goita SF, et al. Feasibility of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: first evidence from studies in Mali and Senegal. PLoS Negl Trop Dis. 2009;3(7):e497.
doi: 10.1371/journal.pntd.0000497 pubmed: 19621091 pmcid: 2710500
NTD Modelling Consortium Onchocerciasis Group. The World Health Organization 2030 goals for onchocerciasis: insights and perspectives from mathematical modelling. Gates Open Res. 2019;3:1545.
doi: 10.12688/gatesopenres.13067.1 pmcid: 6820451
Crisp G. Simulium and onchocerciasis in the Northern Territories of the Gold Coast. Postgrad Med J. 1956;34(388):103–4.
John ONS. On the presence of a filaria in craw-craw. Lancet. 1875;105(2686):265–6.
doi: 10.1016/S0140-6736(02)30941-3
WHO. Onchocerciasis control programme in West Africa. Geneva: Report of the WHO; 1995.
Biritwum N-K, de Souza DK, Asiedu O, Marfo B, Amazigo UV, Gyapong JO. Onchocerciasis control in Ghana (1974–2016). Parasites Vectors. 2021;14(1):1–9.
doi: 10.1186/s13071-020-04507-2
Otabil KB, Ankrah B, Bart-Plange EJ, Donkoh ES, Avarikame FA, Ofori-Appiah FO, et al. Prevalence of epilepsy in the onchocerciasis endemic middle belt of Ghana after 27 years of mass drug administration with ivermectin. Infect Dis Poverty. 2023;12(1):75.
doi: 10.1186/s40249-023-01117-9 pubmed: 37587500 pmcid: 10433588
Ghana Statistical Service. 2010 Population and Housing Census: Wenchi district analytical report. Accra, Ghana: GSS; 2014.
Thompson BH. Studies on the flight range and dispersal of Simulium Damnosum (Diptera: Simuliidae) in the rainforest of Cameroon. Ann Trop Med Parasitol. 1976;70(3):343–54.
doi: 10.1080/00034983.1976.11687130 pubmed: 971003
Katabarwa MN, Zarroug IMA, Negussu N, Aziz NM, Tadesse Z, Elmubark WA, et al. The Galabat-Metema cross-border onchocerciasis focus: the first coordinated interruption of onchocerciasis transmission in Africa. PLoS Negl Trop Dis. 2020;14(2):e0007830.
doi: 10.1371/journal.pntd.0007830 pubmed: 32027648 pmcid: 7004312
Stolk WA, Blok DJ, Hamley JID, Cantey PT, de Vlas SJ, Walker M, et al. Scaling-down mass ivermectin treatment for onchocerciasis elimination: modelling the impact of the geographical unit for decision making. Clin Infect Dis. 2021;72(Suppl 3):S165–71.
doi: 10.1093/cid/ciab238 pubmed: 33909070 pmcid: 8201558
Cochran W. Calculation of sample size when population is infinite. Sampling techniques. 3rd ed. New York: John Wiley & Sons, Inc; 1977.
Thylefors B, Philippon B, Prost A. Transmission potentials of Onchocerca Volvulus and the associated intensity of onchocerciasis in a sudan-savanna area. Tropenmed Parasitol. 1978;29(3):346–54.
pubmed: 214908
WHO. Training module for national entomologists in the management and supervision of the entomological activities in onchocerciasis control. Onchocerciasis control programme in West Africa; 2002.
Kale OO. A simplified technique for counting onchocercal microfilariae in skin snips. Bull World Health Organ. 1978;56(1):133–7.
pubmed: 307442 pmcid: 2395539
Collins RC, Brandling-Bennett AD, Holliman RB, Campbell CC, Darsie RF. Parasitological diagnosis of onchocerciasis: comparisons of incubation media and incubation times for skin snips. Am J Trop Med Hyg. 1980;29(1):35–41.
doi: 10.4269/ajtmh.1980.29.35 pubmed: 7352625
Rust K, Graubard B, Fuller WA, Stokes SL, Kott PS, editors. Finite population correction factors (Panel Discussion). Proc Surv Res Methods Sect. 2006.
WHO. Report of the third meeting of the WHO onchocerciasis technical advisory subgroup: Geneva, 26–28 February 2019. 2020.
Atekem K, Dixon R, Wilhelm A, Biholong B, Oye J, Djeunga HN, et al. Evaluating the impact of alternative intervention strategies in accelerating onchocerciasis elimination in an area of persistent transmission in the West Region of Cameroon. PLoS Negl Trop Dis. 2022;16(12):e0010591.
doi: 10.1371/journal.pntd.0010591 pubmed: 36542603 pmcid: 9770396
WHO. Guidelines for stopping mass drug administration and verifying elimination of human onchocerciasis: criteria and procedures. World Health Organization; 2016.
Otabil KB, Gyasi SF, Awuah E, Obeng-Ofori D, Tenkorang SB, Kessie JA, et al. Biting rates and relative abundance of Simulium flies under different climatic conditions in an onchocerciasis endemic community in Ghana. Parasit Vectors. 2020;13(1):229.
doi: 10.1186/s13071-020-04102-5 pubmed: 32375902 pmcid: 7204027
WHO. Conceptual and operational framework of onchocerciasis elimination with ivermectin treatment. African programme for onchocerciasis control; 2010.
Clark J, Davis EL, Prada JM, Gass K, Krentel A, Hollingsworth TD. How correlations between treatment access and surveillance inclusion impact neglected tropical disease monitoring and evaluation-A simulated study. PLoS Negl Trop Dis. 2023;17(9):e0011582.
doi: 10.1371/journal.pntd.0011582 pubmed: 37672518 pmcid: 10506705
Gass K, Deming M, Bougma R, Drabo F, Tukahebwa EM, Mkwanda S, et al. A multicountry comparison of three coverage evaluation survey sampling methodologies for neglected tropical diseases. Am J Trop Med Hyg. 2020;103(4):1700.
doi: 10.4269/ajtmh.19-0946 pubmed: 32840202 pmcid: 7543869
Nditanchou R, Dixon R, Atekem K, Biholong B, Wilhelm A, Selby R, et al. Ivermectin and doxycycline treatments against Onchocerciasis: adaptations and impact among seminomadic population in Massangam Health District, Cameroon. PLoS Negl Trop Dis. 2023;17(7):e0011463.
doi: 10.1371/journal.pntd.0011463 pubmed: 37437096 pmcid: 10365309
Lamberton PH, Cheke RA, Walker M, Winskill P, Osei-Atweneboana MY, Tirados I, et al. Onchocerciasis transmission in Ghana: biting and parous rates of host-seeking sibling species of the Simulium damnosum complex. Parasit Vectors. 2014;7:1–23.
doi: 10.1186/s13071-014-0511-9
Lamberton PH, Cheke RA, Winskill P, Tirados I, Walker M, Osei-Atweneboana MY, et al. Onchocerciasis transmission in Ghana: persistence under different control strategies and the role of the simuliid vectors. PLoS Negl Trop Dis. 2015;9(4):e0003688.
doi: 10.1371/journal.pntd.0003688 pubmed: 25897492 pmcid: 4405193
Wahl G, Enyong P, Ngosso A, Schibel JM, Moyou R, Tubbesing H, et al. Onchocerca ochengi: epidemiological evidence of cross-protection against Onchocerca Volvulus in man. Parasitology. 1998;116(4):349–62.
doi: 10.1017/S003118209700228X pubmed: 9585937
Boakye D, Mackenzie C, Tallant J, Heggen A, Leff S, Nadjilar L, et al. Enhancing onchocerciasis elimination program management: a biological approach to deciding when to begin stop mass drug administration activities. PLoS Negl Trop Dis. 2023;17(7):e0011348.
doi: 10.1371/journal.pntd.0011348 pubmed: 37440479 pmcid: 10343055
Osei-Atweneboana MY, Awadzi K, Attah SK, Boakye DA, Gyapong JO, Prichard RK. Phenotypic evidence of emerging ivermectin resistance in Onchocerca Volvulus. PLoS Negl Trop Dis. 2011;5(3):e998.
doi: 10.1371/journal.pntd.0000998 pubmed: 21468315 pmcid: 3066159
Verver S, Walker M, Kim YE, Fobi G, Tekle AH, Zouré HGM, et al. How can onchocerciasis elimination in Africa be accelerated? PLoS Negl Trop Dis. 2023;17(9):e0011582.
WHO. Progress in eliminating onchocerciasis in the WHO region of the Americas: doxycycline treatment as an end-game strategy. Wkly Epidemiol Rec. 2019;94(37):415–9.

Auteurs

Rogers Nditanchou (R)

Sightsavers Cameroon Country Office, Immeuble No 1067 bis Rue 1750 Nouvelle Route Bastos, P.O. Box 4844, Bastos, Yaoundé, Cameroon. rnditanchou@sightsavers.org.

David Agyemang (D)

Sightsavers Ghana Country Office, The Elizabeth, No. 39, Senchi Link Airport Residential Area, P.O. Box 18190 KIA, Accra, Ghana.

Ruth Dixon (R)

Technopolis Group, 3 Pavilion Buildings, Brighton, BN1 1EE, UK.

Susan D'Souza (S)

Sightsavers, 35 Perrymount Road, Haywards Heath, RH16 3BW, UK.

Richard Selby (R)

Sightsavers, 35 Perrymount Road, Haywards Heath, RH16 3BW, UK.

Joseph Opare (J)

Neglected Tropical Diseases Programme, Ghana Health Service, PMB, Ministries, P.O. Box MB-190, Accra, Ghana.

Edward Jenner Tettevi (EJ)

The Council for Scientific and Industrial Research (CSIR), P. O. Box AH 38, Achimota, Accra, Ghana.

Manfred Dakorah Asiedu (MD)

The Council for Scientific and Industrial Research (CSIR), P. O. Box AH 38, Achimota, Accra, Ghana.

Bright Idun (B)

The Council for Scientific and Industrial Research (CSIR), P. O. Box AH 38, Achimota, Accra, Ghana.

Alexandre Chailloux (A)

Sightsavers, 35 Perrymount Road, Haywards Heath, RH16 3BW, UK.

Elena Schmidt (E)

Sightsavers, 35 Perrymount Road, Haywards Heath, RH16 3BW, UK.

Louise Hamill (L)

Sightsavers, 35 Perrymount Road, Haywards Heath, RH16 3BW, UK.

Laura Senyonjo (L)

Sightsavers, 35 Perrymount Road, Haywards Heath, RH16 3BW, UK.

Mike Yaw Osei-Atweneboana (MY)

The Council for Scientific and Industrial Research (CSIR), P. O. Box AH 38, Achimota, Accra, Ghana.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH