https://orcid.org/0000-0002-2260-8821
ABSTRACT
Concern about the zoonotic Hepatitis E virus (HEV) is rising. Since, food handlers are at greater risk in contracting HEV, the present study aims to determine awareness, knowledge, prevention practices against HEV, and immunization attitudes. A cross sectional study was conducted among 400 food handlers in Klang Valley, Malaysia from December 2021 to March 2022. A structured questionnaire was employed for data collection and analysis with Statistical Package for Social Science (SPSS) version 29. Approximately 4.5% of the respondents (18) reported having heard of HEV, while the median scores for the knowledge and practice domains were 0/10 and 1/5, respectively. A total of 316 (79%) respondents expressed willingness to obtain vaccination if made available. This study also found that those respondents who completed their tertiary education were significantly possessed better knowledge of the disease [odd ratio (OR) = 8.95, and 95% confidence interval (CI) 4.98–16.10]. Respondents with HEV awareness reported considerably better practices (OR = 8.24, 95% CI 1.72–39.63). Food handlers with one to five years of experience in the industry expressed notable willingness to take vaccination (OR = 7.71, 95% CI 1.79–33.18). Addressing poor HEV awareness and knowledge and poor practices against the disease is crucial in enlightening the policy makers about awareness among food handlers and general population. Nonetheless, a good immunization attitude, significant acceptance toward vaccination even with the vaccine being unavailable in Malaysia, and limited awareness of HEV highlight a promising development.
Introduction
Hepatitis E is a disease caused by Hepatitis E virus (HEV).Citation1,Citation2 Approximately one in eight individuals worldwide has been infected with HEV.Citation3 Nevertheless, the actual burden of the disease is unknown.Citation2 The predominant clinical manifestation of hepatitis E infection is acute viral hepatitis, which could lead to acute liver failure in specific individuals. The disease is also frequently associated with extrahepatic symptoms and mortality.Citation2,Citation3 Based on global annual burden, a mortality rate of 0.35% was reported. Whereas pregnant women who are at high risk of developing acute liver failure, face higher mortality rates that ranging from 15% to 25%.Citation4
From a clinical perspective, genotypes HEV-1 to −4 cause concerns. Viruses HEV-1 and −2 are often correlated to outbreaks in developing countries, considering they are enterically transmitted.Citation2 On the other hand, HEV-3 and −4, referred to as zoonotic, have a wide range of hosts, including swine, cattle, wild boar, goat, camel, deer, yak, and seafood.Citation1,Citation5,Citation6 The HEV-3 virus has been found globally, while HEV-4 is predominantly in Asia.Citation4,Citation7
A systemic review conducted from 2011 to 2022 has identified four outbreaks that were zoonotic in origin.Citation8 Moreover, the shifting trend of HEV infections toward zoonotic transmissions has increased the likelihood of contracting it by 50% among the high-risk group which includes of farmers raising livestock, veterinarians, slaughterers, and food handlers, than the general population.Citation4,Citation9,Citation10 Although there were numerous reports on HEV seroprevalence, but the studies focusing on the knowledge level and prevention practices against the disease are limited.Citation11–15
Food handlers have a critical role in the food supply chain.Citation16 Efficient HEV surveillance implementation also requires stakeholders’ participation, including food handlers. Few factors, such as awareness and knowledge about the disease, predominantly determine the level of involvement of food handlers.Citation12 Although adherence to hygiene protocols is critical in disease prevention, knowledge enables effective executions of the preventive measures.Citation17,Citation18
Understanding the potential willingness of food handlers to obtain vaccination if made available is crucial, considering the occupational risks associated with food handling. Among the three HEV vaccines developed thus far, HEV239 has been subjected to phase III of clinical trials and its administration license was approved within China in 2012.Citation19 Over 100,000 individuals in China of 16 to 65 years predominantly with HEV-4 genotype reported no significant side effects in a year with 100% efficacy of the 0,1, and 6 months dose regime of the vaccine.Citation3
The World Health Organization (WHO) has not recommended the application of the HEV239 vaccine outside China due to information scarcity on HEV prevalence and vaccination usage outside the trial cohort.Citation3 Similarly, large-scale population research on HEV prevalence in Malaysia is scarce. Furthermore, available data are primarily from Klang Valley. Chronic hepatitis B patients in a hospital in Klang Valley reported 9.8% seroprevalence. The study found that all isolates belonged to HEV-4, genetically related to swine and boars.Citation20 On the other hand, blood donors in the same area documented 3.1% HEV seroprevalence. The report revealed that individuals of increasing age and nonprofessional workers, including cooks, were significantly associated with seropositivity.Citation21
Considering that HEV could lead to liver disease and unwanted consequences, and food handlers are classified as a high-risk group in contracting it, awareness, knowledge, and preventive practices against the HEV complemented with a willingness to be vaccinated would be guidance in developing surveillance and comprehensive strategies in reducing transmission risks. Consequently, the current study explored the multifaceted HEV aspects within occupational risk context among food handlers in Klang Valley, Malaysia.
Methods
The study design
A questionnaire-based cross-sectional study designed to target the food handlers in Klang valley, Malaysia, was employed in the present study. After reading the questions, the respondents’ answers were filled in by the investigators to avoid disturbing their work and reduce the nonresponse biases. A convenience sampling approach was applied in this study. It was conducted from December 2021 to March 2022, involving food handlers of 18 years and above that handled raw meat and seafood directly on food premises. The exclusion criteria applied were language barriers, including unfamiliarity with English and Malay.
Study instrument
A questionnaire with five domains was utilized to collect data in the present study. The domains were demographic details, hepatitis and HEV awareness, HEV knowledge (10 items), disease prevention practices (5 items), and immunization attitude (8 items). An extensive literature search in English was performed before adapting the questions from previous studies.Citation17,Citation22–25 Content validation is imperative in establishing the relevance of the questions according to study objectives.Citation26 Consequently, the evaluation was conducted by six experts, involving public health specialists, medical officer from the Health Risk Assessment Unit, and research officers from Virology Unit and Occupational unit from the Institute for Medical Research.
Officers from the Institute for Medical Research and certified translators performed forward translation from English to Malay language and backward translation vice versa. Subsequently, food handlers were approached to determine the clarity and comprehension of the questions. The respondents in the present study were of Malay, Chinese, Indian and other ethnicities. Validation forms in Malay and English were provided to 10 respondents each, comprising a mixed ethnicity, resulting in satisfactory clarity and comprehension ratings respectively. The questionnaires were also piloted to 50 food handlers, which were not included in the current study. Slight alterations were made following the pilot study. The overall Cronbach alpha was 0.78.
In the knowledge domain, there were five items on transmission and symptoms with “yes,” “no” and “don’t know” answer options were included. Each correct answer was allocated one point, while no point was provided for incorrect or “don’t know” answers. The maximum point assigned for the knowledge domain was 10. The HEV preventive practices domain comprised of Likert scale-based options. The “all the time” answer was correct and provided one point.Citation27 The immunization attitude items were also assessed based on a Likert-scale (5 points), which ranged from strongly agree to disagree strongly. The answers in the domain were not scored. The respondents were informed that the HEV vaccine is unavailable in Malaysia, but China has licensed its application.Citation19
Statistical analysis
Data entry and analysis were performed using the Statistical package for Social Science (SPSS) version 29.0 (IBM, United States). Descriptive statistics was employed during respondents’ demographic details and hepatitis and HEV awareness, knowledge, practices, and immunization attitude analyses. Categorical variables were also expressed in frequencies and percentages. Chi-square test and Fisher Exact assessment determined significant differences between the variable groups.Citation28 This study applied the Fisher Exact evaluation when the expected frequency was under 5 in over 20% of the cells.Citation29
Binary logistic regression was utilized in the present study to establish associations between independent variables and levels of HEV knowledge and preventive practices and willingness to obtain vaccination if available. The variables with a p-value of less than 0.25 in the univariate assessment were applied in multivariate regression.Citation30 Each independent variable was provided with a 95% odd Ratio (OR) confidence interval (CI). Subsequently, Hosmer-Lemeshow assessment was employed to assess model fit, where p-values less than .05 were considered poor. Nevertheless, statistical significance was denoted by p-values less than .05.
Sample size calculation
The 380 sample size in the present study was determined through a proportion method supplied by OpenEpi software version 3. The software applied the n = [DEFF*Np(1-p)]/[(d2/Z21-oe/2*(N-1) + p*(1-p)] formula, where n = sample size, DEFF = design effect, N = population size, p = hypothesized percentage frequency of outcome in the population, and d = confidence limits. Given that there is no literature pertaining to HEV among food handlers in Asia, 50% was considered to be the proportion of outcome in the food handler population in Klang Valley. The current study also assumed a 10% non-response rate hence the sample size was 417.
Results
Demographic attributes
A total of 471 food handlers were approached to participate in the present study, and 400 completed the survey at an 85% response rate. summarizes the socio-demographics and job characteristics of the respondents. The mean age of the respondents was 37.5 ± 8.60 years, while their distribution was almost similar for gender and ethnicity.
Table 1. The characteristics of the respondents regarding HEV awareness (N = 400).
Hepatitis awareness
Most of the respondents involved in this study had knowledge about hepatitis (n = 334, 83.5%). Awareness was higher in the 31 to 40 years old (n = 165, 49.4%), male gender (n = 178, 53.3%), and ethnicity of Chinese (n = 106, 31.7%) groups compared to their respective counterparts. Cook (n = 219, 65.6%) and food handlers with five to 10 years of working experience (n = 192, 57.5%) also recorded higher awareness prevalence. Nonetheless, the distribution of respondents reporting awareness of hepatitis was similar between education levels.
HEV awareness
Among the respondents with awareness of hepatitis, only 18 have heard about HEV (5.4%) (see ). Most HEV-aware respondents mentioned that the knowledge was obtained in universities and training school (n = 16,88.9%), while some were educated by their family members or relatives (n = 2, 11.1%).
Knowledge assessment towards HEV
delineates the proportion of correct responses of items in the knowledge domain on transmission and symptoms of HEV among the respondents. A majority of the respondents in this study stated blood transfusion as HEV transmission mode. Nevertheless, among the food handlers that reported HEV awareness (n = 18), most expressed that the disease was transmitted through food (n = 17, 94.4%) or water (n = 16, 88.9%). Consequently, over half of the respondents (n = 217,54.3%) scored zero.
Figure 1. The proportion of respondents correctly answered the responses on items of transmission and symptoms of HEV (knowledge domain) (N = 400).
The median score for the knowledge domain was zero. Respondents who scored zero were adjudged to have poor knowledge, while those with one or more points were considered to have better knowledge. A total of 116 respondents (29%) scored five and above, with seven (3.8%) answering all items in the knowledge domain correctly. Moreover, a majority of respondents with HEV awareness (n = 18) scored five and above (n = 16, 88.9%) points, with approximately half (n = 7, 46.7%) scoring 10 points. lists the univariate and multivariate analyses of the factors associated with the paricipants’ knowledge levels.
Table 2. The multivariate logistic analysis of factors associated with HEV knowledge levels among the respondents (N = 400).
Preventive practices against HEV infections
illustrates the self reported measures against HEV infections practiced by the respondents. A total of 146 respondents scored zero (36.5%), while 19 (4.8%) obtained the maximum five points (5/5). The median score for the preventive practice against the HEV infection domain was one. Accordingly, the participants with more than one point were considered to have better practices than those who scored zero, which were considered poor. More than half of the food handlers in this study reported poor HEV prevention practices (n = 249, 62.3%). summarizes univariate and multivariate analyses of the factors associated with the practices against HEV prevention.
Figure 2. The proportion of respondents on self-reported practices against HEV infection (N = 400).
Table 3. The multivariate logistic analysis of the factors associated with level of practices against HEV prevention among the food handlers participating in the present study (N = 400).
Immunisation attitude towards HEV
A majority of the respondents in the present study had a positive immunization attitude (see ). Approximately 79% (n = 316) of the respondents intended to get vaccinated against HEV, while over half (n = 213, 53%) strongly agreed to be vaccinated if the vaccine is available in Malaysia. Among those who were not willing to get vaccinated (n = 84), 54 expressed safety (n = 49, 83.1%, p < .001) and affordability (n = 41, 78.8%, p < .001) were their concerns.
Table 4. The respondents’ immunization attitude toward HEV vaccine.
The respondents of the ‘others’ ethnicity recorded the most notable vaccination concerns (OR = 7.34, 95% CI 1.50–35.97, p = .014), followed by the cooks (OR = 6.50, 95% CI 1.200–21.16, p = .002), 31 to 40 years individuals (OR = 5.75, 95% CI 1.68–19.66, p = .005), and food handlers with a secondary school education level (OR = 2.93, 95% CI 1.08–7.99, p = .035). Nonetheless, the respondents who had concerns were open to vaccination if provided with adequate information (n = 33, 91.7%) or someone they know is taking it (n = 39, 95.1%). demonstrates the factors associated with HEV vaccination acceptability if available in Malaysia.
Table 5. The factors associated with willingness to take HEV vaccination if available.
Discussion
Only a few studies have reported HEV awareness and knowledge among different populations.Citation12,Citation22,Citation31,Citation32 Besides HEV awareness, the findings in this study provided valuable insights into hepatitis awareness levels among the respondents, where 83.5% were aware of the disease. The data also provided a better understanding of the demographic and occupational factors linked to hepatitis awareness among Malaysian food handlers.
This present study revealed a relatively lower percentage (4.5%) of HEV awareness than hepatitis. Surveys in Brazil, France, and Saudi Arabia highlighted HEV knowledge variations across different populations.Citation12,Citation31,Citation32 The studies attributed the differences to factors such as population groups, geographic dispersion, and exposure level. In this study, HEV awareness was predominantly expressed by the respondents who received tertiary education and 31 to 40 years of age group, and a majority of them gained cognizance through their universities or training schools. The results revealed that targeted education could be a potential path for improving HEV awareness.
The data in this study indicated HEV knowledge gaps among the food handlers. Poor awareness among the respondents might be due to the disease being an emerging and is not notable.Citation22 Despite the biases, the results produced several interesting findings on HEV knowledge. This could be corroborated with our findings that hepatitis awareness contributed significant differences in the scores for the HEV knowledge.
Furthermore, most of the respondents reported blood transfusions as HEV transmission mode, which emphasized potential knowledge gaps among food handlers, who are in the high-risk group of contracting the disease. Nonetheless, a notable perception shifts among the respondents on HEV awareness was documented. A substantial majority of the food handlers attributed transmission to contaminated food or water. The findings highlighted the pivotal role of enlightening the respondents on the transmission modes in the occupational exposure context.
The zero score and median obtained by most respondents in the knowledge domain were expected. The data indicated a widespread lack of awareness and understanding about HEV transmission and symptoms among the food handlers. Nevertheless, the respondents with HEV awareness expressed better knowledge. A previous study reported food handlers possessing tertiary education demonstrated a greater knowledge of foodborne pathogens compared to their counterparts.Citation25 Similarly, in the present study, the food handlers with better knowledge were those who received tertiary education. This highlights the role of education in fostering a deeper understanding of HEV and, consequently, in promoting more effective practices for its prevention.
The findings in this study emphasized that targeted educational programs are necessary to improve awareness and knowledge among individuals with lower educational backgrounds. The objective could be achieved through integration into food handling courses, aligning with the regulatory framework in Malaysia, where attending such courses is mandatory for acquiring or renewing a food handlers license.Citation17 Utilizing existing educational platforms could be a beneficial strategy to enhance HEV awareness and knowledge among the high-risk population group.
Good hygienic practices are critical in managing and preventing disease.Citation17 Nonetheless, some reports have revealed poor translation into practices despite of good personal hygiene knowledge.Citation24,Citation33 Similarly, the results on HEV prevention measures among the respondents in the current study revealed a worrying trend, where over half reported poor practices. Another survey among food handlers noted that employing soap for handwashing and drinking water source were statistically significant risk factors for HEV seropositivity.Citation34 Alarmingly, less than a quarter of the current study respondents reported using soap to wash their hands after handling raw foods, Emphasizing a specific area of concern. Nevertheless, the respondents with HEV awareness had better prevention practices than the rest, implying that awareness is imperative in disease control.Citation35
In this study, the willingness to receive HEV vaccine despite its unavailability revealed an interesting scenario. A substantial 79.1% of the respondents involved in the current study expressed a desire to be vaccinated against HEV, with 53% stating strong agreement despite their low awareness. The results highlighted positive attitudes toward preventive measures. The unique focus of this study on HEV vaccine acceptance despite its unavailability in the country is particularly significant, considering comparable data scarcity.
Several reports noted that the acceptance rates for hypothetical dengue and coronavirus 2019 (COVID-19) vaccines were higher (88.4–94.3%).Citation36–38 Hypothetical dengue vaccine acceptance was also notably high at 88% in different states of Malaysia, even with approximately three-quarters of the participants having a moderate level of knowledge on dengue.Citation36 A similar response was recorded to the COVID-19 vaccine.Citation37,Citation39 Receptiveness to immunization despite limited awareness implied a potential openness to new vaccine introduction. Consequently, leveraging disease awareness would aid the successful implementation of new vaccines.
The present study also elucidated factors affecting the willingness to take vaccination. Respondents aged 31 to 40 years showed a higher inclination toward HEV vaccination compared to the younger demographic (18 to 30 years). Conversely, in an another survey, the younger demographic demonstrated a greater willingness to obtain the COVID-19 vaccine among the general population of Malaysia.Citation39 However, in present study, the demographic group aged 31 to 40 reported having better knowledge than their counterparts, which could be attributed to this variation.
In the current study, the respondents who received tertiary education recorded 2.83 times more willingness to be vaccinated than their counterparts. The findings concurred with other studies on COVID-19 vaccine acceptance in low- and middle-income countries.Citation40,Citation41 Conversely, COVID-19 and hypothetical dengue vaccine acceptability among Malaysians documented no significant differences when considering education level.Citation36–38 The inconsistencies might be due to population variations.
An advantage of this study was evaluating ethnicity as a factor in predicting intention to receive the HEV vaccine, particularly in of the diverse, multiracial population in Malaysia. A study revealed higher seropositivity rates of anti-HEV immunoglobulin G (anti-HEV IgG) among Chinese blood donors in Klang Valley, Malaysia (n = 19, 95%), than other ethnic groups.Citation21 The current study recorded Chinese and Indian respondents 5.94 and 6.04, respectively, times higher openness be vaccinated than their Malay counterparts.
Although the findings in the current study contradicted the results of survey on the hypothetical dengue vaccine, in which the Malay participants were more willing to receive the vaccine, the higher level of knowledge in dengue did affect the acceptability rate.Citation36 Furthermore, on the results of COVID-19 vaccine acceptance in another study revealed the respondents’ concern about the halal status of the vaccine.Citation37 Non-halal vaccines are forbidden under Islam, hence they could be a barrier to Muslims to be vaccinated. Consequently, considering the factor during vaccine production is imperative. The present study noted the limitation in assessing the mentioned concern, which requires consideration in future studies.
The present study also highlighted the influence of job characteristics on the intention to receive HEV vaccination. Specifically, the cooks involved in this study exhibited a more significant purpose to be vaccinated, than the helpers. Moreover, the respondents with one to five and six to 10 years of working experience were more willing to take the HEV vaccine, respectively, than those who have worked less than a year. These findings could be corroborated with higher hepatitis awareness predominance among them, suggesting that occupation-specific knowledge significantly influences attitudes toward immunization.
The importance of hepatitis awareness in affecting vaccination acceptability was highlighted in the current study. Although HEV awareness was not a predictor, creating awareness about HEV disease could be critical in preparing food handlers to protect themselves from infection. Furthermore, disease awareness is a primary factor that motivates individuals to participate in surveillance.Citation12 Heightened HEV awareness could aid sub-high-risk group identification within the population. A proactive surveillance approach could also be invaluable in determining immunization strategies. Moreover, fostering awareness could contribute to developing a positive attitude toward immunization when the vaccine becomes available.
Vaccine perceptions and acceptance among respondents were determined in the present study. Although most respondents recognized vaccines as a protection against infections, no significant parameters that influenced the perceived benefits of vaccines toward vaccinated willingness were identified. This study also highlighted the importance of addressing barriers toward vaccination acceptance, a crucial consideration for policymakers in managing future interventions. Vaccine affordability concerns were a notable factor influencing vaccination intentions among the respondents.
The contextual nature of vaccine safety concerns was revealed in the current study. Interestingly, vaccine safety concerns did not significantly correlate with willingness to be vaccinated despite the vaccine being only licensed for application in China. The perception that vaccines are safe for consumption if available in Malaysia due to regulatory processes might have contributed to the findings. A study in Malaysia found that more participants believed vaccines registered with the Ministry of Health were safe for usage.Citation36
In this study, the subgroup of respondents unwilling to obtain HEV vaccination represented a significant strength. Comprehending vaccine hesitancy, characterized by safety and affordability concerns with potential openness for vaccination upon availability under certain conditions, could provide valuable insights for stakeholders and policymakers for future interventions.
One of the limitations of this study was that the respondents were only from one state. The regional specificity requires caution in generalizing the findings to the entire nation, considering the diverse cultures and beliefs across the different states in Malaysia. Moreover, opting for convenience sampling might be a drawback in inferring the results on the whole population. Nevertheless, the study contributed valuable perspectives for future interventions and emphasized the need for more comprehensive, multi-state studies to enhance finding generalizability on similar topics.
Conclusions
The current study provided information on hepatitis and HEV awareness levels among Malaysian food handlers. The data highlighted a significant knowledge gap. Demographic and occupational factors influencing awareness highlighted the importance of targeted educational initiatives. Furthermore, respondents who were aware of HEV exhibited better prevention practices than their counterparts, demonstrating the role of education in fostering understanding. The results emphasized creating awareness to facilitate surveillance efforts, aiding sub-high-risk group identification, and shaping effective prevention measures, including disease prevention and immunization practices. Nonetheless, poor HEV prevention practices indicated the urgent need for intervention. The action is imperative not only for HEV but also to address the broader risk of other infectious diseases with similar transmission routes that food handlers might be susceptible to. Notably, the respondents’ significant willingness to be vaccinated upon availability despite low awareness reflected a positive attitude toward immunization. The receptiveness to preventive measures was also encouraging. The observations suggested food handlers’ readiness to adopt new vaccines even with limited awareness.
Author contributions
Conceptualization, S.R., W.L.P. and S.S.A.T.; methodology, S.R. and S.S.A.T.; software, S.R.; validation, S.R. and S.S.A.T.; formal analysis, S.R.; investigation, S.R., Y.V. and S.S.A.T; resources, S.R.; data curation, S.R.; writing – original draft preparation, S.R.; writing – review and editing, S.S.A.T., W.L.P. and Y.V.; visualization, S.R.; supervision, W.L.P and S.S.A.T.; project administration, S.R. All authors have read and agreed to the published version of the manuscript.
Informed consent statement
Informed consent was obtained from all subjects involved in the study.
Institutional review board statement
The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board (or Ethics Committee) of Medical Research and Ethics Committee, Malaysia (protocol code NMRR-21-1621–60740) for studies involving humans.
Acknowledgments
The authors are grateful to the Director General of Health of Malaysia for his permission to publish this article. In addition, the authors would like to thank the Deputy Director General of Health (Research and Technical Support) and the Director of the Institute of Medical Research (IMR), Director of Food Safety and Quality Division for their support and the respondents who willingly participated in this study. We would like to acknowledge the external reviewer of this paper as well.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Additional information
Funding
References
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