Epidemiology and Infection Prevalence of Coxiella burnetii seropositivity and shedding in farm, pet and feral cats and cambridge.org/hyg associated risk factors in farm cats in Quebec, Canada Original Paper 1 1,2 1,2 1,2 1,3 Cite this article: Cyr J et al (2021). Prevalence J. Cyr , M.-È. Turcotte , A. Desrosiers , D. Bélanger , J. Harel , of Coxiella burnetii seropositivity and shedding D. Tremblay4, A. Leboeuf5, C. A. Gagnon3,4, J.-C. Côté1 and J. Arsenault1,2,3 in farm, pet and feral cats and associated risk factors in farm cats in Quebec, Canada. 1 2 Epidemiology and Infection 149,e57,1–9. Faculté de médecine vétérinaire, Université de Montréal, Saint-Hyacinthe, QC, Canada; Groupe de Recherche en https://doi.org/10.1017/S0950268821000364 Épidémiologie des Zoonoses et Santé Publique (GREZOSP), Université de Montréal, Saint-Hyacinthe, QC, Canada; 3Faculté de médecine vétérinaire, Université de Montréal, Swine and poultry infectious diseases research center Received: 8 October 2020 (CRIPA) – Fonds de Recherche du Québec, Saint-Hyacinthe, QC, Canada; 4Service de diagnostic, Faculté de Revised: 13 January 2021 médecine vétérinaire, Université de Montréal, Saint-Hyacinthe, QC, Canada and 5Ministère de l’Agriculture, Accepted: 2 February 2021 des Pêcheries et de l’Alimentation du Québec, Quebec, QC, Canada Key words: cats; Coxiella burnetii; prevalence; risk factors Abstract Author for correspondence: Cats represent a potential source of Coxiella burnetii, the aetiological agent of Q fever in Julie Arsenault, humans. The prevalence and risk factors of C. burnetii infection in farm, pet and feral cats E-mail: [email protected] were studied in Quebec, Canada, using a cross-sectional study. Serum samples were tested using a specific enzyme-linked immunosorbent assay (ELISA) for the presence of antibodies against C. burnetii, whereas rectal swabs were assayed using real-time quantitative polymerase chain reaction (qPCR) for the molecular detection of the bacteria. Potential risk factors for farm cats were investigated using clinical examinations, questionnaires and results from a con- current study on C. burnetii farm status. A total of 184 cats were tested: 59 from ruminant farms, 73 pets and 52 feral cats. Among farm cats, 2/59 (3.4%) were ELISA-positive, 3/59 (5.1%) were ELISA-doubtful and 1/59 (1.7%) was qPCR-positive. All pets and feral cats were negative to C. burnetii ELISA and qPCR. Farm cat positivity was associated with a posi- tive C. burnetii status on the ruminant farm (prevalence ratio = 7.6, P = 0.03). Our results sug- gest that although pet and feral cats do not seem to pose a great C. burnetii risk to public health, more active care should be taken when in contact with cats from ruminant farms. Introduction Q fever is a zoonotic disease caused by Coxiella burnetii, an obligate intracellular, Gram-negative bacterium [1]. Human Q fever has been documented in many parts of the world [2]. The bacteria can infect a wide range of hosts, including domestic cattle, sheep and goats, companion animals, cats and dogs and several vertebrate and invertebrate wildlife species [1, 3, 4]. Experimental findings have shown that a single bacterium could initiate infec- tion in humans [5]. Although most human infection cases remain asymptomatic or develop flu-like symptoms, fever, myalgia and/or headache, serious acute Q fever may lead to abortion, pneumonia, hepatitis, pericarditis, myocarditis, endocarditis and meningitis, and may further develop into persistent infection [1]. The most common mode of transmission to humans is airborne by inhalation of aerosol particles contaminated with parturient secretions from infected animals [6]. Coxiella burnetii is resistant to drying and can survive in the soil for several weeks [7]. Although human infec- tions have historically been mostly associated with close contact with domestic ruminants [1, 8], cats that live in close proximity to humans are regarded as a potential source of C. burnetii [9–11]. Many studies reported the detection of antibodies against phase I and/or phase II C. burnetii antigens in cat sera [12–15], and some cases of human Q fever were linked with © The Author(s), 2021. Published by exposure to parturient cats [16–19]. Although little is known on the main sources of infection Cambridge University Press. This is an Open in cats, it has been proposed that cats may become infected by consumption of placenta or Access article, distributed under the terms of milk from infected ruminants, consumption of contaminated raw meat intended for pet con- the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), sumption, inhalation from environmental contamination, ingestion of infected prey, or tick which permits unrestricted re-use, bites [3, 20, 21]. Considering evidence supporting that rats could be involved as reservoirs distribution, and reproduction in any medium, for C. burnetii, they could maintain the bacterial infection in preying cats [22]. Some studies provided the original work is properly cited. reported inconsistent differences in the prevalence of C. burnetii infection between client-owned and shelter or stray cats [9, 10, 12]. To the best of our knowledge, no study has been conducted to evaluate the risk of C. burnetii infection in farm cats, which may be more likely to be exposed owing to their close contact with domestic ruminants. In addition, although some studies confirmed the presence of C. burnetii in the reproductive system of Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.93, on 02 Oct 2021 at 15:44:32, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268821000364 2 J. Cyr et al. female cats [10, 11], no study that we know of has used PCR to these areas, clinics were randomly selected and invited to partici- screen cat faeces for the presence and shedding of the bacteria. pate in our study until two clinics by region were recruited. Each The purpose of this study was two-fold: (1) to estimate the clinic was asked to recruit a target of 10 cats. Cats were chosen at prevalence of C. burnetii seropositivity and faecal shedding in each clinic by their respective staff following specific inclusion cats living on farms, in pet cats from households and in feral criteria: (1) the cat was 12 weeks of age or older, (2) the owner cats from an urban environment, and (2) to identify risk factors lived in the MRC as the clinic location, (3) the owner was fluent associated with seropositivity and/or shedding of C. burnetii. in French and (4) the owner provided informed written consent for participation. At the beginning of the study, two additional criteria were used: (1) the cat belonged to the same owner since Methods 2 months of age or younger, and (2) the owner did not move to a new dwelling since owning the cat. However, due to difficul- Study design and cat selection ties in recruiting cats meeting all inclusion criteria, these two cri- A cross-sectional study was performed in 2011 in three regions teria were discarded as they were not expected to be associated (Rimouski-Neigette/La Mitis, Les Maskoutains, Montreal) with cat exposure status, but were rather initially used to allow encompassing four regional county municipalities (MRC), for a lifelong appraisal of the potential risk factors, which was which are administrative areas used in Quebec, Canada then revised to only consider exposures over the last 6 months. (Supplementary Fig. S1). The first two regions included the Sampling was extended to the summer of 2012 to reach the sam- MRC of Rimouski-Neigette and Les Maskoutains, respectively. ple size. Only one cat per client was included in the study. They were mostly rural and were selected for the farm and pet A financial compensation of 20$CAN per sampled cat was cat samplings as part of a concurrent study on C. burnetii in provided to the veterinary clinics. ruminants [23]. Besides, another MRC adjacent to All feral cats were taken from the Montreal region. They were Rimouski-Neigette, ‘La Mitis’, was added for pet cat sampling street cats living in outdoor colonies and caught within the in this region. The MRC of Montreal, which is the largest ‘Trap-Neuter-Release-Maintain Program’ of the Montreal div- urban area in Quebec, Canada, was also included for pet cat sam- ision of the Society for the Prevention of Cruelty to Animals pling and to investigate whether feral cats could represent a source (SPCA). This programme consists of trapping, sterilising, vaccin- of C. burnetii infection in a densely populated city. ation and deworming stray and feral cats and returning them to The selection of cats was based on three distinct categories: farm their colony. Cats were caught using TRU-CATCH© traps (Belle cats, pet cats and feral cats. The target sample size was calculated to Fourche, SD, USA) with food bait under the surveillance of volun- include at least 60 cats per category from a combination of all teers. No financial compensation was given to the SPCA, except regions. This number was estimated using an online calculator that SNAP Feline Triple Tests (IDEXX, Westbrook, ME, USA) [24] to allow the detection of at least one C. burnetii-enzyme-linked were provided to their veterinarian for screening cats for feline immunosorbent assay (ELISA)- or -quantitative polymerase chain immunodeficiency virus (FIV), feline leukaemia virus (FeLV) reaction (qPCR)-positive cat with a confidence level of 95%, assum- and feline heartworm infection. ing a prevalence of at least 5% in each cat category. This approach was chosen given (1) the absence of prior information on the Cat sampling and physical examination expected apparent prevalence in this specific population, (2) the absence of prior information on the diagnostic performance of All farm cat sampling was performed by the research team.