Entomological assessment of lymphatic filariasis transmission in "hotspot" and control districts after several rounds of mass drug administration in Ghana

Background Lymphatic filariasis (LF) is a major health problem, which mostly affects individuals in tropical and subtropical regions despite global efforts to control and interrupt its transmission in endemic countries. An estimated 120 million are infected, with about 40 million disfigured and incapacitated worldwide. The main strategy for the control of LF by the Global Programme to Eliminate Lymphatic Filariasis (GPELF) is through mass chemotherapy. In West Africa, specifically in Ghana, mass drug administration (MDA) commenced in the year 2000 with endemic districts receiving at least eight rounds of treatment. In principle, transmission of infections should have been interrupted in all areas after this long period of treatment with reported therapeutic coverage of more than 65%. However, recent information gathered from the Ghana Neglected Tropical Diseases Programme Unit has revealed ongoing transmission in some districts despite their involvement in at least eight rounds of MDA. The main aim of the GPELF is to eliminate this disease by year 2020. However, the current elimination status in Ghana poses a serious challenge in meeting this goal. It is therefore important to investigate driving factors that could possibly be responsible for the observed ongoing LF transmission in endemic districts in Ghana having undergone several rounds of MDA. This will provide information that will add on to existing evidence for appropriate intervention or approach specific to each district. Aim and objectives The main aim of this study was to explicitly look at entomological and sociological factors which might possibly be contributing to persistent LF transmission in “hotspot” districts, together with the development and validation of a community-based vector collection system. The specific objectives were (i) to establish a system for collecting large numbers of mosquito samples for xenomonitoring, through the development of a community-based vector collection system; (ii) to determine the mosquito species composition in the various study districts; (iii) to determine the role of different species of mosquitoes in the transmission of lymphatic filariasis in the “hotspot” and control districts; (iv) to determine the role and variations in the cibarial armature of different mosquito species in the study communities; and (v) to undertake a questionnaire survey to determine compliance to MDA and possession and use of bednets and other vector control measures in the study districts. Methods This study was conducted in Ahanta West and Kassena Nankana West districts located in the Western and Upper East regions of Ghana, respectively. Both study areas were identified as “hotspot” districts in the country by the Ghana Neglected Tropical Disease Unit of the Ghana Health Service. This was due to high prevalence of LF in sentinel and cross check communities. Additionally, two control districts, Mpohor and Bongo, were also selected due to their zero microfilariae (mf) prevalence. A 13-month (July 2015 - July 2016) collection of mosquitoes was concurrently conducted in all study districts. This involved the training of community vector collectors (CVCs) in the various mosquito collection methods, which included human landing catches, pyrethrum spray catches and window exit traps. Supervisors were further trained on how to package samples for shipment to the Noguchi research team. Sampled mosquitoes from the respective districts were later subjected to molecular analysis for the detection of Wuchereria bancrofti infections as well as determine the sibling species of the Anopheles gambiae complex. Mosquito dissections were also done to estimate various entomological transmission indices. Variations in cibarial armatures of various mosquito species were investigated by clearing of mosquito heads with chloral hydrate to make cibarial teeth visible for counting. Questionnaires were administered in the various districts to obtain information on MDA compliance and vector control activities. Data were also obtained from the Ghana Neglected Tropical Disease Unit on the number of rounds and MDA coverage in the respective districts. Results A total number of 31,064 mosquitoes were collected from all the districts using human landing collections, pyrethrum spray catches and windows exit traps. Mosquitoes sampled were Aedes, Anopheles coustani, An. gambiae, An. pharoensis, Culex and Mansonia species. Molecular identification of An. gambiae complex showed An. gambiae s.s. in all districts. An. arabiensis and An. melas sibling species were identified from Kassena Nankana West/Bongo and Ahanta West districts, respectively. Furthermore, there was no difference in the shape and mean number of cibarial teeth of mosquitoes collected from hotspot and control districts in the Western and Upper East regions. In general, MDA coverage was ≥65% for all districts. However, MDA coverage in the Upper East region was <65% for Kassena Nankana West in 2003 and 2004/2005 in Bongo district. Validation of mosquitoes sampled by CVCs showed no significant difference in the numbers sampled by CVCs and the research team in the dry (P = 0.258) and rainy (P = 0.309) season in southern Ghana. However, there was significant difference in the numbers sampled by research team and CVCs during the rainy (P = 0.005) and dry (P = 0.033) season in northern Ghana. Assessment of the cost-effectiveness of sampling mosquitoes for xenomonitoring activities using CVCs and research team was done. Results indicated that the cost of sampling mosquitoes was lower using CVCs compared to research team (USD 15.17 vs 53.74 USD). The highest recurrent and capital cost was personnel (USD 21,370.04) and transportation (USD 2,900.14) costs, respectively. Furthermore, the assessment of W. bancrofti infection in mosquitoes as post-MDA surveillance tool using xenomonitoring was done. Results showed the sampling method human landing collections (27,739: 89.3%) recording the highest number of mosquitoes, followed by pyrethrum spray collections (2,687: 8.7%) and windows exit traps (638: 2.1%). Restriction fragment length polymorphism (RFLP) showed the high presence of An. coluzzii species in almost all districts. Dissections reported the presence of W. bancrofti in An. melas from Ahanta West district. Also, the annual transmission potential (ATP) for An. melas from the Ahanta West district was 7.4. Conclusion/recommendations Persistent LF transmission in “hotspot” areas in this study presents information that shows the importance of local understanding of factors affecting elimination of LF. However, the study shows that it is feasible to use CVCs to sample large numbers of mosquitoes with minimal supervision. It is also cost-effective to use CVCs to collect mosquitoes for xenomonitoring compared to a dedicated research team. The inclusion of CVCs in xenomonitoring activities promotes active community participation and ownership of vector control activities. Additionally, W. bancrofti infections are found and sustained in Ahanta West district in An. melas that uses the phenomenon of limitation for lymphatic filariasis transmission. This study also showed the possibility of using xenomonitoring as a post-MDA surveillance tool. We recommend that LF interventions should consider spatial heterogeneities and best approach to use in all endemic foci. Moreover, xenomonitoring should be considered in the decision-making processes to stop or continue MDA by stakeholders and programme managers. Also, mosquito traps and sampling methods should be safe, practical and convenient for CVCs to use with less supervision and the inclusion of vector control activities by programme managers and stakeholders in planning intervention programmes

Entomological assessment of lymphatic filariasis transmission in "hotspot" and control districts after several rounds of mass drug administration in Ghana

Background Lymphatic filariasis (LF) is a major health problem, which mostly affects individuals in tropical and subtropical regions despite global efforts to control and interrupt its transmission in endemic countries. An estimated 120 million are infected, with about 40 million disfigured and incapacitated worldwide. The main strategy for the control of LF by the Global Programme to Eliminate Lymphatic Filariasis (GPELF) is through mass chemotherapy. In West Africa, specifically in Ghana, mass drug administration (MDA) commenced in the year 2000 with endemic districts receiving at least eight rounds of treatment. In principle, transmission of infections should have been interrupted in all areas after this long period of treatment with reported therapeutic coverage of more than 65%. However, recent information gathered from the Ghana Neglected Tropical Diseases Programme Unit has revealed ongoing transmission in some districts despite their involvement in at least eight rounds of MDA. The main aim of the GPELF is to eliminate this disease by year 2020. However, the current elimination status in Ghana poses a serious challenge in meeting this goal. It is therefore important to investigate driving factors that could possibly be responsible for the observed ongoing LF transmission in endemic districts in Ghana having undergone several rounds of MDA. This will provide information that will add on to existing evidence for appropriate intervention or approach specific to each district. Aim and objectives The main aim of this study was to explicitly look at entomological and sociological factors which might possibly be contributing to persistent LF transmission in “hotspot” districts, together with the development and validation of a community-based vector collection system. The specific objectives were (i) to establish a system for collecting large numbers of mosquito samples for xenomonitoring, through the development of a community-based vector collection system; (ii) to determine the mosquito species composition in the various study districts; (iii) to determine the role of different species of mosquitoes in the transmission of lymphatic filariasis in the “hotspot” and control districts; (iv) to determine the role and variations in the cibarial armature of different mosquito species in the study communities; and (v) to undertake a questionnaire survey to determine compliance to MDA and possession and use of bednets and other vector control measures in the study districts. Methods This study was conducted in Ahanta West and Kassena Nankana West districts located in the Western and Upper East regions of Ghana, respectively. Both study areas were identified as “hotspot” districts in the country by the Ghana Neglected Tropical Disease Unit of the Ghana Health Service. This was due to high prevalence of LF in sentinel and cross check communities. Additionally, two control districts, Mpohor and Bongo, were also selected due to their zero microfilariae (mf) prevalence. A 13-month (July 2015 - July 2016) collection of mosquitoes was concurrently conducted in all study districts. This involved the training of community vector collectors (CVCs) in the various mosquito collection methods, which included human landing catches, pyrethrum spray catches and window exit traps. Supervisors were further trained on how to package samples for shipment to the Noguchi research team. Sampled mosquitoes from the respective districts were later subjected to molecular analysis for the detection of Wuchereria bancrofti infections as well as determine the sibling species of the Anopheles gambiae complex. Mosquito dissections were also done to estimate various entomological transmission indices. Variations in cibarial armatures of various mosquito species were investigated by clearing of mosquito heads with chloral hydrate to make cibarial teeth visible for counting. Questionnaires were administered in the various districts to obtain information on MDA compliance and vector control activities. Data were also obtained from the Ghana Neglected Tropical Disease Unit on the number of rounds and MDA coverage in the respective districts. Results A total number of 31,064 mosquitoes were collected from all the districts using human landing collections, pyrethrum spray catches and windows exit traps. Mosquitoes sampled were Aedes, Anopheles coustani, An. gambiae, An. pharoensis, Culex and Mansonia species. Molecular identification of An. gambiae complex showed An. gambiae s.s. in all districts. An. arabiensis and An. melas sibling species were identified from Kassena Nankana West/Bongo and Ahanta West districts, respectively. Furthermore, there was no difference in the shape and mean number of cibarial teeth of mosquitoes collected from hotspot and control districts in the Western and Upper East regions. In general, MDA coverage was ≥65% for all districts. However, MDA coverage in the Upper East region was <65% for Kassena Nankana West in 2003 and 2004/2005 in Bongo district. Validation of mosquitoes sampled by CVCs showed no significant difference in the numbers sampled by CVCs and the research team in the dry (P = 0.258) and rainy (P = 0.309) season in southern Ghana. However, there was significant difference in the numbers sampled by research team and CVCs during the rainy (P = 0.005) and dry (P = 0.033) season in northern Ghana. Assessment of the cost-effectiveness of sampling mosquitoes for xenomonitoring activities using CVCs and research team was done. Results indicated that the cost of sampling mosquitoes was lower using CVCs compared to research team (USD 15.17 vs 53.74 USD). The highest recurrent and capital cost was personnel (USD 21,370.04) and transportation (USD 2,900.14) costs, respectively. Furthermore, the assessment of W. bancrofti infection in mosquitoes as post-MDA surveillance tool using xenomonitoring was done. Results showed the sampling method human landing collections (27,739: 89.3%) recording the highest number of mosquitoes, followed by pyrethrum spray collections (2,687: 8.7%) and windows exit traps (638: 2.1%). Restriction fragment length polymorphism (RFLP) showed the high presence of An. coluzzii species in almost all districts. Dissections reported the presence of W. bancrofti in An. melas from Ahanta West district. Also, the annual transmission potential (ATP) for An. melas from the Ahanta West district was 7.4. Conclusion/recommendations Persistent LF transmission in “hotspot” areas in this study presents information that shows the importance of local understanding of factors affecting elimination of LF. However, the study shows that it is feasible to use CVCs to sample large numbers of mosquitoes with minimal supervision. It is also cost-effective to use CVCs to collect mosquitoes for xenomonitoring compared to a dedicated research team. The inclusion of CVCs in xenomonitoring activities promotes active community participation and ownership of vector control activities. Additionally, W. bancrofti infections are found and sustained in Ahanta West district in An. melas that uses the phenomenon of limitation for lymphatic filariasis transmission. This study also showed the possibility of using xenomonitoring as a post-MDA surveillance tool. We recommend that LF interventions should consider spatial heterogeneities and best approach to use in all endemic foci. Moreover, xenomonitoring should be considered in the decision-making processes to stop or continue MDA by stakeholders and programme managers. Also, mosquito traps and sampling methods should be safe, practical and convenient for CVCs to use with less supervision and the inclusion of vector control activities by programme managers and stakeholders in planning intervention programmes

Building the capacity of West African countries in Aedes surveillance: inaugural meeting of the West African Aedes Surveillance Network (WAASuN)

Arboviral diseases such as dengue, Zika and chikungunya transmitted by Aedes mosquitoes have been reported in 34 African countries. Available data indicate that in recent years there have been dengue and chikungunya outbreaks in the West Africa subregion, in countries including Côte d’Ivoire, Burkina Faso, Gabon, Senegal, and Benin. These viral diseases are causing an increased public health burden, which impedes poverty reduction and sustainable development. Aedes surveillance and control capacity, which are key to reducing the prevalence of arboviral infections, need to be strengthened in West Africa, to provide information essential for the formulation of effective vector control strategies and the prediction of arboviral disease outbreaks. In line with these objectives, the West African Aedes Surveillance Network (WAASuN) was created in 2017 at a meeting held in Sierra Leone comprising African scientists working on Aedes mosquitoes. This manuscript describes the proceedings and discusses key highlights of the meeting

A Comparative Study of Lymphatic Filariasis-Related Perceptions among Treated and Non-Treated Individuals in the Ahanta West Municipality of Ghana

Background: Ghana joined the Global Programme to Eliminate Lymphatic Filariasis (GPELF), established in the year 2000, with the aim of eliminating the disease as a public health problem through annual mass treatment of entire endemic populations. Since 2001, the country has implemented mass drug administration (MDA) in endemic districts, with great reductions in the population at risk for infection. However, in many districts, the elimination programme is faced with the presence of hotspots, which may be due in part to individuals not taking part in MDA (either intentionally or unintentionally) who may serve as reservoirs to sustain transmission. This paper compares the LF-related perceptions among individuals who regularly take the MDA drugs and those who seldom or never take part in the MDA in the Ahanta West Municipality of Ghana to determine community acceptable ways to implement an intervention aimed to track, engage, and treat individuals who regularly miss MDA or to test individuals who intentionally refuse MDA and treat them if positive for LF. Methods: This was a mixed method study employing questionnaire surveys and focus group discussions (FDG) for data collection. Survey participants were randomly selected from the 2019 treatment register to stratify respondents into treated and non-treated groups. FGD participants were selected purposively such that there are at least two non-treated persons in each discussion session. Results: Over 90% of the respondents were aware of the disease. Poor hygiene/dirty environment was wrongly reported by most respondents (76.8%) as the causes. MDA awareness was very high among both treated (96.9%) and non-treated (98.6%) groups. A low sense of vulnerability to LF infection was evident by a reduction in the number of people presenting clinical manifestations of the disease in communities. Slightly more, 65 (29.0%) of the non-treated group compared to the 42 (19.4%) treated group reported ever experiencing adverse effects of the MDA drugs. Barriers to MDA uptake reported in both groups were poor planning and implementation of the MDA, lack of commitments on the part of drug distributors, and adverse drug reactions. About 51% of the non-treated group reported never taking the drugs even once in the last five years, while 61% among the treated group took the MDA drug consistently in the past five years. Respondents in both groups believed that, when engaged properly, most non-treated persons will accept to take the drug but insisted community drug distributors (CDDs) must be trained to effectively engage people and have time for those they will be engaging in dialogue. The chiefs emerged as the most influential people who can influence people to take MDA drugs. Conclusions: The reduction in risk perception among respondents, adverse reactions and the timing of MDA activities may be influencing MDA non-participation in the study area; however, respondents think that non-treated individuals will accept the interventions when engaged properly by the CDDs

Assessing the Presence of Wuchereria bancrofti Infections in Vectors Using Xenomonitoring in Lymphatic Filariasis Endemic Districts in Ghana

Mass drug administration (MDA) is the current mainstay to interrupt the transmission of lymphatic filariasis. To monitor whether MDA is effective and transmission of lymphatic filariasis indeed has been interrupted, rigorous surveillance is required. Assessment of transmission by programme managers is usually done via serology. New research suggests that xenomonitoring holds promise for determining the success of lymphatic filariasis interventions. The objective of this study was to assess Wuchereria bancrofti infection in mosquitoes as a post-MDA surveillance tool using xenomonitoring. The study was carried out in four districts of Ghana; Ahanta West, Mpohor, Kassena Nankana West and Bongo. A suite of mosquito sampling methods was employed, including human landing collections, pyrethrum spray catches and window exit traps. Infection of W. bancrofti in mosquitoes was determined using dissection, conventional and real-time polymerase chain reaction and loop mediated isothermal amplification assays. Aedes, Anopheles coustani, An. gambiae, An. pharoensis, Culex and Mansonia mosquitoes were sampled in each of the four study districts. The dissected mosquitoes were positive for filarial infection using molecular assays. Dissected An. melas mosquitoes from Ahanta West district were the only species found positive for filarial parasites. We conclude that whilst samples extracted with Trizol reagent did not show any positives, molecular methods should still be considered for monitoring and surveillance of lymphatic filariasis transmission

Implementing a community vector collection strategy using xenomonitoring for the endgame of lymphatic filariasis elimination

BACKGROUND: The global strategy for elimination of lymphatic filariasis is by annual mass drug administration (MDA). Effective implementation of this strategy in endemic areas reduces Wuchereria bancrofti in the blood of infected individuals to very low levels. This minimises the rate at which vectors successfully pick microfilariae from infected blood, hence requiring large mosquito numbers to detect infections. The aim of this study was to assess the feasibility of using trained community vector collectors (CVCs) to sample large mosquito numbers with minimal supervision at low cost for potential scale-up of this strategy. METHODS: CVCs and supervisors were trained in mosquito sampling methods, i.e. human landing collections, pyrethrum spray collections and window exit traps. Mosquito sampling was done over a 13-month period. Validation was conducted by a research team as quality control for mosquitoes sampled by CVCs. Data were analyzed for number of mosquitoes collected and cost incurred by the research team and CVCs during the validation phase of the study. RESULTS: A total of 31,064 and 8720 mosquitoes were sampled by CVCs and the research team, respectively. We found a significant difference (F(1,13) = 27.1606, P = 0.0001) in the total number of mosquitoes collected from southern and northern communities. Validation revealed similar numbers of mosquitoes sampled by CVCs and the research team, both in the wet (F(1,4) = 1.875, P = 0.309) and dry (F(1,4) = 2.276, P = 0.258) seasons in the southern communities, but was significantly different for both wet (F(1,4) = 0.022, P = 0.005) and dry (F(1,4 ) = 0.079, P = 0.033) seasons in the north. The cost of sampling mosquitoes per season was considerably lower by CVCs compared to the research team (15.170 vs 53.739 USD). CONCLUSIONS: This study revealed the feasibility of using CVCs to sample large numbers of mosquitoes with minimal supervision from a research team at considerably lower cost than a research team for lymphatic filariasis xenomonitoring. However, evaluation of the selection and motivation of CVCs, acceptability of CVCs strategy and its epidemiological relevance for lymphatic filariasis xenomonitoring programmes need to be assessed in greater detail

Potential factors influencing lymphatic filariasis transmission in “hotspot” and “control” areas in Ghana: the importance of vectors

BACKGROUND: Mass drug administration (MDA) programmes for the control of lymphatic filariasis in Ghana, have been ongoing in some endemic districts for 16 years. The current study aimed to assess factors that govern the success of MDA programmes for breaking transmission of lymphatic filariasis in Ghana. METHODS: The study was undertaken in two "hotspot" districts (Ahanta West and Kassena Nankana West) and two control districts (Mpohor and Bongo) in Ghana. Mosquitoes were collected and identified using morphological and molecular tools. A proportion of the cibarial armatures of each species was examined. Dissections were performed on Anopheles gambiae for filarial worm detection. A questionnaire was administered to obtain information on MDA compliance and vector control activities. Data were compared between districts to determine factors that might explain persistent transmission of lymphatic filariasis. RESULTS: High numbers of mosquitoes were sampled in Ahanta West district compared to Mpohor district (F = 16.09, P = 0.002). There was no significant difference between the numbers of mosquitoes collected in Kassena Nankana West and Bongo districts (F = 2.16, P = 0.185). Mansonia species were predominant in Ahanta West district. An. coluzzii mosquitoes were prevalent in all districts. An. melas with infected and infective filarial worms was found only in Ahanta West district. No differences were found in cibarial teeth numbers and shape for mosquito species in the surveyed districts. Reported MDA coverage was high in all districts. The average use of bednet and indoor residual spraying was 82.4 and 66.2%, respectively. There was high compliance in the five preceding MDA rounds in Ahanta West and Kassena Nankana West districts, both considered hotspots of lymphatic filariasis transmission. CONCLUSIONS: The study on persistent transmission of lymphatic filariasis in the two areas in Ghana present information that shows the importance of local understanding of factors affecting control and elimination of lymphatic filariasis. Unlike Kassena Nankana West district where transmission dynamics could be explained by initial infection prevalence and low vector densities, ongoing lymphatic filariasis transmission in Ahanta West district might be explained by high biting rates of An. gambiae and initial infection prevalence, coupled with high densities of An. melas and Mansonia vector species that have low or no teeth and exhibiting limitation

Entomological risk assessment for transmission of arboviral diseases by Aedes mosquitoes in a domestic and forest site in Accra, Ghana.

Dengue, Zika and chikungunya are Aedes-borne viral diseases that have become great global health concerns in the past years. Several countries in Africa have reported outbreaks of these diseases and despite Ghana sharing borders with some of these countries, such outbreaks are yet to be detected. Viral RNA and antibodies against dengue serotype-2 have recently been reported among individuals in some localities in the regional capital of Ghana. This is an indication of a possible silent transmission ongoing in the population. This study, therefore, investigated the entomological transmission risk of dengue, Zika and chikungunya viruses in a forest and domestic population in the Greater Accra Region, Ghana. All stages of the Aedes mosquito (egg, larvae, pupae and adults) were collected around homes and in the forest area for estimation of risk indices. All eggs were hatched and reared to larvae or adults for morphological identification together with larvae and adults collected from the field. The forest population had higher species richness with 7 Aedes species. The predominant species of Aedes mosquitoes identified from both sites was Aedes aegypti (98%). Aedes albopictus, an important arbovirus vector, was identified only in the peri-domestic population at a prevalence of 1.5%, significantly higher than previously reported. All risk indices were above the WHO threshold except the House Index for the domestic site which was moderate (19.8). The forest population recorded higher Positive Ovitrap (34.2% vs 26.6%) and Container (67.9% vs 36.8%) Indices than the peri-domestic population. Although none of the mosquito pools showed the presence of dengue, chikungunya or Zika viruses, all entomological risk indicators showed that both sites had a high potential arboviral disease transmission risk should any of these viruses be introduced. Continuous surveillance is recommended in these and other sites in the Metropolis to properly map transmission risk areas to inform outbreak preparedness strategies