Profile of studies on the welfare of dogs: a systematic review of the literature from 1999 to 2020

: This systematic review of the literature investigates the characteristics of studies related to the welfare of dogs. A survey of the literature data was carried out using PRISMA criteria. It searched for scientific articles published in the electronic database PubMed between 1990 and 2021, in English and/or Portuguese, that offered free electronic access. We searched for the following descriptor terms: apartment dogs, confined dogs, dog welfare, dog well-being, free-ranging dogs, household confined dogs, indoor dogs, movement restrictions of dogs, roaming owned dogs, sheltered dogs, and spatial restriction. Using the PICO strategy included 4 components: studies on dogs (population); welfare assessment (intervention); studies that used positive behavior measures, such as interaction and behavioral responses, to assess dog welfare (comparator); peculiarities of studies referring to the welfare condition of dogs (result). In total, 44 articles published on PubMed were reviewed. Studies related to dog behavioral assessment comprised 50% of those reviewed. The studied population involved 85,492 animals, of which 75% belonged to the following categories: domiciled (household confined – 2 studies – 4,55% plus indoor – 7 studies – 15,9%); free-ranging (7 studies – 15,9%); and shelter (4 studies – 9,1%). The descriptor term most cited in the articles was roaming-owned dogs (10 studies – 22,7%). We conclude that the behavioral assessment of dog welfare is fundamental to improve the relationship between humans and dogs to prevent abandonment.


Introduction
Welfare assessment is a complex variable that depends on hematological, immunological, biochemical, and behavioral parameters, among others.In relation to shelter dogs, there is a protocol often used denominated Shelter Quality, based on four welfare principles: good feeding, good housing, good health, and appropriate behavior (Barnard et al., 2016).
Dogs are affected by experiences lived throughout their lives, in their relationships with humans and other animals.From the evolution of the concept of the five freedoms, the Farm Animal Welfare Council (Fawc, 2009) formulated the concept of animal welfare as a life worth living.This concept aims to minimize negative experiences and maximize those that are positive from the point of view of the animal.For this, we luckily have several tools to assess animal welfare.
Space deprivation can certainly be included among the limiting situations for the comfort that one hopes to offer animals.However, free access to the outdoors can also be life-threatening.Therefore, domiciled and loose dogs are expected to be the group with the best quality of life.In the British Animal Welfare Act (Animal Welfare Act, 2006), we find the concept of Duty of Care, which mentions that a person responsible by an animal must steps as are reasonable in all the circumstances to ensure that its needs are met according good practice.In the case that this not occur, the person commits an offense.Thus, examples of these needs are a suitable environment, a suitable diet, to be able to exhibit normal behavior patterns, to be housed with, or apart from, other animals, and to be protected from pain, suffering, injury and disease (Animal Welfare Act, 2006).
There is a trend toward assessing dog welfare via measures that reflect positive response behaviors, indicators of positive emotional status.These measures include animal autonomy, play, positive affect, positive human-animal relationships, social interaction, and appropriate genetic selection.Since this, positive welfare measures are more aligned with preventing behavioral disorders and, consequently, dog abandonment to the detriment of behavioral responses indicating responses to negative experiences, such as fear, stress, and pain (Vigors and Lawrence, 2019).
Finally, it is important to mention that the prioritized welfare issues include the lack of knowledge of welfare needs, social behavior issues, problem behaviors, inappropriate diet and environment, lack of veterinary care, consequences from breeding decisions, poor pain management, delayed euthanasia and chronic ill health (Rioja-Lang et al, 2020).However, a study listed the top 10 reasons for relinquishment due behavior of dogs: bites, aggressive toward people, escapes, destructive inside, destructive outside, disobedient, problems between new pet and other pets, aggressive toward animals, soil house, and loud vocalization (Salman et al., 2000).
In view of the above, we conducted a descriptive study via a systematic review of the literature using the criteria of Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRIMA) (Moher et al., 2015), which seeks to identify the main characteristics of studies analyzing dog welfare.

Materials e Methods
A survey of literature data was carried out by selecting scientific articles published on the PubMed database between January 1990 to January 2021 which were written in English or Portuguese and offered free electronic access.We searched for the following descriptor terms: apartment dogs, confined dogs, dog welfare, dog well-being, free-ranging dogs, household confined dogs, indoor dogs, movement restrictions of dogs, roaming owned dogs, sheltered dogs, and spatial restriction of dogs.Initially, the studies were separated by title, and then by abstract.Finally, the selected studies were fully read.Studies were chosen as eligible only after these steps.Studies involving purebred dogs; mixed-breed; female; male; of any age; in variable body condition; spayed or not; neutered or not; owned confined, owned free-roaming, free-ranging, and shelter dogs were included.Studies assessing the welfare of dogs in any type of confinement via clinical, physiological, hormonal, and immunological parameters were selected, as well as studies measuring behavior by ethograms.
This systematic review sought to compare studies which used measures of positive behavior for evaluating dog welfare, such as interaction and behavioral responses.Our results show the connection between the preference of dogs for human proximity as gauged by their positive behavioral outcomes.For the construction of the Wordcloud data from the articles were imported into a spreadsheet using Bibliometrix.The analysis was conducted with a focus on titles, enabling the identification of the most frequent words.Consequently, the Wordcloud was generated to illustrate the terms that exhibited higher occurrences.

Results
Our results evinced the peculiarities of the studies assessing dog welfare.Initially, we found 87 articles containing the search terms descriptors (Figure 1) on the PubMed database.However, we included 44 articles in this systematic review, as follows: confined dogs ( 6), dog welfare (1), dog well-being (1), free-ranging dogs (7), household confined dogs (2), indoor dogs (7), movement restrictions of dogs (3), roaming owned dogs (10), sheltered dogs (4) and spatial restriction of dogs (3) (Table 1).The most common descriptor term in the studies was roaming owned dogs with a 22.72% frequency.

Title Year Country
Confined dogs Regarding the year of publication of the studies included in this review, we found that 65.91% (29) were published in the years 2017, 2018, 2019, and 2020.This finding shows the growing interest in animal welfare in recent years.The countries of origin of the selected studies with the highest frequency were: United States (7); India (6); Australia (4); United Kingdom (4); and France (4), representing 54.54% (24) of the studies included in this research.The n sampling of dogs in the studies included in this systematic review totaled 85,492 animals (Table 2).Only 10 articles provided information about the sex of the studied dogs.Of these, 30,581 were females and only 6,505 were males.

N sampling
Group of dogs  Regarding the group of dogs studied in the articles included in this review: 75% belonged to the following categories: domiciled (16); strays (9); and shelter dogs (8) (Table 2).

Parameters evaluated grouped by descriptor term confined dogs
Confinement, neutering, and vaccinations for rabies Antibodies against rabies virus in sera Behavioral observations: Dog Personality Questionnaire Survey of dog owners about escape rates for confined dogs and history of biting Elimination behavior of shelter dogs

Estimates of fecundity and longevity in roaming dogs
dog welfare

Retrospective study about eight common canine disease dog well-being
Assessment of the effectiveness of a combined people and pet weight loss programme free-ranging dogs

Assessment of reproductive patterns and disorders during neutering
Immediate social reward and long-term food and social rewards Roaming monitoring in free-roaming domestic dogs using global positioning system (GPS); identification of roaming predictors (the sex and reproductive status of the dogs) Denning habits and preference for human proximity

Behavioral interactions
Persistence when presented with a novel object containing food that could not be accessed
Regarding behavioral parameters, 54.55% ( 12) of studies were related to positive behavior measures, such as interaction and behavioral responses, whereas 45.45% (10) of the behavioral studies emphasized negative measures of behavior such as disorders and stress.Among the studies that used positive behavior measures, seven (58.33%) evinced the preference of dogs due to human proximity and five (41,67%) were conducted only with canine behavior.Finally, when we build a Wordcloud (Figure 2) including the most cited words in the articles.

Discussion
In view of the importance to perform studies of welfare of dogs, the present review of literature compiled 44 studies around this issue, demonstrating the main characteristics of dog welfare studies.The studies address domiciled (named household confined dogs and plus indoor) dogs; totaling 85.492 animals.However, the studies described more about free-ranging dogs.
In relation to dogs behavior, the studies included in this review demonstrated different standards when analyzed by category as domiciled, free-ranging or shelter dogs.In this sense, domiciled dogs prefer to stay near humans and this preference of dogs for denning close to humans is a behavior adaptation (Majumder et al., 2016).Furthermore, the dogs tend to build trust based on affection, not food (Bhattacharjee et al., 2017).However, free-ranging dogs show a different behavior than that of the shelter and pet dogs (Bhattacharjee et al., 2019).According a study performed by Brubaker et al. (2019) studying canine gazing behavior, they found that free-ranging dogs responded to the human's change in attentional state by looking significantly less at the human in the inattentive condition compared to the attentive condition.On the other hand, pet and shelter dogs gazed significantly more at the human in both the inattentive and attentive conditions and also spent more time in the proximity of the experimenter.
According to a Serpell (2017) study, pet and shelter dogs pay special attention to humans and especially to their owners or caregivers with whom they usually have a more interactive relationship, different from free-ranging dogs.As an example for this, Duranton and her group of researchers conducted three studies with indoor pet dogs (Duranton et al., 2017), outdoor pet dogs (Duranton et al., 2018) and shelter dogs (Duranton et al., 2019).Regarding indoor pet dogs, they visibly synchronized their location with their owner (staying in close proximity and moving to the same area), as well as their activity and temporal changes in activity (moving when their owner moved, standing still when their owner stood still, and gazing in the same direction as their owner) (Duranton et al, 2017).About outdoor pet dogs, they synchronized both their location (staying in close proximity) and their activity (moving when their owner moved, and at the same pace, and standing still when their owner stood still) with those of their owners (Duranton et al., 2018).Finally, in relation to shelter dogs, they synchronized their locomotor activity with their caregiver less strongly than pet dogs of the both previous studies.Shelter dogs also maintained greater distances to their caregivers than pet dogs with their owners (Duranton et al., 2019).

Conclusion
There is a growing interest in monitoring dog welfare, especially in developed countries.This study found that most studies on dog welfare use tools to assess the behavior of owned dogs, following the trend of using positive welfare indicators.With the advances in our understanding of canine behavior, we will be able to use tools and strategies to improve our relationship with dogs, preventing undesirable behaviors that often lead to their abandonment.Dogs prefer proximity to humans and are even able to synchronize their behavior with their owners or caregivers.The history of the relationship between humans and dogs started centuries ago, motivated by mutual benefit.This relationship, nowadays, requires commitment from humans, as well as respect for our friendship with dogs.

Figure 1 -
Figure 1 -Article selection flowchart.* One of the articles identified was neither a duplicate nor a complete article.

Figure 2 -
Figure 2 -Wordcloud with the main words presented into the 44 articles included in this systematic review.

Table 1 -
Escape rates and biting histories of dogs confined to their owner's property through the use of various containment methods United States 5 Elimination behavior of shelter dogs housed in double compartment kennels 2014 United States 6 Fecundity and longevity of roaming dogs in Jaipur, India 2008 India Assessing reproductive patterns and disorders in free-ranging dogs in Jodhpur, India to optimize a population control program India 10 Free-ranging dogs prefer petting over food in repeated interactions with unfamiliar humans India 11 What influences the home range size of free-roaming domestic dogs?Australia 12 Denning habits of free-ranging dogs reveal preference for human proximity India 13 The great Indian joint families of free-ranging dogs India 14 The role of life experience in affecting persistence: A comparative study between free-ranging dogs, pet dogs and captive pack dogs Austria 15 Free-ranging dogs show age related plasticity in their ability to follow human pointing India Household confined dogs 16 Clinical features and outcome in dogs and cats with obsessive-compulsive disorder: 126 Cases Articles selected grouped by descriptor term and included in the systematic review.
1 Care of Dogs and Attitudes of Dog Owners in Port-au-Prince, the Republic of Haiti 2012 Haiti 2 Prevalence of antibody against rabies among confined, free-roaming and stray dogs in a transit city of Nigeria.2011 Nigeria 3 Companion and free-ranging Bali dogs: Environmental links with personality traits in an endemic dog population of South East Asia 2018 Bali 4

Table 2 -
Characterization of the studied dog population grouped by descriptor term.
Acceptability and preference for sucrose and monosodium glutamate; anhedonia assessment in domestic dogs Behavioral and physiological measurements of dogs in chronic stress subjected to social and spatial restriction Hormonal and immunological responses of dogs in chronic stress subjected to social and spatial restriction; catecholamines, cortisol, and leucocytes

Table 3 -
Parameters evaluated in selected studies.