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Tuberculosis in Imported Nonhuman Primates -- United States, June 1990-May 1993

Nonhuman primates (NHPs) shipped to the United States must be quarantined and monitored for evidence of infectious diseases transmissible to humans. During May-October 1992, CDC investigated reports from NHP importers of mycobacterial infections in NHPs recently imported from Mauritius. This report describes a review of tuberculosis (TB) in all 249 imported shipments of CDC-permitted NHP species in the United States from June 1990 through May 1993 and updates recommendations regarding the identification and control of TB in imported NHPs and in workers exposed to such animals.

To determine mycobacterial infection rates in recently imported NHPs, in May 1993 CDC reviewed health records of all 249 shipments of imported cynomolgus (Macaca fascicularis), African green (Cercopithicus aethiops), and rhesus (Macaca mulatta) monkeys. These NHPs had completed a minimum 31-day import quarantine during June 1990-May 1993 under special permits issued by CDC (1,2). The review included 22,913 NHPs (20,580 cynomolgus, 1621 rhesus, and 712 African green monkeys) from nine countries (Barbados, Canada, China, Indonesia, Mauritius, Myanmar {Burma}, the Philippines, Saint Kitts, and Tanzania).

Information was obtained from health records maintained for animals at all 18 NHP quarantine facilities that held special permits during this period and from records at five other facilities that received previously quarantined NHPs. All animals had received routine tuberculin skin tests (TSTs) (three tests, with 2-week intervals between tests) by experienced personnel in well-established quarantine facilities using accepted methods and a U.S. Department of Agriculture-licensed skin-test antigen. A diagnosis of TB infection was based on TST reactions and/or histopathologic examination or culture of granulomatous lesions found at necropsy.

Of the 20,580 cynomolgus monkeys, 8910 (43%) originated in the Philippines, 7703 (37%) in Indonesia, and 3967 (19%) in Mauritius. Of the 1621 rhesus monkeys, 1515 (93%) originated in China, 68 (4%) in Myanmar, and 38 (2%) in Canada. Of the 712 African green monkeys, 394 (55%) originated in Saint Kitts, 198 (28%) in Barbados, and 120 (17%) in Tanzania.

Overall, evidence of TB infection was identified in 90 (81 cynomolgus and nine rhesus monkeys) (0.4%) of the 22,913 NHPs, representing 17 (7%) of the 249 shipments. Sixteen of the shipments contained cynomolgus monkeys. Within these shipments, the prevalence of infection ranged from 0.8% (one of 130 cynomolgus monkeys shipped) to 80% (48 of 60 cynomolgus monkeys), with a median rate of 3%.

The prevalence of TB infection in cynomolgus monkeys varied by country of origin and included 2% (76 of 3967) of animals from Mauritius, 0.04% (three of 7703) from Indonesia, and 0.02% (two of 8910) from the Philippines. In addition, of the 81 total infected cynomolgus monkeys, 76 (94%) originated in Mauritius.

TB-infected NHPs were identified from 11 (69%) of the 16 total cynomolgus monkey shipments from Mauritius. Eight of these 11 shipments arrived from August 1991 through February 1992; the most highly infected shipment arrived during November 1991. TB surveillance and eradication efforts were increased by the exporters in Mauritius after U.S. importers notified them of the identification of TB-infected animals in May 1992. Of the seven shipments received since February 1992, two shipments have contained one TST-positive animal each. No evidence of additional secondary transmission has been reported by importers or by facilities receiving animals after quarantine.

Evidence of TB was detected during the initial 31-day quarantine period in 11 (65%) of the 17 shipments. However, most (69 {77%} of 90) infected animals were in the six shipments in which infection was first identified only after the completion of the routine 31-day postimport quarantine period, including one infected animal identified more than 15 months after release from quarantine. When 16 apparently healthy, TST-negative cynomolgus monkeys were euthanized to control the spread of infection at one facility, nine (56%) were found at necropsy to have granulomatous lesions suggestive of TB. Infection was confirmed by the presence of acid-fast bacilli (histopathologic sections) and/or positive mycobacteriologic culture.

During the review process, one NHP facility worker was reported to have developed a positive TST after exposure to infected animals but did not develop active TB. In addition, facility managers reported that TST conversion occasionally occurs among long-time NHP workers.

Reported by: Div of Quarantine, National Center for Prevention Svcs; Scientific Resources Program, National Center for Infectious Diseases, CDC.

Editorial Note

Editorial Note: Regulation of the importation and quarantine of NHPs was instituted in 1948 to prevent the introduction and transmission of human pathogens. Beginning in 1975, importers of NHPs for permitted scientific, educational, or exhibition purposes were required to register with CDC, and a system was established for monitoring and reporting disease in quarantine facilities. * Following the identification of filovirus infection among cynomolgus monkeys imported from the Philippines during 1989- 1990, CDC intensified disease-control measures for the handling of NHPs during importation and quarantine, including 1) unannounced inspection of registered importer quarantine facilities; 2) special permit requirements for the handling of imported cynomolgus, African green, and rhesus monkeys during transit and quarantine; 3) monitoring of arriving shipments of NHPs at U.S. ports of entry; and 4) surveillance of postimportation quarantine and distribution procedures (1,3).

CDC regulations require that newly imported NHPs undergo a 31-day quarantine period in the United States. Many registered importers and recipients of imported NHPs extend quarantine beyond the 31-day minimum. Because TB in captive NHPs is both an animal and a human health problem, surveillance by TST of imported NHPs and workers at NHP facilities is routine (4,5). Any NHP with a positive TST during import quarantine is considered to be infectious and to represent a high risk for disease transmission. When a quarantined TST-positive NHP is identified, the standard practice is to euthanize the animal, attempt laboratory confirmation of TB, and reinstitute quarantine and tuberculin skin testing (at 2-week intervals) of all other exposed NHPs until three consecutive negative TSTs have been completed (5).

The findings in this report indicate that the risk for TB infection in cynomolgus monkeys recently imported from Mauritius was substantially higher than that among those imported from Indonesia or the Philippines. However, all macaques are considered to be highly susceptible to TB, and virtually all are imported from areas of the world with high prevalences of TB in humans and animals. Close confinement of these and other NHPs in holding facilities and shipping crates creates conditions whereby one infected animal could potentially infect many others. Cynomolgus monkeys from Mauritius may have been held longer in identifiable groups than animals from other geographic areas; they are especially desirable for breeding colonies in the United States because they are free of herpes B, a pathogen fatal to humans and for which macaques are the natural hosts. The longer quarantine may have increased both the likelihood of transmission and detection of TB.

In the investigation described in this report, nine TST-negative animals had evidence of TB. The TST is less reliable for NHPs than for humans because of timing of the TST relative to individual exposure, lack of uniformity in testing procedures, and differences in host responses to the skin-test antigen. Ancillary TB diagnostic procedures commonly used in humans (e.g., booster or second-strength TST, chest radiographs, and sputum smears) are not standard elements of the NHP quarantine protocols.

The potential for transmission of TB and other pathogens among NHPs and humans underscores the importance of improved surveillance and testing procedures in NHP quarantine and research facility settings. The American Association for Accreditation of Laboratory Animal Care requires that its accredited facilities routinely perform TSTs in NHPs; however, test results are not routinely reported to any federal agency. CDC's NHP permit system is the only national disease-reporting system for imported NHPs, and TB reporting has not been required under this system. Daily contact with groups of potentially infected animals in the quarantine facility work environments may present an increased risk for exposure for humans. Although workers whose skin tests convert are referred to their health-care providers for medical evaluation, reporting of these cases with information on occupational exposure is not required by any federal public health agency, and therefore, background incidence and prevalence data for workers in this industry are not available.

The findings in this report indicate the need for improved estimates of the risks for TB in both NHPs and human contacts. The Division of Quarantine in CDC's National Center for Prevention Services is working with the Association of Primate Veterinarians, the American Association of Zoo Veterinarians, other federal agencies, and industry groups to address these issues. In addition, CDC has developed interim recommendations that update and modify procedures used to identify and control TB in imported NHPs and in workers exposed to such animals (see box). Interim Guidelines for Tuberculin Skin Testing of Nonhuman Primates During Quarantine

  1. All imported nonhuman primates (NHPs) should be administered a minimum of three tuberculin skin tests (TSTs), with at least 2 weeks between tests (5), before release from import quarantine. All cohorts containing animals with positive or suspicious reactions should remain in quarantine and be administered at least five additional TSTs following removal of the last affected animal.

  2. Records of all TSTs performed during the lifetime of each imported NHP should be maintained at the facility housing the NHP and should accompany the NHP during moves to other facilities.

  3. Necropsies of imported NHPs should be performed only by qualified veterinary pathologists or laboratory-animal veterinarians accredited by the American Association for Accreditation of Laboratory Animal Care. Necropsies of tuberculosis (TB)-suspect animals (NHPs with positive or suspicious TST results or NHPs from cohorts within which TB-infected animals have been identified previously) should be performed under animal biosafety level 3 conditions (6). Regardless of gross necropsy findings, fresh and formalin-fixed tissue specimens -- to include tracheobronchial lymph node, liver, lung, and spleen -- from all such NHPs should be collected for laboratory examination. Granulomatous lesions found in any NHP at necropsy, regardless of whether TB was previously suspected, should be submitted both for laboratory examination for acid-fast bacilli and for mycobacterial culture. Necropsy reports should address all major organ systems and should incorporate clinical history and laboratory findings.

  4. All NHPs with positive or suspicious TST results, necropsy findings, or laboratory results should be reported to CDC (telephone {404} 639-8108; fax {404} 639-2599) within 48 hours, along with a copy or summary of the individual NHP's health records.

  5. All facilities that house NHPs should adhere to the Institute for Laboratory Animal Research recommendations regarding baseline and (at a minimum) annual TST screening of employees and routine safe work practices involving NHPs (5). Results of employee TSTs should be maintained and reviewed by the occupational health professional responsible for the employee health program. Skin-test conversions among employees may suggest transmission of TB in the facility. Workers exposed to NHPs with laboratory-confirmed TB should receive a postexposure TST and, if negative, a TST 3 months after exposure. Workers with a reactive skin test should be referred for medical evaluation.

  6. All persons directly involved in the transportation and quarantine of imported NHPs should adhere to the importer's standard operating procedures approved by CDC under the special permit process.

  7. In addition to the protective clothing requirements described in previously published guidelines (3), inspection personnel and other transit workers who handle crates or pallets containing imported NHPs should wear disposable dust/mist respirator masks and be trained in their proper use. Because of the potential for aerosol transmission of certain pathogenic bacteria (e.g., TB) and viruses, face shields or eye protection should be worn by workers whose faces may come within 5 feet of the NHPs.

  8. All NHPs should be individually identified with a unique number or alphanumeric code permanently applied to the animal by tattoo. Health certificates, shipping documents, and animal health records should always include this number or code and the age, sex, and species of the NHP (5).


  1. CDC. Requirement for a special permit to import cynomolgus, African green, or rhesus monkeys into the United States. Federal Register 1990;77:15210.

  2. CDC. Update: nonhuman primate importation. MMWR 1991;40:684- 5,691.

  3. CDC. Update: ebola-related filovirus infection in nonhuman primates and interim guidelines for handling nonhuman primates during transit and quarantine. MMWR 1990;39:22-4,29-30.

  4. Committee on Care and Use of Laboratory Animals, Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council. Guide for the care and use of laboratory animals. Bethesda, Maryland: US Department of Health and Human Services, Public Health Service, National Institutes of Health, 1985; DHHS publication no. (NIH)86-23.

  5. Institute of Laboratory Animal Research. Laboratory animal management: nonhuman primates. Washington, DC: National Academy Press, 1980:27-30.

  6. CDC/National Institutes of Health. Biosafety in microbiological and biomedical laboratories. 2nd ed. Atlanta: US Department of Health and Human Services, Public Health Service, CDC/ National Institutes of Health, 1988; DHHS publication no. (NIH)88-8395.

    • 42 CFR section 71.181-189 (40 FR 33661).

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