Introduction

Cysticercosis is a neglected tropical disease (NTD) caused by infection with the metacestode larval stage of Taenia solium and is associated with heavy public health and economic burden in marginalized areas of Africa, Asia, and South America [1,2]. Neurocysticercosis is a major cause of acquired seizures and epilepsy, and a recent study showed a high prevalence of cysticercosis in people with epilepsy in Rwanda [3].

Rwanda has a fast-growing pig production industry dominated by smallholder farmers who raise pigs for rapidly available income and to get manure for crop production [4]. Increases in smallholder pig production and pork consumption in sub-Saharan Africa are often associated with the emergence of porcine cysticercosis and, consequently, taeniasis and human cysticercosis [5]. Cysticercosis is known to be prevalent in pigs [6] and humans in Rwanda [3,7], and an analysis of pig value chains in Rwanda [4] showed sanitary practices embedded in the community to be inadequate, possibly due to various factors including lack of knowledge. The Rwanda strategic plan for NTDs highlights the lack of robust community awareness activities that would disseminate information on available preventive measures for cysticercosis [8]. Therefore, there is a need for additional methods targeting behavior changes through education.

Community health workers (CHWs) are considered by the World Health Organization (WHO) as important players for providing universal health coverage, especially to the most marginalized populations of low- and middle-income countries (LMIC) [9]. In Rwanda, the CHW started in 1995 after the Genocide against the Tutsi to respond to the unavailability of health infrastructures and enough health professionals. CHWs were elected by the community primarily during the monthly nationwide community service on the last Saturday of every month. CHWs must meet a few criteria, including the ability to read, calculate, and write, being from the community they are willing to serve, and serving as volunteers. In addition, they must not be a community leader or receive any remuneration from any health facility. They must be between 20 and 50 years old and have the community trust as an honest and reliable person [10]. In each Rwandan village (aggregation of about 50–200 households), three CHWs are designated. A pair of female and male CHWs known as agents de santé binôme which ensures integrated community case management of childhood illnesses, and a female CHW called Assistante Maternelle de Santé (ASM) taking care of maternal and newborn health services [10]. In Nyamagabe district, a 4^th CHW focuses on health promotion.

CHWs receive a three-month initial training; however, the training content, duration, and frequency are limited by available funds.

Since their deployment in 1995, CHWs have been at the center of important health-related achievements such as reduction of under-five and maternal mortality, improved family planning and vaccination coverage, as well as reduction of HIV/AIDS, malaria and tuberculosis [11,12]. Therefore, they could have an important role in tailored health education interventions for T. solium especially as education is increasingly being validated as an effective tool that complements other control and elimination programs [13,14].

The Vicious Worm educational tool (TVW) original English version, https://theviciousworm.be) was developed in 2014 by the University of Copenhagen [15]. TVW contains structured information on cysticercosis/taeniasis intended to support the training of a wide range of stakeholders ranging from school-age children to policymakers. Versions also exist in other languages spoken in Africa such as Swahili [16]. The novel digital-based tool is free and can be easily downloaded to smartphones or computers for teaching or self-study sessions. TVW has been shown to increase the knowledge of cysticercosis in pork supply chain workers and primary school children in Zambia [17–19]–but has not previously been tested in community health workers. The aims of the current study were to assess the baseline knowledge about cysticercosis in CHWs in an endemic area of Rwanda and then to evaluate the usefulness of the Kinyarwanda version of TVW for knowledge acquisition and retention.

Materials and methods

Study area

Rwanda is a low-income country located in East Africa. It has a population of 13,246,394 and is one of the highest densities in Africa, with 501 inhabitants per sq. km [20]. Rwanda has a decentralized governance system designed to promote good governance, national development, and service delivery. Hence, the nation is geographically split into five provinces, including the City of Kigali. The provinces are subdivided into 30 districts. Furthermore, these districts are divided into 416 Sectors and further into 2,148 cells and 14,837 villages. This study was conducted in Nyamagabe, one of the seven districts of Southern Province, Rwanda (Fig 1). Nyamagabe has an area of 1090km² with a total population estimated at 371,501, comprising 52.4% women and 47.6% men. The population is distributed in the district’s 17 sectors, 92 cells, and 536 villages, with an average density of 441/km² [20].

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Fig 1. Map of Nyamagabe district and the two targeted sectors (QGIS Ver. 3.28—CC-BY license 4.0.).

The layers are freely accessible from https://www.diva-gis.org/datadown and can be shared under CC-BY license 4.0.

https://doi.org/10.1371/journal.pntd.0012140.g001

Previous research highlighted sanitary risks that prompt the prevalence of cysticercosis and taeniasis in the area [4]. In addition, hospital records showed laboratory-confirmed cases of adult tapeworm infections in 236 and 334 patients in 2018 and 2019, respectively. This, coupled with the importance of pig production in the area, calls for interventions aiming at improving the knowledge on cysticercosis with the assumption that increased knowledge would trigger improvement in attitudes and practices and impact the disease endemicity in Nyamagabe.

Results

Knowledge of taeniasis/cysticercosis

Originating from a T. solium endemic area, all participants had already heard about or seen taeniasis/cysticercosis. Of the total, 18.4% reported that either they or a family member had experienced Taeniasis. In addition, 78.8% had seen cysts of T. solium in a slaughtered pig carcass, and 38% did not recall any specific measures such as meat condemnation, taken on the infected carcass (Table 1).

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Table 1. Demographic profile of Community Health Workers that participated in the three VWT testing phases (N = 206).

https://doi.org/10.1371/journal.pntd.0012140.t001

The median score before the training was 15/21 (71.4%), with the participants individual scores ranging from 2/21 (9.5%) to 21/21 (100%). The detailed results of the study participants are shown in S3 Table.

The CHWs’ sector of origin was significantly associated with knowledge at baseline (p < 0.001), with median scores of 13.5/21 (64.3) in Tare and 15/21 (71.4) in Kibirizi. There was no other significant association across the participants’ demographic groups.

The score improved significantly to a median score of 19/21 (90.5%) after the training (p < 0.001) and was maintained at the same level (90.5%) four weeks later (p < 0.001). The score ranged between 15/21 (71.4%) and 100% immediately after the intervention; and 16/21 (76.2%) and 100% at follow-up (Fig 2 and Table 2).

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Fig 2. Percentage of overall score obtained for the three evaluations done.

https://doi.org/10.1371/journal.pntd.0012140.g002

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Table 2. Effects of the TVW on Knowledge Acquisition and Retention among Community Health Workers in Rwanda.

https://doi.org/10.1371/journal.pntd.0012140.t002

When the score is broken down by themes evaluated, general aspects of cysticercosis scored 75.1% at baseline and increased to 83.8% and 82.7% at post and follow-up, respectively. For taeniasis-related questions, 87.2% of correct answers were recorded at baseline, and the score improved to 97.8% and 98.5%, respectively, for the post and follow-up sessions.

For aspects related to human cysticercosis and neurocysticercosis, 67.2% and 28.8% of correct answers were recorded at baseline, respectively. The knowledge related to the two aspects was increased after the training, and participants registered 97.1% and 77.9%, and the scores were sustained at 4-week follow-up with 99% and 72.6%, respectively (Table 2).

Participants had generally good knowledge on taeniasis, but much lower levels of knowledge on human cysticercosis, especially neurocysticercosis. For example, only 63/206 (30.6%) of participants could correctly answer whether humans can get cysticercosis. Correct answers increased with 200/206 (97.1%) at post-training assessment and 206/206 (100%) when the same question was asked at follow-up. Similarly, only 31/206 (15%) of the participating CHWs could accurately define neurocysticercosis. The proportion of good answers improved with 204 (99%) and 197/206 (95.6%) at post- and follow-up evaluation, respectively. Moreover, only 14/206 (6.8%) participants could tell how a person can get neurocysticercosis compared to 177/206 (85.9%) and 150/206 (72.8%) participants at post- and follow-up, respectively.

1. TVW promotes education and comprehension

The participants reported that TVW was informative, precise, and coherent. They found that the tool had various concepts about taeniasis, porcine cysticercosis, and neurocysticercosis that were new to them and yet explained in simple terms using their native language.

CHWs acknowledged that the most striking finding was that humans could also suffer from cysticercosis and neurocysticercosis.

"The part of the tool that was most useful for me was where I learned the difference between porcine cysticercosis and human cysticercosis. This was the first time I learned that humans can also get cysticercosis. That part was useful to me, especially when teaching it to someone else in my village; they were very curious and happy to learn it."

The tool provided knowledge and confidence to the participants, and they intended to use it against myths and misconceptions about cysticercosis. The tool is helpful as a guide to teaching others and ensures effective dissemination of knowledge within rural communities. It is easy to navigate with a good flow, has well-structured successive topics, and its visual contents and short stories encourage the reader to progress their reading and promote learning.

"The training also helped me; for example, in my village, we learned that eating poorly cooked meat can infect you. We also learned that not using the toilets appropriately and allowing pigs access to human faeces exposes them to being infected with T. solium eggs, thus acquiring cysticercosis. In addition, we learned that eating vegetables we get from the markets without washing them well can infect us and get neurocysticercosis".

"I will use the tool to teach the community about cysticercosis preventive measures. In my village, when a CHW is given an opportunity to speak, they say they will share the educative materials they gained from the tool. We will teach the community members how to look for signs of cysticercosis in a pig and mobilize them to destroy the carcass if a pig is slaughtered and found to have cysticercosis. We will convey the message that infected pigs should not be eaten under any circumstances".

"People from my village get curious to read the tool when they see the images and short stories. For example, the story of someone who goes to buy a pig and asks the owner of the pig to first test for cysticercosis by checking the tongue."

A CHW provided further explanations on the widespread lack of knowledge in people working along the pig value chain and stressed how the tool could help to address some gaps:

"I once went to a pig slaughter slab to train, and they all said, "We are done; we didn’t know that cysticercosis is inside the meats; we thought it only exists on the tongue. We never thought it could also be in the muscles." The tool taught us that cysticercosis can exist in any body part of the pig."

2. TVW teaches proper pig husbandry for socio-economic development and the reduction of health risks

The CHWs reported that TVW prompted changes whether themselves, members in their households, or their communities after learning from the tool. The tool enlightened them about the dangers of cysticercosis as well as the risks associated with poor pig farming practices and poor hygiene practices on their health. They learned that inadequate practices are responsible for the health problems witnessed within their communities. This inspired them to be ambassadors of change in the practices within their communities.

To highlight the above point, one CHW reported:

"I learned that the best way to build a pig pen is to put planks on the floor and to provide a covered roof so that pigs can find a shed away from the sun. I also learned how the pen should have a place for feeding and where to put water. Lastly, I also learned not to release pigs because that is how they get infected."

The tool also provided knowledge on how best to ensure pig husbandry for a profitable business. A participant explained:

"You see, now I know that if I want to start a project on pig farming, I will look for good breeds and try to find where I can get healthy pigs that are not infected by cysticercosis. I also know good farming practices like building a good pen for the pigs and not letting them roam freely because it could lead them to contracting cysticercosis."

3. Digital literacy and access are key to the optimal use of TVW

The participants consistently raised digital illiteracy as a challenge they faced during the time they were attempting to use TVW. Most of them mentioned that they had no previous experience using a smart device, thus being stuck at every step as they tried to navigate through the tool. However, they mentioned that when they were facilitated, the navigation of the tool turned out to be easy, and they were able to lead their own revision of the materials independently. They also recommended the addition of more audiovisuals to each section of the tool to serve illiterate audiences. Furthermore, the participants expressed the need for regular workshops for continuous learning. Other recommendations included scaling up the implementation of the tool to educate the many communities in Rwanda and other countries.

To show the need for expanding the training to other actors and areas, participants explained:

"It would be very important to other health care providers elsewhere in the country because even ourselves we did not know about this. Therefore, it would be important to them and their people."

"Yes, like in Cyangugu [south-west Rwanda], there are a lot of pigs; I don’t know any other place with a lot of pigs, but the tool can also be used there and generate a positive impact."

In the absence of smartphones, they suggested the provision of hard copies of the tool in the form of a booklet to facilitate them to revise the materials while they are in their homes. They reported that a well-printed booklet would help them to quickly disseminate the information since most of them do not own any kind of smart device through which they can access the tool regularly.

"The way to improve this tool is that you would make it into a booklet so that my colleagues and I can easily access it, memorize the content on respective pages and use it comfortably."

Discussion

Health education can be an excellent weapon to support the elimination of T. solium [13,22] as a public health problem. CHWs are essential actors in healthcare systems, and they are the closest professional group to the population. They can act as agents of communities’ behavior change in Rwanda when they are effectively trained with the proper knowledge and given the right tools [23]. Community Health Workers are essential members of the community that can drive change through participation in awareness campaigns, early detection of disease symptoms in the community (on people and animals), as well as serving as a vessel of prevention and response information to the public health governing bodies. To be able to do so, the CHWs need to be trained and provided with adequate information that enables them to communicate effectively and without ambiguity, and to continuously improve their skills through continuing professional development.

The current study recruited CHWs in a cysticercosis-endemic region in the district of Nyamagabe in southern Rwanda. The overall baseline knowledge about several aspects of T. solium biology and public health risk was good, with higher scores associated with questions related to general knowledge, porcine cysticercosis, and taeniasis. However, participants scored poorly on questions about human cysticercosis and neurocysticercosis, highlighting the clear need for further training. Knowledge of porcine cysticercosis is generally good in the local population of endemic areas [24,25] as also shown here. This is not surprising because 83.5% had reportedly seen T. solium cysts in slaughtered pigs, while 18.4% of the participants had had Taeniasis (infection with the adult worm in the gut). However, quite a high proportion of participants were confused about the details of how pigs acquire infection: more than 40% (87/206) thought that a pig could acquire cysticercosis after mating with an infected pig, while 44% (90/206) believed that some pigs are born with the disease.

Despite the participants’ quite good knowledge of porcine cysticercosis and taeniasis and their experience with the parasite, specific knowledge about human cysticercosis and especially neurocysticercosis was lacking. This pattern has been observed by other studies carried out in India, Mexico, Kenya, and Tanzania [14,19,24,26–29]. The life cycle of T. solium is complex and can be difficult to understand and explain [15], especially as this parasite is associated with three related conditions: porcine cysticercosis, human taeniasis and human (neuro)cysticercosis, and with both environmental transmission and food-borne transmission elements. These details are often confusing for the public and may appear even more complex when new learners hear that human cysticercosis can evolve into neurocysticercosis and go on to cause symptoms which include epilepsy.

Knowledge of the disease was greatly improved in all those trained with TVW tool, at least over the time scale which we assessed, as has been found in other studies in Tanzania [19] and Zambia [17,18] where TVW tool was used in health education. At our follow-up, the acquired knowledge was maintained, however as this was only after 4 weeks, there is a need for longer term follow-up.

As a digital-based tool, TVW has the advantage of conveying standardized messages that can be adapted to different levels from the community to policymakers. As reported by our own participants, the tool has the advantage of being visual with easy-to-understand messages. Also, participants commended the inclusion of non-directly human health-related information, such as husbandry practices and economic aspects behind properly keeping pigs. Pig production is a mechanism of saving for many smallholders in Rwanda and other countries [4,30]. Thus, health education should include aspects that attract the interest of the community using real-life experience as part of the routine life of the trainees. In addition, using standardized message helps in avoiding unintended consequences such as associating epilepsy with pigs and thus deterring people from engaging in safe pig production.

The digital educational tools could, however, be challenging to operate, especially in rural areas where prior experience using smartphones is lacking. This was a consistent report from the study participants who seemed intimidated by the tool at the start of the training, although they got better at using it throughout the training. A previous study [23] that investigated opportunity costs and benefits among CHWs reported that some CHWs suggested that receiving smartphones would help them submit reports via the Internet, thus cutting transportation fees. In fact, if provided, smartphones can also be used for CHWs self-trainings and during their involvement in community awareness activities, using an educational tool like TVW. Phones are increasingly considered essential tools for a community-based surveillance system [31]. Hence, equipping community members such as CHWs could provide additional tools for community interventions, including awareness campaigns on health issues such as T. solium. There have been efforts aiming at enhancing CHWs access to smartphones to boost healthcare service [32,33]. With various initiatives that provide CHWs with phones, digitalization is expected to improve with time.

Conclusion

This study confirmed a low level of proper understanding of T. solium transmission cycle, even in an endemic region. Using TVW, we demonstrated that knowledge can rapidly be improved and maintained in a short-term period. CHWs are essential actors in Rwanda’s health systems and are part of the key cadres of staff who could be involved in the elimination of NTDs in Rwanda. Therefore, equipping them with proper knowledge of the transmission and prevention of diseases is an essential aspect of the disease response mechanism. Including community animal health workers and community workers in charge of water and hygiene would also be important. Health education using TVW has proven effective in providing T. solium knowledge acquisition among CHWs and should be considered in integrated control programs.

Supporting information

Acknowledgments

We would like to acknowledge all the Community Health Workers from Kibirizi and Tare sectors who took part in this training/study. We are grateful to data enumerators for their participation in data collection during this study. We thank Nyamagabe District authorities for providing the necessary authorizations to conduct the study. We are also grateful to the District Directorate of Health, which was crucial for accessing the Community Health Workers.