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SHORT COMMUNICATION |
1 Pingtung Rescue Center for Endangered Wild Animals, Pingtung University of Science and Technology, Neipu, Pingtung 91201, Taiwan
2 Institute of Wildlife Conservation, Pingtung University of Science and Technology, Neipu, Pingtung 91201, Taiwan
3 Department of Veterinary Medicine, National Pingtung University of Science and Technology, Neipu, Pingtung 91201, Taiwan
4 Unites States Department of Agriculture, Veterinary Services, 530 Center Street NE, Suite 335, Salem, Oregon 97301, USA
5 Corresponding author (email: kcjpei{at}mail.npust.edu.tw)
ABSTRACT:
Canine distemper is an acute or subacute, highly contagious, febrile disease that is caused by canine distemper virus (CDV). Two CDV-infected wild Taiwan ferret-badgers (Melogale moschata subauantiaca) were found in Kaohsiung County, southern Taiwan, in 2005. Each case was confirmed by detecting CDV RNA in lung and brain tissues. A suspected third case was detected based on clinical signs and histology. These cases are the first record of wildlife infected by CDV in Taiwan. It is believed that domestic dogs or coexisting wild carnivores infected with the virus were the most likely source, and a serologic survey is needed to fully understand the host range of this virus in Taiwan. In addition, further genetic sequencing is needed to determine the source of these CDV cases.
Key words: Canine distemper virus, carnivores, domestic dogs, Melogale moschata subauantiaca, Taiwan ferret-badgers.
Canine distemper virus (CDV), which belongs to the genus Morbillivirus within the family Paramyxoviridae, is a relative large (150–250 nm) single-stranded RNA virus with a lipoprotein envelope (Deem et al., 2000). Canine distemper is an acute or subacute, highly contagious, febrile disease in many carnivore species, and it can affect respiratory, integumentary, gastrointestinal, or central nervous systems (Appel and Summers, 1995; Van Moll et al., 1995; Fox et al., 1998; Barrett, 1999; Frölich et al., 2000). Transmission of this virus from one individual to the other typically occurs through aerosolization of respiratory exudates. Virus shedding begins approximately 7 days postinfection. An acutely infected carnivore, with or without clinical signs, can shed virus through many body excretions (Appel and Summers, 1995; Deem et al., 2000).
Canine distemper is one of the most dangerous infectious diseases to domestic dogs (Canis familiaris) worldwide (Anderson, 1995; Appel and Summers, 1995; Deem et al., 2000; Frölich et al., 2000). Other than Canidae, species of Ailuridae, Mustelidae, Hyaenidae, Ursidae, Viverridae, Procyonidae, and Felidae, have been reported susceptible to CDV, but morbidity and mortality vary greatly among species (Appel et al., 1994; Anderson, 1995; Appel and Summers, 1995; Hur et al., 1999; Deem et al., 2000; Frölich et al., 2000; Hirama et al., 2004). Mustelidae seem to be most susceptible to CDV (Deem et al., 2000), whereas Canidae, and perhaps Viverridae, are less susceptive (Machida et al., 1993; Deem et al., 2000). For example, an outbreak of CDV in the black-footed ferret (Mustela nigripes) population in Wyoming, USA, occurred in 1985, where most individuals in the colony died; the population became extinct shortly thereafter (Williams et al., 1988).
In Taiwan, CDV causes disease and mortality in domestic dogs (Wu et al., 2000), but little is known about CDV infections in other species. Recently, a serologic survey examined four farmed masked palm civets (Paguma larvata) and two captive leopard cats (Felis bengalensis) from central and northern Taiwan; antibodies to CDV were detected in one leopard cat (Ikeda et al., 2001). In this article, we report and discuss two confirmed and one possible case of canine distemper in wild Taiwan ferret-badgers (Melogale moschata subauantiaca).
Taiwan ferret-badgers are small nocturnal animals belonging to the family Mustelidae, commonly found in many habitats (except city and human settlements) at elevations below 2,000 m in southern Taiwan (Pei, 2001). To our knowledge, these are the first known cases of CDV infections of wild carnivores in Taiwan.
In November and December 2005, two extremely weak (TY1, LG1) and one dead (LG2) wild Taiwan ferret-badgers were found in the Taoyuan and Liouguei districts, Kaohsiung County, Taiwan. They were discovered in second-growth forests near farmlands or villages, and they were taken to the Pingtung Rescue Center for Endangered Species (Table 1
).
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For PCR, brain and lung tissues were homogenized, and total RNA was extracted using TRIzol reagent (Invitrogen, Carlsbad, California, USA) and resuspended in diethylpyrocarbonate-treated water (Xiang et al., 2001). The primers CDV-dF (forward: 5'-GGATTGCTGAGGACCTATC-TTTGAGGCG; nucleotides 772–797) and CDV-dR (reverse: 5'-CCAAGATAAC-CATGTACGGTGCTGTTTCAC; nucleotides 1027–1056) were designed from the sequence of CDV nucleocapsid protein. RT-PCR was performed with 5 µl of RNA, 2.5 µl of 0.4 mM dNTP mix, 2.5 µl of 10x RT-PCR buffer, 0.5 µl of 2 mM forward and reverse primers, 0.5 U of Taq DNA polymerase, 0.5 µl (10 U/µl) of AMV reverse transcriptase, and 0.5 µl (40 U/µl) of RNase inhibitor. Ultrapure sterile water was added to obtain a final volume of 25 µl. The final concentration of magnesium chloride was 2.5 mM. Thermocycling conditions for RNA amplification were reverse transcription 42 C (40 min) followed by 35 cycles of denaturation (94 C; 30 sec), annealing (62 C; 30 sec), and extension (72 C; 40 sec). The PCR products were analyzed on a 1.2% Seakem® agarose gel (Lonza Rockland, Inc., Rockland, Maine, USA) after staining with ethidium bromide.
Clinical signs observed with TY1 and LG1 were severe dehydration, apnea, ocular and nasal discharge, diarrhea, hypothermia, convulsions, and coma. All three animals were in good body condition with no evidence of external or internal trauma.
At necropsy, lungs seemed hemorrhagic, and meningeal blood vessels were hyperemic. Histopathologic examination revealed a variety of lesions relating to CDV (Table 2). Mild to moderate diffuse interstitial pneumonia and pulmonary hemorrhage and edema were found in all cases (Fig. 1). Nonpurulent meningoencephalitis was found with lymphocytic infiltration and perivascular cuffing in the meninges and cerebral cortex, respectively. Neuronal degeneration was scattered in cerebral cortex and eosinophilic intracytoplasmic and intranuclear inclusion bodies in cerebrum neurons and bronchiolar epithelium were found in LG1 and LG2 (Fig. 1). There were no significant histopathologic changes in other body organs.
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). All of these tissues were RT-PCR positive, with expected size of DNA fragment (285 bp).
The detection of RNA of the canine distemper virus confirmed that the LG1 and LG 2 were infected by CDV. For TY1, tissue samples were not available for RT-PCR and eosinophilic inclusion bodies were not observed (Table 2). Clinical signs and lesions in this animal, which included interstitial pneumonia, nonpurulent meningoencephalitis and perivascular cuffing, however, were consistent with canine distemper.
All three cases occurred in a very short time, and all came from a small geographical region, which suggests they might not be independent events. Because it is difficult to detect illness and mortality in wild animal populations, more cases may have been undetected and mortality often is underestimated based only on carcass recovery (Gulland, 1995). Based on the acute lesions found in the three cases presented herein and because all died in an apparent short period, CDV is highly likely to be new to the wild Taiwan ferret-badger in Taiwan. Further sequencing effort is underway to compare additional samples with other CDV strains from Taiwan.
Because the locations where these animals were found are close to rural villages, it is likely that these ferret-badgers were infected from domestic dogs. A similar case has been suggested for the CDV outbreak in lion populations near Serengeti National Park (Cleaveland et al., 2000) and in the masked palm civet population in Japan (Hirama et al., 2004). It has been estimated that 57% of CDV-infected domestic dogs may become asymptomatic carriers (Deem et al., 2000). Domestic dogs in rural Taiwan are present in high numbers compared with larger urban cities; CDV vaccination efforts in these villages are limited (Chen, pers. obs.). Unrestrained house dogs and a small number of stray dogs were observed in the rural areas where our cases were found.
Nevertheless, the possibility of these wild Taiwan ferret-badgers being infected from other coexisting wild carnivores that were carrying the virus should not be ruled out. As mentioned, unlike Mustelidae, which are highly susceptible to and easily killed by CDV (Deem et al., 2000), some carnivores, such as Viverridae, may be more resistant to CDV infections (Machida et al., 1993). Two Viverridae, the masked palm civet and the small Indian civet (Viverricula indica), are also commonly found in the same area (Chen, 2002), and they may represent reservoirs of CDV.
The impact of CDV infection to the local population of wild Taiwan ferret-badgers, and other sympatric carnivores, could be significant. For example, in August 1991, one masked palm civet was diagnosed with CDV infection in the Nishi-Tama area, near Tokyo, Japan (Machida et al., 1992, 1993). More than 200 wild raccoon dogs (Nyctereutes procyonoides) were found dead in the same area from September to December 1991; canine distemper was diagnosed based on clinical and pathologic results (Machida et al., 1993). The epizootic lasted about 3 mo, and it may have resulted in more than 70% of the raccoon dogs in the Nishi-Tama area (Machida et al., 1993). A timely CDV serologic survey done in both wild carnivores and domestic dogs in Taoyuan and Liouguei, Kaohsiung County will be valuable in assessing the level of CDV exposure in the local wild carnivore community.
The authors thank Zong-Ming Ye for laboratory examinations and the Department of Veterinary Medicine of the National Pingtung University of Science and Technology. Thanks also to the forest ranger, Xin-Da Wu, for help on sample collection and habitat information. Funding was provided by the Taiwan Forest Bureau, Council of Agriculture (grant 94 Forest Management-4.1-Conservation-02).
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Received for publication 6 November 2006.
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