Behavioural changes secondary to organic diseases are relatively common and justify a careful clinical examination during a consultation for behavioural problems (Fig. 1).
In the light of the model proposed by P. Pageat, the diagnosis of a behavioural disorder is a differential diagnosis, not a “hold all” diagnosis when an organic disease cannot be identified. An organic disease should be particularly suspected when:
- a behavioural disorder appears abruptly or evolves rapidly without apparent cause;
- there is rapid exploitation of the aggressive behaviours;
- phobias appear unexpectedly, with no traumatic cause, in an adult dog;
- there is worsening of already present phobias characterized by symptoms that suddenly become “very productive”;
- the animal’s symptoms do not fit into a well-defined clinical picture or there is inconsistency in the origin of the behavioural disorder.
The veterinarian should suspect the presence of an organic disease, whose symptoms mimic a behavioural disorder, when: (i) it is not possible to make a nosographic diagnosis (name the disease), but only a functional one (the presence of a pathological state such as phobia, anxiety, depression, dysthymia and so on); (ii) the symptoms shown by the animal appear to be “inconsistent” with the normal behavioural pattern of the species under examination; and (iii) the symptoms appear “unexpectedly”, with no history of prior behavioural disorders.
HYPOTHYROIDISM
In clinical practice, aggressive behaviour in the dog represents a non-pathognomonic sign of a thyroid disorder. Indeed, this sign seems to be quite frequent. The prevalence of hypothyroidism in the canine population is not known, but it is estimated that it can reach 40% in some breeds (W. J. Dodds). Hypothyroidism in the dog is usually a primary disorder of the gland, due to a lymphocytic thyroiditis (probably immune-mediated), or to idiopathic follicular atrophy and less frequently to a neoplasm (adenoma). Rarely the hypothyroidism may be secondary to a pituitary gland disorder, the most frequent cause of this being development of a neoplasm. There are anecdotal reports of pituitary malformations and various causes of congenital hypothyroidism (M. Bernardini). In humans, hypothyroidism leads to a reduction in cognitive capacity, lack of concentration, changes in short-term memory, as well as visual and auditory hallucinations. Fear, anxiety and aggressive behaviours have been described in patients with hypothyroidism. For this reason, the condition is often confused with disorders related to attention deficits/hyperactivity, psychosis and schizophrenia.
Hypothyroidism in the dog is accompanied by changes in mood or depression caused by diminished noradrenergic activity. The thyroid hormones (T4) not only modulate the activity of noradrenaline and serotonin but also the sensitivity of beta–adrenergic receptors. The turnover of serotonin in the central nervous system is increased while the concentration of this neurotransmitter in the cortex and the density of the 5-HT2A receptors are decreased (W. J. Dodds). Alterations of these processes can cause signs of phobia or depression characterized by profound emotional and cognitive changes. In general, behavioural signs are more evident when an animal is psychologically or physically stressed. Since endogenous glucocorticoids inhibit the production and release of thyroid hormones (and their conversion into active forms) it is not surprising that stress can induce a true state of hypothyroidism, initially manifested by behavioural signs, in dogs with optimal or borderline thyroid function (W. J. Dodds).
Numerous patients with hypothyroidism are not obese or apathetic, but show considerable emotional instability, a lack of reactions or unexpected reactions (altered vigilance), changes in primary behaviours (for example, sleep) and cognitive alterations. Hyperthyroidism is often associated with excitability and hyperaesthesia while the onset of sudden phobias (particularly of noises and storms) is not uncommon in hypothyroidism; these phobias are often among the manifestations of aggressive behaviour (fear-elicited aggression), which is usually directed against the animal’s owner or other dogs.
HYPERADRENOCORTICISM
In clinical practice, aggressive behaviour in the dog represents a non-pathognomonic sign of an increased concentration of cortisol in the blood. Hyperadrenocorticism occurs above all in elderly dogs. The breeds most susceptible to this condition are the German Shepherd, Dachshund, Poodle and numerous Terriers (M. Bernardini). This disorder is related to an excessive amount of cortisol, which is the consequence of adrenal or pituitary gland disease. Iatrogenic hyperadrenocorticism can occur following prolonged treatment with corticosteroids. The relationships between changes in the secretion of the various adrenal gland hormones during emotional responses have been studied for a long time. From among these hormones, cortisol is the one whose interactions with emotional stress are best known.
In the case of stress, the release of adrenocorticotropic hormone (ACTH) increases, which, in its turn, causes a higher concentration of circulating cortisol. This is considered an adaptive response because it enables the animal to respond to internal and external stresses. Cortisol modulates the activity of metabotropic receptors in the limbic system and, for this reasons, endocrine disorders of the adrenal glands are frequently accompanied by changes in behaviour, emotions and mood. In Cushing’s syndrome the behavioural signs often precede the classical clinical signs: the behavioural picture includes apathy, indifference, moaning, excessive attachment and aggressive behaviour that cannot be explained by the entourage. Increased appetite is a sign that may be ignored by the owner. Indeed, while owners associate a decrease in appetite with illness, a good appetite is usually taken as evidence that a dog is in good health. Dogs affected by hyperadrenocorticism can steal food from the table and break open rubbish bags. They beg continuously and may show hierarchy aggression to defend food from their owners or other dogs. Chronically raised levels of circulating cortisol together with the loss of adaptability of secretion of the hormone cause changes in mood and severe cognitive modifications that lead, in the elderly dog, to the clinical picture of involutional depression.
SEX HORMONES
In clinical practice, aggressive behaviour in the dog represents a non-pathognomonic sign of physiological/modified secretion of sex hormones (oestradiol, testosterone, progesterone). Receptors for sex steroids (cytoplasmic for progesterone, nuclear for oestradiol and testosterone) are present in different parts of the brain. Their distribution seems to be homogeneous in higher mammals (limbic system, amygdala, hippocampus, cerebral and cerebellar cortex, corpus callosum, thalamus, reticular formation). Progestin receptors are predominantly present in the hypothalamus-pituitary axis and in the vomiting centre. The receptors for oestradiol and testosterone are distributed in numerous areas, although their concentrations are highest in the hypothalamus-pituitary axis.
Many studies have shown that the sex hormones influence the sensitivity of dopaminergic receptors and suggest that there is antagonism between the groups of hormones as far as regards behavioural effects, emotional reactions and mood. Oestradiol and testosterone increase voluntary motor activity (because they increase dopaminergic transmission) while progesterone seems to have the opposite effect. According to P. Pageat, the sex steroids modify reactive states and contribute to the onset of some behavioural responses. Physiological changes in the secretion of the sex hormones can underlie the development of a dysthymic state in females, particularly at the time of oestrus, and of irritation-elicited aggression or maternal aggression in the presence of puppies or pseudocyesis. Clinically important changes in the function of sex glands cause dysthymic or depressive type alterations of mood. A relationship between sex hormones and some behaviours has been repeatedly demonstrated, particularly for aggressiveness. Male dogs (independently of whether they are sexually intact or castrated) more often show behavioural problems, in particular aggressiveness. Numerous authors (Borchelt, Fajò and Manteca, Guy et al., O’Farrell, Overall, Sparagetti and Verga, Takeuchi et al., Wells and Hepper, etc.) have shown that:
- Male dogs (independently of whether they are sexually intact or castrated) more often show behavioural problems, in particular aggressiveness;
- Sterilised females are more aggressive than sexually intact ones (they more often show fear-elicited aggression) particularly if the operation was performed specifically to reduce this undesired behaviour;
- Sexually intact males are more aggressive than neutered ones or females.
It is thought that only some types of aggressive behaviour can be controlled by castration. Hopkins et al. reported that, for dogs, only aggression between males was reduced notably (in 60% of cases) by this type of operation. Their study found some effect only on fear- and territorial-elicited aggression and aggression between males: social or dominance (hierarchy) aggressiveness towards the owner was not particularly influenced by castration. In a retrospective study, urinary marking, sexual mounting and fighting among males were reduced in only 50 to 60% of adult male dogs, while roaming was decreased in up to 90% (N. H. Dodman). The effects of this treatment are not always immediate: in some cases several weeks are needed in order to observe them. The therapeutic results achieved with castration have been challenged by other authors.
Salmeri et al. evaluated the effects of gonadectomy in immature dogs who did not have signs of behavioural disorders: they were found to be more active and excitable than their sexually intact peers. Neilson et al. investigated the effects of castration on animals that had been aggressive towards family members, showing that only one third of the animals improved after this operation, a much lower percentage than that reported in other studies on castration. In some subjects the physiological increase in oestrogens causes an increase in aggression between bitches. Ovariectomy is indicated to eliminate aggressive behaviours related to oestrus and pseudocyesis, but is absolutely contraindicated when dominance (hierarchy) aggressiveness is present. In such cases sterilisation can cause subsequent worsening (O’Farrell). One study that compared the behaviour of 150 bitches before and 6 months after sterilisation showed a significant increase in dominance (hierarchy) aggressiveness towards human members of the family. This effect was, however, most marked in animals under 1 year old which had already shown aggressive tendencies of this type: in 50% of these subjects the aggressive behaviour increased, while in the other 50% it decreased. In comparison, in the control group of sexually intact females, 14% showed an increase in aggressive tendencies and 86% a decrease (N. H. Dodman).
It is worth noting that surgical castration and ovariectomy are ineffective if not accompanied by appropriate behavioural therapy. In fact, once a behaviour has developed, it changes the emotions, motivations and arousal of the individual permanently. The learning-related cognitive component remains even after surgical removal of the gonads. Although Neilson et al. demonstrated that there is no correlation between the age of the dog, the duration of the problem prior to the operation and the efficacy of the operation, surgery should be performed as early as possible in order that cognitive processing of the behaviour is prevented.
Suggested readings
- BERNARDINI M, Neurologia del cane e del gatto, Poletto editore, 2002, Gaggiano (Mi);
- COLANGELI R, GIUSSANI S, Medicina comportamentale del cane e del gatto, Poletto editore, 2005 Gaggiano (Mi);
- DAMINT S, BEATA C, (2005) Endocrinology and behaviour, About Hierarchy, Behaviour and Internal Medicine ESVCE, Marseille 8 – 9 october;
- DODDS WJ, (2004) Behavioral issues and thyroiditis: theory and case review. Proceedings American Holistic Veterinary Medical Association;
- DODMAN NH, SHUSTER L, Farmacologia comportamentale veterinaria, Masson s. p. a., 2000, Milano;
- FATJO’ J., MANTECA X. (1999) “Problemas de comportamiento en perros y gatos”. Dal: Seminario Iberoamericano de Comportamiento en Perros y Gattos, Univ. de Ciencias Aplicadas y Ambientales (U.D.C.A), Facultad de Ciencias Agropecuarias, Carrera de Medicina Veterinaria - Universtad Autónoma de Barcelona (U.A.B.). 4 e 5 Novembre 1999, Santa Fe de Bogotà, D.C;
- FERRIERE C, Eduquer un chien sourd, La communication, collection Zoopsychiatrie, 2005, Solal Editeur;
- GIUSSANI S, Perte de la vision et modifications comportementales chez les carnivores domestiques, Mémoire pour l’obtention du diplome de Vétérinaire Comportementaliste del Ecoles Nationales Vétérinaires, 2002 Nantes;
- HOPKINS S.G., Schulbert T.A., Hart B.L. (1976) Castration of adult male dogs: effects on roaming, aggression, urine making and mounting;
- MEGE C, BEAUMONT – GRAFF E, BEATA C, DIAZ T, HABRAN T, MARLOIS N, MULLER G, Patologia comportamentale del cane, Masson s. p. a ed EV s. r. l., Milano/ Cremona, 2006 prima edizione;
- Neilson J.C., Eckstein, R.A., Hart B.L. (1997) Effects of castration on problem behaviors in male dogs with reference to age and duration of behavior. J Am Vet Med Assoc 1997 Jul 15;211(2);
- O'Farrell V, Peachey E.. Behavioural effects of ovariohysterectomy on bitches. J Small Anim Pract. 1990;.
- OVERALL KL, La clinica comportamentale del cane e del gatto, C. G. Edizioni Medico Scientifiche s. r. l., Torino, prima edizione italiana;
- PAGEAT P, “La patologia comportamentale del cane” – Edizione Le Point Veterinaire Italie Milano 2000;
- SALMERI, K.R., BLOOMBERG, M.S., SCRUGGS,S.L., SCHILLE, V. (1991) Gonadectomy in immature dogs: effects on skeletal, physical, and behavioural development. J. Am. Vet. Med. Assoc.