American Journal of Primatology 3485-96 (1994) Imports: Current Trends and Usage J.R. HELD' AND T.L. WOLFLE' 'Biotechnologv Group, Microbiological Associates, Inc., Rockuille, Maryland: 'Institute for Laboratory Animal Resources, National Research Council, Washington, D.C. Nonhuman primates are essential to the advancement of some areas of biomedical research and testing. Some populations of these species in the wild may be threatened with extinction because of habitat destruction; therefore, the biomedical community has been monitoring trends in their importation and use, and supporting various conservation activities. During the past 25 years, there has been a marked decrease in importations into the United States, a large proportion of which is the result of a 1975 ban on their importation for the pet trade. During the same period, the need for biomedical purposes has remained fairly constant. Nonetheless, the reductions in imports have been augmented by the biomedical community through reducing losses during quarantine and conditioning, ensuring a more judicious use of these animals, and by increasing the availability of animals from breeding programs both in source countries and the United States. o 1994 Wiky-Liss, Inc. Key words: nonhuman primates, biomedical, import, export, national health programs INTRODUCTION The conservation of primate species studied in biomedical research is of paramount concern, not only for species preservation, but also to ensure that these essential animals are available for future requirements. Many advances in modern medicine have been, and are continuing to be made because of the availability of nonhuman primates. This is one reason that the biomedical community has been a n important source of support for many aspects concerning primate conservation. In this presentation, we shall attempt to give you some personal perspectives based on nearly forty years of involvement with the subject. Both my co-author and I, trained as veterinarians, became involved with primates by accident. My first work with primates occurred in 1955, when I was a young Epidemic Intelligence Officer a t the U S . Communicable Disease Center, or as i t is known today, the Centers for Disease Control and Prevention, or CDC. The year 1955 was the first year in which the polio vaccine was licensed in the United States, and thousands of monkeys were being imported for vaccine production and testing. Over 200,000 nonhuman primates were imported that year. There were high rates of mortality Received for publication August 26, 1993; revision accepted December 26, 1993 Address reprint requests to Dr. J.R. Held, Biotechnology Group, Microbiological Associates, Inc., 9000 Blackwell Road, Rockville, MD 20850. 0 1994 Wiley-Liss, Inc. 86 / Held and Wolfle among some groups of these animals, and I became part of a team that was put to work to find the causes and to attempt to lessen the losses. My specialty became the epidemiology of the zoonoses, and repeatedly this caused me to become involved with primate disease problems. My co-author, Dr. Thomas Wolfle, was a n Air Force veterinary officer who began his career in 1961 working with nonhuman primates a t the Balcones Laboratories in Texas. Through a series of assignments he became involved with behavioral research, and eventually obtained a Ph.D. degree in psychology to further his work in this field. Eventually, our careers coincided while we worked together at the National Institutes of Health, where we both were concerned with primate resources. Both of us continue to be involved in this field. In retrospect, a great deal has changed since 1955. Many populations of nonhuman primates, which we just took for granted would always be there, have become threatened through expanding human populations and habitat destruction. Public awareness regarding these problems has increased, and new laws and conventions have been passed to help protect these species. We have become much more knowledgeable about primates: how to care for and breed them, and how to prevent and treat their diseases. The biomedical community is continually improving its methods for conserving primate resources, and using these species more judiciously. During this period, in various parts of the world, several specialized facilities for the proper care of primates were developed. The multiple use of primates for various projects, where this could be done humanely, has been encouraged. Large-scale breeding programs were also initiated, both in countries from which these species originate, and in those which have no natural nonhuman primate populations, but need primates for biomedical programs. Some of these changes have resulted from a need for a different quality of animal. Cost is one factor that has also changed greatly. According to Wolfle , “The cost of purchasing and maintaining nonhuman primates has become a major factor in their use. In 1964, the National Institutes of Health paid $14 for a 2-3 kg rhesus monkey. Today, the cost of the same domestically bred animal is $1,000-a net increase of 7,043 percent! One hundred thousand monkeys in 1964 cost $1.4 million.” And now we can add that the $1,000 domestically bred animal of 1983 would probably cost you about $2,500 on today’s market. Thus, 100,000 of those animals would cost $250 million, but in reality, today you could not buy 100,000 monkeys, at any price! You cannot buy a wild-caught rhesus monkey. You can buy some wild-caught cynomolgus monkeys, which in many ways have become the substitute for the rhesus, but even those cost the investigator close to $1,000. Many factors besides scarcity have caused the price increases. Longer quarantine and conditioning periods, more stringent transport and import requirements, and greater facility and management costs have all contributed to these increases. An important result has been that the quality of the animals has also increased. It is estimated that 40,000 nonhuman primates are required worldwide for biomedical purposes each year. The U S . Government Interagency Primate Steering Committee (IPSC) prepared a report L19781 showing that 34,000 nonhuman primates are needed for such programs in the United States alone. While accurate data are not available on a worldwide basis, it can be assumed that a t least a n additional 25% of that number is needed by the remaining countries of the world for research and testing. Primates are currently being used for AIDS research that has become so important that research would clearly be impeded if these animals were not available. They are also essential for the testing of new drugs, and are playing a n even greater role in the development of new products for biotechnology. Import Trends and Usage / 87 These animals are needed by government laboratories, the pharmaceutical industry, and academic institutions for research purposes, and for the safety testing of drugs and other agents. The IPSC reported that of the 34,000 nonhuman primates required in the United States, 21,000 are macaques, 4,500 are squirrel monkeys, 2,400 are marmosets and tamarins, 2,100 are African green monkeys, 1,500 are owl monkeys, 1,300 are baboons, and the balance of 1,200 are a mixture of various other species. Although specific information on primate utilization is difficult to obtain, there are many indications that the Committee’s projections were accurate. These requirements are being met through domestic breeding, importation, and through multiple use of the same animal for various procedures. Because of the importance of these animals, data are collected by various agencies regarding their importation and utilization. The Institute for Laboratory Animal Resources (ILAR) has published special articles on this subject in the past [Gray-Schofield & Chandler, 1984; Mack, 1981, 1982, 19831. The purpose of this paper is to examine sources of information on the topic, and to analyze the trends in the utilization of nonhuman primates during the past quarter century. SOURCES OF INFORMATION ILAR Surveys From 1965-1971, the Institute for Laboratory Animal Resources (ILAR), National Academy of Sciences, National Research Council conducted annual surveys on the use of animals in biomedical research, which included information on the number of each species of nonhuman primates used each year during this period. United States Government Various United States governmental agencies systematically collect information on nonhuman primates for various purposes. These include the following: Department of Commerce The U.S. Department of Commerce collects information on the number of nonhuman primates imported each year. Information is collected and is made available on the numbers of animals by the country of origin for each shipment, and the customs value of the shipment. Department of the Interior The U.S. Department of the Interior has been collecting information since 1983 on the numbers of nonhuman primates imported and exported each year. This is done as part of its function as the Government’s Management Authority under the International Convention for Trade in Endangered Species of Flora and Fauna (CITES). Information is collected and reported on the numbers of animals imported and exported by species, country of origin, country to and from which each shipment is made, and whether the shipments are of live animals, biological specimens from live animals, or specimens from dead animals. Department of Agriculture The U.S. Department of Agriculture (USDA), Animal Plant Health Inspection Service (APHIS), a s part of its responsibilities concerning managing the Animal Welfare Act, gathers information on the numbers of nonhuman primates used in experimental procedures that are carried out each year in registered institutions. The information is reported annually as part of a global report. 88 / Held and Wolfle Department of Health and Human Services, Public Health Service Two agencies in the Department of Health and Human Services’ (DHHS) U.S. Public Health Service (USPHS) collect information on nonhuman primates. Centers for Disease Control As part of its responsibilities pertaining to the quarantine of nonhuman primates brought into the United States, the Centers for Disease Control and Prevention (CDC) collects information regarding primate importation and quarantine. Much of the CDC information is considered confidential business information, and generally only special reports are made available. National Institutes of Health The National Institutes of Health (NIH) gathers information from institutions supported through its grants and contracts on the numbers of animals that they are producing through breeding programs in the United States. This is generally done through surveys, and is made available periodically through special reports. As the lead agency for the Government’s Interagency Research Animal Committee (IRAC), NIH also distributes data on primate use through special reports. The diversity of purposes for which these data are collected leads to degrees of TABLE I. Primate Imports or Use, 196k1990, by Source of Data Imports Year 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 Commerce data 62,526 124,440 99,668 85,151 86,535 75,784 69,548 46,581 40,814 33,539 28,559 29,588 23,676 23,024 22,457 16,651 13,148 14,392 13,790 15,756 16,523 19,220 25,262 14,424 Use Interior data ILAR data USDA data 63,294 62,783 70,416 85,283 68,002 54,437 56,547 3 12,342 11,530 14,311 16,422 16,773 18,137 9,521 56,024 57,515 46,388 54,926 55,338 57,271 48,540 61,392 51,641 51,688 47,177 42,620 Import Trends and Usage I 89 o ' l I I I , I I I I , I I l l I I , I I I 1 1 , I 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 YEAR Fig. 1. Nonhuman primate imports in the United States, 1967-1990. \AMERICA 40 - 30- 4 25- . ) V c 0 t 20- 15- 10- I EUROPE YEAR Fig. 2. Nonhuman primate imports i n the United States, 1972-1990; by geographic source incomparability between information gathered from the various agencies. Nonetheless, these are useful data, and if one is aware of the differences, analyses and comparisons can be made on trends in importations, production, and utilization. 90 / Held and Wolfle 130 110 l21 I 67 I m , I 70 69 I 1 71 72 YEAR Fig. 3. Nonhuman primate imports in the United States, 1967-1972 PAST UTILIZATION The numbers of nonhuman primates imported, or used in the United States during the 27-year period 1965-1991, according to data taken from these diverse sources, illustrate a number of interesting points (Table I). The number of procedures for which these species are required has tended to decrease slightly, but the number of animals reported to the USDA from 1980-1991 remains at a level close to 50,000 per year. There has been a much greater drop in imports during the same period. The difference between imports and a continued high level of utilization can be accounted for in many ways. An important consideration is that many of the primates imported before 1975 were used in the pet trade, and not for biomedical programs. Further drops have been compensated for through breeding in the United States, and more instances of multiple use of the same animal. Approximately 3,000 per year are recycled under the auspices of the USPHS-Sponsored Primate Information Center of the University of Washington (Bowden, personal communication). In reviewing the import data from the U S . Department of Commerce for the 24-year period 1967-1990 (Fig. 11, following the peak of 124,000 imports in 1968, there was a steady decline until 1983. From 1983 until 1989, there was a modest increase until 1989, followed by a sharp drop in 1990. There were several important milestones during this period, and these will be discussed in more detail later. In reviewing information from the same data base but with separation according to geographic source (Fig. 21, the largest numbers of animals came from the Americas during the earliest years of this period, and it is likely that most of these animals were going into the pet trade. Most of the animals from Asia and Africa were probably destined for biomedical programs, or zoos and other educational and research institutions. Throughout this period, there has been a continuing trickle of animals from Europe, and this source has increased in recent years. Some of Import Trends and Usage / 91 U W m I 3 Z 30- 73 74 75 76 77 78 YEAR Fig. 4. Nonhuman primate imports in the United States, 1973-1978. 24 22 14- 12 I 79 I 80 I 1 82 81 , 83 I 84 YEAR Fig. 5. Nonhuman primate imports in the United States, 1979-1984 these animals may have been reexportations, but some increases in more recent years can also be attributed to exchanges within the scientific community. Returning to the data for all imports, and examining it in 6-year increments, we can observe several milestones that affected importations. I n 1967, a law was 92 / Held and Wolfle 12 ' I 8s I 86 I I a7 88 1 89 I 90 YEAR Fig. 6. Nonhuman primate imports in the United States, 1985-1990. enacted in Brazil which later resulted in a n embargo on the exportation of primates (Fig. 3). During the next few years, most of our New World primates came from Colombia and Peru. In 1969, the U S . Congress enacted the Endangered Species law prohibiting certain primate species from being imported. During the next 6-year period, from 1973 to 1978 (Fig. 4), many important events contributed to decreased imports. In July of 1973, the Government of India announced that the number of rhesus monkeys permitted to be exported annually would be reduced by 20,000. The effects of this action began to take place in 1974. In October of 1973, the Government of Peru announced that trapping of primates would be prohibited except for research purposes, and then only under very stringent conditions. Within a few months in 1974, the Government of Colombia also stopped issuing primate export permits. These actions resulted in some shortages of rhesus monkeys, and the virtual unavailability of certain New World species or subspecies. In 1975, the CDC put into place regulations prohibiting the importation of primates for sale as pets. During the same year, the U S . Government IPSC was established and charged with coordinating programs to ensure adequate primate supplies to meet national needs for health programs. In 1975, the International Convention on Conservation of Endangered Species of Flora and Fauna was promulgated, and in 1977, the placing of all species of primates on either Appendix I or I1 of the Treaty further restricted international movement of primates. Late in 1977, the Government of India announced that it would stop all primate exports on April 1, 1978. During 1978, the IPSC issued its National Primate Plan which charted a course for various government agencies to contribute to the support of activities which would: foster the conservation of wild populations of nonhuman primates; improve the capture, conditioning, and shipping of these species; promote a more judicious utilization in biomedical programs; and develop captive breeding to meet Import Trends and Usage / 93 -181614[r - 12- g 10- w U 3 2 s 0 Z t 8642- ............................... ...................-................... ...................... ........................ .......... ..... .... %.. ..... I - IMPORTS ............... EXPORTS I Fig. 7. U S . primate importsiexports, 1984-1990 (interior data). All Other (14 . 5 % ) ~ (20.3%) Philippines (14.1 %) - Bolivia (612%) sia (13.6%) Fig. 8. Primate imports in the United States, 1972-1990 (540,503 total) specific needs. During the first 5 years of the next period (Fig. 51, imports continued to decrease. In 1984, at the end of this period, however, a modest increase in imports began to occur. This increase continued well into the first 5 years of the next period (Fig. 6 ) . Part of this increase could be attributed to breeding colonies that had been established in various source countries. It should be noted that exports from the United States also began to increase during this period (Fig. 7). This included animals that came from U.S. breeding colonies, and also others that had been imported into the country for quarantine and conditioning. This trend was abruptly ended in 1990 when filovirus infections were detected in some recent imports, and the CDC placed a n embargo on the importation of certain species of macaques and cercopithecus monkeys for a period of six months. Once the importation of these species 94 / Held and Wolfle All Other (19 . 0 % ) ~ ~ India (35.3%) Fig. 9. Primate imports in the United States, 1972-1976 (266,266 total) Indonesia (20.1%) Philippines (19.7%) Fig. 10. Primate imports in the United States, 1977-1981 (127,304 total) All Other (9.9%) Ethiopia (3.4%) Malavsia (3.5%) 7 % L L Indonesia (27.2%) Fig. 11. Primate imports in the United States, 1982-1986 (73,737 total). was started again, new CDC requirements led to a situation in which decreased numbers were imported. Reviewing the data by country of origin, considering all imports from 1972 through 1990 (Fig. 8), 48% of the primates came from three countries: India, the Philippines, and Indonesia. Most of these were probably macaques, rhesus from India, and cynomolgus from the Philippines and Indonesia. In the overall period, Peru, Bolivia, Malaysia, Colombia, Kenya, and Guyana were also important source countries. During the first 5 years of the period, 1972-1976 (Fig. 91, three countries served as the source for 65% of the primates: India, Peru, and Colombia. India alone was the source for 35%.By the next 5-year period, 1977-1981 (Fig. lo), Import Trends a n d Usage I 95 All Other (10.7O/o) 7 UK (8.6%)- Fig. 12. Primate imports in the United States, 1987-1990 (73,196 total) Peru and Colombia were out of the picture a s major sources, and India’s role was reduced to 11.8% of the total. By the 1982-1986 period (Fig. 111, India was also out of the picture, and four countries accounted for nearly 80% of the imports: the Philippines, Indonesia, Guyana, and Bolivia. During the last 4 years of the period, 1987-1990 (Fig. 12), six countries accounted for 87% of the imports, with some very interesting changes. Indonesia and the Philippines continued to play dominant roles, and between them, provided 57% of the animals. Guyana continued to serve a s a principal source of South American primates. Of particular note is the addition of China, the United Kingdom, and Mauritius to the list; much of this could be attributed to the development of breeding programs. Many of the imports from the U.K. were of Callithrix jacchus, which were purpose bred in that country. Those from China were virtually all captive bred rhesus monkeys. Many of the macaques imported from Indonesia, the Philippines, and Mauritius were also captive bred in that country, a trend which is likely to continue. Information on imports by species is collected by the U.S. Department of the Interior, and is available only since 1983 (Table 11). Of the approximately 100,000 animals imported during this period, 85% were macaques. Cercopithecus aethiops accounted for about 5%, and many of these animals came not from Africa, but from the Caribbean where they were introduced several hundred years previously, and where various commercial breeding operations have been established. Looking to the future, we shall undoubtedly see a continuation of the trend of captive breeding, both in source countries and in user countries. In fact, by the end of the century, this will probably be the norm. We can also expect prices to increase, as captive breeding is more expensive. The quality of the animals will undoubtedly also increase. It is important that we have primates for biomedical purposes, and it is important that these species be conserved. It has already been demonstrated that the biomedical community can work with those responsible individuals and groups concerned with the conservation of important resources to attain goals that are mutually beneficial. This is a collaboration which it will behoove all of us to foster, not only for the good of people, but also for the good of primates. There is cause for concern; however, upon looking back over nearly 40 years to see how much has been accomplished, there is also cause for optimism: it will be interesting to see what develops during the next forty. ACKNOWLEDGMENTS This work was presented at the Symposium on Conservation of Primate Species Studied in Biomedical Research, XIVth Congress of the International Primatological Society, Strasbourg, France, August 20, 1992. 96 / Held and Wolfle TABLE 11. Primate Imports-USA; by Species 1983-1990 Importslive Macaca fascicularis Cercopithecus aethiops Macaca mulatta Callithrir jacchus Cebus apella Aotus trivirgatus Cebus capucinus Saimiri sciureus Macaca nemestrina Papio anubis All others 100,739 79,416 5,414 4,769 2,187 1,558 1,317 907 771 535 465 1,700 REFERENCES Gray-Schofield, L.; Chandler, J.L. Trends in primate imports into the United States. Including a discussion on worldwide trade in primates. ILAR NEWS 27(4):6-11, 1984. IPSC. National Primate Plan, U.S. Department of Health and Human Services, Public Health Service, NIH Publication No. 801520, 1978. Mack, D. Trends in primate imports into the United States. ILAR NEWS 25(4):12-13, 1981. Mack, D. Trends in primate imports into the United States. ILAR NEWS 25(4):10-13, 1982. Mack, D. Trends in primate imports into the United States. ILAR NEWS 26(4):10-15, 1983. Wolfle, T.L. Nonhuman primates in research: Trends in conservation, importation, production and use in the United States. LAB ANIMAL 12(3):19-27, 1983.