ResearchAssessment of serotonin in serum, plasma, and platelets of aggressive dogs
Introduction
Canine aggression is the most common reason for the referral of dogs to animal behaviorists (Bamberger and Houpt, 2006, Fatjó et al., 2007). Dog bites represent an important problem for public health (Overall and Love, 2001, Palacio et al., 2005). They also pose a problem in the field of animal welfare, as a significant proportion of aggressive dogs is euthanized or abandoned (Hunthausen, 1997, Mikkelsen and Lund, 2000). If these problems are to be prevented and effectively managed, it is necessary to deepen the understanding of the biological basis of canine aggression.
Serotonergic neurotransmission is believed to play a critical role in the control of aggression in several species (Ferrari et al., 2005). Low concentrations of the main serotonin (5-HT) metabolite 5-hydroxyindoleacetic acid in cerebrospinal fluid (CSF) have been associated with low thresholds for aggression or impulsivity in human and nonhuman primates (Mehlman et al., 1994, Stanley et al., 2000, Soderstrom et al., 2001, Howell et al., 2007) as well as in dogs (Reisner et al., 1996).
Technical and ethical restrictions linked to the study of the serotonergic system in psychiatric disorders through CSF and neurohistochemical studies have led scientists to search for more easily accessible biological samples. The platelet where blood 5-HT is mainly stored (Kema et al., 2000) has been proposed as a peripheral marker of the serotonergic neuron (Plein and Berk, 2001). Although blood 5-HT does not cross the hematoencephalic barrier, a correlation between blood and CSF serotonergic parameters has been found in humans (Sarrias et al., 1990). In the realm of human aggression, the measurement of blood 5-HT has offered inconclusive results, as both low (Goveas et al., 2004) and high (Golubchik et al., 2009) concentrations have been found to be linked to aggressive behavior in different populations. In canine species, 2 recent studies have reported low serum serotonin concentrations in aggressive individuals (Çakiroglu et al., 2007, Rosado et al., 2010a).
The aim of the present study was 2-fold. First, to assess the suitability of different types of blood samples for measuring circulating 5-HT in clinical studies in canine species. Second, to further investigate the relationship between the serotonergic system and canine aggression. To this end, the assessment of 5-HT was simultaneously carried out in serum, plasma, and platelets of aggressive and nonaggressive dogs.
Section snippets
Aggressive animals
Two Spanish veterinary teaching hospitals (Universidad de Zaragoza and Cardenal Herrera-CEU, Valencia) contributed to the collection of cases. Dogs included in the present study were referred to the Companion Animal Behavior Services within the respective hospitals owing to problems of aggression toward people and/or other dogs. Displaying any other type of behavioral problem did not constitute an exclusion criterion. Animals showing an underlying causative medical condition to the problem of
Results
The unifactorial multivariate analysis of variance showed a significant effect of the factor “aggression” on 5-HT concentrations (P < 0.01). Aggressive animals showed lower 5-HT concentrations in serum, plasma, and platelets than nonaggressive animals. The higher mean 5-HT concentration was detected in serum samples. Serotonin results according to the type of sample are summarized in Table.
Serotonin concentration in platelets was positively correlated with that in serum (r = 0.465; P < 0.01)
Discussion
In the present study, the assessment of 5-HT in serum, plasma, and platelets was carried out both in aggressive and nonaggressive dogs. Regardless of the type of sample, aggressive dogs showed significantly lower concentrations of circulating 5-HT than nonaggressive dogs. This finding agrees with previous studies that found an association between high aggression or impulsivity and low concentrations of CSF 5-hydroxyindoleacetic acid and circulating 5-HT in primates (CSF: Mehlman et al., 1994,
Acknowledgment
The authors are grateful to María Yetano for language support.
References (39)
- et al.
Determination of serotonin in whole blood, platelet-rich plasma, platelet-poor plasma and plasma ultrafiltrate
Life Sci.
(1987) - et al.
Analysis of 1040 cases of canine aggression in a referral practice in Spain
J. Vet. Behav.: Clin. Appl. Res.
(2007) - et al.
Platelet poor plasma serotonin level in delinquent adolescents diagnosed with conduct disorder
Prog. Neuropsychopharmacol. Biol. Psychiatry
(2009) - et al.
Platelet serotonin content correlates inversely with life history of aggression in personality-disordered subjects
Psychiatry Res.
(2004) - et al.
Clinical chemistry of serotonin and metabolites
J. Chromatogr. B. Biomed. Sci. Appl.
(2000) - et al.
The effects of paroxetine and tianeptine on peripheral biochemical markers in major depression. Prog
Neuropsychopharmacol. Biol. Psychiatry
(2002) - et al.
Serotonergic status in human blood
Life Sci.
(1988) - et al.
Aspectos epidemiológicos de las mordeduras caninas
Gac. Sanit.
(2005) - et al.
Comparison of cerebrospinal fluid monoamine metabolite levels in dominant-aggressive and non-aggressive dogs
Brain Res.
(1996) - et al.
Blood concentrations of serotonin, cortisol and dehydroepiandrosterone in aggressive dogs
Appl. Anim. Behav. Sci.
(2010)
Serotonin transporter activity in platelets and canine aggression
Vet. J.
Novel mechanisms for neuroendocrine regulation of aggression
Front. Neuroendocrinol
Accumulation of 5-hydroxytryptamine by aging platelets: studies in a model of suppressed thrombopoiesis in dogs
Thromb. Haemost.
Signalment factors, comorbidity, and trends in behavior diagnoses in dogs: 1,644 cases (1991-2001)
J. Am. Vet. Med. Assoc.
Relationship between the serum concentrations of serotonin and lipids and aggression in dogs
Vet. Rec.
Free and conjugated catecholamines and serotonin in canine thoracic duct lymph: effects of feeding
Am. J. Physiol.
Effect of dietary protein content and tryptophan supplementation on dominance aggression, territorial aggression, and hyperactivity in dogs
J. Am. Vet. Med. Assoc.
Council Directive of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes
Official Journal of the European Communities Serie
Intraluminal release of serotonin, substance P, and gastrin in the canine small intestines
Dig. Dis. Sci.
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