Global burden of human food-borne trematodiasis: a systematic review and meta-analysis

Summary

Background

Food-borne trematodiases are a group of neglected tropical diseases caused by liver, lung, and intestinal parasitic fluke infections. As part of the Global Burden of Diseases, Injuries, and Risk Factors Study (GBD 2010 study) and a WHO initiative, we assessed the global burden of human food-borne trematodiasis, as expressed in disability-adjusted life years (DALYs) for the year 2005.

Methods

We systematically searched electronic databases for reports about human food-borne trematodiasis without language restriction, between Jan 1, 1980, and Dec 31, 2008. We used a broad search strategy with a combination of search terms and parasite and disease names. The initial search results were then screened on the basis of title, abstract, and, finally, full text. Relevant quantitative and qualitative data on human prevalence, morbidity, and mortality of food-borne trematodiasis were extracted. On the basis of available information on pathological and clinical appearance, we developed simplified disease models and did meta-analyses on the proportions and odds ratios of specified sequelae and estimated the global burden of human food-borne trematodiasis.

Findings

We screened 33 921 articles and identified 181 eligible studies containing quantitative information for inclusion in the meta-analyses. About 56·2 million people were infected with food-borne trematodes in 2005: 7·9 million had severe sequelae and 7158 died, most from cholangiocarcinoma and cerebral infection. Taken together, we estimate that the global burden of food-borne trematodiasis was 665 352 DALYs (lower estimate 479 496 DALYs; upper estimate 859 051 DALYs). Furthermore, knowledge gaps in crucial epidemiological disease parameters and methodological features for estimating the global burden of parasitic diseases that are characterised by highly focal spatial occurrence and scarce and patchy information were highlighted.

Interpretation

Despite making conservative estimates, we found that food-borne trematodiases are an important cluster of neglected diseases.

Funding

Swiss National Science Foundation; Institute for Health Metrics and Evaluation.

Introduction

Our analysis of the global burden of human food-borne trematodiasis is part of the Global Burden of Diseases, Injuries, and Risk Factors Study (the GBD 2010 study)¹ and an initiative by WHO to estimate the global burden of food-borne diseases, facilitated by WHO's Foodborne Disease Burden Epidemiology Reference Group (FERG).² Food-borne trematodiases are a cluster of infections with trematodes transmitted by consumption of undercooked, mainly aquatic, products. Species-specific life cycles have been presented elsewhere.³ Although the first documented cases of human food-borne trematodiasis date back several thousand years,3, 4 uncertainty remains about taxonomy, with new species being identified and described.5, 6 Over 80 different species of food-borne trematode have been reported from human infections (webappendix pp 1–3).5, 6, 7, 8

Food-borne trematodes are classified as liver, intestinal, or lung flukes, on the basis of their typical location in the host. From a public health point of view, the most important species are Clonorchis sinensis, Opisthorchis felineus, Opisthorchis viverrini, Fasciola gigantica, and Fasciola hepatica among the liver flukes, Echinostoma spp, Fasciolopsis buski, Heterophyes spp, and Metagonimus spp among the intestinal flukes, and Paragonimus spp among the lung flukes.5, 6, 7, 8 Other species rarely infect human beings, and are less relevant to public health.

Direct parasitological techniques via detection of eggs in the hosts' faeces, sputum, and more rarely other biofluids (eg, bile or duodenal content) are widely used for diagnosis. However, accurate detection and species-specific distinction of eggs is a challenge.3, 5, 6, 7, 8, 9, 10 Immunodiagnostic techniques and molecular methods are comparatively resource and skill intensive alternatives and therefore unlikely to become methods for routine diagnosis in endemic settings in the foreseeable future.3, 6, 7, 8, 10

Chemotherapy is the mainstay for treatment and morbidity control of food-borne trematodiasis; drugs of choice are praziquantel (against clonorchiasis, opisthorchiasis, intestinal fluke infections, and paragonimiasis)3, 5, 6, 7, 8, 10, 11 and triclabendazole (against fascioliasis).3, 7, 10, 11 Integrated control strategies, including preventive and curative measures such as improved access to adequate sanitation, information, communication, and education campaigns, food inspections, and, as much as possible, control of intermediate and final-reservoir hosts are essential.3, 6, 7, 9, 10, 12, 13 Unfortunately, awareness of food-borne trematodiasis as a public health problem is limited, and hence only a few endemic countries (eg, Japan and South Korea) have successfully initiated or maintain fully fledged national control programmes.9, 13, 14

Because of the diversity of causative pathogens, diagnostic challenges, and idiosyncrasies in the natural histories of diseases, food-borne trematode infections are among the most neglected of the so-called neglected tropical diseases.3, 15, 16 As with most other neglected tropical diseases, these trematode infections are intimately connected with and exacerbate conditions of poverty.3, 15, 17 However, because consequences are not overt and morbidity often subtle, the social, economic, and public health effects of food-borne trematodiasis are underestimated, which might also explain previous lack of estimates of global burden.3, 15, 16, 17, 18

Our study had two aims: first, to estimate the global burden of human food-borne trematodiasis in terms of disability-adjusted life years (DALYs) by following the guidelines and concepts of the GBD 2010 study;¹ and second, to identify knowledge gaps in the respective epidemiological disease parameters. Furthermore, our method is presented and discussed in detail, because it could be useful for estimating the global burden of other parasitic diseases that are characterised by highly focal spatial occurrence and scarce, scattered, and patchy information.