Abstract

Three of seven (43%) captive wild Pacific common murres (Uria aalge) and 11 of 11 (100%) captive reared pigeon guillemots (Cepphus columba) exhibited cutaneous and intraoral avian pox over the course of 7 months. The disease was mild and self limiting in the murres but 4 of 5 male pigeon guillemots died and the remaining pigeon guillemots had severe and long lasting infections. Lesions included multi-focal hyperplastic and secondarily infected nodules inside the mouth and on the muco-cutaneous junctions of the beak, nostrils and eyes. In the pigeon guillemots, nodules were more common inside the mouth (diphtheritic form) with typical cutaneous lesions also seen on the face, the foot webs and, in one case, the skin of the head, back and wings. All affected birds continued to eat their regular diet of vitamin supplemented previously frozen fish and krill but exhibited varying weight loss and, in some cases, loss of waterproofing. Histopathology revealed marked epidermal hyperplasia with intracellular Bollinger bodies in acute lesions. Marked chronic ulcerative dermatitis with intralesional bacteria and severe weight loss was seen in dead birds. Cardiovascular collapse and bacterial septicemia were considered as the immediate cause of death. The incubation period appeared to range from 30 to greater than 60 days and duration of lesions was 2 to 3 weeks in the common murres and 7 to 10 weeks in the pigeon guillemots. Use of laser surgery early in the disease did not appear to alter the course of the infection. Pox virus was isolated in chicken egg embryo cultures from active lesions but none was found in environmental or cloacal and choanal swabs collected 4 and 8 weeks after resolution of visible lesions. The source of the original infection could not be positively established. Multiple other avian species in an open air captive exhibit were exposed and none showed evidence of infection. Further research is planned to further characterize this virus and to develop diagnostic screening tools.

History and Clinical Findings

Seven Pacific common murres (Uria aalge), 2 male and 5 female, were declared non releasable after rehabilitation efforts in Oregon and transferred to the Alaska SeaLife Center in January 2004. Ages ranged from 7 months to adults. After a 2 month quarantine period, four of the birds were placed in a mixed species open air exhibit while the remaining three were held for continued treatment of various chronic infections (pododermatitis, high WBC and a bone injury). Avian pox was subsequently diagnosed from a biopsy of a 6 mm nodule excised from one of the female murres remaining in treatment. The lesion appeared 56 days after the birds had arrived in quarantine and was found in an atypical location in the middle of the keratinized portion of the mandibular beak but histopathology revealed typical marked epidermal hyperplasia with intralesional Bollinger bodies.

The affected common murre continued to be held in the quarantine pool with her two pool mates and the lesion healed uneventfully within 3 weeks. In April, 29 days after their last exposure to the originally affected bird, the two female murres previously released into the exhibit each developed a single cutaneous pox lesion at the commissure of the beak. All four murres were removed from the exhibit and returned to the quarantine pool room. All lesions in the three affected birds resolved uneventfully without specific treatment within 10 to 20 days of appearance and the remaining four murres showed no signs of infection. All seven birds were returned to the Oregon facility in mid May after resolution of the pox lesions and their pre existing health problems.

On May 10, a 4-year-old captive reared male pigeon guillemot was removed from the exhibit and placed in a portable net enclosed backholding pool due to mate aggression. The pool had previously been used to hold one of the affected common murres but had been cleaned and disinfected with bleach prior to reuse. One week after moving to the backholding pool, a lesion typical of cutaneous pox was noted on the margin of the beak of this guillemot and full quarantine was instituted. 10 additional adult guillemots (5 males and 5 females) were left in the exhibit and observed for signs of lesions along with 10 tufted puffins (Fratercula cirrhata), 10 red-legged kittiwakes (Rissa brevirostris), 3 longtail ducks (Clangula hyemalis), 2 black oystercatchers (Haematopus bachmani) and a horned puffin (Fratercula cornicualta). Four weeks later, a second male pigeon guillemot developed an intraoral lesion, typical of diphtheritic pox. At that point, all of the pigeon guillemots were removed from the exhibit. Unaffected birds were placed together in a large quarantine pool room and the two affected birds held in a second quarantine pool room. Over the next three months, additional guillemots were found to have pox lesions and were transferred to the "affected" room until all 11 birds had developed lesions by the first week of August. Attempts to ablate early lesions in 3 guillemots with laser surgery were unsuccessful and lesions recurred at the same and additional sites in these birds. All of the pigeon guillemots developed multifocal hyperplastic and secondarily infected nodules inside the mouth and on the muco-cutaneous junctions of the beak, nostrils or eyes. Nodules were also seen on the foot webs and, in one case, the skin of the head, back and wings. Intraoral lesions were massive in some birds and all had long courses of infection ranging from 7 to 10 weeks. Affected birds continued to eat their regular diet of vitamin supplemented previously frozen fish and krill but exhibited varying weight loss and, in some cases, loss of waterproofing. Severely debilitated birds were handled once daily for force feeding and administration of trimethoprim sulfamethoxazole (60 mg / kg / day) and itraconazole (10 mg / kg/day) placed in the force fed fish.

Four of the five male pigeon guillemots died yielding an overall mortality of 36% (4/11). Necropsy and histopathology revealed severe weight loss and marked chronic ulcerative dermatitis with intra-lesional bacteria. Shock and bacterial septicemia were considered as the immediate cause of death and no pox lesions were seen internally. All visible lesions on the remaining seven birds (one male and six females) had resolved by the end of September 2004 Tissues obtained from swabs and biopsy of active lesions, and from necropsy, were submitted for viral culture on the chorioallantoic membrane of specific pathogen free chicken egg embryos and a pox virus isolated and preserved for further study. Blood samples were collected each month from all birds. Moderate elevations were seen in total white blood cell count in some birds but other hematologic parameters were normal. Serum was archived and submitted for commercially available avian pox serology. An agar gel precipitate test using a concentrated pox antigen showed some positive results but they did not correlate with onset of clinical signs in all cases.

No lesions were seen in any of the remaining birds held in the exhibit. The area was placed under quarantine for four months after the removal of the pigeon guillemots in June and all above water surfaces cleaned thoroughly with diluted bleach water and a commercial ozone enriched washer (Del Ozone MPI-300 Multi-Point Intervention Ozone Sanitation System, San Luis Obispo, CA). The portable backholding pool and net were destroyed and all staff adhered to strict isolation and quarantine protocols while husbanding and treating the common murres and pigeon guillemots in the hospital area. Mosquito netting was utilized to prevent possible insect transmission. Follow up fecal and cloacal / choanal swabs were collected twice at a one month interval from the surviving pigeon guillemots after resolution of lesions. These swabs were submitted for viral isolation and were negative. The birds are currently being held in a separate back holding pool area that has been totally enclosed with mosquito netting. They will be observed through the next breeding season for signs of viral recrudescence. The Oregon facility has reported that the seven common murres returned to them had no additional lesions and there had been no signs of pox in any birds at that facility during 2004.²

Discussion

Avian pox is a proliferative epidermal infection caused by several different virus strains belonging to the genus Avipoxvirus. The disease is known to have a highly variable course depending on the strain of pox involved, the route of infection and the species, age and condition of the bird infected.⁴ Pox is transmitted by direct contact or by insect vectors and virus can remain viable in dried epithelial crusts for up to 1 year.¹ Most cases are generally mild and self limiting with few cases of horizontal transmission.^2,3 but severe lesions, complicated by Pseudomonas infections, have been reported as a cause of mortality in common murres in rehabilitation.³ Immunity is believed to be life-long following infection but latent infections have been reactivated experimentally in chickens.¹ The incubation period is highly variable ranging from 10 days to three months or more. Both cutaneous and diphtheritic forms are reported, with the diphtheritic form typically exhibiting the greatest mortality.⁴

To our knowledge, this is the first time that avian pox has been documented in pigeon guillemots. The incubation period during this outbreak was 4 to 8 weeks or more and lesions persisted in the pigeon guillemots for 7 to 10 weeks. It is unclear whether the originally affected common murre was a previously infected bird completing a long incubation period or suffering a recrudescence of the disease as a result of stress or seasonality, or if it might have become infected through invasion of the enclosure by a feather mite from one of several local common murres admitted to adjacent pools in the same quarantine area during a die off in Resurrection Bay in early February. None of the local birds was noted to have visible pox lesions while they were in rehabilitation or during necropsy but feather lice were seen. Raptor pox and pox lesions on terrestrial birds are occasionally seen in this area of Alaska but we could find no reports of pox in any alcid species in Alaska. No cases of pox were observed in any of the other birds housed at the facility in Oregon during 2004.²

The pathogenicity of this pox virus in the pigeon guillemots was much greater than that in the common murres. This may have been due to different host species susceptibility, an increased virulence of the virus, decreased resistance in this group of captive reared pigeon guillemots, onset during the breeding season or the additional stress of the enclosed quarantine housing and close contact between the infected birds. Multiple other avian species were exposed and none showed evidence of infection.

Virus obtained from culture of the lesions in these birds has been preserved and further research is planned with the intent of sequencing sections of the DNA of the virus. Development of diagnostic tools such as ELISA or PCR would be useful for screening for exposure or infection.

Acknowledgements

The authors wish to thank the staff of the Alaska SeaLife Center Avian Husbandry Department, Veterinary Services Department and Rehabilitation Program for the months of care provided to these birds and Dr. A.S. Dhillon and the staff of the Washington State Avian Health and Food Safety Laboratory, Dr, Michael Garner of Northwest Zoo Path, and Debra Tosto of the Charles River Laboratories of SPAFAS Avian Health Products and Services for their advice and assistance in testing of samples.

References

1.  Altman RB, SL Clubb, GM Dorrestein, K Quesenberry, 1997. "Viruses", Avian Medicine and Surgery, W.B. Saunders Company, Philadelphia, PA, pg 300-304.

2.  Brown S. Oregon Coast Aquarium, 2004, pers. com.

3.  Harris JM, AS Williams, FR Dutra, 1978 "Avian Pox in a group of common (California) murres (Uria aalge)", Veterinary Medicine/ Small Animal Clinician, Vol. 73: 7, pg 918-919.

4.  Ritchie BW, 1995 "Poxviridae", Avian Viruses: Function and Control, Wingers Publishing, Inc., Lake Worth, FL, p 285-311.