Background and Context for Occupational Health and Safety in the Care and Use of Nonhuman Primates
According to annual reports published by the US Department of Agriculture, the number of nonhuman primates used or intended for use in research has remained generally stable for the last decade at about 52,000 animals per year. Over 87% of the states, districts, and territories in the United States use primates in research. Primates are used in diverse projects, including research in infectious diseases, cancer, neuroscience, heart disease, nutrition, and reproduction; drug development and safety assessment; and behavioral studies (Sibal and Samson 2001). The steady and widespread use of nonhuman primates strongly suggests that they will continue to be important animal models for a number of human diseases.
Many research projects require physical proximity between people and nonhuman primates or their tissues, and institutions have an ethical responsibility to provide for the health and safety of people exposed to the hazards resulting from that proximity. This responsibility is particularly important at institutions that use primate species that pose known and significant infectious hazards, such as the macaques and chimpanzees. Although economics will have a role in any animal care and use program, cost alone must not dictate the scope or relevance of the OHSP implemented at an institution.
A successful OHSP has seven basic elements: knowing the hazards, avoiding and preventing exposures to the hazards, providing effective
training and reinforcement, promulgating and enforcing sound rules and guidelines, ensuring consistency and reliability in occupational behavior, maintaining proper records (a database) and providing comprehensive medical surveillance and feedback, and developing key leadership and staffing based on a commitment to a safe workplace (NRC 1997).
The importance of an OHSP in any laboratory animal care and use program is highlighted in the Guide for the Care and Use of Laboratory Animals (NRC 1996). The Guide identifies the essential elements of an OHSP, although more specifically in the context of animal care and use: hazard identification and risk assessment; personnel training; use of personal protective equipment; facilities, procedures, and monitoring; medical evaluation and preventive medicine; and addressing animal experimentation that involves hazards.
One of the most commonly identified deficiencies in animal care and use programs evaluated by the Association for Assessment and Accreditation of Laboratory Animal Care International (AAALAC International) is in the OHSP (DeLong and others 2001). Overarching concerns identified by AAALAC International were a failure to base the OHSP on hazard identification and risk assessment and a failure to include in the program the general hazards of working with animals (as opposed to experimental hazards themselves, which are usually taken into account); inadequate training on such OHS topics as zoonoses and allergies; inadequate inclusion in the OHSP of all personnel potentially at risk, such as students, the nonaffiliated member of the IACUC, and visiting scientists; and inadequate linkage between the IACUC and institutional safety personnel. AAALAC International’s expectations for a sound OHSP are that the individual components of the program are appropriate for the institution and that the components work together effectively. Thus, there must be sound implementation strategies and effective coordination of program components and personnel.
INTENT OF THIS REPORT
The National Research Council report Occupational Health and Safety in the Care and Use of Laboratory Animals (1997) provides an excellent overview of OHS issues. However, in light of AAALAC International’s findings and the potentially serious risk that working with nonhuman primates can pose to workers, the present report is intended to serve as a tool for developing and improving OHSPs that must address the particular hazards posed by nonhuman primates. The intent of this report is to provide specific information to safeguard the health of people working with nonhuman primates; however, an additional benefit is the protection of animal health. This report will serve as a resource for health care
providers, institutional officials who are responsible for the OHSP, and the various personnel working with nonhuman primates or their tissues. References provided throughout the report will assist people who seek more detailed information on particular aspects of an OHSP.
The information presented here is intended to guide the implementation of an OHSP that must address the use of nonhuman primates and that is appropriate for the size and function of the institution. Any analysis of the risks posed by nonhuman primates to people must take into account the specific animal use (for example, how direct is the contact with animals or animal tissues), the nature of nonhuman primates being used (including species, age, sex, and previous experience of the animals), the qualifications of the people working with the animals or animal tissues, as well as support staff who might come into contact with the animals (e.g., maintenance or housekeeping personnel) or animal-associated equipment (e.g., cage-wash staff). Practices, procedures, and attitudes in place at an institution are essential components of an OHSP. Because the hazards associated with the use of nonhuman primates will be specific for each institution, no single approach to addressing the risks can be offered in this report. Instead, general guidance is provided on the types of hazards encountered in different settings with various primates and on how to avoid those hazards and manage exposures.
IMPLEMENTING THE OCCUPATIONAL HEALTH AND SAFETY PROGRAM
Responsibility, Authority, and Accountability
A successful OHSP begins with strong administrative support. The senior official at the institution must understand the health and safety issues related to working with nonhuman primates, support the development and implementation of policies to safeguard workers, communicate the importance of OHSP participation to them, ensure that suitable funding and other resources are available to implement and maintain the program, designate appropriate staff to serve on the design and implementation team, and identify the individual or office that will manage the OHSP.
The design and implementation team should comprise persons who have expertise in providing occupational health care and who might be exposed to hazards in the workplace, depending on their role in the institution. The team should include representatives of animal care and use staff, research staff, environmental health and safety staff, occupational health and medical staff; administration and management (NRC 1997) assisting with the design and implementation of the OHSP should be qualified to do so through training or experience with relevant hazards.
A successful OHSP relies on the identification of health and safety concerns at all levels of the institution. Animal care and use staff typically have the most frequent and direct contact with nonhuman primates and therefore typically have a practical approach to identifying and reducing potential hazards. The IACUC, through its animal study proposal review process and semiannual facility inspections, has the opportunity to investigate possible risks associated with a proposal, to seek ways to reduce the risk, and to assess the animal facility and animal procedure areas for potential hazards that should be avoided or minimized.
The Environmental Health and Safety (EHS) staff, whether they are employees of the institution or contract staff, may be involved in radiation and chemical safety, waste management, and monitoring of the OHSP. EHS personnel often provide input into the development of work practices and should maintain a liaison with the IACUC for review of animal-study proposals involving hazardous agents. In institutions where nonhuman primates are used, the EHS staff should have appropriate knowledge of all associated infectious, chemical, and physical hazards and ergonomic concerns, along with the importance of protection of the animals from human disease. Persons assigned these responsibilities can be invaluable in the implementation of a program modification. Information gathering is particularly important when research programs include novel infectious agents or viral vectors on which little reference information is available. The senior official, through reports provided by the research directors and staff, the IACUC, the EHS and OHS directors and staff, and the NHP director and animal care staff provides the highest level of oversight by ensuring that problems identified by others in the institution are resolved (Figure 2-1).
The OHSP is also reviewed by external oversight organizations, such as OSHA and corresponding state agencies, the National Institutes of Health Office of Laboratory Animal Welfare (for institutions receiving Public Health Service [PHS] funding), and AAALAC International (for institutions seeking or renewing accreditation). Those organizations can take different actions when an institution is not in compliance with their standards, such as imposition of fines, withdrawal of grant funds, and revocation of accreditation, respectively.
Hazard Identification and Risk Assessment
Risk assessment is the basis for designing and managing occupational health and safety programs to reduce workplace risks to an acceptable level. Risk assessment measures the likelihood of adverse health effects resulting from occupational injuries or exposures and is discussed further
in Chapter 5. An important aspect of risk assessment is hazard identification. A hazard is a source of risk, such as a substance or action that can cause harm. Hazards can be inherent to working in an animal facility or result from a specific research project. Everyone in the facility should be considered responsible for identifying hazards as part of his/her duties to ensure a culture of safety in the institution. Hazards can be categorized as biologic, chemical, or physical, and they can be introduced by dermal or mucous membrane contact or through respiratory, oral, or auditory routes. Occupational hazards associated with nonhuman-primate facilities are principally those related to physical injury and infectious disease (viral, bacterial, and parasitic). The process of identifying hazards should be continuous as new equipment or materials, new species, and new research are introduced into the institution. Experience in and qualifications for working with one species of primate cannot necessarily be translated to a different species, even if the species belong to the same genus. Therefore, hazard identification must include knowledge of the biology and behavior of the primate species in question. Table 2-1 shows some of the key factors involved in identifying hazards and then conducting a risk assessment. Risk assessment should be used to manage identified hazards, avoid or minimize potential exposures, and guide treatment if an exposure occurs.
TABLE 2-1 Factors Involved in Risk Assessment
• Experimental conditions
• History of health concerns in facility/program
• Employment outside primary workplace
• Hobbies, circumstances at home that may predispose for risk at primary workplace (e.g., sports, pets)
• Duration of study
• Frequency of exposure
• Protection afforded through regulatory (e.g., CDC) requirements
• Of animal
• Potential for zoonotic disease
• Potential for injury
• Of experimental agent
• Specific agent properties
• Intensity of exposure
Protection Afforded Through:
• Facility engineering
• Required personal protective equipment
• Required biosafety equipment
• Health status of worker
• Experience of worker
SOURCE: Adapted from AAALAC International, see www.aaalac.org.
HAZARDS ASSOCIATED WITH NONHUMAN-PRIMATE BEHAVIOR
Personnel working with nonhuman primates should receive basic training in nonhuman-primate behavior. Understanding the behavior of primates assists personnel in predicting the animals’ actions and identifying potential hazards. Such an understanding includes a basic knowledge of the animals’ anatomy and perceptual capabilities; this information indicates the physical capabilities of the animals (leaping or spitting long distances, running rapidly, exercising manual dexterity, and so forth) and what it perceives in its environment (such as depth, color, and smells). Knowledge of the animals’ cognitive abilities aids colony managers, scientists, and veterinarians in selecting housing or testing equipment that is appropriate and enhances personnel safety and in determining what kind of training program can be used with the animals. Knowledge of animal
behavior is an important factor in the safe handling of large animals (Grandin 1999) such as nonhuman primates. This background information can be overlaid with detailed knowledge regarding individual animals, such as an animal’s previous use (and familiarity with people and procedures) and level of aggressiveness or other behavior, which can be relevant to personnel safety.
Standard operating procedures (SOPs) or institutional policies are critical to safeguarding people at risk. Such documents may restrict entry to the animal facility, require that visitors be older than some minimal age (e.g., 18 years), or require particular health checks of visitors (for example, tuberculosis testing and measles vaccination) to protect both the animals and the people. SOPs may specify a variety of procedures for husbandry or research that maximize animal well-being and minimize potential risk to the individual. SOPs and institutional policies should be customized to the facility and kept current by periodic review (for example, by the IACUC).
Occupational hazards associated with nonhuman primates can occur in zoologic parks, in research and testing environments, and in teaching or breeding programs. Thus, several categories of people, perhaps with different training in primate work, are potentially at risk. People at risk include employees; students, visiting scientists, and other trainees; contract workers; and visitors or guests to the facility. The categories of people at risk vary not only in expertise, but also in physical proximity to the animals, the type of use of the animals (for example, the animal might be conscious or unconscious), and the species and number of animals being handled (i.e., the risk posed by working with some species can increase with the number of animals).
Training programs should be made available to individuals at risk to provide information on potential hazards and avoidance of risks. Depending on the primate species and the target audience, the training program should address zoonotic diseases of primates, ergonomic hazards, methods of reporting injuries, first aid, follow-up health care, and principles of primate behavior. One-on-one training by supervisors is critical to tailor the information conveyed so that it is specific to the task and species to which the trainee will be exposed. A combination of didactic and hands-on training may optimize personnel safety.
The order Primata is diverse, comprising, in addition to humans, more than 200 species of prosimians, New World monkeys, Old World monkeys, and apes. That diversity is reflected in the wide variety of habitats occupied by nonhuman primates and by their anatomic, physiologic, and behavioral differences. Of the numerous nonhuman species, relatively few are used in research, although a larger number are maintained in zoological parks. Some of the behavioral considerations in handling those
species most prevalent in research are discussed below. A detailed discussion of this topic is included in The Psychological Well-Being of Nonhuman Primates (NRC 1998).
The prosimians or lower primates (suborder Strepsirhini) include tarsiers, lemurs, sifakas, indris, aye-ayes, lorises, pottos, and galagos (Nowak 1999). Lemurs and lorises are often seen in zoos. The prosimians are a diverse group, whose members range from 12 cm and less than 100 g (the mouse lemur) to 90 cm and 10 kg (the indri). Prosimians are considered the primates most removed taxonomically from humans, and there has been no published report of disease transmission from prosimians to humans (NRC 1998). In general, prosimians are not aggressive, although some species actively resist restraint by kicking and biting. The bite of a slow loris may be of particular concern because of its poisonous mix of saliva and glandular secretions (Alterman, 1995). Some prosimians are inquisitive and may leap onto people to investigate them more closely. Personnel entering these animals’ quarters should be prepared for such behavior.
New World Monkeys
The New World monkeys are found in Central America and South America. They include marmosets and tamarins, which are collectively known as callitrichids (Callitrichidae), as well as squirrel monkeys, owl monkeys, titi monkeys, capuchin monkeys, spider monkeys, howler monkeys, woolly monkeys, sakis, and uacaris, which are collectively known as cebids (Cebidae). The common marmoset (Callithrix jacchus) is used in biomedical research and in zoological exhibits; other callitrichids are typically only maintained in zoos.
The callitrichids are distinct from the cebids by having claws on most digits. They are also principally arboreal, descending to the ground only occasionally. Callitrichids are highly territorial, and their territoriality can occasionally be directed at personnel coming close to their housing enclosure. Marmosets and tamarins have well-developed visual, olfactory, and auditory perception and long memories, so they are able to recognize individual humans and can develop strong likes and dislikes of them (NRC 1998). Threatening behavior may be detected in some species of callitrichids in an arching of the back and concomitant stiff-legged walk, presentation of the testes, or a chest display (achieved by standing bipedally and turning the elbow out) (Hershkovitz 1975). Occasionally, the bipedal stance will be accompanied by swaying from side to side. In
addition, the entire pelage may be piloerected in a threat display. Hand-raised animals can become very aggressive toward people when they reach puberty. Their territorial and occasionally aggressive behavior, in combination with sharp claws and procumbent incisors (marmosets) or long canine teeth (tamarins), poses a risk of bite wounds to personnel.
Of the cebids, squirrel monkeys and less often capuchins, spider monkeys, and owl monkeys are used in research. These and the other cebids can also be found in zoological exhibits. In general, New World monkeys are not aggressive toward humans and do not respond aggressively to direct eye contact, as Old World monkeys do (NRC 1998). Like prosimians, however, they resist restraint vigorously. Capuchins have excellent manual dexterity and manipulative abilities; these characteristics have resulted in their occasionally unlocking their enclosures and getting free in an animal holding room. Staff should exercise care in capturing these animals because they might bite in self-defense or when frightened. Similarly, a cebid attempting to climb on a person might bite the person if pushed away or frightened (NRC 1998). Occasionally, a cebid will defend a person it likes from other people.
Old World Monkeys
The Old World monkeys are native to Africa and Asia, although introduced populations exist throughout the world. The family of cercopithecids (Cercopithicidae) comprises two subfamilies, the cercopithecines (Cercopithecinae) and the colobines (Colobinae). The macaques, baboons, drills/mandrills, geladas, mangabeys, guenons, talapoins, African green monkeys (a.k.a. grivets or vervets), patas monkeys (military monkeys, hussar monkeys, and mustached monkeys), and Allen’s swamp monkeys are cercopithecines. The colobines include colobus monkeys, langurs, Chinese golden monkeys, and proboscis monkeys. Of the cercopithecids, the rhesus monkey and cynomolgus monkey are the most commonly used in research; baboons, African green monkeys, and a few other species of macaques are also used. Most of the cercopithecids and colobines can be found in zoological parks.
Many species of Old World monkeys have well-developed cognitive abilities, although most studies of cognition have been done in macaques. The cercopithecines are also strong for their body size and are skilled at manipulating objects. Studies have demonstrated macaques’ puzzle-solving ability, even in the absence of a food reward (Washburn and Rumbaugh 1992). The combination of cognition, strength, and propensity to manipulate objects can result in animals’ escaping from their enclosures, thereby posing a risk to personnel. Macaques have well-developed visual capabilities (Bayne and Davis 1983; DeValois and Jacobs 1971; Leary
and others 1985), and visual signals (such as coloration, facial expressions, and body posture) are important in conspecific communication. A lack of knowledge or understanding of the visual signals on the part of people working with macaques can lead to the inadvertent communication of mild threats, such as through direct eye contact and jerky arm movements, and the primates might respond to these perceived threats aggressively. Because the cercopithecines are generally social animals, any action by humans that is perceived as threatening to an infant (such as removing the infant from a group) can also elicit aggression. Basic training of key personnel in primate behavior can decrease the primates’ aggressive actions in response to human behavior. Risk can be reduced in some instances by training the animals (for example, macaques) to cooperate in specific activities, such as cage transfer, venipuncture, and vaginal swab sampling. This can minimize the handling of conscious animals and reduce the need for chemical immobilization.
The superfamily of apes or hominoides (Hominoidea) consists of the hylobatids (Hylobatidae), or lesser apes, and the hominids (Hominidae), which includes great apes and humans. Some taxonomists place the orangutan in its own family (Pongidae). Gibbons and siamangs make up the lesser apes. The great apes comprise chimpanzees, bonobos, gorillas, and orangutans. Both lesser and great apes are frequently maintained in zoological parks; the chimpanzee is the most common ape used in research.
The lesser apes exhibit specialized locomotion known as brachiation (arm-swinging) aided by their long arms and elongated hands and fingers. Those features also result in a long reaching grasp through enclosure barriers to grab at unwary people who are too close. Gibbons are capable of rapid movement, and they may bite (NRC 1998).
The great apes are extremely strong, including in their hands. Chimpanzees and gorillas will use objects in their environment in their charge displays, occasionally throwing the objects at specific targets. Chimpanzees and orangutans will also spit saliva or water and throw feces at nearby persons with great accuracy. A response to this behavior from a person encourages it to the point of becoming routine in the animal’s behavioral profile. Young chimpanzees can pinch and bruise people with their rough play. Great apes have a highly developed cognitive level, with excellent skills in complex learning and tool-using. Some species are even capable of recognizing themselves in mirrors and in televised images (Gallup 1977, 1982; Lambeth and Bloomsmith 1992; Menzel and Lawson 1985). Great apes do not often trust unfamiliar persons and can
even be devious in their relationships with people (NRC 1998), which can place those individuals at additional risk. Chimpanzees have long memories, and their aggressive actions can be unpredictable and appear pre-meditated. Enclosures should be designed to prevent great apes from reaching out and grabbing people; nonhuman primates have been reported to grab neckties, loose-fitting laboratory coats, or long hair (NRC 1997). Because of their cognitive skills, great apes can be trained by using a food reward for cooperation in such activities as venipuncture and injections. This training can reduce the need to sedate the animals while minimizing risks to personnel.
RISKS AND RISK REDUCTION ASSOCIATED WITH ENVIRONMENTAL ENRICHMENT
Ethical reasons and federal regulatory requirements mandate that an environmental enrichment program be provided to captive nonhuman primates to improve their well-being. The Guide (NRC 1996) suggests that this enrichment be provided vis-à-vis a behavioral management program that comprises three principal elements: the structural environment, the social environment, and activity. An appropriately designed behavioral management program can be a useful tool to reduce risks associated with working with nonhuman primates. However, each of the components of the behavioral management program also poses its own OHS challenges for personnel.
A key way in which a behavioral management program can improve worker safety is by reducing atypical behavior expressed by nonhuman primates. Animals that are exhibiting behavioral pathology resulting from their captive conditions can be unpredictable and excessively aggressive, thereby increasing the risk of injury to workers. Efforts to maintain animals in a state of well-being so that they express species-typical, and thus more predictable, behaviors will improve worker safety.
In addition, when the animals associate the presence of personnel with positive experiences, such as the provision of food treats or cognitive activities, their behavior toward staff will more likely be affiliative rather than aggressive. As described previously, training animals to participate in routine procedures, as a part of the behavioral management program, reduces the risk of injury to workers because the animals will be cooperating in the activity rather than resisting.
Care must be exercised when personnel are forming social pairs or groups of primates for enrichment purposes because the animals will form dominance hierarchies through acts of aggression and submission that can inadvertently involve staff members. Published reports have
described methods of forming pairs or groups to maximize the safety of animals (Bernstein 1991; Fritz 1994; Reinhardt 1988, 1990, 1991). Those methods will also protect the personnel involved.
Many enrichment techniques involve attaching items (such as foraging devices and toys) to the front of a cage or placing items inside the cage, so there is the potential for animals to grab, bite, or scratch personnel as they provide upkeep of these items. In general, enrichment items kept inside the cage should be handled only when the cage is empty (for example, during cage-change procedures). Good judgment must be used when considering the upkeep of items attached to the front of an animal’s enclosure; the practice might be safe with some enrichment items and for some species of nonhuman primates but not others. Consideration should also be given to the risks associated with handling and transport of the enrichment devices themselves. These devices can become contaminated with saliva, urine and feces and can be an infectious hazard to any personnel that contact them, including staff that may wash the devices. Further, it should be noted that microbial growth can persist on enrichment devices after sanitation in a commercial cage washer (Bayne and others 1993).
Because the provision of environmental enrichment is a required aspect of captive-primate husbandry, staff with a variety of expertise may be involved in the behavioral management program. Institutions should ensure that staff receive training in the safe implementation of enrichment that is specific to the species held, the type of caging used, and the methods of enrichment being implemented.