Assessment of a 10-year dog deworming programme on the transmission of Echinococcus multilocularis in Tibetan communities in Sichuan Province, China.

Human alveolar echinococcosis (AE) is considered a neglected zoonotic disease by the World Health Organization (WHO). The causative pathogen, Echinococcus multilocularis, lives as an adult tapeworm in the intestinal tract of canines. AE was identified as an emerging public health issue in Tibetan communities of Shiqu County 20 years ago. On St. Lawrence Island, Alaska (USA), in the 1980s peri-domestic transmission of E. multilocularis was controlled by regular deworming of owned dogs over a 10-year period. In Tibetan communities, on the Tibetan Plateau, control of E. multilocularis transmission is challenging due to the continental setting, complex epidemiology, disease ecology, geography, and socio-cultural factors. However, a control programme based on deworming owned dogs using praziquental (PZQ) has been carried out since 2006. Assessment was conducted in townships where baseline data were available 10 years prior. Purging of dogs by oral administration of arecoline was used to measure E. multilocularis prevalence, trapping small mammals around communities was employed to assess the change in infection of pikas and voles, and analysis of human AE abdominal ultrasound-based data was used to understand the change in prevalence in the past decade. In all three evaluated townships, the E. multilocularis prevalence in owned dogs was significantly (P < 0.01) reduced from 7.23% (25/346) during 2000-2003 to 0.55% (1/181) in 2016. Human AE ultrasound-based prevalence (adjusted for age and sex) in five evaluated townships decreased significantly (P < 0.01) from 6.25% (200/3,198) during 2000-2002 to 3.67% (706/19,247) during 2015-2017. The 2016 prevalence of E. multilocularis metacestodes in small mammal intermediate hosts was not significantly different from the prevalence in 2008. The control programme was effective in reducing E. multilocularis infection in owned dogs and human AE prevalence, but did not significantly impact infection in wildlife intermediate hosts.

The effects of dog management on Echinococcus spp. prevalence in villages on the eastern Tibetan Plateau, China.

BACKGROUND: The pastoral area of the eastern Tibetan Plateau is highly endemic for human echinococcosis. Domestic dogs are the main definitive host for the transmission of both Echinococcus granulosus (sensu lato) and E. multilocularis to humans. To control the infection risks, a national-level canine echinococcosis prevention and control programme has been implemented since 2015 in Shiqu County, Ganze Tibetan Autonomous Prefecture, Sichuan, China. The objective of this study was to evaluate its effect on Echinococcus spp. prevalence in dogs. METHODS: We surveyed 69 households with 84 owned dogs, for dog fecal samples and dog keeping information in the villages of Rizha and Eduoma. A total of 105 dog fecal samples (75 from owned dogs and 30 unknown dog fecal samples) were collected between 2015-2017 to determine Echinococcus spp. prevalence using copro-PCR. Eight variables based on household surveys were included into a logistic regression model for significant risk factors to canine echinococcosis prevalence in dogs. RESULTS: Between 2015-2017, the overall Echinococcus spp. copro-DNA prevalence decreased significantly in dogs from 51.2% (2015) to 20.0% (2017) in Rizha, and insignificantly from 11.5% (2016) to 4.3% (2017) in Eduoma. Echinococcus multilocularis was the most prevalent species continually copro-DNA detected during the entire study period, while E. granulosus was rare and not detected in 2017. Echinococcus shiquicus copro-DNA prevalence (a probable non-zoonotic wildlife species) was as high in dogs as that of E. multilocularis, although only detected in 2015 in Rizha. Unleashed dog feces were mainly collected in Rizha in 2015. Although 93.2% of owned dogs were leashed, and the monthly praziquantel dosing rate reached 97%, E. multilocularis infection could still be detected in 11.1% of owned dogs in 2017. Monthly deworming, leashing dogs 24 h per day, and the avoidance of dogs feeding on livestock viscera were significant measures to prevent canine echinococcosis infection in owned dogs. CONCLUSIONS: Carrying out a canine echinococcosis prevention and control programme can significantly decrease Echinococcus spp. prevalence. The potential contact between leashed dogs and wild small mammals is still a risk for re-infection of owned dogs with E. multilocularis. This study shows that the long-term application of regular dog treatment with praziquantel in the vast and remote echinococcosis endemic areas of the eastern Tibetan Plateau can reduce transmission in dogs but remains a challenging intervention.

Long-term retrospective assessment of a transmission hotspot for human alveolar echinococcosis in mid-west China.

BACKGROUND: Human alveolar echinococcosis caused by infection with Echinococcus multilocularis is one of the most potentially pathogenic helminthic zoonoses. Transmission occurs involving wildlife cycles typically between fox and small mammal intermediate hosts. In the late 1980s/early 1990s a large focus of human AE was identified in poor upland agricultural communities in south Gansu Province, China. More detailed investigations in 1994-97 expanded community screening and identified key risk factors of dog ownership and landscape type around villages that could support susceptible rodent populations. A crash of the dog population (susceptible domestic definitive host) in the early 1990s appeared to stop transmission. METHODOLOGY/FINDINGS: We subsequently undertook follow-up eco-epidemiological studies based on human population screening and dog survey, in 2005/6 and in 2014/15. Our observations show a decrease in human AE prevalence, especially marked in the 11-30 year old age category. In 2015, although the dog population had recovered and in addition, forest protection and the reforestation of some areas may have favoured red fox (wild definitive host) population growth, there was no evidence of infection in owned dogs. CONCLUSIONS/SIGNIFICANCE: Those observations suggest that over decades socio-ecological changes resulted in a cascade of factors that exacerbated and then interrupted parasite emergence, with probable elimination of peri-domestic transmission of E. multilocularis in this area, despite the relative proximity of large active transmission foci on the eastern Tibetan Plateau. This study case exemplifies how anthropogenic land use and behavioural changes can modify emergence events and the transmission of endemic zoonotic parasite infections, and subsequently the importance of considering processes over the long-term in a systems approach in order to understand pathogen and disease distribution.

Impact of increased economic burden due to human echinococcosis in an underdeveloped rural community of the People's Republic of China.

BACKGROUND: Ningxia is located in western People's Republic of China, which is hyperendemic for human cystic echinococcosis (CE) throughout the entire area with alveolar echinococcosis (AE) hyperendemic in the south. This is in part due to its underdeveloped economy. Despite the recent rapid growth in P.R. China's economy, medical expenditure for hospitalization of echinococcosis cases has become one of the major poverty generators in rural Ningxia, resulting in a significant social problem. METHODOLOGY/PRINCIPAL FINDINGS: We reviewed the 2000 inpatient records with liver CE in surgical departments of hospitals from north, central and south Ningxia for the period 1996-2002. We carried out an analysis of health care expenditure of inpatient treatment in public hospitals, and examined the financial inequalities relating to human echinococcosis and the variation in per capita income between various socioeconomic groups with different levels of gross domestic product for different years. Hospital charges for Yinchuan, NHAR's capital city in the north, increased approximately 35-fold more than the annual income of rural farmers with the result that they preferred to seek health care in local county hospitals, despite higher quality and more efficient treatment and diagnosis available in the city. Household income levels thus strongly influenced the choice of health care provider and the additional expense impeded access of poor people to better quality treatment. CONCLUSIONS/SIGNIFICANCE: Information on socioeconomic problems arising from echinococcosis, which adds considerably to the burden on patient families and communities, needs to be collected as a prerequisite for developing policies to tackle the disease in rural Ningxia.

Landscape composition and spatial prediction of alveolar echinococcosis in southern Ningxia, China.

BACKGROUND: Alveolar echinococcosis (AE) presents a serious public health challenge within China. Mass screening ultrasound surveys can detect pre-symptomatic AE, but targeting areas identified from hospital records is inefficient regarding AE. Prediction of undetected or emerging hotspots would increase detection rates. Voles and lemmings of the subfamily Arvicolinae are important intermediate hosts in sylvatic transmission systems. Their populations reach high densities in productive grasslands where food and cover are abundant. Habitat availability is thought to affect arvicoline population dynamic patterns and definitive host-intermediate host interactions. Arvicoline habitat correlates with AE prevalence in Western Europe and southern Gansu Province, China. METHODS AND FINDINGS: Xiji County, Ningxia Hui Autonomous Region, borders southern Gansu. The aims of this study were to map AE prevalence across Xiji and test arvicoline habitat as a predictor. Land cover was mapped using remotely sensed (Landsat) imagery. Infection status of 3,205 individuals screened in 2002-2003 was related, using generalised additive mixed models, to covariates: gender; farming; ethnicity; dog ownership; water source; and areal cover of mountain pasture and lowland pasture. A Markov random field modelled additional spatial variation and uncertainty. Mountain pasture and lowland pasture were associated with below and above average AE prevalence, respectively. CONCLUSIONS: Low values of the normalised difference vegetation index indicated sub-optimality of lowland pasture for grassland arvicolines. Unlike other known endemic areas, grassland arvicolines probably did not provide the principal reservoir for Echinococcus multilocularis in Xiji. This result is consistent with recent small mammal surveys reporting low arvicoline densities and high densities of hamsters, pikas and jerboas, all suitable intermediate hosts for E. multilocularis, in reforested lowland pasture. The risk of re-emergence is discussed. We recommend extending monitoring to: southern Haiyuan County, where predicted prevalence was high; southern Xiji County, where prediction uncertainty was high; and monitoring small mammal community dynamics and the infection status of dogs.

Canine echinococcosis in northwest Libya: assessment of coproantigen ELISA, and a survey of infection with analysis of risk-factors.

In order to determine the prevalence and risk factors for canine echinococcosis in different endemic localities in the Tripoli area of northwest Libya, stray dogs were examined post-mortem, and owned dogs screened for Echinococcus granulosus infection using a standardised genus specific coproantigen ELISA. The prevalence of E. granulosus infection at necropsy in stray-dogs was 25.8% (15/58, 95% CI 15.3-39.0%), and 21.6% (72/334, 95% CI 17.3-26.4%) of owned dogs tested were positive by coproantigen ELISA. Sheepdogs appeared to have a significantly higher copro-positive prevalence (19/19 positive, p=0.003), compared to 23.6% of other dog classes (e.g. 52/220 guard dogs and household pets). Worm burdens in necropsied dogs ranged from 29 to 2900 (mean 1064) and were positively correlated to coproantigen ELISA OD values (r(s)=0.87, p<0.001), but negatively correlated with dog age (r(s)=-0.69, p=0.001). Dog age was a significant factor in copro-prevalence as there was an increasing coproantigen-positive tendency in younger dogs (< or =5 years, p=0.04). A total of 45/132 (34%, 95% CI 25.9-42.1%) of farms/homestead had at least one dog that was coproantigen positive. Overall copro-prevalence in dogs by locality varied, with Alkhums (Leptis-Magna) district having the highest copro-prevalence at 38.7% (24/62, 95% CI 26.6-50.8%) (p=0.001). Coproantigen testing of a cohort of owned dogs before and approximately 15 months after praziquantel treatment showed a significant decrease in the coproantigen positive rate from 21.6% (72/334) to 9% (21/233) post-treatment. The overall E. granulosus coproantigen positive rate ('re-infection rate') within the same cohort of dogs was 22 % (10/45) by 15 months post-treatment. Significant risk factors for a copro-positive owned dog were associated with non-restraint of dogs, and owners that did not de-worm their dogs. Home slaughtering of livestock and lack of knowledge about E. granulosus transmission were also significant risk factors for a canine coproantigen positive result.

Modeling the transmission of Echinococcus granulosus and Echinococcus multilocularis in dogs for a high endemic region of the Tibetan plateau.

Echinococcus granulosus and Echinococcus multilocularis abundance and prevalence data, for domestic dogs of Shiqu County, Sichuan Province, People's Republic of China, were fitted to mathematical models to evaluate transmission parameters. Abundance models, assuming the presence and absence of immunity, were fit for both E. granulosus and E. multilocularis using Bayesian priors, maximum likelihood, and Monte Carlo sampling techniques. When the models were compared, using the likelihood ratio test for nested models, the model assuming the presence of immunity was the best fit for E. granulosus infection, with a purgation based prevalence of 8% (true prevalence interval of 8-19% based on the sensitivity of purgation) and a mean abundance of 80 parasites per dog, with an average infection pressure of 560 parasites per year. In contrast, the model assuming the absence of immunity was the best fit for E. multilocularis infection, with a purgation based prevalence of 12% (true prevalence interval of 13-33% based on the sensitivity of purgation) and a mean abundance of 131 parasites per dog, with an average infection pressure of 334 or 533 parasites per year assuming a 5 or 3 month parasite life expectancy, respectively. The prevalence data for both parasites was then fit to a set of differential equations modeling the transition between infection states in order to determine number of infectious insults per year. Infection pressure was 0.21, with a 95% credibility interval of 0.12 to 0.41, infections per year for E. granulosus and 0.52, with a 95% credibility interval of 0.29-0.77, infections per year for E. multilocularis assuming a 5 month parasite lifespan or 0.85, with a 95% credibility interval of 0.47-1.25 infections per year, assuming a 3 month E. multilocularis lifespan in dogs.