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1.  Dynamics of the Force of Infection: Insights from Echinococcus multilocularis Infection in Foxes 
Characterizing the force of infection (FOI) is an essential part of planning cost effective control strategies for zoonotic diseases. Echinococcus multilocularis is the causative agent of alveolar echinococcosis in humans, a serious disease with a high fatality rate and an increasing global spread. Red foxes are high prevalence hosts of E. multilocularis. Through a mathematical modelling approach, using field data collected from in and around the city of Zurich, Switzerland, we find compelling evidence that the FOI is periodic with highly variable amplitude, and, while this amplitude is similar across habitat types, the mean FOI differs markedly between urban and periurban habitats suggesting a considerable risk differential. The FOI, during an annual cycle, ranges from (0.1,0.8) insults (95% CI) in urban habitat in the summer to (9.4, 9.7) (95% CI) in periurban (rural) habitat in winter. Such large temporal and spatial variations in FOI suggest that control strategies are optimal when tailored to local FOI dynamics.
Author Summary
Human alveolar echinococcosis (AE) is caused by the fox tapeworm E. multilocularis and has a high fatality rate if untreated. The frequency of the tapeworm in foxes can be reduced through the regular distribution of anthelmintic baits and thus decrease the risk of zoonotic transmission. Here, we estimate the force of infection to foxes using a mathematical model and data from necropsied foxes. The results suggest that the frequency of anthelmintic baiting of foxes can be optimised to local variations in transmission that depend upon season and type of fox habitat.
PMCID: PMC3961194  PMID: 24651596
2.  Human Alveolar Echinococcosis in Kyrgyzstan 
Emerging Infectious Diseases  2013;19(7):1095-1097.
Human echinococcosis is a reportable disease in Kyrgyzstan. Between 1995 and 2011, human alveolar echinococcosis increased from <3 cases per year to >60 cases per year. The origins of this epidemic, which started in 2004, may be linked to the socioeconomic changes that followed the dissolution of the former Soviet Union.
PMCID: PMC3713972  PMID: 23763935
Echinococcus multilocularis; emergence; Alveolar echinococcosis; Kyrgyzstan; Central Asia; tapeworms; parasites; zoonoses
3.  A Systematic Review of the Epidemiology of Echinococcosis in Domestic and Wild Animals 
Human echinococcosis is a neglected zoonosis caused by parasites of the genus Echinococcus. The most frequent clinical forms of echinococcosis, cystic echinococcosis (CE) and alveolar echinococcosis (AE), are responsible for a substantial health and economic burden, particularly to low-income societies. Quantitative epidemiology can provide important information to improve the understanding of parasite transmission and hence is an important part of efforts to control this disease. The purpose of this review is to give an insight on factors associated with echinococcosis in animal hosts by summarising significant results reported from epidemiological studies identified through a systematic search.
Methodology and Principal Findings
The systematic search was conducted mainly in electronic databases but a few additional records were obtained from other sources. Retrieved entries were examined in order to identify available peer-reviewed epidemiological studies that found significant risk factors for infection using associative statistical methods. One hundred studies met the eligibility criteria and were suitable for data extraction. Epidemiological factors associated with increased risk of E. granulosus infection in dogs included feeding with raw viscera, possibility of scavenging dead animals, lack of anthelmintic treatment and owners' poor health education and indicators of poverty. Key factors associated with E. granulosus infection in intermediate hosts were related to the hosts' age and the intensity of environmental contamination with parasite eggs. E. multilocularis transmission dynamics in animal hosts depended on the interaction of several ecological factors, such as hosts' population densities, host-prey interactions, landscape characteristics, climate conditions and human-related activities.
Results derived from epidemiological studies provide a better understanding of the behavioural, biological and ecological factors involved in the transmission of this parasite and hence can aid in the design of more effective control strategies.
Author Summary
Echinococcosis is considered a neglected zoonotic disease caused by the larval form of Echinococcus spp. tapeworms. Humans become infected through the accidental intake of parasitic eggs excreted by the faeces of definitive hosts (dogs, foxes and other canids). Infection involves the development of cysts, primarily in the lungs and liver, causing damage as they enlarge like a slowly growing tumor. Transmission is facilitated by the general lack of awareness of infection factors and epidemiological models can identify them. Nevertheless, there has never been a systematic review summarizing the significant determinants for echinococcosis in animals. One hundred publications were included in the results after evaluating 1,935 entries and screening the references lists of the eligible papers. Principal factors associated with canine infection included the access of dogs to infected offal, allowing dogs to roam free, being a young and/or male dog and social behaviours linked with poor health conditions and poor living environments of dog owners. Ecological factors influencing E. multilocularis transmission encompassed population densities of foxes and rodents, predator-prey relationships, geographical characteristics, climate conditions and the movement of foxes towards urban areas. These findings are important, as intervention to control echinococcosis requires intervention in animal populations.
PMCID: PMC3674998  PMID: 23755310
4.  Latent-Class Methods to Evaluate Diagnostics Tests for Echinococcus Infections in Dogs 
The diagnosis of canine echinococcosis can be a challenge in surveillance studies because there is no perfect gold standard that can be used routinely. However, unknown test specificities and sensitivities can be overcome using latent-class analysis with appropriate data.
We utilised a set of faecal and purge samples used previously to explore the epidemiology of canine echinococcosis on the Tibetan plateau. Previously only the purge results were reported and analysed in a largely deterministic way. In the present study, additional diagnostic tests of copro-PCR and copro-antigen ELISA were undertaken on the faecal samples. This enabled a Bayesian analysis in a latent-class model to examine the diagnostic performance of a genus specific copro-antigen ELISA, species-specific copro-PCR and arecoline purgation. Potential covariates including co-infection with Taenia, age and sex of the dog were also explored. The dependence structure of these diagnostic tests could also be analysed.
Principle findings
The most parsimonious result, indicated by deviance-information criteria, suggested that co-infection with Taenia spp. was a significant covariate with the Echinococcus infection. The copro-PCRs had estimated sensitivities of 89% and 84% respectively for the diagnoses of Echinococcus multilocularis and E. granulosus. The specificities for the copro-PCR were estimated at 93 and 83% respectively. Copro-antigen ELISA had sensitivities of 55 and 57% for the diagnosis of E. multilocularis and E. granulosus and specificities of 71 and 69% respectively. Arecoline purgation with an assumed specificity of 100% had estimated sensitivities of 76% and 85% respectively.
This study also shows that incorporating diagnostic uncertainty, in other words assuming no perfect gold standard, and including potential covariates like sex or Taenia co-infection into the epidemiological analysis may give different results than if the diagnosis of infection status is assumed to be deterministic and this approach should therefore be used whenever possible.
Author Summary
Dogs are a key definitive host of Echinococcus spp; hence, accurate diagnosis in dogs is important for the surveillance and control of echinococcosis. A perfect diagnostic test would detect every infected dog (100% sensitivity) whilst never giving a false positive reaction in non-infected dogs (100% specificity). Since no such test exists, it is important to understand the performance of available diagnostic techniques. We used the results of a study that used three diagnostic tests on dogs from the Tibetan plateau, where there is co-endemicity of E. granulosus and E. multilocularis. In this study opro-antigen ELISA and copro-PCR diagnostic tests were undertaken on faecal samples from all animals. The dogs were also purged with arecoline hydrobromide to recover adult parasites as a highly specific but relatively insensitive third diagnostic test. We used a statistical approach (Bayesian latent-class models) to estimate simultaneously the sensitivities of all three tests and the specificities of the copro-antigen and copro-PCR tests. We also analysed how some determinants of infection can affect parasite prevalence. This approach provides a robust framework to increase the accuracy of surveillance and epidemiological studies of echinococcosis by overcoming the problems of poor diagnostic test performance.
PMCID: PMC3573084  PMID: 23459420
5.  Toxoplasma gondii Infection in Kyrgyzstan: Seroprevalence, Risk Factor Analysis, and Estimate of Congenital and AIDS-Related Toxoplasmosis 
HIV-prevalence, as well as incidence of zoonotic parasitic diseases like cystic echinococcosis, has increased in the Kyrgyz Republic due to fundamental socio-economic changes after the breakdown of the Soviet Union. The possible impact on morbidity and mortality caused by Toxoplasma gondii infection in congenital toxoplasmosis or as an opportunistic infection in the emerging AIDS pandemic has not been reported from Kyrgyzstan.
Methodology/Principal Findings
We screened 1,061 rural and 899 urban people to determine the seroprevalence of T. gondii infection in 2 representative but epidemiologically distinct populations in Kyrgyzstan. The rural population was from a typical agricultural district where sheep husbandry is a major occupation. The urban population was selected in collaboration with several diagnostic laboratories in Bishkek, the largest city in Kyrgyzstan. We designed a questionnaire that was used on all rural subjects so a risk-factor analysis could be undertaken. The samples from the urban population were anonymous and only data with regard to age and gender was available. Estimates of putative cases of congenital and AIDS-related toxoplasmosis in the whole country were made from the results of the serology. Specific antibodies (IgG) against Triton X-100 extracted antigens of T. gondii tachyzoites from in vitro cultures were determined by ELISA. Overall seroprevalence of infection with T. gondii in people living in rural vs. urban areas was 6.2% (95%CI: 4.8–7.8) (adjusted seroprevalence based on census figures 5.1%, 95% CI 3.9–6.5), and 19.0% (95%CI: 16.5–21.7) (adjusted 16.4%, 95% CI 14.1–19.3), respectively, without significant gender-specific differences. The seroprevalence increased with age. Independently low social status increased the risk of Toxoplasma seropositivity while increasing numbers of sheep owned decreased the risk of seropositivity. Water supply, consumption of unpasteurized milk products or undercooked meat, as well as cat ownership, had no significant influence on the risk for seropositivity.
We present a first seroprevalence analysis for human T. gondii infection in the Kyrgyz Republic. Based on these data we estimate that 173 (95% CI 136–216) Kyrgyz children will be born annually to mothers who seroconverted to toxoplasmosis during pregnancy. In addition, between 350 and 1,000 HIV-infected persons are currently estimated to be seropositive for toxoplasmosis. Taken together, this suggests a substantial impact of congenital and AIDS-related symptomatic toxoplasmosis on morbidity and mortality in Kyrgyzstan.
Author Summary
A serological study on toxoplasmosis was undertaken in a rural and urban population in Kyrgyzstan. The observed seroprevalence was adjusted because of differences between age and gender stratifications in the study group compared to population census figures. This gave an estimated seroprevalence in rural and urban populations of 5.1% and 16.4% respectively. In our analysis we determined the risk-factors for infection in the rural population to be age, low social-status and low number of sheep owned. While the seroprevalence in this rural population was relatively low, the seroprevalence found in the urban population of Bishkek correlated better with international data. Extrapolating from our data, about 173 seroconversions during pregnancy may be expected annually in Kyrgyzstan. In addition, considering a prevalence of HIV-Toxoplasma-co-infection between 7/100,000 (official HIV-prevalence data) and 19.4/100,000 (UNAIDS-estimates), 350–1,000 people are at risk for AIDS-related toxoplasmosis. Therefore, in the face of the rising prevalence of HIV infection education of medical personnel on treatment and prevention of toxoplasmosis is recommended.
PMCID: PMC3566989  PMID: 23409201
6.  The Global Burden of Alveolar Echinococcosis 
Human alveolar echinococcosis (AE) is known to be common in certain rural communities in China whilst it is generally rare and sporadic elsewhere. The objective of this study was to provide a first estimate of the global incidence of this disease by country. The second objective was to estimate the global disease burden using age and gender stratified incidences and estimated life expectancy with the disease from previous results of survival analysis. Disability weights were suggested from previous burden studies on echinococcosis.
Methodology/Principal Findings
We undertook a detailed review of published literature and data from other sources. We were unable to make a standardised systematic review as the quality of the data was highly variable from different countries and hence if we had used uniform inclusion criteria many endemic areas lacking data would not have been included. Therefore we used evidence based stochastic techniques to model uncertainty and other modelling and estimating techniques, particularly in regions where data quality was poor. We were able to make an estimate of the annual global incidence of disease and annual disease burden using standard techniques for calculation of DALYs. Our studies suggest that there are approximately 18,235 (CIs 11,900–28,200) new cases of AE per annum globally with 16,629 (91%) occurring in China and 1,606 outside China. Most of these cases are in regions where there is little treatment available and therefore will be fatal cases. Based on using disability weights for hepatic carcinoma and estimated age and gender specific incidence we were able to calculate that AE results in a median of 666,434 DALYs per annum (CIs 331,000-1.3 million).
The global burden of AE is comparable to several diseases in the neglected tropical disease cluster and is likely to be one of the most important diseases in certain communities in rural China on the Tibetan plateau.
Author Summary
Human alveolar echinococcosis (AE), caused by the larval stage of the fox tapeworm Echinococcus multilocularis, is amongst the world's most dangerous zoonoses. Transmission to humans is by consumption of parasite eggs which are excreted in the faeces of the definitive hosts: foxes and, increasingly, dogs. Transmission can be through contact with the definitive host or indirectly through contamination of food or possibly water with parasite eggs. We made an intensive search of English, Russian, Chinese and other language databases. We targeted data which could give country specific incidence or prevalence of disease and searched for data from every country we believed to be endemic for AE. We also used data from other sources (often unpublished). From this information we were able to make an estimate of the annual global incidence of disease and disease burden using standard techniques for calculation of DALYs. Our studies suggest that AE results in a median of 18,235 cases globally with a burden of 666,433 DALYs per annum. This is the first estimate of the global burden of AE both in terms of global incidence and DALYs and demonstrates the burden of AE is comparable to several diseases in the neglected tropical disease cluster.
PMCID: PMC2889826  PMID: 20582310
7.  Human Alveolar Echinococcosis after Fox Population Increase, Switzerland 
Emerging Infectious Diseases  2007;13(6):878-882.
An increase in fox population has led to an increase in incidence of human alveolar echinococcosis.
We analyzed databases spanning 50 years, which included retrospective alveolar echinococcosis (AE) case-finding studies and databases of the 3 major centers for treatment of AE in Switzerland. A total of 494 cases were recorded. Annual incidence of AE per 100,000 population increased from 0.12– 0.15 during 1956–1992 and a mean of 0.10 during 1993–2000 to a mean of 0.26 during 2001–2005. Because the clinical stage of the disease did not change between observation periods, this increase cannot be explained by improved diagnosis. Swiss hunting statistics suggested that the fox population increased 4-fold from 1980 through 1995 and has persisted at these higher levels. Because the period between infection and development of clinical disease is long, the increase in the fox population and high Echinococcus multilocularis prevalence rates in foxes in rural and urban areas may have resulted in an emerging epidemic of AE 10–15 years later.
PMCID: PMC2792858  PMID: 17553227
Alveolar echinococcosis; Echinococcus multilocularis; epidemiology; fox (Vulpes vulpes); zoonosis; incidence; Switzerland; research
8.  Global Socioeconomic Impact of Cystic Echinococcosis 
Emerging Infectious Diseases  2006;12(2):296-303.
Because the human and economic losses of cystic echinococcosis are substantial, global prevention and control measures should be increased.
Cystic echinococcosis (CE) is an emerging zoonotic parasitic disease throughout the world. Human incidence and livestock prevalence data of CE were gathered from published literature and the Office International des Epizooties databases. Disability-adjusted life years (DALYs) and monetary losses, resulting from human and livestock CE, were calculated from recorded human and livestock cases. Alternative values, assuming substantial underreporting, are also reported. When no underreporting is assumed, the estimated human burden of disease is 285,407 (95% confidence interval [CI], 218,515–366,133) DALYs or an annual loss of US $193,529,740 (95% CI, $171,567,331–$217,773,513). When underreporting is accounted for, this amount rises to 1,009,662 (95% CI, 862,119–1,175,654) DALYs or US $763,980,979 (95% CI, $676,048,731–$857,982,275). An annual livestock production loss of at least US $141,605,195 (95% CI, $101,011,553–$183,422,465) and possibly up to US $2,190,132,464 (95% CI, $1,572,373,055–$2,951,409,989) is also estimated. This initial valuation demonstrates the necessity for increased monitoring and global control of CE.
PMCID: PMC3373106  PMID: 16494758
echinococcosis; cestodes; cost of illness; burden of illness; economics; zoonoses

Results 1-8 (8)