Abstract

Various species of primates are susceptible to natural and experimental infection with the Morbillivirus that causes measles.^1,4 A Morbillivirus antigenically similar to the measles virus can cause enteritis in marmosets.^3,5 A commercial canine distemper-measles vaccine has been tested as efficacious in macques.² This report describes two separate episodes of Morbillivirus infection and associated disease occurring in a zoological collection of white faced saki monkeys (Pithecia pithecia) and pygmy marmosets (Callithrix pygmaea), and a possible link to administration of a modified live measles-distemper vaccine.

Four adult female pygmy marmosets were received into quarantine, at which time they were vaccinated for rabies and tetanus, and tested for tuberculosis. All had negative tuberculin responses at 72 hr. None were given measles vaccine during quarantine. Six weeks later, one marmoset was noted to be lethargic, with a swollen face and inflamed oral membranes. Supportive care was administered, but this animal became recumbent and obtunded, and was euthanatized. Canine distemper/measles vaccine and tetanus boosters were administered to the remaining marmosets. Two weeks later a second marmoset became lethargic and developed facial edema and inflamed oral membranes. Supportive care was initiated, but this animal was euthanatized due to disease progression and poor prognosis.

All three saki monkeys were adults. All received tuberculin testing, rabies vaccination and distemper/measles vaccination. Two had previously received rabies vaccinations without adverse effect. None had ever received measles vaccines. All had negative tuberculin responses. All three presented 14 days after vaccination for acute onset of lethargy, inappetence, dehydration, and weakness. In addition, two of the three were noted to be icteric. All three had elevated AST, ALT, bilirubin (direct and indirect) and GGT levels at this time. All received supportive care but two died. Necropsy revealed icterus, mediastinal hemorrhage, reddened tracheal mucosa, dark purple distal lung fields, and slightly enlarged abdominal lymph nodes.

Histologically, necrosis and moderate to severe mixed cell inflammation were seen in the salivary glands, pancreas, intestine, lymph nodes, spleen, uterus, ovary, trachea, lung, oral mucous membranes, skin and brain of the marmosets and saki monkeys. Inflammation was associated with epithelial syncytial cell formation in most tissues. Intracytoplasmic and intranuclear eosinophilic inclusions were frequent in the marmosets but rare in the sakis. Electron microscopy performed on one marmoset revealed that the intranuclear inclusions in the salivary gland consisted of dense conglomerates of electron dense material. Twisting filamentous profiles were seen in the cytoplasm of some cells, and elongate structures budded from the cytoplasmic membrane of some cells.

RNA lysates were made from formalin-fixed, paraffin-embedded tissue by Proteinase K digestion and phenol/chloroform extraction. Reverse transcription reaction was performed with random hexamers and PCR was performed on the cDNA with Morbillivirus consensus primers. Of the five cases, two sakis were positive for human measles, the two marmosets were positive for canine distemper and one saki was indeterminate due to negative result for RNA actin housekeeping gene control. Results of immunohistochemistry for measles were positive for the sakis and positive for canine distemper in the marmosets.

The Morbillivirus outbreak in the saki monkeys appears to be related to the administration of a modified live distemper/measles vaccine, and may represent a vaccine break. Apparently a natural canine distemper virus infection occurred in one marmoset, although the other marmoset’s disease was closely linked to vaccine administration as with the saki monkeys.

Acknowledgments

The authors appreciate the assistance of Jamie Kinion for data retrieval, Christie Buie for literature retrieval, and Roy Brown of Histology Consulting Service for slide preparation. We also appreciate the technical support of Jean Przybocki and Daisy Johnson.

Literature Cited

1.  Choi YK, MA Simon, DY Kim, BI Yoon, SW Kwon, KW Lee, IB Seo, DY Kim. 1999. Fatal measles virus infection in Japanese macaques (Macaca fuscata). Vet. Pathol. 36:594–600.

2.  Christe KL, MB McChesney, A Spinner, AN Rosenthal, PC Allen, CR Valverde, JA Roberts, NW Lerche. 2002. Comparative efficacy of a canine distemper-measles and a standard measles vaccine for immunization of rhesus macaques (Macaca mulatta). Comp. Med. 52: 467–72.

3.  Fraser CE, L Chalifoux, P Sehgal, RD Hunt, NW King. 1978. A paramyxovirus causing fatal gastroenterocolitis in marmoset monkeys. Primates Med. 10:261–70.

4.  Kobune F, H Takahashi, K Terao, T Ohkawa, Y Ami, Y Suzaki, N Nagata, H Sakata, K Yamanouchi, C Kai. 1996. Nonhuman primate models of measles. Lab. Anim. Sci. 46: 315–20.

5.  Levy BM, RR Mirkovic. 1971. An epizootic of measles in a marmoset colony. Lab. Anim. Sci. 21:33–39.