Preface
Echinococcosis: transmission biology and epidemiology
- P. S. CRAIG, D. P. McMANUS, L. H. CHAPPELL
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- 04 March 2004, p. S1
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Research Article
Echinococcosis: disease, detection and transmission
- P. S. CRAIG, M. T. ROGAN, M. CAMPOS-PONCE
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- Published online by Cambridge University Press:
- 04 March 2004, pp. S5-S20
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Echinococcosis is one of the world's most geographically widespread parasitic zoonoses, with transmission occurring in tropical, temperate and arctic biomes. Most human infections are due to Echinococcus granulosus transmitted between domestic dogs and livestock, but this cosmopolitan species also cycles between wild carnivores (principally canids) and wild ungulates. The other species with significant zoonotic potential is E. multilocularis that occurs naturally in fox definitive hosts and small mammal intermediate hosts. These two species cause human cystic or alveolar echinococcosis respectively, which may be considered serious public health problems in several regions including developed countries. This review provides an introductory overview to the Supplement and summarises the biology and epidemiology of these two related cestodes with an emphasis on applied aspects relating to detection, diagnosis and surveillance in animal and human populations, and includes aspects of transmission ecology, and also considers aspects of community epidemiology and potential for control.
Application of ultrasound in diagnosis, treatment, epidemiology, public health and control of Echinococcus granulosus and E. multilocularis
- C. N. L. MACPHERSON, B. BARTHOLOMOT, B. FRIDER
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- 04 March 2004, pp. S21-S35
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The last 30 years have seen an impressive use of ultrasonography (US) in many fields of veterinary and clinical medicine and the technique is being increasingly applied to a wide variety of parasitic infections including the cestode zoonoses Echinococcus granulosus and E. multilocularis. US provides real-time results which are permanently recordable with a high resolution and diagnostic accuracy. These properties, coupled with the clinical value of the images obtained and the non-invasive nature of the test which is safe, require no special patient preparation time; it is easy to operate and this has resulted in the establishment of US as the diagnostic technique of choice for cystic (CE) and alveolar (AE) echinococcosis. The lack of ionizing radiation and side-effects mean that examination times are not restricted. The hand-held probes facilitate what amounts to a rapid, bloodless non-invasive laparotomy, enabling a search from an infinite number of angles for lesions producing information on their number, size and type of cysts, their location and clinical implications. Such clinical information has facilitated the development of treatment protocols for different cyst types. Less invasive surgical techniques, such as US guidance for PAIR (Puncture, Aspiration, Injection, Re-aspiration), PAIRD (PAIR plus Drainage) or PPDC (Percutaneous Puncture with Drainage and Curettage) are also possible. Longitudinal US studies have facilitated monitoring the effects of the outcome of treatment and chemotherapy. Portable ultrasound scanners which today weigh as little as a few pounds, powered by battery or generators have facilitated the use of the technique in mass community-based screening studies. The majority of these studies have been conducted in remote, low socio-economic areas where there were few, if any, hospitals, veterinary facilities, schools or trained personnel. The surveys led to the discovery of unexpectedly high prevalences of CE and AE in asymptomatic individuals of endemic areas and especially amongst transhumant or nomadic pastoralists living in various parts of the world. Screening for CE and AE is justified as an early diagnosis leads to a better prognosis following treatment. The application of US in field and clinical settings has led to a better understanding of the natural history of CE and AE and to the development of a WHO standardized classification of cyst types for CE. This classification can be used in helping define the treatment options for the different cysts found during the surveys, which in turn can also be used to calculate the public health cost of treating the disease in an endemic community. The case mix revealed can also influence the specificity (particularly proportions of cyst types CE4 and CE5 and cystic lesions – CL) of US as a diagnostic test in a particular setting. Community based US surveys have provided new insights into the public health importance of CE and AE in different endemic settings. By screening whole populations they disclose the true extent of the disease and reveal particular age and sex risk factors. Through the treatment and follow-up of all infected cases found during the mass screening surveys a drastic reduction in the public health impact of the disease in endemic communities can be achieved. Educational impacts of such surveys at the national, community and individual levels for both professional and lay people are beginning to be appreciated. The translation of the information gained into active control programmes remains to be realized. In areas where intermediate hosts, such as sheep and goats, are not slaughtered in large numbers mass US screening surveys to determine the prevalence of CE in livestock has proved possible. Longitudinal studies in such intermediate hosts would reveal changes in prevalence over time, which has been used as a marker for control success in other programmes. Mass US screening surveys in an ongoing control programme in Argentina has demonstrated the early impact of control in the human population and identified breakthroughs in that control programme. Mass US screening surveys must adhere to the highest ethical standards and the outcome of surveys should result in the application of appropriate WHO recommended treatment options for different cyst types. Follow-up strategies have to be in place prior to the implementation of such surveys for all infected individuals who do not require treatment and for all suspected, but not confirmed, cases found during the surveys. The use of US in community screening surveys has revealed the complexity of ethical issues (informed consent, confidentiality, follow-up, detection of lesions that are not the focus of the study etc) and also provided real solutions to providing the most ethical guidelines for the early detection and treatment of CE and AE.
Molecular epidemiology of cystic echinococcosis
- D. P. McMANUS, R. C. A. THOMPSON
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- 04 March 2004, pp. S37-S51
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Echinococcus granulosus exhibits substantial genetic diversity that has important implications for the design and development of vaccines, diagnostic reagents and drugs effective against this parasite. DNA approaches that have been used for accurate identification of these genetic variants are presented here as is a description of their application in molecular epidemiological surveys of cystic echinococcosis in different geographical settings and host assemblages. The recent publication of the complete sequences of the mitochondrial (mt) genomes of the horse and sheep strains of E. granulosus and of E. multilocularis, and the availability of mt DNA sequences for a number of other E. granulosus genotypes, has provided additional genetic information that can be used for more in depth strain characterization and taxonomic studies of these parasites. This very rich sequence information has provided a solid molecular basis, along with a range of different biological, epidemiological, biochemical and other molecular-genetic criteria, for revising the taxonomy of the genus Echinococcus. This has been a controversial issue for some time. Furthermore, the accumulating genetic data may allow insight to several other unresolved questions such as confirming the occurrence and precise nature of the E. granulosus G9 genotype and its reservoir in Poland, whether it is present elsewhere, why the camel strain (G6 genotype) appears to affect humans in certain geographical areas but not others, more precise delineation of the host and geographic ranges of the genotypes characterised to date, and whether additional genotypes of E. granulosus remain to be identified.
Molecular tools for studies on the transmission biology of Echinococcus multilocularis
- P. DEPLAZES, A. DINKEL, A. MATHIS
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- 04 March 2004, pp. S53-S61
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Two novel approaches for diagnosis of intestinal Echinococcus multilocularis infection, the detection of E. multilocularis-specific coproantigens in ELISA and of copro-DNA by PCR, have been successfully implemented. These methods have proven their value for the post mortem and the intra vitam diagnosis of E. multilocularis in definitive hosts. They have also made novel approaches possible to study the transmission biology of the parasite as they allow detection of the infection in faecal samples collected in the environment. Coproantigen detection is the diagnostic method of choice as it is sensitive, fast and cheap. Studies on faecal samples collected in the field revealed that coproantigen detection did reflect the different prevalences in fox populations as assessed from foxes at necropsy and also the effect of deworming efforts in foxes as achieved by long-term distribution of praziquantel-containing baits. The use of PCR for routine diagnostic or large-scale purposes is hampered by the fact that DNA extraction from faecal material is a very laborious task. Therefore, PCR is rationally used for confirmatory purposes of copro-antigen-positive samples. As taeniid eggs cannot further be differentiated morphologically, PCR is the method of choice to identify E. multilocularis infections in faecal or environmental samples containing taeniid eggs. In intermediate rodent hosts, PCR is routinely used in epidemiological studies for identifying E. multilocularis from liver lesions which are often very small, atypical or calcified.
Transmission ecology of Echinococcus in wild-life in Australia and Africa
- D. J. JENKINS, C. N. L. MACPHERSON
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- 04 March 2004, pp. S63-S72
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Following the introduction of E. granulosus into Australia with domestic animals during European settlement, the parasite quickly became established in the E. granulosus-naive native animals of the continent. The distribution of E. granulosus in wildlife in Australia is restricted by rainfall, but nevertheless the parasite is currently widespread and highly prevalent in many areas including numerous national parks and privately owned farms. The human population of Africa is rapidly increasing resulting in ever more pressure on wild-life populations and habitat. National parks, reserves and conservation areas now provide important tracts of preserved habitat for maintaining populations of wildlife that are also important in the maintenance of E. granulosus. In some parts of Africa, hydatid-infected humans provide a source of E. granulosus infection to wildlife definitive hosts. In many areas felids may also act as important definitive hosts for E. granulosus with the parasite being maintained in a prey/predator relationship between lions and a range of intermediate hosts. Populations of E. granulosus-infected wild-life both in Australia and Africa act as important reservoirs in perpetuating the transmission of E. granulosus to both domestic animals and humans. In Australia, E. granulosus-infected wild-life is infiltrating urban areas and currently represents a potentially important new public health problem.
Cystic echinococcosis in the Arctic and Sub-Arctic
- R. L. RAUSCH
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- 04 March 2004, pp. S73-S85
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The northern biotype of Echinococcus granulosus occurs throughout the holarctic zones of tundra and taiga, from eastern Fennoscandia to the Bering Strait in Eurasia and in North America from arctic Alaska approximately to the northern border of the United States. The cycle of the cestode is complex in taiga at lower latitudes, because of the greater diversity of potential hosts. In the Arctic and Subarctic, however, four patterns of predator/prey relationships may be discerned. Two natural cycles involve the wolf and wild reindeer and the wolf and elk (moose), respectively. Where deer of the two species coexist, both are prey of the wolf; the interactions of the wolf and elk are here described on the basis of long-term observations made on Isle Royale (in Lake Superior near the southern limit of taiga), where only the wolf and elk serve as hosts for E. granulosus. A synanthropic cycle involving herding-dogs and domesticated reindeer caused hyperendemicity of cystic echinococcosis in arctic Eurasia, mainly in northeastern Siberia. The 4th pattern, a semi-synanthropic cycle, formerly existed in Alaska, wherein sled-dogs of the indigenous hunters became infected by consuming the lungs of wild reindeer. The sequence of changes in life-style inherent in the process of acculturation affected the occurrence of cystic echinococcosis among nomadic Iñupiat in arctic Alaska. When those people became sedentary, the environs of their early villages soon became severely contaminated by faeces of dogs, and cases of cystic echinococcosis occurred. Compared to cystic echinococcosis caused by E. granulosus adapted to synanthropic hosts (dog and domestic ungulates), the infection produced by the northern biotype is relatively benign. Nearly all diagnosed cases of cystic echinococcosis (>300) in Alaska have occurred in indigenous people; only one fatality has been recorded (in a non-indigenous person). After sled-dogs were replaced by machines, cases have become rare in Alaska. A similar effect has been observed in Fennoscandia, in the Saami and domesticated reindeer. Recent records indicate that the prevalence of cystic echinococcosis is increasing in Russia, suggesting that dogs are used there in herding.
Epidemiology of alveolar echinococcosis with particular reference to China and Europe
- D. A. VUITTON, H. ZHOU, S. BRESSON-HADNI, Q. WANG, M. PIARROUX, F. RAOUL, P. GIRAUDOUX
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- 04 March 2004, pp. S87-S107
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Human alveolar echinococcosis (AE), caused by the metacestode of the fox tapeworm Echinococcus multilocularis, is the most pathogenic zoonosis in temperate and arctic regions of the northern hemisphere. Prospective collection of human cases in some areas and mass screenings using ultrasound imaging and confirmation with serological techniques have markedly improved our knowledge of the epidemiology of the disease in humans during the past two decades. Transmission occurs when eggs of the tapeworm, excreted by the final hosts (usually foxes but also dogs, wolves and cats), are ingested accidentally by humans or during normal feeding by a variety of rodents and small lagomorphs. However, the species of host animals differ according to regional changes in mammalian fauna. This review mostly focuses on epidemiology of alveolar echinococcosis in those parts of the world where new and more accurate epidemiological data are now available, i.e. China and Europe, as well as on new epidemiological trends that can be suspected from recent case reports and/or from recent changes in animal epidemiology of E. multilocularis infection. The People's Republic of China (PRC) is a newly recognized focus on AE in Asia. Human AE cases were firstly recognized in Xinjiang Uygur Autonomous Region and Qinghai Provinces at the end of 1950s and infected animals were first reported from Ningxia in central China and north-east of Inner Mongolia in the 1980s. E. multilocularis (and human cases of AE) appears to occur in three areas: (1) Northeastern China (northeast focus): including Inner Mongolia Autonomous region and Heliongjiang Province (2) Central China (central focus): including Gansu Province, Ningxia Hui Autonomous Region, Sichuan Province, Qinghai Province and Tibet Autonomous Region and (3) Northwestern China: including Xinjiang Uygur Autonomous Region, bordered with Mongolia, Russia, Kazakhstan and Kyrgyzstan. The highest prevalence of the disease, up to 15 per cent of the population in some villages, is reached in China. In Europe, data from the European Echinococcosis Registry (EurEchinoReg: 1982–2000) show 53 autochthonous cases of AE in Austria, 3 in Belgium, 235 in France, 126 in Germany, 1 in Greece, and 112 in Switzerland, and 15 ‘imported’ cases, especially from central Asia; 14 cases were collected in Poland, a country not previously considered endemic for AE. Improved diagnostic technology, as well as a real increase in the infection rate and an extension to new areas, can explain that more than 500 cases have been reported for these 2 decades while less than 900 cases were published for the previous 7 decades. New epidemiological trends are related to an unprecedented increase in the fox population in Europe, to the unexpected development of urban foxes in Japan and in Europe, and to changes in the environmental situation in many countries worldwide due to climatic or anthropic factors which might influence the host–predator relationship in the animal reservoir and/or the behavioural characteristics of the populations in the endemic areas.
Echinococcosis on the Tibetan Plateau: prevalence and risk factors for cystic and alveolar echinococcosis in Tibetan populations in Qinghai Province, China
- P. M. SCHANTZ, H. WANG, J. QIU, F. J. LIU, E. SAITO, A. EMSHOFF, A. ITO, J. M. ROBERTS, C. DELKER
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- 04 March 2004, pp. S109-S120
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Infections by larval stages of tapeworms of the genus Echinococcus (echinococcosis or hydatid disease) are zoonotic infections of major public health importance throughout much of the world. Humans become infected through accidental ingestion of eggs passed in faeces of canid definitive hosts. Tibetan populations of China have some of the highest documented levels of infections by both Echinococcus granulosus and E. multilocularis, the causes of cystic and alveolar echinococcosis, respectively. In this study we measured the prevalence of cystic (CE) and alveolar (AE) echinococcosis disease in Tibetan communities in Qinghai, Province, China, and identified putative risk factors for both infections in these communities. 3703 volunteers in three predominately Tibetan counties of Qinghai were surveyed between June 1997 and June 1998. Parasitic lesions were diagnosed by imaging of characteristic space-occupying lesions in abdominal organs (ultrasound) or the lungs (radiographs). Specific serodiagnostic assays (Dot-ELISA and Em2-ELISA) were performed on sera of positively imaged subjects to further distinguish the disease agent. All participants completed a questionnaire documenting age, sex, education level, occupation, lifestyle (nomadic or settled), slaughter practices, drinking water source, hygienic practice and association with dogs. Data were analyzed using SAS version 8. 6·6% of the volunteers had image-confirmed infection with E. granulosus (CE) and 0·8% had E. multilocularis (AE) infection. The significant univariate factors for echinococcal infection (both CE and AE) included livestock ownership, Tibetan ethnicity, female gender, low income, herding occupation, limited education, water source, age greater than 25 years old, poor hygienic practices, offal disposal practices and dog care. Multivariate analysis revealed that livestock ownership was a significant risk factor for both forms of the disease, as well as age greater than 25 years, female gender, herding occupation, and being nomadic (vs semi-nomadic or settled). No additional significant risk factors were identified among the 344 nomadic participants. Being female and being older than 25 years of age were significant factors among the 1906 semi-nomadic participants. Among the 1445 settled participants, allowing dogs to sleep indoors was statistically significant. Issues such as inadequate assessment of animal ownership, selection bias, disease misclassification, and loss of information may have led to reduction in strength of some risk factor associations and need to be addressed in future epidemiologic analysis of echinococcosis in this population.
Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission
- P. GIRAUDOUX, P. S. CRAIG, P. DELATTRE, G. BAO, B. BARTHOLOMOT, S. HARRAGA, J.-P. QUÉRÉ, F. RAOUL, Y. WANG, D. SHI, D.-A. VUITTON
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- 04 March 2004, pp. S121-S131
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An area close to the Qinghai-Tibet plateau region and subject to intensive deforestation contains a large focus of human alveolar echinococcosis while sporadic human cases occur in the Doubs region of eastern France. The current review analyses and compares epidemiological and ecological results obtained in both regions. Analysis of rodent species assemblages within quantified rural landscapes in central China and eastern France shows a significant association between host species for the pathogenic helminth Echinococcus multilocularis, with prevalences of human alveolar echinococcosis and with land area under shrubland or grassland. This suggests that at the regional scale landscape can affect human disease distribution through interaction with small mammal communities and their population dynamics. Lidicker's ROMPA hypothesis helps to explain this association and provides a novel explanation of how landscape changes may result in increased risk of a rodent-borne zoonotic disease.
Multi-scale spatial analysis of human alveolar echinococcosis risk in China
- F. M. DANSON, A. J. GRAHAM, D. R. J. PLEYDELL, M. CAMPOS-PONCE, P. GIRAUDOUX, P. S. CRAIG
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- 04 March 2004, pp. S133-S141
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Risk factors for the transmission of Echinococcus multilocularis to humans operate at a range of spatial scales. Over a large area, such as China, regional scale risk is correlated with variation in climatic conditions because of its effect on the spatial distribution of landscapes that can support E. multilocularis transmission in wildlife hosts and the probability of egg survival. At a local scale of a few kilometres, or tens of kilometres, transmission risk is related to the spatial proximity of human populations and landscapes with active transmission. At the patch scale, when considering individual villages or households, human behavioural factors are important and for individuals genetic and immunological factors play a role. Satellite remote sensing can provide landscape information at a range of spatial scales and provide a spatial framework within which to examine transmission patterns. This paper reviews the application of remotely sensed data and spatial data analysis to develop a better understanding of disease transmission and shows how such data have been used to examine human alveolar echinocossosis infection patterns, at a range of spatial scales, in an endemic area in central China.
Transmission dynamics and control options for Echinococcus granulosus
- P. R. TORGERSON, D. D. HEATH
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- 04 March 2004, pp. S143-S158
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Cystic echinococcosis, caused by the larval stage of Echinococcus granulosus, is a global public health problem. Whilst in a few localities, such as New Zealand, the parasite has been effectively controlled or even eradicated, in most endemic regions it remains a persistent problem. In some areas, such as the former Soviet Union, the disease incidence in humans has increased rapidly in recent years. It is important to have an understanding of the transmission dynamics, both between dogs and domestic livestock where the parasite maintains itself and from dogs to people. It is from this knowledge that effective control measures can be devised to reduce the prevalence of the parasite in animals and hence reduce the incidence of human disease. Mathematical models to describe the transmission of the parasite and the effects of different control strategies were first proposed over twenty years ago. Since then further information has been acquired, new technology has been developed and better computing technology has become available. In this review, we summarise these developments and put together a theoretical framework on the interpretation of surveillance information, how this affects transmission and how this information can be exploited to develop new intervention strategies for the control of the parasite. In particular, the parasite remains a persistent or re-emerging problem in countries of low economic output where resources for an intensive control programme, that has been successful in rich countries, are not available. By understanding of the transmission biology, including mathematical modelling, alternative and cost-effective means of control can be developed.
Perspective on control options for Echinococcus multilocularis with particular reference to Japan
- A. ITO, T. ROMIG, K. TAKAHASHI
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- 04 March 2004, pp. S159-S172
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Following a brief introduction of recent advances in molecular and immunological technology for detection of persons and animals infected with Echinococcus multilocularis and an overview of the current situation of alveolar echinococcosis (AE) in Japan, perspectives on control options are discussed with reference to different epidemiological situations. AE is considered the most serious parasitic zoonosis in temperate and arctic regions of the northern hemisphere. The number of human cases differs drastically among regions. While high numbers of patients are apparently associated with high E. multilocularis prevalence in domestic dogs, e.g. in parts of Alaska and western China, the number of cases is moderate or low in areas where the parasite is mainly transmitted by wild canid species (e.g. in central Europe or temperate North America). However, the severity of the disease, the absence of curative treatment for most cases, the high cost of long-term chemotherapy and the anxiety caused for the population in highly endemic areas call for the development of preventive strategies even in regions where human AE is rare. Furthermore, in view of (1) drastically increasing numbers and infection rates of foxes involved in transmission of E. multilocularis, and (2) increasingly close contact between humans and foxes e.g. in Europe and Japan, there is considerable concern that AE incidences may in future increase in these regions. Control options depend on a variety of factors including the species of canid principally responsible for transmission and the socio-economic situation in the region. Where domestic dogs (stray or owned) are the principal hosts for E. multilocularis, control options can include those applicable to E. granulosus, i.e. reduction of the number of stray dogs, registration and regular preventive chemotherapy of owned dogs, and information campaigns for the population promoting low-risk behaviour for man and dogs. Where E. multilocularis is mainly transmitted by wild canids, the situation is far more difficult with preventive strategies still being in trial stage. Integrated control measures could include prevention information campaigns, restricting access of pet animals (dogs and cats) to rodents, chemotherapy of foxes on local or regional scales, and strategies to minimize contacts between people and foxes.