Impact of annual and semi-annual mass drug administration for Lymphatic Filariasis and Onchocerciasis on Hookworm Infection in Côte d’Ivoire

Mass Drug Administration (MDA) programs to eliminate Lymphatic Filariasis (LF) in western Africa use the anthelminthics ivermectin plus albendazole. These drugs have the potential to impact also Soil-Transmitted Helminth (STH) infections, since the drugs have a broad range of anthelminthic activity. Integration of preventive chemotherapy efforts for LF, onchocerciasis and STH is recommended by the World Health Organization (WHO) in order to avoid duplication of MDA and to reduce costs. The objective of the current study was to determine whether five semi-annual rounds of community-wide MDA to eliminate LF and onchocerciasis have a greater impact on STH than three annual rounds of MDA with similar compliance. The effects of MDA using ivermectin (IVM, 0.2 mg/kg) combined with albendazole (ALB, 400 mg) on the prevalence and intensity of hookworm infection were evaluated in the Abengourou (annual MDA) and Akoupé (semi-annual MDA) health Districts in eastern Côte d’Ivoire from 2014 to 2017. A cross-sectional approach was used together with mixed logistic regression, and mixed linear models. Subjects were tested for STH using the Kato-Katz technique before the first round of MDA and 12, 24, and 36 months after the first round of MDA. The mean self-reported MDA compliance assessed during the survey was 65%, and no difference was observed between treatment areas. These results were confirmed by an independent coverage survey as recommended by WHO. Hookworm was the most prevalent STH species in both areas (23.9% vs 12.4%) and the prevalence of other STH species was less than 1%. The crude prevalence of hookworm dropped significantly, from 23.9% to 5.5% (p <0.001, 77% reduction) in the annual MDA treatment area and from 12.4% to 1.9% (p <0.001, 85% reduction) in the semi-annual treatment area. The average intensity of hookworm infection decreased in the annual MDA area (406.2 epg to 118.3 epg), but not in the semi-annual MDA area (804.9 epg to 875.0 epg). Moderate and heavy infections (1% and 1.3% at baseline) were reduced to 0% and 0.4% in the annual and semi-annual treatment areas, respectively. Using a mixed logistic regression model, and after adjusting for baseline prevalence, only the year 2 re-examination showed a difference in prevalence between treatments (OR: 2.26 [95% CI: 1.03, 4.98], p = 0.043). Analysis of intensity of hookworm infection indicated also that treatment differences varied by follow-up visit. In conclusion twelve months after the last treatment cycle, three annual and five semi-annual rounds of community-wide MDA with the combination of IVM and ALB showed strong, but similar impact on hookworm prevalence and intensity in eastern Côte d’Ivoire. Therefore, an annual MDA regimen seems to be an efficient strategy to control hookworm infection in endemic areas with low and moderate infection prevalence. Trial registration: The study was registered at ClinicalTrial.gov under the number NTC02032043.

[1]  E. N'Goran,et al.  Prevalence, Intensity of Soil-Transmitted Helminths, and Factors Associated with Infection: Importance in Control Program with Ivermectin and Albendazole in Eastern Côte d'Ivoire , 2019, Journal of tropical medicine.

[2]  J. Keiser,et al.  Drug Combinations Against Soil-Transmitted Helminth Infections. , 2019, Advances in parasitology.

[3]  M. Mitreva,et al.  Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia , 2018, Microbiome.

[4]  R. Anderson,et al.  Helminth lifespan interacts with non-compliance in reducing the effectiveness of anthelmintic treatment , 2018, Parasites & Vectors.

[5]  R. Laing,et al.  Ivermectin – Old Drug, New Tricks? , 2017, Trends in parasitology.

[6]  R. Anderson,et al.  The past matters: estimating intrinsic hookworm transmission intensity in areas with past mass drug administration to control lymphatic filariasis , 2017, Parasites & Vectors.

[7]  L. Coffeng,et al.  Comparison and validation of two mathematical models for the impact of mass drug administration on Ascaris lumbricoides and hookworm infection , 2017, Epidemics.

[8]  U. Ekpo,et al.  Assessment of the burden of soil-transmitted helminthiasis after five years of mass drug administration for Onchocerciasis and Lymphatic filariasis in Kebbi State, Nigeria , 2017, Parasite epidemiology and control.

[9]  J. Walson,et al.  Integrated Healthcare Delivery: A Qualitative Research Approach to Identifying and Harmonizing Perspectives of Integrated Neglected Tropical Disease Programs , 2016, PLoS neglected tropical diseases.

[10]  I. Bogoch,et al.  Efficacy and safety of albendazole plus ivermectin, albendazole plus mebendazole, albendazole plus oxantel pamoate, and mebendazole alone against Trichuris trichiura and concomitant soil-transmitted helminth infections: a four-arm, randomised controlled trial. , 2015, The Lancet. Infectious diseases.

[11]  J. Utzinger,et al.  Sustaining control of schistosomiasis mansoni in moderate endemicity areas in western Côte d’Ivoire: a SCORE study protocol , 2014, BMC Public Health.

[12]  B. Babu,et al.  Coverage of, and compliance with, mass drug administration under the programme to eliminate lymphatic filariasis in India: a systematic review. , 2014, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[13]  P. Hotez,et al.  The contribution of mass drug administration to global health: past, present and future , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  J. Utzinger,et al.  Infection and Co-infection with Helminths and Plasmodium among School Children in Côte d’Ivoire: Results from a National Cross-Sectional Survey , 2014, PLoS neglected tropical diseases.

[15]  S. Brooker,et al.  Global numbers of infection and disease burden of soil transmitted helminth infections in 2010 , 2014, Parasites & Vectors.

[16]  G. Weil,et al.  A Review of Factors That Influence Individual Compliance with Mass Drug Administration for Elimination of Lymphatic Filariasis , 2013, PLoS neglected tropical diseases.

[17]  S. Brooker,et al.  How Effective Is School-Based Deworming for the Community-Wide Control of Soil-Transmitted Helminths? , 2013, PLoS neglected tropical diseases.

[18]  K. Adoubryn,et al.  [Intestinal parasites in children in Biankouma, Ivory Coast (mountaineous western region): efficacy and safety of praziquantel and albendazole]. , 2012, Medecine et sante tropicales.

[19]  J. McCarthy,et al.  A Research Agenda for Helminth Diseases of Humans: The Problem of Helminthiases , 2012, PLoS neglected tropical diseases.

[20]  P. Newton,et al.  A review of parasitic zoonoses in a changing Southeast Asia. , 2011, Veterinary parasitology.

[21]  Shannon K. McClintock,et al.  A Community-Based Study of Factors Associated with Continuing Transmission of Lymphatic Filariasis in Leogane, Haiti , 2010, PLoS neglected tropical diseases.

[22]  Peter J. Hotez,et al.  Neglected Tropical Diseases in Sub-Saharan Africa: Review of Their Prevalence, Distribution, and Disease Burden , 2009, PLoS neglected tropical diseases.

[23]  Steven A. Williams,et al.  The Impact of Repeated Rounds of Mass Drug Administration with Diethylcarbamazine Plus Albendazole on Bancroftian Filariasis in Papua New Guinea , 2008, PLoS neglected tropical diseases.

[24]  L. Wen,et al.  A randomized, double-blind, multicenter clinical trial on the efficacy of ivermectin against intestinal nematode infections in China. , 2008, Acta tropica.

[25]  Peter J Hotez,et al.  Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm , 2006, The Lancet.

[26]  V. Nantulya,et al.  Linking disease control programmes in rural Africa: a pro-poor strategy to reach Abuja targets and millennium development goals , 2004, BMJ : British Medical Journal.

[27]  Peter J Hotez,et al.  Human hookworm infection in the 21st century. , 2004, Advances in parasitology.

[28]  T. Gyorkos,et al.  Helminth Control in School-age Children: A Guide for Managers of Control Programmes , 2002 .

[29]  A. Bennett,et al.  Reducing intestinal nematode infection: efficacy of albendazole and mebendazole. , 2000, Parasitology today.

[30]  H. Guyatt,et al.  Worm burden in intestinal obstruction caused by Ascaris lumbricoides , 1997, Tropical medicine & international health : TM & IH.

[31]  S. Cousens,et al.  Ivermectin dose assessment without weighing scales. , 1993, Bulletin of the World Health Organization.

[32]  Leon X. Liu Basic laboratory methods in medical parasitology , 1992 .

[33]  F. Cox Basic laboratory methods in medical parasitology , 1992 .

[34]  E. Lauber,et al.  [Development of anthropometric parameters for 5-to-15-year-old children and the effect of parasitic diseases on their growth]. , 1980, Acta tropica. Supplementum.