Baseline and postprandial concentrations of cortisol and ghrelin in companion dogs with chronic stress-related behavioural problems: A preliminary study
Introduction
Numerous behavioural problems in dogs involve stress and anxiety. In fact, some forms of aggression, separation stress disorders and noise phobias are classified as anxiety-related problems by several authors (Overall, 2013; Ogata, 2016; Wormald et al., 2017). Usually, suffering from these problems occurs for long periods of time, even the whole life of the animal, which entails the dogs living under a permanent condition of chronic stress. Habitual exposure to anxiety-inducing stimuli for a certain period of time can negatively affect the physical, mental or social health of dogs (Dreschel, 2010; Mills et al., 2014) and thus reduce their quality of life. Daily stress, fears and anxieties have been clearly shown to be related to health problems (mainly skin diseases) and shortage of lifespan in dogs (Dreschel, 2010; Shihab et al., 2011; Snitcofsky and Mentzel, 2015). In addition, comorbidity of different anxiety-related problems is frequently observed in the same animal (Bamberger and Houpt, 2006; Fatjó et al., 2007; Yalcin and Batmaz, 2007; Tiira et al., 2016). Finally, the fact of having a dog with these problems may prompt owners to use aversive training methods or inappropriate behavioural modification techniques that can compromise welfare (Blackwell et al., 2008; Herron et al., 2009; Yeates, 2012).
Besides the just cited direct effects on the animal, it is important to mention that behavioural problems are one of the main causes for dog relinquishment as well as for returning to shelter after being adopted (Salman et al., 2000; Shore, 2005; Diesel et al., 2008, 2010; Coe et al., 2014; Hill and Murphy, 2016), and also for euthanasia (RSPCA, 2007). Considering all of this, behavioural problems have been pointed out as an important canine welfare concern (Fatjó et al., 2007; Sonntag and Overall, 2014; Col et al., 2016; Luño et al., 2017).
Blood or salivary cortisol levels have been traditionally used to measure stress either acute or chronic in dogs (Beerda et al., 1996; Kobelt et al., 2003; Hellhammer et al., 2009; Hennessy, 2013). Regarding behavioural problems, a previous study showed concentrations of plasma cortisol in aggressive dogs, especially those showing aggression towards the family members, significantly higher than those found in a control group (Rosado et al., 2010, 2011). In fact, dogs displaying owner-directed aggression frequently display ambivalent signals during conflict situations, which are believed to be indicative of high arousal and suggest the presence of fear or stress (Bamberger and Houpt, 2006; Reisner et al., 2007). In the case of dogs showing separation anxiety, to the authors' knowledge, basal cortisol has not been analyzed in comparison with a control population, but salivary cortisol has been used to measure stress during different test conditions related to separation from the owner (see Mongillo et al., 2013; Shin and Shin, 2016).
More recently, ghrelin has been suggested as an essential element regulating the hypothalamic pituitary adrenal (HPA) axis when the individual is exposed to both acute and chronic stress. Ghrelin is a hormone (28aa peptide) mainly synthesized in the stomach that acts as a hunger signal for stimulating food intake (Yokoyama et al., 2005). The ghrelin receptor (GHSR) is expressed throughout the brain, including in feeding and metabolism-associated areas, in the pituitary gland and in stress response-associated brain regions such as the amygdala. Ghrelin is increased in both acute and chronic stress situations (Perelló and Zigman, 2012) and this increase takes place together with a stress-induced rise in glucocorticoids (Spencer et al., 2015). Previous studies in humans and rodents have shown that abnormalities in the ghrelin system contribute to the development of stress response-related mood disorders (Perelló and Zigman, 2012).
Both cortisol and ghrelin are purported to be related to so called “emotional or stress-related eating”, that is, the change in the eating behaviour in response to (negative) emotional states or stress as a way of coping with that situation (McMillan, 2013). Emotional eating especially involves the intake of food with specific characteristics, the so called “comfort foods”, which are rich in energy, fat or sugar, and are consumed to obtain psychological comfort and emotional wellness (Dubé et al., 2005; la Fleur et al., 2005; Zellner et al., 2006). In rats, the intake of these foods has been demonstrated to stimulate the hypothalamic release of endogenous opioids (Dum et al., 1983; Mercer and Holder, 1997) and to decrease cortisol levels, so the intake of these comfort foods has been considered as a coping strategy for stressed individuals (Wiener et al., 1983; Foster et al., 2009; Ulrich-Lai et al., 2010). On the other hand, ghrelin has been suggested to increase the rewarding properties of certain foods by acting on the mesolimbic dopamine reward system in mice (Chuang and Zigman, 2010). Thus, intact ghrelin signaling would be required for normal eating behaviour and body weight responses, especially to hedonically rewarding high-fat diets (Perelló and Zigman, 2012).
It has been observed that the meal-induced fall in plasma cortisol occurs together with a fall in plasma ghrelin, which is consistent with reports showing that ghrelin promotes glucocorticoid secretion by stimulating ACTH release from the anterior pituitary (revised by Spencer et al., 2015). Raspopow et al. (2010) observed that stress-induced elevations in plasma ghrelin found in high “emotional eaters” (so-called due to their experienced food cravings and increased consumption of comfort foods in response to negative emotions and stress), fail to decline acutely following food consumption.
In canine species, ghrelin levels have been studied in relation to the metabolism of growth hormone (Yokoyama et al., 2005; Bhatti et al., 2006) and obesity (Jeusette et al., 2005a, b) as well as in relation to the effect of diet and ovariectomy (Jeusette et al., 2006; Lubbs et al., 2010; Schauf et al., 2016, 2018). Only one study has analyzed differences in baseline ghrelin and cortisol in dogs with and without compulsive tail chasing (Yalcin et al., 2017). However, no studies exist that focus on the relation of this hormone with stress, either acute or chronic, or emotional eating in dogs. According to a previous survey, a great proportion of owners (82.7%) noticed that their dog showed emotional eating at some level of intensity, and a high perception of emotional eating was related to some behavioural problems (Luño et al., 2018).
The aim of the present work was to analyze baseline and post-prandial cortisol and ghrelin levels in dogs showing chronic stress-related behavioural problems and a control group. We hypothesized that stressed dogs would show higher baseline cortisol and ghrelin levels than control dogs and that both hormones would decrease after eating a portion of high energy palatable food.
Section snippets
Materials and methods
The study was approved by the Ethic Advisory Committee for the Animal Experimentation of the University of Zaragoza with the authorisation reference number PI15/17, and an informed consent was obtained before enrolling any dog in the study.
Results
Demographic information of the group of dogs diagnosed with SCA and SA are described in Table 1. Thus, SCA was diagnosed as the main diagnostic category in the 62.5% (n = 10) of the cases, and 31.3% (n = 5) of the dogs suffered from SCA and SA at the same time. In addition to these main diagnoses, comorbidity with other behavioural problems was observed in the totally of recruited cases, following this order: aggression towards dogs (75.0%), noise phobia (43.8%), inappropriate elimination
Discussion
In the present study, baseline and post-prandial serum levels of cortisol and ghrelin were measured in a group of dogs showing behavioural problems believed to be associated with chronic stress, in particular social conflict-related aggression (SCA) and separation anxiety (SA), in comparison with a group of normally behaved control dogs. Both entire and neutered dogs were included in the study, and there were not statistical differences in either ghrelin or cortisol levels according to sex or
Conclusions
The present study shows that SCA dogs but not SA were more stressed than a group of control dogs in basal conditions and that their cortisol and ghrelin levels did not decrease after eating, suggesting the possibility of a failure to suppress ghrelin after meals in these dogs and, consequently, to decrease cortisol. On the contrary, both cortisol and ghrelin decreased in the SA dogs after the intake of food, suggesting a positive effect of eating in decreasing stress. Thus, the results suggest
Conflict of interest statement
The authors declare that no conflicts of interest exist in any financial, personal or other relationships with other people or organizations within the years of beginning the submitted work that could inappropriately influence, or be perceived to influence, the work.
Declaration of interests
None.
Authorship
The idea for the paper was conceived by Belén Rosado. The experiments were designed by Sylvia García-Belenguer, Jorge Palacio, Belén Rosado and Isabel Luño. The experiments were performed by Belén Rosado and Isabel Luño. The data were analyzed by Sylvia García-Belenguer, Jorge Palacio, Belén Rosado and Isabel Luño. The paper was written by Belén Rosado and Isabel Luño. The paper was revised by Sylvia García-Belenguer, Jorge Palacio, Belén Rosado and Isabel Luño.
Acknowledgements
The authors wish to thank Professor Mercedes Jaime Sisó, María Yetano and Bradley Earl for language support, and Ana Muniesa for her inestimable help during statistical analysis.
References (73)
- et al.
Stress, eating and the reward system
Physiol. Behav.
(2007) - et al.
The use of saliva cortisol, urinary cortisol, and catecholamine measurements for a noninvasive assessment of stress responses in dogs
Horm. Behav.
(1996) - et al.
The relationship between training methods and the occurrence of behavior problems, as reported by owners, in a population of domestic dogs
J. Vet. Behav. Clin. Appl. Res.
(2008) - et al.
An epidemiological analysis of dog behavior problems presented to an Australian behavior clinic, with associated risk factors
J. Vet. Behav. Clin. Appl. Res.
(2016) - et al.
Factors affecting the success of rehoming dogs in the UK during 2005
Prev. Vet. Med.
(2008) The effects of fear and anxiety on health and lifespan in pet dogs
Appl. Anim. Behav. Sci.
(2010)- et al.
Affect asymmetry and comfort food consumption
Physiol. Behav.
(2005) - et al.
Activation of hypothalamic β-endorphin pools by reward induced by highly palatable food
Pharmacol. Biochem. Behav.
(1983) - et al.
Ghrelin and leptin levels in patients with obsessive–compulsive disorder
Prog. Neuro-Psychopharmacol.
(2007) - et al.
Analysis of 1040 cases of canine aggression in a referral practice in Spain
J. Vet. Behav. Clin. Appl. Res.
(2007)
Salivary cortisol as a biomarker in stress research
Psychoneuroendocrinology
Using hypothalamic–pituitary–adrenal measures for assessing and reducing the stress of dogs in shelters: a review
Appl. Anim. Behav. Sci.
Survey of the use and outcome of confrontational and non-confrontational training methods in client-owned dogs showing undesired behaviors
Appl. Anim. Behav. Sci.
Stress, cortisol, and obesity: a role for cortisol responsiveness in identifying individuals prone to obesity
Domest. Anim. Endocrinol.
Factors associated with canine resource guarding behaviour in the presence of people: a cross-sectional survey of dog owners
Prev. Vet. Med.
Effects of chronic obesity and weight loss on plasma ghrelin and leptin concentrations in dogs
Res. Vet. Sci.
Sources of sampling variation in saliva cortisol in dogs
Res. Vet. Sci.
Emotional eating in companion dogs: owners’ perception and relation with feeding habits, eating behavior and emotional state
J. Vet. Behav. Clin. Appl. Res.
Stress-induced and emotional eating in animals: a review of the experimental evidence and implications for companion animal obesity
J. Vet. Behav. Clin. Appl. Res.
Food cravings, endogenous opioid peptides, and food intake: a review
Appetite
Stress—its effects on health and behavior: a guide for practitioners
Vet. Clin. North Am. Small Anim. Pract.
Does the attachment system towards owners change in aged dogs?
Physiol. Behav.
Separation anxiety in dogs: What progress has been made in our understanding of the most common behavioral problems in dogs?
J. Vet. Behav. Clin. Appl. Res.
The role of ghrelin in reward-based eating
Biol. Psychiatry
Psychosocial stressor effects on cortisol and ghrelin in emotional and non-emotional eaters: influence of anger and shame
Horm. Behav.
Blood concentrations of serotonin, cortisol and dehydroepiandrosterone in aggressive dogs
Appl. Anim. Behav. Sci.
Direction of post-prandial ghrelin response associated with cortisol response, perceived stress and anxiety, and self-reported coping and hunger in obese women
Behav. Brain. Res.
Behavioral changes in dogs associated with the development of idiopathic epilepsy
Epilepsy Behav.
Evaluation of effects of olfactory and auditory stimulation on separation anxiety by salivary cortisol measurement in dogs
J. Vet. Sci.
Ghrelin’s role in the hypothalamic-pituitary-adrenal axis stress response: implications for mood disorders
Biol. Psychiatry
Prevalence, comorbidity, and behavioral variation in canine anxiety
J. Vet. Behav. Clin. Appl. Res.
Comfort food is comforting to those most stressed: evidence of the chronic stress response network in high stress women
Psychoneuroendocrinology
Relationship between stress, eating behaviour, and obesity
Nutrition
Influence of perinatal malnutrition on adult physiological and behavioral reactivity in rats
Physiol. Behav.
Reduced heart rate variability in pet dogs affected by anxiety-related behavior problems
Physiol. Behav.
Maximising canine welfare in veterinary practice and research: a review
Vet. J.
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