ArticlesGlobal burden of human food-borne trematodiasis: a systematic review and meta-analysis
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.
Section snippets
Search strategy and selection criteria
We did a broad-based computer-aided systematic review to identify all relevant information about the global burden of food-borne trematodiasis. We searched PubMed, WHOLIS, FAOBIB, Embase, CAB Abstracts, Literatura Latino Americana e do Caribe em Ciências de Saùde (LILACS), ISI Web of Science, BIOSIS preview, Science Direct, African Journals OnLine (AJOL), and the System for Information on Grey Literature in Europe (SIGLE). A broad-based search strategy was used, applying, whenever available,
Results
Our systematic review identified 33 921 studies; 181 were included in the quantitative analyses (figure 2, webappendix pp 5–13). The highest national prevalence rates of food-borne trematodiasis occurred with regard to O viverrini in Laos and Thailand (table 2). More men than women were infected with C sinesis, Opisthorchis spp, all intestinal flukes, and Paragonimus spp, whereas slightly more women than men were infected with Fasciola spp (table 3). Most pronounced sex-specific and
Discussion
We estimate that in 2005 about 56·2 million people were infected with food-borne trematodes, 7·9 million had severe sequelae, and 7158 died. Taken together, the global burden of food-borne trematodiasis was 665 352 DALYs. Importantly, food-borne trematode infections are also a disease of veterinary importance causing substantial losses in animal production and trade9 and thereby affecting human wellbeing in indirect ways.
Several peculiarities of the initial model inputs and intermediate results
References (104)
Global Burden of Disease Study, 2010
Initiative to estimate the Global Burden of Foodborne Diseases, 2011
- et al.
Food-borne trematodiases
Clin Microbiol Rev
(2009) - et al.
Fascioliasis and other plant-borne trematode zoonoses
Int J Parasitol
(2005) Intestinal flukes
- et al.
Paragonimiasis
- et al.
Plant-borne trematode zoonoses: fascioliasis and fasciolopsiasis
- et al.
Liver flukes
Control of foodborne trematode infections. Report of a WHO study group
WHO Tech Rep Ser
(1995)- et al.
Food-borne trematodes
Chemotherapy for major food-borne trematodes: a review
Expert Opin Pharmacother
Liver flukes and liver cancer
Cancer Surv
Emerging foodborne trematodiasis
Emerg Infect Dis
Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria
PLoS Med
Control of neglected tropical diseases: integrated chemotherapy and beyond
PLoS Med
Asymmetries of poverty: why global burden of disease valuations underestimate the burden of neglected tropical diseases
PLoS Negl Trop Dis
The global burden of disease. A comprehensive assessment of mortality and disability form diseases, injuries, and risk factors in 1990 and projected to 2020
Clonorchiasis and cholangiocarcinoma: etiologic relationship and imaging diagnosis
Clin Microbiol Rev
Liver fluke induces cholangiocarcinoma
PLoS Med
Precancerous lesions of intrahepatic cholangiocarcinoma
J Hepatobiliary Pancreat Surg
Infection with liver flukes (Opisthorchis viverrini, Opisthorchis felineus and Clonorchis sinensis)
IARC Monogr Eval Carcinog Risks Hum
A review of human carcinogens—Part B: biological agents
Lancet Oncol
Cholangiocarcinoma
Clin Liver Dis
Fasciolosis and tumour growth
Helminthologia
Human fasciolosis
Multiple brain hemorrhages and hematomas associated with ectopic fascioliasis in brain and eye
Surg Neurol
Food-borne intestinal trematodiases in humans
Parasitol Res
Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature
Trop Dis Bull
Paragonimus and paragonimiasis in China: a review of the literature
Chin J Parasitol Parasit Dis
Trematode infections. Opisthorchiasis, clonorchiasis, fascioliasis, and paragonimiasis
Infect Dis Clin North Am
Paragonimiasis: a view from Columbia
Clin Chest Med
Pathobiology of opisthorchiasis: an update
Acta Trop
Clonorchiasis in Korea
Korean J Parasitol
Cross-sectional study of Opisthorchis viverrini infection and cholangiocarcinoma in communities within a high-risk area in northeast Thailand
Int J Cancer
Intestinal trematodes of humans in Korea: metagonimus, heterophyids and echinostomes
Korean J Parasitol
Paragonimiasis: an important food-borne zoonosis in China
Trends Parasitol
Fecal egg output in relation to worm burden and clinical features in human opisthorchiasis
Southeast Asian J Trop Med Public Health
Relationship between faecal egg count and worm burden of Opisthorchis viverrini in human autopsy cases
Parasitology
Opisthorchis viverrini—relationships between egg counts, worms recovered and antibody-levels within an endemic community in Northeast Thailand
Parasitology
Relationship between prevalence and intensity of Opisthorchis viverrini infection, and clinical symptoms and signs in a rural community in north-east Thailand
Bull World Health Organ
Liver
Global burden of disease 2004 update: disability weights for diseases and conditions, 2004
Opisthorchiasis control in Thailand
Acta Trop
Parasitic diseases morbidity in the Russian Federation in 1999
Med Parazitol (Mosk)
Nationwide survey of human parasite in China
Southeast Asian J Trop Med Public Health
The rate of cerebral involvement in paragonimiasis: an epidemiologic study
Jpn J Parasitol
Cited by (423)
Immunology and pathology of echinostomes and other intestinal trematodes
2024, Advances in ParasitologyRare liver diseases in Egypt: Clinical and epidemiological characterization
2024, Arab Journal of GastroenterologyLiver abscess caused by the ingested foreign body without sign of gastrointestinal perforation: A case report
2023, Radiology Case ReportsExudative pleural effusion caused by lung fluke infection: A practical diagnostic approach
2023, International Journal of Infectious Diseases