Assessment of Knowledge, Attitude and Practices and the analysis of Risk Factors regarding Schistosomiasis Among Fishermen and Boatmen in the Dongting Lake Basin, P.R. China

Background: Fishermen and boatmen are a risk population for contracting schistosomiasis due to their high frequency of water contact in endemic areas of schistosomiasis in the People’s Republic of China (P. R. China). To develop specific interventions towards this population, our present study was designed to assess the knowledge, attitudes and practices (KAPs) towards schistosomiasis of fishermen and boatmen, and to identify the risk factors associated with schistosome infection using molecular technique in the selected area of Hunan Province in P.R. China. Methods: A cross sectional survey was conducted in the Dongting Lake Basin of Yueyang County, Hunan Province, P. R. China. A total of 601 fishermen and boatmen were interviewed between October and November 2017. Information regarding socio-demographic details and KAPs towards schistosomiasis were collected using a standardized questionnaire. Fecal samples of participants were collected and tested by Polymerase Chain Reaction (PCR), and logistic regression analysis was conducted to explore the risk factors related to the positive results of PCR. Results: Of the 601 respondents, over 90% knew schistosomiasis and how the disease was contracted, the intermediate host of schistosomes and preventive methods. The majority of respondents had a positive attitude towards schistosomiasis prevention. However, only 6.66% (40/601) of respondents had installed a latrine on their boats, while 32.61% (196/601) of respondents defecated in the public toilets on shore. In addition, only 4.99% (30/601) respondents protected themselves while exposed to freshwater. The prevalence of schistosomiasis, as determined by PCR, among fishermen and boatmen in Yueyang County was 13.81% (83/601). Age, years of performing the current job, number of times receiving treatment, and whether they were treated in past three years were the main influencing factors of PCR results among this population. Conclusions: and boatmen are still at high risk of in gaps exist in KAPs towards schistosomiasis in this population group. Chemotherapy, and health education encouraging behavior change in combination with other integrated approaches to decrease the transmission risk in environments should be improved.


Introduction
Schistosomiasis has been considered to be one of neglected tropical diseases of public health importance in tropical and subtropical areas of the world [1][2][3]. It is endemic in 78 countries and territories globally with 250 million people infected [4]. The People's Republic of China (P.R. China) used to have the world's highest disease burden of schistosomiasis caused by Schistosoma japonicum. National surveys conducted in 1950sestimated that China had 11.60 million human cases and one million infected cattle [5]. Schistosomiasis is acquired when people or domestic animals contact freshwater contaminated with free swimming cercariae of schistosomes.
During the past seven decades, great efforts have been made to control schistosomiasis through consecutive and vertical control programs by the Chinese government. This is especially true over the past decade when preventing schistosomiasis was ranked as a high priority among four important infectious diseases nationally, including HIV/AIDS, tuberculosis and hepatitis B [6]. During that time, an integrated control strategy was also implemented for schistosomiasis according to the medium-and long-term national control plan [7][8][9]. The prevalence and intensity of infections with S. japonicum in humans has been reduced substantially, and the number of endemic provinces has decreased from twelve to seven [10,11]. Currently schistosomiasis is mainly endemic in areas surrounding the Dongting Lake, Poyang Lake and beaches along the Yangtze River [12][13][14][15], with fishermen, boatmen and farmers being groups at high risk of infection and suffering the highest disease burden [16].
In spite of the great success in schistosomiasis control in P.R. China as a result of these programs, there are still enormous difficulties and challenges surrounding transmission interruption and the elimination of schistosomiasis [17]. Potential risk factors for the resurgence of schistosomiasis still exist and the prevalence of schistosomiasis can rapidly rebound in the lake and marshland region due to its unique environment [18]. Tools used to determine the infection status or prevalence of schistosomiasis in humans are still heavily reliant on traditional methods, such as Kato-Katz, which presents the increasingly obvious disadvantage of poor sensitivity, especially in low endemic situations of mild infection [19,20]. The false negative result could eventually contribute to inappropriate decisions or policies made by the government. According to the national surveillance data, floating populations, in particular, fishermen and boatmen, are becoming increasingly significant in schistosomiasis transmission [21]. Reinfection with S. japonicum among fishermen and boatmen is still a key issue impeding the transmission interruption or elimination of schistosomiasis in the lake and marshland regions in P.R. China [16].
Adequate knowledge, positive attitudes and the correct preventive practices of populations towards schistosomiasis prevention and control in endemic regions can provide an effective sustainable environment for the success and sustainability of schistosomiasis control [22][23][24]. Although health education is an important approach for schistosomiasis intervention, information on the current infection status and KAPs on schistosomiasis among fishermen and boatmen remains unclear. This study aimed at assessing the KAPs towards schistosomiasis among fishermen and boatmen in selected areas within Hunan Province of the P.R. China. Infectious status and its influencing factors were also identified in this population.

Study Design
This study was a cross-sectional survey that assessed the knowledge, attitude and practices (KAPs) on schistosomiasis, evaluated the prevalence of schistosomiasis and its risk factors among fishermen and boatmen in the study area.

Study Area and Population
The study was conducted between October and November 2017 in Yueyang county, Hunan province, which is located on the eastern bank of the Dongting Lake in southern China ( Fig. 1). Two villages, Lujiao and Matang, in this county were sampled randomly from those fishing villages with 3-5% prevalence of schistosomiasis in population determined by stool examinations last year. As typical lake and marshland endemic areas of schistosomiasis, these villages had numerous fishermen and boatmen at high risk of schistosomes infection. Fishermen and boatmen in this region commonly live or work on ships for at least four months per year, and their economic income mainly comes from fishing and goods transportation. The respondents in our study was comprised of either professional or non-professional fishermen and boatmen. All participants involved had not received any anti-schistosome treatment within a period of six months before the study.
The interviews were conducted when their ships berthed at Lujiao and Matang in Yueyang County, Hunan Province, P. R. China.

Questionnaire Survey
A pretested semi-structured questionnaire was developed after performing a thorough literature review of comparable studies [22,[25][26][27][28], to assess the KAPs of participants towards schistosomiasis prevention. This survey was conducted by well-trained interviewers who received training by professionals from National Institute of Parasitic Diseases, and was monitored by quality control supervisors who were assigned to each group before the interviews. The questionnaire consisted of four main sections. The first section covered socio-demographic information such as age, gender, education, family income, years of practices, history of receiving treatment against schistosomiasis. The  Table S1.

Sampling collection
One fecal sample from each participant was collected using a specific container, and coded by a unique identifier. The samples were then transferred to a laboratory of local schistosomiasis control station. Two grams of feces from each sample was filtered using a nylon membrane and placed in a cryopreservation tube at -20℃ within one month for DNA extraction.

Socio-Demographic Characteristics
A total of 753 fishermen and boatmen were enrolled in this cross-sectional study.
However, 122 people provided none or insufficient amounts of stool to prepare for PCR and 30 individuals had no or incomplete questionnaire data. Therefore, 601 individuals who completed the questionnaire and provided sufficient stool samples were included in the final analysis. The socio-demographic characteristics of the respondents are presented in

Attitude to Schistosomiasis Prevention and Control
Most respondents (95.34%, 573/601) indicated that they were willing to install toilet facilities on their boats. Of the 28 respindents who refused to install toilet facilities, 57.14% complained that fishing boats were too small to accommodate any toilet facilities.
With regards to visiting onshore public toilets, 96.17% (578/601) reported that they would like to use onshore public toilets, while 72.7% of respondents who were reluctant to use onshore public toilets gave the reason that it was inconvenient to go ashore to find toilets over such a long distance when they were working in the middle of the lake. The majority of respondents (98.50%, 592/601) were willing to accept examination for schistosomiasis and if diagnosed as positives, 98.50% (592/601) of the respondents expressed willingness to take medicine regularly following doctors' prescriptions. Of those surveyed, 89.85% (540/601) believed this disease could be prevented, while 71.88% (432/601) understood schistosomiasis could be cured (Table 3).

Practices towards Schistosomiasis
Of the 601 respondents, only 6.66% installed and used fecal containers in the correct way.
In terms of protective behaviors when contacting S. japonicum infested water, only 4.99% (30/601) of the respondents reported always wearing rubber shoes, gloves, protective clothing or using ointment on their skin. The main reason given by respondents who did not protect themselves when contacting freshwater in the Dongting Lake was that it was a bother (83.98% or 471/561). Only 32.61% (196/601) of the participants reported always defecating in onshore public toilets (Table 3).

S. japonicum Infection Status and Related Risk Factors
Among 601 participants who provided adequate stool samples, 13.81% (83/601) were detected as positive by PCR. The PCR amplification products of all the positive samples were sequenced and the results showed that the DNA fragment was 469 bp, which was consistent with the target DNA both in length and sequence (Fig 2). The positive rate of Schistosoma nucleic acid in males (14.78%) was higher than that of females (12.50%), but not statistically different (χ 2 =0.643 p=0.423). The subgroup of participants who were aged less than 30 years old, performing their current job for more than 30 (Table 4). In addition, the respondents who received treatment six to 10 times, or more than 10 times showed lower odds of presenting positive PCR results (OR 6-9 = 0.156 (95%CI: 0.035-0.689), OR ≥ 10 = 0.100 (95%CI: 0.021-0.476)), compared to those never receiving treatment for schistosomiasis.

Discussion
The study showed that the overall awareness of schistosomiasis control knowledge among respondents was satisfactory, which was attributed to the persistent health education conducted over the years [30][31][32]. Despite sufficient knowledge and good attitudes towards schistosomiasis prevention, the behavioral practices of fishermen and boatmen were quite unsatisfactory. People preferred to receive examinations and treatment, rather than to prevent disease altogether. Only 6.66% of respondents had installed toilet facilities on their boats and only 32.61% of respondents defecated in the onshore public toilets. There were many reasons for such findings given by the interviewed fishermen and boatmen, including the boat size and stools could overflow from containers because of boat instability, or that fecal odors could make such containers intolerable on board. Of the respondents, only 4.99% protected themselves when contacting freshwater, and the main concern of such respondents was that it was troublesome and inconvenient to wear protection apparatus when fishing or working on the water. Adequate knowledge and positive attitudes did not convert to effective behavior changes, mainly due to the strong economic drive of their work, which agreed with previous studies [22,33].
The gaps observed between knowledge, attitude and practices indicated that effective methods and enormous efforts should be made to better address the problem of transmission caused by behavior approaches. First, appropriate health promotion activities should be provided to this high risk population. Second, existing interventions should be improved or modified to be more accessible and attractive to fishermen and boatmen. Finally, integrated approaches to eliminate the transmission risk of schistosomiasis in freshwater areas should be further explored and strengthened [14]. The prohibition of fishing activities is going to be implemented along the Yangtze River, which can assist in handling the current situation. An effective monitoring system needs to be established and run efficiently to guarantee this policy.
In P. R. China, a two-step detection pattern with serological screening first, followed by stool examinations for serological positives is used for the field diagnosis of schistosomiasis in China [16]. This method presented great advantages in earlier programs because of its enormous capacity for large scale screening and examination. However, with the persistent implementation of integrated control strategies for schistosomiasis, the prevalence and intensity of schistosomiasis in China has reached a historically low level [20,34]. The infected fishermen and boatmen can be easily misdiagnosed by traditional methods, such as the Kato-Katz method or miracidia hatching technique, and therefore, are not targeted for medication, which brings great challenge to the elimination of schistosomiasis in China [35,36].
As a classic nucleic acid amplification technique, PCR has many advantages over stool examinations, such as higher sensitivity and specificity, the low cost of reagents, and the availability of universal equipment in laboratories, which will facilitate schistosomiasis detection in the future [37]. It was reported that only 2.16 eggs per gram of feces were required to detect schistosomiasis by PCR [37]. This study found a high burden of schistosomiasis in fishermen and boatmen in Yueyang County using PCR (13.81%), which is higher than the average prevalence obtained from the national surveillance system [16,22,38]. The following considerations are therefore initiated for discussion. Firstly, the study population generally spend most of their lives onboard and are in frequent contact with S. japonicum infested water , which is thought to be the main reason for their vulnerability to infection and re-infection by schistosomes [36,39]. Secondly, interventions against schistosomiasis were difficult to cover all fishermen and boatmen due to their high mobility [25,40]. Although treatment should be delivered to fishermen and boatmen with high risk of schistosome infection according to local treatment strategy, 4.16% of respondents had never received treatment and 36.61% had only received treatment two years before our study. Thirdly, our study used a nucleic acid-based detection method rather than traditional methods. The PCR technique used in this study had an excellent sensitivity as it could detect 10 pg/μl of schistosome genomic DNA (based on internal assessments), as well as great specificity reflected by DNA sequencing of the PCR products. Therefore, PCR could facilitate the diagnosis and treatment of individuals with low-level infections and assist in the elimination of schistosomiasis in P.

R. China.
Logistic regression analyses showed that four variables, including age, years of performing the current job, times received treatments in history, and whether received treatments in the past three years were significantly associated with the PCR results.
Younger fishermen and boatmen are more likely to be infected by schistosomes, which is similar to results of previous research [25]. As the main labor forces of their families, young fishermen and boatmen are more likely to be involved in fishing or household chores, which means higher frequency and greater level of exposure to S. japonicuminfested water, therefore, increasing the likelihood for infection. In addition, there are also studies showing that aged fishermen and boatmen with long-term exposure to water can produce an acquired immunity towards Schistosoma, which protects them to a certain degree [6]. It was found that the number of years performing the current job was positively correlated with the infection of S. japonicum. Study findings showed that the prevalence decreased significantly with increasing treatment times among this population.
Prevalence was higher in the participant subgroup that did not receive any treatment in the past three years. These results all indicated that PZQ treatment is still an effective way to control schistosomiasis among this population, so as to promote the elimination of schistosomiasis in P.R. China [26].
One of the limitations of this study is that 152 fishermen and boatmen were excluded from the final analysis due to incomplete response on the questionnaire or lack of stool samples for PCR test. This might have impact on the study's results. On the other side, such phenomenon reflected the difficulties of conducting control or prevention activities in low endemic areas after many years of intervention. To eliminate schistosomiasis, new approaches should be considered and explored how to improve the coverage rate of control activities on risk population and increase their compliance to ensure the effectiveness of intervention activities. China (20170717). During these meetings, the objectives of the study, the study procedures, sampling, study benefits, and potential risks and discomforts were orally explained and informed to all participants. All adult participants gave informed consent, and informed consent for all children who participated in the study was sought from parents or legal guardians. Assent was sought from all participants who were also informed of their rights to refuse to participate in this study and to withdraw from the study at any time. Participants with positive PCR results received free treatments with a standard dose of praziquantel.

Consent for publication
Not applicable.

Availability of data and materials
All relevant data are contained within the paper and its additional files.

Competing interests
The authors declare that they have no competing interests.

Funding
This study was financially supported by the National Special Science and Technology province, for permission and support.