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1 Owl Research Institute, PO Box 39, Charlo, Montana 59824, USA
2 North Slope Borough, Veterinary Clinic, Public Health Department, PO Box 925, Barrow, Alaska 99723, USA
3 North Slope Borough, Department of Wildlife Management, PO Box 69, Barrow, Alaska 99723, USA
4 Alaska Veterinary Pathology Services, PO Box 773072, Eagle River, Alaska 99577, USA
5 Barrow High School, Barrow, Alaska 99723, USA
9 Corresponding author (email: owlmontana{at}charlo.net)
ABSTRACT:
We identified Echinococcus multilocularis for the first time in brown lemmings (Lemmus trimucronatus) from Barrow, Alaska, USA. Of 467 brown lemmings trapped between 1995 and 2000, two males and two females (0.9%; 95% confidence interval=0.9±0.9%) were found to be infected with metacestodes of E. multilocularis. No metacestodes were found in 17 collared lemmings (Dicrostonyx rubricatus) also trapped at Barrow. In humans, E. multilocularis causes alveolar echinococcosis, which is potentially fatal. Knowledge of the distribution of this parasite is important to protect the public health.
Key words: Alaska, alveolar echinococcosis, brown lemming, Echinococcus multilocularis.
The cestode Echinococcus multilocularis is the cause of alveolar echinococcosis, also known as alveolar hydatid disease in humans. It is a potentially fatal disease that primarily affects the liver of its host (Rausch, 1967, 1986, 1995; Rausch et al., 1990a, b). In natural cycles, transmission is governed by predator–prey relationships. In North America, the ecology of E. multilocularis has been thoroughly studied in the Arctic, particularly on Saint Lawrence Island, Alaska, USA (Rausch et al., 1990b; Rausch and Fay, 2002). Herein, we report the first identification of E. multilocularis in the brown lemming (Lemmus trimucronatus) from the tundra near Barrow, Alaska, USA (71°18'N, 156°40'W). Barrow is located on the northern coastal plain and lies about 15 km southwest of Point Barrow, the most northerly point in Alaska (Brown et al., 1980). It is the largest Eskimo village in Alaska, numbering about 4,600 people.
During our study of the breeding ecology of the snowy owl (Nyctea scandiaca), lemmings were snap-trapped during June and July 1992–2004. Between 1995 and 2000, 467 brown lemmings and 17 collared lemmings (Dicrostonyx rubricatus) were trapped and their internal organs were examined for metacestodes of E. multilocularis and other taeniids. Suspicious lesions on internal organs, especially liver and kidney, were noted, and these organs were removed and placed in neutral buffered 10% formalin. They were shipped to the Alaska Veterinary Pathology Services, Eagle River (Alaska, USA) for gross pathology and histopathology. Hepatic lesions observed grossly contained metacestodes of E. multilocularis. Brood capsules containing protoscolices and calcareous corpuscles were present. Normal hepatic parenchyma was significantly reduced.
Infection with E. multilocularis was found in two male (82 and 108 g) and two female (50 and 60 g) brown lemmings captured in 1997 and 2000, respectively. The four were captured within 4 km of the neighborhoods of Barrow and Browerville. Prevalence over 5 yr was 4 of 467 (0.9%; 95% confidence interval=0.9±0.9%). No metacestodes were found in collared lemmings.
Infection of brown lemmings by E. multilocularis has rarely been described in the wild, although they are readily infected experimentally (Rausch, 1995). Despite extensive research on brown lemmings in Barrow from 1949 to 1974, metacestodes of E. multilocularis were not reported (Rausch, 1950; Pitelka, 1973; Rausch and Fay, 1988). Indeed, of 421 brown lemmings examined specifically for helminths from 1949 to 1960, none were infected with metacestodes of E. multilocularis, although other metacestodes (Taenia spp.) were found in 1953 (Rausch and Fay, 1988). The collared lemming apparently is not a suitable intermediate host in the wild (Rausch, 1995) and also appears to be refractory to experimental infection with E. multilocularis (Ohbayashi et al., 1971).
Echinococcus multilocularis is a public health concern. The pathway to humans is most commonly through ingestion of eggs from feces of dogs (Rausch et al., 1990b). Humans are believed to be infected at a young age and preclinical periods can be 20–30 yr. The median age at which alveolar echinococcosis was detected during the Saint Lawrence Island study was 53 yr (Rausch et al., 1990b).
Detection of eggs of E. multilocularis in canid feces is difficult; however, detection of E. multilocularis in the local environment is possible by monitoring small rodent hosts such as the brown lemming. Public health measures could be initiated thereafter. For example, treatment of sled dogs with praziquantel reduced infection rates of E. multilocularis by 83% (Rausch et al., 1990b). Thus, responsible animal care and monitoring of small rodents may be important measures to prevent human infection with this parasite.
We thank J. Petersen-Parett, L. Parett, A. Paulson, and M. Seidensticker for helping trap and dissect lemmings. We thank the Ukpëa
vik Iñupiat Corporation for permission to work on Iñupiat lands. D.W.H. thanks the North Slope Borough Department of Wildlife Management for support of the research on snowy owls and lemmings. We thank E. Layne for reviewing the final version of the manuscript and helping with terminology. Finally, R. Rausch made significant efforts to help us present this manuscript. We are very grateful to him.
6 Current address: North Slope Borough, Department of Wildlife Management, PO Box 69, Barrow, Alaska 99723, USA 
7 Current address: Institute of Arctic Biology, University of Alaska, PO Box 757000, Fairbanks, Alaska 99775-7000, USA
8 Current address: North Slope Borough, Department of Wildlife Management, PO Box 69, Barrow, Alaska 99723, USA
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OHBAYASHI, M., R. L. RAUSCH, AND F. H. FAY. 1971. On the ecology and distribution of Echinococcus spp. (Cestoda: Taeniidae), and characteristics of their development in the intermediate host. II. Comparative studies on the development of the larval E. multilocularis Leuckart, 1863, in the intermediate host. Japanese Journal of Veterinary Research 19(Suppl 3): 1–53.
PITELKA, F. A. 1973. Cyclic pattern of lemming populations near Barrow, Alaska. In Proceedings of the 25th celebration of the Naval Arctic Research Laboratory: Alaskan Arctic tundra, M. E. Britton (ed.). Arctic Institute of North America Technical Paper 25. University of Calgary, Alberta, Canada, pp. 199–215.
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———. 1967. On the ecology and distribution of Echinococcus spp. (Cestoda: Taeniidae), and characteristics of their development in the intermediate host. Annales de Parasitologie Humaine et Comparee 42: 1–63.
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———, AND F. H. FAY. 1988. Postoncopheral development and cycle of Taenia polyacantha Leuckart, 1856 (Cestoda: Taeniidae). Annales de Parasitologie Humaine et Comparee 63: 263–277 and 334–348.[Medline]
———. 2002. Epidemiology of alveolar echinococcosis, with reference to St. Lawrence Island, Bering Sea. In Cestode zoonoses: Echinococcosis and cysticercosis—An emergent and global problem, P. Craig and Z. Pawlowski (eds.). IOS Press, Amsterdam, Netherlands, pp. 309–325..
———, F. H. FAY, AND F. S. L. WILLIAMSON. 1990a. The ecology of Echinococcus multilocularis (Cestoda: Taeniidae) on Saint Lawrence Island, Alaska: II—Helminth populations in the definitive host. Annales de Parasitologie Humaine et Comparee 65: 131–140.[Medline]
———, J. F. WILSON, AND P. M. SCHANTZ. 1990b. A program to reduce the risk of infection by Echinococcus multilocularis: The use of praziquantel to control the cestode in a village in the hyperendemic region of Alaska. Annals of Tropical Medicine and Parasitology 84: 239–250.[Medline]
———. 1995. Life cycle patterns and geographic distribution of Echinococcus species. In Echinococcus and hydatid disease, R. C. A. Thompson and A. L. Lymbert (eds.). CAB International, Oxfordshire, UK, pp. 89–134.
Received for publication 6 May 2004.
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