Exotic-Animal Puzzler: What caused this cockatiel's temporomandibular rigidity?

Four cockatiel fledglings from two clutches owned by the same breeder were reported to have developed temporomandibular rigidity at about 5 weeks of age. The owner said that the birds were unable to open their beaks to eat or drink and that one bird had died. Previous clutches had experienced similar problems. The fledglings had been fed a commercial hand-feeding formula. The fledglings' veterinarian had suspected nutritional myopathy due to selenium deficiency and had recommended oral selenium supplementation, but the selenium therapy had proved unsuccessful. Two birds had developed slight or severe beak deviations and had been taken to another veterinarian for a second opinion. The bird with the severe beak deviation was euthanized and submitted for necropsy.

Necropsy and laboratory findings

A postmortem examination revealed that the bird had a good body condition. The mouth could not be opened, and the upper beak was markedly deviated to the right. A complete gross examination revealed no other lesions. The temporomandibular joint and overlying musculature appeared normal grossly. A histologic examination revealed subacute mucopurulent rhinitis and sinusitis and proliferative temporomandibular osteoarthritis. The nasal cavity and sinuses contained abundant mucus mixed with moderate numbers of heterophils and cellular debris. Patchy areas of the nasal mucosa were covered with a palisade of small gram-negative, cilia-associated bacilli. The inflammation involving the temporomandibular joint was mild and did not extend into the masticatory musculature.

At necropsy, we seared the exterior of the nasal cavity with the flame from an alcohol burner and opened the nasal cavity sufficiently to introduce a sterile swab. We did not open the temporomandibular joint for examination or culture because the damage produced by these procedures would have prevented microscopic evaluation of the affected tissues. We streaked the nasal swab onto a MacConkey agar plate and incubated the plate at about 98.6 F (37 C). Numerous convex, nonpigmented, 0.1- to 1.5-mm diameter colonies were observed after 24 hours of incubation. After 48 hours, the colonies were umbonate, opaque gray, and about 1 to 1.5 mm in diameter. The organism produced an alkaline slant when inoculated and stabbed into a triple sugar iron (TSI) agar. The colonies were catalase-positive, cytochrome oxidase-positive, and urease-positive. By using a VITEK (bioMérieux) card, we identified the organism as Bordetella bronchiseptica, which we presumed caused the rhinitis, sinusitis, and temporomandibular osteoarthritis. (The VITEK card system is a fully automated bacteriology system that performs bacterial identification and susceptibility testing analyses by using a standard inoculum.) The colony characteristics, TSI slant, and colony biochemical profile findings were consistent with this organism.

Discussion

Anecdotal reports indicate that lockjaw syndrome is well-recognized by cockatiel breeders; however, veterinary practitioners are frequently not aware of this syndrome or its potential causes. Bordetella avium was the first reported cause of a syndrome that included nestling mortality, rhinitis, sinusitis, and temporomandibular rigidity in 2- to 4-week-old cockatiels and less commonly in conures, cockatoos, and macaws.1 The organism was cultured from the choanae and cloacae of affected birds. Researchers reproduced the syndrome by intranasally instilling a pure culture of B. avium into a group of unaffected cockatiels. Five years later, Enterococcus species infection secondary to feeding with a sharp-edged, curve-tipped syringe was reported to have caused an outbreak of lockjaw syndrome in 3- to 6-week-old cockatiels.2

Recently, lockjaw syndrome was reported in 3- to 10-week-old cockatiels.3 This report indicated that not only B. avium but numerous other bacteria were isolated from affected juveniles.3 Other organisms isolated included Escherichia coli, Enterococcus species, Aerococcus species, Bacillus species, Klebsiella species, Mycoplasma gallisepticum, and Mycoplasma synoviae. These researchers observed that all reports had been restricted to sinusitis and upper respiratory problems in captive-reared, young cockatiels. Thus, they suggested that cockatiels may be predisposed to bacteria-related lockjaw because of an unusual cranial air sac or nasal sinus conformation through which an upper respiratory infection can easily disseminate to adjacent muscles, nerves, or joints. An alternative hypothesis was that young cockatiels have weaker local immune responses in their nasal passages than other young psittacine species.3

Bordetella avium can cause turkey coryza, a highly contagious upper respiratory tract disease in young turkeys.4 And both B. avium and B. bronchiseptica have been indicated as a cause of pseudomembranous tracheitis and septicemia in ostrich chicks.1 Both Bordetella species produce a dermonecrotic toxin. The toxin produced by B. bronchiseptica can cause atrophic rhinitis in swine.5 So a dermonecrotic toxin produced by B. avium and B. bronchiseptica may play an important role in producing rhinitis, sinusitis, and temporomandibular osteomyelitis. Additionally, damage caused by a dermonecrotic toxin produced during a subclinical Bordetella species infection could predispose cockatiels and other psittacine birds to secondary opportunistic bacterial infections. Secondary invaders could rapidly become the predominant organisms since Bordetella species proliferate at a slower rate than many of the other cited organisms, at least when grown on culture media.

No effective treatment is available for cockatiel chicks or fledglings exhibiting signs of disease. Euthanasia is the most humane solution. A vaccine is not available for use in cockatiels, though vaccines are available for use in turkeys.

REFERENCES

1. Clubb SL, Homer BL, Pisani J, et al. Outbreaks of bordetellosis in psittacines and ostriches, in Proceedings. Annu Conf Assoc Avian Vet 1994;63-68.

2. Greenacre CB, Wilson GH, Ritchie BW. Enterococcus species-associated temporomandibular arthritis in cockatiels. Vet Med 1999;94:907-909.

3. Fitzgerald SD, Hanika C, Reed WM. Lockjaw syndrome in cockatiels associated with sinusitis. Avian Pathol 2001;30:49-53.

4. Skeeles JK, Arp LH. Bordetellosis (turkey coryza). In: Calnek BW et al, eds. Diseases of poultry. 10th ed. Ames: Iowa State University Press, 1977;275-288.

5. Brockmeier SL, Register KB, Magyar T, et al. Role of the dermonecrotic toxin of Bordetella bronchiseptica in the pathogenesis of respiratory disease in swine. Infect Immunol 2002;70

The information for this case was provided by Neil Allison, DVM, DACVP, and Alice Smith, BS, C.E. Kord Animal Disease Laboratory, Ellington Agriculture Center, 440 Hogan Road, Nashville, TN 37220. Dr. Allison’s current address is Experimental Pathology Laboratories Inc., P.O. Box 12766, Research Triangle Park, NC 27709.