Burden, cost of disease and optimization of clinical practice of human cystic echinococcosis in Mongolia

Our goal was to facilitate prevention and control of cystic echinococcosis (CE) in Mongolia by measuring the disease burden and societal cost, investigating the zoonotic linkages, and identifying the key challenges in clinical management of CE with proposed improvement. The disease is caused by the larval stage of Echinococcus granulosus sensu lato, and transmitted between dogs and various species of ungulates and also transmitted to humans. In humans, large cystic lesions can occur, mainly in the liver and lungs. Mongolia is one of the areas most affected by CE. The numbers of dogs and livestock are high, and a nomadic herding lifestyle is commonly practiced in most parts of the country. However, existing health services in Mongolia for CE barely reach the targeted populations, and CE cases are only detected at a late stage. For adequate diagnosis and treatment, herders must often travel hundreds of kilometers. Surgical procedures and hospitalization, travel costs, and lifelong disability following complicated surgeries are common for most patients. There is very limited information on infection in livestock populations due to the lack of public slaughterhouses and animal surveillance tools in the country.
We collected data on human CE cases from hospital records, statistical departments, and ultrasound examination records. Estimates of the reported incidence were used to calculate disability-adjusted life years (DALYs). To estimate the economic cost, we interviewed 65 patients who had CE surgery. The societal cost, including direct medical, direct non-medical and indirect costs, was estimated. We investigated the zoonotic linkages using the data of surgical CE cases and the livestock population of four species, including sheep, goats, cattle, and camels. To support the statistical analysis, samples were collected from CE infected animals in an endemic province. The subspecies identification, genetic diversity and haplotype network analysis were conducted. To understand the current clinical management of CE, we organized Focus Group Discussions (FGD), surveyed health professionals using a questionnaire. The ultrasound cyst images were reviewed by international experts to critically contrast current national practice with WHO-Informal Working Group on Echinococcosis (WHO-IWGE) guideline. Key challenges and further potential improvements were discussed during a workshop with Mongolian and international experts to reach consensus for standardization of clinical practice.
The incidence of surgical cases, diagnosed cases, and total cases including undiagnosed cases was estimated to be 2.2 per 100 000, 15 per 100 000 and 60 per 100 000 person-years, respectively. The DALY was estimated to be 11461 for total cases including undiagnosed cases and 3017 for diagnosed cases. The total societal cost due to human CE is USD 2.7million which equals 0.024% of total gross domestic product (GDP). The cost decreases to USD 0.3million when the productivity loss of undiagnosed and diagnosed cases is excluded. The impact on the household economies is high for surgical cases where 76% of the direct cost is paid by the patients. In total out-of-pocket expense, the cost of albendazole contributed most. US images of 84 patients were staged and assessed for interrater-agreement. The average raw agreement was 77.2%. Unweighted Kappa coefficient and weighted Kappa was 0.57 and 0.59, respectively. Mean proportion of images judged as stages CE1, CE2, CE3a, CE3b, CE4 and CL were 0.59, 0.01, 0.19, 0.08, 0.03 and 0.11 respectively. 40 cysts met the inclusion criteria of treatment modality analysis. The mean proportion of cases with a single cyst assigned to medical, percutaneous treatment, surgery and watch & wait were 52.5% (95% CI 42-65), 25.8% (95% CI 15-30), 5.1% (95% CI 0-10) and 3.3% (95% CI 0.0-10), respectively. 13.3% (95% CI 5–25) of cysts were staged as CL and therefore assigned to further diagnostic requirement. The incidence of surgical CE cases increased by a factor of 1.71 for one interquartile range increment in the density of the camel population. No significant association was observed with other livestock species. The samples collected from 96 camels and 15 goats in an endemic region showed a CE prevalence of 19.7% and 6.7%, respectively. All livestock CE were caused by E.granulosus s.l. G6/7 (formerly identified as E.granulosus canadensis G6/7) of the of the E. granulosus s.l. complex. Four haplotypes were identified within the livestock samples, two of which had not been previously reported. A common haplotype was identified between humans, camels, goats, and a wolf, all of which were within the same geographical area. A mixed infection of E. granulosus s.l. G6/G7 with different haplotypes in the intermediate host was identified first time.
This is the first estimate of the burden and societal cost of human CE in Mongolia. Mongolia has a substantial proportion of the population suffering from cystic echinococcosis. The disease causes a significant amount of loss to society and household economy. Access to fully equipped treatment centers is limited by geographic distance and economic resources. Availability of albendazole is sparse,and the price is high. WHO-IWGE guidelines are not implemented for allocating patients within the four treatment options based on CE cyst staging, with the result that all CE patients are referred for surgical treatment. This creates an unnecessary high-risk approach for patients who could either be treated with albendazole or percutaneously or observed. Our study revealed evidence that camels play an important role contributing to human CE in Mongolia, which is a critical information for further control and prevention of CE.