Epidemiology and Prevention of Healthcare-Associated Infections Related to Animals in the Hospital

Michael Ben-Aderet

Rekha K. Murthy

In 2019, an American pet industry survey revealed that 68% of U.S. households included a pet, an increase from 58% in 1988, the first year of polling.¹ This year alone Americans are estimated to spend over 75 billion dollars on their pets,¹ confirming that animals play an important part of the lives in our society. Although specific laws regarding the use of service animals in public facilities were established in the United States in 1990, the widespread presence of animals in hospitals, including service animals to assist in patient therapy and research, has resulted in the increased presence of animals in acute care hospitals and ambulatory medical settings. Surveys have shown that, there is substantial variability across healthcare institutions in the roles of animals and policies relating to their presence in the healthcare environment.² This variability of practice is likely related to the lack of strong evidence-based studies on both the risks and the benefits of animals regarding human health.

While it is important to note the relatively low infectious risk of companion animals compared with other emerging trends in hospital infection prevention, there is still a risk and a need for infection control measures to mitigate it. This chapter is a practical guide to infections associated with animal use in hospitals in developed nations and how to prevent them. This chapter will not address challenges with wild animals, animal contamination in hospitals, outpatient issues related to animals nor detail the risk of zoonotic pathogens in the broader sense—as these have been addressed in a more systematic fashion elsewhere.

The nature of human-animal interaction in the hospital is diverse. In general, the most common human-animal contact in U.S. hospitals is in the context of animal-assisted interventions or service animals, though hospitals deal with other possible animal exposures such as patient requests for pet visitation, laboratory requests to use hospital facilities for care of lab animals, or other less common situations.² This chapter will attempt to link the infection control risks and prevention strategies with the specific roles of animals in the hospital as well as reference the recent efforts to formally categorize these roles and provide evidence-based regulation for their use.²

HISTORY

The origin of human domestication of animals for companionship and assistance with tasks and work is older than recorded human history, but it is estimated that the domestication of animals started with dogs between 40 000 and 15 000 years ago, possibly in multiple locations across the world.³ Domestication of cows, pigs, sheep, goats, cats, and other animals has occurred more recently.⁴

The use of domestic animals to assist the sick and disabled has a more recent history, possibly dating back to the Roman empire as evidenced by frescos from the walls of Pompeii. In the modern era, dogs were first used to assist the blind in Paris in the 1780s. Throughout the following century, there were continued sporadic reports of individually trained seeing eye dogs.⁵

The first systematic training of dogs for this purpose began after World War I in Germany, where Dr. Gerhard Stalling trained over 600 guide dogs at his guide dog school in Oldenburg, Germany, primarily to assist veterans blinded by gas warfare. These dogs were also provided to people throughout the world and influenced the worldwide establishment of guide dog schools.⁶ The formal use of dogs for other disability, such as for the hearing impaired or physically disabled, has a more recent history, only becoming widespread during the later decades of the 20th century.⁶

The use of animals specifically for therapy, primarily for patients with psychiatric illness, similarly has a long history, dating back to the 19th century. Since then, animals have been employed in a variety of settings, including prisons, nursing homes, and mental institutions primarily as “socialization” tools. This usage also evolved substantially in the 20th century into the current manifestations of animal-assisted therapies.⁵ Aside from service animals, there are few high-quality studies examining the health benefits of the use of animals in healthcare settings, likely reflecting the difficulty of performing research in this field.²

However, there is emerging research to support benefits of animal companionship. The American Heart Association has stated that pet ownership is likely causally related to reduction in cardiovascular disease,⁷ and the U.S. Centers for Disease Control and Prevention (CDC) endorses pet ownership as having a positive effect on blood pressure, cholesterol levels, and triglyceride levels, as well as on feelings of loneliness, opportunities for exercise and outdoor activities, and increased opportunities for socialization.⁸

EPIDEMIOLOGY OF INFECTIONS ASSOCIATED WITH ANIMALS

A zoonotic illness refers to a disease that is shared between animals and humans.⁹ These illnesses are the primary concern of much of the literature concerning the risks to people posed by animals in public settings. In developed countries, these illnesses are relatively uncommon⁹ and are even less prevalent in the healthcare setting. However, until more definitive information is available, priority should be placed on patient, visitor, and healthcare provider safety and the use of standard infection prevention measures to prevent animal-to-human transmission of these potential pathogens in healthcare settings.

Much like in transmissible human disease, classifying infections by transmission mechanism from animals is useful to help illustrate the logical basis for prevention measures. Transmission of disease from animals to people occurs most commonly via contact (direct or indirect) but may also occur through aerosols or droplets as well (Table 25-1).¹⁰

Contact

Contact with animals includes positive or neutral interactions such as petting, touching, kissing, or being in the direct environment of the animal as well as negative interaction such as biting or scratching.¹⁰ Diseases that can be transmitted by contact include enteric diseases, internal parasites, skin infections, external ectoparasites, and diseases that are consequences of bites or scratches.¹⁰

Enteric bacteria and parasites pose the highest risk of disease transmitted from humans to animals in public settings.¹¹ In the United States in 2012 alone, it was estimated that there were over 400 000 cases of enteric illness attributed to animal contact, almost 5000 hospitalizations, and 76 deaths.¹² Enteric diseases can be transmitted through direct contact with an infected or colonized animal or through environmental contamination. The mechanism of transmission of enteric organisms are fecal-oral, but contact with animal fur, hair, feathers, scales, and saliva can transmit these pathogens due to fecal contamination of the animal or environment.¹⁰ In addition, there have been exposures associated with contaminated animal bedding, cages, environmental surfaces, clothing, shoes, or other objects.¹³^,¹⁴^,¹⁵^,¹⁶ Some enteric pathogens can also persist in the environment for long periods of time, documented up to weeks or months in various outbreak investigations.¹⁷^,¹⁸^,¹⁹ Susceptibility of people to these pathogens is variable but is influenced by human hygiene practices as well as age, gastric acid suppression, and immune status.⁹

Other infections associated with animal contact include other bacterial illnesses such as tularemia, leptospirosis, and brucellosis; internal parasites such as Toxocara, Toxoplasma, or Baylisascaris; ectoparasites such as Sarcoptes mites or fleas; skin infections such as poxviruses (monkeypox, orf, cowpox, etc.); Mycobacterium marinum (from contact with fish tank water) or tinea fungi (ringworm); biteassociated infections such as rabies, Pasteurella multocida, Capnocytophaga, and other oral pathogens; or scratch-associated infections such as Bartonella henselae.¹⁰

Droplet and Aerosol

The droplet-associated zoonotic infection of highest global concern is influenza A virus, especially variant strains associated with pigs and birds. There are reports of infections and outbreaks associated with various strains of avian- or swine-associated influenza, though most of these infections reported in the United States are in individuals who have direct contact with pigs.²⁰ Unfortunately, it has been shown that even apparently healthy pigs and birds may shed influenza virus.²⁰

Notable aerosol transmitted zoonotic illness include Q fever due to the bacteria Coxiella burnetii, especially due to peripartum animals, tularemia due to Francisella tularensis, and psittacosis from Chlamydia psittaci acquired from psittacine birds.¹⁰

Fortunately, most illnesses associated with animal contact are acquired in nonhospital settings in facilities like zoos, petting zoos, pet stores, fairs, and farms.¹⁰

TABLE 25-1 Zoonotic Infection Routes and Infection Classification

*Infection route*	*Infection type*	*Infectious agents (common examples)*
Contact	Enteric bacteria/protozoa Ectoparasites Internal parasites Skin infections Bite-associated infections Scratch-associated infections	STEC, Salmonella, Shigella, Campylobacter, Cryptosporidium, Giardia Scabies, mites, fleas Baylisascaris, Toxoplasma Pox viruses, Mycobacterium marinum Rabies virus, Pasteurella, Capnocytophaga Bartonella henselae
Droplet	Respiratory infection	Influenza, Chlamydia psittaci
Aerosol	Various	Coxiella burnetii, Mycobacterium tuberculosis (in elephants)
STEC, shiga toxin-producing E coli.

In addition to the above zoonotic pathogens, in the healthcare environment, there is also the concern that animals can serve as fomites from acquiring infection or colonization with hospital-acquired multidrug-resistant organisms (MDROs) or opportunistic pathogens (such as Clostridioides difficile) and transmitting them horizontally between patients and/or the environment. In the household setting, studies have shown an interplay between human and animal colonization with bacteria, including pathogens such as methicillin-resistant Staphylococcus aureus (MRSA).²¹ Animals with histories of medical illness and veterinary care may have been exposed to antibiotics and may harbor medically significant multidrug-resistant pathogens such as carbapenem-resistant Enterobacteriaceae (CRE) or Pseudomonas.²² Animal or handler behavior issues can pose a risk to patients, especially those with indwelling devices or disabilities. Finally, there are infection risks associated with animal handlers themselves (similar to any other human visitor to the hospital).

Research animals add an additional complication, as these animals will not be housebroken or behaviorally controlled, and may harbor unique pathogens, based on species or usage in research. Spread of infections from research animals to laboratory workers has been reported, such as ratbite fever (Streptobacillus moniliformis or Spirillum minus) from rats and B virus (herpes B, monkey B virus, herpesvirus simiae) encephalitis from macaque monkeys.⁴⁶^,⁴⁷

The healthcare setting offers unique challenges for preventing spread of infection from animals to people. Hospitalized patients may have altered host defenses that could increase susceptibility to zoonotic infections and/or increase the severity of clinical disease, and the necessity of sterility and hygiene in the hospital increases potential opportunities for infection. Different populations in the hospital will have different degrees of susceptibility to zoonotic illnesses (pregnant patients, pediatrics, neutropenic patients, oncology patients, etc.) and will potentially interact with animals in different ways. In addition, there is greater regulatory and legal oversight and scrutiny of hospitals than other settings where animals might encounter people. While there will be overlap with other uses of animals in nonhospital public settings, some of the use of animals in hospitals will be unique, such as certain animalassisted activities or research animals.

Despite this increased risk, there are few reports of disease outbreaks directly associated with animals in hospitals, and most fail to identify a causal link (Table 25-2). In general, there is no evidence that animals carry any more risk of transmitting infection than do people.³² While there are isolated case reports such as MRSA colonization of the
paws of a cat in a geriatric unit during an MRSA epidemic²⁴ or a therapy dog with MRSA and C difficile colonization,³³ formal studies evaluating the potential risks of zoonotic illness in hospitals are lacking.³²

TABLE 25-2 Studies of Pathogens and Outbreaks Associated With Animals in Healthcare (AHC)

*Author, year (ref. no)*	*Methodology*	*Findings*
Lefebvre et al., 2006²³	Healthy visitation dogs (n = 102) assessed for presence of zoonotic pathogens	Zoonotic agents isolated from 80% of animals including toxigenic C difficile (40.1%), Salmonella spp. (3%), ESBL-producing E coli (4%), Pasteurella spp. (29%), Malassezia pachydermatis (8%), Toxocara canis (2%), and Ancylostoma caninum (2%).
Scott et al., 1988²⁴	Outbreak of methicillin-resistant Staphylococcus aureus (MRSA) on a geriatric ward	Paws and fur of a cat that roamed the ward were heavily colonized by MRSA; the cat was a possible vector for the MRSA transmission.
Lyons et al., 1980²⁵	Outbreak of Salmonella Heidelberg in a hospital nursery	Outbreak traced to infected calves on a dairy farm, where the mother of the index patient lived.
Richet et al., 1991²⁶	Outbreak of Rhodococcus (Gordona) bronchialis sternal surgical site infections after coronary-artery bypass surgery	Outbreak linked to a nurse whose hands, scalp, and vagina were colonized with the pathogen. Skin cultures from two of her three dogs were also positive; however, it was unclear if the dogs were the source for colonizing the nurse or whether the dogs and nurse were colonized from an environmental reservoir.
Chang et al., 1998²⁷	Outbreak of Malassezia pachydermatis in an intensive care nursery	Isolates all 15 case patients, 9 colonized infants, 1 healthcare worker (HCP), and 3 pet dogs owned by HCP were identical. The authors believed it likely that M pachydermatis was introduced into the intensive care nursery from the HCW’s hands after being colonized from pet dogs at home and then persisted in the nursery through patient-topatient transmission. Patient infections included 8 bloodstream infections, 2 urinary tract infections, and 1 meningitis and 4 others with asymptomatic colonization.
Mossovitch et al., 1996²⁸ Snider et al., 1993²⁹	Multiple nosocomial outbreaks of Microsporum canis (ringworm) in newborn nurseries or neonatal ICUs	Person-to-person transmission described in a neonatal ICU outbreak; the source of infection was a nurse likely infected from her pet cat.
Enoch et al., 2005³⁰	Therapy dog screened for MRSA and isolate compared to clinical isolates of MRSA in the hospital	An 11-year-old border collie acquired MRSA in a UK general hospital after visiting care-of-the-elderly wards. All isolates from seven patients with known MRSA on the wards visited by the dog were characterized phenotypically and genotypically. Seven isolates displayed five different PFGE patterns, and all differed from the dog isolate.
Boyle et al., 2019³¹	Two-part study investigating the risk of zoonotic pathogen animal colonization in a university-based AAA program as well as the handlers’ understanding of the risks of zoonoses and their adherence to infection control practices	17 positive screening results from 118 performed, 14 of which were potential pathogens. In part two of the study, 70% of respondents expressed no concerns regarding infectious disease transmission in AAA settings. Despite handler education and guidelines, adherence to infection control practices was lacking.
ESBL, extended-spectrum beta-lactamase; HCP, healthcare provider; RFLP, restriction fragment length polymorphisms; ICU, intensive care unit.