How To Evaluate and Manage Stress in Dogs - A Guide For Veterinary Specialist

Applied Animal Behaviour Science 243 (2021) 105458
Contents lists available at ScienceDirect
Applied Animal Behaviour Science

journal homepage: www.elsevier.com/locate/applanim
How to evaluate and manage stress in dogs – A guide for

veterinary specialist
I.A. Kartashova a, *, K.K. Ganina a, E.A. Karelina a, S.A. Tarasov a, b
a
OOO "NPF" Materia Medica Holding", Moscow, Russian Federation
b
The Institute of General Pathology and Pathophysiology, Moscow, Russian Federation
A R T I C L E I N F O A B S T R A C T
Keywords: Stress has a significant impact on the health and well-being of dogs and can seriously affect the quality of daily
Stress life, veterinary clinics procedures and shelters routine. That means veterinary specialists need to be armed with
Dogs valid and convenient tools to assess their patients’ stress levels, both behavioral and physiological. For this re
Cortisol
view we analyzed 128 articles in order to summarize methods of stress assessment in different clinical and
Welfare
Stress scale
experimental environments, as well as methods to alleviate stress. We have also identified the most common
forms of stress-related behavior in various situations. Stress in dogs seems to be well studied, but we have not
found any universal quantitative and qualitative indicators of stress, nor clear reference intervals even for such a
basic stress hormone as cortisol, nor standard generally accepted protocols for the prevention, control and
correction of stress in pets. That means an individual approach is necessary for each case. Analysis of the animal’s
behavior during a veterinary appointment together with collecting a detailed patient history and correct se
lection and appropriate combination of different physiological stress markers is the most reliable way to interpret
psychological state of the dog and make a more accurate diagnosis.
1. Introduction their reliability in pets both separately and in combination. In addition

to cortisol as the most popular stress marker, prolactin (Gutiérrez et al.,
The issue of stress and anxiety attracts a lot of attention not only in 2019a), secretory immunoglobulin A (Lensen et al., 2019), saliva cate
the context of daily life of a domestic dog, but also as a complicating statin and vasostatin (Srithunyarat et al., 2018) and other potential
factor at veterinary clinics appointments and in shelters (Edwards et al., markers are being studied. Blood biochemistry analysis and cell count
2019a; Gunter et al., 2019; Lloyd, 2017; Mariti et al., 2015; Willen et al., can also be used for stress measurement along with physiological values
2018). In the absence of universally approved guidelines and defined such as heart rate and heart rate variability (Bergeron et al., 2002; Liang
normal ranges of stress markers, veterinarians need to make complex et al., 2018; Ortmeyer and Katzel, 2020; Perego et al., 2014).
decisions to find an accurate diagnosis and analysis stress levels (Lefman Currently, in addition to the physiological parameters of stress, sci
and Prittie, 2019). Choosing physiological markers and explaining the entists have begun to consider the visual assessment of dogs’ behavior
analysis results can be the first difficult question when working with under stress (Dreschel and Granger, 2005; Srithunyarat et al., 2018).
stressed animals, since for a more accurate identification of stress it is Interpreting animal behavior at a veterinarian’s appointment, in a
important to rely not only on physiological parameters, but also to take shelter or at home can also be difficult for a veterinarian, because in
into account the details of the dog’s daily life, their age, concomitant different articles we found different sets of terms describing calm
diseases and treatment, experience of veterinary clinics visits, level of behavior and behavior under stress (Dreschel and Granger, 2005;
physical activity and even the temperament of the owner, and other Hernander, 2008; Srithunyarat et al., 2018). Fixed definitions would be
factors (Landsberg et al., 2011; Packer et al., 2019; Srithunyarat et al., particularly useful. Of course, when interpreting the dog’s behavior at
2017; Sundman et al., 2019). While the owners typically are able to the appointment, it is also necessary to consider individual experience,
recognize the signs of stress in their pets, sometimes behavioral patterns environmental conditions and the method of sampling. Invasive and
can be misinterpreted (Mariti et al., 2015). The difficulty of biomarker non-invasive methods of taking samples can cause severe stress in dogs
selection also increases because of the insufficient amount of data on that are not accustomed to the procedures in advance. To understand
* Corresponding author.
E-mail address: kartashovaia@materiamedica.ru (I.A. Kartashova).
https://doi.org/10.1016/j.applanim.2021.105458
Received 19 February 2021; Received in revised form 28 August 2021; Accepted 16 September 2021
Available online 20 September 2021
0168-1591/© 2021 Elsevier B.V. All rights reserved.
I.A. Kartashova et al. Applied Animal Behaviour Science 243 (2021) 105458
whether dogs experience stress during diagnostic procedures and diseases requiring hospital treatment (Yuki et al., 2019). However,
whether this may affect further results, some researchers focus on invasive diagnostic methods can be painful and cause acute stress and
analyzing the animal’s behavior, body position, and vocalization (Sri short-term elevation of cortisol level (Corder-Ramos et al., 2019; Righi
thunyarat et al., 2018). et al., 2019). Can a sharp increase in the level of the hormone be reli
In this review, we analyzed the described physiological methods of able? Measuring saliva cortisol is a less painful and stressful method of
stress assessment, their advantages and disadvantages, summarized vi analysis, but it is also not the easiest sampling method, for example, in
sual signs of calm and stressed dogs’ behavior, and reviewed pharma aggressive or dehydrated patients (Schöberl et al., 2017). But both in
cological and non-pharmacological methods to alleviate stress. Analysis blood and in saliva, there is a fairly large range of variation of cortisol
of the animal’s behavior and changes in physiological parameters under concentration according to the research results. We have analyzed the
stress can help to correctly interpret its psychological state, make a more literature and collected results of changes in the concentration of
accurate diagnosis and choose the correct pharmacological therapy. We cortisol in blood and saliva in various stress-related situations in Table 1,
studied various scales of visual signs of stress in dogs, identified the most as well as indicated some reference intervals. Since the articles listed
common forms of stressful behavior in various situations and concluded different units for measuring cortisol concentration, it was decided to
on the most reliable way to approach the problem of stress detection and convert everything into the most commonly used unit nmol/L. We
treatment. included only those articles that indicated the exact values of cortisol
concentrations. Table 1 shows data on blood and saliva, as these in
2. Methods for literature review dicators are most common. The level of cortisol in faeces and fur is less
studied, so there is not enough data to compare the results. This is
For this review references from 1997 to 2021 were analyzed in order probably because research on acute stress is most relevant in veterinary
to assess different approaches to stress level measurement both in clinics, and chronic stress is more often studied in shelters and in wild
experimental and everyday circumstances, as well as methods of stress animal populations. Despite the availability and popularity of cortisol
management. More than half of the articles (57%) were published after assessment, Table 1 shows that norms vary, so you cannot rely on it
2016. PubMed database and websites of specialized scientific journals alone when assessing stress.
were used for the information search. To determine the relevance of the Assessment of fecal cortisol levels is convenient when working with
articles first of all the abstracts were considered. To clarify the infor shelter dogs (Righi et al., 2019) and wild animals. For example, Van den
mation the articles were considered in more detail. After that, some Berghe and colleagues evaluated the effect of pheromones on stress
articles were excluded because they did not contain relevant informa levels in wild African dogs (Van den Berghe et al., 2019) and Molnar
tion for this review. The search for articles was conducted on such et al. studied changes in the concentration of fecal cortisol metabolites
keywords as "stress", "dogs", "behavior", "correction", "therapy", "stress (FCM) as a stress indicator in members of eleven wolf packs (Molnar
scale", "emotional contagion", "markers", "cortisol", "prolactin", "alpha- et al., 2015). It was found that the level of FCM changes in animals
amylase", "sIgA", "heart rate", "pain", "disease", "shelter", "veterinary during social and territorial instability, but does not depend on age,
clinic" and their combinations. After analyzing the literature, 128 arti gender, or social status (Molnar et al., 2015). The concentration of
cles were selected that fit the purposes of this review. cortisol in a dog’s fur can be a good indicator of chronic stress (Heather
M Bryan et al., 2013; Packer et al., 2019). This is a perspective method
3. Physiological markers of stress. Can we rely on them for studying long-term stress. The method is convenient because a single
completely? probe can show how the cortisol level changed in a certain time period.
The study of dog hair cortisol revealed common factors associated with
The mechanisms of stress response by the hypothalamic-pituitary- increased cortisol concentrations, such as living in a home with more
adrenal and the sympathetic-adrenal medullary systems are well than three dogs and participating in sports competitions. Anxiety in the
described (Marques et al., 2010; Overall, 1997). Glucocorticoids, in presence of a stranger, social anxiety, and the presence of concomitant
particular cortisol, are diagnostically measured in dogs in cases of diseases were factors that lower the concentration of cortisol in the hair
endocrine or dermatological diseases and for determining the level of (Packer et al., 2019). Interestingly, when moving kennel dogs from a
stress (Wenger-Riggenbach et al., 2010). In most cases, severe acute or single enclosure to a double enclosure, the level of cortisol in the hair
chronic stress is reflected by an increased or decreased blood level of decreased, which indicates the importance of the social factor in the
catecholamines, which can be accompanied by the changes of neu study of chronic stress (Grigg et al., 2017). Cortisol immunoreactivity in
trophils/lymphocytes ratio, bradycardia or tachycardia, heart rhythm hair has also been shown to be less variable than saliva and faeces
disorder and other parameters(Ortmeyer and Katzel, 2020; Overall, (Heather M Bryan et al., 2013). However, it is also dependent on other
1997). But all these indicators are ambiguous. For example, the level of pathological processes. For example, a significant positive correlation
corticosteroids during isolation or overpopulation of dogs may depend was revealed in a study of the effect of the degree of skin damage in
on how socially active the dog is, and how much the animal seeks atopic dermatitis of dogs according to modified CADESI-03 scale on the
contact with individuals of its own species in a calm situation (Overall, level of hair cortisol (Park et al., 2016). In addition to that age, preg
1997). The concentration of a physiological indicator depends not only nancy, hair color, body region, sex and season of year may affect the
on the level of stress experienced, but also on concomitant somatic concentration of hair cortisol (Heimbürge et al., 2019). There is
diseases, as well as medication (Boretti et al., 2015; Packer et al., 2019; currently insufficient evidence to conclude that cortisol concentration in
Pessina et al., 2009). hair accurately reflects long-term blood cortisol concentrations. Simi
larly, there is a lack of information surrounding the mechanisms of
3.1. Cortisol cortisol incorporation into the hair (Burnard et al., 2017). So, while the
level of hair cortisol is convenient for chronic stress assessment in dogs,
Cortisol is one of the most studied biomarkers of stress. It is generally it should be further researched.
assumed that an increase in its concentration is a clear indicator of stress
in an animal, but is this true? It has been shown that chronic stress can 3.2. Somatic diseases and medication
lead to the depletion of energy resources and, as a result, to a decrease in
cortisol levels, as the adrenal glands become unable to maintain its When studying stress levels, it is also important to consider the
concentration at a certain level (Righi et al., 2019). Another issue is possible presence of various acute and chronic diseases, as they can
related to methods of probe collection. Serum cortisol concentrations affect cortisol levels. In some diseases, the level of cortisol may decrease,
can be a useful biomarker for predicting the survival of dogs with while in others it may become higher. Epilepsy can trigger a decrease in
2
Table 1
Ranges of blood and saliva levels of cortisol.
Cortisol concentration Comment Reference
Blood (nmol/L)
Data presented as min – max values Dogs (n = 5) were administered saline treatment two weeks prior to (Corder-Ramos et al., 2019)
Saline lipopolysaccharide (LPS) treatment. Blood samples were collected 24 h before
Baseline 33.1 − 80.0 treatment (baseline data) and 3, 6 and 24 h after treatment in the clinic.
3 h. 46.9 − 703.5 The institutional reference interval for canine cortisol (based on n = 95
6 h. 27.6 – 93.8 clinically healthy dogs of varying breeds) is declared as 27.6–165.5 nmol/L
24 h. (n = 4) 27.6–38.6
LPS
Baseline 2.2–96.6
3 h. 441.6 − 712.1
6 h. 74.5 – 364.3
24 h. (n = 4) 33.1–113.2
Data presented as average ± SE Dogs of group I (n = 9) were delivered to the veterinary clinic and stayed in (Juodžentė et al., 2018)
Group I T0 69.0 ± 7.4 the room for 12 h before the operation (T0 and T1), and dogs of group II (n =
Group I T1 187.9 ± 9.4 9) were in the room for 10 min before the operation (T1).
Group II T1 73.1 ± 39.2
Data presented as interquartile range The survival rate for 30 days from the moment of hospitalization was studied (Yuki et al., 2019)
At 0 h in dogs (n = 67). The number of neutrophils, lymphocytes, blood glucose
Survivor group (n = 42) 126.9–504.9 concentration and cortisol were measured after 0 and 24 h after
Non-survivor group (n = 25) 173.8–631.8 hospitalization.
At 24 h The institutional reference interval 27.6–165.5 nmol/L
Survivor group (n = 42) 102.1–237.3
Non-survivor group (n = 20) 195.9–435.9
Data presented as mean ± SD The study compared the effectiveness of a simple method of laparoscopic (Devitt et al., 2005)
LAOHE assisted ovariohysterectomy (LAOHE) with open ovariohysterectomy (OHE).
Preoperative 93.8 ± 57.9 Concentration of cortisol and glucose in the blood serum was measured
1 h 173.8 ± 132.4 before the operation and 1, 2, 4, 6, 12 and 24 h after the operation in dogs (n
2 h 126.9 ± 124.2 = 20).
4 h 115.9 ± 132.4
6 h 85.5 ± 66.2
12 h 66.2 ± 52.4
24 h 57.9 ± 35.9
OHE
Preoperative 85.5 ± 52.4
1 h 242.8 ± 99.3
2 h 182.1 ± 115.9
4 h 143.5 ± 63.5
6 h 85.5 ± 63.5
12 h 80.0 ± 52.4
24 h 60.7 ± 38.6
Data presented as mean ± SD, min –max values All dogs (n = 40) were kept in the shelter for more than 155 days. Blood (Gutiérrez et al., 2019a)
71.7 ± 55.2, 12.2–234.9 serum samples were collected in the range of 5–15 min after entering the
sampling room with minimal possible stress level. All dogs were healthy and
regularly checked by a veterinarian.
Data presented as min–max values Relationship among cortisol, oxytocin and exploratory and play-soliciting (Rossi et al., 2018)
3.0 – 23.5 behaviors was studied in dogs (n = 14). Blood samples were taken in the clinic
after conducting behavioral tests.
Data presented as mean ± SD Healthy female dogs (n = 30) admitted for planned ovariohysterectomy. (Srithunyarat et al., 2016)
Before surgery 174.6 ± 78.5 Blood samples for cortisol measurement were collected before surgery, 3 h
Three hours after extubation 162.4 ± 88.4 after extubation, and once 7–15 days after surgery. Dogs were pretreated with
Recall 122.8 ± 63.5 morphine and received carprofen as an analgesic for 7 days in the
postoperative period.
Data presented as mean ± SE Saliva and blood samples were taken before ground and air transportation (Bergeron et al., 2002)
Before ground transportation (baseline) and after air transportion. Dogs (n = 24) were transported either under
C 146.2 ± 24.6 S 122.8 ± 22.3 sedation (S) with 0.5 mg / kg body weight of acepromazine maleate or
Before air transportation without sedation (С), after being transported by road. The results for saliva
C 215.4 ± 32.4 S 235.2 ± 49.0 cortisol of the same dogs are presented below in this Table.
After air transportation
C 115.0 ± 26.8 S 191.5 ± 27.4
Data presented as median (IQR), min and max value Prospective observational study. Cortisol variability was studied in healthy (Höglund et al., 2016)
Boxer dogs (n = 531) of 9 different breeds at 5 veterinary centers.
31.5 (20.3–40.3), 13.0–97.0
Belgian Shepherd
39.0 (26.0–65.0), 6.0 – 321.0
Cavalier King Charles Spaniel 39.0 (32.0–60.5),
13.0 – 105.0
Dachshund
41.0 (26.0–50.5), 9.0 – 205.0
Doberman Pinschers
37.5 (32.3–72.3), 19.0 – 103.0
Lapphund
85.0 (52.0–127), 17.0 –253.0
German Shepherd
55.0 (28.5–96.5), 9.0 – 250.0
(continued on next page)
3
Table 1 (continued )
Cortisol concentration Comment Reference
Labrador retriever
45.0 (30.0–88.8), 6.0 – 271.0
Newfoundland
63.5 (37.0–89.8), 12.0 – 198.0
Median cortisol concentration 46.0 (IQR,
29.0–80.8) in all dogs
Data presented as mean ± SD The dogs were divided into 2 groups: group A waited inside the clinic (n = 9) (Perego et al., 2014)
Group A 179.89 ± 91.87 and a control group B (n = 9) waited outside in the garden.
Group B 79.74 ± 32.00 Reference interval from Clinical Diagnostic Laboratory, Department of
Clinical Science, University of Milan (CI 95%); n = 120 dogs. Cortisol (nmol/
L) 18.21–82.77
Data presented as mean ± SD A group of dogs familiar (n = 33) and not familiar (n = 30) with the blood (Srithunyarat et al., 2018)
Familiar 65 ± 28 sampling procedure.
Not familiar 175 ± 79
Data presented as mean ± SD Dogs (n = 14) with fractures of the hind limb or pelvis and healthy dogs (n = (Srithunyarat et al., 2017)
Healthy dogs 174.6 ± 78.5 30). Blood was collected once in healthy dogs and in dogs with fractures
Before morphine 108.1 ± 69.0 before and 35–70 min after administration of morphine.
After morphine 130.9 ± 93.6
Data presented as median (IQR) Blood samples were taken before and after interaction with dogs (n = 18). (Odendaal and Meintjes, 2003)
Median before 366.5 (202.0) Interaction consisted only of social gestures (quiet conversation, gentle
Median after 416.0 (248.0) stroking the dog with long, smooth movements, low-key games, and
scratching its body and ears). During this time, people’s attention was
completely focused on the dog.
Saliva (nmol/L)
Data presented as mean ± SE Saliva samples were taken before ground and air transportation and after air (Bergeron et al., 2002)
Before ground transportation (baseline) transportation. Dogs (n = 24) were transported either under sedation (with
C 12.3 ± 1.2 S 12.8 ± 1.2 0.5 mg / kg body weight of acepromazine maleate) or without sedation
Before air transportation (control), after being transported by road.
C 16.8 ± 2.0 S 15.6 ± 2.1
After air transportation
C 15.3 ± 2.5 S 14.4 ± 1.8
Data presented as mean ± SD Dogs (n = 7) were kept at the University of Saskatchewan’s Zoo resource (Heather MBryan et al., 2013)
3.9 ± 0.2 center for veterinary students training. Saliva samples (n = 181) were
collected from each dog twice a week.
Data presented as mean ± SD А significant relationship was found between the level of cortisol in saliva of (Handlers, 2020)
Before the examination 11.6 ± 7.7 search and rescue dogs (n = 41) and their guides. Participants did not report
After the examination chronic illnesses in their dogs or constant medication. Saliva was collected
13.5 ± 8.8 from dogs before and immediately after the clinical examination
(approximately 30 min after taking the first sample).
Data presented as mean ± SD In dogs (n = 9) after training session cortisol dropped by 18.8%. During saliva (Da SilvaVasconcellos et al., 2016)
Before training collection, as well as during training sessions, the animals were rewarded
6.3 ± 0.4 only with cheese to control the effect of proteins in the saliva samples. Saliva
After training was collected 2–10 min before and 15 min after the end of each workout.
5.1 ± 0.4
the level of hair cortisol, and various antiepileptic drugs were also experience, and environment in the sample collection room may also
demonstrated to affect cortisol concentration. It was shown that after affect the results. The time spent in a veterinary clinic should also be
administration of phenobarbital and potassium bromide cortisol levels taken into account when analyzing the level of cortisol in patients. In
decreased, while after imepitoin treatment cortisol levels were signifi dogs that were brought for surgery in advance (12 h), the level of cortisol
cantly increased (Packer et al., 2019). When Cushing’s syndrome was was significantly higher than in dogs that were brought to the clinic 10
diagnosed using an ACTH stimulation test or a low-Dexamethasone test, min before the examination and procedures. The level of cortisol
there was a difference in cortisol response to treatment depending on the significantly changed if the dog remained without an owner for a long
dog’s sex. The increase in cortisol levels after ACTH injection in female time, which could lead to a slowdown in wound healing and to other
dogs was significantly higher than in males. In male dogs treated with health problems (Juodžentė et al., 2018). It is also important where the
dexamethasone, cortisol levels decreased to normal levels faster than in dog waits for the appointment. If the dog and its owner stay in a quiet
female dogs (Pessina et al., 2009). In dogs with hypoadrenocorticism the place, such as a garden outside the clinic, cortisol levels are lower than
cortisol-to-ACTH ratio was significantly lower than in healthy dogs and for those who spend a lot of time in the waiting room (Perego et al.,
in dogs with diseases that mimic hypoadrenocorticism (Boretti et al., 2014). In addition, previous experience and familiarity with clinical
2015). Serum cortisol concentrations in dogs with atypical hyper procedures can also alter the level of cortisol in the dog’s blood (Sri
adrenocorticism were elevated compared to controls, but less than in thunyarat et al., 2017). The concentration of cortisol in the blood serum
dogs with hyperadrenocorticism. The authors suggest that excess can be a useful predictive marker in dogs during hospitalization. The
cortisol can serve as a characteristic marker of the pathophysiology of survival rate in dogs after 30 days of hospitalization was significantly
atypical hyperadrenocorticism (Frank et al., 2015). Since stress and higher if 24 h after hospitalization the analysis showed a lower con
other somatic conditions play a large role and their effects can interfere, centration of cortisol (Yuki et al., 2019). That means that during the first
it is necessary to make a very careful differential diagnosis with cortisol day of being admitted it is extremely important to relieve stress,
level as a marker. including the stress from hospitalization.
When interpreting stress levels based on cortisol concentration, it is
important to consider the level of acute stress, as well as the patient’s
3.3. Stress in the clinic personal experience, emotional state, and the environmental conditions
during waiting and manipulations.
It is important to remember that sample collection method, the dog’s
4
3.4. Pain and post-surgery stress behavior of dogs depending on the emotional state of their owners. An
increase in the dogs’ heart rate was shown only during the stress of the
Pain as a stress factor can also be the cause of an increase of cortisol owner. There were no significant differences in the saliva level of
blood level (Mastrocinque and Fantoni, 2003), and this change may cortisol in dogs tested with stressed or calm owners. However, the
serve as a tool for determining analgesic efficacy (Martins et al., 2010). presence of strangers and new environment could have influenced the
A separate category of stress associated with veterinary clinics is post results in both groups. (Carballo et al., 2020). The study of chronic stress
operative stress (Devitt et al., 2005). Both from the etiological point of showed a seasonal interspecific correlation of cortisol concentration in
view and from the point of view of correction, it differs from psycho the hair of dogs and humans (summer and winter). In addition, the
logical stress. Analysis of the operation time, severity of complications, emotional state of dogs can be affected by the stress resistance and
indicators of surgical stress and postoperative pain when comparing the temperament of their owners. Such human personality traits as
effectiveness of two types of surgery (laparoscopic assisted ovar neuroticism, conscientiousness, and openness significantly affected the
iohysterectomy (LAOHE) or open ovariohysterectomy (OHE)) showed hair cortisol concentrations of their dogs (Sundman et al., 2019). When
that cortisol concentrations were significantly higher 1 and 2 h after studying dog’s attachment to the owner the correlation, was found not
surgery in the OHE group (Devitt et al., 2005). Serum cortisol level was only between changes in the physiological indicators of stress of the dog
also elevated in the NOTES (natural orifice transluminal endoscopic and the owner, but also in the behavior of the dog (Ryan et al., 2019). A
surgery) group from 6 to 72 h after surgery, while in the laparoscopic similar pattern was also found for the level of cortisol in saliva of search
procedure group – only up to 12 h (Freeman et al., 2010). Another study and rescue dogs and their guides. In addition, it turned out that this
showed that postoperative serum cortisol concentrations increase hormonal synchronization in the pairs was stronger between female
significantly for dogs, and the rise in serum cortisol was not significantly (woman – female dog) than male (man – male dog) individuals (Han
affected by surgeon experience or the duration of the ovariohyster dlers, 2020). In other studies it has been shown that as a rule, male
ectomy (Michelsen et al., 2012). In the study of dogs with orthopedic owners – male dogs pairs had the lowest cortisol reactivity compared to
diseases, the analysis of serum cortisol level did not reveal significant all other combinations of the owner’s gender and the dog’s sex (Schöberl
differences between the pain groups. The authors believe that the level et al., 2016). However, female owners of male dogs had a lower cortisol
of cortisol should not be regarded as a “critical", but rather as an dispersion coefficient (Schöberl et al., 2017). More research is needed to
”indicative” biomarker of pain in the clinical assessment of dogs (Mar determine the relationship of cortisol concentration to the sex of the
kovszky et al., 2020). Similarly, to stress measurement, there is no owner-pet pair. Meanwhile, during clinical appointment it is important
universal specific biomarker that can assess the degree of pain in ani to pay attention to the behavior of not only the patient, but also of its
mals. Therefore, for an objective assessment, it is necessary to compre owner. These observations may be helpful for the interpretation of
hensively analyze physiological parameters such as heart rate, cortisol analysis results and its role in the animal’s stress level (Ryan
respiratory rate, blood pressure, temperature, and biochemical markers et al., 2019; Sundman et al., 2019).
such as cortisol, catecholamines, lactate, glucose, and IL-1, IL-6 in
addition to the assessment of the PTA index or HRV and behavior-based 3.6. Stress and physical activity
pain scales (Hernández-Avalos et al., 2021).
Intense physical activity causes oxidative stress and possible
3.5. Interspecies and intraspecies synchronization of emotions and stress inflammation of the gastrointestinal tract in dogs (Zannoni et al., 2020).
High rates of gastritis and stomach ulcers were observed in sled dogs
Emotional contagion is a common factor of everyday life. This psy participating in endurance races (Fergestad et al., 2016). Participation
chological phenomenon can affect the mood and emotional state of both in the 500–600 km race was associated with a significant increase in the
owners and their pets. The comparison between breed groups showed blood level of gastrin, cortisol and C-reactive protein. However, studies
that herding dogs most often show interspecific long-term synchroni have shown that not every type of physical activity can induce promi
zation of stress, and ancient breed groups are the least affected by the nent changes in cortisol levels. Higher level of daily activity together
owner. Hunting dogs show clear dependence of stress-related parame with the owner did not increase the concentration of hair cortisol and
ters on both owner personality traits and their relationship. Long-term neither did the number of training sessions per week during summer and
stress synchronization may be a characteristic feature of breeds specif winter periods (Sundman et al., 2019). Interestingly, assessment of
ically selected for human cooperation. (Höglin et al., 2021). In dogs with gastrointestinal disorders in hunting dogs revealed no differences in the
noise phobia during the imitation of thunderstorm sounds cortisol content of fecal cortisol metabolite and IgA between rest and training
concentration increased more than twice, but if the dog lived in a house period, although there was a decrease in overall antioxidant activity
with another dog, the recovery was faster (Dreschel and Granger, 2005). (Zannoni et al., 2020). Therefore, low to moderate physical exercises can
Many studies indicate that the presence of a dog can reduce cortisol be considered as a mild stressful stimulus, but exhausting physical ac
levels in stressful situations in children and adults, including people tivity strongly affects general health and levels of the physiological
working in difficult conditions, such as doctors and military (Barker markers.
et al., 2005; Krause-Parello et al., 2019). Similarly, interaction with Overall, when using cortisol as a marker of the stress level in dogs it
humans and training sessions have been shown to reduce cortisol levels is important to consider many different factors such as individual dif
in social animals living near humans, such as dogs and wolves (Da Sil ferences in physiological responses to stress and associations with
vaVasconcellos et al., 2016). However, results from another study show behavioral traits such as fearfulness, reactivity or responsiveness to
that concentrations of beta-endorphin, oxytocin, prolactin, training (Lensen et al., 2019), age, sex, and social relationship with the
beta-phenylethylamine and dopamine increased in both dogs and owner (Schöberl et al., 2016; Svobodova et al., 2014; Wojtaś et al.,
humans after positive interspecies interaction, while cortisol concen 2020), excessive exercise (Fergestad et al., 2016), comorbidities (Cor
trations decreased only in humans (Odendaal and Meintjes, 2003). der-Ramos et al., 2019), familiarity with the clinical procedures (Sri
Perhaps the blood concentration of cortisol in dogs was increased due to thunyarat et al., 2018) and social environment (Dreschel and Granger,
overexcitation or stress from unusual experimental conditions or test 2005). The concentration of cortisol may also depend on the way the
procedures. It is believed that acute stress can be "contagious" not only animal is transported (Bergeron et al., 2002) or its reaction to a new
for people, but also for dogs. Yong and Ruffman watched the reaction of environment (Rossi et al., 2018). Cortisol levels can also have breed
dogs and humans to the babies crying. It turned out that during crying, differences (Höglund et al., 2016).
cortisol levels increased not only in people, but also in their dogs (Yong Thus, given all these factors, it can be assumed that cortisol con
and Ruffman, 2014). In two trials, the research team studied the centration is not sufficient to accurately determine the level of short-
5
term or acute stress in dogs. A combination of different stress markers increase in body weight increased the concentration of IgA (van de
and other visual parameters may give more reliable results. At the same Velde et al., 2012). These factors should also be considered when
time, cortisol levels can be used as a marker of surgical (blood, saliva) or interpreting tests results.
chronic (hair) stress. The relationship between the levels of physiological markers such as
cortisol, chromogranin A, and sIgA in puppies and the analysis of their
3.7. Prolactin behavior patterns in everyday life were analyzed in another study
(Lensen et al., 2019). IgA itself is not an objective marker of stress, but in
One of the roles of prolactin in the central nervous system was shown combination with cortisol, other biomarkers, and behavior analysis it is
to be the preservation of adult hippocampal neurogenesis during chronic possible to develop a good scheme for interpreting stress levels. More
stress exposure. Different mechanisms might account for this activity: research is needed to understand all aspects of the correlation between
prolactin might counteract the antiproliferative effects of glucocorti IgA and stress levels. Blood test for IgA is not a common service yet in
coids during the first days of stress, promote neuronal growth and dif veterinary clinics. This may probably depend on the availability of
ferentiation or support the survival of newly generated cells after enzyme immunoassay kits or the limited necessity for this parameter for
continuous stress exposure (Torner et al., 2009). diagnosing most widely spread somatic diseases. But adding secretory
Serum prolactin level has been proposed as a biomarker of both acute IgA to an expanding range of physiological biomarkers may increase our
and chronic stress in dogs (Gutiérrez et al., 2019a), but the research ability to use animal welfare research to link physiological stress and
results did not support the hypothesis. In addition to measuring cortisol affective states with immunity and general health. This will complement
and prolactin blood levels, the research team analyzed video recordings the usually measured levels of glucocorticoids and help you better un
of dogs’ behavior in the sample collection room, which helped to un derstand the health-related results of poor well-being. Also sIgA can
derstand whether the dogs were afraid of the manipulations or not. demonstrate the long-lasting action of positive experience after the
However, measuring the saliva level of prolactin using an ELISA kit stimulus on the immune system and general welfare, while the con
designed to assess the blood prolactin concentration was unreliable. The centration of glucocorticoids reflects only physiological arousal. (Staley
level of prolactin in saliva in some cases was below the detection limit, et al., 2018). The perception of negative or positive stimuli can depend
and there was also no correlation with the level of prolactin in plasma on species ecology and the animal’s experience, so it is important to
(Gutiérrez et al., 2019b). The lack of available reagent kits limits the collect data before introducing the stimulus. But perhaps stimuli
sample collection technique and the validity of results. More research perceived negatively can lead to a short-term increase in sIgA concen
and methodological development are needed to use prolactin level as a tration, while chronically stressful conditions can eventually lead to sIgA
reliable marker of dog stress as well as possible differences in females at suppression. Positive experience and motivation can also lead to an in
various stages of reproductive cycle should be taken into account crease in the concentration of sIgA, and over time, a stable concentration
(Concannon, 2011). can indicate a good well-being of the animal. (Staley et al., 2018). Such
controversy in the experimental and clinical data suggests that sIgA does
3.8. Alpha-amylase not have much perspective as a valid stress marker, but its dependence
on the psychological state and experience of the dog should be taken into
Salivary alpha-amylase (sAA) can be used to measure stress in consideration. It should also be taken into account that sIgA is not the
humans noninvasively in both routine clinical practice and in specific most popular and affordable agent for analysis, and to implement such a
studies of stress effects (Kang, 2010). In humans the potential value of test in clinical practice it is necessary to develop not only normal values
sAA measurement is discussed because it is an inexpensive and range, but also kits for analysis.
non-invasive procedure to obtain information about the activation sta
tus of the central nervous system (Warren et al., 2017). It is likely that in 3.10. Other potential biochemical markers of stress
dogs sAA activity also increases in both serum and saliva due to
disease-induced stress (Hong et al., 2019). Another study supports the Catestatin is considered to be a new biomarker of stress. The con
use of concentration of alpha-amylase as a non-invasive stress marker. It centration of catestatin in saliva increased along with the level of
has been shown that sAA level in dogs increased after sympathetic cortisol in the blood serum of dogs in the stress group, and the results
activation which typically corresponds with stress reaction (Con correlated with behavioral indicators of stress (Srithunyarat et al.,
treras-Aguilar et al., 2017). 2018). Serum levels of catestatin did not significantly differ between the
stress group (healthy dogs that were unacquainted with sampling pro
3.9. Secretory immunoglobulin A cedures) and the control group (dogs that were familiar with sampling
procedures) (Srithunyarat et al., 2018). However, another study sug
Secretory immunoglobulin A (sIgA) monitoring is proposed as gests that in dogs with broken bones changes in serum catestatin con
another physiological measure of the animals’ wellbeing besides of the centrations before and after morphine administration have some
more commonly used levels of glucocorticoids (Staley et al., 2018). potential as a clinically useful biomarker of pain stress (Srithunyarat
Combined assessment of stress by cortisol and IgA levels showed that et al., 2017).
interpretation of results is complicated by various factors. For example, In dogs with behavioral signs of separation anxiety the level of
the response to acute stress may depend on age. Puppies were observed vasopressin was higher than in the control group of dogs that were
to have higher concentrations of sIgA after stress. In adult dogs, how separated from their owners. However, concentrations of oxytocin and
ever, the level of saliva IgA decreased after stress (Svobodova et al., vasopressin in saliva did not differ between samples taken before and
2014). In order to understand how accurately the concentration of IgA after separation (Srithunyarat et al., 2018). The level of arginine vaso
correlates with the age of the dog, it is necessary to conduct more pressin in saliva significantly decreased after noise and environmental
research and create tables with age norms. Measurement of saliva sIgA stimulation in the group with a higher level of stress. The stress level was
concentration during a stress-free period showed considerable varia also analyzed using physiological parameters such as blood pressure,
tions in daily rhythm, with an increase in the morning and subsequent body temperature, heart rate, and respiratory rate (Jeong et al., 2020).
decrease (Kikkawa et al., 2003). During the stress test, the concentration Oxytocin levels increased for dogs and their owners when interacting
of sIgA significantly decreased immediately after and 30 min after noise positively with each other (Handlin et al., 2011; Miller et al., 2009; Ogi
stress, and then returned to control values 60 min after stress. It is also et al., 2020). This once again shows how important social interactions
worth noting that blood level of IgA concentration also depends on the are for the dog and how important it is to take them into account when
physiological indicators of the dog’s health, for example, a sharp planning the design of the experiment and interpreting clinical analyses.
6
At the same time, the controversy of the data still requires further 3.12. Heart rate and heart rate variability
research.
Increase of heart rate (HR) and decrease of heart rate variability
3.11. Standard biochemistry and full blood count (HRV) are basic physiological responses to stress and can also be
considered when analyzing stress and anxiety levels in dogs. These in
Blood count data such as number of neutrophils, lymphocytes, and dicators are standard and can mostly be assessed without much diffi
glucose concentration are also mentioned as markers of stress in dogs. culty, with the only condition that the animal does not have concomitant
The study of stress during land and air transportation showed that the cardiovascular problems. Transportation is also frequently considered as
average number of neutrophils was significantly higher, and the average a stressor for dogs. It was shown that the heart rate increased and HRV
number of lymphocytes was significantly lower after transportation decreased at the beginning of transportation, and these physiological
(Bergeron et al., 2002). In another study, it was shown how the con changes did not depend on the experience of the dogs (Herbel et al.,
centration of monocytes, neutrophils and lymphocytes changes when 2020). The influence of the waiting environment before appointment
dogs adapt after air transportation. It turned out that the absolute was also demonstrated. Studies in dogs show that HR accurately reflects
number of neutrophils, lymphocytes and monocytes, as well as the the effect of stressful waiting room environment in healthy dogs (Perego
percentage of neutrophils, significantly increased within 1 day after the et al., 2014). It turned out that the average, maximum, and minimum
flight (Liang et al., 2018). The well-being of dogs in the shelter was heart rate was significantly higher in the group of dogs that waited in the
assessed by the blood concentration of neutrophils, lymphocytes and clinic’s waiting room, compared to the group of dogs that waited outside
lysozyme. The concentration of lymphocytes increased, and the in the garden (Juodžentė et al., 2018). Aside from stress, factors asso
remaining indicators decreased after four weeks compared to the first ciated with the increase of HR include intense physical activity, inter
days in the shelter, which indicates an improvement in general health action with the owner and a stranger (Palestrini et al., 2005). Taken
and adaptation of dogs over time (Righi et al., 2019). These studies can together, that data makes HR an important parameter which should
not only detect specific stressful situations, but also should be consid always be considered in the context of other clinical and emotional
ered for the total blood count interpretation to differentiate somatic factors.
disorders from acute or chronic stress response. Blood tests showed that Every year there is new data on physiological markers of stress in
lipopolysaccharide (LPS)-induced downregulation of toll like receptor 4 dogs and studies of already known and popular markers, but it is still not
(TLR4) was blunted and neutrophils and monocytes major histocom possible to identify the most effective and accessible one. Markers are
patibility complex class II (MHCII) expression increased after trans often compared and studied in combinations. For example, cortisol has
portation to the veterinary clinic, the cytotoxicity function of peripheral been studied in combination with prolactin (Gutiérrez et al., 2019a),
blood mononuclear cells was also blunted during transportation and chromogranin A (Ryan et al., 2019), secretory immunoglobulin A
hospitalization. Neutrophil apoptosis was higher in stressed dogs, but (Lensen et al., 2019), saliva catestatin and vasostatin (Srithunyarat
this effect decreased significantly after the stress of hospitalization et al., 2018) and oxytocin (Rossi et al., 2018). However, it is still not
(DeClue et al., 2020). In the study of the metabolic features associated clear how to transfer these approaches into routine clinical practice. A
with fear in dogs of different breeds, it turned out that the increase in the comprehensive analysis that includes a combination of correctly
level of glutamine and gamma-glutamylglutamine (gamma-Glu Gln) in selected stress markers, together with the general and specific parame
the plasma was most noticeable (Puurunen et al., 2018). Thus, when ters of the physiological state of the animal (heart rate, HRV, etc.) and
interpreting the results of a blood test, great attention should be paid not analysis of dog behavior can give a more complete picture of the level of
only to the concomitant diseases of the patient, but also to the condition stress that the animal is experiencing. It is also important to pay atten
of the animal before and during the appointment and sample collection. tion to the reproducibility of the analysis results and observe the pa
rameters in dynamics.
Table 2
General behavioral markers of stress in dogs.
Stress and negative emotional state Low stress level, no stress
General condition Anxious/hypervigilant (C, F, G), shaking/trembling (B, C, G, F), obviously very tense (but Low stress: alert, but calm and cooperative (C, G).
can be cooperative) (C, G, H), impossible to sample (Е), impossible to touch (Е), needs to No stress: extremely friendly (G), outgoing (G), solicitous of
be lifted up or brutally forced when pulled by the leash (C, G), difficult to maneuver on attention (G), calm (C, G), relaxed (C, G), seemingly unmoved
leash and encouragement doesn’t help (C, G), looking/acting sleepy (when not tired) or (C, G).
distracted (G), refusing to eat (H).
Behavior Moving away (Е, C, G), hiding (C, D, G, F), refusing to sit/lie down (C, G), walking back
and forth (B, D), not remaining in one place (D), cowering (B), attacking (E), biting (E, F),
snapping (F), destroys/scratches/chews at surfaces (windows, doors, carpeting,
furniture) (D), circling (B), panting (B, C, F, G), yawning (B, D, F, G), eliminating (B, D, F),
spitting (E), refusing treats (G), sniffing (G), attempting to jump off the table (F).
Body and Head Low head position (F),side-turning of the head (B, E), turning the head away (E), whale
eye (F,G), ear drive (A), flattened ears (A), licking nose or lips (A, D, F, G), lifted lip (E),
tongue out (B), dropped jaw (A), swallowing a lot (D), lifting or withdrawing paws (E),
raised hair (E), salivating (G), skin and muscles visibly moving (D), tucking the tail (B, F).
Vocalization Barking/howling (B, C, D, G, F), growling (E, F), whining (B, C, D, G), whimpering (D).
(A) (Bremhorst et al., 2019).

(B) (Gutiérrez et al., 2019a).
(C) (Hernander, 2008).
(D) (Dreschel and Granger, 2005).
(E) (Srithunyarat et al., 2018).
(F) (Scalia et al., 2017).
(G) (Lloyd, 2017).
(H) (Mariti et al., 2017).
7
4. General behavioral markers of stress trainability (Harvey et al., 2019).

Invasive and non-invasive methods of taking samples can cause se
A veterinarian can use physiological markers to assess stress levels, vere stress in dogs that are not accustomed to the procedures in advance.
but this method takes time and results can be ambiguous as is shown To understand whether dogs experience stress during tests and whether
above. Analysis of the dog’s behavior and identification of behavioral this may affect further results, some researchers focus on analyzing the
signs of stress, however, can be done right during the appointment. The animal’s behavior, body position, and vocalization (Srithunyarat et al.,
body language of dogs and their facial expressions can be used to 2018).
instantly determine emotional states of different valence (Bremhorst A clinic dog stress scale, from zero to five, on entry to the clinic,
et al., 2019). Therefore, in addition to physiological criteria, scientists weighing and entering the exam room and its variations were used to
and specialists in dog behavior rely on behavior analysis. There is no determine the level of stress in dogs in the veterinary clinic in several
generally accepted scale for visualizing stress yet. After analyzing a studies (Hernander, 2008; Lloyd, 2017). Another veterinary clinic used
number of articles, it was noticed that there are terms and descriptions the VAS scale (stress behavior Visual Analog Scale) to assess the level of
of behavior that are common, while other behavioral features are stress when taking saliva and blood (Srithunyarat et al., 2018). Both
mentioned only in some studies. In some articles the behavior of dogs is scales are based on visual assessment of certain behavioral traits. The
described according to the observations of veterinarians and after stress behavior score on the scale was significantly higher in the group of
analyzing the video (Bremhorst et al., 2019; Dreschel and Granger, dogs not familiar with sampling procedures than in dogs familiar with
2005; Mariti et al., 2017). Sometimes the authors qualitatively divided blood and saliva collection procedures. It is important to note that the
the signs of stress into "Severe stress", "Moderate stress" and "Mild stress" criteria in the saliva sampling group were different from those in the
categories (Srithunyarat et al., 2017). More often, specialists take blood sampling group, since invasive methods are more stressful, and
already published scales and adjust them for their own experiment. For behavior can change. When working with dogs at the appointment, it is
the practicality of using behavior descriptions and quantifying stress, convenient to use numerical rating scales. Points make the comparison
behavior and body language are assigned points. The sum of the scores is of changes in the patient’s condition much more convenient, and it has
then compared to evaluate the improvement/deterioration of the con already been established above that stress level measurements are more
dition and the effectiveness of therapy (Hernander, 2008; Karelina et al., reliable in dynamics.
2018; Lloyd, 2017). General and individual terms were summarized in Another scientific group in addition to measuring cortisol and pro
Table 2. After analyzing and summarizing tables with signs for deter lactin levels in the blood, analyzed video recordings of behavior in the
mining stress in dogs, we identified the most common behaviors under sample collection room, which helped to understand whether the dogs
stress in various situations (Table 2) (Dreschel and Granger, 2005; were afraid of the manipulations being performed or not. In order to
Hernander, 2008; Karelina et al., 2018; Srithunyarat et al., 2018). calculate the stress score, the total number of episodes of stress-related
behaviors was measured: yawning, shaking, paw lifting, tongue out,
4.1. Analysis of the stress level by the dog’s behavior during the eliminating, growling, head turning, tail tucking, cowering, trembling,
appointment circling, pacing, hiding, panting, salivating, howling, whining, etc. The
most common signs of stress were tongue out (50%), yawning (37.5%)
Since a complete absence of stress at a veterinary clinic appointment and shaking (22.5%) (Gutiérrez et al., 2019a). These are the signs of
is virtually impossible, it is important to accurately assess its level and acute stress that are rarely noticed and associated with stress by owners.
understand how to reduce stress levels, which equally benefits patients,
their owners, staff and the clinic in general (Lloyd, 2017). The level of 4.2. Assessment of the animal’s stress level in the shelter
stress in the clinic for each dog was classified according to the analysis of
its behavior in three situations (entering the waiting room, passive The environment of the shelter can greatly affect the quality of life of
waiting in the rest area, and during weigh measurement) (Hernander, dogs, and therefore there is a need to develop effective tools for assessing
2008). their welfare. These tools should be sensitive not only to the physical
The survey found out that in the waiting room, according to the health of the animals, but also to their mental health, including the
owners, only 36.4% of the dogs looked calm, while the majority showed assessment of positive and negative emotions (Arena et al., 2019). On
signs of fear (24.4%), excitement (37.6%) and/or aggression (3.4%). the one hand, it is more convenient to conduct research in shelters,
Visiting the examination room seemed unpleasant for half of the dogs, because it is easier to recruit groups with specific features, you can
73.2% of the dogs seemed to feel discomfort on the examination table, observe animals as often as necessary, and there are many stress factors
tried to jump off the table (31.8%), shivered (16.8%), or put their tail in shelters. But, on the other hand, the living conditions and behavior
between their legs (18.0%), and tried to hold on to their owners profile of animals differ from those of domestic dogs observed in clinical
(21.0%). When approached by a veterinarian, the majority of dogs practice. It is probably better to study stress in shelters that has not yet
(63.2%) were tense but not aggressive, 11.2% were aggressive (growled led to serious clinical problems. To assess stress, behavioral scales can be
or bared teeth), and only 25.6% showed no signs of discomfort. How adapted to these conditions. For example, indicators of emotional and
ever, communication with the dog before the examination, encourage mental state of dogs were analyzed using a modified Richmond
ment and attention of the veterinarian was positively associated with the Agitation-Sedation Scale (RASS) scale (Sessler et al., 2002). The scale is
dog’s calmness in the waiting room and on the examination table (Mariti typically used for anesthesia assessment, but the parameters used in it
et al., 2017). Considering the relationship between stress levels and also characterize the level of excitation of the animal. The dogs were
biochemical and physiological parameters described above, this practice randomly assigned to the drug and placebo groups so that the average
can help to significantly improve the objectivity of diagnostics. Other initial values of emotional and mental state scores on the RASS scale did
studies have identified 10 typical behavioral signs associated with sep not differ (Karelina et al., 2018). The use of numerical scale allowed to
aration in hospitalized dogs. Destructive behavior, vocalization, inap analyze the treatment results statistically.
propriate elimination, escape attempts, pacing, trembling, depression, A fixed list of terms was also developed and tested for qualitative
and self-harm are the most typical (Flannigan and Dodman, 2001). An assessment of the behavior of dogs in the kennel (Arena et al., 2019).
analysis of the effect of the severity of itching in dogs with canine atopic Fixed definitions are especially useful because there is no clear official
dermatitis on behavior showed that the severity of itching increases the framework for defining calm, agitated, or stressful behavior. Emma K
likelihood of behavior indicating psychological stress such as mounting, Grigg and colleagues noted that the most variable behaviors of dogs in
chewing, hyperactivity, coprophagia, begging for and stealing food, the shelter were active alertness and repetitive movements such as
attention-seeking, excitability, excessive grooming, and reduced jumping and walking back and forth (Grigg et al., 2017). Although in
8
contrast to the experimental or shelter conditions, in clinical practice classes is the education of owners in order to help them to accurately
behavioral scales are difficult to be properly validated, they can be used assess behavioral signs of stress in dogs in daily life, in the waiting room
at least for the primary determination of the presence of stress in dogs. It or at a veterinarian’s appointment (Chmelíková et al., 2020; Denenberg
may be especially useful to add the most popular manifestations of stress and Landsberg, 2008; González-Martínez et al., 2019; Howell et al.,
to the routine description of the sampling procedure. 2015; Mariti et al., 2015).
The description of the behavior and condition of the animal requires Adult dogs may experience stress due to the lack of the usual level of
precise terms and the possibility of avoiding subjective assessments. attention from the owner. Reduced mental and physical activity can
When analyzing the strength of the dogs’ response to noise stimuli from result in faster aging of dogs, lower quality of life, and can reduce the
the video, only 10 of the 396 raters were able to give a reliable assess strength of the dog’s bond with the owner. It is very important to
ment of the behavior from the video, and the responses of the others maintain the quality of walks and the necessary level of physical activity
observers depended on gender, age, and attitude to the animals not only for young, but also for older dogs, in accordance with their
(Root-Gutteridge et al., 2021). Thus, when evaluating the results, the health (Wallis et al., 2017).
veterinarian can immediately pay attention to the fact that some pa Environmental enrichment is another important step towards animal
rameters could be altered not only depending on the physiological state welfare and reducing stress. It often happens that animals are bored in a
of the patient, but also on the psychological condition. In this case house that is not equipped for their life. Signs of boredom include
appropriate adjustment of tests results interpretation, differentiating increased sleepiness with bouts of anxiety, avoidance, and sensation-
symptoms, and suitable treatment prescription can be made. seeking behavior (Burn, 2017).
5. Methods of correction and prevention of stress 5.2. Pharmacological methods
5.1. Non-pharmacological methods In addition to non-pharmacological methods of behavior correction,

drugs are also used. In some situations, drugs are needed for rapid re
While acute stress at the appointment is more often noticeable and covery of the central nervous system and a calmer reaction to further
can be prevented or managed by the doctor and taken into account when correction methods. Sometimes drugs are prescribed in parallel with the
interpreting the tests results, chronic psychological stress is a health correction of behavior, for example, to adapt to new living conditions,
problem that may not be so obvious, but also requires attention and improve the taming process, as well as cognitive functions during
correction. Often an animal is brought to a veterinarian or a behavioral training (Karelina et al., 2018).
correction specialist only when the behavior deviation becomes pro In addition to strong anxiolytic and antidepressant drugs (such as
gressive (Overall, 1997). Therefore, the problem cannot be solved easily, trazodone (Gilbert-Gregory et al., 2016), dexmedetomidine (Hauser
especially if it involves aggression. Efforts to correct behavior should be et al., 2020), gabapentin, pregabalin, amantadine and amitriptyline
aimed at minimizing not only the deviations themselves, but also their (Moore, 2016)), which are well-described (Riemer et al., 2021) and are
possible causes and consequences. In clinical setting special measures prescribed by a neurologist or veterinary behaviorists in cases of severe
have been described that can help animals and their owners to reduce symptoms and are rarely used for mild to moderate stress therapy,
the level of anxiety at the appointment (Edwards et al., 2019b; Herron milder drugs based on plants, pheromones and modified antibodies are
and Shreyer, 2014; Riemer et al., 2021). For example, it is very impor also being developed.
tant to make the waiting area of the veterinary clinic safe, to introduce For example, a homeopathic drug based on senna and aloe was shown
various tactile and cognitive distractions to minimize stress during the to change the behavior of dogs, and it can be used as a possible alter
examination and treatment (Riemer et al., 2021). Сlassical music can native to treating separation anxiety (Ancken et al., 2020). Chewing
also influence behavioral and physiological parameters, such as heart tablets based on Magnolia officinalis and Phellodendron amurense reduced
rate variability, vocalization level and time spent resting (McDonald and the time of fear-related inactivity or freezing in dogs with noise phobia
Zaki, 2020). In addition to the style of music, tonality is probably also (DePorter et al., 2012). A positive experience was obtained with the use
important. It was shown that low-pitched tracks could be perceived by of Codonopsis pilosula during air transportation in beagles (Liang et al.,
dogs as more disturbing, which increased the animals alertness (Amaya 2018). Trials with a thunderstorm model of noise aversion showed that
et al., 2021). It is also important to teach owners to correctly interpret the drug based on the vine Souroubea sympetala reduced anxiety be
the dog’s signals and behavior (Kujala et al., 2017). Special programs are haviors and cortisol levels in dogs (Liu et al., 2017). However, no
being developed to teach children and their parents to understand the reduction of such behaviors as displacing activities and stereotypes was
body language of dogs. Such programs help to reduce the level of found after the use of cannabidiol (Corsetti et al., 2021).
aggression, bites and stress in the family (Meints et al., 2018), and In the study of the effect of dog-appealing pheromone (DAP) collar
reduction of stress in the family can subsequently lead to calmer on the anxiety level of dogs with noise phobia, it was found that the use
behavior in the stressful conditions of a veterinary clinic. of DAP reduced the number of fear and anxiety scores, as well as
Counter-conditioning and desensitization training and the application of increased the frequency of using shelter in response to thunder sound,
relaxation protocols are also widely used to minimize stress in the clinic possibly by countering the increased noise sensitivity (Landsberg et al.,
and for working with fears such as noise phobias and separation anxiety 2015). Dog-appealing pheromone (DAP) collars have also been shown to
(Riemer, 2020; Riemer et al., 2021; Sargisson, 2014; Stellato et al., be effective for reducing anxiety and fears in puppies during socializ
2019). ation (Denenberg and Landsberg, 2008). However, no such obvious
There are several effective ways to prevent chronic stress-related effectiveness of DAP has been shown in studying the effects of phero
problems in pets. For example, early socialization of dogs can improve mones on barking intensity or frequency, and stress-related behaviors in
their behavior in a stressful situation test in adulthood (Foyer et al., the shelter (Hermiston et al., 2018). When conducting laboratory ex
2013). A survey of 6000 owners showed that poor socialization of the periments during separation from owner, the effect of DAP on the
puppies, lack of training and attending events often led to the devel behavior, heart rate, eye or ear temperature of dogs was also not shown
opment of social phobia (Puurunen et al., 2020). Socialization can begin (Taylor et al., 2020). Another study showed that the use of DAP can
a few days after birth and should continue with age. Dogs that were reduce separation-induced anxiety, anxiety and fear in inpatient pa
socialized in time are less likely to be aggressive and fearful in adult tients and, possibly, facilitate recovery in hospitalized dogs (Kim et al.,
hood. Puppy training classes in veterinary clinics can be a good practice 2010). It is likely that additional studies on larger samples and with
for socializing and adapting a puppy to the environment and standard different experimental design and individual approach to therapy are
procedures in a veterinary clinic. The second important role of such needed to determine the effectiveness of DAP more accurately.
9
Treatments aimed at the integrative function of the brain are also Table 3
considered promising. One of such approaches is to modulate the ac Recom mendations for veterinary specialists: Factors to be considered when
tivity of endogenous regulators, such as S100 protein. Among other evaluating the level of stress?
functions, S100 proteins are involved in the pathogenesis of anxiety Behavior Behavioral history
(Ackermann et al., 2006; Bell et al., 2003; Khakimova et al., 2016). The Stress signs in the waiting room and at the appointment
effects of the novel oral drug based on technologically processed Behavior of the owner and other pets
Biomarkers Biochemical parameters (cortisol, prolactin, alpha-amylase, secretory
(Epstein, 2018) antibodies to S100 protein have been studied in a shelter
immunoglobulin A etc.)
on wild, aggressive, non-socialized dogs with various types of phobias Blood count
and fears that were exposed to stressors during their lives. The drug Physiological parameters (heart rate and heart rate variability)
caused an improvement in the emotional and mental state of dogs and is Therapy Surgery outcome
Non-pharmacological methods of correction and prevention of stress
recommended for use to relieve symptoms of stress and anxiety in dogs,
(training of owners, socialization, environmental enrichment,
their adaptation to new living conditions, improve the process of tam desensitization etc.)
ing, as well as cognitive functions during training (Karelina et al., 2018). Commonly prescribed psychoactive drugs – for therapy of severe cases
Some drugs show effectiveness in specific stressful situations. For (trazodone, dexmedetomidine, gabapentin, pregabalin, amantadine
example, a survey of dog owners found that they were more likely to and amitriptyline, etc.)
Mild anti-stress drugs – for gentle therapy or prevention (plant-,
consider diazepam effective in reducing anxiety with noise phobia than
pheromones- and modified antibodies-based drugs)
dog owners who used it during separation anxiety. However, adverse Possibility of interaction with concomitant therapy
effects included sedation, increased appetite, ataxia, agitation, increased
activity, and aggression have been mentioned (Herron et al., 2008).
Receiving dexmedetomidine during the noise of fireworks significantly problems. This will help to interpret the results more accurately.
reduced the expression of signs of fear and anxiety in dogs (Korpivaara Some cases of stress in dogs require pharmacological correction,
et al., 2017). Imepitoin has been shown to be effective for controlling however, there is no clear marker that would determine the necessity of
anxiety and fear in noise phobias (Engel et al., 2019; Perdew et al., drug treatment. Everything is very individual and depends on the level
2021). Conventional methods of reducing excitement during trans of response of the dog to stressors in the past and present. When the
portation in dogs are not always available and can have adverse con veterinarian is well versed in the degree of stress of the patient, the
sequences. Some studies suggest alternative options, for example, such choice of a drug for stress prevention and/or treatment may become
as aromatherapy in the form of a diffuse smell of lavender (Wells, 2006). more objective in terms of the dosage, regimen and side effects man
There is evidence that a combination of pharmacological and agement. For example, before prescribing drugs for noise phobia, you
non-pharmacological methods may be a most effective strategy. An can first analyze the body language of dogs from video recordings and
automated behavior shaping device has been developed to work with determine the level of stress. Also the standard behavior in noise phobias
separation anxiety in addition to pharmacological treatment (fluoxetine can be analyzed by such characteristics as a backward-directed ear po
hydrochloride). The use of the device consisting of machine sition, increased mobility, panting, vocalizations, blinking, and hiding
learning-enabled computer vision and a positive reinforcement mecha (Gähwiler et al., 2020). Further, based on the level of anxiety, you can
nism significantly reduced the signs of separation anxiety during 12 prescribe either a mild drug for the prevention of phobia, or for the
weeks of therapy and allowed the dogs to stay at home for 30 min treatment of severe anxiety. Our analysis of the available anti-stress
without signs of anxiety and stress (Mundell et al., 2020). drugs proposes that a soft correction with the mentioned plant-, pher
omones- and antibodies-based treatments can be a method of choice for
6. Conclusion the prevention and improvement of the physiological state in the early
stages or mild representations of acute and chronic stress in pets.
The sphere of behavioral medicine and the basic level of attention of The choice of methods of stress assessment depends on multiple
owners and doctors to the emotional health of pets is growing in many factors and should be made individually. Some of them can already be
countries, and the necessity to develop the methodological basis is clear. used in clinical practice, others still need more in-depth research and
It is important for a veterinarian to remember about the factors associ discussion. In clinical practice in addition to the medical background of
ated with stress not only at the stages of diagnostics, but also during the the patient the technical and logistical opportunities of the facility
further therapy (see Table 3 for a brief review). Most veterinary spe should be considered, including the availability of qualified personnel.
cialists initially base their conclusions on the behavioral signs of stress, We believe that when all the factors described in this article are taken
which are reliable. But in order to specify the diagnosis and choose the into account by veterinary specialist and the owners are cooperative and
correct treatment regimen in each individual case additional physio sufficiently informed about their role in the pets’ well-being, the accu
logical markers are necessary (both in cases of stress-induced behavioral rate diagnostics of stress-induced problems can lead to the most efficient
problems and stress as a concomitant condition of another disease). correction.
After analyzing a large amount of data on such markers, we realized that
the concept of "norm" still needs to be defined, a general range of Conflict of Interest
reference values, and a set of tests that will allow us to draw objective
conclusions about stress level are still to be determined. Importantly, The authors declared the following potential conflicts of interest with
these should be inexpensive and methodologically convenient tests that respect to the authorship, and/or publication of this article: Kartashova
include indicators that are routinely measured in animals. It should be I., Karelinа E., Ganina K., Tarasov S. are employees of OOO “NPF
also noted that dogs that are more prone to stress in everyday life often ”MATERIA MEDICA HOLDING” (full-time or part-time employment).
have higher basic levels of stress markers, which can lead to a weakening Modified antibodies to the S100 protein that are mentioned in the article
of the acute stress response due to negative physiological feedback are the active component of the commercial drug Anoten produced and
(Protopopova, 2016). marketed by OOO “NPF “MATERIA MEDICA HOLDING” and several
The interpretation of biochemical marker concentrations will differ other drugs produced and marketed by the company. The authors have
for dogs with chronic stress and for those who had an acute response to disclosed those interests fully to Apply Animal Behaviour Science.
the clinic environment and sample collection. The level of stress during
sampling and treatment can also be traced by the patient’s behavior, so
it is important to add such details of the appointment in the medical
history for all patients, not only for those with evident stress-related
10
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Applied Animal Behaviour Science 243 (2021) 105458

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Applied Animal Behaviour Science

How to evaluate and manage stress in dogs – A guide for

1. Introduction their reliability in pets both separately and in combination. In addition

(A) (Bremhorst et al., 2019).

4. General behavioral markers of stress trainability (Harvey et al., 2019).

5. Methods of correction and prevention of stress 5.2. Pharmacological methods

5.1. Non-pharmacological methods In addition to non-pharmacological methods of behavior correction,

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