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Compendium of Measures to Prevent Disease Associated with Animals in Public Settings, 2007

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

Prepared by NASPHV

Summary

This report has been endorsed by CDC, the Council of State and Territorial Epidemiologists, and the American Veterinary Medical Association. The material in this report originated in the Coordinating Center for Infectious Diseases, Mitch Cohen MD, Director; and the Division of Foodborne, Bacterial, and Mycotic Diseases, David Warnock PhD, Director.

Corresponding preparer: J.B. Bender DVM, Co-chair, NASPHV Animal Contact Compendium Committee, University of Minnesota, Veterinary Public Health, 136F Andrew Boss, 1354 Eckles Avenue, St. Paul, MN 55108, Telephone: 612-625-6203; Fax: 612-624-4906; E-mail: bende002@umn.edu.

Certain venues encourage or permit the public to contact 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, farm tours, livestock-birthing exhibits, educational exhibits at schools, and wildlife photo opportunities. Although multiple benefits of human-animal contact exist, infectious diseases, rabies exposures, injuries, and other human health problems associated with these settings are possible. Infectious disease outbreaks reported during the previous decade have been caused by Escherichia coli O157:H7, Salmonella, Cryptosporidium, Coxiella burnetii, Mycobacterium tuberculosis, ringworm, and other pathogens. Such incidents have substantial medical, public health, legal, and economic effects.

This report provides recommendations for public health officials, veterinarians, animal venue staff, 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 single most important prevention step for reducing the risk for disease transmission. Other critical recommendations are that venues not allow food in animal areas, venues include transition areas between animal areas and nonanimal areas, visitors be educated about disease risk and prevention procedures, and animals be properly cared for and managed.

Introduction

Contact with animals in public settings (e.g., fairs, farm tours, petting zoos, and schools) provides opportunities for entertainment and education. However, 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 from animals to humans. Of particular concern are instances in which large numbers of persons become ill. Since 1991, approximately 50 human infectious disease outbreaks involving animals in public settings have been reported to CDC (1). During the preceding 10 years, an increasing number of enteric disease outbreaks associated with animals in public settings (e.g., fairs and petting zoos) have been reported (1).

The National Association of State Public Health Veterinarians (NASPHV) understands the positive benefits of human-animal contact. Although eliminating all risk from animal contacts is not possible, this report provides recommendations for minimizing 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. Multiple venues exist where public contact with animals is permitted (e.g., animal displays, petting zoos, animal swap meets, pet stores, zoological institutions, nature parks, circuses, carnivals, farm tours, livestock-birthing exhibits, county or state fairs, schools, and wildlife photo opportunities). Persons responsible for managing these venues should use the information in this report to reduce risk for disease transmission.

Guidelines to reduce risks for disease from animals in health-care and veterinary facilities and from service animals (e.g., guide dogs) have been developed (2--5). These settings are not specifically addressed in this report, although the general principles and recommendations are applicable to these settings.

Methods

NASPHV periodically reviews the "Compendium of Measures to Prevent Disease Associated with Animal in Public Settings". This includes reviewing recent literature; updating reported outbreaks, diseases, or injuries attributed to human-animal interactions in a public setting; and soliciting comments or suggestions from the NASPHV membership and questions posed by the public. During November 27--29, 2006, NASPHV members and external expert consultants met at CDC in Atlanta, Georgia. The first day of the meeting was dedicated to reviewing scientific information regarding recent outbreaks, associated risk factors, pathogen biology, and interventional studies. A moderated discussion of each section of the recommendations was conducted. The committee reviewed scientific evidence and expert opinion in revising the document. A committee consensus was needed to add or modify existing language or recommendations.

Enteric (Intestinal) Diseases

Infections with enteric bacteria and parasites pose the highest risk for human disease from animals in public settings (6). Healthy animals can harbor human enteric pathogens. Many of these organisms have a low infectious dose (7--9). Because of the popularity of animal venues, a substantial number of persons might be exposed. Illness and outbreaks of enteric diseases among visitors to fairs, farms, and petting zoos are well documented. Pathogens responsible for outbreaks include Escherichia coli O157:H7 and other Shiga toxin-producing E. coli (STEC), Campylobacter, Salmonella, and Cryptosporidium (10--22). Although reports often document cattle, sheep, or goats as sources for infection, poultry (23--26), rodents (25--27), and other domestic and wild animals also are potential sources.

The primary mode of transmission for enteric pathogens is fecal-oral. Because animal fur, hair, skin, and saliva (28) can become contaminated with fecal organisms, transmission can occur when persons pet, touch, feed, or are licked by animals. Transmission has occurred from fecal contamination of food, including raw milk (29--31), sticky foods (e.g., cotton candy [32]), and water (33--35). Illness also has been associated with contaminated clothing and shoes (11,17), animal bedding, flooring, barriers, and other environmental surfaces (15,17,25,36--38).

Animals carrying enteric organisms pathogenic to humans (e.g., STEC, Salmonella, and Campylobacter) frequently exhibit no signs of illness and can shed these pathogens intermittently. Removing ill animals (especially those with diarrhea) is necessary but not sufficient to protect animal and human health. Animals that appear to be healthy often shed pathogens that contaminate the environment (39). Some pathogens live for months or years in the environment (40--44). Because of intermittent shedding and limitations of laboratory tests, culturing fecal specimens or attempting to identify, screen, and remove infected animals might reduce, but will not eliminate, the risk for transmission. Antimicrobial treatment of animals cannot reliably eliminate infection and shedding of enteric pathogens or prevent reinfection.

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 by persons (45--51). Commingling increases the probability that animals shedding organisms will infect other animals (52). The prevalence of certain enteric pathogens is often higher in young animals (53--55), which are frequently used in petting zoos and educational programs. Shedding of STEC and Salmonella is highest in the summer and fall when substantial numbers of traveling animal exhibits, agricultural fairs, and petting zoos are scheduled (50,55,56).

The risk for infections 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) (57). Children are particularly attracted to animal venues and have increased risk for serious infections.

The layout and maintenance of facilities and animal exhibits also can affect the risk for infection (58). Risk factors include inadequate hand-washing facilities (59), structural deficiencies associated with temporary food-service facilities (12,14,17), inappropriate flow of visitors, and incomplete separation between animal exhibits and food preparation and consumption areas (60). Other factors include contaminated or inadequately maintained drinking water and sewage- or manure-disposal systems (33--35,38).

Lessons from Outbreaks

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 (60,61). 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. In addition to the reported cases, an increased number of diarrhea cases in the community were attributed to visiting the farm. An assessment of the farm environment determined that no areas existed for eating and drinking separate from the animal contact areas, and the limited hand-washing facilities were not configured for children (60).

The protective effect of hand washing and the persistence of organisms in the environment were demonstrated in an outbreak of Salmonella infections at a Colorado zoo in1996. A total of 65 cases (most among children) were associated with touching a wooden barrier around a temporary Komodo dragon exhibit. Children who were not ill were substantially more likely to have washed their hands after visiting the exhibit. Salmonella was isolated from 39 patients, a Komodo dragon, and the wooden barrier (17).

In 2005, an E. coli O157:H7 outbreak among 63 patients, including seven who had HUS, were associated with multiple fairs in Florida. Both direct animal contact and contact with sawdust or shavings were associated with illness (12). Persons who reported feeding animals were at increased risk. Among persons who washed their hands after leaving the animal area, using soap and water was protective for those who created a lather (62). Drying hands on clothes increased the risk for illness. Persons were less likely to become ill if they reported washing their hands before eating or drinking or were aware of the risk for illness before visiting the fair.

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 were protective factors in two outbreaks involving multiple enteric organisms. A total of 84 illnesses were documented among attendees. Implicated organisms for the human infections were E. coli O157:H7, Cryptosporidium parvum, non-O157 STEC, Salmonella enterica serotype Typhimurium, and Campylobacter jejuni. These organisms and Giardia were isolated from calves. Risk factors for children included caring for an ill calf and getting visible manure on their hands (20).

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 (38,40,42,63). Prolonged environmental persistence of pathogens was documented in an Ohio outbreak in 2001 of E. coli O157:H7 infections in which 23 persons became ill at a fair after handling sawdust, attending a dance, or eating and drinking in a barn where animals were exhibited during the previous week (38). Fourteen weeks after the fair, E. coli O157:H7 was isolated from multiple environmental sources within the barn, including 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 infection was associated with attendance at the North Carolina State Fair goat and sheep petting zoo (12). 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 (58). In 2003, a total of 25 persons acquired E. coli O157:H7 at a Texas agricultural fair. The strain isolated from patients also was found in environmental samples 46 days after the fair ended (15).

Transmission can occur even in the absence of direct animal contact if the pathogen is disseminated in the environment. In an Oregon county fair outbreak, 60 cases occurred, mostly among children (25). 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. The same organism was recovered from ill persons and the building. Transmission of E. coli O157:H7 from contaminated dust was implicated in two outbreaks in Ohio and Oregon (25,38).

Improper facility design and inadequate maintenance might increase risk, as illustrated by one of the largest waterborne outbreaks in the United States (34,35). In 1999, approximately 800 suspected cases of E. coli O157:H7 and Campylobacter infection were identified among attendees of a New York county fair where the water and sewage systems had deficiencies. Temporary facilities are particularly vulnerable to design flaws (12,17). Such venues include those that add an animal display or petting zoo for the purpose of attracting children to zoos, festivals, roadside attractions, farm stands, pick-your-own-produce farms, and Christmas tree lots. In 2005, an E. coli O157:H7 outbreak in Arizona was associated with a temporary petting zoo at a municipal zoo (12). Child care 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 (14). The same strain of E. coli was found both in children and in a petting zoo goat. Running water and signage recommending hand washing were not available, and alcohol hand sanitizers were at a height that was unreachable for some children. A total of 163 persons became ill with STEC O111:H8 and/or Cryptosporidium at a New York farm stand that sold unpasteurized apple cider and had a petting zoo with three calves (64).

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 (18). A subsequent outbreak occurred with 37 illnesses. Hand-washing procedures were inadequate (e.g., only water available, crowding at sink, and drying hands on clothes). Coveralls and boots were dirty, cleaned infrequently, and removed after hand-washing. In addition, inadequate hand washing and cleaning of contact surfaces resulted in an outbreak of salmonellosis associated with dissection of owl pellets in elementary schools (65).

Sporadic Infections

Although not identified as part of recognized outbreaks, sporadic infections have been associated with animal environments. A study of sporadic E. coli O157:H7 infections in the United States determined that patients, especially children, were more likely than healthy persons to have visited a farm with cows (66). Additional studies also documented an association between E. coli O157:H7 infection and visiting a farm (67) or living in a rural area (68). Studies of human cryptosporidiosis have documented contact with cattle or visiting farms as risk factors for infection (69--71). A case-control study identified multiple factors, including raw milk consumption and contact with farm animals, associated with Campylobacter infection (72). In other studies, farm residents were at a lower risk for infection with Cryptosporidium (71) and E. coli O157:H7 (73) than farm visitors, presumably because the residents had acquired immunity as a result of their early and frequent exposure to these organisms. However, livestock exhibitors became infected with E. coli O157:H7 in at least one fair outbreak (15).

Additional Health Concerns

Although enteric diseases are the most commonly reported illnesses associated with animals in public settings, other health risks are of concern. For example, allergies can be associated with animal dander, scales, fur, feathers, body wastes (e.g., urine), and saliva (74--76). Additional health concerns addressed in this report include injuries, rabies exposures, and other infections.

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 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 (77).

Rabies Exposures

Contact with rabid mammals can expose persons to rabies virus through bites or contamination of mucous membranes, scratches, or other wounds with infected saliva or nervous tissue. Although no human rabies deaths caused by animal contact in public exhibits have been recorded, multiple rabies exposures have occurred, requiring extensive public health investigation 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 cats, goats, bears, sheep, ponies, and dogs) at a variety of venues: a pet store in New Hampshire (78), a county fair in New York State (79), petting zoos in Iowa (80,81) and Texas (J. Wright, Texas Department of Health, personal communication, 2004), and school and rodeo events in Wyoming (59). 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 agents have been associated with animal contact. These 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, Francisella tularensis (82), Staphylococcus, Streptococcus, Capnocytophaga canimorsus, Bartonella henselae (cat-scratch disease), and Streptobacillus moniliformis (rat-bite fever). Certain monkey species (especially macaques) kept as pets or used in public exhibits can be infected with herpes B virus, either asymptomatically or with mild oral lesions. Human exposure through monkey bites or bodily fluids can result in a fatal meningoencephalitis (83,84).

Skin contact with animals in public settings is also a public health concern. In 1995, a total of 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 during a show season (85). Ringworm in 23 persons and multiple animal species was traced to a Microsporum canis infection in a hand-reared zoo tiger cub (86). Orf virus infection (contagious ecthyma or sore mouth) has occurred following contact with sheep at a public setting (E. Lederman, CDC, personal communication, 2006). In addition, orf virus infection has been described in goats and sheep at a children's petting zoo (87) and in a lamb used for an Easter photo opportunity (M. Eidson, New York State Department of Health, personal communication, 2003). After handling various species of infected exotic animals, a zoo attendant experienced an extensive papular skin rash from a cowpox-like virus (88). In 2003, multiple cases of monkeypox occurred among persons who had contact with infected prairie dogs either at a child care center (89,90) or a pet store (J.J. Kazmierczak, Wisconsin Department of Health and Family Services, personal communication, 2004).

Ecto- 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 (91, 92). 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 (92,93). 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 unintentionally swallow the flea (94,95). Animal parasites also can infect humans who ingest soil or other materials contaminated with animal feces. Parasite control through veterinary care and proper husbandry combined with hand washing reduces the risks associated with ecto- and endoparasites (96).

Tuberculosis (TB) is another disease of concern in certain animal settings. In 1996, a total of 12 circus elephant handlers at an exotic animal farm in Illinois were infected with Mycobacterium tuberculosis, and one handler had signs consistent with active disease after three elephants died of TB. Medical history and testing of the handlers indicated that the elephants had been a probable source of exposure for most of the human infections (97). During 1989--1991 at a zoo in Louisiana, seven animal handlers who were previously negative for TB tested positive after a Mycobacterium bovis outbreak in rhinoceroses and monkeys (98). In 2003, the U.S. Department of Agriculture (USDA) developed guidelines regarding removal of TB-infected animals from public contact as a result of concerns over the risk for exposure to the public (99).

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 are frequently available for petting afterwards. Q fever (Coxiella burnetii), leptospirosis, listeriosis, brucellosis, and chlamydiosis are serious zoonoses that can be acquired through contact with reproductive materials (100).

Coxiella 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 that might 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 patients and 41 hospitalizations was linked to goats and sheep giving birth at petting zoos in indoor shopping malls (101). Indoor-birthing exhibits might pose an increased risk for Q fever transmission attributed to inadequate ventilation.

Chlamydophila psittaci infections cause respiratory disease (commonly called psittacosis) and are usually acquired from psittacine birds (102). For example, an outbreak of C. psittaci pneumonia occurred among the staff at the Copenhagen, Zoological Garden (103). On rare occasions, chlamydial infections acquired from sheep, goats, and birds result in reproductive problems in humans (102,104,105).

Recommendations

Guidelines from multiple organizations contributed to the recommendations in this report (106--108). No federal laws in the United States address the risk for transmission of pathogens at venues where the public has contact with animals. Certain states have specific legislation for venues where animals are present in public settings (59,61,109--111). In 2005, after a state fair outbreak, North Carolina passed a law requiring agricultural fairs to obtain a permit from the Department of Agriculture for all animal exhibits open to the public (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 (112). In accordance with the Animal Welfare Act, USDA licenses and inspects certain animal exhibits for humane treatment of animals; however, the act is not intended for human health protection. In 2001, CDC issued guidelines to reduce the risk for infection with enteric pathogens from farm visits (61). CDC also has issued recommendations for preventing transmission of Salmonella from reptiles to humans (113). The Association for Professionals in Infection Control and Epidemiology (APIC) developed guidelines to address risks associated with the use of service animals in health-care settings (2).

Recommendations for Local, State, and Federal Agencies

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

  • Disseminate this report to venue operators. Most states do not have a complete list of animal contact venues (59). 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 (109,110,114).
  • Encourage or require oversight to ensure compliance with recommendations at animal contact venues.

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

  • Conduct thorough epidemiologic investigations of outbreaks.
  • Include questions about exposure to animals and their environment on disease report forms and outbreak investigation questionnaires.
  • Follow appropriate protocols for sampling of humans, animals, and the environment and for testing and subtyping of isolates.
  • Report outbreaks to state health departments and CDC.

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 (12). 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:

  • Know the risks for disease and injury associated with animals and be able to explain risk-reduction measures to staff and visitors.
  • Be familiar with and implement the recommendations contained in this report.
  • Consult with state and local agencies and county extension agents on implementation of the recommendations.
  • Develop or obtain training and education materials and train staff.
  • Assure 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 (Appendix 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 they can educate participants before the visit.
     

Venue staff should:

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

Recommendations for Managing Public and Animal Contact

The recommendations in this report were developed for settings in which direct animal contact is encouraged (e.g., petting zoos) 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. The public's contact with animals should occur in settings where measures are in place to reduce the potential for injuries or disease transmission and to increase the probability that incidents or problems identified with animal contact settings will be reported, documented, and handled appropriately.

The design of facilities and animal pens (Figure) should minimize the risk associated with animal contact, including contact with manure, and should encourage 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 interaction areas. Temporary exhibits should be carefully planned, designed, and managed to avoid problems identified from previous outbreaks. Common problems include inadequate barriers, floor surfaces that are difficult to keep clean, insufficient plumbing, and inadequate hand-washing facilities (12,17,34,35). Specific guidelines might be necessary for certain settings (i.e., schools [Appendix D]).

Recommendations for cleaning procedures also 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., half a cup of 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 at http://www.cfsph.iastate.edu/BRM/resources/disinfectants/Disinfection101Feb2005.pdf. All compounds require a contact time of >10 minutes.

The venue 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 both entrances and exits to animal areas), and animal areas (where animal contact is possible or encouraged) (Figure).

Nonanimal Areas

Nonanimal areas are those in which animals are not permitted.

  • 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. One-way visitor flow is preferred with separate entrance and exit points. The transition areas should be designated as clearly as possible, even if they must be 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.
  • Instruct visitors not to eat, drink, smoke, place their hands in their mouth, or use bottles or pacifiers while in the animal area.
  • Exclude strollers, food, and beverages (establish storage or holding areas for these items).
  • Control visitor traffic to avoid overcrowding.

Exit transition areas should be designed to facilitate hand washing.

  • Post signs or otherwise instruct visitors to wash their hands.
  • Provide accessible hand-washing stations for all visitors, including children and persons with disabilities (Figure).
  • Position venue staff near exits to encourage compliance with hand washing.

Animal Areas

  • Provide adequate ventilation for both animals (115) and humans.
  • Exclude food and beverages. Animal feed and water should not be accessible to the public.
  • Exclude toys, pacifiers, spill-proof cups, baby bottles, and strollers.
  • Prohibit smoking.
  • 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 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.
  • Supervise children closely to discourage hand-to-mouth activities (e.g., thumb-sucking), contact with manure, and contact with soiled bedding. If hands become soiled, supervise hand washing.
  • Assign trained staff to encourage appropriate human-animal interactions, to identify and remove potential risks for patrons (e.g., by promptly cleaning up wastes), and to process reports of injuries and exposures.
  • 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 persons (e.g., ice cream cones) to prevent children from eating food that has come into contact with animals.
  • Use animals or animal products (e.g., animal pelts, animal waste, and owl pellets) (65) for educational purposes only in designated animal areas (Figure). Animals and animal products should not be brought into school cafeterias and other food-consumption areas.
  • Do not use animal areas for public (nonanimal) activities. Zoonotic pathogens can contaminate the environment for substantial periods of time (38). If animal areas must be used for public events (e.g., weddings and dances), these 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 animals 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 injuries from animal contacts can be reduced by carefully managing the specific animals used for such contacts. These 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. Animals should be housed to minimize stress and overcrowding, which can increase shedding of pathogens.
  • Veterinary care: Retain and use the services of a licensed veterinarian. Vaccination, preventive care, 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 TB in elephants (97-99) and primates, and for Q fever in ruminants in birthing exhibits (116,117).
  • Rabies: All animals should be housed to reduce potential exposures from wild animal rabies reservoirs. Mammals should also be up-to-date on their rabies vaccinations (118). 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 used in a setting where public contact occurs (e.g., goats, swine, llamas, and camels), consultation with a veterinarian is recommended regarding the off-label use of rabies vaccine. Use of off-label vaccine cannot provide the same level of assurance as vaccines labeled for use in particular species; however, off-label use of vaccine might provide protection for certain animals and thus decrease the probability of rabies transmission. 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 only if additional restrictive measures are available to reduce risks. These measures can include using only animals that were born to vaccinated mothers and housed to avoid rabies exposure.
  • Dangerous animals: Because of their strength, unpredictability, venom, or the pathogens that they might carry, prohibit certain domestic, exotic, or wild animals 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/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. 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 is preferable. If held indoors, ventilation should be maximized.

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 on immunosuppressive therapy). Persons at high risk 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 uses 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 these settings in which treated municipal water is not available should consider alternative methods for disinfection of their water supply or should consider methods to disinfect their water supply.

References

  1. Steinmuller N, Demma L, Bender JB, Eidson M, Angulo FJ. Outbreaks of enteric disease associated with animal contact: not just a foodborne problem anymore. Clin Infect Dis 2006;43:1596--602.
  2. Duncan SL. APIC State-of-the-art report: the implications of service animals in health care settings. Am J Infect Control 2000;28: 170--80.
  3. Sehulster L, Chinn R, Arduino M, et al. Guidelines for environmental infection control in health-care facilities: recommendations of CDC and the Healthcare Infection Control Practices Advisory Committee (HICPAC). Chicago, IL: American Society for Healthcare Engineering/American Hospital Association, 2004. Available at http://www.cdc.gov/ncidod/dhqp/pdf/guidelines/enviro_guide_03.pdf.
  4. Guay DR. Pet-assisted therapy in the nursing home setting: potential for zoonosis. Am J Infect Control 2001;29:178--86.
  5. National Association of State Public Health Veterinarians. Compendium of veterinary standard precautions, zoonotic disease prevention in veterinary personnel, 2006. Available at http://www.nasphv.org/Documents/VeterinaryPrecautions.pdf.
  6. LeJeune JT, Davis MA. Outbreaks of zoonotic enteric disease associated with animal exhibits. J Am Vet Med Assoc 2004;224:1440--5.
  7. Chappell CL, Okhuysen PC, Sterling CR, DuPont HL. Cryptosporidium parvum: intensity of infection and oocyst excretion patterns in healthy volunteers. J Infect Dis 1996;173:232--6.
  8. Bell BP, Goldoft M, Griffin PM, et al. A multistate outbreak of Escherichia coli O157:H7-associated bloody diarrhea and hemolytic uremic syndrome from hamburgers: the Washington experience. JAMA 1994;272:1349--53.
  9. Tilden J, Jr., Young W, McNamara AM, et al. A new route of transmission for Escherichia coli: infection from dry fermented salami. Am J Public Health 1996;86:1142--5.
  10. Shukla R, Slack R, George A, Cheasty T, Rowe B, Scutter J. Escherichia coli O157 infection associated with a farm visitor centre. Commun Dis Rep CDR Rev 1995;5:R86--R90.
  11. Sayers G, Dillon M, Connolly E, et al. Cryptosporidiosis in children who visited an open farm. Commun Dis Rep CDR Rev 1996;6:R140--R144.
  12. CDC. Outbreaks of Eschericia coli O157:H7 associated with petting zoos---North Carolina, Florida, and Arizona, 2004 and 2005. MMWR 2005;54:1277--80.
  13. Crump JA, Sulka AC, Langer AJ, et al. An outbreak of Escherichia coli O157:H7 infections among visitors to a dairy farm. N Engl J Med 2002;347:555--60.
  14. David ST, MacDougall L, Louie K, et al. Petting zoo-associated Escherichia coli O157:H7---secondary transmission, asymptomatic infection, and prolonged shedding in the classroom. Can Commun Dis Rep 2004;30:173--80.
  15. Durso LM, Reynolds K, Bauer N, Jr., Keen JE. Shiga-toxigenic Escherichia coli O157:H7 infections among livestock exhibitors and visitors at a Texas County Fair. Vector Borne Zoonotic Dis 2005;5:193--201.
  16. Evans M, Gardner D. Cryptosporidiosis outbreak associated with an educational farm holiday. Commun Dis Rep CDR Rev 1996; 1996:R50--R51.
  17. Friedman CR, Torigian C, Shillam PJ, et al. An outbreak of salmonellosis among children attending a reptile exhibit at a zoo. J Pediatr 1998;132:802--7.
  18. Kiang KM, Scheftel JM, Leano FT, et al. Recurrent outbreaks of cryptosporidiosis associated with calves among students at an educational farm program, Minnesota, 2003. Epidemiol Infect 2006;134:878--86.
  19. Pritchard GC, Willshaw GA, Bailey JR, Carson T, Cheasty T. Verocytotoxin-producing Escherichia coli O157 on a farm open to the public: outbreak investigation and longitudinal bacteriological study. Vet Rec 2000;147:259--64.
  20. Smith KE, Stenzel SA, Bender JB, et al. Outbreaks of enteric infections caused by multiple pathogens associated with calves at a farm day camp. Pediatr Infect Dis J 2004;23:1098--104.
  21. Warshawsky B, Gutmanis I, Henry B, et al. An outbreak of Escherichia coli O157:H7 related to animal contact at a petting zoo. Can J Infect Dis 2002;13:175--81.
  22. Chapman PA, Cornell J, Green C. Infection with verocytotoxin-producing Escherichia coli O157 during a visit to an inner city open farm. Epidemiol Infect 2000;125:531--6.
  23. CDC. Salmonella hadar associated with pet ducklings---Connecticut, Maryland, and Pennsylvania, 1991. MMWR 1992;41:185--7.
  24. CDC. Salmonella serotype Montevideo infections associated with chicks---Idaho, Washington, and Oregon, spring 1995 and 1996. MMWR 1997;46:237--9.
  25. Keene W, deBroekert M, Gillette K. A large Escherichia coli O157:H7 outbreak at a county fair [Abstract 55:77]. In: Programs and abstracts of the International Conference on Emerging Infectious Diseases; February 29--March 3, 2004; Atlanta, GA; 2004.
  26. CDC. Salmonellosis associated with chicks and ducklings---Michigan and Missouri, Spring 1999. MMWR 2000;49:297--9.
  27. Swanson SJ, Snider C, Braden CR, et al. Multidrug-Resistant Salmonella enterica Serotype Typhimurium Associated with Pet Rodents. N Engl J Med 2007;356:21--8.
  28. Keen JE, Elder RO. Isolation of shiga-toxigenic Escherichia coli O157 from hide surfaces and the oral cavity of finished beef feedlot cattle. J Am Vet Med Assoc 2002;220:756--63.
  29. Djuretic T, Wall PG, Nichols G. General outbreaks of infectious intestinal disease associated with milk and dairy products in England and Wales: 1992 to 1996. Commun Dis Rep CDR Rev 1997;7: R41--R5.
  30. Korlath JA, Osterholm MT, Judy LA, Forfang JC, Robinson RA. A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 1985;152:592--6.
  31. Sharp JC. Infections associated with milk and dairy products in Europe and North America, 1980--85. Bull World Health Organ 1987;65:397--406.
  32. Payne CJ, Petrovic M, Roberts RJ, et al. Vero Cytotoxin-producing Escherichia coli O157 gastroenteritis in farm visitors, North Wales. Emerg Infect Dis 2003;9:526--30.
  33. Anonymous. Waterborne outbreak of gastroenteritis associated with a contaminated municipal water supply, Walkerton, Ontario, May--June 2000. Can Commun Dis Rep 2000;26:170--3.
  34. Bopp DJ, Sauders BD, Waring AL, et al. Detection, isolation, and molecular subtyping of Escherichia coli O157:H7 and Campylobacter jejuni associated with a large waterborne outbreak. J Clin Microbiol 2003;41:174--80.
  35. CDC. Outbreak of Escherichia coli O157:H7 and Campylobacter among attendees of the Washington County Fair---New York, 1999. MMWR 1999;48:803--5.
  36. Croft DR, Archer J, Roberts C. Johnson, et al. Outbreak of Escherichia coli O157:H7 infections associated with a pancake breakfast served in a stock pavilion with contaminated livestock bedding---Wisconsin, 2001. In: Programs and abstracts of the 51st Annual Epidemic Intelligence Conference (EIS); April 22--26, 2002; Atlanta, GA; 2002.
  37. Doorduyn Y, Van Den Brandhof WE, Van Duynhoven YT, Wannet WJ, Van Pelt W. Risk factors for Salmonella Enteritidis and Typhimurium (DT104 and non-DT104) infections in The Netherlands: predominant roles for raw eggs in Enteritidis and sandboxes in Typhimurium infections. Epidemiol Infect 2006;134:617--26.
  38. Varma JK, Greene KD, Reller ME, et al. An outbreak of Escherichia coli O157 infection following exposure to a contaminated building. JAMA 2003;290:2709--12.
  39. Keen JE, Wittum TE, Dunn JR, Bono JL, Durso LM. Shiga-toxigenic Escherichia coli O157 in agricultural fair livestock, United States. Emerg Infect Dis 2006;12:780--6.
  40. Kudva IT, Blanch K, Hovde CJ. Analysis of Escherichia coli O157:H7 survival in ovine or bovine manure and manure slurry. Appl Environ Microbiol 1998;64:3166--74.
  41. LeJeune JT, Besser TE, Hancock DD. Cattle water troughs as reservoirs of Escherichia coli O157. Appl Environ Microbiol 2001;67:3053--7.
  42. Maule A. Survival of verocytotoxigenic Escherichia coli O157 in soil, water and on surfaces. J Appl Microbiol 2000;88:S71--S8..
  43. Rahn K, Renwick SA, Johnson RP, et al. Persistence of Escherichia coli O157:H7 in dairy cattle and the dairy farm environment. Epidemiol Infect 1997;119:251--9.
  44. Randall LP, Wray C, Davies RH. Survival of verocytotoxin-producing Escherichia coli O157 under simulated farm conditions. Vet Rec 1999;145:500--1.
  45. Corrier DE, Purdy CW, DeLoach JR. Effects of marketing stress on fecal excretion of Salmonella spp in feeder calves. Am J Vet Res 1990;51:866--9.
  46. Hurd HS, McKean JD, Griffith RW, Wesley IV, Rostagno MH. Salmonella enterica infections in market swine with and without transport and holding. Appl Environ Microbiol 2002;68:2376--81.
  47. Hurd HS, McKean JD, Wesley IV, Karriker LA. The effect of lairage on Salmonella isolation from market swine. J Food Prot 2001;64: 939--44.
  48. Isaacson RE, Firkins LD, Weigel RM, Zuckermann FA, DiPietro JA. Effect of transportation and feed withdrawal on shedding of Salmonella typhimurium among experimentally infected pigs. Am J Vet Res 1999;60:1155--8.
  49. Marg H, Scholz HC, Arnold T, Rosler U, Hensel A. Influence of long-time transportation stress on re-activation of Salmonella typhimurium DT104 in experimentally infected pigs. Berl Munch Tierarztl Wochenschr 2001;114:385--8.
  50. US Department of Agriculture. Escherichia coli O157 in the United States feedlots. Fort Collins, CO: US Department of Agriculture, Centers for Epidemiology and Animal Health, Animal and Plant Health Inspection Service, Veterinary Services; 2001. Available at http://www.aphis.usda.gov/vs/ceah/ncahs/nahms/feedlot/Feedlot99/FD99ecoli.pdf..
  51. Williams LP, Newell KW. Salmonella excretion in joy-riding pigs. Am J Public Health Nations Health 1970;60:926--9.
  52. Webb CR. Investigating the potential spread of infectious diseases of sheep via agricultural shows in Great Britain. Epidemiol Infect 2006;134:31--40.
  53. Garber LP, Wells SJ, Hancock DD, et al. Risk factors for fecal shedding of Escherichia coli O157:H7 in dairy calves. J Am Vet Med Assoc 1995;207:46--9.
  54. Hancock DD, Besser TE, Kinsel ML, Tarr PI, Rice DH, Paros MG. The prevalence of Escherichia coli O157.H7 in dairy and beef cattle in Washington state. Epidemiol Infect 1994;113:199--207.
  55. Hancock DD, Besser TE, Rice DH, Herriott DE, Tarr PI. A longitudinal study of Escherichia coli O157 in fourteen cattle herds. Epidemiol Infect 1997;118:193--5.
  56. US Department of Agriculture. Salmonella in United States feedlots. Fort Collins, CO: US Department of Agriculture, Centers for Epidemiology and Animal Health, Animal and Plant Health Inspection Service, Veterinary Services; 2001. Available at http://www.aphis.usda.gov/vs/ceah/ncahs/nahms/feedlot/Feedlot99/FD99salmonella.pdf.
  57. McMillian M, Dunn JR, Keen JE, Brady KL, Jones TF. Human behaviors, hand hygiene, and environmental contamination associated with petting zoos. In: Programs and abstracts of the International Conference on Emerging Infectious Diseases; March 19--22, 2006; Atlanta, GA; 2006.
  58. Keen JE, Durso LM, Meehan TP. Isolation of Salmonella enterica and Shiga-toxigenic Escherichia coli O157 from feces of animals in public contact areas of United States zoological parks. Appl Environ Microbiol 2007;73:362--5.
  59. Bender JB, Shulman SA. Reports of zoonotic disease outbreaks associated with animal exhibits and availability of recommendations for preventing zoonotic disease transmission from animals to people in such settings. J Am Vet Med Assoc 2004;224:1105--9.
  60. Crump JA, Braden CR, Dey ME, et al. Outbreaks of Escherichia coli O157 infections at multiple county agricultural fairs: a hazard of mixing cattle, concession stands and children. Epidemiol Infect 2003;131:1055--62.
  61. CDC. Outbreaks of Escherichia coli O157:H7 infections among children associated with farm visits---Pennsylvania and Washington, 2000. MMWR 2001;50:293--7.
  62. Chertow D. Outbreak of Escherichia coli O157:H7 related to direct and indirect animal contact in petting zoos---Florida, 2005. In: Programs and abstracts of the 55th Annual Epidemic Intelligence Service Conference; April 24--28, 2006; Atlanta, GA; 2006.
  63. North Carolina Department of Health and Human Services. E. coli outbreak. Raleigh, NC: North Carolina Department of Health and Human Services; 2004. Available at http://www.epi.state.nc.us/epi.gcdc/ecoli/EColiReportFinal062905.pdf.
  64. Coronado F, Johnson G, Kacica M, Lurie M, Teal A, Root T, Zansky S, Calkins-Lacombe D, Simmerly D, Halse T. A large outbreak of cryptosporidiosis and Escherichia coli O111 infections associated with consumption of unpasteurized apple cider---New York, 2004. In: Programs and abstracts of the 54th Annual Epidemic Intelligence Service Conference; April 11--15, 2005; Atlanta, GA; 2005.
  65. Smith KE, Anderson F, Medus C, Leano F, Adams J. Outbreaks of salmonellosis at elementary schools associated with dissection of owl pellets. Vector Borne Zoonotic Dis 2005;5:133--6.
  66. Kassenborg HD, Hedberg CW, Hoekstra M, et al. Farm visits and undercooked hamburgers as major risk factors for sporadic Escherichia coli O157:H7 infection: data from a case-control study in 5 FoodNet sites. Clin Infect Dis 2004;38:S271--S8.
  67. O'Brien SJ, Adak GK, Gilham C. Contact with farming environment as a major risk factor for Shiga toxin (Vero cytotoxin)-producing Escherichia coli O157 infection in humans. Emerg Infect Dis 2001;7:1049--51.
  68. Haack JP, Jelacic S, Besser TE, et al. Escherichia coli O157 exposure in Wyoming and Seattle: serologic evidence of rural risk. Emerg Infect Dis 2003;9:1226--31.
  69. Hunter PR, Hughes S, Woodhouse S, et al. Sporadic cryptosporidiosis case-control study with genotyping. Emerg Infect Dis 2004;10:1241--9.
  70. Roy SL, DeLong SM, Stenzel SA, et al. Risk factors for sporadic cryptosporidiosis among immunocompetent persons in the United States from 1999 to 2001. J Clin Microbiol 2004;42:2944--51.
  71. Soderlund D, Smith K, Bender J, Hedberg C. An epidemiologic investigation of cryptosporidiosis in Minnesota. In: Programs and abstracts of the International Conference on Emerging Infectious Diseases; July 16--19, 2000; Atlanta, GA; 2000.
  72. Friedman CR, Hoekstra RM, Samuel M, et al. Risk factors for sporadic Campylobacter infection in the United States: a case-control study in FoodNet sites. Clin Infect Dis 2004;38:S285--S96.
  73. Belongia EA, Chyou PH, Greenlee RT, Perez-Perez G, Bibb WF, DeVries EO. Diarrhea incidence and farm-related risk factors for Escherichia coli O157:H7 and Campylobacter jejuni antibodies among rural children. J Infect Dis 2003;187:1460--8.
  74. Bardana EJ Jr. What characterizes allergic asthma? Ann Allergy 1992;68:371--3.
  75. American Academy of Allergy Asthma and Immunology. Executive summary report, 1998. Milwaukee, WI: Task Force on Allergic Disorders, 1998.
  76. Lincoln TA, Bolton NE, Garrett AS, Jr. Occupational allergy to animal dander and sera. J Occup Med 1974;16:465--9.
  77. Siemaszko C. Tiger kills Kansas teen: mauled while posing for pic. New York Daily News. New York, NY, 2005:3.
  78. CDC. Mass treatment of humans exposed to rabies---New Hampshire, 1994. MMWR 1995;44:484--6.
  79. Chang HG, Eidson M, Noonan-Toly C, et al. Public health impact of reemergence of rabies, New York. Emerg Infect Dis 2002;8:909--13.
  80. CDC. Public health response to a potentially rabid bear cub---Iowa, 1999. MMWR 1999;48:971--3.
  81. CDC. Multiple human exposures to a rabid bear cub at a petting zoo and barnwarming---Iowa, August 1999. MMWR 1999;48:761.
  82. CDC. Tularemia associated with a hamster bite---Colorado, 2004. MMWR 2005;53:1202--3.
  83. CDC. Fatal Cercopithecine herpesvirus 1 (B virus) infection following a mucocutaneous exposure and interim recommendations for worker protection. MMWR 1998;47:1073--6,1083.
  84. Cohen JI, Davenport DS, Stewart JA, Deitchman S, Hilliard JK, Chapman LE. Recommendations for prevention of and therapy for exposure to B virus (Cercopithecine herpesvirus 1). Clin Infect Dis 2002;35:1191--203.
  85. Hullinger G, Cole JJ, Elvinger F, Stewart R. Dermatophytosis in show lambs in the United States. Vet Dermatol 1999;10:73--6.
  86. Scott WA. Ringworm outbreak [letter]. Vet Rec 1986;118:342.
  87. Stover J, Dolensek E, Basford B, Beheny J. Contagious Ecthyma in a children's zoo. J Zoo An Med 1986;17:115--6.
  88. Marennikova SS, Maltseva NN, Korneeva VI, Garanina N. Outbreak of pox disease among carnivora (felidae) and edentata. J Infect Dis 1977;135:358--66.
  89. CDC. Update: Multistate outbreak of monkeypox---Illinois, Indiana, Kansas, Missouri, Ohio, and Wisconsin, 2003. MMWR 2003;52: 642--6.
  90. Kile JC, Fleishchauer AT, Kuehnert MJ, et al. Transmission of monkeypox among exposed daycare attendees: Indiana, 2003 [Abstract 51:132]. In: Programs and abstracts of the International Conference on Emerging Infectious Diseases; February 29--March 3; Atlanta, GA; 2004.
  91. Angarano DW, Parish LC. Comparative dermatology: parasitic disorders. Clin Dermatol 1994;12:543--50.
  92. Arlian LG. Biology, host relations, and epidemiology of Sarcoptes scabiei. Annu Rev Entomol 1989;34:139--61.
  93. Scott DW, Horn RT, Jr. Zoonotic dermatoses of dogs and cats. Vet Clin North Am Small Anim Pract 1987;17:117--44.
  94. Currier RW, 2nd, Kinzer GM, DeShields E. Dipylidium caninum infection in a 14-month-old child. South Med J 1973;66:1060--2.
  95. Molina CP, Ogburn J, Adegboyega P. Infection by Dipylidium caninum in an infant. Arch Pathol Lab Med 2003;127:e157--e9.
  96. Schantz PM. Toxocara larva migrans now. Am J Trop Med Hyg 1989; 41:21--34.
  97. Michalak K, Austin C, Diesel S, Bacon MJ, Zimmerman P, Maslow JN. Mycobacterium tuberculosis infection as a zoonotic disease: transmission between humans and elephants. Emerg Infect Dis 1998; 4:283--7.
  98. Stetter MD, Mikota SK, Gutter AF, et al. Epizootic of Mycobacterium bovis in a zoologic park. J Am Vet Med Assoc 1995;207:1618--21.
  99. US National Tuberculosis Working Group for Zoo and Wildlife Species. Guidelines for the control of tuberculosis in elephants, 2003. Riverdale, MD: US National Tuberculosis Working Group for Zoo and Wildlife Species; 2003. Available at http://www.aphis.usda.gov/ac/TBGuidelines2003.pdf..
  100. Heymann D. Control of Communicable Diseases. In: Heymann D, ed. Washington D.C.: American Public Health Association, 2004.
  101. Milford F, Vibien A, Lambert L, Morin M, Petit G, Trottier J. Large Q-fever outbreak related to exposure to petting zoos in two shopping malls. Programs and abstracts of the 51st Annual Conference on Diseases in Nature Transmissible to Man; June 2001; Austin, TX; 2001.
  102. Smith KA, Bradley KK, Stobierski MG, Tengelsen LA. Compendium of measures to control Chlamydophila psittaci (formerly Chlamydia psittaci) infection among humans (psittacosis) and pet birds, 2005. J Am Vet Med Assoc 2005;226:532--9.
  103. Christensen A, Jarlov J, Ingeberg S. The risk of ornithosis among the staff of Copenhagen Zoo. Ugeskr Laeger 1990;152:818--20.
  104. Eidson M. Psittacosis/avian chlamydiosis. J Am Vet Med Assoc 2002;221:1710--2.
  105. Hyde SR, Benirschke K. Gestational psittacosis: case report and literature review. Mod Pathol 1997;10:602--7.
  106. Casemore D. Educational farm visits and associated infection hazards. Commun Dis Rep CDR Rev 1989;19:R3.
  107. Dawson A, Griffin R, Fleetwood A, Barrett NJ. Farm visits and zoonoses. Commun Dis Rep CDR Rev 1995; 5:R81--R6.
  108. Warshawsky B, Henry B, Gutmanis I, et. al. An E. coli O157:H7 outbreak associated with an animal exhibit: Middlesex-London Health Unit investigation and recommendations---executive summary. Vol. 2006. Middlesex, London, Ontario, Canada: Middlesex-London Health Unit; 1999. Available at http://www.healthunit.com/index.asp?mode-article&long=english&articleID=10173&rank=380.
  109. Washington State Department of Health. Recommendations to reduce the risk of disease transmission from animals to humans at petting zoos, fairs and other animal exhibits. Olympia, WA: Washington State Department of Health, Office of Environmental Health and Safety, 2001. Available at http://www.doh.wa.gov/ehp/ts/Zoo/RecommendationsPettingZoo.pdf.
  110. Animal Exhibition Sanitation Act 211 of 2002. Pennsylvania Bureau of Animal Health and Diagnostic Services. (May 6, 2002). Available at http://www.agriculture.state.pa.us/animalhealth/lib/animalhealth/sb1325p1990-e.coli._act_211_of_2002.pdf.
  111. Commonwealth of Massachusetts Department of Public Health. Recommendations for petting zoos, petting farms, animal fairs, and other events and exhibits where contact between animals and people is permitted. Boston, MA: Commonwealth of Massachusetts Department of Public Health, Bureau of Communicable Disease Control; 2004. Available at http://www.mass.gov/dph/cdc/epii/rabies/petzoo.htm.
  112. American Zoo and Aquarium Association. Guide to accreditation of zoological parks and aquariums (and accreditation standards). Silverspring, MD: American Zoo and Aquarium Association; 2005. Available at http://www.aza.org/Accreditation/Documents/AccredStandPol.pdf.
  113. CDC. Reptile-associated salmonellosis---selected states, 1998--2002. MMWR 2003;52:1206--9.
  114. CDC. Healthy pets healthy people. Atlanta, GA: US Department of Health and Human Services, CDC, National Center for Infectious Diseases; 2004. Available at http://www.cdc.gov/healthypets.
  115. Midwest Plan Service. Heating, cooling and tempering air for livestock housing. Ames, IA: Iowa State University; 1990.
  116. McQuiston JH, Childs JE, Thompson HA. Q fever. J Am Vet Med Assoc 2002;221:796--9.
  117. Ross C, Morrow PS. Q fever: an issue in occupational health & safety? An overview of the methods of control and the effects of Coxiella burnetii on the human host. J R Soc Health 1994;114:151--2.
  118. National Association of State Public Health Veterinarians. Compendium of animal rabies prevention and control, 2006. Available at http:// www.nasphv.org/83416/index.html.

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

Co-Chairpersons: Jeffrey B. Bender, DVM, MS, DACVPM, University of Minnesota, St. Paul, MN; Carina Blackmore, DVM, PhD, Florida Department of Health, Tallahassee, FL.

Members: John R. Dunn, DVM, PhD, Tennessee Department of Health, Nashville, TN; Kirk E. Smith, DVM, MS, PhD, Minnesota Department of Health, St. Paul, MN; James H. Wright, DVM, MPVM, DACVPM, Texas Department of State Health Services, Tyler, TX.

Consultants to the Committee: Casey Barton Behravesh, DVM, DrPH, CDC, Atlanta, GA; Sue K. Billings, DVM, MSPH, National Assembly of State Animal Health Officials; James E. Keen, DVM, PhD, U.S. Department of Agriculture, Washington, D.C.; John P. Huntley, DVM, MPH, Council on Public Health and Regulatory Veterinary Medicine, Schaumburg, IL; Timothy F. Jones, MD, Council of State and Territorial Epidemiologists, Atlanta, GA; Thomas P. Meehan, DVM, Association of Zoos and Aquariums, Silver Spring, MD.


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