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STANDARD ARTICLE
Association between indoor air pollution and respiratory disease
in companion dogs and cats
Chung-Hui Lin
1,2
|
Pei-Ying Lo
1
|
Huey-Dong Wu
3
|
Chinhao Chang
4
|
Lih-Chiann Wang
2
1
National Taiwan University Veterinary
Hospital, National Taiwan University, Taipei,
Taiwan
2
Graduate Institute of Veterinary Clinical
Sciences, School of Veterinary Medicine,
National Taiwan University, Taipei, Taiwan
3
Section of Respiratory Therapy,
Department of Integrated Diagnostics and
Therapeutics, National Taiwan University
Hospital, National Taiwan University, Taipei,
Taiwan
4
Department of Medical Research, National
Taiwan University Hospital, National Taiwan
University, Taipei, Taiwan
Correspondence
Chung-Hui Lin, National Taiwan University
Veterinary Hospital and Graduate Institute
of Veterinary Clinical Sciences, National
Taiwan University, Taiwan, No. 1, Sec 4,
Roosevelt Road, Taipei, Taiwan.
Email: chunghuilin@ntu.edu.tw
Funding information
Ministry of Science and Technology,
Taiwan (MOST 105-2313-B-002-055 -)
Background: Indoor air pollution (IAP) leads to important respiratory morbidity and mortality in
humans. Companion dogs and cats share the same household environment with their owners and
are exposed to IAP.
Hypothesis: Pets with respiratory disease are more commonly exposed to indoor air pollutants in
their homes and to worse air quality than pets without respiratory disease.
Animals: Three hundred and forty-eight animals (230 dogs and 118 cats) were recruited.
Methods: Dogs and cats attending the National Taiwan University Veterinary Hospital were prospec-
tively enrolled over a 12-month period. Questionnaires were collected from pet owners regarding the
status of signs of respiratory problem of animals and air pollutants in their homes. Clinical assessment
was performed by veterinarians on all animals included in the case-control study and the presence/
absence of respiratory disease and diagnoses were recorded. Individual exposure to particulate matter
of 2.5 lm or less (PM2.5) was estimated in the domestic microenvironment of the animals.
Results: Dogs with respiratory disease were more commonly exposed to incense burning than
control dogs (30 versus 13%, P5.045), but household PM2.5 level was not different between
dogs with and without respiratory disease [median 30.8 lg/m
3
, range 10.8-214.2 versus median
38.2 lg/m
3
, range 5.4-69.4, P5.57]. Signalment factors (age, body weight, and body condition
score) instead of IAP factors were associated with respiratory disease in dogs using multivariable
logistic regression. In contrast, household PM2.5 level was significantly higher in cats with respira-
tory disease than in control cats [median 38.6 lg/m
3
, range 17.8-131.2 versus median 27.4 lg/m
3
,
range 15.4-70.0, P5.017]. Cats living in households with PM2.5 >35 lg/m
3
were more likely to
have respiratory disease than those living in households with acceptable levels of PM2.5
(OR 54.13, 95% CI 1.12-15.27, P5.03).
Conclusions and Clinical Importance: The link between IAP and respiratory disease in dogs is
complicated. An unacceptable level of household PM2.5 (>35 lg/m
3
) is significantly associated
with respiratory disease in cats. The effect of IAP on the respiratory health of companion animals
warrants further attention.
KEYWORDS
airway, canine, feline, environmental tobacco smoke, indoor air pollution, one medicine, pm2.5,
respiratory disease, spontaneous disease model
Abbreviations: CI, confidence intervals; ETS, environmental tobacco smoke; IAP, indoor air pollution; OR, odds ratio; PM2.5, particulate matter of 2.5 lm or less;
WHO, World Health Organization
.
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This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in
any medium, provided the original work is properly cited and is not used for commercial purposes. V
C2018 The Authors. Journal of Veterinary Internal Medicine
published by Wiley Periodicals, Inc. on behalf of the American College of Veterinary Internal Medicine.
J Vet Intern Med.2018;1–9. wileyonlinelibrary.com/journal/jvim
|
1
Received: 5 November 2017
|
Revised: 3 February 2018
|
Accepted: 3 April 2018
DOI: 10.1111/jvim.15143
Journal of Veterinary Internal Medicine
1
|
INTRODUCTION
Indoor air pollution (IAP) has been recognized as a worldwide health
threat by the World Health Organization (WHO) for over a decade
and results in acute respiratory effects, worsening of chronic respira-
tory disease, and death in humans.
1–3
Of the millions of deaths asso-
ciated with IAP every year, many occur in children and women, who
spend more time indoors.
1
In urban areas, pet dogs and cats fre-
quently live an indoor lifestyle and share the same household envi-
ronment with their pet owners. Detection of cotinine, nicotine, and
organohalogenated contaminants in the serum, urine, and hair of pet
dogs and cats has shown the existence of indoor pollution exposure
in these companion animals.
4–9
Therefore, the impact of IAP on
respiratory health care shall be an important issue for both human
and veterinary medicine.
To date, few studies have investigated the health effect of IAP on
client-owned dogs and cats. Among various well-known air pollutants,
environmental tobacco smoke (ETS) has long been suspected of caus-
ing or exacerbating some chronic respiratory diseases in the veterinary
literatures, such as feline lower airway disease, canine chronic bronchi-
tis, and canine lymphoplasmacytic rhinitis.
10,11
In a controlled study
using a questionnaire survey, exposure to ETS was not found to be a
significant risk factor for chronic cough in client-owned dogs.
12
Never-
theless, differences on lower airway cytology and pulmonary function
were detected between dogs with and without ETS exposure deter-
mined by serum or urine cotinine concentration.
4,7
The risk of respira-
tory system cancer has also been investigated in dogs, and exposure to
ETS was not found to be a strong risk factor in these earlier
studies.
13–15
However, indoor kerosene or coal combustion was identi-
fied as an important environment risk factor for sinonasal cancer
among pet dogs in one study.
15
Sources other than ETS also contribute to poor indoor air quality.
For instance, byproducts from cooking and numerous household chem-
icals are common indoor environmental hazards.
1,15,16
Moreover,
regionally prevalent household air pollutants in some countries, such as
incense burning for religious use, should also be considered as impor-
tant sources of IAP.
17
Many of these pollutants result in dramatic
increase in particulate matter of 2.5 lmorless(PM2.5),whichcanbe
used as an indicator for air quality level.
16,18
Studies have shown the
adverse effect of PM2.5 on respiratory health in both experimental ani-
mals and human patients,
3,16,19
but little is known about it in compan-
ion dogs and cats.
The aims of our study were to: (1) investigate the association
between the existence of well-known household air pollutants and the
presence of respiratory disease in pets living an indoor lifestyle, (2) esti-
mate air quality by screening PM2.5 level in the domestic microenvir-
onment of pet dogs and cats, and (3) compare the air quality level in
the domestic microenvironment between pets with and without respi-
ratory disease. We hypothesized that the proportion of pets having
respiratory disease is associated with the presence of indoor air
pollutants in their homes, and pets with respiratory disease expose to
worse air quality than pets without respiratory disease.
2
|
MATERIALS AND METHODS
2.1
|
Animals and study design
The study population consisted of client-owned dogs and cats that
attended the National Taiwan University Veterinary Hospital, which is
a teaching hospital located in the middle of Taipei city receiving both
referred and nonreferred cases. Dogs and cats were prospectively
recruited over a 12-month period (August 2016 through July 2017).
Animals with and without respiratory disease were enrolled in a case-
control study if their owners signed an inform consent, joined a written
questionnaire survey, and agreed quantifiable measurement of PM2.5
concentration around the household areas where the animal spent
most of its time. The definition of “signs of respiratory problem”in our
study is having any of the following clinical signs: coughing, sneezing,
reverse sneezing, nasal discharge, noisy breathing, snoring, respiratory
distress, tachypnea, cyanosis, and syncope; the definition of “respira-
tory disease”in our study is having a clinical diagnosis of a disease
involving the respiratory system.
Written questionnaires were collected from the pet owners
regarding the presence or absence of various signs of respiratory prob-
lem as well as the presence or absence of common household air pollu-
tants in their home. Proper instruction or assistance was provided by
veterinarians, veterinary assistants, or veterinary students to help the
owners understand all of the investigated signs of respiratory problem.
Clinical assessment was performed by veterinarians (C-H Lin and P-Y
Lo) on each animal. History taking and thoracic auscultation were car-
ried out on all animals, while further diagnostics such as thoracic radi-
ography, pulmonary function testing, bronchoalveolar lavage with or
without bronchoscopy, echocardiography, or computed tomography
were suggested if there were appropriate indications. Assignment to
the group with or without respiratory disease was determined by the
clinical judgment of the veterinarians according to the findings of the
clinical assessment. Animals with chronic or current respiratory disease
(alone or along with various other diseases) were assigned to the respi-
ratory disease group, whereas animals without current respiratory dis-
ease and history of previous respiratory disease (could be either
healthy or ill) were assigned to the control group. Exclusion criteria
were animals living an outdoor lifestyle (eg, unlimited outdoor access,
no confinement indoors, or having daily activities such as sleeping and
eating outside the house) rather than an indoor lifestyle (eg, having
daily activities such as sleeping and eating inside the house, being con-
fined indoors, and with no or restricted outdoor access), animals that
had moved into the present house for less than 2 months at enroll-
ment, the age of the animal being younger than 1 year old, and lack of
sufficient information for veterinarians to make a judgment of the pres-
ence or absence of respiratory disease.
2
|
Journal of Veterinary Internal Medicine LIN ET AL.
For estimating the prevalence of signs of respiratory problem and
household air pollutants, additional written questionnaires (not for the
animals enrolled in the case-control study) were collected from the pet
owners who visited the hospital for various purposes. There was no
requirement for interviewing with veterinarians while answering the
questionnaire and assistance was provided only if the owners
requested it. Questionnaires for estimating the prevalence were
excluded from analysis if more than 50% of the responses were miss-
ing, more than one questionnaire had been filled in for the same animal
(medical record number and signalment information were examined), or
questions had been answered with inappropriate responses (eg, multi-
ple boxes were checked for single choice questions).
2.2
|
Questionnaire for household air pollutants and
signs of respiratory problem
The existence of well-known and regionally popular household air pol-
lutants were investigated through a written questionnaire. The ques-
tionnaires for both case-control study and prevalence estimation used
identical questions. The pet owners responded to questions about the
presence or absence of “long-term or intermittent exposure to second-
hand smoke,”“cooking behavior/cooking fume exposure,”“incense
burning for religious use,”and “frequent use of household chemicals
(eg, paint)”in their homes by checking boxes on the questionnaire. If an
owner selected there was the existence of second-hand smoke in the
house, a following question regarding three different exposure levels
(“always,”“often,”“occasionally”) was offered. In addition to the choice-
type questions, an open question was provided to let the owners
describe other possible household air pollutants in their houses.
Three different frequency levels (“often or more,”“sometimes,”
“rarely or never”) for various clinical signs, including “coughing,”“sneez-
ing/reverse sneezing/nasal discharge,”“noisy breathing/snoring,”
“respiratory distress or tachypnea,”and “cyanosis or syncope,”were
rated by the owners. If any of the above clinical signs was noted by the
owner, the duration of the clinical sign was also requested on the
questionnaire.
2.3
|
Household PM2.5 estimation
Quantifiable assessment of household air pollution was estimated by
the measurement of PM2.5 concentration (lg/m
3
) for which a PM2.5
air quality monitor (TES-5321, TES Electrical Electronic Corp, Taiwan)
was used in accordance with the manufacturer’sinstructionswitha
measurement range of 0–500 lg/m
3
, a resolution of 1 lg/m
3
,andan
accuracy of 65lg/m
3
for 50 lgand610% for >50 lg. All the sam-
plings were performed when the owners were present at their homes.
The air was sampled at the height of the animal’s breathing zone, and
readings were taken from five places most commonly frequented by
the animal in the house. The temperature and humidity were measured
and recorded at the same time. The average PM2.5 concentration of
the 5 breathing zones was used for the final analysis.
2.4
|
Statistical analysis
Statistical analyses were processed with commercial software (SPSS
19.0.0; IBM Corporation, Armonk, New York; SAS 9.4; SAS Institute
Inc, Cary, North Carolina). Variables were tested for Gaussian distribu-
tion using the Shapiro-Wilk test, and data were expressed as mean 6
SD for normally distributed data or median with range for nonparamet-
ric data. Comparisons of qualitative factors and the prevalence of
household air pollutants between animals with and without respiratory
disease were made using the chi-squared test or Fisher exact test
(when at least one expected value in the cells of a contingency table
was less than five). Continuous variables were compared using t-test or
the Mann-Whitney rank sum test. The concentration of PM2.535
lg/m
3
was defined as an acceptable level in our study. A cut-off value
of 35 lg/m
3
was chosen and modified from the standard for indoor air
quality announced by the Environmental Protection Administration of
Taiwan, WHO air quality guidelines, and evidence from research on
humans.
20,21
Univariable and multivariable logistic regression models
were used to analyze the association between IAP and respiratory dis-
ease. Univariable logistic regression analysis was used to estimate the
odds ratios (ORs) and 95% confidence intervals (CIs) of exposure fac-
tors for respiratory disease. The variables with Pvalue<.1 in the uni-
variable logistic regression model were selected into the multivariable
logistic regression model, and only one variable was selected from two
variables with collinearity. The Box-Tidwell approach was used to eval-
uate linearity between the log-odds and the continuous variables.
22
The continuous variables were changed into categorical variables if the
assumption of linearity was not met. Statistical significance was set at
P<.05.
3
|
RESULTS
A total of 348 companion animals were recruited over a 12-month
period (August 2016-July 2017): 202 of them were enrolled in the
case-control study (121 pet dogs and 81 pet cats), and 146 additional
written questionnaires were collected for estimating the prevalence of
signs of respiratory problem and household air pollutants.
The prevalence of signs of respiratory problem in pet dogs and
cats was 89.0% and 73%, respectively, and the presence of signs of
respiratory problem with “often or more”frequency was found for
45.0% of pet dogs and 19% of pet cats. The prevalence of second-
hand smoke, cooking behavior/cooking fumes, incense burning, and
household chemicals in the pets home were 32.9%, 72.6%, 17.1%, and
11.6%, respectively.
3.1
|
Dogs
Eighty-three dogs with various respiratory diseases and 38 control
dogs without respiratory disease (attending for routine health care or
problems other than signs of respiratory illness) were included in the
case-control study. Among the dogs with respiratory disease, approxi-
mately half of them (54%) were diagnosed with more than one cate-
gory of respiratory disease or problem. Clinical diagnoses of dogs with
LIN ET AL.Journal of Veterinary Internal Medicine
|
3
respiratory disease included lower respiratory tract disease (such as,
bronchomalacia or chronic bronchitis) in 65/83 dogs, tracheal collapse
in 28/83 dogs, upper airway disease (such as, rhinitis or laryngeal dis-
ease) in 25/83 dogs, concurrent left atrial enlargement in 16/83 dogs,
and pneumonia in 7/83 dogs along with other infrequent diagnoses
such as undetermined etiology (3/83), esophageal disease-related
cough (2/83), obesity-related respiratory problems (2/83), or nasal
tumor (1/83).
The baseline characteristics of the pet dogs with and without
respiratory disease are summarized in Table 1, in which the proportion
of presence of long-term/intermittent exposure to second-hand smoke,
cooking behavior/fumes, and frequent use of household chemicals in
the household between pet dogs with and without respiratory disease
were not significantly different. The proportion of existence of incense
burning (30% versus 13%) in the household were statistically higher in
the pet dogs with respiratory disease than those without (P5.045).
Median household PM2.5 concentration in dogs with and without
respiratory disease were 30.8 lg/m
3
(range, 10.8–214.2) and 38.2 lg/
m
3
(range, 5.4–69.4), respectively (Figure 1A). There was no statistically
significant difference between the two groups (P5.57). A PM2.5 con-
centration>35 lg/m
3
in the household was found for 48.3% of all
dogs with no statistical difference between dogs with and without
respiratory disease (45% versus 55%, P5.30).
The results of univariable and multivariable logistic regression anal-
yses are reported in Table 2. After adjustment for age, body weight,
body condition score, and environmental temperature and humidity,
second-hand smoke or incense burning was not recognized as a signifi-
cant risk factor for respiratory disease in pet dogs. Older age, smaller
body weight (refers to small breeds), and increased body condition
score (refers to level of obesity) were associated with an increased risk
of respiratory disease in pet dogs.
3.2
|
Cats
Sixty-four cats with various respiratory diseases and 17 control cats
without respiratory disease (attending for routine health care or prob-
lems other than signs of respiratory illness) were included in the case-
control study. Among cats with respiratory disease, only a minority
(22%) were diagnosed with having more than one category of respira-
tory disease or problem. Clinical diagnoses of cats with respiratory dis-
ease included feline lower airway disease including feline asthma,
chronic bronchitis, or mixed-type inflammatory airway disease in 40/64
cats, upper airway disease such as rhinitis, nasopharyngeal, or laryngeal
disease in 15/64, pneumonia in 12/64, interstitial lung disease in 6/64,
primary or metastatic lung cancer in 5/64, and undetermined etiology
in 5/64 as well as other infrequent diagnoses such as nasal tumor (2/
64), pneumothorax because of ruptured bullae or emphysema (1/64),
or diaphragmatic hernia (1/64).
The baseline characteristics of the pet cats with and without respi-
ratory disease are summarized in Table 1, in which the proportion of
existence of long-term/intermittent exposure to second-hand smoke,
incense burning, cooking behavior/fumes, and frequent use of house-
hold chemicals in the household were not significantly different
between cats with and without respiratory disease. Median household
PM2.5 concentration in pet cats with respiratory disease (38.6 lg/m
3
;
range, 17.8–131.2) was significantly higher than for those without
(27.4 lg/m
3
;range,15.4–70.0; P5.017; Figure 1B). An unacceptable
level of PM2.5 concentration (>35 lg/m
3
) in the household was
TABLE 1 Baseline characteristics of dogs and cats with and without respiratory disease, proportion of existence of selected household air
pollutants, and household PM2.5 measurements
Dogs Cats
Variable
Respiratory
group (n 583)
Control
group (n 538) P
Respiratory
group (n 564)
Control
group (n 517) P
Age (years) 9.8 63.3 7.7 64.3 .0092 8.0 (1–19) 5.0 (1–14) .063
Sex (males) 51.8 (43/83) 44.7 (17/38) .47 57.8 (37/64) 52.9 (9/17) .72
Body weight (kg) 5.1 (1.5-44.2) 10.9 (1.4-36.2) <.001 4.7 (2.9–10.9) 4.6 (2.4–7.1) .49
9-point body condition score 5 (2–8) 5 (3–7) .076 5 (3–9) 5 (4–6) .65
Second-hand smoke (%) 33 (27/81) 18 (7/38) .093 27 (17/64) 12 (2/17) .33
Incense burning (%) 30 (25/83) 13 (5/38) .045 22 (14/64) 6 (1/17) .17
Cooking behavior/fume (%) 71 (58/82) 79 (30/38) .34 70 (45/64) 53 (9/17) .18
Household chemicals (%) 2 (2/83) 5 (2/38) .59 3 (2/63) 12 (2/17) .20
Average PM2.5 (lg/m
3
) 30.8 (10.8–214.2) 38.2 (5.4–69.4) .57 38.6 (17.8-131.2) 27.4 (15.4–70.0) .017
Environmental temperature (8C) 25.2 63.7 27.1 62.9 .0087 26.0 63.3 27.8 63.0 .045
Environmental humidity (%) 65.7 68.5 69.3 68.7 .034 64.3 68.1 62. 3 68.8 .36
Unacceptable PM2.5 level (%) 45 (36/80) 55 (21/38) .30 59 (38/64) 29 (5/17) .028
Bolded values indicating 2-tailed P<.05.
Data are presented as mean 6standard deviation, median with range, or percentage with numbers.
4
|
Journal of Veterinary Internal Medicine LIN ET AL.
present in 53% of all cats with a significant difference between cats
with and without respiratory disease (59% versus 29%, P5.028).
The results of univariable and multivariable logistic regression anal-
yses are shown on Table 3. An unacceptable level of PM2.5 concentra-
tion (>35 lg/m
3
) and lower environmental temperature were found to
be possible risk factors for respiratory disease in cats in the univariable
analyses. After adjustment for age and environmental temperature, we
found that cats living in households with a PM2.5 level >35 lg/m
3
were more likely to have respiratory disease than those living in house-
holds with an acceptable level of PM2.5 (OR 54.13, 95% CI 1.12–
15.27; P5.03).
4
|
DISCUSSION
In our study, we investigated the prevalence of several well-known
household air pollutants and quantified household air quality by esti-
mating PM2.5 concentration in the animals’breathing zones in pets
with and without respiratory disease. The results of our study revealed
that cats with respiratory disease were living in households with signifi-
cantly higher PM2.5 concentration compared to cats without respira-
tory disease. A household PM2.5 concentration >35 lg/m
3
was
significantly associated with respiratory disease in pet cats but not in
pet dogs.
Some previous studies have found that dogs’exposure to cigarette
smoking or concentrated ambient 0.1–2.5 lm fine particles was able to
cause mucosal lesions in central airways and bronchioles, impair muco-
ciliary function, increase neutrophil percentage or lymphocyte and mac-
rophage count in bronchoalveolar lavage fluid, and induce changes on
pulmonary function.
4,7,19,23
In our study, exposure to second-hand
smoke and several other indoor air pollutants was not found to be a
significant risk factor for respiratory disease in dogs. This finding is very
similar to a previous study, which also failed to recognize the associa-
tion between second-hand smoke in the house and chronic coughing
signs in pet dogs.
12
Although the inclusion criteria for patient enroll-
ment and the overall study design in our study were different from this
previous study, it is noteworthy that the majority of dogs had a diagno-
sis of lower airway problems in both studies, implying the population
composition in the two studies might be comparable. These results
suggest that a strong association between respiratory disease and IAP
either does not exist in pet dogs or is undetectable through question-
naire methodology.
Moreover, the household PM2.5 level of dogs with respiratory dis-
ease were even lower than those of the control dogs in our study—a
finding that might further disapprove the association between IAP and
respiratory disease in dogs. Nevertheless, there were more outliers and
extreme values observed in dogs with respiratory disease compared
with the control dogs (Figure 1A), inferring that extremely high values
of PM2.5 readings tended to be present in the households of dogs
with respiratory disease. When second-hand smoke and incense burn-
ing were combined under a single exposure category, the proportion of
its presence between dogs with and without respiratory disease was
significantly different (14% versus 0%, P5.016). Therefore, it cannot
be simply concluded that IAP was not important in dogs with respira-
tory disease, but the association might be far more complicated than
previously supposed. Compared with air pollution factors, signalment
characteristics such as age, body weight, and body condition were
more evident risk factors for respiratory disease in dogs. Furthermore,
over half of the pet dogs presented with multiple respiratory diagnoses,
which might have complicated subsequent analysis. Many of these
dogs had concurrent structural problems, such as bronchomalacia or
tracheal collapse, which are congenital disorders and typically induce
coughing, thus respiratory disease status in these dogs was less likely
to be related to IAP.
In contrast to dogs, less than one-fourth of cats were diagnosed
with more than one respiratory disease. Inflammatory disease (eg,
FIGURE 1 A, Distribution of household PM2.5 concentration for
dogs wi thout respiratory disease (n 538) and dogs with respiratory
disease (n 583). The box represents the interquartile range (25th-
75th percentile). The horizontal line within each box represents the
median. The whisker bars represent the highest and lowest values
within 1.5 times of the interquartile range, the open circle indicates
outlier that is more than 1.5 times the interquartile range, and the
black star indicates extreme value that is more than 3 times the
interquartile range. There was no statistical difference in household
PM2.5 level between dogs without and with respiratory disease
(P5.57). B, Distribution of household PM2.5 concentration for
cats wi thout respiratory disease (n 517) and cats with respiratory
disease (n 564). Cats with respiratory disease lived in the
households with significantly higher PM2.5 level compared to cats
without respiratory disease (P5.017)
LIN ET AL.Journal of Veterinary Internal Medicine
|
5
inflammatory lower airway disease, rhinitis, or pneumonia) comprised
the majority of the respiratory diagnoses in our study cats, which might
explain why unacceptable household air quality was found to signifi-
cantly affect cats in our study. Indoor particulate matter could have
induced inflammatory respiratory illness through oxidative stress and
proinflammatory effects.
16
Airway neutrophilic inflammation, prolifera-
tion of goblet cells in larger airways, increased nonspecific airway
responsiveness, impairment of bacteriosuppressive activity of alveolar
macrophages, and lung injury after exposure to air pollutants have
been reported in experimental animals.
23,24
Human epidemiologic stud-
ies have extensively presented evidence that associates IAP with
chronic obstructive pulmonary disease, asthma, pneumonia, rhinitis,
and acute respiratory clinical signs.
1–3,25
The results in our study indi-
cate that a similar scenario was observed among pet cats living an
TABLE 2 Univariable and multivariable logistic regression analyses of factors potentially associated with the presence of respiratory disease
in dogs
Univariable analysis Multivariable analysis
Variable Crude OR 95% CI PAdjusted OR 95% CI P
Age (years) 1.17 1.05-1.31 .0049 1.16 1.02-1.33 .027
Body weight (kg)
a
<4.3 1.00 1.00
4.3–6.4 0.28 0.07-1.06 .062 0.21 0.04-1.13 .069
>6.4 0.15 0.05-0.43 .0004 0.08 0.02-0.28 .0001
9-Point body condition score 1.36 0.96-1.93 .081 1.86 1.14-3.04 .013
Second-hand smoke (%) 2.21 0.86-5.68 .098 2.37 0.72-7.80 .15
Incense burning (%) 2.84 0.99-8.14 .051 1.96 0.53-7.24 .31
Cooking behavior/fume (%) 0.64 0.26-1.61 .35 NA NA NA
Household chemicals (%) 0.44 0.06-3.28 .43 NA NA NA
Average PM2.5 (lg/m
3
) 1.01 0.99-1.02 .50 NA NA NA
Environmental temperature (8C) 0.85 0.75-0.96 .011 0.89 0.76-1.04 .14
Environmental humidity (%) 0.95 0.91-1.00 .037 0.97 0.92-1.04 .39
Unacceptable PM2.5 level (%) 0.66 0.30-1.44 .30 NA NA NA
Bolded values indicating 2-tailed P<.05.
Abbreviation: NA, not applicable (not included in multivariable model).
a
The continuous body weight variable was divided into three categories by tertile since the assumption of linearity between the log-odds and the body
weight was not met.
TABLE 3 Univariable and multivariable logistic regression analyses of factors potentially associated with the presence of respiratory disease
in cats
Univariable analysis Multivariable analysis
Variable Crude OR 95% CI PAdjusted OR 95% CI P
Age (years) 1.13 0.99-1.30 .076 1.09 0.94-1.26 .24
Body weight (kg) 1.25 0.80-1.96 .32 NA NA NA
9-point body condition score 1.29 0.80-2.09 .30 NA NA NA
Second-hand smoke (%) 2.71 0.56-13.12 .21 NA NA NA
Incense burning (%) 4.48 0.55-36.78 .16 NA NA NA
Cooking behavior/fume (%) 2.11 0.71-6.28 .18 NA NA NA
Household chemicals (%) 0.25 0.03-1.89 .18 NA NA NA
Average PM2.5 (lg/m
3
) 1.04 1.00–1.09 .080 NA NA NA
Environmental temperature (8C) 0.84 0.70-1.00 .051 0.79 0.64-0.97 .023
Environmental humidity (%) 1.03 0.97-1.10 .36 NA NA NA
Unacceptable PM2.5 level (%) 3.51 1.10-11.15 .033 4.13 1.12-15.27 .033
Bolded values indicating 2-tailed P<.05.
Abbreviation: NA, not applicable (not included in multivariable model).
6
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Journal of Veterinary Internal Medicine LIN ET AL.
indoor lifestyle. While “One Medicine”or “One Health”is a growing
issue, the concept of using companion animals as sentinels for human
health has been proposed in many aspects of the veterinary and medi-
cal professions.
26,27
It could have the potential of considering pet cats
as a spontaneous disease model for IAP-related respiratory disease.
The concentration of PM2.5 in the animals’breathing zones was
chosen to estimate air quality in places most commonly frequented by
the study animal in the house. The deposition of ambient particulate
matter in the respiratory tract is determined by particle size, chemical
composition, and characteristics of the airflow. In average human
adults, larger size particulate matter (2.5–10 lm) is likely to be depos-
ited in the nasal cavity, pharynx, and larynx, whereas fine (0.1–2.5 lm)
and ultrafine (<0.1 lm) particulate matter are likely to be deposited in
the tracheobronchial tree and alveoli.
16,18
Species differences such as
disparate airway caliber, anatomical geometry, and nasal versus mouth
breathing could affect airflow characteristics and particles deposition.
18
Little is known about the actual deposition of particulate matter in the
respiratory tract of cats, but the diameter of a cat’s terminal bronchiole
(100–432 lm)
28
shall allow fine particles (PM2.5) to be inhaled without
anatomical obstruction. An unacceptable PM2.5 level was significantly
associated with respiratory disease in cats in our study, implying these
fine particles were able to deposit in the respiratory tract of cats and
cause detrimental effects.
When one particular indoor air pollutant was considered, exposure
to second-hand smoke (27% versus 12%), incense burning (22% versus
6%) and cooking behavior/fumes (70% versus 53%) in the household
were more common in cats with respiratory disease but not statistically
different from cats without respiratory disease. Nevertheless, when an
overall indicator (PM2.5) was used, significantly worse air quality was
recorded in the households of cats with respiratory disease. Levels of
PM2.5 were reported to be significantly correlated with the presence
of smokers in the household in a previous study
3
; however, no statisti-
cally significant association was found between the average PM2.5
level and any of the household air pollutants investigated in our study
(data not shown). This is not surprising because the measured PM2.5
levels would track with cumulative instead of individual sources of par-
ticulate matters. Even though different exposure levels of second-hand
smoke were considered in additional analyses, we were still unable to
detect statistically significant correlation between the existence of
second-hand smoke and respiratory disease. This might reflect that the
reason for poor air quality is multifactorial,
16
and the complexity of
human activity affects the strength of the contribution of a particular
indoor air pollutant. For instance, some pet owners with a smoking
habit were aware of the detrimental effect of ETS exposure to their
family members, thereby they would avoid smoking indoors or try
improving air circulation whenever possible. The owner’sbehavior
could dramatically affect the amount of pollutants that an animal
received, thus the information from a questionnaire cannot actually
correspond to the extent of IAP in a given household.
In clinical practice, it is usually not possible to quantify air quality
in a pet’s household. Therefore, whether an environmental factor exists
that induces or exacerbates signs of respiratory problem is usually
determined through history taking by clinicians. Our study showed that
the result of quantitative assessment for IAP rather than qualitative
evaluation was associated with respiratory disease. It should be kept in
mind that the presence or absence of IAP as an exacerbating factor
could not be fully ruled out from the patient history while evaluating
and managing clinical cases with respiratory disease.
Our study had some limitations. Firstly, the prevalence of signs of
respiratory problem was high among the study population, and so it
was more difficult to recruit animals free of any respiratory disease into
the control group. It has been reported that the prevalence of signs of
respiratory problem were as high as 56.3% in Swedish Yorkshire terri-
ers, a small breed of dog prone to respiratory disease.
29
Small breeds
also comprised the majority of the dogs in our study (68%), which
might explain the extremely frequent signs of respiratory problem
observed. Secondly, household PM2.5 level was estimated by averag-
ing the real-time readings taken from several places most commonly
frequented by the animal in the house in our study, whereas air sam-
pling in human epidemiologic studies has usually been performed by
installing a monitor in the living room or selected location over a period
of time (eg, 24 hours) and averaging all readings over the sampling
period.
2,3,16
It should be borne in mind that a single time assessment of
household PM2.5 levels might not reflect the day-in, day-out exposure.
The main problem with our method was that dynamic changes in
PM2.5 concentrations during a period of time were not considered,
3
although the effect of this possible measurement bias was equal for
both the case and control groups. Otherwise, for house pets, we
believe that air sampling from breathing zones of multiple places that
the animals spent most time at was more representative for the air
quality level in their domestic microenvironment. More accurate esti-
mation of PM2.5 concentration during a certain time period in the
breathing zone can be obtained by utilizing wearable monitor technol-
ogy,
18,30
but applying this to pet dogs and cats is not feasible at the
moment. Thirdly, some invasive diagnostic procedures such as lower
airway sampling or biopsy would not be allowed in pets without clini-
cally apparent respiratory disease. Therefore, it remains unknown if
some animals in the control group had a subclinical respiratory disease,
and misclassification of grouping might have affected the outcome of
statistical analysis. Lastly, cases in respiratory disease group included
various etiologies, but IAP might impact the risk of each type of respira-
tory disease differently. This is an important limitation because the clin-
ical case mix can be associated with low power and might thus lead to
insignificant results. The case numbers in each disease category in our
study were insufficient for appropriate subgroup analyses; therefore,
further investigations are warranted to examine the effect of IAP on
individual respiratory illness in companion animals, particularly in pet
cats.
In conclusion, our study provided clinical evidence of the role of
IAP on the respiratory health of companion dogs and cats. Exposure to
household incense burning was significantly more common in dogs
with respiratory disease compared with dogs without respiratory dis-
ease, but there was no strong association found between IAP and
respiratory disease in pet dogs. In contrast to dogs, cats with respira-
tory disease lived in the households with significantly higher PM2.5
concentration compared to cats without respiratory disease. After
LIN ET AL.Journal of Veterinary Internal Medicine
|
7
adjusting for age and environmental temperature, an unacceptable level
of household PM2.5 concentration (>35 lg/m
3
) was found to be sig-
nificantly associated with respiratory disease in cats (OR 54.13, 95%
CI 1.12–15.27). Quantifying IAP can help recognize and monitor envi-
ronmental hazards to animal health, and the effect of IAP on the respi-
ratory health of companion animals warrants further attention.
ACKNOWLEDGMENTS
Part of the data was presented in the format of poster presentations
at the 35th Annual Symposium of Veterinary Comparative Respira-
tory Society, October 2017, in Champaign, Illinois. The authors
acknowledge statistical assistance provided by the Department of
Medical Research in National Taiwan University Hospital. They also
thank all those dedicated pet owners involved in this study for their
collaboration. The work was done at National Taiwan University
Veterinary Hospital, National Taiwan University, Taiwan. This study
was supported by Ministry of Science and Technology, Taiwan
(MOST 105–2313-B-002–055 -).
CONFLICT OF INTEREST DECLARATION
Authors declare no conflict of interest.
OFF-LABEL ANTIMICROBIAL DECLARATION
Authors declare no off-label use of antimicrobials.
INSTITUTIONAL ANIMAL CARE AND USE COMMITTEE
(IACUC) OR OTHER APPROVAL DECLARATION
Authors declare no IACUC or other approval was needed.
ORCID
Chung-Hui Lin http://orcid.org/0000-0002-5276-3179
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How to cite this article: Lin C-H, Lo P-Y, Wu H-D, Chang C,
Wang L-C. Association between indoor air pollution and respira-
tory disease in companion dogs and cats. J Vet Intern Med.
2018;00:1–9. https://doi.org/10.1111/jvim.15143
LIN ET AL.Journal of Veterinary Internal Medicine
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