Abstract
Background
Canine infectious respiratory disease complex (CIRDC) is a common respiratory condition typically associated with high-density populations.
Objectives
The objectives of this study were to determine the most common pathogens involved in CIRDC and to identify risk factors (pathogens, environmental exposures) associated with the diagnosis.
Animals and procedure
A prospective, multi-clinic, case-control study was conducted in Canada from April 2017 to May 2018. A total of 110 dogs (74 cases, 36 controls) were enrolled by participating veterinary clinics. Pathogens were detected using a respiratory PCR panel.
Results
Canine parainfluenza virus (CPIV), Bordetella bronchiseptica, and canine respiratory coronavirus (CRCoV) were detected in cases only. According to 2 logistic regression models, detection of CPIV (OR: 14.42; 95% CI: 2.24 to ∞) and CRCoV (OR: 8.64; 95% CI: 1.26 to ∞) were associated with CIRDC disease status. In another model, exposures to multiple-dog gatherings also increased the odds (OR: 3.39; 95% CI: 1.26 to 9.81) of CIRDC diagnosis.
Conclusions
Consistent with other studies, this study determined that CPIV, CRCoV, and B. bronchiseptica were important contributors to CIRDC cases. Detection of CPIV and CRCoV and exposure to areas of dog gatherings were identified as having a role in disease status when evaluated statistically, under the conditions of this study.
RÉSUMÉ
Facteurs de risque du complexe de maladies respiratoires infectieuses canines et agents pathogènes associés à la maladie
Contexte
Le complexe de maladies respiratoires infectieuses canines (CIRDC) est une affection respiratoire courante généralement associée aux populations à forte densité.
Objectifs
Les objectifs de cette étude étaient de déterminer les agents pathogènes les plus courants impliqués dans le CIRDC et d’identifier les facteurs de risque (agents pathogènes, expositions environnementales) associés au diagnostic.
Animaux et procédure
Une étude prospective multi-clinique cas-témoins a été menée au Canada d’avril 2017 à mai 2018. Au total, 110 chiens (74 cas, 36 témoins) ont été recrutés par les cliniques vétérinaires participantes. Les agents pathogènes ont été détectés à l’aide d’un panel de PCR respiratoire.
Résultats
Le virus parainfluenza canin (CPIV), Bordetella bronchiseptica et le coronavirus respiratoire canin (CRCoV) n’ont été détectés que dans les cas. Selon 2 modèles de régression logistique, la détection de CPIV (OR: 14,42; IC à 95 %: 2,24 à ∞) et de CRCoV (OR: 8,64; IC à 95 %: 1,26 à ∞) était associée au statut de la maladie CIRDC. Dans un autre modèle, l’exposition à des rassemblements de plusieurs chiens augmentait également les chances (OR: 3,39; IC à 95 %: 1,26 à 9,81) de diagnostic de CIRDC.
Conclusions
Conformément à d’autres études, cette étude a déterminé que CPIV, CRCoV et B. bronchiseptica étaient des contributeurs importants aux cas de CIRDC. La détection de CPIV et de CRCoV et l’exposition à des zones de rassemblement de chiens ont été identifiées comme ayant un rôle dans le statut de la maladie lorsqu’elles ont été évaluées statistiquement, dans les conditions de cette étude.
(Traduit par Dr Serge Messier)
INTRODUCTION
Canine infectious respiratory disease complex (CIRDC), also known as “kennel cough” and “infectious tracheobronchitis” (1,2), is an infection of the upper respiratory tract characterized by paroxysmal dry cough as well as nasal and ocular discharge, sneezing, and inappetence (2–7). The disease is typically self-limiting, and most animals recover spontaneously, but severe infections or secondary pneumonia can occur (2). Canine infectious respiratory disease complex often occurs in high-density dog populations or situations where there is transient mixing of multiple dogs. Environmental exposures identified as risk factors include boarding kennels (6,8) and veterinary hospitals (1,9). In addition, CIRDC can also occur in the general population (4,6), but specific environmental exposures have not been well investigated in client-owned animals. Canine infectious respiratory disease complex has been associated with a wide range of pathogens, including canine parainfluenza virus (CPIV) (10), canine adenovirus Type 2 (11), canine distemper virus (2,12), Bordetella bronchiseptica (13), canine influenza virus (H3N8, H3N2), canine herpesvirus, canine respiratory coronavirus (CRCoV), Streptococcus equi spp. zooepidemicus, canine pneumovirus, Mycoplasma cynos, and M. canis (4,5,9). Because of the multifactorial nature of CIRDC, it is challenging to understand how pathogens, environmental exposures, and patient demographics have roles in infection, severity of disease, and duration. The objectives of this study were to evaluate the occurrence of common causative agents in dogs with CIRDC and healthy controls, and to identify risk factors (pathogens, environmental exposures) associated with the diagnosis of CIRDC.
MATERIALS AND METHODS
Study design and data collection
A prospective, case-control study design was used. Five primary-care veterinary clinics in British Columbia, Alberta, Ontario, and Quebec were selected because of their affiliations with VCA Canada and practitioners’ willingness to participate in the study.
The projected total sample size of 140 animals was determined based on investigation of a range of scenarios with constant confidence and power values of 95 and 80%, respectively, and with a case to control ratio of 2:1. The projected sample size was expected to be sufficient to detect a minimum odds ratio (OR) between 2 and 2.5 when the proportion of exposed controls varied between 10 and 20%. To meet the necessary sample size, each veterinary clinic aimed to enroll 20 cases and 10 controls. Data collection began in April 2017 and concluded in May 2018.
Dogs were enrolled by veterinarians at each clinic at the time of visit. To be included as a case, a dog must have had an acute cough of duration < 7 d and clinical signs (e.g., cough that was acute, paroxysmal, or honking) typical of CIRDC at the time of visit. A dog was excluded as a case if it had any of the following: i) a chronic cough or a cough lasting > 7 d at the time of visit, ii) treatment with systemic antibiotics in the 2 mo before the visit, iii) comorbidities that could lead to coughing at the time of visit, or iv) oral or intranasal CIRDC vaccines within the 3 wk before the visit. To be included as a control, a dog must have been i) in the same age range as the most recently enrolled case (age ranges are shown in Figure 1), ii) historically healthy for at least 3 mo before the visit, and iii) normal on physical examination. A dog was excluded as a control if it i) had an acute or chronic cough on presentation, ii) had significant illness upon physical examination, iii) was treated with systemic antibiotics in the 2 mo before the visit, or iv) received oral or intranasal CIRDC vaccine within 1 mo before the visit. For every second case, a control was enrolled on the same day from the same clinic. Samples for pathogen detection were collected from the nasal cavity, oropharynx, and conjunctival sac at the time of visit. Nasal swabs were collected using the technique described by Hanson and Tripp (14). Oropharyngeal swabs were collected by rolling a dry Copan swab across the tissues of the deep pharynx. Conjunctival swabs were collected by rolling a dry Copan swab in the conjunctival sac. Pathogens were detected using a PCR-based respiratory panel (T995 — Fast Panel PCR Canine Respiratory Disease Profile; Antech Diagnostics, Fountain Valley, California, USA) that included M. cynos, CPIV, B. bronchiseptica, CRCoV, canine herpesvirus, canine influenza virus (H1N1, H3N8, H5N1), canine adenovirus, canine distemper virus, and S. equi spp. zooepidemicus.
FIGURE 1.
Distributions of age (in years) for cases and controls, with results of univariable exact logistic regression with disease status as the outcome.
Demographic and vaccination status data (within the 3 y before the visit) for each dog were collected via surveys completed by the veterinarian. Collected demographic data included information on animal age, breed, and sex. Vaccination status was also collected, and included whether dogs received vaccines against B. bronchiseptica, CPIV, or canine adenovirus, but was not considered in this report because vaccination patterns of individual animals have high variability with respect to administration route, interval since last vaccination, vaccine composition, and vaccine types. This complicated categorization of vaccination status for discrete pathogens. Environmental risk factor data (within the 2 wk before the visit) were collected via surveys administered to dog owners, and included data regarding visits to specific animal facilities (boarding kennels, day cares, dog parks, veterinary clinics, groomers), as well as the number of times a day the dog went outside into the yard. Owners were provided a free-text box to describe any other exposures between their dog and other dogs.
Data analysis
Descriptive analyses were completed to identify trends in how each risk factor (demographics, pathogens detected, environmental exposures) affected disease status. Exact univariable logistic regressions were run for each risk factor, to identify any statistically significant associations with disease status. Results of univariable analyses were then used to inform the building of the 2 final exact logistic regression models. The 1st model would identify pathogens associated with disease status (pathogen model); the 2nd model would identify environmental exposure associated with disease status (environmental exposure model). A causal diagram was used to guide analysis and provide insight into any potential confounders between disease status and pathogen detection (i.e., exposure in the pathogen model) and environmental exposures (i.e., exposure in the environmental model). For the latter model, a composite variable, “multiple-dog gathering,” was created, based on the reported exposure of dogs to settings in which interaction with other dogs could occur. This included exposure to the following settings: kennels, day cares, dog parks, or groomers. These were the settings in which such exposure could have occurred and for which information was available in this study. Exact logistic regressions were run for both the pathogen and environmental exposure models. The 2 final models were built using a manual, forward-selection approach while taking into consideration the causal model and the logistic rule, which limited the number of potential variables included in the final model (15). Logistic regressions were conducted using Stata 15 statistical software (StataCorp, College Station, Texas, USA). This study was approved by the Research Ethics Board and the Animal Care Committee at the University of Guelph (REB #: 17-05-005).
RESULTS
Descriptive analysis
A total of 110 dogs (74 cases, 36 controls) were enrolled. Missing age data (2 cases, 1 control) were replaced with the median age scores for cases and controls, respectively. Missing breed data or breeds described as “mixed” (15 cases, 7 controls) were replaced with “other.” Missing sex data (2 cases, 1 control) were replaced with “unknown.” A summary of data collected for selected variables is presented in Tables 1, 2, and 3. The distributions of age for cases and controls are presented in Figure 1.
TABLE 1.
Results of descriptive analysis for demographic variables and univariable exact logistic regression with canine infectious respiratory disease complex (CIRDC) status as outcome in a case-control study (2017 to 2018).
| Risk factors | Levels | Cases (n = 74) (%) | Controls (n = 36) (%) | Exact logistic regression | ||
|---|---|---|---|---|---|---|
|
| ||||||
| OR (95% CI) | P-value | Global P-value | ||||
| Demographics | ||||||
| Age range (y) | < 1 | 17 | 3 | |||
| 1 to 3 | 23 | 10 | Not tested | |||
| > 3 to 7 | 17 | 8 | ||||
| > 7 | 17 | 15 | ||||
| Brachycephalic | No | 47 (64) | 27 (75) | Reference | — | |
| Other | 15 (20) | 7 (19) | 1.23 (0.41 to 4.03) | 0.8 | 0.29 | |
| Yes | 12 (16) | 2 (6) | 3.41 (0.68 to 33.61) | 0.13 | ||
| Sex | Spayed female | 23 (31) | 18 (50) | Reference | — | |
| Unknown | 2 (3) | 1 (3) | 1.55 (0.08 to 97.40) | 1 | ||
| Castrated male | 30 (41) | 14 (39) | 1.67 (0.63 to 4.47) | 0.27 | 0.1 | |
| Male | 11 (15) | 0 (0) | 11.21 (1.65 to 8) | 0.01 | ||
| Female | 8 (11) | 3 (8) | 2.06 (0.41 to 13.78) | 0.1 | ||
TABLE 2.
Results of descriptive analysis for pathogens detected and univariable exact logistic regression with canine infectious respiratory disease complex (CIRDC) status as outcome in a case-control study (2017 to 2018).
| Risk factors | Levels | Cases (n = 74) (%) | Controls (n = 36) (%) | Exact logistic regression | ||
|---|---|---|---|---|---|---|
|
| ||||||
| OR (95% CI) | P-value | Global P-value | ||||
| Pathogens detected | ||||||
| Mycoplasma cynos | No | 30 (41) | 19 (53) | Reference | — | 0.31 |
| Yes | 44 (59) | 17 (47) | 1.63 (0.68 to 3.95) | 0.31 | ||
| Canine parainfluenza virus | No | 56 (76) | 36 (100) | Reference | — | < 0.01 |
| Yes | 18 (24) | 0 (0) | 15.86 (2.59 to 8) | < 0.01 | ||
| Bordetella bronchiseptica | No | 69 (93) | 36 (100) | Reference | — | 0.17 |
| Yes | 5 (7) | 0 (0) | 3.42 (0.45 to 8) | 0.17 | ||
| Canine respiratory coronavirus | No | 64 (86) | 36 (100) | Reference | — | 0.02 |
| Yes | 10 (14) | 0 (0) | 7.62 (1.17 to 8) | 0.02 | ||
| Canine herpesvirus | No | 74 (100) | 36 (100) | Assumes 1 value only | — | — |
| Yes | 0 (0) | 0 (0) | — | |||
| Canine distemper virus | No | 74 (100) | 36 (100) | Assumes 1value only | — | — |
| Yes | 0 (0) | 0 (0) | — | |||
| Canine influenza virus (H1N1, H3N8, H5N1) | No | 74 (100) | 36 (100) | Assumes 1 value only | — | — |
| Yes | 0 (0) | 0 (0) | — | |||
| Canine adenovirus | No | 74 (100) | 36 (100) | Assumes 1 value only | — | — |
| Yes | 0 (0) | 0 (0) | — | |||
| Streptococcus equi spp. zooepidemicus | No | 74 (100) | 36 (100) | Assumes 1 value only | — | — |
| Yes | 0 (0) | 0 (0) | — | |||
TABLE 3.
Results of descriptive analysis for environmental risk factors and univariable exact logistic regression with canine infectious respiratory disease complex (CIRDC) status as outcome in a case-control study (2017 to 2018).
| Risk factors | Levels | Cases (n = 74) (%) | Controls (n = 36) (%) | Exact logistic regression | ||
|---|---|---|---|---|---|---|
|
| ||||||
| OR (95% CI) | P-value | Global P-value | ||||
| Environmental risk factors (within past 2 wk) | ||||||
| Kennel | No | 62 (84) | 33 (92) | Reference | — | 0.38 |
| Yes | 12 (16) | 3 (8) | 2.12 (0.52 to 12.50) | 0.38 | ||
| Day care | No | 50 (68) | 33 (92) | Reference | — | 0.01 |
| Yes | 24 (32) | 3 (8) | 5.21 (1.41 to 29.20) | 0.01 | ||
| Dog park | No | 50 (68) | 28 (78) | Reference | — | 0.37 |
| Yes | 24 (32) | 8 (22) | 1.67 (0.62 to 4.90) | 0.37 | ||
| Veterinary clinic | No | 61 (82) | 19 (53) | Reference | — | < 0.01 |
| Yes | 13 (18) | 17 (47) | 0.24 (0.09 to 0.63) | < 0.01 | ||
| Groomer | No | 56 (76) | 34 (94) | Reference | — | 0.02 |
| Yes | 18 (24) | 2 (6) | 5.40 (1.17 to 50.88) | 0.02 | ||
| Multiple-dog gathering | No | 28 | 24 | Reference | — | < 0.01 |
| Yes | 46 | 12 | 3.29 (1.32 to 8.34) | < 0.01 | ||
| Number of times per day outside in yard | 0 to 2 | 12 (16) | 2 (6) | Reference | — | 0.48 |
| 3 to 5 | 36 (49) | 17 (47) | 0.36 (0.04 to 1.89) | 0.32 | ||
| ≥ 6 | 26 (35) | 17 (47) | 0.26 (0.03 to 1.40) | 0.11 | ||
| Contact with other dogs | No contact | 55 (74) | 32 (89) | Reference | — | 0.48 |
| Potential contact | 12 (16) | 1 (3) | 6.89 (0.94 to 307.61) | 0.06 | ||
| Confirmed contact | 7 (9) | 3 (8) | 1.35 (0.28 to 8.68) | 0.74 | ||
Canine parainfluenza virus, B. bronchiseptica, and CRCoV were identified in cases only (Tables 2, 4). Canine influenza virus, canine herpesvirus, and S. zooepidemicus were not detected in any enrolled dogs. Mycoplasma cynos was the only organism (Tables 2, 4) detected in both cases and controls. The most common pattern among cases (35.1%) was detection of M. cynos only, followed by the pattern of no detection of any tested pathogen (25.7%). The maximum number of pathogens detected was 3 and consisted of detection of CPIV, B. bronchiseptica, and M. cynos (4.0%; Table 4).
TABLE 4.
Frequencies of patterns of detected pathogens in a case-control study of canine infectious respiratory disease complex (CIRDC) in Canada (2017 to 2018).
| Total (%) | Mycoplasma cynos (%) | Canine parainfluenza virus (%) | Bordetella bronchiseptica (%) | Canine respiratory coronavirus (%) | # pathogens detected |
|---|---|---|---|---|---|
| Cases | |||||
| 19 (26) | − | − | − | − | 0 |
| 1 (1) | − | − | + | − | 1 |
| 3 (4) | − | − | − | + | 1 |
| 6 (8) | − | + | − | − | 1 |
| 26 (35) | + | − | − | − | 1 |
| 1 (1) | − | + | − | + | 2 |
| 1 (1) | + | − | + | − | 2 |
| 6 (8) | + | − | − | + | 2 |
| 8 (11) | + | + | − | − | 2 |
| 3 (4) | + | + | + | − | 3 |
| Total | |||||
| 74 | 44 (59) | 18 (24) | 5 (7) | 10 (14) | — |
|
| |||||
| Controls | |||||
| 19 (53) | − | − | − | − | 0 |
| 17 (47) | + | − | − | − | 1 |
| Total | |||||
| 36 | 17 (47) | 0 | 0 | 0 | — |
The following pathogens were not detected in any CIRDC case or control animal: canine herpesvirus, canine distemper virus, canine influenza virus (H1N1, H3N8, H5N1), canine adenovirus, Streptococcus equi spp. zooepidemicus.
Risk factors for case status
Results of the univariable exact logistic regression (disease status as outcome) are shown in Figure 1. Results of the multivariable exact logistic regression with disease status as outcome and pathogens or environmental risk factors as predictors are presented in Table 5. Canine parainfluenza virus and CRCoV were associated with disease in the multivariable logistic regression model. With respect to environmental risk factors, exposure to multiple-dog gatherings (OR: 3.39; CI: 1.25 to 9.81) increased the odds of being included as a CIRDC case, whereas a veterinary clinic visit (OR: 0.18; CI: 0.06 to 0.54) decreased the odds of being included as a case, after adjusting for sex.
TABLE 5.
Multivariable exact logistic regression with canine infectious respiratory disease complex (CIRDC) status as the outcome and pathogens (pathogen model) and environmental exposures (environmental exposure model) as predictors.
| Risk factors | Odds ratio (95% CI) | P-value |
|---|---|---|
| Pathogen model | ||
| Canine parainfluenza virus | ||
| + | 14.42 (2.24 to 8) | < 0.01 |
| − | Reference | — |
| Canine respiratory coronavirus | ||
| + | 8.64 (1.26 to 8) | 0.02 |
| − | Reference | — |
| Age (y) | 0.98 (0.88 to 1.10) | 0.76 |
| Male | ||
| + | 6.00 (0.78 to 8) | 0.07 |
| − | Reference | — |
|
| ||
| Environmental exposure model | ||
| Multiple-dog gathering | ||
| + | 3.39 (1.25 to 9.81) | 0.01 |
| − | Reference | — |
| Veterinary clinic | ||
| + | 0.18 (0.06 to 0.54) | < 0.001 |
| − | Reference | — |
| Male | ||
| + | 12.99 (1.75 to 8) | 0.01 |
| − | Reference | — |
DISCUSSION
This study adds to the body of literature indicating that CPIV and CRCoV are associated with disease diagnosis (1,3,4,6,10,16). This emphasizes the important role of CPIV in CIRDC in this study and in other studies (17), though detection of CPIV has also been reported in healthy animals in some settings (18). Bordetella bronchiseptica in this study was detected only in case animals, but detection of B. bronchiseptica could not be identified as significantly associated with CIRDC status via either univariable or multivariable logistic regression. This was likely due to the lack of statistical power to identify association of the magnitude observed in this study. Nonetheless, the importance of B. bronchiseptica for CIRDC development has been identified in other studies (17), and should not be ignored when designing preventive and disease-management strategies. In the current and other studies (19–21), M. cynos was detected in both healthy and diseased dogs. This suggests that M. cynos may be, at best, a component cause, but care must be taken not to overinterpret positive PCR results in dogs with CIRDC, given the high baseline prevalence in healthy dogs. Whether M. cynos is minimally pathogenic or pathogenic only in some circumstances (e.g., patient factors, coinfections) is unclear (8,19).
Not surprisingly, cases were more likely to have been exposed to environmental risk factors (e.g., “multiple-dog gatherings”) than controls, which is in line with the contagious nature of many pathogens involved in CIRDC. Interestingly, exposure to veterinary clinic visits was protective, although veterinary clinics may be crowded with other dogs and thus could be considered multiple-dog gatherings. This could be a true effect (e.g., veterinary hospital visits may be associated with vaccination and/or reduced disease risk due to infection control practices) or the result of a selection bias (e.g., the patterns of visiting veterinary clinics among control owners may be different from those of the source population) or measurement bias (e.g., owners of control animals recall exposures differently than owners of case animals). Because of this, the veterinary clinic visit and multiple-dog gathering variables were kept separate.
This study had several limitations. First, the target sample size was not achieved due to time constraints. Therefore, some existing associations in the source population might have been missed. Second, an attempt was made to age-match every other case to a control dog. Nonetheless, recruitment of younger (< 1 y) dogs as controls was challenging, though the reason for this is unclear. One possibility is that owners of healthy dogs aged < 1 y are less amenable to sampling procedures typically used in sick dogs. Thus, it is possible that owners submitting their young and healthy dogs as controls were different from the source population. This is another reason why age was forced into regression models. Finally, the test used for canine influenza virus was based on H1N1, H3N8, H5N1. Nonetheless, H3N2 canine influenza virus is the dominant, if not sole, canine influenza virus in North America (22). It is therefore possible that some cases of canine influenza virus were missed. Similarly, an understanding of diagnostic sensitivity and specificity of tests for individual pathogens on a test panel would be valuable for interpretation of the occurrence of pathogens and the associations reported in this study. This is not only an important issue for the current study, but it is also important for future studies and is a critical point for making informed clinical decisions. Reporting results of assay accuracy with respect to diagnostic test sensitivity and specificity is therefore warranted.
In conclusion, the results of this study were aligned with previous findings that CPIV, CRCoV, and B. bronchiseptica are important contributors to CIRDC cases in Canada. The roles of CPIV, CRCoV, and exposures to areas where multiple dogs congregate (e.g., boarding kennels, day cares, dog parks, or groomers) were identified as risk factors when evaluated statistically, under the conditions of this study. Information gathered from this study could assist clinicians to better choose empirical therapies and develop appropriate vaccination strategies to address this disease complex.
ACKNOWLEDGMENTS
This publication is part of ZO’s PhD dissertation, supported by the IDEXX Chair in Emerging Technologies and Preventive Healthcare at the University of Guelph. The authors thank the clinicians and staff at VCA Canada Island Animal Hospital, Nanaimo, British Columbia; VCA Canada Calgary North Animal Hospital, Calgary, Alberta; VCA Canada Blue Cross Animal Hospital, Sarnia, Ontario; VCA Canada O’Sullivan Animal Hospital, Barrie, Ontario; and Vet et Nous Hopital Veterinaire St-Eustache Deux-Montagnes, Quebec, for their help with this study. CVJ
Funding Statement
Supported by the IDEXX Chair in Emerging Technologies and Preventive Healthcare at the University of Guelph.
Footnotes
Copyright is held by the Canadian Veterinary Medical Association. Individuals interested in obtaining reproductions of this article or permission to use this material elsewhere should contact Permissions.
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