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Imports Current trends and usage.

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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 [1983],
“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.
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