Boireau P; Food and Agriculture Organization of the United Nations, World Health Organization, 2014. Multicriteria-Based Ranking for Risk Management of Food-Borne Parasites: Report of a Joint FAO/WHO Expert Meeting, September 3–7, 2012, FAO Headquarters, Rome, Italy. Rome, Italy, Geneva, Switzerland: Food and Agriculture Organization of the United Nations; World Health Organization.
Wen H, Vuitton L, Tuxun T, Li J, Vuitton DA, Zhang W, McManus DP, 2019. Echinococcosis: advances in the 21st century. Clin Microbiol Rev 32: e00075-18.
Torgerson PR, Keller K, Magnotta M, Ragland N, 2010. The global burden of alveolar echinococcosis. PLoS Negl Trop Dis 4: e722.
Eckert J, Thompson RC, 2017. Historical aspects of echinococcosis. Adv Parasitology 95: 1–64.
Thompson RCA, 2017. Chapter two - biology and systematics of Echinococcus. Thompson RCA, Deplazes P, Lymbery AJ, eds. Advances in Parasitology, Vol. 95. London, UK: Academic Press, 65–109.
Corsini M, Geissbuhler U, Howard J, Gottstein B, Spreng D, Frey CF, 2015. Clinical presentation, diagnosis, therapy and outcome of alveolar echinococcosis in dogs. Vet Rec 177: 569.
Craig PS, Hegglin D, Lightowlers MW, Torgerson PR, Wang Q, 2017. Chapter two - echinococcosis: control and prevention. Thompson RCA, Deplazes P, Lymbery AJ, eds. Advances in Parasitology, Vol. 96. Academic Press, 55–158.
Eckert J, Deplazes P, 2004. Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev 17: 107–135.
Chauchet A et al. 2014. Increased incidence and characteristics of alveolar echinococcosis in patients with immunosuppression-associated conditions. Clin Infect Dis 59: 1095–1104.
Vuitton DA, Demonmerot F, Knapp J, Knapp J, Richou C, Grenouillet F, Chauchet A, Vuitton L, Bresson-Hadni S, Millon L, 2015. Clinical epidemiology of human AE in Europe. Vet Parasitol 213: 110–120.
Brunetti E, Kern P, Vuitton DA, 2010. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 114: 1–16.
Buttenschoen K, Gruener B, Carli Buttenschoen D, Reuter S, Henne-Bruns D, Kern P, 2009. Palliative operation for the treatment of alveolar echinococcosis. Langenbecks Arch Surg 394: 199–204.
Siles-Lucas M, Casulli A, Cirilli R, Carmena D, 2018. Progress in the pharmacological treatment of human cystic and alveolar echinococcosis: compounds and therapeutic targets. PLoS Negl Trop Dis 12: e0006422.
Aliakbarian M, Tohidinezhad F, Eslami S, Akhavan-Rezayat K, 2018. Liver transplantation for hepatic alveolar echinococcosis: literature review and three new cases. Infect Dis (Lond) 50: 452–459.
Spotin A, Boufana B, Ahmadpour E, Casulli A, Mahami-Oskouei M, Rouhani S, Javadi-Mamaghani A, Shahrivar F, Khoshakhlagh P, 2018. Assessment of the global pattern of genetic diversity in Echinococcus multilocularis inferred by mitochondrial DNA sequences. Vet Parasitol 262: 30–41.
Nakao M, Xiao N, Okamoto M, Yanagida T, Sako Y, Ito A, 2009. Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitol Int 58: 384–389.
James E, Boyd W, 1937. Echinococcus alveolaris: (with the report of a case). Can Med Assoc J 36: 354–356.
Klein C, Massolo A, 2015. Demonstration that a case of human alveolar echinococcosis in Minnesota in 1977 was caused by the N2 strain. Am J Trop Med Hyg 92: 477–478.
Gamble WG, Segal M, Schantz PM, Rausch RL, 1979. Alveolar hydatid disease in Minnesota. First human case acquired in the contiguous United States. JAMA 241: 904–907.
Wilson JF, Rausch RL, 1980. Alveolar hydatid disease. A review of clinical features of 33 indigenous cases of Echinococcus multilocularis infection in Alaskan Eskimos. Am J Trop Med Hyg 29: 1340–1355.
Polish LB, Pritt B, Barth TFE, Gottstein B, O’Connell EM, Gibson PC, 2020. Echinococcus multilocularis: first European haplotype identified in the United States: an emerging disease? Clin Infect Dis. 2020 Mar 21 (Epub ahead of print): ciaa245. https://doi.org/10.1093/cid/ciaa245.
Bartel MH, Seesee FM, Worley DE, 1992. Comparison of Montana and Alaska isolates of Echinococcus multilocularis in gerbils with observations on the cyst growth, hook characteristics, and host response. J Parasitol 78: 529–532.
Hildreth MB, Sriram S, Gottstein B, Wilson M, Schantz PM, 2000. Failure to identify alveolar echinococcosis in trappers from South Dakota in spite of high prevalence of Echinococcus multilocularis in wild canids. J Parasitol 86: 75–77.
Massolo A et al. 2019. European Echinococcus multilocularis identified in patients in Canada. New Engl J Med 381: 384–385.
Gesy K, Hill JE, Schwantje H, Liccioli S, Jenkins EJ, 2013. Establishment of a European-type strain of Echinococcus multilocularis in Canadian wildlife. Parasitology 140: 1133–1137.
Gesy KM, Jenkins EJ, 2015. Introduced and native haplotypes of Echinococcus multilocularis in wildlife in saskatchewan, Canada. J Wildl Dis 51: 743–748.
Jenkins EJ, Peregrine AS, Hill JE, Somers C, Gesy K, Barnes B, Gottstein B, Polley L, 2012. Detection of European strain of Echinococcus multilocularis in North America. Emerg Infect Dis 18: 1010–1012.
Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, 2008. Global trends in emerging infectious diseases. Nature 451: 990–993.
Gottstein B, Schantz PM, Todorov T, Saimot AG, Jacquier P, 1986. An international study on the serological differential diagnosis of human cystic and alveolar echinococcosis. Bull World Health Organ 64: 101–105.
Xiao N et al. 2003. Evaluation of use of recombinant Em18 and affinity-purified Em18 for serological differentiation of alveolar echinococcosis from cystic echinococcosis and other parasitic infections. J Clin Microbiol 41: 3351–3353.
Muller N, Frei E, Nunez S, Gottstein B, 2007. Improved serodiagnosis of alveolar echinococcosis of humans using an in vitro-produced Echinococcus multilocularis antigen. Parasitology 134: 879–888.
Muller N, Zimmermann V, Forster U, Bienz M, Gottstein B, Welle M, 2003. PCR-based detection of canine Leishmania infections in formalin-fixed and paraffin-embedded skin biopsies: elaboration of a protocol for quality assessment of the diagnostic amplification reaction. Vet Parasitol 114: 223–229.
Trachsel D, Deplazes P, Mathis A, 2007. Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134: 911–920.
Bremermann HJ, Thieme HR, 1989. A competitive exclusion principle for pathogen virulence. J Math Biol 27: 179–190.
Massolo A, Liccioli S, Budke C, Klein C, 2014. Echinococcus multilocularis in North America: the great unknown. Parasite 21: 73.
Luong LT, Chambers JL, Moizis A, Stock TM, St Clair CC, 2018. Helminth parasites and zoonotic risk associated with urban coyotes (Canis latrans) in Alberta, Canada. J Helminthol 94: e25.
Liccioli S, Kutz SJ, Ruckstuhl KE, Massolo A, 2014. Spatial heterogeneity and temporal variations in Echinococcus multilocularis infections in wild hosts in a North American urban setting. Int J Parasitol 44: 457–465.
Catalano S, Lejeune M, Liccioli S, Verocai GG, Gesy KM, Jenkins EJ, Kutz SJ, Fuentealba C, Duignan PJ, Massolo A, 2012. Echinococcus multilocularis in urban coyotes, Alberta, Canada. Emerg Infect Dis 18: 1625–1628.
Nation PN, St Clair CC, 2019. A forensic pathology investigation of dismembered domestic cats: coyotes or cults? Vet Pathol 56: 444–451.
Sailer M, Soelder B, Allerberger F, Zaknun D, Feichtinger H, Gottstein B, 1997. Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. J Pediatr 130: 320–323.
Zingg W et al. 2004. Alveolar echinococcosis of the liver in an adult with human immunodeficiency virus type-1 infection. Infection 32: 299–302.
Stojkovic M, Mickan C, Weber TF, Junghanss T, 2015. Pitfalls in diagnosis and treatment of alveolar echinococcosis: a sentinel case series. BMJ Open Gastroenterol 2: e000036.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 7280 | 2233 | 238 |
Full Text Views | 1335 | 28 | 4 |
PDF Downloads | 892 | 30 | 0 |
Human alveolar echinococcosis (AE) is a zoonotic cestode infection which is usually fatal in the absence of treatment. Treatment involves major surgery or indefinite antiparasitic therapy. The incidence is rising in Europe and Asia, with an increased risk observed in immunocompromised individuals. Previously, AE acquisition in North America was extremely rare, except for one remote Alaskan Island. Recent studies have demonstrated a new European-like strain of Echinococcus multilocularis (Em) in wildlife and in human AE in western Canada. We report the experience of all AE patients diagnosed in Alberta. Each was diagnosed by histopathology, serology, and PCR-confirmed by a reference laboratory. Seventeen cases of human AE, aged 19–78 years, nine females, were diagnosed between 2013 and 2020: all definitely or probably acquired in Alberta. Six lived in urban areas, and 14 had kept dogs. In eight, the lesions were found incidentally on abdominal imaging performed for other indications. Six were immunocompromised to varying degrees. Six were first diagnosed at surgery. All have been recommended benzimidazole therapy. One died of surgical complications. Clinicians should be aware of this diagnostic possibility in patients presenting with focal nonmalignant hepatic mass lesions. Greater urbanization of coyotes, the predominant definitive host of Em in Alberta, and growing numbers of immune suppressed individuals in the human population may lead to increasing recognition of AE in North America.
Disclosure: The University of Alberta (REB Pro00097735) approved the study.
Authors’ addresses: Stan Houston, Department of Medicine/Public Health, University of Alberta, Edmonton, Canada, E-mail: shouston@ualberta.ca. Sara Belga, Department of Medicine, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada, and Department of Medicine, Faculty of Medicine, University of British Columbia, Vancouver, Canada, E-mail: sara.belga@ubc.ca. Klaus Buttenschoen and Jutta Preiksaitis, Department of Surgery, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada, E-mails: klaus.buttenschoen@ualberta.ca and jutta@ualberta.ca. Ryan Cooper, Department of Medicine, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada, E-mail: rdcooper@ualberta.ca. Safwat Girgis, Department of Anatomical Pathology, University of Alberta, Edmonton, Canada, E-mail: sgirgis@ualberta.ca. Bruno Gottstein, Institute of Parasitology, University of Bern, Bern, Switzerland, E-mail: bruno.gottstein@ifik.unibe.ch. Gavin Low and Philippe Sarlieve, Department of Radiology and Diagnostic Imaging, University of Alberta Faculty of Medicine and Dentistry, Edmonton, Canada, E-mails: low1@ualberta.ca and sarlieve@ualberta.ca. Alessandro Massolo, Department of Biology, University of Pisa, Pisa, Italy, E-mail: alessandro.massolo@unipi.it. Clayton MacDonald, University of Alberta Faculty of Medicine and Dentistry, Alberta, Edmonton, Canada, E-mail: clayton.macdonald2@vch.ca. Norbert Müller, Department of Parasitology, Vetsuisse Faculty Bern, Bern, Switzerland, E-mail: norbert.mueller@vetsuisse.unibe.ch. Stephen Vaughan, Department of Infectious Diseases, Universiity of Calgary, Calgary, Canada, E-mail: stephen.vaughan@albertahealthservices.ca. Kinga Kowalewska-Grochowska, Provincial Laboratory of Public Health, University of Alberta Faculty of Medicine and Dentistry, Edmonton, Canada, E-mail: kinga.kowalewska-grochowska@albertaprecisionlabs.ca.
Boireau P; Food and Agriculture Organization of the United Nations, World Health Organization, 2014. Multicriteria-Based Ranking for Risk Management of Food-Borne Parasites: Report of a Joint FAO/WHO Expert Meeting, September 3–7, 2012, FAO Headquarters, Rome, Italy. Rome, Italy, Geneva, Switzerland: Food and Agriculture Organization of the United Nations; World Health Organization.
Wen H, Vuitton L, Tuxun T, Li J, Vuitton DA, Zhang W, McManus DP, 2019. Echinococcosis: advances in the 21st century. Clin Microbiol Rev 32: e00075-18.
Torgerson PR, Keller K, Magnotta M, Ragland N, 2010. The global burden of alveolar echinococcosis. PLoS Negl Trop Dis 4: e722.
Eckert J, Thompson RC, 2017. Historical aspects of echinococcosis. Adv Parasitology 95: 1–64.
Thompson RCA, 2017. Chapter two - biology and systematics of Echinococcus. Thompson RCA, Deplazes P, Lymbery AJ, eds. Advances in Parasitology, Vol. 95. London, UK: Academic Press, 65–109.
Corsini M, Geissbuhler U, Howard J, Gottstein B, Spreng D, Frey CF, 2015. Clinical presentation, diagnosis, therapy and outcome of alveolar echinococcosis in dogs. Vet Rec 177: 569.
Craig PS, Hegglin D, Lightowlers MW, Torgerson PR, Wang Q, 2017. Chapter two - echinococcosis: control and prevention. Thompson RCA, Deplazes P, Lymbery AJ, eds. Advances in Parasitology, Vol. 96. Academic Press, 55–158.
Eckert J, Deplazes P, 2004. Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev 17: 107–135.
Chauchet A et al. 2014. Increased incidence and characteristics of alveolar echinococcosis in patients with immunosuppression-associated conditions. Clin Infect Dis 59: 1095–1104.
Vuitton DA, Demonmerot F, Knapp J, Knapp J, Richou C, Grenouillet F, Chauchet A, Vuitton L, Bresson-Hadni S, Millon L, 2015. Clinical epidemiology of human AE in Europe. Vet Parasitol 213: 110–120.
Brunetti E, Kern P, Vuitton DA, 2010. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 114: 1–16.
Buttenschoen K, Gruener B, Carli Buttenschoen D, Reuter S, Henne-Bruns D, Kern P, 2009. Palliative operation for the treatment of alveolar echinococcosis. Langenbecks Arch Surg 394: 199–204.
Siles-Lucas M, Casulli A, Cirilli R, Carmena D, 2018. Progress in the pharmacological treatment of human cystic and alveolar echinococcosis: compounds and therapeutic targets. PLoS Negl Trop Dis 12: e0006422.
Aliakbarian M, Tohidinezhad F, Eslami S, Akhavan-Rezayat K, 2018. Liver transplantation for hepatic alveolar echinococcosis: literature review and three new cases. Infect Dis (Lond) 50: 452–459.
Spotin A, Boufana B, Ahmadpour E, Casulli A, Mahami-Oskouei M, Rouhani S, Javadi-Mamaghani A, Shahrivar F, Khoshakhlagh P, 2018. Assessment of the global pattern of genetic diversity in Echinococcus multilocularis inferred by mitochondrial DNA sequences. Vet Parasitol 262: 30–41.
Nakao M, Xiao N, Okamoto M, Yanagida T, Sako Y, Ito A, 2009. Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitol Int 58: 384–389.
James E, Boyd W, 1937. Echinococcus alveolaris: (with the report of a case). Can Med Assoc J 36: 354–356.
Klein C, Massolo A, 2015. Demonstration that a case of human alveolar echinococcosis in Minnesota in 1977 was caused by the N2 strain. Am J Trop Med Hyg 92: 477–478.
Gamble WG, Segal M, Schantz PM, Rausch RL, 1979. Alveolar hydatid disease in Minnesota. First human case acquired in the contiguous United States. JAMA 241: 904–907.
Wilson JF, Rausch RL, 1980. Alveolar hydatid disease. A review of clinical features of 33 indigenous cases of Echinococcus multilocularis infection in Alaskan Eskimos. Am J Trop Med Hyg 29: 1340–1355.
Polish LB, Pritt B, Barth TFE, Gottstein B, O’Connell EM, Gibson PC, 2020. Echinococcus multilocularis: first European haplotype identified in the United States: an emerging disease? Clin Infect Dis. 2020 Mar 21 (Epub ahead of print): ciaa245. https://doi.org/10.1093/cid/ciaa245.
Bartel MH, Seesee FM, Worley DE, 1992. Comparison of Montana and Alaska isolates of Echinococcus multilocularis in gerbils with observations on the cyst growth, hook characteristics, and host response. J Parasitol 78: 529–532.
Hildreth MB, Sriram S, Gottstein B, Wilson M, Schantz PM, 2000. Failure to identify alveolar echinococcosis in trappers from South Dakota in spite of high prevalence of Echinococcus multilocularis in wild canids. J Parasitol 86: 75–77.
Massolo A et al. 2019. European Echinococcus multilocularis identified in patients in Canada. New Engl J Med 381: 384–385.
Gesy K, Hill JE, Schwantje H, Liccioli S, Jenkins EJ, 2013. Establishment of a European-type strain of Echinococcus multilocularis in Canadian wildlife. Parasitology 140: 1133–1137.
Gesy KM, Jenkins EJ, 2015. Introduced and native haplotypes of Echinococcus multilocularis in wildlife in saskatchewan, Canada. J Wildl Dis 51: 743–748.
Jenkins EJ, Peregrine AS, Hill JE, Somers C, Gesy K, Barnes B, Gottstein B, Polley L, 2012. Detection of European strain of Echinococcus multilocularis in North America. Emerg Infect Dis 18: 1010–1012.
Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, 2008. Global trends in emerging infectious diseases. Nature 451: 990–993.
Gottstein B, Schantz PM, Todorov T, Saimot AG, Jacquier P, 1986. An international study on the serological differential diagnosis of human cystic and alveolar echinococcosis. Bull World Health Organ 64: 101–105.
Xiao N et al. 2003. Evaluation of use of recombinant Em18 and affinity-purified Em18 for serological differentiation of alveolar echinococcosis from cystic echinococcosis and other parasitic infections. J Clin Microbiol 41: 3351–3353.
Muller N, Frei E, Nunez S, Gottstein B, 2007. Improved serodiagnosis of alveolar echinococcosis of humans using an in vitro-produced Echinococcus multilocularis antigen. Parasitology 134: 879–888.
Muller N, Zimmermann V, Forster U, Bienz M, Gottstein B, Welle M, 2003. PCR-based detection of canine Leishmania infections in formalin-fixed and paraffin-embedded skin biopsies: elaboration of a protocol for quality assessment of the diagnostic amplification reaction. Vet Parasitol 114: 223–229.
Trachsel D, Deplazes P, Mathis A, 2007. Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134: 911–920.
Bremermann HJ, Thieme HR, 1989. A competitive exclusion principle for pathogen virulence. J Math Biol 27: 179–190.
Massolo A, Liccioli S, Budke C, Klein C, 2014. Echinococcus multilocularis in North America: the great unknown. Parasite 21: 73.
Luong LT, Chambers JL, Moizis A, Stock TM, St Clair CC, 2018. Helminth parasites and zoonotic risk associated with urban coyotes (Canis latrans) in Alberta, Canada. J Helminthol 94: e25.
Liccioli S, Kutz SJ, Ruckstuhl KE, Massolo A, 2014. Spatial heterogeneity and temporal variations in Echinococcus multilocularis infections in wild hosts in a North American urban setting. Int J Parasitol 44: 457–465.
Catalano S, Lejeune M, Liccioli S, Verocai GG, Gesy KM, Jenkins EJ, Kutz SJ, Fuentealba C, Duignan PJ, Massolo A, 2012. Echinococcus multilocularis in urban coyotes, Alberta, Canada. Emerg Infect Dis 18: 1625–1628.
Nation PN, St Clair CC, 2019. A forensic pathology investigation of dismembered domestic cats: coyotes or cults? Vet Pathol 56: 444–451.
Sailer M, Soelder B, Allerberger F, Zaknun D, Feichtinger H, Gottstein B, 1997. Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. J Pediatr 130: 320–323.
Zingg W et al. 2004. Alveolar echinococcosis of the liver in an adult with human immunodeficiency virus type-1 infection. Infection 32: 299–302.
Stojkovic M, Mickan C, Weber TF, Junghanss T, 2015. Pitfalls in diagnosis and treatment of alveolar echinococcosis: a sentinel case series. BMJ Open Gastroenterol 2: e000036.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 7280 | 2233 | 238 |
Full Text Views | 1335 | 28 | 4 |
PDF Downloads | 892 | 30 | 0 |