Knowledge, attitude, and practices (KAP) and risk factors analysis related to cystic echinococcosis among residents in Tibetan communities, Xiahe County, Gansu Province, China

Graphical abstract

Dogs are often feed with internal organs of livestock in Tibetan communities, where home slaughtering is still popular.

Highlights

• •A community based cross-sectional study of CE was conducted in Tibetan communities.
• •This is the first knowledge, attitude, and practice (KAP) study of CE in the areas.
• •Most of residents had positive attitude toward treatments of the disease.
• •Their practice about prevention and control of the disease was not so good.
• •Feeding dogs with offal is still one of risk factors of CE transmission.

Abstract

Cystic echinococcosis (CE) is a global parasitic zoonosis caused by Echinococcus granulosus. The disease is highly endemic in western China, especially in Tibetan areas, because of poor economic development and hygiene conditions, limited community knowledge of CE, a large scale of dogs, and home slaughtering of livestock. Although many researchers have analyzed risk factors of CE transmission in Tibetan Plateau, there are rare reports of knowledge, attitude, and practice (KAP) of residents about CE in Tibetan communities. In our current study, community based cross-sectional study was conducted in three townships in Xiahe County, Gannan Tibetan Autonomous Prefectures of Gansu Province from May to September 2013. A total of 972 participants originating from Tibetan communities of 31 villages in the 3 townships were registered and data were collected using structured questionnaires. From the total of 972 study participants (457 males and 515 females), 65.9% heard of the disease CE. Most of them (96.1%) would like to accept CE inspection. About half of the peoples feed their dogs often and major of them do not play with the dogs. Risk factors included resident, knowing dog could be infected, knowing eating could be route of infection, oldest dog's age, usually feed your dog by self, feed dogs with internal organs. In general our findings showed that most of residents had positive attitude toward treatments of the disease, but their practice about disease prevention and control was low. Therefore, our study called for continued and strengthened education of changing the life style, especially the behaviors related to dogs.

1. Introduction

Human cystic echinococcosis (CE) or hydatid diseases is caused by larval stage of Echinococcus granulosus. People acquire the infection by accidental ingestion of Echinococcus eggs voided in the feces of infected dogs. It is one of the most geographically widespread helminth zoonoses (Schantz, 1991). CE is a chronic, systemic disease characterized by long-term growth of metacestode (hydatid) cysts in the intermediate host. It has been reported that there are 10 genotypes (G1–G10) within E. granulosus (Alvarez Rojas et al., 2014). Three genotypes (G1, G3, and G6) have been found in China (Bart et al., 2006; Yan et al., 2013). All of these strains are infectious to humans. The adult stage of E. granulosus consist of tapeworms that reside in the intestines of the definitive host (dogs, foxes, and other canids) that become infected after ingesting organs of infected intermediate hosts containing hydatid cysts. The synanthropic cycle involving domestic dogs and livestock (e.g., sheep and cattle) is the most common transmission pattern and the main source of infection for human (Eckert, 2001).

E. granulosus has a worldwide geographical range and occurs in all continents and in circumpolar, temperate, subtropical, and tropical zones. The highest prevalence of the parasite is found in parts of Eurasia, Africa, Australia, and South America (Eckert, 2001). Although control programs were established in many areas, recent surveys show that CE is persisting in many parts of the world, and re-emerging in some countries (Eckert et al., 2000).

In China, human CE is known as one of the major public health problems with increasing concern (Wang et al., 2008). E. granulosus has been identified endemic in at least 21 of China's 31 provinces, autonomous regions and municipalities, corresponding to approximately 87% of the country's territory (Wang et al., 2008; Wen and Yang, 1997). The highest prevalence of CE locates in the northwestern provinces and regions, including the provinces of Xinjiang, Qinghai, Gansu, Ningxia, Inner Mongolia, Tibet, and parts of Sichuan and Yunnan (Bai et al., 2002; Wang et al., 2014; Yang et al., 2006, 2009; Yu et al., 2008).

Gansu Province, with a population of 2.56 million, is one of the provinces in the north-western region. Even though it has been controlled for 10 years, the serological prevalence of CE remain comparatively stable, about 10% (Anonymous, 2005; Jiang, 2002). Xiahe County is the most important grazing land of Gannan Tibetan Autonomous Prefecture, Gansu Province. The inhabitants of Xiahe County are primarily herdsmen of the Tibetan ethnic group. Due to their physical environment, socio-economic situation, and religious beliefs they live under conditions with a poor standard of hygiene and have a close relationship with their livestock and dogs. Deworming of dogs is not widely performed though anthelmintics are provided free by the local CDC.

As an infectious disease, the success of CE prevention and control programs depends on the community cooperation of the affected people. Understanding of the disease-related knowledge, attitude, and practices of the community is the important determinants of community participation in the program implement. There for we conducted this community survey to investigate the knowledge, attitude, and practices of residents toward CE and risk factors analysis for transmission of E. granulosus in Xiahe County, Gansu Province, China.

2. Methods

2.1. Study area and population

Xiahe County is located in the southern part of Gansu Province at an altitude of approximately 2200–3600 m above the mean sea level. This county is ethnically diverse with members of different populations such as Han, Tibetan, Hui, Mongolian, 18 ethnic groups in all. The Tibetans of Gansu Province live primarily in the Gannan Tibetan Autonomous Prefecture, of which Xiahe County is part. The population exceeds 80,000, who live on an area of 6274 square kilometers. Xiahe County, one of the key pastoral areas in Gansu Province, is culturally Tibetan and has a population composed primarily of herdsmen, who live in close contact with their own and stray dogs. Even though the numerous stray dogs can be vicious, villagers will not destroy them, or let outsiders destroy them, due to their strong Buddhist religious beliefs. Poor socioeconomic and hygiene conditions, in addition to a close relationship with these dogs, lead to an extremely high Echinococcus spp. prevalence in the current human population.

2.2. Study design and sample size calculation

A community based cross-sectional study was adopted to process this study, and multi-stage cluster random sampling methods were used to collect the study samples. The calculation (N = t²PQ/d²) of the sample size for cross sectional study was adopted. Where t is the statistic of t-distribution, P is the prevalence, Q = 1 − P, and d is the tolerance error (precision).

According to the data from Gansu Centers for Disease Control (CDC), the serologically positive rate of CE in was about 9.45%. For people, P = 0.0945, Q = 0.9055, α = 0.05, Z_α = 2, and d = 0.2P. The sample size was N ≈ 958. It was a cross-sectional study, and we just considered the predicted prevalence (P), precision (tolerance error d), and alpha (α = 0.05) while calculating the sample size. The lifestyle (nomadic life) of villagers in each village was the same as all households live far away from each other and evenly spread out in the county. We omit the design effect (DEFF), but we expanded the search scope and collected much more villages in the research.

2.3. Sampling techniques

Multi-stage cluster random sampling methods were used. Firstly, three townships were randomly selected (all of the townships were numbered in SPSS, and a column of corresponding random numbers were created, which were descending ordered; then, the first three numbers were selected and the corresponding townships were selected); secondly, all of the villages from these three townships were numbered for selection, then 15 villages were randomly selected (the selection method was the same as that in the first step) and the lists of households for 15 villages were collected from the township governments or health centers. All of the households were numbered for selecting, and 300 households (altogether 3–4 family members of each selected household) were selected for research (the selection method was the same as that in the first step).

2.4. Questionnaires and survey methods

For each participant, two questionnaires were completed with the help of translators. The first questionnaire consisted of three sets of questions. The first set of questions includes general information about the participant, such as village name, occupation, and livestock ownership. The second set focuses on the environment and heath. Information on water source, hygiene conditions and any previously diagnosed cases of human CE in the household is also obtained. The last set is a form for recording the results of examinations, including ultrasound and laboratory investigations. The second one was the KAP questionnaire, which was used to evaluate knowledge, attitude and practice with respect to CE. Questions about dog were asked, including the feeding habits of dog, daily contact with dog, how to deal with purgation if feces could not be collected, and whether or not there were stray dogs in the area.

Almost all of the participants were Tibetan, and they could only speak Tibetan language, which researchers could not speak. So, local health workers were hired as investigators to ask these interviewees questions and to fill in the questionnaires. Two training sessions were organized before the formal investigation. We asked the investigators to read these questionnaires carefully and try to translate them into Tibetan language as detailed as possible. The questionnaires were modified twice after pilot study, in which the questionnaires were filled by a few Tibetan herdsmen with the translation of investigators. The final version of questionnaires was also revised by experts of WHO. According to the lists of the households (selected by cluster random sampling), the researchers and local health worker were divided into three groups and search for the participants in three directions in the snowing prairie.

All of the participants were also received abdominal ultrasound evaluation using a portable ultrasound machine by trained doctors. After the abdominal ultrasound, all the participants were asked to give a 2 ml venous blood sample for detection of antibodies against E. granulosus using a commercial ELISA Kit (Diagnostic Kit for IgG Antibody to Hydatid (ELISA), Zhuhai S.E.Z. Haitai Biological Pharmaceuticals Co., Ltd., China).

2.5. Data management and analysis

Epidata 3.0 was adopted for data entry. Double entry and recheck by a third person were also adopted to ensure the data accuracy. The database was generated which included patients for further epidemiological analysis to describe prevailing CE. Risk factors were identified by univariate and multivariate logistic regression analyses (conditional forward method was adopted, entry criteria is 0.05, and removal criteria is 0.10). All of the statistical analyses were carried out using SPSS 20.0 software (SPSS Inc., IBM, Chicago, Illinois, USA).

2.6. Ethical considerations

Ethical approvals for all works were obtained from the Medical Sciences Expert Consultant Committee, Beijing Health Bureau, Beijing, P.R. China and the WPRO's Ethics committee, Manila. In this study, informed consents were used to introduce to study participants to the procedures and to convince them that all data on this survey would be kept confidential.

3. Results

3.1. Distribution of the participants

A total of 972 participants coming from Tibetan communities of 31 villages in 3 townships in Gansu Province were registered and asked to fill the questionnaires. Population sample (age ranged from 5 to 91 years; mean 36.18 years) comprised 53% (515) females and 47% (457) males, and the means of age were 35.9 for male and 36.9 for female. Persons of Tibetan ethnicity comprised 910 of the sample population. The other participants listed their ethnicity as Hans (5.7%). About 83.4% (811) were herdsmen who raised livestock including yaks, sheep, and/or goats as the primary source of their income. Other listed occupations included part-time herdsman (14.4%), farmer (1.2%). Regarding their level of education 372 (38.3%) were unable to read and write, and Buddhism was the dominant religion 964 (99.2%) in these area. Among all the participants, half chose settle life style and half chose nomadism. The majority of participants drunk the water from spring 512 (52.7%) or river 499 (51.3%), only 163 (16.8%) people could drink running water. For Livestock slaughter methods, most of them chose to slaughter at family. More details were shown in Table 1.

Table 1.

Demographic information for participants in Tibetan townships of Gansu province.

Items	Frequency	Proportion
County
Ganjia	324	33.3
Madang	320	32.9
Sangke	328	33.7
Gender
Male	457	47.0
Female	515	53.0
Races
Tibetans	910	93.6
Hans	55	5.7
Huizu	7	0.7
Occupations
Herdsmen	811	83.4
Part-time herdsman	140	14.4
Peasant	12	1.2
Education
Student	1	0.1
Preschooler	136	14.0
Illiteracy	372	38.3
Primary school	288	29.6
Middle school	143	14.7
High school or above	14	2.3
Religion
Buddhism	964	99.2
Islam	6	0.6
Other	2	0.2
Resident
Settle	423	43.5
Nomadism	402	41.4
Settle and nomadism	132	13.6
Serological tests
Positive	92	9.5
Negative	880	90.5

3.2. Knowledge on CE among study subjects

There were five questions concerning Knowledge in KAP questionnaire. Among the total participants, 641 (65.9%) had heard the disease, 320 (32.9%) knew the symptoms of CE. Eight hundred sixty two (88.7%) interviewees responded that they understood which animals might suffer from this disease too, among which 618 (63.6%) believed sheep, and 244 (25.1%) thought dog. Six hundred thirty (64.8%) respondents knew how humans were infected by hydatid disease. Although most families have dogs, only less than half participants 464 (47.7%) knew that playing with dogs could make themselves get infected with hydatid disease. More details were shown in Table 2.

Table 2.

Knowledge on CE among study participants in Tibetan townships of Gansu province, 2013.

Items	Frequency	%
1. Do you know echinococcosis disease?
Yes	641	65.9
No	331	34.1
2. Which are the symptoms of echinococcosis?
Don’t know	411	42.3
Asymptomatic abdominal discomfort	320	32.9
Gastrointestinal symptoms	241	24.8
3. Do you know which animals may suffer from hydatid disease?
Sheep	244	25.1
Dog	618	63.6
Horse	125	12.9
Bull	153	15.7
Mouse	7	0.7
Other animals	4	0.4
4. Do you know how humans are infected by hydatid disease?
Through the air	25	2.6
By eating	630	64.8
Through sexual contact	1	0.1
Through blood transfusion	7	0.7
5. Do you know that playing with dogs could make you get infected with hydatid disease?
Yes	464	47.7
No	358	36.8
I don’t know this disease	150	15.4

3.3. Attitude of participants toward CE in Xiahe County

Five questions were concerning the Attitude of participants toward CE in the KAP questionnaire. Most of participants (934, 96.1%) would like to accept hydatid disease inspection, and 851 (87.5%) to take free medicine treatment if suffering from it. According the reason why they do not want to take medicine, 298 (30.7%) were “because felt uncomfortable,” 168 (17.3%) were “because had other diseases not suitable for medicine,” and 57 (5.9%) were “because they thought the curative effect of medicine were not good enough.” More than 75% of the respondents (753, 77.4%) said that they would like to accept the surgery if they need surgery because of echinococcosis. More details were shown in Table 3.

Table 3.

Attitude toward CE among study participants in Tibetan townships of Gansu province, 2013.

Items	Frequency	%
6. Would you like to receive hydatid disease inspection?
Yes	934	96.1
No	22	2.3
Not decided	16	1.6
7. Did you have a medical check-up recently?
By ultrasound	831	85.5
Blood test	203	20.9
Don’t know	84	8.6
8. If you have suffered from echinococcosis, would you like to take free medicine treatment?
Yes	851	87.5
No	49	5.0
Have not decided	72	7.4
9. If you don’t want to take medicine, why is that?
Not comfortable	298	30.7
Curative effect not good	57	5.9
There may be other diseases, not suitable for medication	168	17.3
10. If you need surgery because of echinococcosis, would you like to undergo surgery?
Yes	753	77.4
No	101	10.4
Have not decided	118	12.1

3.4. Practice of participants on CE in Xiahe County

Among all the participants, 183 (18.8%) never tie up their dogs. People who often feed their dog (440, 45.3%) and who not often (532, 54.7%) were about half and half. The majority (734, 75.5%) do not play with the dogs usually. Six hundred fifty six (67.5%) respondents clean up the dog feces never. Regarding the usage of dog feces, the majority (735, 75.6%) did not use it for any purpose, like fertilizer, methane production, or fish feed. Among the dogs of the participants, 606 (66.4%) dogs often ate animal internal organs and 126 (13.0%) never been medicated. Regarding how to deal with the internal organs when they slaughter livestock animals, 173 (17.8%) of respondents chose to use it to feed dogs. Most of participants (930, 94.1%) ate foods at home with chopsticks, but 214 (22.0%) wash hands before eating only occasionally. More details were shown in Table 4.

Table 4.

Practice of respondents toward CE prevention and control in Tibetan townships of Gansu province, 2013.

Items	Frequency	%
11. Do you tie up your dog?
Never	183	18.8
Always	622	64.0
In the day time	160	16.5
Only for the night	7	0.7
12. Do you usually feed your dog?
Yes	440	45.3
No	532	54.7
13. Do you usually play with the dog?
Yes	238	24.5
No	734	75.5
14. Do you always clean up the dog feces?
Yes	316	32.5
No	656	67.5
15. Is there a use for dog feces?
As fertilizer	159	16.4
None	735	75.6
Methane production	13	1.3
Fish feed	48	4.9
Other	51	5.2
16. Does your home dog often eat below food?
Animal internal organs	606	66.4
Small animals	78	8.0
None of above	308	31.7
17. Does your home dog often medication?
Never	126	13.0
Often	270	27.8
Occasionally	433	44.5
Don’t know	143	14.7
18. How do you eat food in your home?
By hand	26	2.7
With a spoon	16	1.6
With chopsticks	930	94.1
19. When you slaughter livestock animals, what do you do with the internal organs?
Throw away	770	79.2
Eat	117	12.0
Use to feed dogs	173	17.8
Bury or burn it	16	1.6
20. Do you wash your hands before you eat?
Often	591	60.8
Sometimes	167	17.2
Occasionally	214	22.0

3.5. Risk factors analysis of CE

Risk factors were identified by binary logistic regression analyses. The dependent variable was the results of Serological tests. There were six variables selected in the model, which were resident (nomad vs. settle down), knowing dog could be infected (knowledge of KAP), knowing eating could be route of infection (knowledge of KAP), oldest dog's age, usually feed your dog by self (practice of KAP), feed dogs with internal organs (practice of KAP). Two knowledge related variables were protective factors: knowing dog could be infected (OR = 0.422), knowing eating could be route of infection (OR = 0.248). The others were risk factors. The model was significant (P < 0.05). More details were shown in Table 5.

Table 5.

Variables and odds ratios for variables selected by logistic regression model.

	P	OR	OR 95% CI
			Lower	Upper
Resident	0.010	2.136	1.203	3.792
Knowing dog could be infected	0.008	0.422	0.223	0.796
Knowing eating could be route of infection	0.004	0.248	0.096	0.638
Oldest dog's age	0.005	1.120	1.034	1.214
Usually feed dogs by self	0.001	2.597	1.466	4.608
Feed dogs with internal organs	0.025	1.969	1.087	3.559

4. Discussion

Human cystic (CE) caused by E. granulosus, results in the lost life abilities of patients and great economic burden in Central Asia and China. The Chinese Ministry of Health carried out a national survey in 2002 for eight important parasitic diseases, and found the prevalence of human CE was the highest (2.5%) in Tibetan communities (Craig et al., 2008). The majority of the population in Xiahe County is Tibetan with animal husbandry as their primary economy. During the seasons from spring to autumn, the Tibetan families move about in search of pasture with their herds of yaks or sheep. This typical nomadic life always carried on along with dogs and the unhygienic conditions on the grasslands highly favorable circumstances for the transmission of CE.

In 2005, a national program for echinococcosis control in China was launched, including population screening, transmission control, and improvement of sanitation. Over the past several years, considerable experience has been gained on how to interfere with transmission dynamics as a way to control E. granulosus. However, in some areas, the prevalence of CE is still at a high level, requiring strengthening of health education and training with respect to people at high-risk. Although lack of knowledge about CE was reported as one of risk factors for E. granulosus transmission, Up to the present, there was no knowledge, attitude, and practice (KAP) research among Tibetan communities. We conducted current study to screening prevalence of CE and KAP analysis on Xiahe County, Gannan Tibetan autonomous prefecture, Gansu Province, China.

Because most of the interviewees were Tibetan and they could only speak Tibetan language, during the interview, the translators (most of them were local epidemic prevention workers or other health workers) asked the participants questions and filled in the questionnaires. The training time for the translators was relatively short, and there might be some misunderstandings in the translation and some information bias while collecting information. Most of the participants with low education level might be confused at the beginning of the interview. During the whole investigating period, we could not control the conversation while investigators asked the questions using Tibetan language. To solve this problem, the same translators were employed during the whole study and they were always accompanied with researchers and asked to pay attention and to be patient.

Besides, selection bias might also exist in the study. Many male family members left home for Cordyceps Sinensis in the mountain, and could not be recruited for the study. Following the guide, we searched these persons as wide as possible in the prairie in order to find enough interviewees, and we expanded the search scope to find more participants. We collected 31 villages in the end of this study, which were over two times more than designed number of villages. There were 650 households (1–2 family members stayed in the house, and others went deep in the mountain) collected in the end of the research, which was also over two times more than designed number of households. It might decrease the DEFF while conducting the cluster random sampling and it might also narrow the potential selection bias.

Our data showed that the ultrasound prevalence of human abdominal echinococcosis was 1.0% and the serum positive rate was 9.5%, which confirms that CE is still highly endemic in Xiahe County (data will be shown in another paper).

The result of our study showed that majority of the participants (65.9%) knew about CE. This result was lower than rural–agricultural (86.0%) but higher than semi-bedouin and bedouin (55.0% and 21.7%) that from a study conducted in Jordan (Qaqish et al., 2003). Although less than half of respondents knew the symptom of echinooccosis, more than 80% of them knew that sheep and dog were the animals might suffer from CE. Sixty four percent of the participants knew humans contact this disease by eating and 47.7% of them knew that playing with dogs could get infection with CE, which was much higher than the knowing rates of all three kinds interviewers in Jordan (11.5%, 9.9%, and 2.4%). The variability between these communities might be due to a long-range supports of health education in Tibetan communities in Xiahe County from local CDC. Most of the participants would like to receive hydatid disease inspection (96.1%) and most of them would like to take medicine treatment (87.5%) if they had suffered from echinococcosis. The attitude toward of disease was positive, but the practices were below expectation. For example, they still feed dogs with animal internal organs (66.4%), and they still do not clean up dog feces (67.5%). More details about the disease should be taught to the people, and primary-level health worker should give assistance during the practicing of preventing CE.

Our survey shows that 89% participants slaughter livestock in their home, which is always dissuaded through education for echinococcosis control. Regarding the internal organs of livestock, 79.2% participants throw away and 17.8% feed dogs directly. Disposal offal is eaten by dog very likely because there are huge number stray dogs in Tibetan communities. These results are similar to a study conducted in Sardinia (Varcasia et al., 2011), where almost all farmers butchered sheep in the farms and gives raw viscera to the dogs either do not treat their dogs al all, or treat them with ineffective drugs.

There are totally different natural environments and social culture between Sardinia and Xiahe County, but our research arrived at similar conclusions: changes in behaviors of farmers and herdsmen were very limited after about 10 years campaign of echinococcosis control, especially in the methods of disposal offal and slaughter livestock. The reason of failure includes social and economic reality that there is no effective framework (Varcasia et al., 2011). Other possible reasons in Tibetan communities are language communication and life style of Tibetan herdsmen. Majority of Tibetans cannot understand standard Chinese, propaganda relies on Tibetan staffs who are not enough obviously. In addition, distances between villages are very far, usually it is need to over mountains. The numbers of families in villages are from several to dozens of range. Most of herdsmen spend more than half of year to move about in search of pasture. These life styles decide that centralized slaughtering is almost impossible in Tibetan communities.

Through the results of logistic regression model, we could infer that people who pasture in the prairie might get more chance to be infected than the people who settle down in one place (OR = 2.136). People with an outdoor life might have difficulty in finding clean water, and might have more chance of contact with stray dogs. Thus, they might more likely be infected by E. granulosus. Usually feed dogs (practice of KAP) might increase the contact with dogs. Thereby, people who feed dogs might get more chance to be infected than those who never feed dogs. The risk being infected by E. granulosus in people who feed dogs by themselves was 1.597 times more than that in those who did not (OR = 2.597). For those people who feed dogs, they should pay much attention to the practice and adopt more protection stuff.

Feeding dogs with internal organs of livestock (practice of KAP) might be another inappropriate practice, which might also increase the chance of people being infected by E. granulosus (OR = 1.969). We could also infer that the older dogs were, the more chance people might get infected (OR = 1.12). Increasing Knowledge level about CE issues might effectively protect people from being infected. People who know dog could be infected (OR = 0.422) and eating could be route of infection (OR = 0.248) might be more careful about their habit, therefore they could avoid CE more effectively than those who do not have this kind of knowledge. Though the results of risk factor analysis, we could found that dogs related issues still might be the most important reasons for CE, and we could also found KAP showed important role in the prevalence of CE (four KAP variables in six factors). Improving the living environment and the knowledge level, changing Practice (living habits) in high-risk groups might effectively reduce the risk for these people.

Our research showed that the effect of education and prevention of CE in Tibetan communities was not idealistic. Even though it has been proved that prevention or restriction of home slaughtering is an effective control method for CE in China (Craig and Larrieu, 2006), for most of Tibetan still kill livestock at home. Measures for CE control that being aimed at Tibetan communities should be implemented in following campaigns. At the same time, to achieve better results, different policies should be designed according to nomadic Tibetans and settled Tibetans. Our study is the first KAP study of CE in Xiahe County that used probability-sampling techniques and provided baseline information for further studies. Moreover, our research identified that lack of knowledge of CE are risk factors of CE transmission in Tibetan communities. These results provided evidences that education of CE would help control this disease. However, it should be noted that this study was not supported by qualitative methods.