Onchocerciasis in the Meme River Basin

The NTD Roadmap indicates that onchocerciasis in all endemic regions is targeted for elimination by 2030, however current research indicates that control approaches in Cameroon require more focused assessment and action to realise these ambitious targets[1, 19, 20]. In the Meme River Basin ongoing control and thus progress towards, elimination of onchocerciasis remains a significant public health challenge despite over 15 years of annual MDA with >65% programmatic therapeutic coverage [7, 10, 21–23]. Recent coverage data from 20 communities in the Meme River Basin show that onchocerciasis prevalence remained 44.4% with only 5.9% of participants reporting taking Ivermectin ≥ 75% of MDA rounds [7]. Additional coverage data related to the Meme Riven Basin can be found within our associated publication by Forrer et al., 2021[7]. The persistence of onchocerciasis in South-West Cameroon highlights that a transition from control to elimination of this disease using MDA is complicated by multiple factors which are well established in the literature. These include the geographical overlap with the related filarial, Loa loa. This is a risk factor for serious adverse events (SAEs) which have negative impact on community perceptions of the safety of Ivermectin (which is commonly known as ‘Mectizan’ within the study communities), and ultimately acceptance and adherence to treatment [21, 23]. Furthermore individuals experience of side effects is strongly associated with uptake of Ivermectin [24]. Other community-based factors associated with the limited impact of MDA in this area include weakening of community participation within the planning of MDA activities and poor sensitization of community members [10, 22, 24]. Potential factors limiting community participation include top-down programme management which exclude communities in the organization and planning of health activities and low community awareness of the financial management of the programme activities [25]. Health system blockages include top-down planning, poor resource mobilization, inadequate staff at frontline health facilities, funding and transparency issues and transportation challenges, all of which negatively impact on the training, supervision and monitoring of the MDA process [10, 24, 25]. These health systems bottlenecks, individual, and community factors all contribute to insufficient treatment coverage and missed treatment rounds for population groups and individuals. However, research that brings together and explores the intersections between structural, environmental, social and contextual factors and the impact these have on onchocerciasis and health systems functioning in the Meme River Basin is lacking [22, 24]. Furthermore, studies tend to use survey techniques rather than large in-depth exploration of community views analysed through an intersectional lens considering age, gender, occupation and other factors which interplay to shape experiences [2]. Kamga et al (2016) and others state that socio-anthropological studies are needed to provide additional information on the intersecting dynamics of risks to exposure and re-infection, drug availability and acceptance to understand the persistence of the disease in this area [10, 15, 16, 22, 26]. Such evidence could support health systems and other sectors to respond and adapt NTD programmes such as integrated MDA, through being responsive to diverse and changing community needs.

Research context and approach

In this paper we review the control of onchocerciasis from different perspectives within communities, informed by the social ecological framework developed by Stokols (27) and further discussed by Gazzinelli, Correa-Oliveira (15). This framework allowed for a wider understanding of the influences on onchocerciasis experience and for making recommendations for more effective and equitable response towards managing and eliminating onchocerciasis, within and beyond the Meme River Basin in Cameroon. A social ecological lens considers the multiple levels of influence on health programmes including individual, intrapersonal, organisational, community and public policy and how these intersect with environmental aspects, social determinants, and disease specific contextual factors[27]. It is recognised that environment is a critical component of social determinants and that they are linked, however we have addressed these separately to illustrate key points. This model promotes the identification of key, often complex, issues which can lead to alternative strategies and recommendations for onchocerciasis elimination in persistently endemic communities.

We built upon and expanded the issues outlined by Gazzineli et al [15], who proposed four interconnected thematic areas for considering effective health interventions to address NTDs These include: 1. Social determinants, 2. Environmental considerations, 3. Multi-level health promotion interventions and 4. Context specific circumstances that affect disease occurrence. Furthermore, as suggested by Gazzinelli et al [15] we examine cross cutting issues of community participation and ownership, as well as gender dimensions of health and health seeking which must be considered in the evaluation of NTD programmes, such as MDA. We chose this framework for analysis as it became apparent during data collection that individual and collective behaviours, beliefs, environmental exposures, economic circumstances, including poverty, housing location and livelihood options and social factors such as age and gender all intersected to determine how onchocerciasis risk was perceived, acted upon and controlled (or not) through medicine uptake and other means. Fig 1 highlights these concepts, which will be expanded upon in the results (Fig 1). This research was conducted as part of a wider multidisciplinary study detailed by Wanji et al [7, 21] to consider alternative strategies for onchocerciasis elimination in the region. Here we report results from the qualitative element collected during the baseline phase of the study, and apply a social ecological lens to assess the effectiveness of current onchocerciasis programmes within the Meme River Basin in Cameroon[15, 27].

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Fig 1. Social-ecological approach for Onchocerciasis control.

https://doi.org/10.1371/journal.pntd.0009433.g001

We aim to highlight nuances of community practices and contextual realities that could be the difference between control and elimination in highly endemic communities such as the Meme River Basin, and make key recommendations for NTD implementers throughout the health system and their partners to consider in their aspirations to leave no one behind.

Ethical statement

This protocol was reviewed and approved by the Liverpool School of Tropical Medicine Research Ethics Committee (reference: 16–027), the Cameroonian National Ethics Committee for Research on Human Health (approval no. 2016/11/838/CE/CNERSH/SP), and the Division of Health Operations Research within the Cameroonian Ministry of Public Health (approval no. 631–03.17).

The objectives, importance and ethical provisions of the study were explained to the respondents with written and verbal consent obtained from literate and non-literate participants respectively before data was collected. Participants less than 18 years gave assent while their parents or guardians gave formal consent for them to participate.

Study design

Seventy-one (71) qualitative in-depth interviews were conducted in September 2017 and then analysed to understand the daily lived realities of communities and drug distributers of Ivermectin within the Meme River Basin including their current knowledge and attitudes to onchocerciasis and their behaviours in relation to transmission, prevention, and treatment with MDA. The data collection instruments were in-depth interview guides and an observation guide. The general community entry strategies used in this study were those described by Kengne-Ouafo et al. (2014, 2015) and outlined in Wanji et al [21].

Study site

This study was carried out in the Meme River Basin where there is still persistent transmission of onchocerciasis [8, 23]. The study site is located in the Rumpi Hills in the South West Region of Cameroon. The main feature is a mountain range characterised by a volcanic ridge. This ridge constitutes a watershed from which several rivers (Munaya, Meme, Mungo, Ndian, and Ube) take their waters. These fast-flowing rivers provide perennial breeding sites for the blackfly leading to continuous onchocerciasis transmission. The inhabitants of this area are in constant contact with the rivers and dense forest due to their socio-economic activities such as farming, fishing, sand mining, washing of clothes, bathing, and swimming. We purposively selected nine (9) communities from this site to be representative of the wider study (Fig 2. Source data: Field data and Global Forest Watch[28]), which included a control group where no intervention would take place, and two arms of an intervention group where different alternative strategies would be implemented[21].

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Fig 2. Map of the study region.

Source data: Field data; Ministry of Public Health Cameroon (https://www.minsante.cm/); and Global Forest Watch (2015) under license CC BY 04 (https://data.globalforestwatch.org/datasets/f5e89ec0b0704be0a5166234aa243e92). Projection system: GCS_Clarke_1880.

https://doi.org/10.1371/journal.pntd.0009433.g002

Study population

The participants selected for this study were community members and drug distributers (CDDs) residing within the Meme River Basin and who had lived for at least five years in the community (Table 1). CDDs are members of the community who are meant to be selected by the community for distribution of medications[29]. In our context, many CDDs also work on other health programmes, as detailed in our results section. Here the focus is on distribution of Ivermectin to the communities. Purposive sampling was used to select the respondents based on a sample frame guided by the principle of maximum variation (including age, gender and history of Ivermectin uptake) to ensure a wide range of perspectives were included [30]. The minimum age for all participants involved in the study was 15 years old.

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Table 1. Summary of data.

https://doi.org/10.1371/journal.pntd.0009433.t001

Data analysis

Data was collected in both English and Pidgin. The data in Pidgin was later translated to English and together with interviews conducted in English transcribed and saved in Microsoft Word 2013 documents. Field notes and observations noted during the interviews were summarized and used to support the analysis. Transcripts were exported into NVivo 11 Pro (QSR international, 2015) and coded following a hybrid process of inductive and deductive thematic analysis to interpret raw data [31]. This analysis technique involved a process of familiarisation with the data, developing a coding framework, coding transcripts and observations to the codes, charting and synthesising the data into themes and sub-themes [30]. The data were coded into corresponding NVivo nodes (or codes) that were later exported to Excel 2013 for further analysis and synthesis into final themes presented in the results section. This approach provided a rigorous and transparent process to document the analysis [32].

Contextual factors on health promotion interventions

Perceptions of NTD programmes

Historical factors shaped community engagement with health interventions, particularly those related to the management of filariasis. One of the women CDDs and a community member observed that even before the start of treatment with Ivermectin, people were taking a drug called “Notozine” (Diethylcarbamazine). This was considered as the drug of choice for the treatment of filariasis at the time and indicates a long history of onchocerciasis programmes within these communities. Respondents acknowledged a considerable change in their behavioural pattern towards ‘Mectizan’ through time. They outlined a number of key factors as contributing to their attrition from treatment adherence including; simple refusal to take the drug without a particular reason, absence during the distribution process, and fear of SAEs, such as death or hospitalisation.

Some participants reported that at first ‘Mectizan’ was distributed free of charge but now they are asked to voluntarily donate 100Central African Francs (XAF), which equates to 18 US cents/0.18 US dollars, before they are given the medicine. A few community members are unwilling to donate, stating that during the inception of the programme they were told that the treatment will be free of charge, and that is how they have been taking the medication over the years. This has had a knock-on effect, with many CDDs reporting that they must take the financial burden on themselves. A few also report that asking community members for money has decreased uptake of ‘Mectizan’.

Although some participants were positive and optimistic about MDA with older men reporting that it has helped in reducing the disease from the community, many women and men acknowledged that others do not like it because of the side effects which they say makes them sick:

“Like when the Mectizan are coming some people are very happy while others are so afraid that might be the sickness that is inside them which has not been disturbing them, once they took that Mectizan, it will disturb them.” (Man, CDD, 21–30 years).

Reported side effects mainly included swollen faces and legs. According to some interviewees only those with good experience of ‘Mectizan’ accept it while those that have experienced side effects, or have seen or heard others experience SAEs, will refuse to take ‘Mectizan’. This was mainly reported by young men and women, as well as farmers who fear Mectizan will prevent them completing their daily chores or will cause them harm.

Social determinants

Environmental determinants

Many participants reported that the most common type of insects in the community are the mbiti (blackflies), also popularly referred to within the communities as ‘mosquitoes’ or red flies because of their biting nature. When prompted by researchers, community members made a distinction between the actual mosquitoes and the onchocerciasis vector, blackflies, present around them. They noted that the blackflies were the most rampant in the communities and bite them everywhere on the body and are found all over the communities, at all times of the day.

Some men noted that, ‘mosquitoes’ (local name for flies which bite) are common because of a dirty environment and swamps in and around the communities. There seemed to be a general agreement among respondents that the blackfly is mostly common around water bodies like rivers such as the Meme River and its tributaries where people usually go and bathe and carry out household chores and socio-economic activities like fishing and swimming for recreation among children and adults. But it was noted that these flies fly from these rivers into the communities where they always bite people.

"It is mostly along the riverbanks we have a big stream here called River Obe, they are so many there. That is where most people go to bathe." (Man, community member, 41–50 years)

“Mosquitoes are mostly in the night and normally follow dirt, while the black fly which gives filaria is mostly around water bodies. Like the Meme River which we have here”. (Woman, community member, 41–50 years)

Men and women had different interactions with the river, which reflected their role in family and communities. Some women reported that, they are mostly exposed to fly biting when they go to the rivers to fetch water and to wash dishes or dresses. This role is mostly associated with women and children (both boys and girls) as a household duty. Likewise, most of the communities’ lack piped water but have boreholes and wells. However, these boreholes and wells often dry up during the dry season, explaining why many people go to the river to fetch water or to wash dresses and dishes. In addition, some participants reported that they get bitten by the blackfly when they go to the river to fish as a source of income or for subsistence especially during the dry season when there are no vegetables in the farm, so they tend to depend on fishing for food.

“…There are some people in the community, mostly women and some men whose main activity is fishing they have this kind of skin… They are much exposed to where those flies are” (Man, community member, 41–50 years).

“Yes. When a lady go to wash her dresses or that of her husband, as she is concentrating to wash her dresses the mbiti will come and bite her, without her knowledge”. (Man, CDD, 31–40 years)

“I even pity but those children who are always there, at times you see so many naked children around there. Some of the little children are there from morning till evening and that’s how the mosquitoes are sucking them.” (Woman, CDD, 31–40 years)

Men reportedly get bitten when accessing the river for leisure, especially when they are having a walk around the riverbanks or when they are sitting in their compound.

“During leisure like when people sit at the veranda… when fetching water or standing or walking by the riverbank” (Man, community member, 31–40 years)

Communities in the Meme River Basin are all located in the heart of the forest with farming of cocoa and other crops as their main economic activity. Most respondents reported that their residences are generally near their farms.

‘About six days in a week only on Sundays that I do not go to the farm….The first farm is about ten minutes, and then the other one is about fifteen minutes and the one furthest I use thirty three minutes.’ (Woman, Community member 51–60 years)

Most farmers build local ovens in their farms to dry cocoa before packaging it in bags for sale. This process takes a lot of time and sometimes the farmers spend days or weeks in the farm before returning to their home or community.

“When we are breaking cocoa to remove the seed from the shell. You know at that moment we are seated in one position and the mosquitoes (blackfly) will bite a lot… “(Women, community member, 21–30 years).

Most participants agreed that blackflies concentrate in farms but are also present in their homes (particularly in villages close to rivers, such as Kumu Kumu).

Health Seeking Pathways and decision-making for treatment

When seeking health care, there is an array of pluralistic providers to choose from including: health centre, hospital, medicine stores/community pharmacy and alternative medical or traditional practitioners and CDDs. Health seeking behaviours are hence complex, and treatment pathways are shaped by (perceived) costs and opportunity costs, trust, familiarity, embeddedness, distance, severity of symptoms and fear of operations. Despite participants in our study citing a preference for health care at the hospital or health centre when they are sick, cost of care acted as a key barrier, resulting in many choosing closer to community health care options (e.g. CDDs).

Recommendation 1: Understand and address the gender dimensions of disease experience through intersectional and gender analysis at a local level

Throughout the results and in the literature, we see that gender roles and relations shape all aspects of onchocerciasis elimination [34, 35]. The distribution of social roles by gender is highlighted here and demonstrated in terms of how differential risks are present for women and men, boys and girls as they interact with their environment in different ways for work, play and household tasks [34, 36]. Gender, sex and their intersections with other social determinants of health shape peoples’ vulnerability to and experience of NTDs, as well as their ability to access care and treatment [2, 37]. Gender and intersectional analysis which aims to understand how the dimensions of age, gender, poverty and other factors intersect with environment to impact transmission, re-infection and access to prevention and treatment is needed to better equip and accelerate localised responses to deliver equitable prevention, diagnosis, and treatment services in the Meme River basin [38]. This could be facilitated by applying gender analysis tools and frameworks [2, 39]. The importance of collecting and reporting sex disaggregated data, and utilising this to strengthen NTD programmes has previously been highlighted by Theobald et al., including gendered considerations for the workforce [2]. In our study both women and men CDDs expressed their motivators and demotivators for continuing with their role. Local level analysis should consider what strategies could better support CDDs and consider gender dimensions which may impact on a sustainable workforce.

Recommendation 2: Address environmental dimensions through intersectoral collaboration, integrated health promotion and education, vector control and access to safe water

The communities that live near to the rivers experience frequent fly biting everywhere and all the time; during economic, social and leisure activities. Adults in these communities are reliant on the rivers for everyday living, as well as being severely limited in their ability to avoid the water sources due to the close proximity of their farms and homes to the rivers. School aged children and young adults often spent long hours without protective clothing by the river increasing their risk. There are potential actions and solutions that could address some of the environmental conditions found here as bottlenecks to eliminating onchocerciasis. These include gender sensitive, frequent and ongoing health education to reduce risks and vulnerabilities, vector control strategies, intersectoral collaboration with sectors such as Water, Hygiene and Sanitation (WaSH), housing, planning and others and increasing access to safe water sources [40] which we explore further below.

Gender sensitive, frequent and ongoing health education to reduce risks and vulnerabilities

Health education, when integrated with other sectors/disciplines such as WaSH, planning, housing and vector control activities can be key to sustaining the benefits of medicines, and preventing infection [15]. Working alongside local organisations, religious institutions and other trusted community structures can improve access and uptake of information. Participatory methods to understand how different community groups interact with the structures around them would support these efforts, as done in Nigeria using transect walks and social mapping techniques [41]. For example, understanding working patterns and reaching specific groups of workers at their locations would be beneficial. Targeted and gender sensitive materials and messages for women, men and children could be researched and co-designed in collaboration with CDDs alongside a review of information, education and communication materials [41, 42].

Vector control

Vector control strategies are recommended in the bordering districts of the Centre and West Regions of Cameroon, as well as in other parts of the country with persistent high prevalence in order to reach onchocerciasis elimination [20]. Walker et al. [43] stress the importance of vector control in high-transmission settings as a complementary intervention strategy to MDA, especially where suboptimal responses to ivermectin are found. The Global Vector Control Response 2017–2030 proposes that for vector control strategies to be successful they need to be embedded in; strong inter and intra sectoral collaboration and action; engage and mobilise communities; have robust surveillance, monitoring and evaluation interventions; and use scalable and integrated tools and approaches[44].

Access to safe water sources

Whilst wells and boreholes were present in these communities, they were often dried out, meaning that community members (especially women) access the rivers where blackflies are breeding for everyday living. Whilst integration and collaboration of WaSH and NTD actors has been advocated for many NTDs such as Trachoma, Schistosomiasis, Lymphatic Filariasis and Soil Transmitted Helminths [45–48] this research suggests that further exploration is needed for how WaSH integrated strategies may reduce risk and exposure to onchocerciasis, particularly in areas which remain endemic despite more than 15 years of MDA. Furthermore, in these communities, visual impairment and blindness (whilst reduced in prevalence) remains a concern. Therefore, accessible safe water and sanitation for these communities is also needed [48].

Recommendation 3: Assess and respond to context specific social and livelihood factors and barriers to uptake of MDA in policy and practice

In accordance with other studies, farmers expressed caution to accepting medication due to fear of SAEs and side effects which will have economic consequences in being unable to work or needing further treatment[7, 16]. In these regions, historical memory of SAE potentially linked with co-endemicity of Loa loa, may heighten fear of associated reactions, and lead to reduced uptake of MDA [7, 23, 49]. Adequate support and management strategies for potential or perceived side effects should be considered [7].

Furthermore, communities migrated for work meaning they were often absent during distribution times, and social barriers to accepting Ivermectin such as alcohol use and related sales will all have an impact on elimination goals. Small changes that respond to context specific social and economic barriers may be the difference between success and failure of elimination efforts. Suggested adaptations to NTD programmes that could be negotiated with donor and implementing partners, to tackle some of the challenges related to these social determinants include being less stringent about MDA timings or further flexibility in the reporting deadlines; in campaign structure so that specific populations who are currently missed can be reached outside of campaign periods, through for example, some medicines being left in health centres to allow for longer term ‘mop up’ or repeat visits strategies[16].

Recommendation 4: Establish disease management, disability and inclusion services in communities that link with existing health system and social infrastructure and ensure a significant focus on stigma reduction activities

Although this research aimed to understand bottlenecks for MDA, the data revealed that many community members are still living with severe onchocerciasis symptoms, including stigmatising skin conditions and eye problems. This highlights that disease management, disability and inclusion strategies are also needed as well as preventative strategies. Prevention strategies should also prioritise the inclusion of people experiencing morbidity and disability. However, in considering disease management, disability and inclusion strategies, it is important to understand how and when different community members access health care, the values placed on different health providers (and why), and the implications this has on a specific disease within a given context. Understanding how relational gender roles intersect with other social factors and wider determinants of health, within specific contexts, and how they may influence health seeking pathways is important [35, 39, 50], and should be considered in all NTD programmes.

This research exposed the range of formal and informal health providers that communities accessed, and the influences on decision making when seeking care. These were related to trust, convenience, cost, travel limitations and balancing the benefits of treatment against reductions in the ability to earn a living. These insights have important implications for all health programmes, including MDA, disease management, disability and inclusion and health promotion strategies.

Furthermore, delays in seeking health care were due to inaccessibility of health facilities, but also fear of associated economic and personal costs of seeking care. Within this research, community members expressed the stigmatising effects for people living with onchocerciasis in the Meme River Basin. Research on NTDs and stigma in Liberia has demonstrated that for people living with NTD morbidity and disability, it was socially acceptable to have initial sickness, however as their illness became more permanent, people described significant negative impacts on their mental-wellbeing, including depression, anxiety and suicide [51]. This delay in health seeking behaviour until symptoms are severe, coupled with limitations in MDA uptake means that preventative strategies alone are not sufficient, and that case detection and disease management strategies are required to adequately complement preventive chemotherapy interventions [43, 51, 52]. Inclusion of people with disability within prevention campaigns is also essential in reaching elimination targets.

Recommendation 5: Assess potential exploitation of community members and CDDs to ensure financial burden does not rest with community members or CDDs

Farming communities are sometimes inaccessible, especially during the wet season, and some respondents reported that they would stay for long periods on their farms. This limits who can be reached by traditional house to house distribution methods and highlights the need to employ new methods of medicine distribution which are context specific, such as fixed-point distribution [16, 53]. CDDs and health facilities could be left with medicines for those who return from work, however current donor restrictions limit this, which places additional burden on CDDs [16]. CDDs still lack sufficient resources to do their roles, such as umbrellas and boots which are needed to reach some communities in order to increase coverage, nevertheless even with appropriate resources this involves long treks, which impacts of on CDDs’ time and other economic activities. Furthermore, the functioning of CDDs as volunteers, who live and work in some of the poorest communities in Cameroon, risks exploitation and potential exacerbation of social and gender inequities.

The financial and resource challenges faced by CDDs in MDA programmes identified here confirms a well-established evidence base beyond Cameroon, including out of pocket spending, transport restrictions and resulting physical and mental stresses from working in challenging environments when delivering medicines [54, 55]. Yet these reported challenges persist. CDDs play a critical role in NTD programmes, but relying on volunteerism, without adequate enablers and incentives is not a sustainable solution, and the international community have a responsibility to promote equitable solutions to the control and elimination of NTDs and to ensure that community members who want to support their communities to deliver medicines are not exploited.

As seen here, some CDDs are sacrificing food to deliver medicines and refer to the work as a ‘type of slavery work without payment’. This clashes with SDGs and should not be ignored as we move forward to achieve UHC. Whilst community ownership is paramount to the success of MDA [56, 57] this does not mean that the financial burden should rest with community members and CDDs, and highlights the need for well-funded, sustainable programmes that respect the wellbeing of volunteers. Duamor et al (2017) highlights that renumeration for CDDs was initially provided through the government and a shift in responsibility to communities to compensate this cadre occurred in 2013, however communities were not aware that government payments had ceased and were reluctant to support CDDs, possibly suspecting CDDs are asking for double remuneration[10]. Our results and published literature show that under funding for the NTD programme is a long-standing issue which needs urgently addressing and actions put in place to address this issue. Furthermore, a recent review, including evidence from Cameroon, emphasised that despite a reliance on CDDs to implement national NTD strategy, there is limited guidance or delineation of what this should look like in practice, such as with motivational support for CDDs. The lack of policy and procedure in this regard impairs the effectiveness of national programme strategy[29].

Limitations

We experienced some challenges during data collection, including being unable to reach one community (Metoko Bekondo) due to inaccessible roads. This highlights the importance of consideration of environmental factors, which can have a significant impact on geographical coverage for elimination strategies. Interviews were not conducted with community members who are ineligible for MDA with Ivermectin (such as pregnant women), due to limitations in recruitment strategies. Inclusion of these individual perspectives would strengthen alternative strategies to reach ineligible populations and should be considered in subsequent research. In addition, interviews were not conducted with health systems actors at this stage. Future research should engage Ministries of Health and other health systems stakeholders to communicate the programmatic challenges found here and engage them in joint solution development as discussed elsewhere [42, 58]. Cost analysis was not conducted as part of this study; however, we recognise that this should be considered in any further research that seeks to implement and evaluate our recommendations.