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Research Article
Revised

Implementing a community vector collection strategy for monitoring vector-borne diseases in Ghana

[version 2; peer review: 1 approved, 1 approved with reservations]
PUBLISHED 29 May 2019
Author details Author details

Abstract

Background: Monitoring vector-borne diseases requires sampling of very large numbers of disease vectors in order to corroborate infections in the human population. This can be challenging, as current vector collection tools are either inefficient, or expensive to implement from a public health perspective. To circumvent this challenge, this study compared a community vector collection strategy using a double-netted mosquito collection method (a tent trap (TT)) to the traditional human landing collection (HLC) method in three communities in lymphatic filariasis-endemic districts in Ghana.
Methods: Following community entry and sensitization, community volunteers appointed by the community leaders were trained in the mosquito collection and storage methods and provided with supplies for mosquito collection over a 7-month period. They were visited occasionally by the study team to retrieve the mosquito samples for identification. The collectors were also assessed to evaluate their perspectives on using community vector collectors for monitoring vector-borne diseases.
Results: The results of the study indicated that the TT method collected significantly more mosquitoes (63%) over the collection period than HLC (37%). Thus, the TTs were observed to be performing relatively better than the HLC (P<0.001). The collectors knew the importance of mosquitoes in transmitting diseases, could identify the main diseases that were locally transmitted within their communities. They appreciated the involvement of the community in the collection as this enhanced community ownership of the programme as well as providing some financial incentives to those directly involved in the collection.
Conclusions: The study revealed that use of community volunteers for the collection of mosquitoes for xenomonitoring purposes can be a viable strategy in the monitoring of vector-borne diseases. However, further development of the strategies and assessments of the costs involved will be required to make this a sustainable approach to monitoring vector-borne disease interventions and enhance community ownership of the programmes.

Keywords

Xenomonitoring, community vector collectors, lymphatic filariasis, Ghana.

Revised Amendments from Version 1

In this revised version of the paper, we addressed the comments by the reviewers. 
Several minor modifications were done to the text to reflect changes recommended by the reviewers. 
One of the reviewers felt that the paper was more oriented towards lymphatic filariasis, than vector-borne diseases in general. We have addressed this. We have also provided new references (Ndebele et al., 2012 and Jamrozik et al., 2015) in relation to the ethical questions around the HLC. 
In the methods section, a new figure (Figure 1) has been created, identifying the study locations in Ghana. 
The methodology section has been expanded to provide detailed information on the human landing collection and the tent trap. 
In the results section, the caption of Figure 2 has also been modified to reflect the “average number of mosquitoes collected per month using the HLC and TT”. 
Table 2 has also been updated to present the communities collectors came from.
In the discussion, we attempted to give reasons why collectors preferred the HLC and perceived it as collecting more mosquitoes than the TT. 
In the acknowledgment, we recognized Harold Nyarko Osei, for the help in producing the map of the study areas.
All the Figures have been renumbered (Figures 1-6) due to the study map requested by reviewer 1.

See the authors' detailed response to the review by Seth R. Irish
See the authors' detailed response to the review by Chadwick Sikaala

Introduction

Vector-borne diseases remain an important threat to the health of the human population. These are diseases caused by pathogens in humans, and transmitted by mosquitoes and other arthropod organisms. It is estimated that more than one billion people get infected with vector-borne diseases every year, with more than one million deaths1, and many more suffering from permanent disability and morbidity. Among the most important vector-borne diseases in the world are malaria, onchocerciasis, lymphatic filariasis, dengue, yellow fever, leishmaniasis, chikungunya, West Nile virus, Chagas and more recently emerging infections such as Zika virus2.

Of all arthropods that transmit diseases, mosquitoes remain the best-known vectors, transmitting diseases such as malaria and lymphatic filariasis, two of the best-known diseases in Africa. Malaria for instance leads to an estimated 210 million cases and 430,000 deaths annually3, while lymphatic filariasis is responsible for an estimated 36.45 million infections, 19.43 million hydrocele cases and 16.68 million lymphedema cases4. While significant efforts and achievements have been made in the control of such diseases, through vector control such as indoor residual sprays (IRS), use of long-lasting insecticide nets (LLINs)5,6 and treatment of endemic populations7,8, there is a need to assess the effectiveness of these interventions.

The most direct timely measure of transmission (or the lack thereof) is through the examination of vectors for the presence of infective stages of the parasites responsible for the infection. To this effect, xenomonitoring (the examination of disease vectors for pathogens) serves as an important assessment tool9,10. However, in order to document that transmission has been interrupted, it is necessary to screen large numbers of insect vectors to assess their infection and infectivity rates. While pool-screen PCR methods have been developed that can efficiently screen large numbers of vectors11, the challenge of collecting large numbers of vectors remains. Several factors such as the placement of traps, use of baits, and the type of trap may influence the number of mosquitoes collected. The gold standard of collecting vector mosquitoes is the human landing method (HLC), which is ethically questionable due to the exposure of the collectors to infections12,13. As a result, modifications of this approach to involve a double-netted human baiting method have been designed.

A further challenge to the collection of large number of mosquitoes is the use of trained entomologists, which significantly increases the cost of the surveys14. To circumvent this challenge, this study opted for the use of community volunteers in the collection of the mosquitoes1416. Operation of the traps by community members themselves has many advantages. First, this would be much less expensive than if trained individuals were required to operate them, and second, this would permit the traps to be more widely distributed and to be operated for longer periods in each community than would be possible if trap operation were confined to traveling teams of trained individuals. Such a community-based operation of the traps has the potential of providing a much more comprehensive estimate of the intensity of transmission, both over time and space, than can be obtained using teams of trained individuals. The usefulness of community vector collection approaches has been demonstrated in Mexico17, and Togo18.

This study therefore sought to evaluate a community-based vector collection approach and to assess the performance of the double-netted human baiting method, the tent traps (TT) for the Anopheles vectors of lymphatic filariasis in Ghana.

Methods

Selection and sensitization of communities

The study communities were Akonu, Asemko and Aketenkyi in the Nzema East, Ellembele and Ahanta West Districts, respectively (Figure 1). All study communities are located in the Western region of Ghana, and the selected districts are lymphatic filariasis endemic. The Districts are approximately 300 km west of Accra, the capital of Ghana. The chiefs, opinion leaders and communities were informed on the purpose of the study, using the information document developed for the study19.

80406284-af2f-4f2e-93b8-36e6f26b4ce8_figure1.gif

Figure 1. Map of Ghana showing the three study sites and their districts.

Recruitment and training of community vector collectors

To enhance community ownership, the chiefs and elders were asked to identify individuals within the community who will serve as vector collectors. Thus, no strict inclusion or exclusion criteria were applied, so long as the collectors were deemed capable by the community. The vector collectors were either male or female, with formal or informal education. No prior knowledge in mosquitoes or mosquito collection was required from the collectors. The vector collectors were trained on setting up the TT (Figure 2), and collecting the mosquitoes using aspirators. Two traps were provided for each community, with two vector collectors per trap. They were also trained on mosquito collection using the HLC method.

80406284-af2f-4f2e-93b8-36e6f26b4ce8_figure2.gif

Figure 2. Setting the tent traps.

(A) The inner sleeping tent. (B) The outer tent.

Mosquito collection

The mosquitoes were collected by the volunteers, without supervision from the study team using human landing catches (HLC) and tent traps (TT). The collectors were advised not to use any repellants, perfumes or fragrances, alcohol or smoking during collection. The collectors were also rotated between collection methods. i.e. HLC collectors for the first collection slept in the TT for the second collection and vice versa. The procedures for the collections were as described below. For the HLC, two collectors were involved. The HLC collections were done outdoors under a shed or a porch. Collections were done from 20:00 till 03:00 hours. At each location, the two collectors sat close to each other and exposed their legs to the knee level to attract the mosquitoes. Each collector captured mosquitoes that landed on their exposed body surface using a test tube with the help of a torch light. The captured mosquito was transferred into a labelled paper cup. Hourly collections were done and different labelled paper cups were used for each hour of collection. After each hour the two collectors switched positions and continued with the collection.

The TT collections were also done outdoors in different locations from the HLC. Two locations of the TT were set, 20–30 meters apart in the same compound. For each, one volunteer slept on a mattress in the inner part of the TT and closed up the inner net. The outer net was raised slightly to enable mosquitoes fly in. This was also done from 20:00 till 03:00 hours. At dawn, the HLC collectors quickly assisted with collection at the TT when they are done. The outer net was released to prevent trapped mosquitoes from escaping. The HLC collectors entered through the outer net and collected trapped mosquitoes using aspirators into labelled paper cups. On days when the collection was prevented by rains, both HLC and TT collections were cancelled, and the collections rescheduled.

Collections were done from June to December 2017. Two TT and two HLC collections were carried out every month at a time suitable to the collectors, but at two weeks interval. On each collection day, the mosquitoes collected for each method were stored in a 50-ml falcon tube, provided to the collectors and labelled with all the information including the collection method and month of collection.

Once every two months, a member of the study team visited the communities to collect the mosquitoes to the laboratory at the Noguchi Memorial Institute for Medical Research, Accra where they were identified, counted and stored.

Evaluation of community xenomonitoring study: perspectives of collectors

The study also assessed the views of the community vector collectors, using a simple questionnaire designed for this purpose19. This was done to enhance future operational activities.

Ethical considerations

The study was approved (CPN 062/16-17) by the NMIMR IRB with Federal Wide Assurance Registration (FWA 00001824). Following community sensitization, verbal approval was obtained from the chiefs and elders of the communities. Written consent was also obtained from the vector collectors. The collectors were given prophylaxis as part of malaria prevention measures.

Statistical analysis

The number of mosquitoes collected was represented through graphs drawn in Microsoft Excel. The difference between the number of mosquitoes collected using the TT and HLC methods was assessed using the chi square test in IBM SPSS Statistics 20.0. Statistical significance was assessed at a p value ≤0.05.

Results

Results of mosquito collection

A total of 3363 mosquitoes (Table 1) were collected from June to December 2017 comprising; 1581 (47%) An. gambiae s.l., 1266 (37.6%) Culex spp., 6 (0.2%) Aedes sp. and 510 (15. 2%) Mansonia sp. An. gambiae s.l. was the only Anopheles species identified. A significantly (P<0.001) higher percentage of mosquitoes were collected using the TT (63%) compared to the HLC (37%). However, the number of Anopheles collected by the TT and the HLC was not statistically significant (P = 0.213). The average monthly collections also revealed higher collections by the TT compared to the HCL, with significant differences observed during the dry season months of August, September, November and December (Figure 3). Generally, the variation (range) in mosquito numbers collected each month was relatively smaller for the HLC (apart from June and October) compared with the TT (Figure 3).

Table 1. Mosquitoes collected as part of the trapping study in Ghana.

AkonuAsemkoAketenkyi
MethodSeasonMonthAn.
gambiae
CulexAedesMansoniaAn.
gambiae
CulexAedesMansoniaAn.
gambiae
CulexAedesMansoniaTotal
Tent trapRainJune491109310065000156
July46600573800138830296
August4722002479027640035298
September1739001563014814025222
Sub-total159681010521102831522360972
DryOctober308400355900600163377
November711300817500198600381
December1810400886100650055391
Sub-total553010020419500908602181149
Human landing collectionRainJune2550012180078600144
July33100834200105400268
August28000339019381010138
September033107321435308124
Sub-total86391010513112325614018674
DryOctober55660020180020088249
November175800151700180050175
December311400212600270025144
Sub-total103138005661004700163568
Total4035462047059815170812234593363
80406284-af2f-4f2e-93b8-36e6f26b4ce8_figure3.gif

Figure 3. Average number of mosquitoes collected per month using HLC and Tent Trap.

Error bars represent the minimum and maximum number of mosquitoes collected. HLC, human landing collection.

The general trend in the total number of mosquitoes collected reflects the influence of seasons on the behavior and the population of mosquito species, with the Anophelines and Culicines revealing opposing trends. The main collection peak for An. gambiae was from June to August, which coincides with the major rains and the beginning of the dry season. On the other hand, the main peak for Culex was during the minor rains and dry season months of October to December (Figure 4). A similar trend was observed in mosquitoes collected using the TT and HLC (Figure 5).

80406284-af2f-4f2e-93b8-36e6f26b4ce8_figure4.gif

Figure 4. Total number of mosquitoes and the species abundance per month irrespective of collection method.

80406284-af2f-4f2e-93b8-36e6f26b4ce8_figure5.gif

Figure 5.

Trends showing species composition of mosquitoes collected using (A) tent trap and (B) human landing collection.

Among the three communities where collection was done, the highest number of mosquitoes was collected from Aketenkyi and the least from Akonu (Figure 6). In Akonu though the number of mosquitoes collected from TT was generally higher than those from the HLC between June and September, the reverse was the case between October and December. Asemko showed higher numbers in TT than HLC in almost all the months apart from June and July, whiles Aketenkyi showed similar pattern except from June where HLC numbers were higher.

80406284-af2f-4f2e-93b8-36e6f26b4ce8_figure6.gif

Figure 6.

Frequency distribution of Anopheles gambiae s.l. mosquitoes collected from (A) Akonu (B) Asemko and (C) Aketenkyi, using HLC and Tent Trap. HLC, human landing collection.

Evaluation of community xenomonitoring study: perspectives of collectors

A summary of the demographic information of mosquito collectors and responses to questionnaire is shown in Table 2. There were 12 collectors involved in the study, three of whom were females. The age of the collectors ranged from 16 to 58 years with a median age of 34 years. Seven of the collectors had received primary/JHS education, 3 secondary education and the remaining 2 post-secondary education. Four of the collectors were farmers, 3 unemployed, 2 seamstresses, 2 students and 1 teacher.

Table 2. Details of the demographic information of mosquito collectors and their responses to questionnaire administered.

Individual responses to questionnaire
#SexAgeEducational
level
OccupationCommunityImportance of
mosquito study
Mosquito-borne
disease at study
area
Importance of
community
involvement
Preference
of collection
method
Willingness
to continue
mosquito
collection
Person to bear
cost of mosquito
collection
To volunteer
without pay
1M32SecondaryTeacherAketenchieTransmit
elephantiasis &
malaria
MalariaSave time and
cost
HLCYesResearch teamYes
2M58Primary/JHSFarmerAketenchieTransmit
elephantiasis &
malaria
MalariaSave time and
cost
HLCYesGHSYes
3M38Post-
Secondary
Not
employed
AketenchieInvestigation
of disease
transmission
Malaria &
elephantiasis
Motivation to be
part of fighting
disease
Tent trapYesGovernmentYes
4M40Primary/JHSFarmerAketenchieTransmit
elephantiasis &
malaria
MalariaTo have more
knowledge on
mosquitoes
HLCYesCommunity can
pay
Yes
5M16Primary/JHSNot
employed
AkonuTransmit
diseases
Malaria & choleraMotivation to be
part of fighting
disease
HLCYesGHSYes
6F25Primary/JHSSeamstressAkonuTransmit
elephantiasis &
malaria
Malaria &
elephantiasis
Save time and
cost
HLCYesGovernmentYes
7F21Primary/JHSNot
employed
AkonuTransmit
elephantiasis &
malaria
Malaria &
elephantiasis
Save time and
cost
HLCYesGovernmentYes
8M37Primary/JHSFarmerAkonuTransmit
elephantiasis &
malaria
Malaria &
elephantiasis
Motivation to be
part of fighting
disease
HLCYesGovernmentYes
9M17SecondaryStudentAsemkoTransmit malaria
and TB
MalariaTo have more
knowledge on
mosquitoes
HLCYesResearch teamNo
10F36Primary/JHSSeamstressAsemkoTransmit
elephantiasis &
malaria
MalariaMotivation to be
part of fighting
disease
Tent trapYesGovernmentYes
11M42Post-
Secondary
FarmerAsemkoTransmit
elephantiasis &
malaria
Malaria &
elephantiasis
Helps to accept
research
findings and
get some
income
HLCYesGHSYes
12M19SecondaryStudentAsemkoTransmit malaria
and TB
Malaria & TBSave time and
cost
HLCYesGovernmentNo

F, female; M, male; JHS, junior high school; HLC, human landing catches; TB, tuberculosis; GHS, Ghana Health Services.

The assessment showed that the mosquito collectors had a fairly good idea about the importance of mosquitoes in disease transmission especially malaria and lymphatic filariasis. This is exemplified by some of the responses below:

“They bite and bring diseases like malaria & elephantiasis, kill pregnant women and children cause us to spend a lot”

“To investigate the disease they transmit”

“They suck blood and contain parasites in them to give diseases”

“They are strange animals that bite and cause diseases such as high fever, rashes & elephantiasis”

Generally, the volunteers were aware of the main diseases transmitted by mosquitoes in their community. They all identified malaria as a disease transmitted by mosquitoes. In addition, others mentioned elephantiasis, with two individuals mentioning cholera and tuberculosis. On the importance/benefits of using community members for mosquito collection, the main views expressed were with the speed of collection, the willingness of the community and individuals to be involved in the study and feel a part of the disease elimination process, and the opportunity costs to the funders and collectors. These are reflected in the views below:

“When we are involved, we believe the results, it also helps to get some income and we feel part of eliminating the disease”

“We will help the GHS reduce cost of travelling to community and also get some income”

“We are able to collect fast. The team from Accra sometimes come late and we cannot do much…. The people also know us so they allow us into their houses”

“So, we can help ourselves to drive away mosquitoes to prevent diseases”

“Saves time and cost, no tension in sample collection, shows commitment level of community”

When asked which of the mosquito collection methods they preferred, 10/12 volunteers stated that they preferred the HLC. The reasons given for their preference were; the number of mosquitoes collected using the HLC, and the speed and ease of collection. The preference to the TT was due to the absence of mosquito bites. All the volunteers responded in the affirmative to the question of using the community to collect mosquitoes for the GHS as part of disease monitoring activities. However, 11/12 volunteers indicated that payment for the collection must come from the government or the Ghana Health Service. When asked whether they will consider collecting mosquitoes for the community without payment, 10/12 volunteers said “yes”. The main reasons given were to help protect the community, themselves and their families from infection. However, two of the collectors said they will not collect the mosquitoes without payment. Below are some of the views expressed:

“Disease is destroying our community & I need to help; I have been doing volunteer work already for NGOs”

“To help the community eliminate the disease and protect my children”

“I could get the disease and the cost will be more to me, also I will receive blessings”

“It is volunteer work and that is my contribution to the community”

“Already involved in a lot of volunteer work without pay”

The volunteers mentioned the need for more logistics such as consumables and better torch lights, malaria prevention using anti-malaria prophylaxis, improved methods for mosquito collection and enhance cohesion between the collection teams, as some of the ways of improving the mosquito collection and the work of the collectors. Complete answers to the questionnaire are available on OSF19.

Discussion

The surveillance of vector-borne diseases requires an assessment of the infection in the human population, whiles at the same time undertaking entomological surveillance to detect the infection in the vectors of the disease. Such is the plan for the post-intervention surveillance phase of lymphatic filariasis20. However, conducting entomological surveys especially in the context of elimination activities is considered expensive due to the limited resources21 and the high number of samples that may be required to assess transmission of the disease after interventions as well as the cost involved in the collection and processing of the mosquitoes14,16. Thus, there is the need for more cost-effective strategies for entomological assessments of infections within vectors of diseases.

In this study, the TTs were observed to be performing relatively better than the HLC (P<0.001). This study showed that the TTs collected higher number of mosquitoes compared to HLC and may be a better tool for the collection of a larger number of mosquitoes for xenomonitoring surveys, even though a majority of the volunteers thought the HLC was better. The preference of collectors for the HLC due to the number of mosquitoes collected could be linked to the high human-mosquito contact, and thus the perception of high mosquito abundance. Nonetheless in a largely unsupervised setting, the TT offers the advantage of collecting similar or higher numbers of mosquitoes, while helping reduce the likelihood of infection presented by the HLC.

Mosquitoes are often observed to be more abundant during the rainy season compared to the dry season22. This is due to the presence of more breeding sites created during the rainy season. In this study this was not the case from the collections as there was no significant differences in the numbers collected in both seasons. On the contrary, the data showed more mosquitoes collected during the dry season. This observation may be attributed to disruptions during rainy days. In fact, the collectors complained about their inability to set up the traps for long periods during the rainy season.

The seasonal changes observed in the distribution pattern of the mosquito species can be explained by their habitat preferences23. The numbers of An. gambiae during the rainy season was higher than the other species but low during the dry season. This is not surprising because An. gambiae prefer breeding in shallow and fresh water which are often abundant during the raining season24,25. Culex spp. on the other hand was higher during the dry season when fresh water is less abundant (Figure 6). This is could be due to its ability to breed in polluted breeding sources26,27, which are prevalent in Akonu and Asemko.

The assessment of the volunteers’ perspectives served to assess the level of understanding and importance of the task given to them as well as the feasibility of using such approach for future national programme implementation activities. The assessment revealed that generally, the collectors knew the importance of mosquitoes in transmitting diseases and were able to identify the main diseases that were locally transmitted within their communities. They appreciated the involvement of the community in the activities as this enhanced community ownership of the programme as well as providing some financial incentives to those directly involved in the collection (Table 2). For example, the community selection of ivermectin drug distributors as part of the Community Directed Treatment with ivermectin, improved access to the drugs and enhanced the community ownership of the activities28,29. The use of the community volunteers also provides opportunity costs to both the programme and the communities involved. To the national programmes, there are fewer expenses on the use of trained entomologists for vector collection and subsequent reduction in transportation and logistics costs. To the community volunteers, this provides some opportunities for them to earn some allowances, even though the work is entirely voluntary. However, the motivation of community volunteers is an important factor that determines the success of programme activities30,31. Recent use of community volunteers for large-scale monitoring activities have suggested that it is a useful strategy for programme implementation18,32. However, this needs to be tailored to country-specific situations.

In conclusion, the study revealed that use of community volunteers for the collection of mosquitoes as part of xenomonitoring purposes, can be an important strategy in the undertaking of monitoring of vector-borne diseases. However, further development of the strategies and assessments of the costs involved will be required in order to make this a public health approach to monitoring vector-borne disease interventions, and enhance community ownership and sustainability of the programmes. Though the use of community members for mosquito collection is promising, there is the need for further community education and training of community volunteers for xenomonitoring purposes.

Data availability

Underlying data

Open Science Framework. A community vector collection strategy for monitoring vector-borne diseases in Ghana. https://doi.org/10.17605/OSF.IO/C6BHP19.

Questionnaire data.xlsx contains the complete responses to each question of the questionnaire.

Extended data

Open Science Framework. A community vector collection strategy for monitoring vector-borne diseases in Ghana. https://doi.org/10.17605/OSF.IO/C6BHP19.

The project contains the following extended data:

  • Collectors’ questionnaire.docx (the questionnaire administered to the mosquito collectors).

  • Information document for mosquito collection using the tent trap.docx.

The data is available under the terms of the Creative Commons Zero “No rights reserved” data waiver (CC0 1.0 Public domain dedication).

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Boakye DA, Frempong KK, Ogoussan KT et al. Implementing a community vector collection strategy for monitoring vector-borne diseases in Ghana [version 2; peer review: 1 approved, 1 approved with reservations]. Gates Open Res 2019, 3:722 (https://doi.org/10.12688/gatesopenres.12933.2)
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Alongside their report, reviewers assign a status to the article:
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Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions

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