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Current Trends Update: Nonhuman Primate Importation

Beginning in November 1989, a number of cynomolgus monkeys (Macaca fascicularis) imported into the United States were found to have been infected with a previously unrecognized Ebola-like filovirus (1). This report summarizes findings of surveillance and serologic testing of nonhuman primates imported under special permits from June 1990 through September 1991.

On January 19, 1990, CDC published interim guidelines for handling nonhuman primates during transit and quarantine (2). CDC notified all importers by letter on March 15, 1990, that compliance with these transit, isolation, and quarantine standards was mandatory for continued registration as an importer of nonhuman primates and that registered importers would be subject to unannounced inspections of nonhuman primate quarantine facilities. In April 1990, CDC implemented a special-permit procedure for importing cynomolgus (the species involved in the initial outbreak), African green, and rhesus monkeys because filovirus seroreactivity was detected in these species (3). To obtain the permit, applicants were required to submit an importation plan describing the steps that would be taken to minimize the risk for filovirus exposure of persons and animals during the entire importation and quarantine process. Serologic testing for filovirus and CDC review of results were required before release of animals from quarantine.

From June 1990 through September 1991, 19 nonhuman primate quarantine facilities in the United States received 130 shipments of cynomolgus, African green, and rhesus monkeys under the provisions of the 13 special permits issued by CDC. A total of 12,245 primates (10,881 cynomolgus, 882 rhesus, and 482 African green monkeys) were imported from eight countries: Barbados, Canada, China, Indonesia, Mauritius, Myanmar, the Philippines, and Saint Kitts. As of September 9, 106 shipments (9287 animals) had completed the 31-day quarantine period and satisfied the filovirus testing requirements for release.

Surveillance of 106 shipments that have completed quarantine and testing indicated that 167 (1.8%) primates died (79 during the first 7 days of quarantine and 88 during days 8-31). Mortality by shipment ranged from 0 to 14.9%. Clinical diagnoses included cold stress, pneumonia, enteritis, dehydration, tuberculosis, and adverse reactions to anesthetics. No hemorrhagic illness has been reported. Filovirus antigen capture or virus isolation was attempted on tissue from 80 of the 88 animals that died after 8 or more days in quarantine; all were negative.

Paired serum specimens were obtained from the 9287 primates completing quarantine (specimens obtained during days 1-7 and on or after day 31 of quarantine) and were tested by a single laboratory for seroreactivity to filovirus antigens using an indirect fluorescent antibody panel that includes both African and Asian filovirus antigens. Of the 9287 specimens obtained during days 1-7 of quarantine, 121 (1.3%) had antibody titers of greater than or equal to 256, suggesting filovirus infection sometime before importation. Fifteen (0.2%) sets of paired specimens demonstrated a significant antibody response by seroconversion (i.e., a fourfold or greater increase in antibody titer to greater than or equal to 256) during the 31-day quarantine period. The animals that seroconverted were from 12 different shipments originating in Indonesia, Mauritius, Myanmar, and the Philippines. Fourteen of the seroconversions occurred in cynomolgus monkeys; one occurred in a rhesus monkey. A total of 728 primates from the 12 shipments containing primates that seroconverted were quarantined for a second 31-day period, and additional serum specimens were obtained. These specimens were paired with those obtained on or after day 31 of the initial quarantine period. Three (0.4%) seroconversions occurred; the groups they represented (from three of these 12 shipments) were quarantined for a third 31-day period. None of the monkeys quarantined for a third time seroconverted.

Among seropositive animals that survived primary infection, no evidence has been found of persistence of filovirus. Monkeys that maintained positive filovirus antibody titers during the quarantine period appeared to be free of active or persistent filovirus infections upon release from quarantine. In addition, among 32 (16 cynomolgus and 16 African green) monkeys experimentally infected at CDC with African or Asian filoviruses, filovirus has been detected in the tissues or fluids of surviving animals no later than 19 days after infection. Filovirus seroconversion has not been associated with illness or death among imported nonhuman primates since the original reports of primate deaths in 1989 and 1990 in Pennsylvania, Texas, and Virginia (1,2,4).

Of 104 special-permit importations that CDC monitored, 43 (41.3%) did not comply with one or more parts of the approved special-permit importation plan, most commonly those parts designed to prevent human exposure to the primates during transit. CDC is continuing to work with importers to improve the level of compliance.

During 1989, the year before identification of filovirus in imported nonhuman primates, approximately 15,900 cynomolgus monkeys were imported; based on mortality at that time (10%-15%), approximately 14,300 animals survived the quarantine period. Of these, an estimated 15%, or 2200 animals, were re-exported. Since January 1991, importations of cynomolgus monkeys have averaged 1000 per month. Based on this rate, an estimated 12,000 of these monkeys will be imported during 1991. Assuming a 1.8% mortality during quarantine, approximately 11,800 animals will survive the quarantine period. Reported by: Div of Quarantine, National Center for Prevention Svcs; Div of Viral and Rickettsial Diseases, Scientific Resources Program, National Center for Infectious Diseases; Office of the Director, National Institute for Occupational Safety and Health, CDC.

Editorial Note

Editorial Note: Since the implementation of a special-permit procedure for importing cynomolgus (the primate species most frequently used in scientific research in the United States), African green, and rhesus monkeys, mortality during quarantine has declined substantially from that reported by industry estimates in December 1989 (i.e., 10%-15%). Because of the increased survival of imported monkeys, the health of animals completing the 31-day quarantine, filovirus test results, and surveillance of nonhuman primate importations, CDC is modifying the special-permit requirements (see box). Compliance with the January 19, 1990, interim guidelines, which supplement existing regulations (42 CFR 71.53), continues to be mandatory for the importation of all nonhuman primate species. New regulations on importation and quarantine of nonhuman primates are being developed and will be published in the Federal Register to allow public comment. CDC will continue to monitor nonhuman primate importations and perform unannounced on-site inspections of registered importers' facilities.

References

  1. CDC. Ebola virus infection in imported primates--Virginia, 1989. MMWR 1989;38:831-2,837-8.

  2. 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.

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

  4. Jahrling PB, Geisbert TW, Dalgard DW, et al. Preliminary report: isolation of Ebola virus from monkeys imported into the USA. Lancet 1990;335:502-5.

Modified Special-Permit Requirements for Importation and Quarantine of Nonhuman Primates

  1. Transit, isolation, and quarantine requirements will remain in effect (2).

  2. Routine testing for filovirus antibody will no longer be required. Instead, serum samples drawn during the first week following arrival of the animals at the holding facility should be stored frozen. If the 31-day quarantine period is completed without incident (i.e., death or illnesses), the serum samples may be discarded.

  3. If a death occurs following the first week of the initial quarantine period, tissue must be tested for filovirus antigen; if positive, the protocol for filovirus testing and release of the entire shipment described in the importer's approved special-permit application must be followed.

  4. If any illness occurs during the initial quarantine period, the entire shipment must be held in quarantine until a second blood sample is drawn from all animals (upon completion of the 31-day quarantine period) and the paired serum specimens from the ill animals tested for filovirus antibodies. If any of the animals tested demonstrate a significant filovirus antibody response (i.e., fourfold or greater titer increase to greater than or equal to 256), the protocol for filovirus testing and release of the entire shipment described in the importer's approved special-permit application must be followed.

  5. Existing regulations (42 CFR 71.53) require that any animal suspected of having yellow fever, monkeypox, or hemorrhagic fever during the 31-day quarantine period must be reported to CDC within 24 hours; telephone (404) 639-1437 or voice mail (404) 330-2705. In addition, if mortality for a shipment exceeds 5%, the importer must immediately report the circumstances, including cause of death, to CDC.



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