Review
Echinococcosis – an international public health challenge

https://doi.org/10.1016/S0034-5288(03)00006-7Get rights and content

Abstract

This review aims to summarise some of the recent studies that have been undertaken on parasites of the genus Echinococcus and the diseases which they cause. Although the adult parasite, which inhabits the intestine of various carnivore species is not pathogenic, the larval or metacestode stages can be highly pathogenic, causing economic losses to livestock and various forms of echinococcosis in humans, some of which have a high fatality rate. There is growing evidence that there are at least 5 species of Echinococcus rather than the generally accepted 4 species. Within these species there are a number of genotypes or strains. This can have implications for surveillance and control. In some wealthy countries, cystic echinococcosis caused by Echinococcus granulosus has been successfully controlled or indeed eradicated. However, in most parts of the world it remains a serious threat to human health. In the former Soviet Union, the disease has rapidly increased in incidence after the end of communist administration. Human alveolar echinococcosis, caused by Echinococcus multilocularis, is more sporadic. However, in some Chinese communities there is a disturbingly high human prevalence and in Europe there has been an increase in the detection rate of E. multilocularis in animals in the last 10 years. Echinococcosis can present diagnostic challenges, particularly in the definitive host in areas of low endemicity. Much of the recent work relating to the use of coproantigen and PCR to overcome these difficulties is summarized. New ideas for controlling the parasite are becoming available and these include both the use of vaccination and the application of mathematical models to determine the most cost effective means of control. Effective measures that are affordable are vital if the parasite is to be controlled in poor countries.

Introduction

The genus Echinococcus is of great importance because it contains a number of zoonotic species that can cause serious ill health in man. There are at least 4 species in the genus, but recent molecular evidence suggests that there should be a taxonomic revision to at least 5 species (Table 1) or even possibly 6 (Le et al., 2002; McManus, 2002; Thompson and McManus, 2002). There is also significant strain variation in the species Echinococcus granulosus. With each species the definitive host is a carnivore, whilst the intermediate host can be one of a large number of mammalian species. The parasite is of pathogenic and economic significance in intermediate and aberrant intermediate hosts, where the larval parasite develops into a hydatid cyst. The genus is found throughout the world although a number of species have a limited geographical distribution.

Section snippets

Species and distribution

Cystic echinococcosis (CE) caused by the larval stage of E. granulosus is the most widespread of these parasites (Fig. 1). Dogs are the usual definitive hosts whilst a large number of mammalian species can be intermediate hosts, including domestic ungulates and man. In the UK, the parasite has a restricted distribution, being found mainly in mid and southern Wales. In Europe, zoonotic strains of E. granulosus are present in every country with the exceptions of Ireland, Iceland and Denmark. It

Clinical aspects

In the definitive host, adult Echinococcus penetrate deeply between the villi into the crypts of Lieberkuhn. Despite this intimate host parasite relationship there are few if any lesions. Consequently, there appears to be no ill effect on the definitive host even in the presence of very heavy infections.

In the intermediate host, hydatid cysts have been found in a large variety of mammalian species and often grow slowly, sometimes taking several years to develop. Cysts most frequently affect the

Human echinococcosis

Human echinococcosis results when man ingests eggs, which have been shed in the faeces of the definitive host. The initial phase of CE is asymptomatic with small well-encapsulated cysts. After an undefined period of several months to years, the infection may become symptomatic as a space-occupying lesion. However, 60% of infections will remain asymptomatic (Pawlowski et al., 2001). The liver is the most common organ involved, usually with over two thirds of cysts. The lungs are infected in

Epidemiology and transmission to man

Echinococcus granulosus has both sylvatic cycles, often involving wild carnivores and ungulates; and domestic cycles, usually involving dogs and farm livestock. It is the latter transmission cycle that is the most common and poses the greatest threat to human health. The highest incidence rates in man are often seen in areas where there is a close association with man and domestic livestock, often using dogs as working dogs. A common source of infection for dogs is offal from infected sheep,

Diagnosis

In the intermediate host, the presence of E. granulosus has usually been detected at post-mortem by examination of the viscera. This can provide important epidemiological data, which can be used to define the likely infection pressure (Cabrera et al., 1996; Ming et al., 1992; Torgerson et al., 1998). The main disadvantage of this approach is that a slaughterhouse sample is potentially biased. In Kenya ultrasound detected hydatid cysts in sheep and goats with a sensitivity and specificity of 54%

Control

Control of CE has always involved a combination of routine anthelmintic treatment of dogs, control and reduction of stray dog populations, supervision of the slaughter of livestock and subsequent disposal of offal, and education of the public. The prepatent period of E. granulosus is approximately 6 weeks and hence this has usually been the recommended treatment interval. Praziquantel is currently the most effective anthelmintic available for this purpose. Mathematical models have been

Conclusions

Despite the large efforts that have been put into the research and control of echinococcosis, it still remains a disease of worldwide significance. In some areas of the world, CE caused by E. granulosus is a re-emerging disease in places where it was previously at low levels. There are also disturbing trends in the distribution of E. multilocularis with an increased detection rate in Europe and a number of intensely infected communities in China. If this deteriorating trend is to be stopped

Acknowledgments

The authors would like to thank INTAS, the National Institutes of Health (USA), and The National Science Foundation (USA) for their financial support.

References (78)

  • M.W. Lightowlers et al.

    Vaccination trial in Australia and Argentina confirms the effectiveness of the EG95 vaccine in sheep

    International Journal for Parasitology

    (1999)
  • R. Malgor et al.

    Coproantigen detection in dogs experimentally infected with Echinococcus granulosus by a monoclonal antibody-based Enzyme-Linked Immunosorbant Assay

    International Journal for Parasitology

    (1997)
  • R. Ming et al.

    Frequency distribution of Echinococcus granulosus hydatid cysts in sheep populations in the Xinjiang Uygur Autonomous region, China

    Veterinary Parasitology

    (1992)
  • A.F. Petavy et al.

    Echinococcus multilocularis in domestic cats in France: A potential risk factor for alveolar hydatid disease contamination in humans

    Veterinary Parasitology

    (2000)
  • O. Roneus et al.

    The longevity of hydatid cysts in horses

    Veterinary Parasitology

    (1982)
  • A.M. Sage et al.

    Evaluation of diagnostic ultrasound as a mass screening technique for the detection of hydatid cysts in the liver and lungs of sheep and goats

    International Journal for Parasitology

    (1998)
  • R.C.A. Thompson et al.

    Equine hydatidosis. A review of the current status in Great Britain and the results of an epidemiological survey

    Veterinary Parasitology

    (1975)
  • R.C.A. Thompson et al.

    Towards a taxonomic revision of the genus Echinococcus

    Trends in Parasitology

    (2002)
  • P.R. Torgerson

    The use of mathematical models to simulate control options for echinococcosis

    Acta Tropica

    (2003)
  • P.R. Torgerson

    Economic aspects of echinococcosis

    Acta Tropica

    (2003)
  • P.R. Torgerson et al.

    Cystic echinococcosis in humans in Kyrgystan: an epidemiological study

    Acta Tropica

    (2003)
  • P.R. Torgerson et al.

    Further evidence for the long distance dispersal of taeniid eggs

    International Journal for Parasitology

    (1995)
  • P.R. Torgerson et al.

    The emerging epidemic of echinococcosis in Kazakhstan

    Transactions of the Royal Society of Tropical Medicine and Hygiene

    (2002)
  • P.R. Torgerson et al.

    Modelling the prevalence of Echinococcus and Taenia species in small ruminants of different ages in Northern Jordan

    Veterinary Parasitology

    (1998)
  • J.C. Allan et al.

    Coproantigen for the detection for immunodiagnosis of echinococcosis and taeniasis in dogs and humans

    Parasitology

    (1992)
  • P.A. Cabrera et al.

    Transmission dynamics of Echinococcus granulosus, Taenia Hydatigena and Taenia ovis in sheep in Uruguay

    International Journal for Parasitology

    (1996)
  • C. Carmona et al.

    Risk factors associated with human cystic echinococcosis in Florida, Uruguay: results of a mass screening study using ultrasound and serology

    American Journal of Tropical Medicine and Hygiene

    (1998)
  • P. Deplazes et al.

    Detection of Echinococcus coproantigens by enzyme-linked immunoabsorbent assay in dogs, dingoes and foxes

    Parasitology Research

    (1992)
  • P. Deplazes et al.

    Echinococcus multilocularis coproantigen detection by immunoabsorbant assay in fox, dog and cat populations

    Journal of Parasitology

    (1999)
  • P. Deplazes et al.

    Urban transmission of Echinococcus multilocularis

  • A. Dinkel et al.

    Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy

    Journal of Clinical Microbiology

    (1998)
  • P. Dowling et al.

    Risk factors associated with human cystic echinococcosis in Jordan: results of a case-control study

    Annals of Tropical Medicine and Parasitology

    (2000)
  • J. Eckert

    Echinococcus multilocularis and alveolar echinococcosis in Europe (except parts of Eastern Europe)

  • J. Eckert

    Epidemiology of Echinococcus multilocularis and E. granulosus in central Europe

    Parassitologia

    (1997)
  • J. Eckert

    Alveolar echinococcosis (Echinococcus multilocularis ) and other forms of echinococcosis (Echinococcus vogeli and Echinococcus oligarthrus)

  • J. Eckert et al.

    Echinococcosis in animals: clinical aspects, diagnosis and treatment

  • P. Economides et al.

    Experience gained and evaluation of the echinococcosis/hydatidosis eradication programmes in Cyprus 1971–1999

  • Fen-Jie, L., 1993. Prevalence of Echinococcus granulosus in Dogs in the Xinjiang Uygur Autonomous Region, PRC. In:...
  • A. Fraser et al.

    Detection of cestode infections in the definitive hosts: present status and future advances

  • Cited by (163)

    • Cystic, Alveolar and Neotropical Echinococcosis

      2023, Manson's Tropical Diseases, Fourth Edition
    • Seroprevalence of human cystic echinococcosis in South Kashmir, India

      2020, Parasite Epidemiology and Control
      Citation Excerpt :

      All serum samples were stored at −70 °C until antibody determination. Specific ELISA was used for detecting specific anti Echinococcus granulosus antibodies in the sera of participants as described earlier (Torgerson and Budke, 2003; Chiraga et al., 2014. Specific ELISA used was a commercially prepared kit (Echinococcus ELISA IgG- NovaTec, Germany –D-63128).

    View all citing articles on Scopus
    View full text