Airborne transmission of viral and bacterial pathogens has not been adequately addressed in disinfection protocols in animal facilities,1 and respiratory pathogens pose a considerable threat to the health of companion animals in these facilities.2 For example, canine infectious respiratory disease complex (so-called kennel cough) is frequently responsible for high morbidity rates among dogs in animal shelters and boarding facilities. For cats, the 5 most prevalent pathogens that cause URIs are feline herpesvirus-1 (infectious rhinotracheitis virus), feline calicivirus, Bordetella bronchiseptica, Chlamydia felis, and Mycoplasma spp.3 Four of these 5 pathogens are of greatest concern in these facilities,4 and 3 (feline herpesvirus-1 and calicivirus4,5 and B bronchiseptica6) are known or suspected to be transmitted through the air. Inhalation of aerosolized droplets containing respiratory pathogens by susceptible animals is one route for infection, and contact with aerosolized droplets deposited onto surfaces is another source of infection. The ability to remove respiratory pathogens from the air may not only reduce the risk of developing an infection through inhalation but also through contact with contaminated surfaces. Concurrent improvement in husbandry, such as preventing overcrowding, increasing ventilation, and improving air quality, may also reduce the risk.7
Aerosols are suspensions of solid or liquid particles that range in size between 0.01 and 100 μm, may contain hair and shed skin cells, and may be produced by coughing, sneezing, vocalization, and breathing.8,9 Droplets rapidly evaporate after expulsion and can remain airborne for an extended period.10 Pathogens that settle on surfaces may likewise be a source of infection for an extended period, by direct contact and after reaerosolization through activity such as walking,11,12 air movement by HVAC systems, and high-pressure washing of cages.13,14 Among pathogens that can infect cats, feline herpesvirus-1 can survive on surfaces for up to 2 days and calicivirus for 7 days.15 Because many respiratory pathogens can be transmitted through the air, disinfection of recirculated air in animal facilities should measurably and consistently reduce the number of airborne pathogens and therefore the number of URIs.
Ultraviolet germicidal irradiation is effective at disinfecting water, environmental surfaces, and air,16 and systems with UV germicidal irradiation systems added to HVAC systems reduce the number of respiratory tract infections in people.17–20 However, the use of UV germicidal irradiation systems in animal shelters has not previously been reported. Therefore, the purpose of the study reported here was to evaluate the effect of UV germicidal irradiation of the air on the incidence of URIs in kittens in a nursery.
Materials and Methods
Animals
Kittens were estimated to be 4 to 8 weeks old; sometimes nursing queens were also in the nursery. Kittens were admitted to the nursery of the Arizona Humane Society through owner and public surrender and the shelter's kitten bottle-feeding program (at a separate campus). Kittens were examined on entry to the shelter and were not admitted to the nursery if they displayed signs consistent with respiratory illness.
Nursery
The kitten nursery operated from May to November in 2016 and April to November in 2018, the typical months for most kitten births (ie, kitten season). The nursery was a freestanding building on the Arizona Humane Society campus, and its dimensions were approximately 9.5 × 6.7 × 3 m (width × length × height). The nursery did not simultaneously house any other animals during kitten season, and access was limited to employees and volunteers that directly worked with the kittens. Capacity was estimated at 100 kittens. During the offseason, the nursery may have been used as overflow housing for cats in the shelter. However, prior to housing any kittens during kitten season, the nursery was completely emptied and disinfected. The HVAC system provided airflow to all areas of the nursery in accordance with recommended guidelines,4,14,17,21 such that it delivered 1,000 cu ft/min and exchanged the air at a rate of approximately 9 air changes/h (ie, rate for which the complete volume of air inside a building or room of a building is replaced with fresh outside air). A minimum of 5 to 8 air changes/h is recommended for animal care facilities.4
Standard operating protocols for cleaning the nursery were maintained throughout the study, and airflow through the HVAC system was constant whether the UV germicidal irradiation systems were or were not in operation. Generally, cleaning involved the use of detergents and chemical disinfectants, similar to the cleaning methods used in human health-care facilities.22–24 Specifically, protocols involved spot cleaning of the cages when the same animal was returned to the same cage and deep cleaning of the cages when an animal was not returned to the same cage and before a new animal was placed there. A hydrogen peroxide–based disinfectant cleaner was used except for the fourth week of the month, when a degreaser and diluted bleach were used. All staff were required to wear personal protective equipment, including gowns and gloves, when handling animals < 6 months of age. Staff changed their personal protective equipment after handling individually caged animals or cohabitating groups of animals. Standard vaccination, isolation, and treatment protocols were maintained during the study.
In 2017, 2 UV germicidal irradiation systems were installed in the nursery and used in 4-week cycles (ie, on for 4 weeks, off for 4 weeks, etc) until 2018, when the systems were used continuously. One systema was installed in the HVAC system above the evaporator coils, situated so that the UV system irradiated both the air supplied to the nursery and the surface of the evaporator coils. A second systemb with a blower was installed on the ceiling above the nursery, where it irradiated the surrounding (360°) air near the ceiling at an airflow rate of 50 cu ft/min. The combined systems produced a UV dose that was calculated to be able to eliminate > 99% of target bacteria and viruses, including B bronchiseptica, influenza virus, and feline calicivirus, on the basis of their susceptibilities to short-wavelength UV light.16 The UV dose is the product of the irradiance (Watt per square meter) times the exposure time (seconds).
Nursery records were reviewed for kittens in which URIs were diagnosed in 2016, when no UV systems were used, and in 2018, when the UV systems were used continuously. Shelter veterinarians confirmed the presence of URIs on the basis of compatible clinical signs, including sneezing, nasal and ocular discharge, conjunctivitis, subjectively high body temperature, inappetence, and oral ulceration. The numbers of kittens admitted to and housed in the nursery were tabulated. The incidence of URIs was calculated for 2016 and 2018 as the number of URI cases/100 kitten admissions, and the incidence in 2016 was compared with the incidence in 2018.
Statistical analysis
The URI data for 2016 and 2018 were compared by use of the Aspin-Welch unequal variance t test with commercial software.c Values of P < 0.05 were considered significant.
Results
The nursery housed a total of 1,142 kittens during the study periods, with 444 kittens in 2016, when no UV systems were used, and 698 kittens in 2018, when the UV systems were used (Table 1). The overall incidence of URIs in 2016 was 12.4 cases/100 kitten admissions and in 2018 was 1.6 cases/100 kitten admissions, representing a significant (P < 0.029) decrease of 87.1% between the years.
Incidence of URIs among 4- to 8-week-old kittens admitted to and housed in a freestanding nursery of an animal shelter campus that operated from May through November in 2016, when UV germicidal irradiation systems were not used, and April through November in 2018, when UV germicidal irradiation systems were used.
| Year | Month | No. of kittens with URIs | No. of kitten admissions | No. of cases/100 kittens |
|---|---|---|---|---|
| 2016 | May | 3 | 159 | 1.9 |
| Â | Jun | 9 | 50 | 18.0 |
| Â | Jul | 15 | 48 | 31.3 |
| Â | Aug | 2 | 56 | 3.6 |
| Â | Sep | 1 | 41 | 2.4 |
| Â | Oct | 20 | 67 | 29.9 |
| Â | Nov | 5 | 23 | 21.7 |
| Â | Total | 55 | 444 | 12.4 |
| 2018 | Apr | 1 | 99 | 1.0 |
| Â | May | 5 | 215 | 2.3 |
| Â | Jun | 2 | 88 | 2.3 |
| Â | Jul | 3 | 112 | 2.7 |
| Â | Aug | 0 | 48 | 0 |
| Â | Sep | 0 | 73 | 0 |
| Â | Oct | 0 | 61 | 0 |
| Â | Nov | 0 | 2 | 0 |
| Â | Total | 11 | 698 | 1.6 |
Discussion
In the present study, a significant reduction in the incidence of URIs among kittens housed in the nursery was evident in 2018, when the UV germicidal irradiation systems were used, compared with the incidence of URIs in 2016, when the UV systems were not used. These findings suggested that airborne transmission of respiratory pathogens through HVAC systems should be considered in a comprehensive approach to reducing the incidence of URIs in animal shelters. Although the UV systems were installed in 2017, they were only used intermittently (4-week cycles); therefore, 2017 data were not included in the analysis, despite an observed reduction of the incidence of URIs between 2016 and 2017. Rather, the incidence of URIs in 2018, when the UV systems were used continuously, was better compared with the incidence of URIs in 2016, when the UV systems were not used.
In animal shelters, surface cleaning and disinfection plus reducing animal stress have been assumed to be the only approaches necessary for controlling the spread of infections, with the implicit assumptions that air disinfection only plays a minor role and existing ventilation practices (eg, changing air filters and regular inspection and maintenance)4 are sufficient at mitigating the risk of airborne exposure to respiratory pathogens. Therefore, little if any attention has been directed toward air disinfection.
In the present study, the nursery staff followed standard operating protocols for cleaning. However, the quality of cleaning may have varied among staff members, and therefore, the results may have been impacted. Yet kittens in the nursery developed URIs more frequently before the UV systems were used. The concurrent decreased incidence of URI suggested that surface cleaning protocols alone may not have been effective at eliminating airborne respiratory pathogens, and the spread of these pathogens through HVAC systems may be more important than has been previously recognized. Because pathogens that cause nonrespiratory tract infections may also be transmitted through the air and deposited onto surfaces, thereby serving as a source of infection (ie, a fomite), UV germicidal irradiation systems may also reduce the incidence of nonrespiratory tract infections.
The present study had limitations that warrant consideration when interpreting the results. Because 2 to 10 days may elapse between exposure to a respiratory pathogen and the onset of clinical signs,25 kittens may have become infected before admission rather than during their stays. In addition, kittens could have become infected during their stays but may not have developed clinical signs until after their discharge from the nursery. Therefore, a few infections may not have been correctly attributed to the use or nonuse of the UV systems.
Additionally, the difference in the incidence of URIs between 2016 and 2018 may have been partly attributable to other variables such as the admittance of kittens and queens with subclinical respiratory tract infections, the overall health of the cats, the presence and virulence of any of the respiratory pathogens, the duration of stay of each kitten, and the lack of a contemporary control group. Risk of infection increases as the duration of stay in a shelter increases.2 Some kittens may have remained in the nursery longer in 2016 than they did in 2018; however, in both years, most kittens were admitted at 4 weeks of age from the shelter's kitten bottle-feeding program and remained until they were 8 weeks of age. A contemporary control group was not possible because the nursery was a single room with a single HVAC system. Therefore, all kittens were exposed to irradiated air such that a control group could not be isolated from the experimental group.
Definitive diagnoses were also not pursued; therefore, the impact of the UV systems on the incidence of URIs caused by specific pathogens could not be determined. Likewise, the prevalence of specific respiratory pathogens for each year of the study and whether they changed from year to year could not be determined.
Although 2 UV germicidal irradiation systems were used in the present study, the proportional effectiveness of each UV system—the one in the HVAC system or the one attached to the ceiling—could not be assessed. Therefore, additional study is needed to investigate the effectiveness of a single UV system. Importantly, this combination of UV systems was specifically designed for this nursery on the basis of its size, airflow, and existing HVAC system to target the array of possible pathogens to which these kittens may be exposed. Therefore, other animal shelters may have different setups than the one used here.
Because the incidence of URIs was reduced when the UV systems were used, the cost of the systems per kitten per stay could be lower than the cost of care per sick kitten per stay after a nominal payback period. The purchase and installation of the UV systems are 1-time costs, and the cost to power the systems is minimal. Costs, however, were not evaluated in the present study.
Acknowledgments
No external funding was used in this study. The authors declare that there were no conflicts of interest.
The authors thank the Arizona Humane Society for their assistance in conducting this study and Dr. Wladyslaw J. Kowalski for assisting in the design of the UV system and reviewing the manuscript.
ABBREVIATIONS
| HVAC | Heating, ventilation, and air conditioning |
| URI | Upper respiratory tract infection |
Footnotes
PAH-N08 in-duct UV system, PetAirapy LLC, St Charles, Ill.
Zone360 upper air UV system, PetAirapy LLC, St Charles, Ill.
NCSS 11 Data Analysis, NCSS LLC, Kaysville, Utah.
References
1. Kowalski WJ, Learned S. Ultraviolet germicidal irradiation for air and surface disinfection of animal facilities. Report P20190209-23. St Charles, Ill: PetAirapy LLC, 2019.
2. Bannasch MJ, Foley JE. Epidemiologic evaluation of multiple respiratory pathogens in cats in animal shelters. J Feline Med Surg 2005;17:109–119.
3. Litster A, Wu CC, Leutenegger CM. Detection of feline upper respiratory tract disease pathogens using a commercially available real-time PCR test. Vet J 2015;206:149–153.
4. Stull JW, Bjorvik E, Bub J, et al. 2018 AAHA infection control, prevention, and biosecurity guidelines. J Am Anim Hosp Assoc 2018;54:297–326.
5. Pesavento PA, Murphy BG. Common and emerging infectious diseases in the animal shelter. Vet Pathol 2014;51:478–491.
6. Jacobs AA, Chalmers WS, Pasman J, et al. Feline bordetellosis: challenge and vaccine studies. Vet Rec 1993;133:260–263.
7. Crawford C. Respiratory infections in shelters. Maddie's Shelter. Available at: www.maddiesfund.org/respiratory-infections-in-shelters.htm. Accessed Feb 1, 2019.
8. Zhang H, Li X, Ma R, et al. Airborne spread and infection of a novel swine-origin influenza A (H1N1) virus. Virol J 2013;10:204–210.
9. Kowalski WJ. Aerobiological engineering handbook: a guide to airborne disease control technologies. New York: McGraw-Hill Book Co, 2006.
10. Steneroden K. Stationary veterinary clinic biological risk management. Ames, Iowa: The Center for Food Security and Public Health, Iowa State University, 2005.
11. Rosati J, Thornburg J, Rodes C. Resuspension of particulate matter from carpet due to human activity. Aerosol Sci Technol 2008;42:472–482.
12. Paton S, Thompson K-A, Parks SR, et al. Reaerosolization of spores from flooring surfaces to assess the risk of dissemination and transmission of infections. Appl Environ Microbiol 2015;81:4914–4919.
13. Maton A, Daelemans J, Lambrecht J. Some fundamentals concerning the construction of animal houses and the building materials to be used. In: Housing of animals: construction and equipment of animal houses. Developments in agricultural engineering 6. Amsterdam: Elsevier, 1985;25–86.
14. Greene C. Environmental factors in infectious disease. In: Infectious diseases of the dog and cat. Philadelphia: WB Saunders Co, 1990;3–20.
15. Griffin B, Baker HJ. Domestic cats as laboratory animals. In: Fox JG, Anderson LC, Loew FM, et al, eds. Laboratory animal medicine. 2nd ed. San Diego, Calif: Academic Press Inc, 2002;450–482.
16. Kowalski WJ. Ultraviolet germicidal irradiation handbook: UVGI for air and surface disinfection. New York: Springer, 2009.
17. Wells MW, Holla WA. Ventilation in the flow of measles and chickenpox through a community. J Am Med Assoc 1950;142:1337–1344.
18. Riley RL. The ecology of indoor atmospheres: airborne infection in hospitals. J Chronic Dis 1972;25:421–423.
19. Menzies D, Popa J, Hanley JA, et al. Effect of ultraviolet germicidal lights installed in office ventilation systems on workers’ health and wellbeing: double-blind multiple crossover trial. Lancet 2003;362:1785–1791.
20. Escombe AR, Moore DA, Gilman RH, et al. Upper-room ultraviolet light and negative air ionization to prevent tuberculosis transmission. PLoS Med 2009;6:312–322.
21. Clark JD, Baldwin RL, Bayne KA, et al. Animal environment, housing, and management. In: Guide for the care and use of laboratory animals. Washington, DC: National Academy Press, 1996;41–104.
22. Möstl K, Addie DD, Boucraut-Baralon C, et al. Something old, something new: update of the 2009 and 2013 ABCD guidelines on prevention and management of feline infectious diseases. J Feline Med Surg 2015;17:570–582.
23. Besch EL. Environmental quality within animal facilities. Lab Animal Sci 1980;30:385–406.
24. Dvorak G, Petersen C. Sanitation and disinfection. In: Miller L, Hurley KF, eds. Infectious disease management in animal shelters. Ames, Iowa: Wiley Blackwell, 2009;49–60.
25. Hurley KF, Sykes JE. Update on feline calicivirus: new trends. Vet Clin North Am Small Anim Pract 2003;33:759–772.
