Compendium of Measures to Prevent Disease Associated with Animals in Public Settings, 2009

National Association of State Public Health Veterinarians, Inc. (NASPHV)

Prepared by NASPHV

This report has been endorsed by CDC, the Council of State and Territorial Epidemiologists, and the American Veterinary Medical Association.

Corresponding preparer: Carina Blackmore, Co-chairperson, NASPHV Animal Contact Compendium Committee, Florida Department of Health, 4052 Bald Cypress Way, Bin A-08, Tallahassee, FL 32330. Telephone: 850-245-4732; Fax: 850-922-8473; e-mail: Carina_Blackmore@doh.state.fl.us.

Summary

Certain venues encourage or permit the public to be in contact with animals, resulting in millions of human-animal interactions each year. These settings include county or state fairs, petting zoos, animal swap meets, pet stores, zoologic institutions, circuses, carnivals, educational farms, livestock-birthing exhibits, educational exhibits at schools and child-care facilities, and wildlife photo opportunities. Although human-animal contact has many benefits, many human health problems are associated with these settings, including infectious diseases, exposure to rabies, and injuries. Infectious disease outbreaks reported during the previous decade have been caused by Escherichia coli O157:H7, Salmonella species, Cryptosporidium species, Coxiella burnetii, Mycobacterium tuberculosis, ringworm, and other pathogens. Such infections have substantial medical, public health, legal, and economic effects.

This report provides recommendations for public health officials, veterinarians, animal venue staff members, animal exhibitors, visitors to animal venues, physicians, and others concerned with minimizing risks associated with animals in public settings. The recommendation to wash hands is the most important prevention step for reducing the risk for disease transmission associated with animals in public settings. Other critical recommendations are that venues prohibit food in animal areas, venues include transition areas between animal areas and nonanimal areas, visitors receive information about disease risk and prevention procedures, and animals be properly cared for and managed. These updated 2009 guidelines also emphasize risks associated with baby poultry, reptiles, and rodents in public settings, and information about aquatic animal zoonoses has been incorporated.

Introduction

Contact with animals in public settings (e.g., fairs, educational farms, petting zoos, and schools) provides opportunities for entertainment and education. The National Association of State Public Health Veterinarians (NASPHV) understands the positive benefits of human-animal contact. However, an inadequate understanding of disease transmission and animal behavior can increase the likelihood of infectious diseases, rabies exposures, injuries, and other health problems among visitors, especially children, in these settings. Zoonotic diseases (i.e., zoonoses) are diseases transmitted between animals and humans. Of particular concern are instances in which zoonoses result in numerous persons becoming ill. During 1991--2005, the number of enteric disease outbreaks associated with animals in public settings increased (1). Since 1996, approximately 100 human infectious disease outbreaks involving animals in public settings have been reported to CDC (CDC, unpublished data, 2008).

Although eliminating all risk from animal contacts is not possible, this report provides recommendations for minimizing associated disease and injury. NASPHV recommends that local and state public health, agricultural, environmental, and wildlife agencies use these recommendations to establish their own guidelines or regulations for reducing the risk for disease from human-animal contact in public settings. Public contact with animals is permitted in numerous types of venues (e.g., animal displays, petting zoos, animal swap meets, pet stores, zoological institutions, nature parks, circuses, carnivals, educational farms, livestock-birthing exhibits, county or state fairs, child-care facilities or schools, and wildlife photo opportunities). Managers of these venues should use the information in this report in consultation with veterinarians, public health officials, or other professionals to reduce risks for disease transmission.

Guidelines to reduce risk for disease from animals in health-care and veterinary facilities and from service animals (e.g., guide dogs) have been developed (2--6). Although not specifically addressed in this report, the general principles and recommendations in this report are applicable to these settings.

Methods

NASPHV periodically updates the recommendations to prevent disease associated with animals in public settings. The revision includes reviewing recent literature; updating reported outbreaks, diseases, or injuries attributed to human-animal interactions in public settings; and soliciting input from NASPHV members and the public. During October 20--22, 2008, NASPHV members and external expert consultants met at CDC in Atlanta, Georgia. A committee consensus was required to add or modify existing language or recommendations. The 2009 guidelines further emphasize risks associated with baby poultry, reptiles, and rodents in public settings, and information about aquatic animal zoonoses has been incorporated.

Enteric (Intestinal) Diseases

Infections with enteric bacteria and parasites pose the highest risk for human disease from animals in public settings (7). Healthy animals can harbor human enteric pathogens, many of which have a low infectious dose (8--10). Enteric disease outbreaks among visitors to fairs, farms, petting zoos, and other venues are well documented. Many pathogens have been responsible, including Escherichia coli O157:H7 and other Shiga-toxin--producing E. coli (STEC), Salmonella species, Cryptosporidium species, and Campylobacter species (11--23). Although reports often document cattle, sheep, or goats (1,13) as sources for infection, poultry (24), rodents (25), reptiles (18) and other domestic and wild animals also are potential sources.

The primary mode of transmission for enteric pathogens is the fecal-oral route. Because animal fur, hair, skin, and saliva (26) often harbor fecal organisms, transmission can occur when persons pet, touch, feed, or are licked by animals. Transmission also has been associated with contaminated animal bedding, flooring, barriers, other environmental surfaces, and contaminated clothing and shoes (12,16,18,27--30). In addition, illness has resulted from fecal contamination of food (31), including raw milk (32--35) and water (36--38).

Removing ill animals (especially those with diarrhea) is necessary but not sufficient to protect animal and human health. Animals carrying human enteric pathogens frequently exhibit no signs of illness. They can shed the organisms intermittently, contaminating the environment (39). Some pathogens live for months or years in the environment (40--44). Because of limitations of laboratory tests, culturing fecal specimens or attempting to identify, screen, and remove infected animals might reduce but cannot eliminate the risk for transmission. Antimicrobial treatment of animals cannot reliably eliminate infection, prevent shedding, or protect against reinfection. In addition, treatment of animals can prolong shedding and contribute to antimicrobial resistance (45).

Multiple factors increase the probability of disease transmission at animal exhibits. Animals are more likely to shed pathogens because of stress induced by prolonged transportation, confinement, crowding, and increased handling (46--52). Commingling increases the probability that animals shedding organisms will infect other animals (53). The prevalence of certain enteric pathogens is often higher in young animals (54--56), which are frequently used in petting zoos and educational programs. Shedding of STEC and Salmonella organisms is highest in the summer and fall, when substantial numbers of traveling animal exhibits, agricultural fairs, and petting zoos are scheduled (51,56,57).

The risk for infection is increased by certain human factors and behaviors, especially in children. These factors include lack of awareness of the risk for disease, inadequate hand washing, lack of close supervision, and hand-to-mouth activities (e.g., use of pacifiers, thumb-sucking, and eating) (58). Children are particularly attracted to animal venues but have increased risk for serious infections. Although farm residents might have some acquired immunity to certain pathogens (59,60), livestock exhibitors have become infected with E. coli O157:H7 in fair outbreaks (16; K. Smith, DVM, PhD, Minnesota Department of Health, personal communication, 2008).

The layout and maintenance of facilities and animal exhibits can increase or decrease the risk for infection (61). Factors that increase risk include inadequate hand-washing facilities (62), structural deficiencies associated with temporary food-service facilities (12,15,18), inappropriate flow of visitors, and incomplete separation between animal exhibits and food preparation and consumption areas (63). Other factors include contaminated or inadequately maintained drinking water and sewage- or manure-disposal systems (30, 36--38).

Outbreaks and Lessons Learned

In 2000, two E. coli O157:H7 outbreaks in Pennsylvania and Washington prompted CDC to establish recommendations for enteric disease prevention associated with farm animal contact. Risk factors identified in both outbreaks were direct animal contact and inadequate hand washing (14,64). In the Pennsylvania outbreak, 51 persons (median age: 4 years) became ill within 10 days after visiting a dairy farm. Eight (16%) of these patients acquired hemolytic uremic syndrome (HUS), a potentially fatal consequence of STEC infection. The same strain of E. coli O157:H7 was isolated from cattle, patients, and the farm environment. An assessment of the farm environment determined that no areas separate from the animal contact areas existed for eating and drinking, and the hand-washing facilities were poorly maintained and not configured for children (14).

The protective effect of hand washing and the persistence of organisms in the environment were demonstrated in an outbreak of Salmonella enterica serotype Enteritidis infections at a Colorado zoo in 1996. A total of 65 cases (primarily among children) were associated with touching a wooden barrier around a temporary Komodo dragon exhibit. Children who were not ill were significantly more likely to have washed their hands after visiting the exhibit. S. enterica serotype Enteritidis was isolated from 39 patients, a Komodo dragon, and the wooden barrier (18).

In 2005, an E. coli O157:H7 outbreak among 63 patients, including seven who had HUS, was associated with multiple fairs in Florida. Both direct animal contact and contact with sawdust or shavings were associated with illness (13). Persons who reported feeding animals were more likely to have become ill. Persons were less likely to have become ill if they reported washing their hands before eating or drinking or were aware of the risk for illness before visiting the fair. Among persons who washed their hands with soap and water, creating lather decreased the likelihood of illness, illustrating the value of thorough hand washing. Drying hands on clothing increased the likelihood of illness (65).

During 2000--2001 at a Minnesota children's farm day camp, washing hands with soap after touching a calf and washing hands before going home decreased the likelihood for illness in two outbreaks involving multiple enteric organisms. Implicated organisms for the 84 human infections were E. coli O157:H7, Cryptosporidium parvum, non-O157 STEC, S. enterica serotype Typhimurium, and Campylobacter jejuni. These organisms and Giardia organisms were isolated from calves. Risk factors for children included caring for an ill calf and getting visible manure on their hands (21).

Disease transmission can occur in the absence of direct animal contact if a pathogen is disseminated in the environment. In an Oregon county fair outbreak, 60 E. coli O157:H7 infections occurred, primarily among children (27). Illness was associated with visiting an exhibition hall that housed goats, sheep, pigs, rabbits, and poultry; however, illness was not associated with touching animals or their pens, eating, or inadequate hand washing. E. coli O157:H7 was likely disseminated to environmental surfaces via contaminated dust (27).

Enteric pathogens can contaminate the environment and persist in animal housing areas for long periods. For example, E. coli O157:H7 can survive in soil for months (37,40,42,66,67). Prolonged environmental persistence of pathogens was documented in 2001 in an Ohio outbreak of E. coli O157:H7 infections in which 23 persons became ill at a fair facility after handling sawdust, attending a dance, or eating and drinking in a barn where animals had been exhibited during the previous week (37). Fourteen weeks after the fair, E. coli O157:H7 was isolated from multiple environmental sources within the barn, including from sawdust on the floor and dust on the rafters. Forty-two weeks after the fair, E. coli O157:H7 was recovered from sawdust on the floor. In 2004, an outbreak of E. coli O157:H7 infections was associated with attendance at the North Carolina State Fair goat and sheep petting zoo (13). Health officials identified 108 patients, including 15 who had HUS. The outbreak strain was isolated from the animal bedding 10 days after the fair was over and from the soil 5 months after the animal bedding and topsoil were removed (67). In 2003, a total of 25 persons acquired E. coli O157:H7 at a Texas agricultural fair; seven cases were culture confirmed. The strain cultured from patients also was found in fair environmental samples 46 days after the fair ended (16).

Improper facility design and inadequate maintenance can increase risk for infection, as illustrated by one of the largest waterborne outbreaks in the United States (37,38). In 1999, approximately 800 suspected cases of infection with E. coli O157:H7 and Campylobacter species were identified among attendees at a New York county fair, where unchlorinated water supplied by a shallow well was used by food vendors to make beverages and ice (38). Temporary facilities such as those associated with fairs are particularly vulnerable to design flaws (13,18). Such venues include those that add an animal display or petting zoo to attract children to zoos, festivals, roadside attractions, farm stands, farms where persons can pick their own produce, and Christmas tree lots. In 2005, an E. coli O157:H7 outbreak in Arizona was associated with a temporary animal contact exhibit at a municipal zoo (13). A play area for children was immediately adjacent to and downhill from the petting zoo facility. The same strain of E. coli O157:H7 was found both in children and 12 petting zoo animals. Child-care facility and school field trips to a pumpkin patch with a petting zoo resulted in 44 cases of E. coli O157:H7 infection in British Columbia, Canada (15). The same strain of E. coli O157:H7 was found both in children and in a petting zoo goat. Running water and signs recommending hand washing were not available, and alcohol hand sanitizers were at a height that was unreachable for some children. In New York, 163 persons became ill with STEC O111:H8, Cryptosporidium species, or both at a farm stand that sold unpasteurized apple cider and had a petting zoo with three calves (68). Stools from two calves were Shiga-toxin 1 positive.

Several outbreaks have occurred because of failure to understand and properly implement disease-prevention recommendations. Following a Minnesota outbreak of cryptosporidiosis with 31 ill students at a school farm program, specific recommendations provided to teachers were inadequately implemented (19), and a subsequent outbreak occurred with 37 illnesses. Hand-washing facilities and procedures were inadequate. Coveralls and boots were dirty, cleaned infrequently, and handled without repeat hand washing.

Outbreaks have resulted from contaminated animal products used for educational activities in schools. Salmonellosis outbreaks associated with dissection of owl pellets have been documented in Minnesota (69) and Massachusetts (C. Brown, DVM, Massachusetts Department of Public Health, personal communication, 2008). In Minnesota, risk factors for infection included inadequate hand washing, use of food service areas for the activity, and improper cleaning of contact surfaces. Persons in a middle school science class were among those infected in a multistate salmonellosis outbreak associated with frozen rodents purchased from the same Internet supplier to feed pet snakes (25).

During 2005--2008, several infectious disease outbreaks were caused by contact with animals and animal products. Although not primarily associated with public settings, the outbreaks have implications for animal contact venues. Turtles and other reptiles, rodents, and baby poultry (e.g., chicks and ducklings) have long been recognized as a source of human Salmonella infections (24,70--77). Since 2006, at least three large multistate outbreaks have been linked to contact with small turtles, including a fatal case in an infant (76,77). Since 2005, at least three multistate outbreaks linked to baby poultry from mail-order hatcheries have been identified; ill persons included those who reported contact with baby poultry at a feed store, school classroom, fair, or petting zoo (75). During 2006--2008, a total of 79 human Salmonella enterica serotype Schwarzengrund infections were linked to multiple brands of contaminated dry dog and cat food produced at a plant in Pennsylvania (78,79). Contaminated pig ear treats and pet treats containing beef and seafood also have been linked to human Salmonella infections (80--83).

Multidrug-resistant human Salmonella infections have been linked to contact with contaminated water from home aquariums containing tropical fish (84,85). A single case of Plesiomonas shigelloides infection in a Missouri infant was identified, and the organism was subsequently isolated from a babysitter's aquarium (86). A survey of tropical fish tanks in Missouri found that four (22%) of 18 tanks yielded P. shigelloides from three pet stores. These findings have implications for risk for infection from aquatic exhibits (e.g., aquariums and aquatic touch tanks).

Sporadic Infections

Sporadic infections also have been associated with animal environments. A study of sporadic E. coli O157:H7 infections in the United States determined that persons who became ill, especially children, were more likely than persons who did not become ill to have visited a farm with cows (87). Additional studies also documented an association between E. coli O157:H7 infection and visiting a farm (88) or living in a rural area (89). Studies of human cryptosporidiosis have documented contact with cattle or visiting farms as risk factors for infection (59,90,91). In addition, a case-control study identified multiple factors associated with Campylobacter infection, including consumption of raw milk and contact with farm animals (92).

Additional Health Concerns

Although enteric diseases are the most commonly reported illnesses associated with animals in public settings, other health risks exist. For example, allergies can be associated with animal dander, scales, fur, feathers, urine, and saliva (93--99). Additional health concerns include injuries, exposure to rabies, and infections other than enteric diseases.

Injuries

Injuries associated with animals in public settings include bites, kicks, falls, scratches, stings, crushing of the hands or feet, and being pinned between the animal and a fixed object. These injuries have been associated with big cats (e.g., tigers), monkeys, and other domestic, wild, and zoo animals. The settings have included public stables, petting zoos, traveling photo opportunities, schools, children's parties, and animal rides (M. Eidson, DVM, New York State Department of Health, personal communication, 2003; J.B. Bender, DVM, University of Minnesota, personal communication, 2003; M.T. Jay-Russell, DVM, California Department of Health, personal communication, 2003; G.L. Swinger, DVM, Tennessee Department of Health, personal communication, 2003). For example, a Kansas teenager was killed while posing for a photograph with a tiger being restrained by its handler at an animal sanctuary (100). In Texas, two high school students were bitten by a cottonmouth snake that was used in a science class after being misidentified as a nonvenomous species (W. Garvin, Caldwell Zoo, Texas, personal communication, 2008).

Exposure to Rabies

Persons who have contact with rabid mammals can be exposed to the rabies virus through a bite or when mucous membranes or open wounds become contaminated with infected saliva or nervous tissue. Although no human rabies deaths caused by animal contact in public settings have been reported, multiple rabies exposures have occurred, requiring extensive public health investigations and medical follow-up. For example, thousands of persons have received rabies postexposure prophylaxis (PEP) after being exposed to rabid or potentially rabid animals, including bats, cats, goats, bears, sheep, horses, and dogs, at various venues: a pet store in New Hampshire (101), a county fair in New York State (102), petting zoos in Iowa (103,104) and Texas (J.H. Wright, DVM, Texas Department of Health, personal communication, 2004), school and rodeo events in Wyoming (62), a horse show in Tennessee, and summer camps in New York (105). Substantial public health and medical care challenges associated with potential mass rabies exposures include difficulty in identifying and contacting persons, correctly assessing exposure risks, and providing timely medical prophylaxis. Prompt assessment and treatment are critical to prevent this disease, which is usually fatal.

Other Infections

Multiple bacterial, viral, fungal, and parasitic infections have been associated with animal contact, and the infecting organisms are transmitted through various modes. Infections from animal bites are common and frequently require extensive treatment or hospitalization. Bacterial pathogens associated with animal bites include Pasteurella species, Francisella tularensis (106), Staphylococcus species, Streptococcus species, Capnocytophaga canimorsus, Bartonella henselae (cat-scratch disease), and Streptobacillus moniliformis (rat-bite fever). Certain monkey species (especially macaques) that are kept as pets or used in public exhibits can be infected with simian herpes B virus; they might be asymptomatic or have mild oral lesions. Human exposure through monkey bites or bodily fluids can result in fatal meningoencephalitis (107,108).

Skin contact with animals in public settings is also a public health concern. In 1995, 15 cases of ringworm (club lamb fungus) caused by Trichophyton species and Microsporum gypseum were documented among owners and family members who exhibited lambs in Georgia (109). In 1986, ringworm in 23 persons and multiple animal species was traced to a Microsporum canis infection in a hand-reared zoo tiger cub (110). Orf virus infection (i.e., contagious ecthyma, or sore mouth) has occurred after contact with sheep at a public setting (111). Orf virus infection also has been described in goats and sheep at a children's petting zoo (112) and in a lamb used for an Easter photo opportunity (M. Eidson, DVM, New York State Department of Health, personal communication, 2003). In the 1970s, after handling various species of infected exotic animals, a zoo attendant experienced an extensive papular skin rash from a cowpox-like virus (113). In 2003, multiple cases of monkeypox occurred among persons who had contact with infected prairie dogs either at a child-care center (114,115) or a pet store (J.J. Kazmierczak, DVM, Wisconsin Department of Health and Family Services, personal communication, 2004). Aquatic animals and their environment also have been associated with cutaneous infections (116). For example, Mycobacterium marinum infections have been described among persons owning or cleaning fish tanks (117,118).

Ectoparasites and endoparasites pose concerns when humans and exhibit animals interact. Sarcoptes scabiei is a skin mite that infests humans and animals, including swine, dogs, cats, foxes, cattle, and coyotes (119,120). Although human infestation from animal sources is usually self-limiting, skin irritation and itching might occur for multiple days and can be difficult to diagnose (120,121). Bites from avian mites have been reported in association with pet gerbils in school settings (122). Animal flea bites to humans increase the risk for infection or allergic reaction. In addition, fleas can carry a tapeworm species that can infect children who swallow the flea (123,124). Animal parasites also can infect humans who ingest soil or other materials contaminated with animal feces or who come into contact with contaminated soil. Parasite control through veterinary care and proper husbandry combined with hand washing reduces the risks associated with ectoparasites and endoparasites (125).

Tuberculosis is another disease associated with certain animal settings. In 1996, 12 circus elephant handlers at an exotic animal farm in Illinois were infected with Mycobacterium tuberculosis; one handler had signs consistent with active disease after three elephants died of tuberculosis. Medical history and testing of the handlers indicated that the elephants had been a probable source of exposure for most of the human infections (126). During 1989--1991 at a zoo in Louisiana, seven animal handlers who were previously negative for tuberculosis tested positive after a Mycobacterium bovis outbreak in rhinoceroses and monkeys (127). In 2003, the U.S. Department of Agriculture (USDA) developed guidelines regarding removal of tuberculosis-infected animals from public settings because of the risk for exposure to the public (128).

Zoonotic pathogens also can be transmitted by direct or indirect contact with reproductive fluids, aborted fetuses, or newborns from infected dams. Live-birthing exhibits, usually involving livestock (e.g., cattle, pigs, goats, or sheep), are popular at agricultural fairs. Although the public usually does not have direct contact with animals during birthing, newborns and their dams might be available for petting afterward. Q fever (Coxiella burnetii), leptospirosis, listeriosis, brucellosis, and chlamydiosis are serious zoonoses that can be acquired through contact with reproductive materials (129).

C. burnetii is a rickettsial organism that most frequently infects cattle, sheep, and goats. The disease can cause abortion in animals, but more frequently the infection is asymptomatic. During birthing, infected animals shed substantial numbers of organisms, which can become aerosolized. Most persons exposed to C. burnetii develop an asymptomatic infection, but clinical illness can range from an acute influenza-like illness to life-threatening endocarditis. A Q fever outbreak involving 95 confirmed cases and 41 hospitalizations was linked to goats and sheep giving birth at petting zoos in indoor shopping malls (130). Indoor-birthing exhibits might pose an increased risk for Q fever transmission because of inadequate ventilation.

Chlamydophila psittaci infections cause respiratory disease and are usually acquired from psittacine birds (131). For example, an outbreak of C. psittaci pneumonia occurred among the staff members Copenhagen Zoological Garden (132). On rare occasions, chlamydial infections acquired from sheep, goats, and birds result in reproductive problems in women (131,133,134).

Swine influenza virus (H1N1) was the suspected cause of a respiratory outbreak in swine and swine exhibitors at an Ohio county fair in 2007. The virus was isolated from swine and from a man and his daughter, who were both exhibitors at the fair (135).

Recommendations

Guidelines from multiple organizations were used to create the recommendations in this report (136--138). Although no federal U.S. laws address the risk for transmission of pathogens at venues where the public has contact with animals, some states have such laws (62,65,139--141). For example, after approximately 100 persons became ill after visiting a state fair petting zoo in 2004, North Carolina passed a law requiring agricultural fairs to obtain a permit from the North Carolina Department of Agriculture and Consumer Services for all animal exhibits open to the public (available at http://www.ncleg.net/sessions/2005/bills/senate/html/S268v4.html).

Certain federal agencies and associations in the United States have developed standards, recommendations, and guidelines for venues where animals are present in public settings. The Association of Zoos and Aquariums has accreditation standards for reducing risk for animal contact with the public in zoologic parks (142). In accordance with the Animal Welfare Act, USDA licenses and inspects certain animal exhibits for humane treatment of animals; however, the act does not address human health protection. In 2001, CDC issued guidelines to reduce the risk for infection with enteric pathogens associated with farm visits (64). CDC also has issued recommendations for preventing transmission of Salmonella from reptiles and baby poultry to humans (74,143). The Association for Professionals in Infection Control and Epidemiology (APIC) and the Animal-Assisted Interventions Working Group (AAI) have developed guidelines to address risks associated with the use of animals in health-care settings (2,6). NASPHV has developed a compendium of measures to reduce risks of human exposure to C. psittaci (131).

Recommendations for Local, State, and Federal Agencies

Communication and cooperation among human and animal health agencies should be enhanced and include veterinarians and cooperative extension offices. Additional research should be conducted regarding the risk factors and effective prevention and control methods for health issues associated with animal contact. To improve use of these recommendations, agencies should take the following steps:

• Disseminate this report to extension agents, venue operators, and others associated with managing animals in public settings. Most states do not have a complete list of animal contact venues (62). States should strive to develop a complete list to facilitate dissemination of recommendations.
• Disseminate educational and training materials to venue operators and other interested persons. Material formats could include PowerPoint slide presentations, videos, and written guidelines (129,130,144).
• Encourage or require oversight to ensure compliance with recommendations at animal contact venues.

To evaluate and improve these recommendations, surveillance for human health issues associated with animal contact should be enhanced. Agencies should take the following steps:

• Conduct thorough epidemiologic investigations of outbreaks.
• Include questions on disease report forms and outbreak investigation questionnaires about exposure to animals, animal environments, and animal products and feed.
• Follow appropriate protocols for sampling and testing of humans, animals, and the environment, including molecular subtyping of pathogen isolates.
• Report outbreaks to state health departments.
• Local and state public health departments should also report all outbreaks of enteric infections resulting from animal contact to CDC through the National Outbreak Reporting System (NORS) (available at http://www.cdc.gov/enterics).

Recommendations for Education

Education is essential to reduce risks associated with animal contact in public settings. Experience from outbreaks suggests that visitors knowledgeable about potential risks are less likely to become ill (13). Even in well-designed venues with operators who are aware of the risks for disease, outbreaks can occur when visitors do not understand and apply disease-prevention recommendations.

Venue operators should take the following steps:

• Become knowledgeable about the risks for disease and injury associated with animals and be able to explain risk-reduction measures to staff members and visitors.
• Become familiar with and implement the recommendations in this compendium.
• Consult with veterinarians, state and local agencies, and county extension agents on implementation of the recommendations.
• Develop or obtain training and education materials and train staff members.
• Ensure that visitors receive educational messages before they enter the exhibit, including information that animals can cause injuries or carry organisms that can cause serious illness (Appendices A and B).
• Provide information in a simple and easy-to-understand format that is age- and language-appropriate.
• Provide information in multiple formats (e.g., signs, stickers, handouts, and verbal information).
• Provide information to persons arranging school field trips or classroom exhibits so that they can educate participants before the visit.

Venue staff members should take the following steps:

• Become knowledgeable about the risks for disease and injury associated with animals and be able to explain risk-reduction recommendations to visitors.
• Ensure that visitors receive educational messages regarding risks and preventive measures.
• Encourage compliance by the public with risk-reduction recommendations, especially compliance with hand-washing procedures (Appendix C) as visitors exit animal areas.
• Comply with local and state requirements for reporting animal bites or other injuries.

Recommendations for Managing Public-Animal Contact

The recommendations in this report were developed for settings in which direct animal contact is encouraged (e.g., petting zoos and aquatic touch tanks) and in which animal contact is possible (e.g., county fairs). They should be tailored to specific settings and incorporated into guidelines and regulations developed at the state or local level. Contact with animals should occur in settings where measures are in place to reduce the potential for injuries or disease transmission. Incidents or problems should be responded to, documented, and reported.

Facility Design

The design of facilities and animal pens should minimize the risk associated with animal contact (Figure), including limiting direct contact with manure and encouraging hand washing (Appendix C). The design of facilities or contact settings might include double barriers to prevent contact with animals or contaminated surfaces except for specified animal interaction areas. Previous outbreaks have revealed that temporary exhibits are often not designed appropriately. Common problems include inadequate barriers, floor surfaces that are difficult to keep clean, insufficient plumbing, lack of signs regarding risk and prevention measures, and inadequate hand-washing facilities (13,18,31,34). Specific guidelines might be necessary for certain settings, such as schools (Appendix D).

Recommendations for cleaning procedures should be tailored to the specific situation. All surfaces should be cleaned thoroughly to remove organic matter before disinfection. A 1:32 dilution of household bleach (e.g., one-half cup bleach per gallon of water) is needed for basic disinfection. Quaternary ammonium compounds (e.g., Roccal or Zephiran) also can be used per the manufacturer label. For disinfection when a particular organism has been identified, additional guidance is available (http://www.cfsph.iastate.edu/disinfection). All compounds require >10 minutes of contact time with a contaminated surface.

Venues should be divided into three types of areas: nonanimal areas (areas in which animals are not permitted, with the exception of service animals), transition areas (located at entrances and exits to animal areas), and animal areas (where animal contact is possible or encouraged) (Figure).

Nonanimal Areas

• Do not permit animals, except service animals, in nonanimal areas.
• Prepare, serve, and consume food and beverages only in nonanimal areas.
• Provide hand-washing facilities and display hand-washing signs where food or beverages are served (Appendix C).

Transition Areas Between Nonanimal and Animal Areas

Establishing transition areas through which visitors pass when entering and exiting animal areas is critical. A one-way flow of visitors is preferred, with separate entrance and exit points. The transition areas should be designated as clearly as possible, even if they are conceptual rather than physical (Figure).

Entrance transition areas should be designed to facilitate education:

• Post signs or otherwise notify visitors that they are entering an animal area and that risks are associated with animal contact (Appendix B).
• Instruct visitors not to eat, drink, smoke, place their hands in their mouth, or use bottles or pacifiers while in the animal area.
• Do not allow strollers and related items (e.g., wagons and diaper bags) in areas where direct animal contact is encouraged. Establish storage or holding areas for these items.
• Control visitor traffic to prevent overcrowding.
• Exit transition areas should be designed to facilitate hand washing.
• Post signs or otherwise instruct visitors to wash their hands when leaving the animal area.
• Provide accessible hand-washing stations for all visitors, including children and persons with disabilities (Figure).
• Position venue staff members near exits to encourage compliance with hand washing.

Animal Areas

• Do not allow food and beverages in animal areas.
• Do not allow toys, pacifiers, spill-proof cups, baby bottles, or strollers in animal areas.
• Prohibit smoking in animal areas.
• Supervise children closely to discourage hand-to-mouth activities (e.g., nail-biting and thumb-sucking), contact with manure, and contact with soiled bedding. Children should not be allowed to sit or play on the ground in animal areas. If hands become soiled, supervise hand washing.
• Ensure that animal feed and water are not accessible to the public.
• Allow feeding only when contact with animals is controlled (e.g., with barriers).
• Do not provide animal feed in containers that can be eaten by humans (e.g., ice cream cones) to decrease the risk for children eating food that has come into contact with animals.
• Assign trained staff members to encourage appropriate human-animal interactions, to identify and remove potential risks for patrons (e.g., by promptly cleaning up wastes), and process reports of injuries and exposures.
• Promptly remove manure and soiled animal bedding from animal areas.
• Store animal waste and specific tools for waste removal (e.g., shovels and pitchforks) in designated areas that are restricted from public access.
• Avoid transporting manure and soiled bedding through nonanimal areas or transition areas. If this is unavoidable, take precautions to prevent spillage.
• Where feasible, disinfect animal areas (e.g., flooring and railings) at least once daily.
• Provide adequate ventilation both for animals (145) and humans.
• Minimize the use of animal areas for public (nonanimal) activities. Zoonotic pathogens can contaminate the environment for substantial periods (37). If animal areas must be used for public events (e.g., weddings and dances), the areas should be cleaned and disinfected, particularly if food and beverages are served. Materials with smooth, impervious surfaces (e.g., steel, plastic, and sealed concrete) are easier to clean than other materials (e.g., wood or dirt floors). Remove organic material (e.g., bedding, feed, and manure) before using disinfectants.
• For birds in bird encounter exhibits, refer to the psittacosis compendium (131) for recommendations regarding disease screening.
• Visitors to aquatic touch tank exhibits who have open wounds should be advised not to participate. Hand washing stations should be provided.
• When using animals or animal products (e.g., animal pelts, animal waste, and owl pellets) (69) for educational purposes, only use them in designated animal areas (Figure). Animals and animal products should not be brought into school cafeterias and other food-consumption areas.
• When animals are in school classrooms, specific areas must be designated for animal contact (Appendix D). Designated animal areas must be thoroughly cleaned after use. Parents should be informed of the benefits and potential risks associated with animals in school classrooms.

Animal Care and Management

The risk for disease or injury from animal contact can be reduced by carefully managing the specific animals used. The following recommendations should be considered for management of animals in contact with the public.

• Animal care: Monitor animals daily for signs of illness, and ensure that animals receive appropriate veterinary care. Ill animals, animals known to be infected with a pathogen, and animals from herds with a recent history of abortion or diarrhea should not be exhibited. To decrease shedding of pathogens, animals should be housed to minimize stress and overcrowding.
• Veterinary care: Retain and use the services of a licensed veterinarian. Preventive care, including vaccination and parasite control, appropriate for the species should be provided. Certificates of veterinary inspection from an accredited veterinarian should be up-to-date according to local or state requirements for animals in public settings. A herd or flock inspection is a critical component of the health certificate process. Routine screening for diseases is not recommended, except for C. psittaci in bird encounter exhibits (131), tuberculosis in elephants (128) and primates, and Q fever in ruminants in birthing exhibits (146).
• Rabies: All animals should be housed to reduce potential exposure to wild animal rabies reservoirs. Mammals should also be up-to-date on rabies vaccinations (147). These steps are particularly critical in areas where rabies is endemic and in venues where animal contact is encouraged (e.g., petting zoos). Because of the extended incubation period for rabies, unvaccinated mammals should be vaccinated at least 1 month before they have contact with the public. If no licensed rabies vaccine exists for a particular species (e.g., goats, swine, llamas, and camels) that is used in a setting where public contact occurs, consultation with a veterinarian regarding off-label use of rabies vaccine is recommended. Use of off-label vaccine does not provide the same level of assurance as vaccine labeled for use in a particular species; however, off-label use of vaccine might provide protection for certain animals and thus decrease the probability of rabies transmission (147). Vaccinating slaughter-class animals before displaying them at fairs might not be feasible because of the vaccine withdrawal period that occurs as a result of antibiotics used as preservatives in certain vaccines. Mammals that are too young to be vaccinated should be used in exhibit settings only if additional restrictive measures are available to reduce risks (e.g., using only animals that were born to vaccinated mothers and housed to avoid rabies exposure). In animal contact settings, rabies testing should be considered for animals that die suddenly.
• Dangerous animals: Because of their strength, unpredictability, or venom or the pathogens that they might carry, certain domestic, exotic, or wild animals should be prohibited in exhibit settings where a reasonable possibility of animal contact exists. Species of primary concern include nonhuman primates (e.g., monkeys and apes) and certain carnivores (e.g., lions, tigers, ocelots, wolves and wolf hybrids, and bears). In addition, rabies-reservoir species (e.g., bats, raccoons, skunks, foxes, and coyotes) should not be used for direct contact.
• Animal births: Ensure that the public has no contact with animal birthing by-products (e.g., the placenta). In live-birth exhibits, the environment should be thoroughly cleaned after each birth, and all waste products should be properly discarded. Holding such events outside or in well-ventilated areas is preferable.

Additional Recommendations

• Populations at high risk: Children aged <5 years are at particularly high risk for serious infections. Other groups at increased risk include persons with waning immunity (e.g., older adults) and persons who are mentally impaired, pregnant, or immunocompromised (e.g., persons with human immunodeficiency virus/acquired immunodeficiency syndrome, without a functioning spleen, or receiving immunosuppressive therapy). Persons at high risk for infection should take precautions at any animal exhibit. In addition to thorough and frequent hand washing, heightened precautions could include avoiding contact with animals and their environment (e.g., pens, bedding, and manure). Animals of particular concern for transmitting enteric diseases include young ruminants, young poultry, reptiles, amphibians, and ill animals.
• Consumption of unpasteurized products: Prohibit the consumption of unpasteurized dairy products (e.g., milk, cheese, and yogurt) and unpasteurized apple cider or juices.
• Drinking water: Local public health authorities should inspect drinking water systems before use. Only potable water should be used for consumption by animals and humans. Back-flow prevention devices should be installed between outlets in livestock areas and water lines supplying other areas on the grounds. If the water supply is from a well, adequate distance should be maintained from possible sources of contamination (e.g., animal-holding areas and manure piles). Maps of the water distribution system should be available for use in identifying potential or actual problems. The use of
• outdoor hoses should be minimized, and hoses should not be left on the ground. Hoses that are accessible to the public should be labeled "water not for human consumption." Operators and managers of settings in which treated municipal water is not available should ensure that a safe water supply is available.

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National Association of State Public Health Veterinarians, Inc., Committee

Co-chairpersons: Carina Blackmore, DVM, PhD, Florida Department of Health, Tallahassee, Florida; John R. Dunn, DVM, PhD, Tennessee Department of Health, Nashville, Tennessee.
Members: Kirk E. Smith, DVM, PhD, Minnesota Department of Health, St. Paul, Minnesota; James H. Wright, DVM, Texas Department of State Health Services, Tyler, Texas; Ron Wohrle, DVM, Washington State Department of Health, Olympia, Washington; Louisa Castrodale, DVM, Alaska Department of Health and Social Services, Anchorage, Alaska.
Consultants to the Committee: Casey Barton Behravesh, DVM, DrPH, CDC, Atlanta, Georgia; Sue K. Billings, DVM, National Assembly of State Animal Health Officials, Washington, DC; Marianne Ash, DVM, American Veterinary Medical Association Council on Public Health and Regulatory Veterinary Medicine, Schaumburg, Illinois; Marla J. Calico, International Association of Fairs and Expositions, Springfield, Missouri; Allan Hogue, DVM, US Department of Agriculture, Riverdale, Maryland; Timothy F. Jones, MD, Council of State and Territorial Epidemiologists, Atlanta, Georgia; Thomas P. Meehan, DVM, Association of Zoos and Aquariums, Silver Spring, Maryland.

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Date last reviewed: 4/23/2009