Prevalence of methicillin-resistant staphylococci in northern Colorado shelter animals

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) and Staphylococcus pseudintermedius (MRSP) have been recognized as significant pathogens in veterinary medicine. There have been documented cases of MRSA infection and colonization in veterinary critical care units, in veterinary personnel, and in equine and feline patients. To date, there have been no studies examining the prevalence of MRSA or MRSP colonization of cats and dogs in animal shelters in the United States. The purpose of the current study was to determine the prevalence of MRSA and MRSP in cats and dogs in a northern Colorado animal shelter. Samples were collected from 200 cats and 200 dogs in an open admission shelter. Each species was divided into 2 smaller groups: 100 dogs or cats housed in the stray ward and 100 dogs or cats housed in the adoption area. Samples were evaluated for the prevalence of MRSA or MRSP, which was verified through aerobic culture and Kirby–Bauer agar disc diffusion to confirm antimicrobial sensitivity. Results revealed MRSA in 0.5% of cat samples, MRSA in 0.5% of dog samples, and MRSP in 3% of dog samples. These results are consistent with previously published prevalence rates for these 2 organisms in non-shelter populations of dogs and cats, indicating that cats and dogs from this Colorado shelter do not appear to pose any greater risk to the public than do cats and dogs in the general pet population.

Methicillin-resistant Staphylococcus aureus (MRSA) is regarded as a significant pathogen in both human and veterinary medicine. It first emerged in human medicine when methicillin resistance was noted in 1961 (Jevons MP: 1961, “Celbenin”-resistant staphylococci. Br Med J 1:124–125. Letter) and was recognized as a significant pathogen in the United States by the 1970s. ¹⁶ Soon thereafter, the pathogen emerged in animal species when it was detected in a dairy cow with mastitis in 1972. ⁴ Since 2005, MRSA has been detected in a variety of species including canine, feline, bovine, and equine patients. ¹⁸ Although S. aureus can colonize and infect companion animal species, the most common commensal staphylococci of canines is Staphylococcus pseudintermedius (formerly S. intermedius). ¹⁸ This is in contrast to human beings, where the most common commensal with pathogenicity is S. aureus. This difference is due to bacterial adherence factors, which are important for colonization and subsequent infection. Consequently, S. aureus colonization rates in cats and dogs typically are low, often recovered from less than 10% of samples, ⁵ as compared to the approximately 30% of human beings that are colonized with S. aureus. ¹⁹

Methicillin-resistant strains are resistant to β-lactam antibiotics. Resistance is mediated by the mecA gene, which encodes for an altered penicillin binding protein (PBP2a). The mecA gene can be transferred horizontally between commensal staphylococci, potentially leading to the development of rapid resistance in multiple staphylococci species. ⁸ Bi-directional transmission of MRSA between human beings and animals has been documented in several cases. ²²

Cases of MRSA infection and colonization have been documented in canine patients in veterinary critical care units, ²³ in veterinary personnel, ⁷ in canines participating in animal-assisted therapy, ¹¹ in equine patients, ¹ and in feline patients. ¹ These are very specific populations, and the findings may not reflect the colonization prevalence in the general community animal population. To date, there have been no studies examining the prevalence of MRSA or methicillin-resistant Staphylococcus pseudintermedius (MRSP) colonization of cats and dogs in animal shelters in the United States. Animal shelters represent a different population of animals from those examined in previous studies and would provide an insight into the level of methicillin-resistant staphylococci colonization within the local pet population, as shelters often provide a broad cross-section of the area animal population. ¹⁵

The emergence of MRSA and MRSP in domestic pets is of particular interest because of the public health consequences and the potential for animals to serve as a reservoir for human beings. It has been hypothesized that MRSA is initially transmitted from human beings to their pets, which leads to the colonization of the pets, which then serve as a source of re-infection to human beings. ² Animals in a shelter may ultimately end up in the homes of a wide range of potential adopters: the healthy individual, the immunocompromised, or homes with young children.

For the current pilot study, samples were collected from 200 cats (100 from the stray ward, 100 from adoptions) and 200 dogs (100 from the stray ward, 100 from adoptions) entering an open admission shelter, from May to August 2009, in northern Colorado. The shelter has an annual intake of approximately 8,800 animals. Animals were examined by 1 of 2 investigators for evidence of skin lesions or other obvious signs of illness such as nasal discharge, sneezing, or evidence of perianal inflammation; any animal that was not apparently healthy or unable to be examined due to temperament was excluded from the study. All animals present at the time of the investigators’ visits were included.

Animal movement in the shelter is as follows. Upon entrance to the shelter, all dogs are placed into kennels in the stray ward. Dogs entering the shelter as strays remain in this ward for at least 5 days. After this mandatory hold period, dogs are evaluated and, if adoptable, are placed on the adoption floor within an average of 3 days. Dogs relinquished by previous owners are evaluated and, if appropriate, enter into the adoption area within an average of 2 days. Cats entering the shelter as strays are placed into the stray holding area and held for a minimum of 5 days. Cats are evaluated and, if adoptable, are placed on the adoption floor within an average of 4 days. Cats relinquished by previous owners are placed in a separate room, accessed through the stray holding area. Relinquished cats suitable for adoption typically are placed on the adoption floor within an average of 3 days.

Sample collection

Sterile cotton-tipped swabs were used to collect nasal and perianal samples from each non-sedated animal. Nasal samples were collected by gently rolling the swab just inside the nares of individual animals. Perianal samples were collected by gently rolling a separate swab around the anus of individual animals. All samples were collected by one of the investigators, placed in Amies medium, and stored at 4°C until transport to the Veterinary Diagnostic Laboratory at Colorado State University (Fort Collins, Colorado) for processing within 12 hr of collection.

Culture techniques

The 2 swabs from individual animals were pooled to increase likelihood of detection, ¹⁰ placed in enrichment broth, ²⁰ and incubated aerobically at 37°C for 24 hr. Swabs then were inoculated on selective, chromogenic media ^a and incubated aerobically at 37°C for up to 48 hr. Staphylococcus aureus and S. pseudintermedius isolates were confirmed via colony morphology, Gram-positive stain, a positive catalase reaction, and a positive coagulase tube test. ⁹ Antimicrobial sensitivity was confirmed via Kirby–Bauer agar disc diffusion using CLSI standards. ³

Of the 200 dogs that were sampled, MRSA was isolated from 0.5% (1/200), and MRSP was isolated from 3% (6/200). The MRSA-positive dog had entered the shelter as a stray and was housed in the stray ward for 3 days prior to sampling. Two of the MRSP-positive samples were obtained from dogs that were housed in the stray ward of the shelter; 1 dog had been relinquished by its previous owner, while the other entered the shelter as a stray. The other 4 MRSP-positive samples were obtained from dogs sampled after their placement on the adoption floor; 1 of these dogs had entered the shelter as a stray, while the other 3 were surrendered by previous owners. The median length of stay in the shelter at the time of sampling for the MRSP dogs was 5 days (range: 1–8).

Of the 200 cats that were sampled, MRSA was isolated from 0.5% (1/200), and MRSP was not isolated from any cat. The MRSA-positive sample was from a 3-month-old kitten, which had been surrendered by the previous owner and was housed in the stray ward of the shelter at the time of sampling. The length of stay at the time of sampling was 2 days. The kitten was housed with 4 littermates, which had been relinquished to the shelter at the same time, and none was positive for MRSA at the time of sampling.

The detection of MRSA in a single dog and a single cat (0.5%) in the current study indicates a very low prevalence of MRSA colonization in the animal shelter population tested and is consistent with previous findings of 1–2% MRSA prevalence in dogs and cats in animal hospitals (Hanselman BA, Anderson M, Kruth S, et al.: 2005, Prevalence of methicillin-resistant Staphylococcus aureus colonization in dogs entering a veterinary teaching hospital. J Vet Intern Med 19:464. Abstract) and 0–0.4% in healthy animals.^1,14 In previous studies of clinically healthy dogs, MRSP prevalence was 0.5%, ¹¹ 1.5%, ²¹ 16.7%, ⁶ and 0%, ¹⁴ and 0% in cats. ¹⁴ The MRSP prevalence in the dogs of the study described herein (3%) is within the range of most studies. However, it is important to note that there are fewer studies evaluating the prevalence of MRSP in various populations as compared to MRSA. Additional studies are needed to determine what an expected prevalence might be.

Animals in the shelter environment may be at increased risk of becoming colonized or diseased with a variety of infectious agents for several reasons including high animal density, potential for nosocomial spread by staff members and volunteers, suboptimal cleaning and disinfectant protocols, the unknown pathogen carriage status of the majority of animals, and the stress of the environment. ¹³ For example, cats sampled for Feline calicivirus (FCV), Felid herpesvirus 1 (FeHV-1), and coronavirus over time while housed in a shelter had increasing prevalence rates for all 3 organisms. ¹⁷ However, in the present study, even though some sampled dogs and cats had been within the shelter for up to 8 days, the prevalence for MRSA and MRSP was low. These data may merely reflect the overall low prevalence. However, it also is possible that these organisms are less likely to spread among animals than FCV, FeHV-1, coronaviruses, and other infectious agents. This hypothesis is supported by the kitten in the current study colonized with a MRSA; the kitten was housed with 4 littermates, all of which were negative for MRSA. The result was similar to a 2010 study that found that dogs housed together in the same kennel did not transmit MRSA to each other. ¹² However, one of the current study limitations is that a convenience sampling was used to select animals without regard to their length of stay in the shelter at the time of sampling. In future work, it would be optimal to sample animals at entry and after a period of time in the shelter to define whether the bacteria are likely to be acquired during a shelter stay. In addition, in future studies, isolates could also be evaluated for the mecA gene.

Overall, the findings of the current study suggest that animals housed in the shelter environment have a lower prevalence of MRSA and MRSP colonization when compared to historical control studies of client-owned dogs and cats. While methicillin-resistant staphylococci are a significant public health concern, results of the present study indicate that shelter animals are likely an uncommon source of infection for shelter personnel or potential adopters. The results are, of course, limited to the individual shelter in the present study, and further studies are necessary to determine if rates were similar across shelters, regions, and other sources of animals including pet stores, breeders, and catteries.

There currently are no shelter-specific MRSA and MRSP control guidelines published by the American Veterinary Medical Association or Centers for Disease Control and Prevention. However, general infection control policies should always be used to attempt to prevent infectious agent transmission among shelter animals and to decrease the likelihood of environmental contamination. Such practices should aid in the control of MRSA and MRSP if the organisms are present in the animals or environment and will help to protect both animal and human populations in the shelter environment.