1. Introduction
Echinococcosis, also referred to as hydatid disease, is a zoonotic parasitic disease that seriously endangers the health of humans and imposes a heavy financial burden on sick families [
1,
2,
3]. Human echinococcosis is caused by tapeworms of the genus Echinococcus [
4,
5]. To date, six forms of this tapeworm have been identified, and four of these represent a public health concern:
Echinococcus granulosus,
E. multilocularis,
E. vogeli and
E. oligarthrus, which cause cystic echinococcosis (CE), alveolar echinococcosis, polycystic echinococcosis and unicystic echinococcosis, respectively [
6,
7]. CE is one of the most common forms and is therefore of significant relevance to humans from a medical and public health point of view [
8]. Data from the World Health Organization (WHO) shows that CE is distributed globally, except for Antarctica [
9]. Worldwide, more than one million people are affected by echinococcosis at any one time [
9].
China is one of the countries reporting the highest prevalence of human echinococcosis in the world, dominated by CE [
10,
11]. Echinococcosis is common in Western China and key areas in the Qinghai-Tibet plateau [
12]. A previous study of the endemic status of echinococcosis [
13] showed that a total of 10,790 cases of echinococcosis were reported in China between 2004 and 2008, and that 98.2% of patients with echinococcosis resided in China’s Western Xinjiang Uygur Autonomous Region, Inner Mongolia Autonomous Region, Ningxia Hui Autonomous Region, Sichuan, Qinghai, and Gansu provinces.
CE is widely distributed in Western China, but its spatial distribution, and the environmental factors driving its prevalence, are not clear. This study aimed to identify the geographical environment factors that affect the spatial distribution of human CE from a regional perspective. Numerous studies [
14,
15,
16,
17,
18,
19,
20,
21,
22,
23,
24] have shown that human CE is closely related to natural, cultural environmental factors, including temperature, rainfall, elevation, vegetation, land use, education, economics, religious beliefs and professional factors; collectively, these factors are thought to underlie the epidemic transmission dynamics of human CE. Over recent years, several studies have evaluated the risk factors for human CE and the specific relationship between these factors and the prevalence of human CE in China. For example, Yang, Y.R. et al. [
23] surveyed the impact of anthropogenic and natural environmental changes on Echinococcus transmission over the past 50 years in Ningxia of China, and they suggested that land use and micro-climate are important for the transmission cycles of CE. In another study, Yang, Y.R. et al. [
15] surveyed 4773 individuals from 26 villages in Ningxia Hui Autonomous Region from 2002 to 2003 and revealed that potential risk factors included income and limited education. Yu, S.H. et al. [
25] conducted an investigation in Jiuzhi County, Qinghai Province, and showed that Jiuzhi County is an important endemic area for human CE, and that risk factors included the Tibetan population, herdsmen, and Buddhist priests. Related research has already been conducted, but these studies have significant limitations. Only qualitative descriptive statistical analysis, which targeted biological factors related to the risk of human CE spreading at an individual level in a local area while rarely taking a quantitative approach to the relationship between environmental factors and the distribution of echinococcosis at a regional scale. Also, the geographical distribution of epidemic diseases has its specific regions. In some places, the disease is distributed and highly prevalent, while in some others, it is not and at low levels. This article addresses the geographical environment background cause of these phenomena, i.e., the significance of this study is to explain the ecological background (ecological driving force) of geographical distribution heterogeneity of human infection rate from a macro perspective (county-level). At the same time, since the distribution of human CE is unknown in all counties in seven western provinces and the prevalence data of echinococcosis are very scarce, leading to inconsistent data acquisition times, it is necessary and meaningful to make a risk prediction to prevent and control the spread of human CE in Western China. Therefore, the purpose of this paper was to determine the risk factors associated with human CE on a macro-scale (county-level) that covers seven provinces, not an individual level in a local area (one county or one village), and to gain a better understanding of the spatial distribution of human CE in Western China.
Data arising from this study could thus be used to prevent and control the spread of human CE. In order to do this, we utilized remote sensing (RS) technologies with strong information acquisition capability. We also used geographic information system (GIS) technology to allow strong geographic spatial analysis and statistical methods which could help us to analyze risk-related factors and the spatial distribution of human CE [
1,
26]. Spatial statistical analyses have been widely applied in terms of spatial distribution estimation and simulation in other aspects of environmental science research [
27]. Herein, these analytical techniques and methods were used to determine the risk factors associated with the spatial distribution of disease and to study the spatial distribution of human CE.
4. Discussion
Our present study identified that the prevalence of human CE is closely related to natural environment and cultural factors, such as precipitation, temperature, NDVI, DEM, LST, land use, occupation, and other factors. However, these factors, which relate to the immediate host of human CE and definitive host habitats, are complicated and exert combined effects, especially in the vast western region of China. Typical factors were selected and quantified using multiple linear regression model analysis (Equation (2)). Our analysis identified grassland area ratio and Tibetan population ratio as significant and positively correlated independent variables, while GDP and LST (Spring) were significant but negatively correlated independent variables. Finally, a predictive risk map of CE was created for Western China.
LST (Spring) was negatively correlated with human CE. Land surface temperature reflects a temperature variable [
38]. In particular, Echinococcus eggs are sensitive to high land surface temperature [
39], and the environment can influence echinococcosis by affecting the maturation and survival time of the eggs [
16,
40,
41]. In theory, areas with low surface temperatures could be more popular for echinococcosis. A recent study [
42] showed that deep-freezing at −18 °C to −20 °C does not kill eggs of E. multilocularis, and they can only be killed at −70 °C to −80 °C. Further research by J. Eckert [
43] showed that land surface temperature has a negative association and is involved in the transmission of CE in Rangtang County of the Tibetan plateau. The western region, due to its high altitude, has a typical plateau mountain climate, and the surface temperature remains low for years; consequently, this is a very suitable area for echinococcosis. LST (Spring) is statistically significant in multivariate regression analysis. However, multivariate regression analysis does not show that LST in autumn and winter is not related to the prevalence of human CE. A possible reason for the preliminary analysis is that LSTs (Spring) have a greater impact on the prevalence of echinococcosis than those in autumn and winter. Other possible reasons are as follows. Some studies [
44] have shown that early winter and early spring are the main infectious seasons for dogs. The larvae develop and reproduce in the dog’s gut, and large numbers of eggs are excreted through feces. Low surface temperatures in spring can affect the survival time of the eggs, which in turn may increase the probability of human infection through the ingestion of water infected with the eggs.
In our study, “Tibetan population ratio” was associated with an increased likelihood of human infection. The detection rate of Tibetan human CE was previously shown to be the highest among different ethnic groups [
45,
46]. This may be associated with the local ethnic customs and religious beliefs. Tibetans generally like to keep a large number of dogs to guard livestock and property, and they are therefore often in close contact with their dogs [
47,
48]. Furthermore, the majority of Tibetans are Buddhists, who claim to be non-violent and ban the killing of any animal, including dogs [
49]. This behavior leads to a large number of stray dogs, which tend to congregate around temples and villages, because they are fed by monks and herders [
46,
50]. Dogs also prey upon small mammals near pastures, and these dogs are usually fed by herders with the heart and lungs of cattle and sheep during the slaughtering season [
12,
47,
51]. These facts are important because dogs are the main host of echinococcosis and have been identified as the primary source of human CE [
47,
52]. Therefore, the Tibetan population ratio plays an important role in the transmission of human CE.
Grassland area ratio represents the grassland coverage density of the environment and was positively correlated with human CE. Grassland vegetation cover directly affects the distribution of intermediate hosts and plays an important ecological role in the spread of the disease [
53,
54]. Grassland is one of the habitat conditions required for the growth and reproduction of intermediate hosts, such as horse, cattle, and sheep [
23,
55]. West China is an important agricultural and pastoral area with vast grasslands, and farmers and herdsmen in this area keep a large number of cattle and sheep. As a result, a large number of cattle and sheep eat the grass, water, and soil infected with Echinococcus eggs. The larvae then develop in the guts of the intermediate host cattle and sheep, and dogs become infected by eating the guts of cattle and sheep. The definitive host dog excretes large amounts of eggs through feces, and eventually, humans become infected by ingesting food such as water infected with the eggs. This chain of events makes it possible to maintain disease transmission between grass and hosts.
GDP was also shown to have a negative effect on human CE. GDP is a common socio-economic indicator that reflects the regional economic development and household income. The underdeveloped economy is one of the main causes of the epidemic of human CE [
24,
56]. In underdeveloped rural areas of Western China, people generally do not have the awareness to accept a medical examination before the illness [
57]. The backwardness of education, lack of knowledge, and poor hygiene habits caused by economic backwardness make people vulnerable to echinococcosis. At the same time, the economic backwardness leads to a lack of medical resources, low family income, and inconvenient transportation, so that patients cannot go to the hospital in sufficient time. Indeed, some studies [
45,
58] have shown that an underdeveloped economy and low income are important factors in the spread of echinococcosis. Furthermore, Yu Rong Yang [
3] showed that household income levels strongly influenced the choice of health care provider, and despite the higher quality and more efficient diagnosis and treatment available in the city, residents preferred to seek health care in local county hospitals in Ningxia of China. A more recent study [
59] showed that echinococcosis is closely related to economic development and residents’ income, and that this can be one of the major factors of disease transmission.
Finally, we simulated and predicted a risk map of human CE in Western China after determining the geographical environment factors that affected disease transmission. As shown in the risk prediction map, the areas with a high prevalence were mainly concentrated in the southern part of Qinghai, the northwest of Sichuan, and most of the Tibet Autonomous Region. The high-risk areas were mainly located in the Qinghai-Tibet plateau region of China; this is an area associated with relatively low surface temperatures and is also the main region of the Tibetan population, with a large number of alpine grasslands [
12,
60]. Further research by Wang showed that the Qinghai-Tibet Plateau is the most endemic area in China [
44]; a subsequent study [
61] showed that the Eastern Tibetan Plateau was highly endemic for CE. In another study, Budke et al. [
52] noted that the Tibetan plateau of Western China showed a very high prevalence of human CE. Our new risk prediction map can reflect the distribution of human CE in Western China.
This study was limited by an inconsistent survey time of the prevalence of human CE across different regions. However, Human CE has a complex propagation path and an asymptomatic incubation period, which can be sustained for years until the parasite larvae evolve and trigger clinical signs. Thus, it is feasible to analyze the relationship between prevalence and environmental factors over several years. However, we also call for continuous systematic echinococcosis monitoring that will support future studies of the spatiotemporal distribution of echinococcosis and the factors that influence the prevalence of this disease.
5. Conclusions
This study investigated the prevalence and geographical environment factors associated with human CE in Western China where the prevention and control of this disease is a most urgent task. Our study provided an efficient approach with which to identify environmental determinants using remote sensing, GIS spatial analysis, and multiple regression analysis modeling at the county-level. Spatial analysis showed that the disease was widely distributed and prevalent in Western China. Our study indicates that GDP, grassland area ratio, Tibetan population ratio, and LST (Spring) were significant risk factors and can contribute to the spread of the disease. The predictive risk map shows the areas with high risk for human CE infection. Echinococcosis remains a serious public health problem, and the prevention and control of echinococcosis is a priority in Western China. Some of our suggestions are as follows. (1) Our findings can be submitted to the Ministry of Agriculture and Rural Affairs and the National Health Commission of the People’s Republic of China to help government agencies understand the current epidemic distribution of echinococcosis in Western China, and can also serve as a practical guide for health workers in local centers for disease control and prevention to implement enhanced surveillance in key endemic areas to reduce the number of future human infections. (2) We suggest that the government should actively carry out health education, popularize the knowledge of echinococcosis and make the Tibetan people form good health behaviors. The government is advised to control the number of infectious dogs, especially wild dogs. (3) The western region is mainly formed of agricultural and pastoral areas, with large numbers of cattle and sheep. The government should strengthen the management of animal slaughter, strictly implement the system of food hygiene inspection and animal quarantine, and guide people not to feed dogs with untreated diseased organs. (4) The government should speed up the development of the economy in the west, especially in remote rural areas and effectively improve people’s medical conditions. (5) It is recommended that the government strengthen drug repellent measures for dogs during the main infectious season of dogs, and that the government should guide people to develop a good habit of drinking clean water. Our findings and suggestions are of great significance to solving the national public health security, reducing economic losses for the country, and reducing the burden for many families in the future.
