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Community awareness and neuroepidemiology of onchocerciasis-associated epilepsy in two rural communities in Cameroon

Community awareness and neuroepidemiology of onchocerciasis-associated epilepsy in two rural communities in Cameroon

Mundih Noelar Njohjam1,&, Mark Olivier Ngoule1, Emanuelle Mylene Tonga1, Annick-Sandra Jouonang Teugang1

 

1Department of Neurology, Cheikh Anta Diop University, Dakar, Senegal

 

 

&Corresponding author
Mundih Noelar Njohjam, Department of Neurology, Cheikh Anta Diop University, Dakar, Senegal

 

 

Abstract

Introduction: onchocerciasis is the leading cause of epilepsy in onchocerciasis-endemic communities. Our study aimed to determine the incidence, prevalence and community awareness of Ochocerciasis-associated epilepsy (OAE) in two onchocerciaisis-endemic rural communities in Cameroon.

 

Methods: we conducted a community-based cross-sectional study in two rural villages (Yangafock I, and Yangafock II) in the Mbam et Kim division of the Center Region of Cameroon. Door-to-door household visits were conducted to screen for individuals with epilepsy. OAE was defined using previously established criteria. Using an established questionnaire, we assessed community awareness of OAE.

 

Results: seven hundred and ninety-nine (799) peoples from 102 households (380 in Yangafock I and 419 in Yangafock II) were screened. Fifty-three (53) peoples, (33 from Yangafock I and 20 from Yangafock II) met the OAE clinical criteria. Two hundred and forty-nine (249) persons completed the community awareness questionnaire. For Yangafock I, the overall prevalence of epilepsy was 78.75 per 1000, while for Yangafock II, it was 47.7 per 1000. The five-year incidence of epilepsy was 23.8 per 1000 and 11.9 per 1000 for 44 Yangafock I and Yangafock II, respectively. The most affected age group was 20-29 years. Community members had a critically low level of OAE awareness and risk perception.

 

Conclusion: the high prevalence and a critically low level of public awareness underscore the need to raise community awareness of OAE to increase community engagement in the fight against onchocerciasis and its complications.

 

 

Introduction    Down

Onchocerciasis, a parasitic infection commonly known as river blindness, is a neglected tropical disease caused by the filarial worm Onchocerca volvulus, which is transmitted through the bites of infected blackflies of the genus Simulium [1]. It is an endemic disease, with the vast majority of cases located in Sub-Saharan Africa (SSA) [1,2]. Until recent years, blindness was the most feared complication of Onchocerciasis [1]. There is a growing body of evidence suggesting that onchocerciasis may induce seizures and epilepsy in people with onchocerciasis living in regions where the disease is endemic [3-11]. This form of epilepsy is known as Onchocerciasis-associated epilepsy (OAE) [3]. Although the underlying mechanisms of OAE are not fully understood, several hypotheses currently exist. One hypothesis suggests that the release of retinoids from dying microfilariae (the larval stage of the parasite) and their gradual accumulation to toxic concentrations in affected tissues may play a role [1]. The parasite may also induce seizures through the migration of microfilariae or the inflammatory response to the dying worms [1]. Two cohort studies done in Cameroon found that having a higher microfilarial load as a child is linked to a higher risk of getting epilepsy later in life [12,13]. Clinical criteria for diagnosing OAE have been developed and validated [3]. Table 1 summarizes the clinical criteria for OAE.

The burden of onchocerciasis and OAE in SSA is huge with significant economic and social impact, as it often affects young individuals, leading to disability, reduced quality of life, and significant healthcare costs [11]. Current evidence suggests that reducing community microfilaria load through ivermectin distribution can delay or prevent the development of seizures in onchocerciasis-infected persons living in onchocerciasis-endemic communities [7,14,15]. Several studies conducted in different countries in SSA have reported a significant reduction in the incidence of OAE after reinforcement of measures for onchocerciasis elimination, such as community distribution of ivermectin [11,14,15].

Ivermectin is an extremely effective antiparasitic drug that has been the main preventive strategy in the fight against onchocerciasis [1]. Mass drug administration with ivermectin has contributed to the tremendous progress made towards global elimination of onchocerciasis [1]. However, there are still several challenges that threaten efforts towards elimination, including poor community participation in elimination efforts. A lack of community participation, such as in taking ivermectin has been consistently reported as a barrier to the elimination of onchocerciasis and has been attributed to low community awareness of onchocerciasis [1,16,17]. Conversely, a high level of community awareness of onchocerciasis has been associated with increased uptake of ivermectin [1,16,17]. The scientific community is increasingly informed by new evidence on the existence of a causal relationship between onchocerciasis and epilepsy. However, the people who are affected by OAE or are at increased risk may not be aware.

Data on community awareness of OAE is sparse in SSA. The main objective of this study was to assess the level of community knowledge or awareness of OAE in two rural onchocerciasis foci in Cameroon. Additionally, we aim to describe the neuroepidemiology of OAE in these communities. Assessing and addressing OAE knowledge gaps could improve community ivermectin uptake and participation in the fight against onchocerciasis. As has been done in many communities where onchocerciasis is common, data on the incidence and prevalence of OAE could also push policymakers or local stakeholders to strengthen current strategies and start develop new ones to ensure elimination of the disease.

 

 

Methods Up    Down

Study site and population

The study was carried out in two rural villages situated in the Ngoro subdivision of the Mbam et Kim division in the Centre Region of Cameroon; Yangafock I and II (Figure 1). The Mbam et Kim division is known to be a hyperendemic focus for onchocerciasis [4]. This is probably because of the presence of fast-flowing rivers such as the Mbam river (which is the largest tributary of the Sanaga river), rivers Ngoro, Mbi and Kenkeng. The many rapids of the Mbam River as well as the Ngoro River are excellent breeding grounds for the black flies, as they provide the oxygenated water that is indispensable for the survival of the larvae of the black fly. Onchocerciasis prevalence is reported to be high in villages along the Mbam River. Yangafock I and II are two small rural villages that are located close to the Mbam River (Figure 1). Yangafock I has a total population size of about 380 while Yangafock II has a total population estimated to be about 1200. The main income-generating activity of the people is agriculture. Other income-generating activities include fishing, animal rearing, and sand extraction. Community-directed treatment with ivermectin is done annually but not regularly due to the non-availability of the drug, as reported by some of the inhabitants.

Sample size calculation

The following formula was used to determine the minimum sample size for the neuroepidemiology component of the study:

Where: n = the required sample size, Z is the Z-score representing the number of standard deviations from the mean, which is 1.96 for a 95% confidence level, p= the expected prevalence of the population, d= desired degree of accuracy.

A previous study reported a prevalence of 7.8% prevalence of OAE in a rural community in Cameroon [4]. We used 5% for the degree of accuracy (d).

With these assumptions, the minimum required sample size n = [[(1.96)² × 0.078(1-0-078)]/(0.05)²] for the neuroepidemiology component was 111 participants. We used the same sample size formula to calculate the minimum sample size for the community awareness component of the study but with the following assumptions:

We reviewed the literature for studies on community awareness of OAE, but we didn´t find any similar studies. We therefore estimated a 50% level of community awareness, 5% for the degree of accuracy (d) and 95% confidence interval. Based on these assumptions, the minimum required sample size n= [[(1.96)² × 0.5(1-0.5)]/ (0.05)²] for the community awareness component was 384.

Study design and period

This was a community-based cross-sectional study conducted from May 1st to May 31st, 2021. We obtained authorizations to conduct the study from each local chief before carrying out study activities in each village, detailing the objectives, procedures, and implications of the research. Each local chief assigned community relay agents to sensitize the entire village before conducting door-to-door visits. These relay agents also assisted the research team in gaining access to the study participants' homes. We conducted door-to-door visits in each village to identify cases of OAE and recruit participants for the knowledge assessment. During house-to-house visits, the study's objectives and procedures were explained to each household head or his representative, as well as the final respondent. Written informed consent was obtained from the head of each household, as well as the suspected case of epilepsy.

Identification of Onchocerciasis-associated epilepsy cases

The OAE cases were identified in multiple stages.

The first stage was the general screening for epilepsy. The general screening was done using a five-item questionnaire validated for epilepsy screening in tropical regions [18]. The five screening questions contained in the questionnaire were: have you ever lost consciousness and experienced either loss of bladder control or foaming in the mouth? Have you ever experienced absence or sudden loss of contact with the surroundings for a short duration of time? Have you ever experienced sudden, uncontrollable twitching or shaking of the arms, legs, or head for a period of a few minutes? Do you sometimes experience sudden and brief bodily sensations, see or hear things that are not there, or smell strange odours, etc.? Have you ever been diagnosed with epilepsy?

The second stage was interrogation and neurological/clinical assessment of suspected cases of epilepsy identified during the general screening by epilepsy-trained physicians. For history taking and general clinical assessment, a standard patient-clerking questionnaire was used to collect data on sociodemographic data, past medical history, clinical data, and physical examination.

In the third stage, the criteria for epilepsy diagnosis proposed by the International League Against Epilepsy (ILAE) were applied to all suspected cases of epilepsy [19]. Based on these criteria proposed by the ILAE, a participant was considered a case of epilepsy if they met at least one of the following criteria: presence of at least two unprovoked (or reflex) seizures occurring greater than 24 hours apart or a single seizure with a probability of recurrence of at least 60%, and having a diagnosis of an epilepsy syndrome.

Finally, the clinical criteria for OAE diagnosis (Table 1) were applied to ensure that only participants with OAE were included in the neuroepidemiology phase of the study.

Definitions

Incidence Rate= total number of new cases of disease / total population at risk x Population size.

Prevalence (%)= all cases of OAE per village / total number of inhabitants surveyed x 100.

Community knowledge assessment

During the door-to-door visits, we invited individuals from the communities to complete a knowledge assessment questionnaire to understand the community's general knowledge of Onchocerciasis-associated epilepsy. This was done using a random selection approach, in which community members were randomly chosen from each household visited. We used a randomization method that involved flipping a coin to determine which household member would receive an invitation to participate. In addition to the door-to-door recruitment, we also visited community schools and religious institutions to identify and recruit participants. This ensured that we included a representative sample of the community, including individuals of different ages and socioeconomic backgrounds. The randomly selected participants were given detailed information about the study and invited to take part in the survey. Those who agreed to participate were asked to provide written informed consent before enrolling in the study. Additionally, participants who were identified as cases of OAE in the neuroepidemiology phase were also invited to participate.

In the community awareness phase of the study, we assessed the level of awareness of community members who did not have OAE as well as those who were identified as cases of OAE during the neuroepidemiology phase.

Inclusion criteria for Onchocerciasis-associated epilepsy cases

To be included in the study, participants had to meet all of the following criteria: must meet the diagnostic criteria for epilepsy and OAE; the patient does not have any other identifiable cause of epilepsy; has willingly consented to participate; parental consent has been given to those aged less than 18 years; has been living in the study site at the time of onset of epilepsy. We excluded those who had epilepsy from other causes, as well as those with OAE who did not consent or were unable to respond to questions.

Inclusion criteria for participants for the community awareness assessment

To be included in the study, participants had to meet all of the following criteria: has willingly consented to participate; parental consent has been given to those aged less than 18 years; must have been a permanent resident in the study site since birth.

We excluded those who did not give informed consent or who were not able to respond to questions. We also excluded those who had recently moved to the study sites.

Ethical considerations

Ethical approval for this study was obtained from the regional ethical review committee for human research in the centre Region of Cameroon. All participants were informed of the study's activities and implications of participating in the study and informed consent was obtained prior to enrolment. The study was conducted following the principles of the declaration of Helsinki. No data that could identify participants such as names and phone numbers were collected.

Bias

The door-to-door approach and the use of community relay agents who knew the addresses of the different cases allowed us to reach every potential case of OAE in the communities. Also, we made sure that only people with OAE were included by carefully screening and evaluating each participant. This included looking at their medical records, talking to their family members, and strictly applying the criteria for OAE diagnosis. Lastly, the use of local translators to translate questions ensured that patients and their caregivers clearly understood questions before responding. Moreover, the random sampling approach that we used to recruit participants without epilepsy ensured that the sample is representative of the community and minimized selection bias.

Data management and analysis

Data was collected in the field using paper forms and entered into SPSS version 26.0. All data collection sheets were checked for correctness and completeness. We excluded incomplete forms from the data analysis. Descriptive statistics such as frequencies, mean and standard deviation were used to summarize categorical data. Continuous data were expressed as means ± standard deviation (SD). Frequencies and percentages were used to summarize data on prevalence and incidence. The level of statistical significance was set at p <0.05.

 

 

Results Up    Down

We visited 102 households and screened 799 individuals during the study period, resulting in the identification of 57 confirmed cases of epilepsy (33 from Yangafock I and 20 from Yangafock II). We assessed the fifty-seven cases neurologically and clinically, and confirmed 53 as OAE using the validated clinical criteria for OAE. Four cases had epilepsy from other causes, including complications from meningitis, perinatal injury, and cerebral malaria. Figure 2 summarizes the recruitment process for participants with OAE.

Sociodemographic profile

There was a predominance of male participants, and most participants were farmers. Primary education was the highest level of educational attainment for most participants. The majority of participants were single. Table 2 summarizes the sociodemographic data of the cases of OAE. One hundred and ninety-six (196) peoples, community members (mean age of 33.85 ± 14) completed the community awareness questionnaire, along with the 53 participants with OAE. Table 3 summarizes the sociodemographic data of the participants without OAE.

Most of the participants without OAE were females, and farming was the most common income-generating activity.

Prevalence of epilepsy

General prevalence

Fifty-three (53) persons (33 from Yangafock I and 20 from Yangafock II) met the ILAE criteria for epilepsy and the clinical criteria for Onchocerciasis-associated epilepsy. For Yangafock I, the prevalence of epilepsy was 8.7% (78.75 per 1000), and for Yangafock II, it was 4.8% (47.7 per 1000).

Age specific prevalence

The most affected age group was 20-29 years, and the prevalence of epilepsy progressively decreased from the 30-39 age group until >50 years. Figure 3 displays the prevalence by age.

Incidence

Nine cases in Yangafock I and 5 cases in Yangafock II had developed epilepsy within the five-year period (2017-2021) preceding the study, giving an incidence of epilepsy of 23.7 per 1000 and 11.9 per 1000 for Yangafock I and Yangafock II, respectively.

Clinical characteristics of epilepsy

Table 4 shows the clinical characteristics of epilepsy in the study population. Most participants had their first seizure between the ages of 5 and 10 years. Generalized tonic-clonic epilepsy was the most common seizure type, and most patients experienced seizures 2-3 times per month.

Community awareness of Onchocerciasis-associated epilepsy

A total of 249 participants (including the 53 participants with OAE) completed the questionnaire for the assessment of community awareness. Table 5 summarizes the community responses to questions on OAE. Most of the participants had never heard that onchocerciasis can cause epilepsy. The majority believed that the high prevalence of epilepsy in their villages was due to witchcraft. Blindness was the most commonly cited complication of onchocerciasis. Most of the participants with OAE did not know if onchocerciasis was responsible for the epilepsy they had. A substantial proportion of participants without OAE believed they were not at risk of developing epilepsy if they developed onchocerciasis. More than 60% of the participants without OAE stated that they would make more efforts to prevent onchocerciasis if they were aware that it causes epilepsy. Many of the participants said their attitude and behaviour towards people with epilepsy would change if they knew that epilepsies were caused by onchocerciasis.

 

 

Discussion Up    Down

We found a concerning low level of community awareness of OAE. While a lot has been done to increase awareness of the relationship between onchocerciasis and epilepsy among health professionals and scientists, these efforts may not have been translated into adequate community-level understanding. Our findings suggest that OAE knowledge has not yet permeated the communities most affected by it. This may act as a significant barrier to addressing the burden of this neglected tropical disease and its neurological sequelae. The implications of this finding are manifold. Firstly, a low level of awareness implies that many patients living with OAE may fail to seek appropriate medical care or support [20]. This can lead to no or suboptimal management of seizures and other symptoms and negatively impact their quality of life [20,21]. Moreover, a limited community understanding of the relationship between onchocerciasis and epilepsy can impede public health efforts to prevent and control onchocerciasis through vector management and mass drug administration [21].

Improving awareness of OAE at community level is thus crucial to the mitigation of the burden of not only OAE but also onchocerciasis [2,7,21]. Targeted educational campaigns, integrated within existing onchocerciasis and epilepsy control programs, could help bridge this knowledge gap at the community level [8,21]. Community outreach efforts should emphasize the causal link between onchocerciasis and epilepsy, as well as the availability of effective treatments and management strategies. Alongside these efforts, it is equally important to challenge the stigma and discrimination often faced by people with epilepsy in affected communities [7,21]. Integrating community education on OAE into existing public health initiatives could be a cost-effective and sustainable strategy [7,21].

We also found that a significant number of participants without OAE would change their attitudes and behaviours toward people with epilepsy if they knew the condition was linked to onchocerciasis. This suggests that increasing awareness could have a tangible impact on reducing stigma and improving social integration for those affected. Additionally, this highlights the need for a holistic approach that addresses not only the medical management of OAE but also the psychosocial and community-level factors that contribute to poor outcomes.

Ivermectin has been shown to effectively reduce the incidence of OAE as well as the frequency and severity of seizures in OAE in many onchocerciasis-endemic areas. A decrease in epilepsy prevalence with age-shift after ivermectin administration has been reported in previous studies [14,15]. In our study, participants with OAE did not believe that their seizure control could be improved by ivermectin. Knowledge of ivermectin's potential to prevent OAE could motivate increased compliance with mass drug administration campaigns.

The high prevalence of epilepsy in our study is consistent with findings from other rural communities in Cameroon [4,12,13] and other African countries where onchocerciasis is endemic [5-9]. The study sites' close proximity to fast-flowing rivers such as the Mbam, Ngoro, Mbi, and Kenkeng rivers puts the local population at a high risk of contracting onchocerciasis from black flies, the vector of O. vulvolus. Constant exposure of the local inhabitants to the high black fly biting rate can lead to increased viral load in the blood and an increased risk of brain injury, seizures, and epilepsy. A cohort study conducted by Chesnais et al. (2018) in the Mbam Valley showed that the risk of developing OAE later in life increased with a higher community viral load. Other studies conducted in the Mbam valley and other African countries, including systematic reviews with metanalysis [10,11] have confirmed the relationship between microfilaria load and increased risk of epilepsy. Another study in the Mbam and Sanaga river valleys of Cameroon reported a crude prevalence of epilepsy of 4.6% in one village and 7.8% in another, which is similar to the prevalence of OAE in our study [4].

The close proximity of Yangafock I to the Mbam River (Figure 1), which implies that the inhabitants of Yangafock I are closest to the black fly's breeding ground, could be the reason for the high prevalence and incidence of OAE in Yangafock I compared to Yangafock II. As a result, the village's inhabitants face a higher risk of contracting O. volvulus, leading to higher community microfilaria loads (CMFL), and consequently, a higher risk of developing epilepsy. Boussinesq et al. (2002) reported similar findings in a case-control study in the Mbam Valley. In the study, the researchers reported that the prevalence of epilepsy increased with increasing community microfilaria load and that the closer the village was to the Mbam River, the higher the prevalence of epilepsy [22].

The highest prevalence among youths between the ages of 20-29 years in our study is consistent with that reported by similar studies in Cameroon [4,22] and other African countries [5-9,11]. Youths aged between 20-29 years constitute the most active group in the study sites. They were actively involved in fishing, swimming, and sand extraction from the rivers compared to other age groups. These activities increase their exposure to black flies, which in turn increases their risk of fly bites, onchocerciasis, and OAE compared to other age groups. Furthermore, an inconsistent supply of medications often limits optimal treatment for epilepsy in rural communities. Patients might sometimes have the money to purchase the medications, but they are not available [21]. This lack of access to diagnostic services and specialized care hinders the ability to accurately diagnose and effectively treat epilepsy, resulting in a higher prevalence of the disease.

Evidence from our study underscores the need to improve community awareness of the relationship between onchocerciasis and epilepsy. Furthermore, our results strengthen the currently available evidence suggesting a causal relationship between onchocerciasis and epilepsy in onchocerciasis-endemic areas. Further studies to assess the ivermectin coverage and risk of transmission of onchocerciasis as well as the impact of ivermectin on the prevention and management of OAE in the study sites are warranted. The results from our study highlight the need to reinforce current strategies for onchocerciasis elimination and epilepsy management in rural communities.

Limitations

In our study, we did not determine the relationship between CMFL density and risk/severity of epilepsy. Additionally, no brain imaging tests were done to identify other causes of epilepsy. We, however thoroughly screened for the presence of other risk factors by asking the necessary questions from the participants, their parents, caregivers, or guardians during the interrogative phase. We also reviewed past medical records (where available) and performed thorough clinical assessments for each participant to rule out epilepsy due to other courses. We conducted this study in only two communities, which limits the generalizability of the findings.

 

 

Conclusion Up    Down

Despite being a significant public health problem in many communities, community awareness of OAE is very low. Raising community awareness is critical to reducing the impact of OAE in high-prevalence communities.

What is known about this topic

  • Epilepsy is a public health problem in onchocerciasis-endemic areas;
  • Onchocerciasis causes epilepsy.

What this study adds

  • Data on the neuroepidemiology of onchocerciasis-associated epilepsy in an onchocerciasis-endemic community that has not been previously investigated;
  • The low level of community awareness of OAE in onchocerciasis-endemic communities with high prevalence of OAE underscores the need for awareness-raising and education at community level, efforts to increase awareness of the causal relationship between onchocerciasis and epilepsy should not only be concentrated on the scientific or healthcare community but should also be directed towards communities where onchocerciasis is endemic;
  • Our study also shows that community engagement in the fight against onchocerciasis as well as community attitudes towards people with epilepsy in onchocerciasis-endemic areas can be improved if communities are educated about the causal relationship between onchocerciasis and epilepsy.

 

 

Competing interests Up    Down

The authors declare no competing interests.

 

 

Authors' contributions Up    Down

Mundih Noelar Njohjam: conception and design, acquisition of data, analysis and interpretation of data, drafting the article. Mark Olivier Ngoule, Emanuelle Mylene Tonga and Annick-Sandra Jouonang Teugang: conception and design, interpretation of data, critical revision of article for important intellectual content. All the authors read and approved the final version of this manuscript.

 

 

Acknowledgments Up    Down

We would like to acknowledge the different chiefs of the communities, the local inhabitants, and participants in this study for their collaboration and participation. We are particularly grateful to the participants with epilepsy for their willingness to participate in the study. We also appreciate the chief of the Mvoundou Baptist Health Center and his staff for their invaluable assistance and guidance in the communities.

 

 

Tables and figures Up    Down

Table 1: summary of proposed case definitions for onchocerciasis-associated epilepsy

Table 2: demographic data of participants with onchocerciasis-associated epilepsy recruited from Yangafock I and II villages from May 1st to May 31st, 2021 (N=53)

Table 3: demographic data of participants without onchocerciasis-associated epilepsy recruited from Yangafock I and II villages, from May 1st to May 31st, 2021 (N=196)

Table 4: clinical characteristics of epilepsy among participants with onchocerciasis-associated epilepsy recruited from Yangafock I and II villages from 1st to May 31st, 2021 (N=53)

Table 5: community awareness of onchocerciasis-associated epilepsy amongst participants with and without onchocerciasis-associated epilepsy recruited from Yangafock I and II villages from May 1st to May 31st, 2021 (N=249)

Figure 1: map showing study sites (encircled)

Figure 2: flow chart for the recruitment of participants with onchocerciasis-associated epilepsy

Figure 3: age specific prevalence of onchocerciasis-associated epilepsy cases

 

 

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