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Application of ultrasound in diagnosis, treatment, epidemiology, public health and control of Echinococcus granulosus and E. multilocularis

Published online by Cambridge University Press:  04 March 2004

C. N. L. MACPHERSON ,
B. BARTHOLOMOT  and
B. FRIDER
C. N. L. MACPHERSON
Affiliation:
Windward Islands Research and Education Foundation at St George's University, Grenada, West Indies
B. BARTHOLOMOT
Affiliation:
WHO collaborating Center for the Prevention and Treatment of Echinococcosis, University of Franche-Compte, Besancon, France
B. FRIDER
Affiliation:
Division of Internal Medicine, Argerich Hospital, Buenos Aires, Argentina
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Abstract

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.

Keywords

Ultrasoundepidemiologypublic healthcommunity based mass screeningcystic and alveolar hydatid disease
Type
Research Article
Information
Parasitology , Volume 127 , Issue S1 , October 2003 , pp. S21 - S35
Copyright
© 2003 Cambridge University Press

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References

REFERENCES

AMMANN, R. W. & ECKERT, J. (1995). Clinical diagnosis and treatment of echinococcosis in humans. In Echinococcus and Hydatid Disease ( ed. Thompson, R. C. A. & Lymbery, A. J. ), pp. 411–463. Wallingford, CAB International.
AMMANN, R. W. & ECKERT, J. (1996). Cestodes. Echinococcus. Gastroenterology Clinical of North America 25, 655–689.CrossRefGoogle Scholar
BAI, Y., CHENG, N., JIANG, C., WANG, Q. & CAO, D. (2002). Survey on cystic echinococcosis in Tibetans, West China. Acta Tropica 82, 381–385.CrossRefGoogle Scholar
BARBIERI, M., SEVERI, M. A., PIREZ, M. I., BATTISTONI, J. & NIETO, A. (1994). Use of specific antibody and circulating antigen serum levels in the hydatid immunodiagnosis of asymptomatic population. International Journal for Parasitology 24, 937–942.CrossRefGoogle Scholar
BARTHOLOMOT, B., VUITTON, D. A., HARRAGA, S., SHI, D. A., GIRAUDOUX, P., BARNISH, G., WANG, Y. H., MACPHERSON, C. N. L. & CRAIG, P. S. (2002). Combined ultrasound and serologic screening for hepatic alveolar echinococcosis in central China. American Journal of Tropical Medicine and Hygiene 66, 23–29.CrossRefGoogle Scholar
BCHIR, A., LAROUZE, B., BOUHAOUIA, H., BOUDEN, L. & JEMMALI, M. (1987). Echotomographic evidence for a highly endemic focus of hydatidosis in central Tunisia. Lancet 2, 684.CrossRefGoogle Scholar
BCHIR, A., LAROUZE, B., SOLTANI, M. A., HAMDI, A., BOUHAOUALA, H., DUCI, S., BOUDEN, L., GANOUNI, A., ACHOUR, A., GANDEBOUT, C., ROUSSET, J. J. & JEMMALI, M. (1991). Echotomographic and serological population based study of hydatidosis in central Tunisia. Acta Tropica 49, 149–153.CrossRefGoogle Scholar
BEGGS, J. (1983). The radiology of hydatid disease. American Journal of Roentgenology and Radium Therapy and Nuclear Medicine 145, 639–648.Google Scholar
BEN AMOR, N., GARGOURI, M., GHARBI, H. A., GOLVAN, Y. J., AYACHI, K. & KCHOUK, K. H. (1986 a). Trial therapy of inoperable abdominal hydatid cysts by puncture Annals de Parasitologie Humane et Camparial. 61, 689–692.Google Scholar
BEN AMOR, N., GARGOURI, M., GHARBI, H. A., GOLVAN, Y. J., HAMMOU-JEDDI, A., KILANI, M. & LAHMAR, S. (1986 b). Traitement du kyste hydatique du foie du mouton par ponction sous échographie. Tunisie Médicale 64, 325–331.Google Scholar
BRESSON-HADNI, S., LAPLANTE, J. J., LENYS, D., ROHMER, P., GOTTSTEIN, B., JACQUIER, P., MERCET, P., MEYER, J. P., MIGUET, J. P. & VUITTON, D. A. (1994). Seroepidemiologic screening of Echinococcus multicularis infection in a European area endemic for alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 51, 837–846.CrossRefGoogle Scholar
CAREMANI, M., BENCI, A., MAESTRINI, R., ACCORSI, A., CAREMANI, D. & LAPINI, L. (1997). Ultrasound imaging in cystic echinococcosis. Proposal of a new sonographic classification. Acta Tropica 67, 91–105.Google Scholar
CHAI, J. (1992). Seroepidemiological surveys for cystic echinococcosis in the Xinjiang Uygur Autonomous Region, PRC. In Campedium on cystic echinococcosis with Special Reference to the Xinjiang Uygur Autonomous Region. The People's Republic of China (ed. Andersen, F. L., Chai, J. & Liu, F.), pp. 153–161. Provo., Utau, Brigham Young University.
CHOJI, K., FUJITA, N., CHEN, M., SPIERS, A. S. D., MORITA, Y., SCHINOHARA, M., NORIMA, T. & IRIE, G. (1992). Alveolar hydatid disease of the liver: Computed tomography and transabdominal ultrasound with histopathological correlation. Clinical Radiology 46, 97–103.CrossRefGoogle Scholar
COHEN, H., PAOLILLO, E., BONIFACINO, R., BOTTA, B., PARADA, L., CABRERA, P., SNOWDEN, K., GASSER, R., TESSIER, R., DIBARBOURE, L., WEN, H., ALLAN, J. C., SOTO DE ALFARO, H., ROGAN, M. T. & CRAIG, P. S. (1998). Human cystic echinococcosis in a Uruguayan community: A sonographic, serologic and epidemiologic study. American Journal of Tropical Medicine and Hygiene 59, 620–627.CrossRefGoogle Scholar
COUNCIL FOR INTERNATIONAL ORGANIZATIONS OF MEDICAL SCIENCES (CIOMS) (1991). International guidelines for ethical review of epidemiological studies. In Ethics and Epidemiology: International Guidelines ( ed. Bankowski, Z., Bryant, J. J. & Last, J. M.), Geneva, CIOMS.
CRAIG, P. S., GIRADOUX, P., SHI, D., BARTHOLOMOT, B., BARNISH, G., DELATTRE, P., QUERE, J. P., HARRAGA, S., BAO, G., WANG, Y., LU, F., ITO, A. & VUITTON, D. A. (2000). An epidemiological and ecological study of human alveolar echinococcosis transmission in south Gansu, China. Acta Tropica 77, 167–177.CrossRefGoogle Scholar
CRAIG, P. S., LIU, D., MACPHERSON, C. N. L., SHI, D., REYNOLDS, D., BARNISH, G., GOTTSTEIN, B. & WANG, Z. (1992). A large focus of alveolar echinococcosis in central China. Lancet 340, 826–831.CrossRefGoogle Scholar
CRAIG, P. S., ROGAN, M. T. & ALLAN, J. C. (1996). Detection, screening and community epidemiology of taeniid cestode zoonoses: Cystic echinococcosis, alveolar echinococcosis and neurocysticercosis. Advances in Parasitology 38, 169–250.CrossRefGoogle Scholar
DAEKI, A. O., CRAIG, P. S. & SHAMBESH, M. K. (2000). IgG subclass antibody responses and the natural history of hepatic cystic echinococcosis in asymptomatic patients. Annals of Tropical Medicine and Parasitology 94, 319–328.CrossRefGoogle Scholar
DEL CARPIO, M., MOGUILANSKY, S., COSTA, M., PANOMARENKO, H., BIANCHI, G., BENDERSKY, S., LAZCANO, M., FRIDER, B. & LARRIEU, E. (2000). Diagnosis of human hydatidosis. Predictive value of a rural ultrasonographic survey in an apprently healthy population. Medicina (Buenos Aires) 60, 466–468.Google Scholar
DIDIER, D., WEILER, S., ROHMER, R., LASSEGUE, A., DESCHAMPS, J. P., VUITTON, D., MIGUET, J. P. & WEILL, F. (1985). Hepatic alveolar echinococcosis correlative US and CT study. Radiology 154, 179–186.CrossRefGoogle Scholar
FRENCH, C. M. & NELSON, G. S. (1982). Hydatid disease in the Turkana District of Lopez. II. A study in medical geography. Annals of Tropical Medicine and Parasitology 76, 439–457.CrossRefGoogle Scholar
FRIDER, B. (1996). Liver hydatidosis. Acta Latinoamerica Gastroenterologie 26, 199–200.Google Scholar
FRIDER, B. (2002). Aporte de la Ultrasonografia al conocimiento de la hidatidosis. In Situación de la Hidatidosis-Echinococcosis en la República Argentina ( ed. Denegri, G. M., Elissondo Y M. C. & Dopcich, M. ), pp. 79–99. Mar del Plata Argentina, Editorial Martín.
FRIDER, B., LARRIEU, E. & ODRIOZOLA, M. (1999). Long-term outcome of asymptomatic liver hydatidosis. Journal of Hepatology 30, 228–231.CrossRefGoogle Scholar
FRIDER, B., LOSADA, C. A., LARRIEU, E. & DE ZAVALETA, O. (1988). Asymptomatic abdominal hydatidosis detected by ultrasonography. Acta Radiologica 29, 431–434.CrossRefGoogle Scholar
FRIDER, B., MOGUILENSKY, J., SALVITTI, J. C., ODRIOZOLA, M., CANTONI, G. & LARRIEU, E. (2001). Epidemiological surveillance of human hydatidosis by means of ultrasonography: Its contribution to the evaluation of control programs. Acta Tropica 79, 219–223.CrossRefGoogle Scholar
FULLER, G. K. & FULLER, D. C. (1981). Hydatid disease in Ethiopia: clinical survey with some immunodiagnostic test results. American Journal of Tropical Medicine and Hygiene 30, 645–652.CrossRefGoogle Scholar
GEMMELL, M. A. & ROBERTS, M. G. (1995). Modelling echinococcus life cycles. In Echinococcus and hydatid disease ( ed. Thompson, R. C. A. & Lymbery, A. J.), pp. 333–354. Wallingford, CAB International.
GHARBI, H. A., HASSINE, B., BRAUNER, M. W. & DUPUCH, K. (1981). Ultrasound examination of the hydatic liver. Radiology 139, 459–463.CrossRefGoogle Scholar
GLOOR, G. (1988). Echinokokkose beim Menschen in der Schweiz 1970–83. Medical Dissertation, University of Zürich.
GOSTIN, L. (1991). Ethical principles for the conduct of human subject research: Population-based research and ethics. Law, Medicine and Healthcare 19, 191–201.CrossRefGoogle Scholar
GOTTSTEIN, B., JAQUIER, P., BRESSON-HADNI, S. & ECKERT, J. (1993). Improved primary immunodiagnosis of alveolar echinococcosis in humans by an enzyme-linked immunosorbent assay using the Em2plus antigen. Journal of Clinical Microbiology 31, 373–376.Google Scholar
GOTTSTEIN, B., LENGELAR, C., BACHMANN, P., HAGEMANN, P., KOCHER, P., BROSSARD, M., WITASSEK, F. & ECKERT, J. (1987). Sero-epidemiological survey for alveolar echinococcosis (by EM2-ELISA) of blood donors in an endemic area of Switzerland. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 960–964.CrossRefGoogle Scholar
GOTTSTEIN, B. & REICHEN, J. (1996). Echinococcosis/hydatidosis. In Manson's Tropical Diseases ( ed. Cook, G. C.), pp. 1486–1508, 20th edition. London, Saunders.
HALL, A. L. (1989). Public health trials in West Africa: Logistics and ethics. IRB 11, 8–10.CrossRefGoogle Scholar
HIRA, P. R., BAHR, G. M., SHWEIKI, H. M. & BEHBEHANI, K. (1990). Diagnostic value of anti-arc 5 IgG antibody and analysis of the IgG subclasses in sera of patients with cystic hydatid disease. Serodiagnosis and Immunotherapy in Infectious Disease 4, 285–293.CrossRefGoogle Scholar
KACHANI, M., MACPHERSON, C. N. L., LYAGOUBI, M., BERRADA, M., BOUSLIKHANE, M., KACHANI, F. & EL HASNAOUI, M. (2003). Public health education/importance and experience from the field. Educational impact of community based ultrasound screening surveys. Acta Tropica 85, 263–269.Google Scholar
KING, D. L. (1973). Ultrasonography of echinococcal cysts. Journal of Clinical Ultrasound 1, 64.CrossRefGoogle Scholar
KLUNGSOYR, P., COURTRIGHT, P. & HENDRICKSON, T. H. (1993). Hydatid disease in the Hamar of Ethiopia: A public health problem for women. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 254–255.CrossRefGoogle Scholar
LARRIEU, E., COSTA, M., CANTONI, G., ALVEREZ, J., GIMENEZ, N. & PEREZ, A. (1994). Control de la hidatidosis en la Provincia de Río Negro, Argentina. Actividades de Atención Veterinaria. Review de Saniol Higene Pública 68, 197–202.Google Scholar
LARRIEU, E., FRIDER, B., DEL CARPIO, M., SALVITTI, J. C., MERCAPIDE, C., PEREYRA, R., COSTA, M., ODRIOZOLA, M., PEREZ, A., CANTONI, G. & SUSTERCIC, J. (2000). Asymptomatic carriers of hydatidosis: Epidemiology, diagnosis and treatment. Pan American Journal of Public Health 8, 250–257.CrossRefGoogle Scholar
LARRIEU, E., GUARNERA, E., COSTA, M., ALVAREZ, J., CANTONI, G., PEREZ, A. & GIMENEZ, N. (1993). Control de la hidatidosis en la Provincia de Rio Negro: evaluación actividades atención médica. Review Sanitarica Hygien Publica 5, 377–384.Google Scholar
LEWALL, D. B. & McCORKELL, S. J. (1985). Hepatic echinococcal cysts: Sonographic appearance and classification. Radiology 155, 773–775.CrossRefGoogle Scholar
LIGHTOWLERS, M. W. & GOTTSTEIN, B. (1995). Echinococcosis/hydatidosis: Antigens, immunological and molecular diagnosis. In Echinococcus and Hydatid Disease ( ed. Thompson, R. C. A. & Lymbery, A. J. ), pp. 355–410. Wallingford, CAB International.
LINDTJORN, B., KISERUD, T. & ROTH, K. (1982). Hydatid disease in some areas of southern Ethiopia. Ethiopian Medical Journal 20, 185–188.Google Scholar
MACPHERSON, C. N. L. (1992). Ultrasound in the diagnosis of parasitic disease. Tropical Doctor 22, 14–20.CrossRefGoogle Scholar
MACPHERSON, C. N. L. (1994). Epidemiology and control of parasites in nomadic situations. Veterinary Parasitology 54, 87–102.CrossRefGoogle Scholar
MACPHERSON, C. N. L. & CRAIG, P. S. (2000). Dogs and Cestodes Zoonoses. In Dogs, Zoonoses and Public Health ( ed. Macpherson, C. N. L., Meslin, F.-X. & Wandeler, A.), pp. 177–201. Wallingford, Oxon, CAB International.CrossRef
MACPHERSON, C. N. L., GOTTSTEIN, B. & GEERTS, S. (2000). Parasitic food-borne and water borne zoonoses. Revue Scientifique et Technique Office International des Epizootics 19, 240–258.CrossRefGoogle Scholar
MACPHERSON, C. N. L. & MILNER, R. (2003). Performance characteristics and quality control of community based ultrasound surveys for cystic and alveolar echinococcosis. Acta Tropica 85, 203–209.CrossRefGoogle Scholar
MACPHERSON, C. N. L., SPOERRY, A., ZEYHLE, E., ROMIG, T. & GORFE, M. (1989). Pastoralists and hydatid disease: An ultrasound scanning prevalence survey in East Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 243–247.CrossRefGoogle Scholar
MACPHERSON, C. N. L., WACHIRA, T. M., ZEYHLE, E., ROMIG, T. & MACPHERSON, C. (1986). Hydatid disease: Research and control in Turkana, IV. The pilot control programme. Transactions of the Royal Society of Tropical and Hygiene 80, 196–200.CrossRefGoogle Scholar
MACPHERSON, C. N. L., ZEYHLE, E., ROMIG, T. & REES, P. (1987). Portable ultrasound scanner versus serology in screening for hydatid cysts in a nomadic population. Lancet ii, 259–262.CrossRefGoogle Scholar
MLIKA, N., LAROUZE, B., GAUDEBOUT, C., BRAHAM, B., ALLEGUE, M., DAZZA, M. C., DRIDI, M., GHARBI, S., GAUMER, B., BCHIR, A., ROUSSET, J. J., DELATTRE, M. & JEMMALI, M. (1986). Echotomatographic and serologic screening for hydatidosis in a Tunisian village. American Journal of Tropical Medicine and Hygiene 35, 815–817.CrossRefGoogle Scholar
MORO, P. L., MCDONALD, J., GILMAN, R. H., SILVA, B., VERASTEGUI, M., MALQUI, V., LESCNO, G., FALCON, N., MONTES, G. & BAZALAR, H. (1997). Epidemiology of Echinococcus granulosus infection in the central Peruvian Andes. Bulletin of the World Health Organization 75, 553–561.Google Scholar
NIRMALAN, N. & CRAIG, P. S. (1997). Immunoblot evaluation of the species-specifity of Em18 and Em16 antigens for serodiagnosis of human alveolar echinococcosis. Transactions of the Royal Society and Tropical Medicine and Hygiene 91, 484–486.CrossRefGoogle Scholar
NJOROGE, E. M., MBITHI, P. M., GATHUMA, J. M., WACHIRA, T. M., MAGAMBO, J. K. & ZEYHLE, E. (2000). Application of ultrasonography in prevalence studies of hydatid cysts in goats north-western Turkana, Kenya and Toposaland, southern Sudan. Onderstepoort Journal of Veterinary Research 67, 251–255.Google Scholar
OWOR, R. & BITAKAMIRE, P. K. (1975). Hydatid disease in Uganda. East African Medical Journal 52, 700–704.Google Scholar
PAWLOWSKI, Z. S., ECKERT, J., VUITTON, D. A., AMMANN, R. W., KERN, P., CRAIG, P. S., DAR, K. F., DE ROSA, F., FILICE, C., GOTTSTEIN, B., GRIMM, F., MACPHERSON, C. N. L., SATO, N., TODOROV, T., UCHINO, J., VON SINNER, W. & WEN, H. (2001). Echinococcosis in humans: Clinical aspects, diagnosis and treatment. WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern, pp. 20–71.Google Scholar
PERDOMO, R., ALVAREZ, C., FERREIRA, C., GENINAZZI, H., MONTI, J., PARADA, J. R. R., CATIVELLI, D., RIVERO, E., BARRAGUE, A. D. & PARARDA, J. (1988). Early diagnosis of hydatidosis by ultrasonography. The Lancet 1, 244.CrossRefGoogle Scholar
PERDOMO, R., ALVAREZ, C., MONTI, J., FERREIRA, C., CHIESA, A., CARBO, A., ALVEZ, R., GRAUERT, R., STEN, D., CARMONA, C. & YARZABAL, L. (1997). Principles of the surgical approach in human liver cystic ecchinococcosis. Acta Tropica 64, 109–122.CrossRefGoogle Scholar
PORRETTI, D., FELLEISEN, E., GRIMM, F., PFISTER, M., TEUSCHER, F., ZUERCHER, C., REICHEN, J. & GOTTSTEIN, B. (1999). Differential immunodiagnosis between cystic hydatid disease and other cross-reactive pathologies. American Journal of Tropical Medicine and Hygiene 60, 193–198.CrossRefGoogle Scholar
PURRIEL, P., SCHANTZ, P. M., BEOVIDE, H. & MENDOZA, G. (1974). Human echinococcosis (hydatidosis) in Uruguay: A comparison of indices and morbidity and mortality, 1962–71. Bulletin of the World Health Organization 49, 395–402.Google Scholar
RAUSCH, R. L., WILSON, J. F., SCHANTZ, P. M. & McMAHON, B. J. (1987). Spontaneous death of Echinococcus multicularis: Cases diagnosed serologically (by Em2-ELISA) and clinical significance. American Journal of Tropical Medicine and Hygiene 36, 576–585.CrossRefGoogle Scholar
ROMIG, T., ZEYHLE, E., MACPHERSON, C. N. L., REES, P. H. & WERE, J. B. O. (1986). Cyst growth and spontaneous cure in hydatid disease. Lancet 1, 861.CrossRefGoogle Scholar
SAGE, A. M., WACHIRA, T. M., ZEYHLE, E., WEBER, E. P., NJOROGE, E. & SMITH, G. (1998). Evaluation of diagnostic ultrasound as a mass screening technique for the detection of hydatid cysts in the liver and lung of sheep and goats. International Journal for Parasitology 28, 349–353.CrossRefGoogle Scholar
SARCIRON, E. M., BRESSON-HADNI, S., MERCIER, M., LAWTON, P., DURANTON, C., LENYS, D., PETAVY, A. F. & VUITTON, D. A. (1997). Antibodies against Echinococcus multilocularis alkaline phosphatase as markers for the specific diagnosis and the serological monitoring of alveolar echincoccosis. Parasite Immunology 19, 61–68.CrossRefGoogle Scholar
SASAKI, F., HATA, Y., SATO, N., HAMADA, H., TAKASHASHI, H. & UCHINO, J. (1994). Alveolar echinococcosis of the liver in children. Pediatric Surgery International 9, 32–34.CrossRefGoogle Scholar
SATO, N., NAMIENO, T., FURUYA, K., TAKAHASHI, H., YAMASHITA, K., UCHINO, J. & SUZUKI, K. (1997). Contribution of mass screening system to resectability of hepatic lesions involving Echinococcus multilocularis. Journal of Gastroenterology and Hepatology 32, 351–354.Google Scholar
SATO, N., UCHINO, J., SUZUKI, K., KAMIYAMA, T., TAKAHASHI, T., SHIMAMURA, T., UNE, Y. & NAKAJIMA, Y. (1993). IX mass screening. In Alveolar Echinococcosis of the Liver ( ed. Uchino, J. & Sato, N. ), pp. 121–129. Sapporo, Hokkaido University Medical School.
SCHANTZ, P. M., CHAI, J., CRAIG, P. S., ECKERT, J., JENKINS, D. J., MACPHERSON, C. N. L. & THAKUR, A. (1995). Epidemiology and control of hydatid disease. In Echinococcus and Hydatid Disease ( ed. Thompson, R. C. A. & Lymbery, A. J. ), pp. 233–332. Wallingford, CAB International.
SCHANTZ, P. M., WILLIAMS, J. F. & RIVA POSSE, C. (1973). The epidemiology of hydatid disease in Southern Argentina. Comparison of morbidity indices, evaluation of immunodiagnostic tests and factors affecting transmission in Southern Rio Negro Province. American Journal of Tropical Medicine and Hygiene 22, 629–641.CrossRefGoogle Scholar
SCHWABE, C. W. (1964). Veterinary Medicine and Human Health, pp. 211 & 395. Baltimore, Williams and Wilkins.
SHAMBESH, M. A., CRAIG, P. S., MACPHERSON, C. N. L., ROGAN, M., GUSBY, A. M. & ECHTUICH, E. F. (1999). An extensive ultrasound and serologic study to investigate the prevalence of cystic echinococcosis in northern Libya. American Journal of Tropical Medicine and Hygiene 60, 462–468.CrossRefGoogle Scholar
SHAMBESH, M. K., MACPHERSON, C. N. L., BEESLEY, W. N., GUSBI, A. & ELSONOSI, T. (1992). Prevalence of human hydatid disease in northwestern Libya: A cross-sectional ultrasound study. Annals of Tropical Medicine and Parasitology 86, 381–386.CrossRefGoogle Scholar
VICARY, F. R., CUSICK, G., SHIRLEY, M. & BLACKWELL, R. J. (1977). Ultrasound and abdominal hydatid disease. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 29–31.CrossRefGoogle Scholar
WANG, Y. H., ROGAN, M. T., VUITTON, D. A., WEN, H., BARTHOLOMOT, B., MACPHERSON, C. N. L., ZOU, P. F., DING, Z. X., ZHOU, H. X., ZHANG, X. F., LUO, J., XIONG, H. B., FU, Y., McVIE, A., GIRAUDOUX, P., WANG, W. G. & CRAIG, P. S. (2001). Cystic echinococcosis in semi-nomadic pastoral communities in north-west China. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 153–158.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION (1996). Informal Working Group on Echinococcosis. Guidelines for treatment of cystic and alveolar echinococcosis in humans. Bulletin of the World Health Organization 74, 231–242.
WORLD HEALTH ORGANIZATION (2001). Informal Working Group on Echinococcosis. PAIR, an option for the treatment of cystic echinoccosis, p. 40. Geneva, WHO.
WORLD HEALTH ORGANIZATION (2003). Informal Working Group on Echinococcosis. (in press). International classification of ultrasound images in cystic echinococcosis for application in clinical and field epidemiological settings. Acta Tropica 85, 253–261.
WILSON, J. F. & RAUSCH, R. L. (1980). Alveolar hydatid disease. A review of clinical features of 33 indigenous cases of Echinococcus multicularis infection in Alaskan Eskimos. American Journal of Tropical Medicine and Hygiene 29, 1340–1355.CrossRefGoogle Scholar
WILSON, J. F., RAUSCH, R. L., McMAHON, B. J. & SCHANTZ, P. M. (1992). Parasiticidal effect of chemotherapy in alveolar hydatid disease. Review of experience with mebendazole and albendazole in Alaskan Eskimos. Clinical Infectious Diseases 15, 234–249.Google Scholar
WRAY, J. R. (1958). Note on human hydatid disease in Kenya. East African Medical Journal 35, 37–39.Google Scholar