Neurocysticerccosis (NCC) is the hematogenous inversion of the central nervous systems (CNS) with the cysts of Taenia (T) solium pork tapeworm and presents serious public health problems in endemic region (Deckers and Pierre, 2010; Goitra et al., 2011). The condition arises from a two-stage development cycle between the pigs and humans when infected with cysticerci (Kungu et al., 2017). The first cycle of development stage occurs in pigs which serve as the intermediate hosts causing porcine cysticercosis. The second cycle of development stage occurs in humans who serve as the definitive hosts leading to taeniasis (Kungu et al., 2017). Humans and pigs acquire the larval form of the worm by ingesting the eggs of the parasite or by consuming food or drinking water contaminated with the worm’s eggs (Moulton et al., 2007; Dahourou et al.; 2018). It has been demonstrated that carriers of adult tapeworms can get cysticercosis by retro-peristaltism (Dahourou et al., 2018). In humans, cysticerci migrate through the intestinal mucosal wall into the blood circulation, penetrate other striated muscles and eventually form cyst in the brain leading to NCC (Lescano et al., 2007). NCC is the most common helminthic infection of the human. CNS and has been recognized as a major cause of secondary epilepsy in endemic areas (Schmidt et al., 2015; Chacha et al., 2014). Globally, 2 billion people suffer from cysticercosis and 50,000 die of cysticercosis-related diseases annually (Ar Ka Aung et al., 2016; Dorny et al., 2017). In Sub-Saharan Africa (SSA) the estimates of NCC range between 1.9 and 6.16 million people (Chacha et al., 2014; Schmidt et al., 2015). In Uganda, despite significant information about NCC, the country still lags behind in respect to this disease in the region (Alarakol et al., 2018). A previous study conducted among patients with epilepsy in Northern Uganda indicates 15% of the patients were exposed to T. solium infections (Alarakol et al., 2017), ostensibly contributing to late onset of epilepsy among NCC patients. The risk factors for NCC  include; consumption of undercooked infected pork, free range rearing of pigs, poor sanitation, deliberate use of human feces as fertilizers or feeds for pigs, open defecation, negative attitudes and beliefs (Powloski et al., 2005; Ar Ka Aung and Spleman, 2016; Mwape, 2018). Additionally, previous studies have reported that knowledge, positive attitudes and practices have influence on the prevention and /or control of parasitic infections (Chacha et al., 2014; Dahourou et al., 2018). However, most of these studies were conducted in regions    with     unique      characteristics      geographic, socioeconomic and cultural settings. Northern Uganda, in particular, is uniquely inhabited by majority of the communities who were formally been in Internally Displaced Camps during the Lord’s Resistance Army (LRA) war and their social, cultural and community structures have been totally disrupted (Baines and Gauvin, 2014). In order to institute effective interventional programs for NCC in the region, it is important to know the current knowledge, attitudes, practices and beliefs about NCC among the rural communities. The aim of the study was to investigate the current knowledge, attitudes and practices (KAP) in relation to NCC prevention and/or control among communities in the districts of Amuru and Gulu, Northern Uganda.

 

Study design

A cross sectional study to investigate the in-depth dimensions of communities knowledge, attitudes, practices and beliefs was conducted between February and March 2019 among rural communities in the two districts of Amuru and Gulu, Northern Uganda.  Quantitative and qualitative methods were used to collect the research data. Qualitative data were collected and analyzed as described by Bryman (2001). Informed consents were obtained from all the respondents. The research protocol was approved by Gulu University Research Ethic Committee (GUREC) and Uganda National Council of Science and Technology (UNCST).

Study setting

This study was conducted in two sub counties in each district of Amuru and Gulu, Northern Uganda. The two districts cover a total area of over 3000 km2 with an estimated population of 600,000 inhabitants (Uganda Population and Housing Census, 2014). The two districts were purposely selected because they are among the pig producing districts in Northern Uganda (Ikwap et al., 2014), and their proximity to Gulu Municipality. Lamogi Sub County (Amuru district) and Unyama Sub County (Gulu district) are the main suppliers of pigs to slaughter houses in Gulu Municipality. Unyama Sub-County has four parishes and 16 villages with approximately 4000 households (population of 15,000). Lamogi Sub- County has five parishes and fourteen villages with 5000 households (population of 16,000). The two Sub-Counties are the sources of the livelihood of many people in the area who largely depend on pig farming in the area. The communities in these areas practice largely subsistence farming where peasant farmers focus on growing food stuffs to feed themselves and their families (Alarakol et al., 2018). These areas have high level of poverty, lack sanitation infrastructure and the communities practiced free range pig farming which provide suitable environment for survival of   T. solium  in  the study population (Alarakol et al., 2017). Most of the pigs are usually kept in pens at night and released in the morning to scavenge for foods in the environment (Alarakol et al., 2017). In addition, these areas have shortage of pit latrines as well as safe sources of water for domestic use.  The pit latrines coverage is estimated at 89% of the population (Uganda Population and Housing Census, 2014). The main sources of water in these areas are: ground springs, wells, bore holes, tap-water and protected wells (Uganda Population and Housing Census, 2014). The research participants including rural communities, community leaders and local authorities were selected from the Sub-County of each district under study.

Sample size determination

The estimation of the sample size for this this study was done according to a formula described by Kish (1965). Since, there are no KAP studies done in the two districts previously, a 50% estimate was considered at 95% confidence interval, with a 10% margin of error.  Therefore, a total of 96 samples were required. In order to minimize the sampling error, this value was doubled and multiplied by the design effect at 1.5 to 288. This was adjusted by 2.5% to 296 to cater for non-responses. Thus, the overall sampled size was 296.

Sampling procedures

A multi-stage cluster sampling technique was used to select eligible study participants. The districts of Amuru and Gulu were purposively selected for the study. A two-stage cluster sampling method was used to select the participants.  In the first stage, two Sub counties clusters were randomly selected using simple random sampling technique. This includes Unyama and Lamogi Sub-counties in Gulu and Amuru districts respectively. In the second stage, two parishes and 8 villages were randomly selected. The identified study participants in the households were selected by simple random sampling. The individuals selected were consented prior to being included in the study.

Data collection

Self-administered semi-structured questionnaires were used to collect the data. The questionnaires were first pretested with a limited number of samples (20%) in Patiko Sub County outside the study area to check for the quality and validity of the questions.  Data on demographic characteristics, knowledge, attitudes and perceptions were collected. The study protocol was fully explained to the participants prior to the administration of the questionnaires. Additionally, key informant interviews were conducted by the researchers using interview guides. Participants provided informed consent to participate in the interviews.  The interview lasted approximately an hour and respondents were compensated in cash. The key issues discussed related to knowledge, attitudes, practices, beliefs and norms.

Statistical analysis

Both descriptive and analytical statistics were used.  The data are presented as mean, standard deviation, frequency and variance. Pearson’s chi-square was used to test for levels of significance between means of proportions. Bivariate logistic regression was used to test for the strength of association between dependent and independent variables. Variables with P  value  less  than  0.2  were included into multivariate logistic regression to detect for possible predictors of knowledge, attitudes and practices towards NCC in the region. All values greater than statistical P value 0.05 was considered significant. Data from the key informant interviews were analyzed manually using thematic analysis. Themes were developed for key words noted from the interview and further analyzed for commonalities, variations and disagreements.

Knowledge, attitudes and practices performance scores

Performance scores were calculated for each of the variables used to assess knowledge on Neurocysicercosis as described by Kungu et al., 2017). Briefly, 0 to 10 points were assigned as overall scores to the responses on questions assessing each knowledge variable. A respondent was considered to have knowledge on a variable when his/her responses scored 8 to 10 points and these were then recoded into dichotomous variables (Yes versus No). Similarly, good and bad practices and/or attitudes were recorded and their mean scores calculated.  The scores were ranked from 1 to 10. The highest score was given to the respondents with the best practices.  Any score greater than their mean scores or higher was considered good. The knowledge, attitudes and practices scores for each study participants were used to calculate percentage scores out of possible maximum assumed points of 73, 53 and 64 for knowledge, attitude and practice respectively.

 

Demographic information of the study population

A total of 296 respondents were interviewed between February and April, 2019 (Table 1). The mean age of the study participants was 37 ± 14.1 years and ranges from 17 to 87 years old. Majority of the participants were in the age groups 20-29 and 30-39, respectively. There was an almost equal gender enrolment for this study with females, 150 (50.7%). Religion distributions were; Catholic 205 (69.3%), Protestants 66(22.3%) and Pentecostal based organization, 15 (5.1%). More than half 164 (55.4%) of the participants had no formal educations and basically derived their livelihood through farming 183 (61.8%).  Most 223 (75.3%) were married persons who have lived in the study area for more than thirty years (Table 1).

 

 

Knowledge on neurocysticercosis among communities

Table 2 shows communities’ knowledge on NCC. Of the 296 respondents, 204 (69%) practiced pig farming with more than half (51%) of the respondents’ pigs were farmed by free range system. Eighty percent (80%) of the pig farmers largely rear pigs for sale and more than sixty percent (62.2%) of them knew pork tapeworms. However, majority (45%) had no knowledge of having ever passed out tape worms in their feces.  Most (80%) respondents could not recognize tape worms when shown  to  them  in study pictures. 80% of the respondents had heard about NCC but only 46% knew how humans get infected with NCC. Majority (74%) did not know how pigs get infected with tapeworm but most (65%) heard about the white nodules (rice) in the pigs.

 

 

Attitudes among communities about neurocysticercosis

Of the 296 respondents, 45 (15.2%) reported that they were diagnosed positive for  tapeworm  infections  (Table 3). 33(11.0%) reported felt extremely sad when diagnosed positive for tapeworm and up to (46%) reported they knew the danger associated with NCC. 55%  routinely   deworm   their   pigs   and   45%   sought veterinary assistance. Majority (74%) of the participants did not have patients with NCC at their homes. However, most (95%) respondents agreed that NCC patients should   be  taken  to  the  hospital  for  medical  services. 73% of respondents reported NCC patients should also enjoy the right to marry. Most (76.7%) of the respondents agreed the NCC patients should be sent to school to study.

 

 

Community’s practices and beliefs on neurocysticercosis

Of the 296 respondents, 66.9% had toilets and reported always washing their hands (94.3%) after using the facility (Table 4). Majority (74.7%) reported eating pork but 5.1%  did  not  throw  away  pork  meat  infested  with cysticerci (condemned pork meat). When asked about eating infested pork, one respondent confessed, “meat is not thrown away but it is smoked, dried on fire, cooked and eaten”. He added, “Meat’s soup is better than vegetable’s soup my dear”. Furthermore, a respondent confessed that meat is never buried in soil as it is a taboo in their culture’’. He added. The most interesting finding in this study was when one of the respondents told the researchers that; “here in the village, no parts of the pigs are thrown away including their hoofs”. Most respondents (75.8%) send their pigs for vaccination and routinely conduct deworming exercises. Respondents with epileptic patients in their homes  send  them  (94.3%)  for medical care and those with pigs routinely (55.4%) seek veterinary assistance.

 

 

Factors associated with knowledge towards neurocysticercosis

The bivariate analysis of the variables sex, age group, marital status, religion, occupation, and residency and education level was conducted to ascertain their association   with   knowledge   on  NCC.  The  data  with p-value less than 0.2 in the bivariate analyses were included into multivariable logistic regression model. Multivariate logistic regression analysis indicated no statistically significant difference between age groups, marital status, religion and duration of residency in respect to factors associated with knowledge on NCC. However, sex (P=0.017, OR=1.27(95%CI: 1.04-1.54), level of education (P=0.006, OR=4.451(95%CI: 1.49-12.20) and occupation (P=0.03, OR=3.843(95%CI:1.13-12.71) were significantly associated with better knowledge on NCC (Table 5).

 

 

Factors associated with positive attitudes and practices towards neurocysticercosis

Furthermore, the study conducted a bivariate analysis on the independent variables sex, age group, marital status, religion, occupation, and residency and education levels as already described. Multivariate logistic regression analysis revealed no statistically significant difference between age groups, marital status, and religion, duration of residency in respect to factors associated with knowledge on NCC. However, being male (P = 0.013, OR= 1.88(95%CI: 1.14-3.10), level of education up to secondary level (P=0.031, OR= 5.43(95%CI: 1.17-25.20) was significantly associated with positive attitudes towards patients with NCC (Table 6).

 

 

Factors associated with practices towards neurocysticercosis

Furthermore, the study conducted a bivariate analysis on the independent variables sex, age group, marital  status, religion, occupation, and residency and education levels and practices/ beliefs as described. Multivariate logistic regression analysis revealed no statistically significant difference between age groups, marital status, and religion, duration of residency and level of education in respect to factors associated with knowledge on NCC. However, being male was significantly associated with better practices towards NCC than the female counterparts (P=0.00) (Table 7).

 

 

Qualitative data

Key Informants (KI) agreed that large numbers of people are rearing pigs in the area. This has been attributed to the increase demand for pork meat in Gulu Municipality. They also agreed that pork consumption have increased among the rural communities and no parts of the pigs are thrown away due to their delicacies.  They also agreed that pig farming has become a source of livelihood since it provides the quickest means of income to the rural communities.   Additionally,   they   agreed   that   in  their tradition, it is a taboo to bury meat in the ground.

 

 

 

 

 

 

 

 

 

 

Community knowledge on NCC

The findings indicate the majority of the respondents (54%) do not have adequate knowledge about NCC and only (46%) knew how humans get infected with NCC. This shows a clear knowledge gap that exists among the communities in the region about NCC. While pig farming is on the increase in the region, there is evidence that the communities are already exposed to tapeworm parasites and many could be carrying the infections (Alarakol et al., 2017). However, with fairly good knowledge of tapeworm (62%) amongst the community, the health authorities could use this information to reinforce public health campaigns for the prevention and control of T. solium infections in the region. It should be noted that up to 45% of respondents in the rural communities reported they do not know and have never seen tapeworms. These are the rural populace who particularly need to be enlightened about NCC through health education programs. They are deficient of knowledge on NCC and yet continue to interface    with    T.   solium    infected   victims   in   their

neighborhoods. Furthermore, most (74%) of the respondents interviewed wee illiterate and/or had only lower primary education. The findings indicate that 67% of the respondents had primary education and most (58%) are able to read and write. Further analysis revealed that male farmers and those who had at least a secondary education level were significantly more associated with better knowledge on NCC. While this is significant in terms of their formal education, translating this limited education into actual practices of behavioral change remains a challenge in most rural communities.  Therefore, more robust behavioral efforts are necessary to enhance community’s knowledge on tapeworms’ infections. Health education to cause behavioral changes in these practices can therefore be an effective intervention strategy (Mishra et al., 2007). These findings are similar with other studies done previously elsewhere. Decker and Pierre (2010) conducted studies in Northwest India and reported that most rural respondents had knowledge of NCC, but some were unable to describe which drugs were used in the treatment of the NCC. Ngowi et al. (2015) in a related study conducted in a rural village in Burkina Faso, reported that most people confessed they had seen worms in their feces or those of others, however, they were unable distinguish between worm species. Similarly, Kungu et al. (2017) reported that male famers were significantly associated with better knowledge about PCC than their female counterpart.  On the other hand, Gutra et al. (2017) reported that low level of education among rural communities increased risk of infections and prevalence of NCC.

In the present study, the knowledge of the populace on NCC may be attributed to the mass treatment of helminthes introduced from 2007 to 2010 in Northern Uganda. Through this effort, significant numbers of people  in  the  rural  communities  received  public health educations on neurocysticercosis in the region. Therefore, it is necessary that knowledge on NCC is provided to communities for the elimination of the negative perceptions and attitudes for the betterment of the welfare of epileptic people (Chacha et al., 2014).

Community attitudes, practices and beliefs

The findings show that the community in the region provides basic healthcare support to patients with NCC and the majority sends them to school. This is an important contribution to the people with epilepsy since leaving them at home would disadvantage them from benefiting from the community social transformation programs. The study revealed that males’ play significant role in ensuring that people with epilepsy are taken care of. Males are 4 times more likely to send people with epilepsy to school than their female counterparts. Similarly males are more likely to send people with epilepsy to medical facility than their female counterparts. This may be attributed to male traditional roles of providing services to their families. Previous studies reported that; males’ were significantly associated with better practices towards neurocysticercosis (Dahourou et al., 2018). In the current study majority (78%) of the respondents care about patients with NCC and many send them to health facilities for medical care, schools and they are also allowed to marry. Up to 90% of the respondents reported that, in case of sickness, the NCC patients are routinely sent to Hospital or health facility. While at least 10% of the respondents reported they send NCC patients to herbalist.  Although, traditional healers enjoy support from a number of people in the rural community, limited data on their operations invalidate and prevent efforts to know the extent of their roles in the prevention of NCC in the region.

Additionally, the findings indicate that majority of respondents confessed consumption of pork and most eat both the roasted and cooked pork. While both pork forms are grossly eaten, there was no statistical difference between those who eat roasted pork and the cooked ones (P=0.02).  The main reason for this may be due to both males and female’s preference to either of the two forms of pork. Chi square analysis indicates that males’ preference on pork consumption significantly deferred between eating roasted and cooked pork (P=0.23). In contrast, the females appear to enjoy cooked pork more than the male counterparts.

There is a misconception within the rural communities that NCC patients suffer from witchcrafts, and that these people are unable to get cure. Such beliefs are embedded within the populace since time immemorial, the practices have been in place, and eradicating it will require extensive health education. This study findings indicate   that   some   NCC  patients  were  taken  to  the traditional healers before they actually seek for help at the health facilities. Gutra et al. (2017) reported that, persons beliefs are centered on tradition attachment and those beliefs are increasingly promoted among rural communities. Parija and Raman et al. (2011) reported that in India, misconception is a reality since; many people believe epilepsy is a form of super natural punishment. In addition, previous studies have reported connection between beliefs and the community’s practices (Feury et al., 2013). In the current study, 30% of the respondents’ believed that meat are not thrown away but can be roasted or cooked and eaten. Interestingly, one of the respondents confessed meat’s soup is better than vegetable’s soup”. Relatedly, Ngowi et al. (2015) in a study conducted in a rural village of Burkina Faso reported that most participants were aware of the health-related risks of eating pork meat, but they could not afford to throw it away. Similarly, in South India, Parija and Raman et al. (2011) reported that T. solium cyst mixed with milk, called “Malal” was known to provide a “delicious” source of “meal”. However, in the current study most respondents do not eat cyst of T. solium but more than 70% eat pork meat. This shows that pork meat is a very delicious and popular source of proteins among the rural communities. Therefore, proactive intervention strategies for prevention and control of NCC need to be put in place to minimize the proliferation of transmissions of T. solium.  Future research should focus on examining the influence of pig husbandry and management practices on pig production among pig farmers in the rural communities. Additionally, further study should establish the sero-epidemiology of T. solium cysticercosis among the rural communities for better understanding level of the exposure or current infection among the population.

 

The findings indicate there is a limited knowledge gap on NCC among the rural communities in the district of Amuru and Gulu, Northern Uganda. In addition, the findings show that the communities practice risky behaviors that are potential drivers for NCC in the region. Therefore, health authorities need to improve communities’ knowledge, attitudes and practices in the prevention/control NCC in the region.

 

The authors have not declared any conflict of interests.

 

The authors are grateful to the research assistants, Okello  Charles,  Mwaka,   and  Ochieng   Ladiro  Michael from the districts of Amuru and Gulu districts who participated in this exercise. Special thanks also go to the statistician - Onen Anthony for the impeccable work done.

 

This work was supported through the DELTAS Africa Initiative grant # DEL-15-011 to THRiVE-2. The DELTAS Africa Initiative is an independent funding scheme of the African Academy of Sciences (AAS)’s Alliance for Accelerating Excellence in Science in Africa (AESA) and supported by the New Partnership for Africa’s Development Planning and Coordinating Agency (NEPAD Agency) with funding from the Wellcome Trust grant # 107742/Z/15/Z and the UK government. The views expressed in this publication are those of the author(s) and not necessarily those of AAS, NEPAD Agency, Welcome Trust or the UK government. BSB receives salary support from DELTAS Africa grant # 107743 to MUII-plus.