Knowledge, Attitudes and Practices Regarding Taeniasis in Pakistan

Taeniasis is a neglected zoonotic disease responsible for serious health disorders, such as seizures, and may even cause death. Humans are the definitive host for the three species Taenia solium (pork tapeworm), T. saginata (beef tapeworm), and T. asiatica, harboring the adult tapeworm in the small intestine. In this study, a structured questionnaire was circulated to assess the knowledge, attitudes, and practices (KAPs) regarding taeniasis among the rural and urban communities of Rawalpindi and Islamabad, Pakistan. A total of 770 individuals participated in the study. Of the total respondents, 44.4% had little knowledge about the disease and its impact, while the majority (70%) of respondents showed a willingness to participate in elimination campaigns by providing fecal samples. Most respondents kept raw meat separated from clean utensils (81.6%) and checked the internal temperature of meat when cooking it (75.1%). Regression analysis showed a significant association between age and knowledge, especially in the 20–30 years (p < 0.05; OR 0.574) and 30 to 40 years (p < 0.05; OR 0.553) age groups, and being a resident in Rawalpindi (p < 0.05; OR 0.68) and other cities (p < 0.05; OR 2.43), except Islamabad. Income ranges of 31,000–50,000 PKR (p < 0.05; OR: 0.574), 51,000–70,000 PKR (p < 0.05; OR 0.531), and above 70,000 PKR (p < 0.05; OR 0.42) were significantly related to attitude, compared with individuals with incomes of 10,000–30,000 PKR. Income above 70,000 PKR (p < 0.05; OR 0.87) and living in an urban area (p < 0.05; OR 0.616) compared to a rural area were significant with practices. A positive attitude was observed regarding awareness and prevention of the disease. Awareness campaigns and providing health education could be key approaches to manage this disease in the general population of developing countries.


Introduction
Human taeniasis is the one of the leading foodborne parasitic disease, according to the World Health Organization (WHO) [1]. The causative agents are tapeworms from the Taeniidae family (subclass Eucestoda, order Cyclophyllidea) [2]. The adult tapeworms of the three responsible species are found in the small intestine of humans. Cattle serve as the vertebrate intermediate host of Taenia saginata, whereas pigs are the larval hosts for T. asiatica and T. solium [3]. The accidental entry of the eggs through contaminated food or water leads to the onset of cysticercosis, in which humans serve as an intermediate host for the parasite. In the human intestine, the worm takes between 5 and 12 weeks to reach adulthood [4]. T. solium can live for at least 25 years. Its eggs are spherical and within the shell are six-hooked tapeworm larvae. These larvae are small cysticerci, about 6-18 mm wide and 4-6 mm in length, and can be found in the muscle or subcutaneous tissues of their intermediate host (generally pigs). The cysticerci can also be found in other tissues, including those of the central nervous system, where they can grow much larger, sometimes many cm in diameter. Adult tapeworms have a median length of approximately 3 m; however, they can develop to up to 8 m in length. A single worm may harbor 800-1000 proglottids filled with eggs [5].
Neurocysticercosis (NCC), due to the development of cysts in the central nervous system (CNS), is frequently reported. NCC is considered the most common parasitic infection of the human nervous system. It is the most preventable cause of epilepsy in developing countries, and about 30% of cases are reported from underdeveloped countries [6]. Cysticercosis is prevalent in various countries and is associated with poverty and illiteracy, as well as the lack of competent diagnostic and management skills and effective preventative and control efforts. Cysticercosis imposes a significant economic burden owing to losses in the meat industry from porcine cysticercosis and hospitalization expenditure in managing NCC [7,8].
The prevalence of taeniasis and cysticercosis in developed countries is likely evolving, but a lack of solid data is one of the biggest barriers in determining the actual size of the problem. In one epidemiological investigation, females were found to have a greater prevalence (61%) than males (32%) [9]. The illness burden brought on by NCC is higher in areas where it is endemic. In Honduras, Ecuador, and Peru, recent controlled studies using computed tomography have revealed a strong association in the field between NCC and seizures, with nearly 30% of seizures attributable to NCC infection [10]. According to the WHO, taeniasis affects 500 million people worldwide, mostly in underdeveloped nations, and leads to the death of 50,000 people per year [11]. Asian countries, such as India, Pakistan, northern China, and Thailand, are affected by the disease [12]. In Nepal, Taenia cysts were discovered in pig flesh from Kangeswari, Kathmandu for the first time in 2019 [13].
The linked variables of a high frequency of infection include risk factors, production systems, food culture, insufficient regulatory mechanisms, and low priority in control programs. The increasing incidence of cysticercosis in pigs and humans is linked to a rapid rise in small-scale pig farming [9]. Cysticercosis is thought to be eradicable due to several factors, including the following: humans are the only definitive host and the only source of infection for intermediate hosts; domestic animals serve as primary intermediate hosts or reservoirs and are easily controlled; there are no significant wildlife reservoirs; and control interventions are readily available. There have been infrequent reports of cysticercosis, particularly the cerebral variant. Additionally, the racemose form has been documented.
Establishing effective control and elimination measures for many illnesses depends heavily on community knowledge, attitudes, and practices (KAPs) [14]. With the right information, people are more likely to adopt prevention measures, such as treating tapeworm infections and adopting better sanitation, cleanliness, and improved pig-rearing techniques, that may reduce the feco-oral spread of numerous infectious diseases. Data from a KAP survey can be used to identify knowledge gaps, cultural norms, or behavioral patterns that could be problematic for understanding and taking action while also hindering efforts to manage or eradicate the disease. However, there is little KAP information about Taenia solium cysticercosis in Asian countries [15,16], especially Pakistan. As a result, the current study sought to assess KAPs regarding taeniasis in Pakistan. The findings can serve as the foundation for the creation of a contextualized health education package that can be used locally to manage or eradicate taeniasis.

Study Site
The study was conducted among the rural and urban populations of the cities of Rawalpindi and Islamabad in Pakistan. Islamabad is located at the northern edge of the Potohar plateau at an elevation of 540 m, and it has a population of 2.015 million, while Rawalpindi lies on the Potohar plateau 9 miles southwest of Islamabad and has a population of approximately 2.908 million. The cities are known as the "twin cities" of Pakistan [17].

Study Design
The study aimed to explore the knowledge, attitudes, and practices (KAP) related to taeniasis among the general population through a descriptive cross-sectional approach. To obtain the requisite information, a pre-validated questionnaire that adhered to standardized protocols was devised. This questionnaire was formulated after a comprehensive evaluation of an English language version. Subsequently, the survey was rendered into informal language to guarantee clarity and understanding for the respondents. The study placed significant emphasis on inclusivity, whereby individuals from a wide range of ethnicities, religions, genders, and geographical locations were considered eligible to participate in the study. The assessment of KAP was restricted to individuals aged between 10 and 70 years, thereby ensuring a targeted sample size that included both adolescent and adult participants. The study focused on providing an extensive understanding regarding the knowledge, attitudes, and practices concerning taeniasis among a representative crosssection of the general public using these selection criteria.

Sample Size Calculation
We used the Raosoft calculator [18], assuming a 95% CI with a 5% margin of error and Z of 1.96, to calculate the sample size. The estimated population of Rawalpindi is 2.908 million, and that of Islamabad is around 2.015 million, and the required sample size was 770.

Data Collection
Data were collected to assess the KAPs related to taeniasis. A structured questionnaire was used, and responses were collected through both an online survey and door-to-door interviews. A wide range of participants, including those who lived in both urban and rural areas, were approached using the online survey.

Questionnaire
We used a self-designed KAP questionnaire as the survey tool to collect data from residents. This questionnaire was prepared in English and divided into four sections. The first section comprised questions gathering socio-demographic information including age, gender, area, residence, income, occupation, education, and number of family members. The rest of the questionnaire comprised three sections of questions to assess knowledge (n = 28), attitudes (n = 10), and practices (n = 7) regarding taeniasis.

Data Analysis
A Microsoft Excel file was used for sorting and storage purposes, and SPSS 24.0 was used for the statistical analysis. Descriptive statistics were used to calculate answer frequency and percentages. The Chi-square test was used to examine the association between two categorical variables. Non-parametric tests were used for non-categorical variables (Mann-Whitney U test and Kruskal-Wallis test). The level of significance was set at 0.05.

Results
The KAP questionnaire was circulated among 800 individuals in Rawalpindi and Islamabad, and 770 responses with complete information were received and included in the analysis.

Demographic Characteristics of Participants
The study population comprised more women (n = 547, 71%) than men (n = 220, 28.6%). In terms of age, 51.9% (n = 400) of participants were between 20-30 years old ( Figure 1). In terms of religion, most respondents were Muslim (96.1%, n = 740). As far as the distribution of the participants is concerned, the majority were from Punjab (n = 716) ( Figure 2). Owing to the distribution of the questionnaire among students, most participants were recorded as undergraduate students (59.61%). The respondents were concentrated in urban areas (86.4%), and 31.6% (n = 243) had a monthly household income of 31,000-50,000 PKR. The most frequent family size was 4-5 members (43.2%, n = 333; Table 1).

Results
The KAP questionnaire was circulated among 800 individuals in Rawalpindi and Islamabad, and 770 responses with complete information were received and included in the analysis.

Demographic Characteristics of Participants
The study population comprised more women (n = 547, 71%) than men (n = 220, 28.6%). In terms of age, 51.9% (n = 400) of participants were between 20-30 years old (Figure 1). In terms of religion, most respondents were Muslim (96.1%, n = 740). As far as the distribution of the participants is concerned, the majority were from Punjab (n = 716) (Figure 2). Owing to the distribution of the questionnaire among students, most participants were recorded as undergraduate students (59.61%). The respondents were concentrated in urban areas (86.4%), and 31.6% (n = 243) had a monthly household income of 31,000-50,000 PKR. The most frequent family size was 4-5 members (43.2%, n = 333; Table 1).

Results
The KAP questionnaire was circulated among 800 individuals in Rawalpindi and Islamabad, and 770 responses with complete information were received and included in the analysis.

Demographic Characteristics of Participants
The study population comprised more women (n = 547, 71%) than men (n = 220, 28.6%). In terms of age, 51.9% (n = 400) of participants were between 20-30 years old (Figure 1). In terms of religion, most respondents were Muslim (96.1%, n = 740). As far as the distribution of the participants is concerned, the majority were from Punjab (n = 716) (Figure 2). Owing to the distribution of the questionnaire among students, most participants were recorded as undergraduate students (59.61%). The respondents were concentrated in urban areas (86.4%), and 31.6% (n = 243) had a monthly household income of 31,000-50,000 PKR. The most frequent family size was 4-5 members (43.2%, n = 333; Table 1).

Knowledge of Participants about Taeniasis
A total of 28 questions assessed knowledge and its impact on taeniasis. The frequency and percentage of these participants showed that the largest percentage of people (44.4%) had little knowledge about the disease and its impact. In terms of diet, 49.6% (n = 382), of the participants cooked beef at home, and only a few of the respondents were nonvegetarian (6.4%, n = 49). Among the participants, 24.5% reported consuming uncooked meat, with the majority eating beef compared to pork (2.6%). Only 11.4% of respondents had seen proglottids in their feces. However, more respondents were aware of taeniasis as a diagnosis, and that tapeworm species causing taeniasis are normally found in meat (52.3%). They were also aware that transmission is linked to poor sanitation and consumption of infected beef and pork (Table 2).

Attitudes of Participants towards Taeniasis
Respondents reported specific attitudes toward the prevention of taeniasis. The inclination was toward avoiding eating raw, undercooked, or unhygienically prepared meat. Positive attitudes regarding awareness and prevention of disease were observed. Most respondents were willing to participate in campaigns (69.1%) and provide blood or feces samples (67.1%) as part of efforts to eliminate the disease. A large percentage of respondents understood that cattle and pigs should be vaccinated (66.5%), and that there should be proper disposal of animal waste other than open defecation. A need for community-level programs to ensure meat inspection was expressed by 61.3% of the participants, and 66.9% showed a willingness to check the internal temperature of food if awareness was raised and thermometers were introduced (Table 3).

Practices of Participants about Taeniasis
A significant proportion of the 770 respondents washed their hands before and after preparing food and washed meat properly before cooking. The majority kept raw meat separated from clean utensils (81.6%) and checked the internal temperature of the meat when it was cooking (75.1%). About 90% of the study population reported washing their hands after defecation. However, 70% ate food from stalls/vendors (Table 4).

Association between Knowledge and Socio-Demographic Characteristics of Participants
We used the independent variables of gender, age, province, residence, occupation, education, area, annual income, and knowledge as dependent variables. We applied binomial logistic regression to the independent variables with the dependent variables and obtained p values and odds ratios (ORs). In terms of the associations between knowledge and socio-demography, we observed a significant association between knowledge and having a family size of eight to nine members (p < 0.05; OR 0.782), as compared to two to three family members. Variables such as age, gender, province, residence, area, religion, and income were not significantly related to knowledge (i.e., p > 0.05). ORs and 95% confidence intervals are shown in Table 5.

Association between Attitudes and Socio-Demographic Characteristics of Participants
Using regression testing as part of our statistical analysis, we determined significant associations between knowledge and age, especially in the 20-30 years (p < 0.05; OR 0.574) and 30-40 years (p < 0.05; OR 0.553) age groups. We also found a significant relationship between knowledge and being a resident in Rawalpindi (p < 0.05; OR 0.68) and other cities (p < 0.05; OR 2.43), except Islamabad. At the same time, a significant association was seen between attitude and being neither employed nor a student (p < 0.05; OR 2.761). Statistical analysis of income showed that income ranges from 31,000-50,000 PKR (p < 0.05; OR: 0.574), 51,000-70,000 PKR (p < 0.05; OR 0.531), and above 70,000 PKR (p < 0.05; OR 0.42) were significantly related to attitude, as compared to income ranging from 10,000 to 30,000 PKR (Table 6).

Association between Practices and Socio-Demographic Characteristics of Participants
Statistical analysis of associations between practices and socio-demographic variables indicated that living in an urban area and income level were significant. Income of more than 70,000 Pkr (p < 0.05; OR 0.87) and living in an urban area (p < 0.05; OR 0.616), as compared to rural areas, were significantly related to practices (Table 7).

Discussion
Taeniasis is widespread in East, Southeast, and South Asia across the region's rich diversity of cultural, traditional, and behavioral norms [19,20]. Many studies have discussed the prevalence of soil-transmitted helminths and other underdiagnosed tropical diseases [21][22][23], but the three co-occurring human Taenia species have rarely been investigated in depth. It is unclear how widespread the problem is in East, Southeast, and South Asia, and incidence rates reported by the various countries and territories vary considerably [5,24,25]. The significant findings on KAPs relating to taeniasis in these countries, however, point to issues with sanitation at an individual, household, and community level. Cysticercosis can be prevented and controlled through better sanitation and health education, the application of food safety precautions, and the use of improved and standardized diagnostic tests, as well as through the reporting of infections at the species level [26]. The holistic approach known as "One Health" can be used to apply these methods, and this approach considers the well-being of humans, animals, and the planet. Most intestinal infections are asymptomatic. Symptoms are often modest and may include stomach discomfort, anorexia, weight loss, or malaise. Cysticercosis has a widespread impact on several essential organs (e.g., brain, eye, heart); however, it has a low death rate, and death is usually caused by complications such as encephalitis, increased intracranial pressure due to edema and/or hydrocephalus, or stroke. The infection affects people of all ages, sexes, and races equally [27].

Socio-Demographic Characteristics
In our study assessing KAPs regarding taeniasis, which is the first of its kind in Pakistan, we sought to describe the socio-demographic factors of the study population, including gender, education, residency marital status, age, and income. As the questionnaire was circulated among students, most of the participants were unemployed and between 20-30 years of age. The major concentration of respondents was in urban areas, and most respondents had a monthly household income of 31,000-50,000 PKR. A similar cross-sectional study was conducted in Punjab, India, comprising a survey questionnaire related to zoonotic diseases that was distributed to 859 participants. The majority were male farmers [28]. In another study, a structured questionnaire was circulated to collect socio-demographic variables and information on knowledge and attitudes regarding taeniasis/cysticercosis, raw meat consumption, latrine usage, and taeniasis treatment practices in two small towns in Ethiopia. The majority of the 195 participants were also male [29]. Food safety KAPs among 772 elementary schoolchildren were surveyed in southern Taiwan, with mostly female respondents [30]. In another cross-sectional study that was conducted in Ibadan, Nigeria, most of the participants were male [31]. In a KAP analysis relating to taeniasis disease that was conducted in South Africa, most participants were male and had only primary school education, with some having obtained secondary education [32]. A similar cross-sectional study conducted in Tanzania related to taeniasis also had mostly male respondents [33].

Knowledge
Our study assessed the basic knowledge of participants about the cause of the disease and the parasite's intermediate host. One study related to taeniasis that was conducted in Tanzania demonstrated knowledge about cysticercosis, particularly among cattle and pig keepers. Many participants had heard about tapeworm (T. solium taeniasis), and their knowledge of the signs and symptoms of the disease was good. Although most of the participants knew about epilepsy, none knew about the relationship or link between cysticercosis and epileptic seizures [34]. In another study conducted on farmer awareness and practices regarding taeniasis with 294 participants, only a small number knew about taeniasis disease [35]. The cross-sectional study conducted in small towns in Ethiopia demonstrated that meat industry workers and a large number of community members in both study areas had heard of human taeniasis [36]. Respondents purchasing pork from home slaughter were about four times less likely to demonstrate good knowledge in a study conducted in Nigeria [37]. In the KAP analysis conducted in South Africa, half of the respondents indicated no knowledge of cysticercosis in pigs, and the majority had never heard of NCC [37]. In a KAP study in Tanzania, the average number of respondents had heard of the pork tapeworm (T. solium taeniasis), and many (n = 163, 65%) were familiar with the signs and symptoms of the infection. However, only a few participants had accurate knowledge of the mode of transmission. Only a small number of respondents reported transmission through improperly cooked pork, and many participants falsely cited contaminated water [38].

Attitudes
In terms of attitudes toward the prevention of taeniasis disease, the inclination of many respondents was towards avoiding eating raw, undercooked, or unhygienically prepared meat. Positive attitudes towards awareness and prevention of disease in the community were observed. Most of the respondents were willing to participate in campaigns and provide blood and feces samples as part of efforts to eliminate it. Our results on respondents' attitudes to taeniasis disease treatment, prevention, control, and the advantage of vaccination were consistent with a similar study conducted in Ethiopia [31]. A study performed in India found that the attitude of respondents towards disease control possibilities was better in those educated at college and university level when compared to illiterate people (p < 0.05) [39]; however, illiterate people were not included in our study. In contrast, the attitude towards the low-risk perception of cysticercosis is indicative of a positive trend in the Tanzanian study on taeniasis [16]. In the Taiwanese KAP analysis related to food safety, the attitude among students was not quite positive [15]. However, in a cross-sectional study conducted on smallholder farms in South Africa, results on the attitudes of individuals were not encouraging, and the community appeared to need more awareness [37]. Communities that are in underdeveloped countries with low literacy rates or are located in peripheral areas need improved understanding and greater awareness of taeniasis through awareness campaigns.

Practices
Most of the participants in our study were practicing hygiene by washing their hands before and after cooking food. The same study was conducted in Swat, Pakistan, and most of the surveyed population kept raw meat separated from clean utensils and checked the internal temperature of the meat. Public education to improve hygiene practices, curb risky culinary habits, promote taeniasis treatment, and discourage backyard slaughtering were suggested in a study conducted in small towns in Ethiopia [38]. Only hand washing before eating was significantly promoted in the practice domain (p < 0.001) in the study that was carried out relating to food safety in southern Taiwan [39,40], and poor practices were observed related to taeniasis in the KAP survey that was conducted in Nigeria. The majority of farmers in South Africa practiced a free-ranging system, as reported in some taeniasis studies, while a small number practiced a semi-intensive system [40,41].

Conclusions
KAPs have an enormous impact on the control of communicable diseases and in informing suitable policies. Owing to a lack of focus on awareness campaigns among the general population, many people are unaware of taeniasis. Our results demonstrated the importance of awareness of handling animals, keeping animals as pets, consuming raw meat, and handling infected animals. Respondents with lower educational levels and those who owned livestock had higher contact with animals but tended to consume more raw meat, not have pre-exposure vaccinations, and not take immediate action with infected animals. This study offers important new information about KAPs associated with taeniasis in the general population. The results show the need for focused education and awareness campaigns, especially among particular age groups and geographic areas. Taeniasis preven-tion initiatives should be tailored to the various professional and educational backgrounds of those involved. The study's findings advance knowledge of taeniasis' KAPs and can direct public health initiatives aimed at lessening the burden of this parasitic infection. In conclusion, populations with lower educational standing should be offered awareness and training programs on the transmission, treatment, prevention, and management of taeniasis, and related information. Additionally, strengthening intersectoral collaboration for the prevention and control of common zoonotic diseases is important.
While the focus of our research was to provide insights into the current state of knowledge and practice, we recognize the importance of conducting extensive research to produce significant results. Understanding the pathogenesis of taeniasis, identifying novel diagnostic techniques, and comparing the efficacy of various treatment options are all possible outcomes of intensive research. These areas of intensive research contribute to the advancement of disease knowledge, the improvement of diagnostic accuracy, and the development of more targeted and effective treatments.

Limitations
The research has utilized self-reported information, which is susceptible to both recall bias and social desirability bias. The reliability of data on participants' knowledge, attitudes, and practices related to taeniasis may have been compromised by memory and reporting biases, which could have introduced some degree of error. The responses provided by the participants were influenced by social desirability bias, resulting in an overestimation of their knowledge, positive attitudes, or healthy practices about taeniasis. The presence of bias has the potential to compromise the precision and validity of the results. As the research utilized cross-sectional data gathering, it did not account for the evolution of knowledge, attitudes, and practices over a period. Adopting a longitudinal approach would yield a more all-encompassing comprehension of the aforementioned factors.

Institutional Review Board Statement:
The current study was approved by the Ethics Review Board of the Department of Biosciences, COMSATS University Islamabad (CUI), and completely followed the ethical considerations.
Informed Consent Statement: Not applicable.

Data Availability Statement:
The data that support the findings of this study are openly available on request.

Conflicts of Interest:
The authors declare no conflict of interest.