Preface
The Compendium of Measures to Prevent Disease Associated with Animals in Public Settings has been published by the NASPHV and the CDC since 2005.1–3 This compendium provides standardized recommendations for public health officials, veterinarians, animal venue operators, animal exhibitors, visitors to animal venues and exhibits, teachers, camp operators, and others concerned with control of disease and with minimizing health risks associated with animal contact in public settings. The report has undergone several revisions, and this document updates information provided in the 2013 compendium.3
I. Introduction
Contact with animals in public settings (eg, fairs, educational farms, petting zoos, and schools) provides opportunities for entertainment and education. The NASPHV understands the positive benefits of human-animal contact. However, an inadequate understanding among animal exhibitors and visitors in regard to disease transmission and animal behavior can increase the likelihood of infectious disease exposures, injuries, and other health problems among visitors in these settings. Zoonotic diseases (ie, zoonoses) are diseases shared between animals and humans; many of these diseases are potentially transmitted from animals to people in public animal contact venues (Appendix 1). Of particular concern are instances in which zoonotic disease outbreaks result in numerous people becoming ill. During 1991 through 2005, the number of enteric disease outbreaks associated with animals in public settings increased.4 During 2010 through 2015, approximately 100 human infectious disease outbreaks involving animals in public settings were reported to the CDC (unpublished data, 2017). Such outbreaks have substantial medical, public health, legal, and economic effects.
Although completely eliminating risks from animal contact is not possible, this report provides recommendations for minimizing associated disease and injury. The NASPHV recommends that local and state public health, agricultural, animal health, wildlife, and environmental 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 (eg, animal displays, petting zoos, animal swap meets, pet stores, feed stores, zoological institutions, nature parks, circuses, carnivals, educational farms, livestock birthing exhibits, agricultural fairs, childcare facilities or schools, camps, agritourism venues, live animal markets, and wildlife photo opportunity settings). Managers of these venues should use the information in this report in consultation with veterinarians, public health officials, state and local agriculture officials, or other professionals to reduce risks for disease transmission.
Guidelines to reduce risks for disease from animals in health-care facilities, veterinary facilities, and various other occupational settings as well as from service animals (eg, guide dogs) have been developed.5–12 Although not specifically addressed here, the general principles and recommendations in this report are applicable to these settings.
II. Methods
The NASPHV periodically updates the recommendations to prevent disease associated with animals in public settings. To revise the 2013 compendium,3 the NASPHV Animal Contact Compendium Committee members and external consultants met in Atlanta from October 4 through 6, 2016. The revision process included reviewing literature pertaining to outbreaks and diseases associated with animals in public settings since the previous compendium was published; examining reports of animal contact–associated enteric and nonenteric disease outbreaks from the CDC National Outbreak Reporting System as well as from CDC subject matter experts and state public health veterinarians; reviewing specific input solicited from NASPHV members and committee consultants; and evaluating publications and presentations from experts on specific topics of relevance to the compendium revision process. A committee consensus was required to add or modify existing language or recommendations. The 2017 recommendations reported here have been updated with new information and data on zoonotic disease outbreaks and prevention measures.
III. Background
A. Infectious diseases associated with animals in public settings
1. Diseases transmitted by direct or indirect animal contact
One of the most common routes of disease transmission from animals to people is direct physical contact with the animal, which includes touching, holding, kissing, being bitten, and being scratched. Disease transmission also occurs through indirect contact with an animal through contact with a surface contaminated by the animal's saliva, blood, urine, nasal secretions, feces, or other bodily fluids.
a. Enteric (intestinal) diseases
In 2012, a group of investigators estimated the burden of enteric illness attributable to animal contact in the United States.13 The pathogens included in that study were Campylobacter spp, Cryptosporidium spp, nontyphoidal Salmonella enterica, STEC O157:H7, non–O157 STEC strains, Listeria monocytogenes, and Yersinia enterocolitica. The investigators estimated that 445,213 illnesses, 4,933 hospitalizations, and 76 deaths caused by these pathogens occurred annually as a result of animal contact in all (ie, private and public) settings. Pathogens with the highest proportion of cases attributable to animal contact were Campylobacter spp (17%), Cryptosporidium spp (16%), nontyphoidal S enterica (11%), non–O157 STEC strains (8%), and STEC O157:H7 (6%).
Enteric bacteria and parasites pose the highest risk for human disease from animals in public settings.14 Enteric disease outbreaks among visitors to fairs, farms, petting zoos, and other public settings are well documented.15–40 Cattle, sheep, or goats15,17,20,21,26–28,30,31,34,36,38,40 have typically been identified as sources for infection; however, live poultry,16,41–48 rodents,49–53 reptiles,33,54–60 amphibians,61 and other domestic4,62,63 and wild4 animals also are established sources. Animals that appear healthy can carry pathogens that cause illness in people. A small number of pathogens is often enough to cause illness.64–68
Outbreaks as well as sporadic infections with nontyphoidal S enterica have been associated with animal contact. Animals that present a high risk for human Salmonella spp infections and have been implicated as sources of outbreaks of human illness include poultry (eg, chicks, chickens, and ducklings)16,41–48,69–72; reptiles (eg, turtles, snakes, or lizards)33,54–60,73–80; and amphibians, especially frogs.61,81–83 From 1990 through 2014, 53 disease outbreaks linked to live poultry in the United States have been documented.16,43,69,84 Some of the ill persons in those outbreaks reported contact with live poultry at feed stores,16,43,69 schools or daycare facilities,16,41,69 fairs,69 petting zoos,69 and nursing homes (CDC, unpublished data, 2010). Since 2014, an additional 14 outbreaks and approximately 1,200 cases of illness associated with exposure to live poultry have been documented (CDC, unpublished data, 2017). Preventive measures at the hatchery level and in agricultural feed stores, along with proper handling of live poultry by poultry owners, can help prevent salmonellosis.42
Reptiles and amphibians can carry Salmonella spp and have been linked to numerous outbreaks of human illness. Despite laws banning their sale or distribution in the United States, small turtles (those with shells that measure < 4 inches long) continue to be distributed. From 2006 through 2014, 15 multi-state outbreaks of salmonellosis, comprising 921 reported illnesses (including a fatal case in an infant), have been linked to contact with small turtles and their habitats.56 Salmonella Typhimurium infections have been linked to contact with African dwarf frogs (an aquatic amphibian), their habitats, or water from their habitats. Ill people included those who reported acquiring frogs at carnivals, pet stores, and other retail stores.61,82 Activities associated with increased risk of zoonotic disease transmission from turtles, frogs, and other aquatic animals include direct and indirect contact with the animal, tank, water, filtration equipment, or other tank contents. These findings have implications for risk of infection from aquatic exhibits (eg, aquariums and aquatic touch tanks).
Other animals associated with outbreaks of Salmonella spp infections in people include hedgehogs63,85 and rodents such as hamsters, mice, and guinea pigs.49–53 In all animal species that might harbor Salmonella organisms, it is possible for animals that appear healthy and clean to carry and shed the bacteria in their excreta, which can contaminate their fur, hair, feathers, scales, or skin. Salmonella spp can also be present in environments where animals or animal excreta, fur, hair, feathers, scales, or skin are present (eg, barns, petting zoos, school classrooms, and pet stores). Pet food and treats, which may be present in public settings such as pet stores, fairs, and school classrooms, have been confirmed as sources of human salmonellosis in several instances.86–92
Case-control studies79,93–96 also have associated sporadic enteric infections (ie, those not linked to an outbreak) with animals including reptiles, amphibians, farm animals, and cats. For example, a study95 of sporadic Escherichia coli O157:H7 infections in the United States determined that people who became ill were more likely to have visited a farm with cows than were people who did not become ill. Other investigations identified associations between E coli O157:H7 infection and visiting a farm97 or living in a rural area.98 Results of studies99,100 of cryptosporidiosis in people found that contact with cattle is a risk factor for infection. Another study101 identified consumption of raw milk and contact with farm animals among the factors associated with Campylobacter infection.
(1) Animals shedding enteric pathogens. Animals carrying human enteric pathogens frequently have no signs of illness but can still shed the organisms in feces.102 Removing ill animals, especially those with diarrhea, from public contact is necessary, but this step alone is not sufficient to protect the health of people and other animals. The fact that some pathogens can be shed intermittently and survive for months or years in the environment,103–107 as well as the limitations of laboratory testing, makes attempts to identify and remove infected animals unreliable as means of eliminating the risk for transmission. Antimicrobial treatment cannot reliably eliminate infection or prevent shedding, and it does not protect against reinfection. Antimicrobial use in animals can also prolong shedding and contribute to antimicrobial resistance.108–110
Disease transmission at animal exhibits can be influenced by multiple factors. Stress induced by transportation, confinement, physical crowding, and increased handling increases the likelihood of animals shedding pathogens.111–117 Commingling increases the probability that the shed pathogens will infect other animals.118 Young animals, which are frequently included in settings such as petting zoos, farm visits, and educational programs for children, have a higher prevalence of shedding enteric pathogens such as E coli O157:H7 than do mature animals.119–121 Animal shedding of E coli O157:H7 and Salmonella organisms is highest in the summer and fall,116,121 when traveling animal exhibits, agricultural fairs, and farm or petting zoo visits are commonly scheduled.
(2) Transmission of enteric pathogens to people. Enteric pathogens are primarily transmitted by the fecal-oral route. Because animal fur, hair, feathers, scales, skin, and saliva harbor fecal organisms,122 transmission can occur when people pet, touch, feed, or are licked by animals. Exposure to contaminated materials such as animal bedding, environmental surfaces, clothing, and shoes has also been associated with transmission of pathogens.29,33,35,82,123,124 In addition, illness has resulted from fecal contamination of food,24,125 unpasteurized juice,126 unpasteurized milk,19,127–130 and drinking water.131–134
Young children (ie, < 5 years of age) are considered to be at greater risk for acquiring enteric pathogens from animals than most adults are. One study135 found that certain risk behaviors for disease transmission such as physical contact with animals and hand-to-face contact were more common in children than in adults during petting zoo visits. In addition, young children, elderly adults, and people with weakened immune systems have an increased risk for developing severe illness, compared with healthy individuals outside these groups, when they do become infected.136 Finally, attendees or visitors to animal venues are not the only persons potentially exposed to pathogens; livestock exhibitors have also become infected with E coli O157:H7 in outbreaks at fairs.35
(3) Environmental exposures to enteric pathogens. Disease transmission can occur in the absence of direct animal contact if a pathogen is present in the environment. Outbreaks of enteric illness have been associated with exposure to environments after animals were removed,137 dust in the environment,124 touching or stepping in manure,32 and falling down or sitting on the ground in a petting zoo.32 Ill people have also reported having contact with manure on a fence without having touched an animal.22 In an outbreak of E coli O157:H7 in 2004, the outbreak strain was isolated from shavings collected from a baby stroller and from the shoes of petting zoo visitors.32
Enteric pathogens can persist in contaminated environments for long periods. For example, E coli O157:H7 can survive in soil for months.22,35,102,103,105,107,124,a In a 2009 E coli O157:H7 outbreak associated with rodeo attendance, the outbreak strain was isolated from the rodeo grounds 90 days after the end of the event.22 Other outbreaks have also demonstrated long environmental persistence of pathogens, including E coli O157:H7 recovered from sawdust on the floor of an animal barn up to 42 weeks after a fair.124
b. Internal parasites
Animal parasites can infect people who ingest materials contaminated with animal feces or who ingest or otherwise come into contact with contaminated soil. Exposure to parasites in public settings has led to outbreaks including toxoplasmosis at a riding stable138,139 and cutaneous larva migrans at a children's camp.140 The presence of Toxocara eggs in public parks