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Socioeconomic and behavior risk factors of human alveolar echinococcosis in Tibetan communities in Sichuan, People's Republic of China

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  • Sichuan Center For Disease Control And Prevention

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Data from two cross-sectional investigations on 7,138 subjects were used to explore risk factors of human alveolar echinococcosis (AE) in Tibetan communities. The overall human AE prevalence was 3.1% (223 of 7,138), females had a higher prevalence (3.6%, 132 of 3,713) than males (2.7%, 91 of 3,425; P = 0.011), and herdsmen had a higher prevalence (5.2%, 154 of 2,955) than farmers (1.8%, 12 of 661; P < 0.001) and urban populations (2.1%, 49 of 2,360; P < 0.001). Age in all populations, number of dogs kept, fox skin ownership in farmers, not preventing flies from landing on food in herdsmen, using open streams as drinking water sources, and playing with dogs in urban populations were statistically significant risk factors. The results suggest that AE is highly endemic in the eastern Tibetan plateau, in Sichuan Province, the role of the dog is important for human infection, and other factors associated with environmental contamination may vary according to structure and practices of communities.
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... Some risk factors are similar in both regions, such as middleaged populations, low education level, and occupations as herdsman or farmers [14]. Within the Qinghai-Tibet Plateau some groups at risk of CE and AE are similar: middle-aged, low-educated women who spend most of their time at home [21]. They frequently feed dogs and livestock, collect cow dung for fuel, shear wool, and perform other household duties. ...
... They frequently feed dogs and livestock, collect cow dung for fuel, shear wool, and perform other household duties. Therefore, they are extremely susceptible to E. granulosus and E. multilocularis [21] infection. Age and low education level are risk factors for echinococcosis based on community studies conducted in Argentina [22]. ...
... People in this region are Buddhists and thus praise and highly respect all life forms. Lamas in temples will often take in or feed abandoned stray dogs, leading to a higher concentration of these dogs, which represent a major risk of infection near temples [20,21]. ...
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Background Echinococcosis is a parasitic zoonotic disease that threatens human health and economic development. In China, 370 counties are endemic for echinococcosis. Qinghai-Tibet Plateau has the most patients and people at risk. Therefore, analyzing the societal factors related to susceptibility to the disease is critical for efficient prevention and control of echinococcosis. Methods The demographic characteristics and lifestyle of echinococcosis cases were clustered using K-means cluster analysis to determine the main factors of risk of echinococcosis. Results Middle-aged and young people as well as those with a low education level and herdsmen are at risk of contracting echinococcosis. Nomadism, domestic and feral dogs in the surrounding environment, and drinking heavily polluted natural surface water are the main behavioral risk factors. The cystic echinococcosis (CE) and alveolar echinococcosis (AE) cluster analysis focused on female, middle-aged, and young people, winter settlement and summer nomadism, and domestic and feral dogs in the surrounding environment. There were significant differences in lifestyle between Qinghai-Tibet Plateau cases and non-Qinghai-Tibet-Plateau cases. Conclusion According to the distribution of cases and CE and AE, this study identified the factors of risk of echinococcosis in the Qinghai-Tibet Plateau and non-Qinghai-Tibet Plateau. Adapted control techniques appropriate for the various epidemic areas should be established to serve as a reference for echinococcosis prevention. Graphical Abstract
... middle-aged, low-educated women who spend most of their time at home [21]. They frequently feed dogs and livestock, collect cow dung for fuel, shear wool, and perform other household duties. ...
... They frequently feed dogs and livestock, collect cow dung for fuel, shear wool, and perform other household duties. Therefore, they are extremely susceptible to E. granulosus and E. multilocularis [21]. Age and low education level are risk factors for echinococcosis based on community studies conducted in Argentina [22]. ...
... People in this region are Buddhists and thus they praise and highly respect all life forms. Lamas in temples will often take in or feed abandoned stray dogs leading to a higher concentration of such dogs, who represent a major risk of infection near temples [20][21]. ...
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Background: Echinococcosis is a parasitic zoonotic disease that threatens human health and economic development. In China, 370 counties are endemic for echinococcosis. Qinghai-Tibet Plateau displays the highest number of patients and people at risk. Therefore, analyzing the societal factors of susceptibility to the disease is critical for efficient prevention and control of echinococcosis. Methods: The demographic characteristics and lifestyle of echinococcosis cases were clustered using K-means cluster analysis to determine the main factors of risk to echinococcosis. Results: Middle-aged and young people as well as those with a low education level and herdsmen are at risk of contracting echinococcosis. Nomadism, domestic and feral dogs in the surrounding environment, but also drinking heavily polluted natural surface water are the main behavioral risk factors. The cystic echinococcosis (CE) and alveolar echinococcosis (AE) cluster analysis focused on females, middle-aged and young people, winter settlement and summer nomadism, and domestic and feral dogs in the surrounding environment. There were significant differences in lifestyle between Qinghai-Tibet Plateau cases and non-Qinghai Tibet-Plateau cases. Conclusion: According to the distribution of cases and CE and AE, this study identified the factors of risk to echinococcosis in the Qinghai-Tibet Plateau and non-Qinghai-Tibet Plateau. Adapted control techniques appropriate for the various epidemic areas should be established to serve as a reference for echinococcosis prevention.
... AE has a relatively low incidence considered fatal (1,7). Risk factors associated with AE infections include dogs, fox-skin products or fox hunting, and sources of drinking water (8,9). The role of wild rodents and dogs in the transmission of E. multilocularis to humans appears to be significant (10). ...
... The higher AE prevalence in farmers may result from contact with dogs or with a dog's environment. Monks or Buddhist nuns (23.8%) in the present study were also at a high risk of infection, which may be due to monks' contact with stray dogs that feed around temples (8,9). Furthermore, we found that more than 95% of patients were illiterate, which implies that the prevalence of echinococcosis may have a relationship with the education level. ...
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Objectives: Intracranial alveolar echinococcosis (IAE), a zoonotic disease, is a critical health problem in the Tibetan region. We aimed to describe the clinical and radiological characteristics and outcomes among patients with IAE. Methods: We screened patients diagnosed with IAE between March 2015 and May 2019 at the Ganzi Tibetan Autonomous Prefecture People's Hospital. Detailed demographics, clinical characteristics, neuroimaging features, and outcomes were recorded. Results: A total of 21 patients with an average age of 44.1 ± 12.7 years were included. Thirteen (61.9%) patients were male. The most common chief neurological complaint was headache ( n = 17, 81.0%), followed by dizziness, seizure, visual disturbances, hemiparesis, disturbed consciousness, and dysphasia. All the patients had coexisting liver localizations. The typical neuroimaging features of IAE on cerebral magnetic resonance imaging scans showed obvious low-signal shadow with multiple small vesicles inside the lesions on T2-weighted images and FLAIR images. The pathological HE staining demonstrates vesicular lesions with several internal sacs. For hepatic alveolar echinococcosis (AE), the hepatic portal was invaded in six (28.6%) patients, and the portal vein ( n = 5, 23.8%) was the mostly commonly involved vessel. As for treatment, 11 patients (52.4%) had poor compliance with albendazole. The duration of patients taken albendazole ranged from 2 months to 3 years. Cerebral AE surgery was performed in 11 patients, five of them underwent partial resection of AE lesions, and six patients received total resection. One patient with primary IAE underwent radical surgery. Ten patients (47.6%) died during the follow-up for a mean of 21.7 ± 11.9 (3–46) months. In total, 28.9% of the patients died within 5 years, and 71.6% died within 10 years. The median interval between the date of diagnosis as AE and death was 84 (19–144) months. Conclusion: Despite substantial advances in diagnostic and therapeutic methods, the treatment of IAE remains difficult and results in unsatisfactory outcomes. The major critical issue is surgical treatment of IAE although the disease is disseminated. Besides, lifelong albendazole would be indicated, but most patients had poor medication compliance. It is important to educate patients about the necessity of medical treatment.
... Seven risk factors for AE were indicated among the studies, and a meta-analysis was executed on nine cross-sectional studies (11,28,33,37,38,(42)(43)(44)(45). The results of the meta-analysis and forest plots are summarized in Table 2, Figure 3. ...
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Background Echinococcosis is a severe zoonotic disease that imposes a substantial burden on human life. This meta-analysis aimed to summarize available data on the prevalence of human echinococcosis and identify the key risk factors for echinococcosis in the Chinese general population. Methods Relevant studies were comprehensively searched in the PubMed, EMBASE, Web of Science, Cochrane, Chinese National Knowledge Infrastructure (CNKI), Chongqing VIP Information (VIP), Wanfang and SinoMed databases until August 22, 2020. A random-effects model was used to estimate the pooled odds ratio (OR) and 95% confidence interval (95% CI). The I ² and Q statistics were calculated to evaluate the heterogeneity, and potential sources of heterogeneity were identified using sensitivity analysis and subgroup analysis. Publication bias was estimated by funnel plots and Egger's test. Results A total of 1026 studies were identified through the database search, of which 26 were eligible for this meta-analysis. The pooled prevalence of AE and CE were 2.88% and 5.66%, respectively. Ethnicity (OR = 2.93, 95% CI: 1.81–4.75; I ² = 0), herdsman occupation (OR = 2.66, 95% CI: 2.25–3.14; I ² = 8.0%), not washing hands before meals (OR = 2.40, 95% CI: 1.34–4.28; I ² = 82.8%) and being female (OR = 1.45, 95% CI: 1.26–1.66; I ² = 33.9%) were risk factors for AE. The top five risk factors for CE were ethnicity (OR = 3.18, 95% CI: 1.55–6.52; I ² = 79.2%), nomadism (OR = 2.71, 95% CI: 1.65–4.47; I ² = 55.8%), drinking nonboiled water (OR = 2.47, 95% CI: 1.36–4.47; I ² = 85.7), feeding viscera to dogs (OR = 2.35, 95% CI: 1.89–2.91; I ² = 21.5%), and herdsman occupation (OR = 2.19, 95% CI: 1.67–2.86; I ² = 85.1%). Conclusions This study generalized articles that have contributed to our current understanding of the epidemic of human echinococcosis (AE and CE) in China over the years. The results support that the ethnicity and dog-related factors are major risk factors for both CE and AE. The identification of echinococcosis risk factors may aid researchers and policymakers in improving surveillance and preventive measures aimed at reducing Echinococcus granulosus and Echinococcus multilocularis infection in humans.
... Human and animal CE cases are strictly associated with the presence of livestock farms [26]. In fact, previous studies [32,33] demonstrated infections depending on variables (i.e., personal hygiene, socio-economic contest) that facilitate close contact with E.g. eggs [34]. The farms recently provide leisure services based on outdoor activities increasingly complementing quality food production and some have developed teaching and learning activities for school children [35]. ...
Article
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Cystic Echinococcosis (CE) is a severe zoonosis caused by the larval stage of the tapeworm Echinococcus granulosus. These parasites are naturally transmitted between canid definitive hosts that harbour the adult stage in the intestine, and mainly ungulate intermediate hosts, with larval cysts developing in their internal organs. The close coexistence between dog and sheep with incorrect hygiene management are the most important factors for the persistence of this parasitic pathology. The Educational Farms (EF) are farms and agritourisms suitably equipped to carry out training activities for people interested in farm practices and agricultural processing, in particular student groups. Public attendance of farms represents a new potential risk factor for the zoonoses transmission. Consumption of contaminated food and water in combination with contact or playing with domestic dogs (Canis familiaris) are possible routes of zoonoses human infection. In fact, Echinococcus spp. eggs may persist in the environment up to several months at low temperatures and moist conditions, having the chance of contaminating different matrices and surfaces. The aim of this investigation was to study environmental contamination by parasitic elements as a risk for zoonoses, such as Echinococcus spp. A total of 116 samples (35 of water, 33 of soil, 23 of vegetables, 25 of dog faeces) were collected in 30 EF in Sardinia. Samples were subjected to biomolecular investigation for the research of specific gene sequences of Echinococcus granulosus, Echinococcus multilocularis and Taenia spp. The study allowed to identify eight positive EF due to the presence of Echinococcusgranulosus in eight dog faeces samples and one positive EF due to the presence of Taenia spp. in a water sample. The work has allowed to develop and harmonise the diagnostic methods and operating protocols essential for controlling the spread of the CE to create “One Health” intervention plans in high endemic areas through the implementation of SOP (standard operating procedures) for monitoring the pathology in animals, humans and environment.
... E. multilocularis is common on the Qinghai-Tibetan Plateau [7,8,40,41] and in Central Asia [20,42]. Geographically these two endemic areas are separated by the Kunlun and Tianshan Mountains and the Taklamakan Desert. ...
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Alveolar echinococcosis (AE) is a life-threatening disease in humans caused by the larval stage of Echinococcus multilocularis . The tapeworm is transmitted between small mammals and dogs/foxes in the Northern Hemisphere. In this study 286 AE cases were reported from eight counties and one city in Yili Prefecture, Xinjiang Autonomous Region, the People’s Republic of China from 1989 to 2015 with an annual incidence (AI) of 0.41/100,000. Among the patients, 73.08% were diagnosed in the last 11 years. Four counties in the high mountainous areas showed higher AI (0.51–1.22 cases//100,000 residents) than the four counties in low level areas (0.19–0.29/100,000 residents). The AI of AE in Mongolian (2.06/100,000 residents) and Kazak (0.93/100,000 residents) ethnic groups was higher than the incidence in other ethnic groups indicating sheep-farming is a risk for infection given this activity is mainly practiced by these two groups in the prefecture. A total of 1411 small mammals were captured with 9.14% infected with E . multilocularis metacestodes. Microtus obscurus was the dominant species in the mountain pasture areas with 15.01% of the voles infected, whereas Mus musculus and Apodemus sylvaticus were the dominant small mammals in the low altitude areas. Only 0.40% of A . sylvaticus were infected with E . multilocularis . PCR amplification and sequencing analysis of the mitochondrial cox1 gene showed that E . multilocularis DNA sequences from the small mammals were identical to isolates of local human AE cases. The overall results show that Yili Prefecture is a highly endemic area for AE and that the high-altitude pasture areas favorable for M . obscurus may play an important role in its transmission in this region.
... Women are also more involved in housework, such as collecting yak feces and sheep shearing. As a result, they are exposed to possible contaminants in dog feces and/or E. multilocularis eggs [33,62]. Thus, specific living habits are a likely cause for the increase in the potential HAE risk in women. ...
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Background: Human alveolar echinococcosis (HAE), caused by the larvae of Echinococcus multilocularis, is a severe parasitic disease that is a major public health concern. New HAE cases in China account for 91% of the global HAE burden every year. Although there are a few studies and systematic reviews (SRs) on the prevalence of HAE in China, trends in the prevalence have not been estimated. This study aims to describe the overall variation in the trend of HAE prevalence in China, and provide evidence for preventive measures in the future. Methods: Thirty-five eligible studies were retrieved from PubMed, Web of Science, EMBASE, CNKI, Wanfang Data, and VIP, and included in the SR and meta-analysis. An adjusted Agency for Healthcare Research and Quality checklist was used to evaluate study quality. The arcsine transformation was used to adjust the individual reported prevalence, and the pooled HAE prevalence was calculated. Heterogeneity was evaluated using the chi-square test and I2 statistic. Forest plots were generated for the meta-analysis, and publication bias of the studies was assessed using the Egger's test and funnel plots. We conducted subgroup analyses, sensitivity analyses, and meta-regression analyses to analyze the source of heterogeneity and factors potentially influencing the prevalence of HAE. Results: The meta-analysis indicated that the pooled HAE prevalence in China was 0.96% (95% CI: 0.71 to 1.25%). Factors potentially influencing HAE prevalence were female sex (OR = 1.60, 95% CI: 1.35 to 1.91, P<0.01), being ≥30 years old (OR = 4.72, 95% CI: 2.29 to 9.75, P<0.01), and being farmers and/or herdsmen (OR = 2.54, 95% CI: 1.60 to 4.02, P<0.01). The results of the meta-regression analysis (R2 = 38.11%, P < 0.01) indicated that HAE prevalence is on a downward trend. Conclusions: HAE prevalence has decreased over time and maintained low levels after 2005 in China. This decline was influenced by the utilization of One Health strategies as intervention measures. Therefore, these One Health strategies should be used as references to formulate future programs for HAE control. More high-quality epidemiological investigations and surveillance programs should be conducted in order to improve HAE control in the future.
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Background Echinococcosis is a severe zoonotic disease that imposes a substantial burden on human life. Numerous studies on echinococcosis have involved a variety of risk factors, and it is difficult to evaluate the key risk factors. The objectives of this meta-analysis are to summarize available data on the prevalence of human echinococcosis and identify the key risk factors for echinococcosis. Methods Relevant studies were comprehensively searched in the PubMed, EMBASE, Web of Science, Cochrane, Chinese National Knowledge Infrastructure (CNKI), Chongqing VIP Information (VIP), Wanfang and SinoMed databases from database inception until August 22, 2020. A random-effects model was used to estimate the pooled odds ratio (OR) and 95% confidence interval (CI) by integrating the OR values of each risk factor. The I² and Q statistics were calculated to evaluate the heterogeneity, and potential sources of heterogeneity were identified using sensitivity analysis and subgroup analysis. Publication bias was estimated by funnel plots and Egger’s test. Results A total of 1026 studies were identified through the database search, of which 26 were eligible for this meta-analysis. In total, 23 and 9 of the 26 studies were cystic echinococcosis (CE) and alveolar echinococcosis (AE) studies, respectively (6 papers included both AE and CE). The pooled prevalence of echinococcosis was 5.52% (95% CI: 5.47%-5.58%). Ethnicity (OR = 2.93, 95% CI: 1.81–4.75; I² = 0), being a herder (OR = 2.66, 95%CI95% CI: 2.25–3.14; I² = 8%), not washing hands before meals (OR = 2.40, 95% CI: 1.34–4.28; I² = 82.8%) and being female (OR = 1.45, 95% CI: 1.26–1.66; I² = 33.9%) were risk factors for AE. The top five risk factors for CE were ethnicity (OR = 3.18, 95% CI: 1.55–6.52; I² = 79.2%), nomadism (OR = 2.71, 95% CI: 1.65–4.47; I² = 55.8%), drinking nonboiled water (OR = 2.47, 95% CI: 1.36–4.47; I² = 85.7), feeding viscera to dogs (OR = 2.35, 95% CI: 1.89–2.91; I² = 21.5%), and being a herder (OR = 2.19, 95% CI: 1.67–2.86; I² = 85.1%). The study design-specific subgroup analysis showed that the heterogeneity of CE risk factors decreased to varying degrees. Conclusions Specific characteristics (i.e., ethnicity and herder status) and behaviors (i.e., not washing hands before meals and feeding viscera to dogs ) are possible risk factors for echinococcosis. This study provided remarkable insight for future prevention and control of echinococcosis.
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Echinococcosis is one of the 17 neglected tropical diseases recognized by the World Health Organization and causes a huge global disease burden. The Tibet Autonomous Region (Tibet) of China is the most epidemic area of echinococcosis worldwide. Echinococcosis poses an enormous threat to local public health and economic development. Identifying vulnerable populations and analyzing people’s knowledge, attitudes, and practices (KAP) with respect to echinococcosis is necessary to prevent and control echinococcosis. Based on reported cases and questionnaire responses, we first used a k-prototypes clustering algorithm to identify vulnerable populations according to human demographics (including gender, age, education level, and occupation). We then used a KAP analysis to evaluate the Tibetan people’s understanding of echinococcosis. The results identified three types of vulnerable population. Vulnerable population I comprised illiterate middle-aged and older women engaged in agriculture and animal husbandry. Vulnerable population II comprised illiterate middle-aged male herdsmen. Vulnerable population III comprised young male farmers with a low education level. The KAP analysis indicated that the pass rate for all participants was 72.6%, 6.4%, 95.0%, and 75.8% for KAP, K, A, and P, respectively. The pass rates were significantly different among different age and gender groups. Based on these results, it is necessary to improve public health education and professional training, and to implement effective control and management measures targeting typical hosts of echinococcosis. This study provides a direct reference for the prevention and control of echinococcosis in Tibet.
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A nationwide (Taiwan Province not included) survey of the distribution of human parasites in China during 1988-1992 was conducted under the auspices of the Ministry of Public Health, with stratified masses randomly sampling. A total of 2,848 pilot sites in 726 counties with a population of 1,477,742 were surveyed, according to unified standard, unified diagnostic method and control quality. The overall infection rate of parasites was 62. 632%. Among them, the infection rate was over 50% in 17 provinces/autonomous regions/municipalities (P/A/M), over 80% in Hainan, Guangxi, Sichuan, Fujian, Zhejiang and Guizhou, being highest in Hainan (94. 735%). Altogether 56 species were detected. Centrocestus formosanus is reported for the first time at home, Echinochasmus liliputanus and Echinostoma angustitestis are reported for the first time at home and abroad. Echinochasmus fujianensis is a new species. E. histolytica, G. lamblia, A. lumbricoides, whipworm and pinworm were distributed nationwide, while Cysticercus (27 P/A/M), Taenia (27), hookworm (26), Balantidium coli (22), Clonorchis sinensis (22), Paragonimus westermani (21), H. diminuta (21), Echinococcus (18), H. nana (17), Fasciolopsis buski (16), T. spiralis (12) were distributed non-nationwide. A preliminary suggestion on intervention of the common and/or most detrimental parasitic diseases was submitted, including hydatidosis, taeniasis, cysticercosis, clonorchiasis, paragonimiasis, trichinellosis, hookworm disease, ascariasis, trichuriasis and enterobiasis.
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The purpose of this study was to identify species-specific protein components of Echinococcus multilocularis by Western blotting and establish a simple and highly sensitive method for differential serodiagnosis of alveolar hydatid disease (AHD) from cystic hydatid disease. Using Western blotting analyses we demonstrated 2 previously undescribed, species-specific, antigenic components of protoscoleces of E. multilocularis easily detectable with sera from active AHD patients exclusively. The 18 kDa component was recognized by sera from all active AHD patients, whereas the 16 kDa antigen was characteristically detected by patients with advanced lesions. The potential utility of these components for differential serodiagnosis of AHD is discussed.