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Preventive Veterinary Medicine 213 (2023) 105882

Contents lists available at ScienceDirect

Preventive Veterinary Medicine


journal homepage: www.elsevier.com/locate/prevetmed

Preventive healthcare among dogs and cats in Chile is positively associated


with emotional owner-companion animal bond and socioeconomic factors
Marília Salgado-Caxito a, Julio A. Benavides b, c, Nicolhole Atero a, Francisca Córdova-Bürhle a,
Romina Ramos a, Miriam Fernandez d, Claudia Sapiente-Aguirre e, Fernando O. Mardones a, f, *
a
Escuela de Medicina Veterinaria, Facultad de Agronomía e Ingeniería Forestal, Facultad de Ciencias Biológicas y Facultad de Medicina, Pontificia Universidad Católica
de Chile, Santiago, Chile
b
MIVEGEC, IRD, CNRS, Université Montpellier, Montpellier, France
c
Centro de Investigación para la Sustentabilidad y Doctorado en Medicina de la Conservación, Facultad Ciencias de la Vida, Universidad Andres Bello, Santiago, Chile
d
Estación Costera de Investigaciones Marinas (ECIM) de Las Cruces y Millennium Nucleus for the Ecology and Conservation of Temperate Mesophotic Reef Ecosystem
(NUTME), Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
e
Programa Nacional de Tenencia Responsable de Animales de Compañía (PTRAC), Subsecretaría de Desarrollo Regional y Administrativo (SUBDERE), Ministerio del
Interior y Seguridad Pública de Chile, Chile
f
Department of Pediatric Infectious Diseases and Immunology, School of Medicine, Pontificia Universidad Católica de Chile, Santiago 7820244, Chile

A R T I C L E I N F O A B S T R A C T

Keywords: Global companion animal population has been increasing as well as the number of dogs and cats being
Human-animal bond considered as a family member. However, it is unclear whether this close relationship could be associated with
Surveys higher preventive healthcare in companion animals. Using data from 7,048 questionnaires of dogs and 3,271 of
Responsible pet ownership
cats from the First National Study on Responsible Companion Animal Ownership, we estimated the proportion of
Veterinary care
Vaccination
preventive healthcare in companion animals of Chile. We also conducted a general linear mixed-effect regression
Parasite control model to identify socioeconomic factors and indicators of the emotional owners-companion animal bond that
Latin America could influence owners’ practices related to vaccination, parasite control, and veterinary visits. Based on the
owner’s answers, Chile has a satisfactory overall rates of parasite control (71%) and annual veterinary visits
(65%) but a low vaccination coverage of both dogs (39%) and cats (25%). ‘Purebred’, ‘live in urban areas’,
‘acquired by monetary compensation’, and ‘dog species’ were associated with a higher probability of preventive
healthcare in companion animals. Conversely, this probability was lower among senior animals compared to
adults, males, and those owned by the Silent Generation or Baby Boomers (i.e., owners born before 1964).
‘Sleeping inside’, ‘acquired for an emotional reason’ (e.g., companionship), and ‘considered a family member’
were positively associated with at least one of assessed preventive measures. Our findings suggest that emotional
owner-companion animal bonds could positively impact the frequency and quality of preventive healthcare in
dogs and cats. However, owners who totally disagreed that a companion animal is a “family member” were also
associated with a higher likelihood of vaccination uptake and veterinary visits for their animals. This highlights
that owner’s compliance with veterinary preventive healthcare is multifactorial. Chile has a high prevalence of
infectious diseases circulating among dogs and cats and increasingly close contacts between owners and com­
panion animals due to emotional bonds. Thus, our study calls for One Health approaches to reduce the risks of
cross-species disease transmission. Specifically, increasing vaccination coverage of companion animals in Chile is
the most urgent preventive measure needed, especially among cats, males, and older animals. Expand preventive
healthcare among dogs and cats will promote public and animal health, including local wildlife that is suscep­
tible to infectious diseases circulating in companion animals.

1. Introduction both animal and human health (López et al., 2009; Overgaauw et al.,
2020). Preventive healthcare in companion animals can increase animal
Maintaining healthy companion animals is essential for promote wellbeing and reduce animal health burden. It also could limit the

* Correspondence to: Marcoleta 391, Oficina 303C, Santiago 7820244, Chile.


E-mail address: femardones@uc.cl (F.O. Mardones).

https://doi.org/10.1016/j.prevetmed.2023.105882
Received 6 September 2022; Received in revised form 1 February 2023; Accepted 18 February 2023
Available online 20 February 2023
0167-5877/© 2023 Elsevier B.V. All rights reserved.
M. Salgado-Caxito et al. Preventive Veterinary Medicine 213 (2023) 105882

circulation of zoonotic diseases transmitted by close contact between as Programa de Tenencia Responsable de Animales de Compañía) of the
domestic animals and humans (Alho et al., 2018; Benavides et al., 2020). Undersecretary of Regional and Administrative Development, Ministry
For example, companion animal vaccination can prevent deadly cases of of the Interior and Public Security, Government of Chile (referred here
rabies in both domestic animals and humans (Astorga et al., 2015; as ’SUBDERE program’) was launched as part of public policies to attend
Benavides et al., 2020; Costa et al., 2018). In addition, vaccination is conflicts of human-animal coexistence and their consequences. This
essential to reduce the morbidity and mortality of infectious diseases, program finances mainly district projects for veterinary services (e.g.,
such as distemper in dogs or respiratory tract diseases in cats (Cohn, surgical sterilizations), microchip identification, registration, vaccina­
2011; Day et al., 2020). Multiple factors have been associated with tion, parasite control, educational campaigns, and other actions (Garde
inadequate veterinary care for dogs and cats. For example, low educa­ et al., 2022; Ministerio de Hacienda de Chile, 2021; Ministerio de
tion levels, reduced economic resources, living in deprived areas, and Desarrollo Social y Familia de Chile). In addition, a companion animal
limited access to veterinary services (Brady et al., 2012; Flores-Ibarra ownership legislation was implemented in 2017 by the SUBDERE, the
and Estrella-Valenzuela, 2004; Rigas et al., 2022; Sánchez-Vizcaíno Ministry of Health, the districts, and other state entities, although rabies
et al., 2017; Savadogo et al., 2021). However, despite its importance for vaccination is the sole preventive healthcare measure among the
animal and human health, socioeconomic factors influencing veterinary mandatory rules. Despite the implementation of the program and
preventive healthcare have not been widely explored in Latin America. legislation, the frequency of preventive healthcare among companion
For example, people of the same age group are expected to have similar animals in Chile remains mostly unknown. However, a low response to
beliefs, attitudes, and practices (Twenge et al., 2012). However, it is not mandatory rules such as the identification and registration of owned
known whether the owners’ age could be associated with the health animals (~2 million registered companion animals in 2022) (unpub­
status of companion animals of Chile. There is also limited under­ lished data of the SUBDERE program) suggest limited responsible
standing on the impact of personal connections between owners and ownership practices, including preventive healthcare. In 2021, the
their animals (defined here as ‘emotional owner-companion animal SUBDERE program led the First National Study on Responsible Com­
bond’) on preventive healthcare in companion animals (Gates et al., panion Animal Ownership to estimate and characterize the companion
2019; Lue et al., 2008; Meyer and Forkman, 2014; Packer et al., 2019; animal population in Chile. Here, we used a subset of the administered
Ramón et al., 2010; Slater et al., 2008). Understanding owners’ moti­ questionnaires in SUBDERE program’s study to (i) estimate the pro­
vation to adopt preventive companion animal healthcare is necessary for portion of dogs and cats receiving preventive healthcare in Chile (i.e.,
designing effective strategies that can improve animal’s wellbeing and vaccinations, parasite control, and visit to a veterinarian) and to (ii)
limit the spread of infectious diseases. identify the socioeconomic factors and indicators of the emotional
Vaccination, parasite control, and annual veterinary visits are the owner-companion animal bond that could be associated to these pre­
main measures for maintaining companion animal health (American ventive healthcare measures.
Animal Hospital Association, 2011). Appropriate immunizations include
core vaccines against most common infectious diseases for dogs (i.e., 2. Materials and methods
distemper, adenovirus, parvovirus, and leptospirosis in high-risk loca­
tions) and cats (i.e., panleukopenia, herpesvirus, and calicivirus) 2.1. Study design
administered every 1–3 years (Day et al., 2020, 2016), and rabies
vaccination in endemic countries (Benavides et al., 2020; Day et al., A one-week field survey of companion animal owners was conducted
2020). Likewise, the regular administration of topical or oral products to simultaneously in 35 districts (approximately 10% out of the total 346
reduce or eliminate endoparasites (e.g., Ancylostoma caninum, Crypto­ districts) of Chile in December 2021 (Fig. 1). All Chilean districts were
sporidium spp., Giardia spp.) and ectoparasites (e.g., ticks and flies) are invited to participate in this study, and all districts that voluntarily
also recommended to maintain companion animals’ good health (Stull expressed interest were included. In-person questionnaires were
et al., 2016). Finally, annual veterinary medical evaluations are essential administered as part of a larger study led by the SUBDERE program to
to monitor companion animals’ health, reduce risk of future health estimate and characterize the national companion animal population.
problems, and perform vaccination (American Animal Hospital Associ­ Interviews were carried out during COVID pandemic following all safety
ation, 2011). The absence of these measures has been associated with measures established by the Chilean health authority (e.g., full vacci­
increased incidence of infectious diseases in dog and cat populations nation schedule, negative PCR, and use of masks). The number of
(Alves et al., 2018; Dias Costa et al., 2017; DiGangi et al., 2019; Gettings questionnaires to be administered per district was estimated using a two-
et al., 2020; Harvey et al., 2020; Salgado-Caxito et al., 2021b; Tion et al., stage random sampling, proportional to rural and urban households, to
2019). Conversely, mass rabies vaccination campaigns have allowed the estimate the number of owned dogs and cats in Chile. Briefly, we esti­
control and even eradication of canine-mediated rabies in both dogs and mated the number of questionnaires based on the number of household
humans in most Latin American countries (Velasco-Villa et al., 2017; at each district extracted from the latest 2017 human national census
Vigilato et al., 2013). Despite being understood as imperative for animal (INE, 2007), an expected 75% of households having at least one dog or
welfare and defended as part of animal rights (McCausland, 2014; cat (Carvelli et al., 2016, 2020; CADEM, 2022), an acceptable margin of
Rollin, 2011; Ryan et al., 2019), many health preventive measures for error of 5%, and a desired confidence of 95%. The name of each district
companion animals are not mandatory. Few exceptions include participating in the study as well as the total of questionnaires admin­
mandatory vaccination in some countries against zoonotic diseases such istered per district are given as Supplementary Material 1.
as rabies (Day et al., 2020; Ministerio de Salud de Chile, 2003; Yamada One person per household was interviewed. All respondents were
et al., 2019), although owners’ compliance is often difficult to regulate. over 18 years old and digitally signed a consent form confirming that
In fact, targeted vaccination coverage to control rabies are still not they understood and accepted that their responses would be collected,
achieved in many low- and middle-income countries promoting stored, and analyzed. Personal data (i.e., name, age, gender) captured by
mandatory dog rabies vaccination (Astorga et al., 2015; Savadogo et al., our study is confidential and property of SUBDERE. However, it can be
2021; Suzuki et al., 2008). requested through the Transparency Portal of the Chilean Government
According to preliminary data, Chile has an estimated population of (https://www.portaltransparencia.cl/). This study was approved by the
more than 9 million companion animals (SUBDERE, 2022). In addition, Research Safety Ethics Committee and by the Social Sciences, Arts and
there is a high prevalence of infectious diseases circulating among these Humanities Ethics Committee of the Pontifical Catholic University of
animals in the country, such as canine distemper, canine parvovirus, and Chile (protocol number: 210922003).
feline retroviruses (Day et al., 2020; López et al., 2009). In 2014, the
Responsible Companion Animal Ownership Program (named in Spanish

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M. Salgado-Caxito et al. Preventive Veterinary Medicine 213 (2023) 105882

2.2. Questionnaire

The questionnaire analyzed in this study was a subset of a larger in-


person questionnaire lasting ~1–1.5 h, including 37 questions aiming to
estimate and characterize the owned dog and cat population of Chile.
The clarity and pertinence of all questions were discussed and edited
between the research team and the governmental entity in charge of the
survey. Given logistic challenges related to the large geographical area
to be covered and lack of availability of local public staff, no pilot study
was conducted. For this study, we selected 15 closed questions grouped
into three sections: (i) characteristics of the owners, households, and
companion animals (n = 9), (ii) owner’s practices related to preventive
healthcare in dogs and cats (n = 3), and (iii) indicators of the emotional
owner-companion animal bond reported in previous studies (n = 3).
Questions included in this study are available as Supplementary Mate­
rial 2. Only one responder per household provided individual informa­
tion of the companion animals of the household. Given time constraints,
we registered the total number of companion animals in the residence
and collected detailed information for a maximum of 5 dogs and 5 cats
per interview (maximum 10 companion animals per household). Data
was recorded using the web interface of KoBoToolbox (https://www.
kobotoolbox.org) using mobile phones (Pham and Vinck, 2020).

2.2.1. Preventive healthcare practices of owners


We investigated three practices for preventive companion animal
healthcare in Chile: (i) immunization with core vaccines in the previous
year (i.e., all companion animals vaccinated with polyvalent and/or
rabies vaccines were included in the GLM analyses), (ii) parasite control
during the previous six-months, and (iii) performing an annual com­
panion animal health checkup by a veterinarian. Core vaccines available
in Chile include (i) polyvalent vaccines (regardless of the brand)
conferring immunity against canine distemper, canine parvovirus,
leptospirosis (Leptospira interrogans serovars canicola and icterohaemor­
rhagiae), canine adenovirus type 2, and canine parainfluenza virus for
dogs; (ii) triple feline vaccines (regardless of the brand) containing
attenuated panleukopenia virus, feline herpesvirus, and feline cal­
icivirus for cats; and (iii) rabies vaccine for both species (Iragüen et al.,
2011; PTRAC, 2022; SAG, 2023). We considered a companion animal as
vaccinated when owners were able to report the type of the vaccine
received. Deworming and/or administration of ectoparasiticides were
grouped as a single measure referred as parasite control to avoid
misinterpretation among owners, since there are oral medications to
treat ectoparasites and topical products to control endoparasites. The
period included in the evaluation for each of the three preventive
measures (e.g., maximum six months for parasite control and one year
for both vaccination and veterinary visits) was chosen based on Chile’s
legislation (annual vaccination required for rabies), the risk of parasite
environmental re-exposure after treatment, and the Chilean guideline of
veterinary medical protocols published by the SUBDERE program (e.g.,
annual vaccination of dogs with polyvalent vaccines) (Ministerio de
Salud de Chile, 2003; Walther et al., 2014; PTRAC, 2022). Although the
protocol of the SUBDERE program recommends core vaccination of cats
every 3 years, they must be annually vaccinated against rabies, as
stipulated by the Chilean health authority (Ministerio de Salud de Chile,
2003).

2.2.2. Owner and companion animal characteristics associated with


companion animal preventive healthcare measures
The recorded characteristics of owners and households included age
Fig. 1. Map of districts in Chile participating in the survey of companion ani­
mal owners built using the free and open source software Qgis 3.24 (QGIS and generational cohort, gender, type of residence (apartment, house, or
Development Team, 2022) and the shapefiles of the communal and national other), living environment (urban or rural), and district and region of
boundaries downloaded from "IDE Chile" (Spatial Data Infrastructure, the residence. Generational cohort referred to the Silent Generation
https://www.ide.cl). (owners born between 1925 and 1945, corresponding to 76–95 years old
in 2021), Baby Boomers (owners born between 1946 and 1964, corre­
sponding to 57–75 years old in 2021), the X Generation (owners born
between 1965 and 1979, corresponding to 42–56 years old in 2021),

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Millennials (owners born between 1980 and 1994, corresponding to vaccination also included whether animals received parasite control as
27–41 years old in 2021), and the Z Generation (owners born between an explanatory variable, and vice-versa.
1995 and 2010, corresponding to less than 26 years old in 2021) (Lissitsa The binary nature of our response variable (i.e., received or not a
et al., 2022; Rank and Contreras, 2021). Characteristics of companion given preventive healthcare measure) required using generalized linear
animals included species (dog or cat), age (divided into puppy/kitten, mixed models (GLMM) with binomial errors. The district’s ID was
adult, and senior), gender, breed (divided into mixed or purebred), and included as a random effect. Models were built with the gmler function of
whether monetary compensation was included during the acquisition of the lme4 package (Bates et al., 2015) in R using the bobyqa model
the companion animal. optimizer. Model fit was evaluated by checking the presence of residual
Three indicators of the emotional owner-companion animal bond outliers (function testOutliers), overdispersion (testDispersion), and
were recorded to evaluate whether they could be associated with pre­ normality (qqplot) using the DHARMa package (Hartig and Lohse,
ventive healthcare in dogs and cats. Indicators were defined by discus­ 2022). Full models were used (no variable reduction) and the statistical
sions between researchers and the governmental agency. Based on significance of each variable (p-value < 0.05) were assessed by Wald’s
previous studies we evaluated: (i) the perception of the dog or cat as a test. Given that up to 10 companion animals could belong to the same
family member, (ii) the designated place for the companion animal to owner, we also included household as a random effect.
sleep, and (iii) the main reason for having a companion animal (Ara­
gunde-Kohl et al., 2020; Bouma et al., 2021; Machado et al., 2020). 3. Results
These indicators have been increasingly reported to reflect personal
connections between owners and their animals. While family can be Our survey included 12 (out of 16) regions of the country. Districts
understood as a highly important social group, access to household participating in the study were mostly located in Central Chile, where
spaces denotes inclusion to the family environment (McConnell et al., the highest fraction of the Chilean population is concentrated (Fig. 1).
2019; White, 2009). Also, giving an emotional reason for owning a Among the 17,458 households visited in the 35 districts, in 8,674 people
companion animal demonstrates owners’ feelings of emotional bonding. were contacted and in 6,275 inhabitants agreed to respond to the
In this context, perceiving companion animals as family members, questionnaire. Of 4,718 responders (one per household) reporting dogs
allowing them to sleep inside the house, and having a companion animal and/or cats, 2,762 only owned dogs, 656 only cats, and 1,300 reported
for emotional reasons indicate strong social connections. owning both species (at least one dog and one cat). The median number
We used a Likert-scale question to assess owners’ attitudes towards of dogs per household was 1 (mean: 1.86, range: 1–88) and 1 for cats
considering the animal as a family member. Respondents could quali­ (mean: 1.88, range: 1–27). After excluding incomplete questionnaires,
tatively answer whether they ‘Totally disagree’, ‘Disagree’, ’Agree’, or we obtained data for 10,319 companion animals, including 7,048 dogs
‘Totally agree’ with the following statement: “This dog/cat is a member and 3,271 cats from 4,682 households.
of my family”. Two alternatives were presented to the informants
regarding the place where the companion animal sleeps: “indoors” when 3.1. Characteristics of the owners and surveyed companion animals
the companion animal was allowed to sleep inside the house or “out­
doors” when not (regardless of whether there was a shelter outside the The median age of owners was 49 (mean: 48.6, range: 18–95) and the
house). Owners were asked to provide the principal reason for having majority were female (69%, 3,226/4,682). The main generational
their companion animal. Responses were captured as free-text answers cohort participating was Baby Boomer (n = 1,412), followed by X
that were then classified as ‘emotional’ or ‘non-emotional’ by our Generation (n = 1,249), Millennial (n = 1,115), Z Generation
research team during data cleaning prior to analysis. (n = 494), and Silent Generation (n = 297). In the remaining 115
questionnaires the age of the owner was not registered.
2.3. Statistical analyses Surveyed dogs included 63% (n = 4,439 out of 7,048) of adults (from
one to seven years old), 22% (n = 1,555) of seniors (above seven years
Data gathered through the KoboToolbox were loaded onto a Micro­ old), and 13% (n = 901) of puppies (less than one year old). There was a
soft Excel© datasheet and then cleaned using R software version 3.6.3. higher proportion of male (54%), and most were mixed-breed (56%).
(R Core Team, 2022). We estimated the proportion of companion ani­ When the dog shared the household with another animal, it was mostly
mals being vaccinated, receiving parasite control, and visiting a veteri­ from the same species (69%). Only 12% of dogs were acquired through
narian, and their 95% confidence intervals (95% CI), using the binom. monetary compensation.
confint function (Agresti-Coull method) in the binom package in R Surveyed cat population was also composed mainly of adults (64%,
(Dorai-Raj, 2022). Correlations between the average (mean) proportion 2,105/3,271), followed by kittens (23%) and senior cats (11%). We
of different healthcare measures across districts were tested using a identified more females (54%) and for most cats the breed was not re­
linear model with the lm function in R. ported (63%) or they were reported as mixed-breed (34%). Many cats
The association between companion animals and owners’ charac­ shared their household with another dog (68%) and/or cat (66%). Only
teristics and the three preventive healthcare measures studied (vacci­ 0.5% of cats were acquired through monetary compensation. Details of
nation, parasite control, and veterinary visits) were tested statistically the characteristics of the dog and cat populations surveyed are provided
by building separate multivariate logistic regressions for each preven­ as Supplementary Material 3.
tive measure at the animal-level (each dog/cat was considered an in­
dependent observation, see below). Models included the following 3.2. Preventive healthcare measures in dogs and cats from Chile
explanatory variables: gender, a categorical age (owners: Silent Gener­
ation, Baby Boomers, X Generation, Millennials, and Z Generation; Parasite control every 6 months was the most performed preventive
companion animals: puppy/kitten, adult, and senior); type of residence healthcare measure by owners for both species (76% of dogs and 60% of
(i.e., house or other) and area (i.e., urban or rural); animal’s species, age, cats) (Fig. 2). The proportion of regular veterinary visits was higher
gender, and breed, whether monetary compensation was included in the among dogs (70%) compared to cats (54%). Only 39% of dogs and 25%
acquisition of the animal, and one of the three variables illustrating the of cats have received core vaccines in the previous year. A slight dif­
emotional owner-companion animal bond. Since the three variables ference was observed between the proportion of companion animals
reflecting owner-companion animal bond can be highly correlated, we vaccinated with rabies (33% of dogs and 19% of cats) and with poly­
tested the significance of each of these variables in a separate model, valent (32% of dogs and 23% of cats) vaccines. Details of the proportions
keeping all other variables and parameters equal. To study the corre­ of preventive healthcare measures by species are provided in Table 1.
lation between vaccination and parasite control, models testing The proportion of animals receiving a given preventive healthcare

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Fig. 2. A) Proportion of vaccination, parasite control, and annual visits to a veterinarian among surveyed dogs and cats. Error bars show confidence intervals of
proportions estimated over the total number of animals in the study using the binom package in R. B) Relationship between the districts’ average percentage of
companion animals vaccinated and receiving parasite control. C) Relationship between vaccination and veterinary visits percentages. D) Relationship between
veterinary visits and parasite control percentages. The R-squared of a linear regression between two variables is provided. The asterisk denotes a significant rela­
tionship in the linear regression (p-value < 0.05). The four panels were generated using data from 10,319 surveys (7,048 of dogs and 3,271 of cats) conducted in 35
districts in 12 regions of Chile in December 2021.

measure varied across districts (Fig. 2). There was a positive significant ‘non-emotional reason’. Responses indicating a sense of personal
correlation between a district’s average proportion of animals checked connection by the owners were considered as ‘emotional reasons’, which
by a veterinarian and the proportion of animals vaccinated (rho=0.4, included ‘companion’, ‘assistance’, ‘therapy’, and ‘temporary housing’.
p < 0.01, Fig. 2C). In contrast, no statistically significant correlation was Otherwise, responses such as ‘security’, ‘work’, ‘hunting’, ‘pest control’,
observed between the district’s average proportion of animals vacci­ ‘sport’, and ‘reproduction’ were classified as ‘non-emotional’. In addi­
nated and receiving parasite control in the last 6 months (rho=0.0, tion, we assumed that non-specific responses (e.g., didn’t know, didn’t
p > 0.05, Fig. 2B), nor between the proportion on animals checked by a answer, or gave ambiguous answers) were unlikely to portray a personal
veterinarian and getting parasite control (rho=0.09, p > 0.05, Fig. 2D). connection of the owners with their animals. Only one reason was
accepted for each companion animal that was mainly of an emotional
3.3. Emotional owner-companion animal bond nature for both dogs (88%) and cats (94%).

Reporting the companion animal as a ‘family member’, allowing the 3.4. Owner and companion animal factors associated with preventive
companion animal ‘sleep inside’ the house, and having the companion healthcare in dogs and cats
animal for ’emotional reasons’ were considered indicators of emotional
owner-companion animal bond. Overall, 94% of dogs and 93% of cats 3.4.1. Vaccination
were reported as a member of the family (their owners “agreed” or The likelihood of vaccination with core vaccines (polyvalent and/or
“totally agreed” with this statement). However, a smaller proportion of rabies) was higher among dogs (GLM, Odds Ratio (OR)= 3.39 [95% CI:
dogs used to sleep indoors (39%, 2,729/7,048) compared with cats 2.25–5.12], p < 0.001), purebred companion animals (GLM, OR= 2.63
(68%, 2,225/3,271). Multiple reasons were given for owning a com­ [95% CI: 1.85–3.74], p < 0.001), and companion animals that regularly
panion animal. The free-text answers registered were divided in two received parasite control (GLM, OR= 197.39 [95% CI: 106.26–366.66],
categories included in the statistical model: an ‘emotional reason’ or p < 0.001) but lower among senior companion animals compared to

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Table 1 considered them as family members at all (have “totally disagreed” with
Summary of answers extracted from questionnaires. Proportion of dogs and cats this statement) (GLM, OR= 28.1 [95% CI: 3.24–243.33], p < 0.01) and
that received periodic preventive healthcare measures, including core vaccina­ owners who strongly considered their companion animal as a family
tion (i.e., polyvalent and/or rabies) within the current year, parasite control member (have “totally agreed” with this statement) (GLM, OR= 14.55
during the last semester, and annual veterinary visits. [95% CI: 2.1–100.67], p < 0.01) were more likely to provide the
Variable Animal species required immunization for their companion animals (Figs. 3 and 4C).
Dogs Cats There was no statistical difference in the likelihood of vaccinating the
(N = 7,048) (N = 3,271) companion animal in relation to the reason for its ownership (emotional
n % n % vs. non-emotional) (Fig. 4B).

Annual veterinary visits Yes 4,932 69.98% 1,776 54.3%


No 2,070 29.37% 1,460 44.63%
3.4.2. Parasite control
N/ 46 0.65% 35 1.07% Dogs (GLM, OR= 9.53 [95% CI: 5.92–15.33], p < 0.001) and com­
Aa panion animals with an updated vaccination status (GLM, OR= 174.35
Regular parasite control (up to Yes 5,377 76.29% 1,978 60.47% [95% CI: 60.81–499.87], p < 0.001) had a higher likelihood to receive
every 6 months) No 1,327 18.83% 1,112 34%
parasite control (Fig. 5). Nonetheless, parasite control was less likely
N/A 344 4.88% 181 5.53%
Vaccination statusb Yes 2,763 39.2% 821 25.1% among senior companion animals compare to adults (GLM, OR= 0.36
No 4,285 60.8% 2,450 74.9% [95% CI: 0.23–0.57], p < 0.001).
Rabies vaccination in the last year Yes 2,364 33.54% 629 19.23% Companion animals that used to sleep inside the house (GLM, OR=
No 4,684 66.46% 2,642 80.77% 2.43 [95% CI: 1.5–3.96], p < 0.001) and were acquired for emotional
Polyvalent vaccination in the last Yes 2,280 32.35% 744 22.75%
year No 4,768 67.65% 2,527 77.25%
reasons (GLM, OR= 2.19 [95% CI: 1.12–4.31], p < 0.05) were more
likely to receive parasite control (Figs. 4A and 4B). However, being or
a
N/A: Refers to the proportion of informants that did not know or chose not to not considered a member of the family did not influence the probability
answer.
b of parasite control in dogs and cats (Figs. 4C and 5).
Refers to the proportion of vaccinated animals. When owners were not able
to specify the type of the vaccine, their animals were considered unvaccinated.
3.4.3. Veterinary visits
Receiving an annual veterinary consultation was more likely among
adults (GLM, OR= 0.69 [95% CI: 0.49–0.97], p < 0.05) (Fig. 3). Ac­
animals living in urban areas (GLM, OR= 5.92 [95% CI: 3.9–8.98],
cording to owners’ age, companion animals owned by the Silent Gen­
p < 0.001), dogs (GLM, OR= 4.74 [95% CI: 3.45–6.52], p < 0.001),
eration (GLM, OR= 0.06 [95% CI: 0.02–0.16], p < 0.001) and Baby
purebred (GLM, OR= 3.52 [95% CI: 2.65–4.66], p < 0.001), and ac­
Boomers (GLM, OR= 0.38 [95% CI: 0.21–0.69], p < 0.01) had lower
quired through a monetary compensation (GLM, OR= 2.24 [95% CI:
probability to receive core vaccines. In contrast, Millennials were two
1.49–3.36], p < 0.001) (Fig. 6). The likelihood of an annual veterinary
times more likely to vaccinate their companion animals (GLM, OR= 2.3
consultation decreased among males (GLM, OR= 0.64 [95% CI:
[95% CI: 1.27–4.16], p < 0.01).
0.52–0.79], p < 0.001) and senior companion animals compared to
Companion animals allowed to sleep indoors (GLM, OR= 3.87 [95%
adults (GLM, OR= 0.53 [95% CI: 0.41–0.69], p < 0.001) and when their
CI: 2.65–5.63], p < 0.001) were more likely to receive vaccination
owner was of the Silent generation (GLM, OR= 0.31 [95% CI: 0.16–0.6],
(Fig. 4A). However, a different pattern was observed when considering
p < 0.001).
the dog or cat as a member of the family. Either owners that not
Similar to vaccination results, companion animals sleeping indoors

Fig. 3. Forest plot for the Odds Ratios (OR) and their 95%
confidence intervals (solid lines) for factors associated with
vaccination in companion animals obtained from a General
Linear Model regression. * Significant variables (p < 0.05).
The following categories were used in the model as a
reference to estimate the effect of other categories: ‘X
Generation’ (owner’s generation variable), ‘Apartment’
(residence), ‘Rural’ (environment), ‘Adult’ (companion
animal’s age), ‘Cat’ (species) and ‘Disagree’ (the compan­
ion animal is family member).

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M. Salgado-Caxito et al. Preventive Veterinary Medicine 213 (2023) 105882

Fig. 4. Proportion (in percentage) of preventive healthcare practices in companion animals according to whether: A) the companion animal sleeping inside/outside
the house, B) the animal was acquired for an emotional reason and C) the companion animal is considered a member of the family. Error bars show confidence
intervals of proportions estimated using the binom package in R.

Fig. 5. Forest plot for the Odds Ratios (OR) and their 95%
confidence intervals (solid lines) for factors associated with
parasite control in companion animals obtained from a
Generalized Linear model. *Significant variables
(p < 0.05). The following categories were used in the
model as a reference to estimate the effect of other cate­
gories: ‘X Generation’ (owner’s generation variable),
‘Apartment’ (residence), ‘Rural’ (environment), ‘Adult’
(companion animal’s age), ‘Cat’ (species) and ‘Disagree’
(the companion animal is family member).

(GLM, OR= 5.58 [95% CI: 4.13–7.52], p < 0.001) and whose owners veterinary medical evaluation and controlled their parasites, but less
have “totally disagreed” (GLM, OR= 4.77 [95% CI: 1.18–19.27], than half vaccinated them. Owner’s age and several characteristics of
p < 0.05) or “totally agreed” (GLM, OR= 4.31 [95% CI: 1.31–14.16], the companion animal (e.g., species, age, gender) were associated with
p < 0.05) that they should be considered a family member were more the likelihood of a preventive healthcare measure. Particularly, all in­
likely to be taken to the veterinarian (Figs. 4A, 4C, and 6). No associa­ dicators of the emotional owner-companion animal bond (companion
tions with the reason for its ownership (emotional vs. non-emotional) animals sleeping indoors, acquired due to an emotional reason, and
were identified. considered as family members) were positively associated with at least
one of the three preventive healthcare measures tested (i.e., vaccination,
4. Discussion parasite control, and veterinary visits). However, owners who did not
consider at all their companion animals as a “family member” (i.e.,
It is generally reasoned that appropriate access to veterinary care and totally disagree) were also more likely to ensure preventive companion
disease prevention contribute to the health and wellbeing of companion animal healthcare. This evidence that other types of relationships be­
animals. However, the factors leading owners to adopt practices of tween owners and their companion animals also can influence owners’
preventive healthcare in companion animal remain poorly understood. practices.
Our results showed that most owners in Chile took their dogs or cats for a Despite the satisfactory overall rates of parasite control (71%) and

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M. Salgado-Caxito et al. Preventive Veterinary Medicine 213 (2023) 105882

Fig. 6. Forest plot for the Odds Ratios (OR) and their 95%
confidence intervals (solid lines) for factors associated with
veterinary visits of companion animals obtained from a
Generalized Linear model. *Significant variables
(p < 0.05). The following categories were used in the
model as a reference to estimate the effect of other cate­
gories: ‘X Generation’ (owner’s generation variable),
‘Apartment’ (residence), ‘Rural’ (environment), ‘Adult’
(companion animal’s age), ‘Cat’ (species) and ‘Disagree’
(the companion animal is family member).

veterinary visits (65%), we identified a low proportion of vaccinated companion animals ‘living in urban areas’ or ‘acquired through mone­
dogs (39%) and cats (25%) in Chile. Chile has recently been classified as tary compensation’, which may be associated with higher number of
a high-income country (World Bank Group, 2022). However, this veterinary facilities and increased economic concentration in Chilean
limited vaccine coverage is more similar to low- and middle-income urban areas (SUBDERE, 2016).
countries (e.g., from 6% in Brazil to 31% in Cameroon in contrast with All tested preventive healthcare measures were at least 30% less
more than 60% in Canada up to 99% in USA) (Alves et al., 2018; Costa likely among senior companion animals compared to adults, as reported
et al., 2018; Evason et al., 2021; Filipe et al., 2021; Kogan et al., 2021; in previous studies (Eschle et al., 2020; Habacher et al., 2010). This may
Prata, 2020). The reasons for not vaccinating their animals were not be related to a greater owners’ concern with primary care in puppies and
asked to owners in our survey. However, a previous SUBDERE pro­ kittens (Eschle et al., 2020) or even a misconception of no risk of in­
gram’s study have associated low levels of responsible ownership of fectious diseases in older animals. The probability of veterinary visits
companion animals with poverty, limited access to public or private was also 40% lower in males. Higher disease prevalence and mortality
veterinary services, lack of knowledge, and other sociodemographic among male companion animals have been associated with a greater
differences between districts and regions across Chile (SUBDERE, 2016). preference of owners to rear males (e.g., to avoid reproductive behav­
Rabies is the only mandatory vaccine in Chile because of the high-risk iors) (Behera et al., 2015; Egenvall et al., 2005; Tagorti, 2019; Uddin
for public health, although the country holds the status of a canine et al., 2021; Yadav et al., 2017). However, our survey included a similar
rabies-free since 2010 (Barrios et al., 2019; Ministerio de Salud de Chile, proportion of male and female companion animals. Further studies on
2003). Given there are no specific regulations for remaining vaccines for behavioral or disease prevalence (e.g., reproductive disorders) differ­
companion animals, we followed the guideline of the SUBDERE program ences between genders are required to understand the lower frequency
(PTRAC, 2022). However, we did not observe differences between the of veterinary visits among males.
proportions of companion animals vaccinated with rabies and with The likelihood of preventive companion animal healthcare in Chile
non-mandatory vaccines. Most infectious diseases circulating among ranged from 3 to 10 times higher among dogs compared to cats, the
dogs and cats in Chile are species-specific (e.g., canine distemper, canine opposite of studies from Europe and North America (Eschle et al., 2020;
parvovirus, and feline retroviruses) (Day et al., 2020; López et al., 2009). Gehrig et al., 2019; Habacher et al., 2010). The proportions of all in­
Therefore, immunizations focused exclusively on animal health may be dicators of the emotional owner-companion animal bond were very
not prioritized by Chilean owners. similar between dogs and cats. Hence, it is unlikely that the dog owners
Vaccinations rates and veterinary visits were positively correlated at of our study were more bonded to their animals than the cat owners.
the district level, which is expected since animal vaccination must be Other reasons not studied here could be reflecting the lower proportion
performed by a veterinarian. This correlation was not detected between of parasite control in cats (61%) compared to dogs (76%) and only 25%
vaccination and parasite control, although they were highly correlated of the cats being vaccinated. For example, restraint techniques during
at the individual level when controlled by other factors in the GLM. In veterinary visits and vaccination may cause stress and fear-aggressive
fact, we found a strong positive association between being vaccinated behavior in feline species (Rodan, 2010; Tateo et al., 2021). Further,
and receiving parasite control, and vice versa. ‘Purebred’ was positively parasite control in cats can also be challenging, particularly if admin­
associated with higher likelihood of both ‘vaccination’ and ‘regular istered orally (e.g., refusing medication in food, spitting out the medi­
veterinary visits’. Owners willing purebreds tend to have more favorable cation, or hypersalivation) (Taylor et al., 2022). These difficulties
economic conditions to buy a companion animal and spend with vet­ experienced by cat owners could discourage them from taking preven­
erinary care (Carvelli et al., 2020; Kardjadj et al., 2020; Sato-Takada tive healthcare measures (Gehrig et al., 2019; Karn-Buehler and Kuhne,
et al., 2022). Veterinary visits were also more likely among 2022). Alternatively, some veterinarians may limit the vaccination

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M. Salgado-Caxito et al. Preventive Veterinary Medicine 213 (2023) 105882

recommendation only to cats at high-risk of viral diseases to avoid side Some limitations in this study could be addressed in future research.
effects (e.g., injection-site associated sarcoma) (Graf et al., 2018; Kass, The subjects of our study were representative of the companion animal
2018). Although this needs further investigation in Chile, a veterinar­ population of Chile (i.e., from districts with different aspects and
ian’s recommendation tends to strongly influence the owners’ decisions randomly selected households). However, responders willing to partic­
regarding their animal (Eschle et al., 2020; Evason et al., 2021). Chile ipate in studies on companion animals could be more aware of respon­
has a high prevalence of feline infectious diseases and urgently needs to sible ownership, which may have resulted in a response bias that cannot
improve preventive healthcare in cats, especially regarding vaccination be easily quantified. In addition, the frequency of vaccination and/or
coverage. Encouraging specializations in feline medicine and adherence veterinary visits may be imprecise as variations related to pandemic
to cat-friendly guidelines in Chile could increase owners’ confidence in COVID could exist. Veterinarians have prioritized emergencies over
adopting preventive healthcare measures. Trained veterinarians could preventive medicine during lockdowns, which could underestimate
reduce negative interactions during consultations, teach owners to preventive healthcare among companion animals in Chile. In contrast,
perform preventive measures at home, and implement preventive health the social isolation caused by the pandemics led owners to spend more
plans for their feline patients. time with their animals, strengthening (or creating) emotional bonds.
Allowing companion animals to sleep indoors was positively corre­ Since this increased interaction could facilitate the recognition of dis­
lated with all preventive healthcare measures evaluated in this study. eases in animals by owners, the demand for veterinary care could have
Further, companion animals acquired for emotional reasons were two increased despite the restrictions. Our main goal in this study was to
times more likely to receive parasite control. Our results support pre­ identify the factors that motivate owners to perform preventive
vious evidence that an emotional owner-companion animal bond could healthcare, regardless of the measure adopted. We have followed the
enhance healthcare in dogs and cats (Gates et al., 2019; Lue et al., 2008; SUBDERE guideline and the Chilean health authority to determinate the
Meyer and Forkman, 2014; Packer et al., 2019). For example, a previous vaccination status of companion animals. While non-mandatory core
study has reported that weak owner-companion animal bonds were vaccinations are recommended annually for dogs and every 3 years for
associated with larger distances covered by free-ranging dogs (Saave­ cats, all companion animals in Chile must be vaccinated annually
dra-Aracena et al., 2021). Conversely, owners who either ‘totally agree’ against rabies. Therefore, all companion animals that received at least
or ‘totally disagree’ with considering their companion animals as family one essential vaccine (polyvalent or rabies) in the last year were
members were more prone to provide vaccination and veterinary visits. considered vaccinated. However, our vaccination coverage results
In fact, the probability was even higher among owners ‘totally dis­ cannot be extrapolated to predict the immunity of the companion ani­
agreeing’ with this statement (5–28 times more likely). Hence, owners’ mal population in Chile, as we did not differentiate between vaccination
willingness to ensure preventive companion animal healthcare may rely agents. Further, many owners were not able to confirm their companion
on multiple factors. For example, non-emotional bonds between owners animal’s vaccination status, which could have underestimated our re­
and their companion animals (e.g., having a companion animal for sults. Therefore, it is crucial to encourage owners to keep a medical
working or sport purposes) can also influence owners’ practices (Eschle record of their companion animals to facilitate access to companion
et al., 2020). Alternatively, we cannot rule out that interviewed owners animal’s health history in the future. Finally, our statistical analyses
could have a better understanding of the importance of preventive could have limited some identification of significance for some vari­
healthcare measures from previous experiences or other sources of in­ ables. For example, within-household and municipality variability could
formation. Thus, additional research focused on other types of social have reduce statistical power to find significant effects for variables with
bonds between owners and companion animals that may influence the high variability. Also, model selection based on their Akaike Information
preventive healthcare in dogs and cats is required. Owners’ ages also Criteria (AIC) was not used giving a relatively large number of missing
factored into preventive healthcare among dogs and cats in Chile. The data across different questions for different individuals. This substan­
Silent Generation and Baby Boomers were 60–94% less likely to vacci­ tially reduced the number of observations required to compare models
nate and take their animals to veterinary visits. Therefore, public pol­ including a combination of different explanatory variables based their
icies promoting preventive healthcare measures in animal health should AIC, since AIC comparison must be performed using the same dataset.
target these generational cohorts (owners with more than 57 years old in
2021). Although the reasons for these observations were not explored by 5. Conclusions
our study, it could be associated with low levels of activity among
elderly owners. Additionally, unhealth behaviors of owners could harm Socioeconomic factors and indicators of the emotional owner-
the health of their companion animals. For example, obese or diabetic companion animal bond were positively associated with preventive
owners are risk factors for nutritional disorders in their animals healthcare among dogs and cats in Chile. Based on our findings, pre­
(Bjørnvad et al., 2019; Delicano et al., 2020). Therefore, encouraging ventive companion animal healthcare interventions should target older,
owners of Silent Generation and Baby Boomers generations to have a male, adopted (not purchased), and mixed-breed animals. Further, it is
healthy lifestyle could simultaneously improve public and animal crucial to promote awareness among cat owners that the benefits of
health. adopting vaccination, parasite control, and regular veterinary visits
In summary, our study highlights that dogs and cats increasingly overcome potential negative and transient effects that might occur.
spend their life in very close physical contact with their owners While our study evidenced the role of the emotional bond in the adop­
(Applebaum et al., 2020; McConnell et al., 2019). As owners and com­ tion of preventive healthcare in companion animals, the owner-
panion animals share a common environment, several infectious dis­ companion animal relationship needs further exploration. For
eases (e.g., antibiotic-resistant bacteria) can be cross-species transmitted example, elucidating how owners interact with their companion animals
in both directions (Baede et al., 2017; Day, 2010; Salgado-Caxito et al., relates to the implementation of preventive veterinary care in dogs and
2021a). Therefore, “One Health” approaches are needed to mitigate cats. Finally, our results highlight an increasingly close contact between
problems that could arise from this close relationship. One Health is a owners and their companion animals that could intensify the risk of
holistic strategy that recognizes that the health of humans, animals, and cross-species disease transmission, leading to important consequences
the environment are intrinsically linked. However, the role of dogs and for public and veterinary health. Enhancing the preventive healthcare in
cats is often underestimated in One Health communications (Overgaauw dogs and cats is essential to overcome the challenges that could arise
et al., 2020). Understanding the owner-companion animal bond and its from this close relationship, encompassing the One Health paradigm.
impact in both animal and public health will require collaborative
transdisciplinary efforts, including psychology, sociology, and other
social sciences.

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M. Salgado-Caxito et al. Preventive Veterinary Medicine 213 (2023) 105882

Funding N., Pompei, J.C.A., Tizzani, P., Carrera, J.E., Ibanez, D., Streicker, D.G., 2020.
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de Animales de Compañía (PTRAC), Subsecretaría de Desarrollo increases the risk of obesity in male dogs but not in bitches — A cross-sectional study
Regional y Administrativo (SUBDERE), Ministerio del Interior y Segur­ of dog- and owner-related risk factors for obesity in Danish companion dogs. Prev.
Vet. Med. 170, 104730 https://doi.org/10.1016/j.prevetmed.2019.104730.
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and their pets: register based cohort study. BMJ m4337. https://doi.org/10.1136/
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