Veterinary Quarterly

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Assessing the pathological extent of aggressive

behaviour in dogs. A review of the literature

C. Jacobs , T. De Keuster & P. Simoens

To cite this article: C. Jacobs , T. De Keuster & P. Simoens (2003) Assessing the pathological
extent of aggressive behaviour in dogs. A review of the literature, Veterinary Quarterly, 25:2, 53-60,
DOI: 10.1080/01652176.2003.9695145

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 53
1

Veterinary Quarterly 2003; 25(2): 53-60

Assessing the pathological extent of aggressive behaviour in dogs

A review of the literature

C. Jacobs", T. De Keuster2 and P. Simoensl

1Department of Morphology, Faculty of Veterinary Medicine, Ghent University, Belgium

20ostveldkouter 222, 9920 Lovendegem, Belgium
3Corresponding author:
Department of Morphology, Faculty of Veterinary Medicine,
Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
E-mail: Christel.Jacobs@UGent.be

TABLE OF CONTENTS

Summary and keywords 54

Introduction 54

Aggression as a part of normal canine behaviour 54

Aggression promoting factors 54

Genetic predisposition 55
Environment 55
(Patho)physiology 55
Disease processes 55

Classification of aggressive behaviour 55

Descriptive classification 56
Functional classification 0

57
Other classification methods 57

Discussion 58

Conclusion 59

References 60
 54

Assesessing the pathological extent of aggressive behaviour in dogs

A review of the literature

C. Jacobs, T. De Keuster and P. Simoens

SUMMARY
In this review the variety of parameters used for evaluating the pathological extent of aggressive
behaviour is summarised and the practical usefulness of each parameter is discussed. The selected
parameters are: the objective analytic description of the aggressive behaviour, the function of the
aggression, the presence of the three phases of a normal aggression sequence, the number of bites per
attack, the duration of the attack and the frequency of the aggressive behaviour. Other criteria such
as the appropriateness of the aggression in relation to the context, the predictability of the aggression
and the severity of the caused injury are biased because of the variation caused by numerous external
factors. The relevance of the most suitable parameters will be assessed in a further study in which the
distribution of aggression modulating neurotransmitter receptors will be determined.
Keywords: Aggression; Aggressive behaviour; Behavioural diseases; Bites; Dog behaviour; Dog diseases;
Dogs; Review.

Introduction repertory of ritualised behaviour. In this context

Canine aggression is the cause of many veterinary
consultations and is of current interest because of
the danger it involves for society. Askew (4)
mentions that aggression towards humans forms
54% of the behaviour problems in dogs while
aggression towards other dogs represents 15% of
all the cases. These facts have lead to an increa-
sing interest in the etiology of aggresion.
For scientific research in this context, it is
important to have the disposal of a reference group
of dogs with low aggressiveness and a test group
of dogs with pathological aggression. A fixed
protocol with unequivocal criteria is required for
the selection of dogs in order to obtain two
homogeneous groups and reproducible test results.
A variety of parameters has been used in canine
behavioural studies to classify aggressive
behaviour but these parameters are seldom linked
to an evaluation of the pathological extent of this
behaviour. Therefore a practical, but still strictly
objective classification standard is required.
In this review the concept of canine aggression
will be approached from different angles, and the
importance and practical use of each point of view
will be discussed.
Aggression as a part of normal canine
behaviour
Dogs are social animals with an extensive
canine aggression is often considered to be a
normal behavioural expression (5,20,26). The
major criterion by which the normality of an
aggressive incident is evaluated, is the
appropriateness of the aggression to a certain
situation (22).
An important note is the fact that dogs tempt to
create a dominance hierachy in which it is
determined which animal is allowed access to a
critical resource such as food, water, shelter and
to a mate without having to fight (11,12,33). Dogs
allow people to enter the hierarchy but maintain
their repertory of behavioural patterns for the
communication with this other species. A wrong
interpretation of interspecific behavioural signs
may lead to misunderstandings and cause aggressi-
ve conflicts (26).
Although aggression is a part of the normal
behavioural pattern of dogs, Netto and Planta (20)
claim that the aggressiveness of some dogs is too
high to be acceptable for the near environment and
for society. Such dogs can be distinguished by
assessing the aggression score by means of
aggression tests. Aggression tests are based on the
ease by which aggressive behaviour can be elicited
in an extensive range of situations and contexts
(20).
Aggression promoting factors
Behaviour is influenced by a variety of factors
 55
such as genetic predisposition, environment
including experience and learning processes,
(patho)physiology and disease processes (8,12,32).
The wide range of aggression promoting factors
illustrates the low specificity of the term
aggression (6).
Genetic predisposition
The significantly higher incidence of behaviour
problems involving aggression in certain canine
breeds indicates a genetic background. Blackshaw
(7) and Roll and Unshelm (27) mention that the
German Shepherd dog and the Bull Terrier are
most frequently involved in aggressive incidents.
Sherman et al. (29) and Uchida et al. (31) add the
Doberman Pinscher and the Lhasa Apso to this
list. Ushida et al. (31) mention the English
Springer Spaniel additionally.
Voith and Borchelt (33) perceive a higher
aggressiveness in pure-bred dogs compared to
mixed breed dogs. In contrast, Beaver (6) descri-
bes a higher incidence of aggressiveness in mixed
breed dogs.
Environment
An important environmental factor in the genesis
of canine aggressive behaviour is a lack of early
experience during the socialisation period (3,12).
Adult dogs are more aggressive towards species
with which they have had little contact in early
life, especially 3 to 12 weeks after birth (12).
Another environmental factor with a considerable
influence on the development of aggression is the
teaching of positive and negative behaviour by the
owner or by certain training programs. Aggressi-
veness can for example be taught intentionally to
fighting dogs, whereas behavioural therapy may
have an appeasing effect on hyperreactive dogs
(12).
Other potential aggression promoting factors are
the restraint from exerting breed-specific tasks
such as hunting or herding, or food scarcity during
gestation (10).
(Patho)physiology
The higher aggressiveness presented by male dogs
is very suggestive for the importance of the
physiological state in the expression of behaviour
(12,26,31,33). Furthermore, aggression is often
more pronounced in intact males compared to
castrated dogs and, although in a lesser amount, in
spayed females than in intact bitches (7,22,33).
The role of the male sex hormone testosteron in
these gender-related behavioural differences cannot
be ignored (22).
Hoerlein (13) however states that castration of
male dogs only affects the intermale aggression
type while territorial and fear-induced aggression
remain unaltered.
According to Voith and Borchelt (33) the higher
incidence of aggression in neutered females could
have three different causes. First, neutered bitches
are present in increasingly higher number in our
modern society. A second explanation for the
higher aggressiveness in spayed females could be
the fact that sterilisation is often the first therapeu-
tical approach to behaviour problems involving
aggression. A third explanation could be that some
bitches are androgenised in utero and spaying of
these animals may facilitate the expression of their
masculine behaviour (22,33).
The expression of masculine behaviour in neutered
females is more pronounced when sterilisation is
performed before the age of 12 months (19,26).
Other aspects with aggression promoting
characteristics are neurochemical dysfunctions (23)
and aging, especially when allied to a loss of
visual and hearing acuity (19).
Disease processes
Medical conditions that may affect aggressiveness
include neoplasia of the central nervous system,
infectious diseases (canine distemper, rabies),
epilepsy, developmental disorders (lissencephaly,
hydrocephaly), metabolic (hyper- or hypothyroidy)
and cardiovascular disorders, trauma and pain
processes (6,12,13,32). Disorders of the central
nervous system can induce aggressive behaviour in
several species, especially when located in the
frontal cortex, the hypothalamus, the thalamus, the
amygdaloid body, the medial mamillary nucleus,
the habenular nuclei, the hippocampus and the
caudate nucleus (9,14,16,17,21,24). These regions
are illustrated in figures 1 through 4. The specific
involvement of the frontal cortex (1),
hypothalamus (15) and amygdaloid body (2,13) in
behavioural changes in dogs has been established.
The behaviour modula-ting properties of the
caudate nucleus in dogs can be assumed because of
its connections with the frontal cortex (30).
Classification of aggressive behaviour
There are different ways to classify aggressive
 56

Figure 1. Medial view of the right brain half of a dog Figure 2. Rostrolateral view of the canine brain. The
showing important brain regions involved in aggression. left frontal lobe has been removed to visualise the
caudate nucleus (9).

Figure 3. Rostrolateral view of the canine brain. The Figure 4. Medial view of the right hemisphere with a
rostral part of the left hemisphere has been removed by lateral view of the dissected left hippocampus (8).
a transversal incision through the piriform lobe (10).
The position of the amygdaloid body (5) has been tinted
for better visualisation.

Legend to figures 1-4:

1. Frontal cortex 2. Cingulate gyms 3. Hypothalamus 4. Thalamus 5. Amygdaloid body
6. Mamillary body 7. Habenula . 8. Hippocampus 9. Caudate nucleus 10. Piriform lobe .

behaviour patterns. First a distinction is made systems, in aggression is classified

which
between intra- and interspecies aggression based according to the form or the context, respectively,
on the species, dog and human respectively, that is are discussed underneath.
the target of the aggressive insult (6,12).
In contrast to other authors, Askew (4) defines Descriptive classification
canine aggression directed towards dogs and The descriptive or empirical-operative classifica-
humans as intraspecies aggression when the dog tion system aims to describe the various
accounts his target as a member of his own behavioural patterns objectively in order to avoid
species, whereas interspecies aggression is directed premature conclusions based on the observer's
to a target that is not considered as belonging to early intuitive table 1 the
impressions. In
his kind. The objectivity of this classification is behavioural components involved in aggressive
challenged however, since the species perception behaviour are summarised. It shows that a single
of the individual dog is difficult to be estimated act can be the expression of several behavioural
unambiguously. ,7?
patterns. Biting and growling for ,example are
The descriptive and the functional classification expressed during both aggression and play.

Table 1. Descriptive classification of aggression
(according to Borchelt and Voith, 1982)
Behaviour Possible etiologies
Biting (snap, nip) Aggression
Play
Growling Aggression
Play
Baring teeth (lift lip) Aggression
Barking (whine, howl) Aggression
Separation behaviour
Play
Reaction to exciting stimuli
Social facilitation
Fear
Functional classification
The functional classification of aggressive
behaviour is the most commonly used method. It
is based on the emotional/motivational incentives
of the aggression. With the functional classification
scheme an attempt is made to deduce the function
of the aggression from its context and from the
relationship between stimulus and response (8).
Moyer (18) has introduced the functional classifi-
cation scheme in the conviction that the different
aggression types have a specific neurological and
endocrine background. Many authors have
extended or adjusted this initial classification with
the consequence that the aggression types
acknowledged by the different authors display a
considerable diversification (table 2). Possessive
aggression for example is considered as a separate
entity by Borchelt and Voith (8) and Overall (22),
while other authors include it within
dominance aggression type.
Each type of aggression is attended with a
description of the specific behavioural pattern and
the possible situations in which this particular form
of aggression can occur (8).
A remarkable approach of aggression classification
is given by Beata (5) who combined the descrip-
tive and functional classification systems. This
author describes five functional classes supplemen-
ted by a sixth descriptive class. The functional
classes are: predatory aggression, irritation
aggression, territorial and maternal aggression
(grouped into 1 class), fear aggression and hierar-
chical aggression.
A normal aggression sequence always exhibits a
57
warning phase (growling, exhibiting teeth,
posture), an action phase (biting) and a stop signal
(appeasing signal). Fear induced aggression is
often devoid of a clear warning phase, but facial
expression and/or posture and autonomic nervous
reactions such as trembling, mydriasis, urination
and defecation lead to the diagnose of this type of
aggression.
The sixth or descriptive class is identified as
instrumentalised aggression and is characterised by
a loss of the normal aggression sequence. The
warning phase and/or the stop signal disappear(s)
and only the action phase is constantly present.
Each of the five functional classes may evolve to
this sixth class of instrumentalised aggression (5).
The altered aggression sequence indicates that the
aggression has reached a pathological level. The
prognosis worsens in proportion to the loss of
sequence integrity (5).
Instrumentalised aggression has also been
described by Moyer (18) who defined it as a
learning process with an increased tendency for
exhibiting aggressive behaviour in response to
certain stimuli.
Other classification methods
Reisner et al. (25) mention other features that can
be used for the classification of aggression. One of
these features is 'the relative degree of inhibition
or disinhibition' by which a distinction is made
between attacks that are limited to a single bite and
attacks with multiple bites. The predictability of
the aggression could also be used as a
classification parameter (25).
Reisner (26) and Sacks et al. (28) describe a
the classification based on the severity of the caused
injury. The duration of the attack is another
possible criterion proposed by Reisner (26) for
assessing the pathological extent of aggression.
The frequency of aggressive insults is used as an
additional parameter by Blackshaw (7) and Reisner
et al. (25).
Discussion
The precise evaluation of aggression in dogs is
difficult because of the large number of factors
that have to be considered. Aggression is part of
the normal canine behaviour and there is a
manifest difference of aggressiveness between
several subpopulations of dogs. In the scientific
search for disorders that can affect the mechanisms
of aggressive behaviour it is desirable to select
 58

Table 2. The functional classification system of aggression types

Moyer (18) Borchelt and Hart and Blackshaw (7) Beaver (6) Overall (22) Beata (5)
Voith (8) Hart (12)

Dominance Dominance Dominance Dominance Dominance Hierarchical

Fear-induced Fear-induced Fear-induced Fear-induced Fear-induced Fear-induced Fear-induced
Territorial Protective Territorial Territorial Protective Territorial Territorial +
,
, maternal
Maternal Maternal Maternal Maternal Maternal . Territorial +
maternal
Predatory Predatory Predatory Predatory Predatory Predatory Predatory
Irritation Irritation
Instrumentalised Instrumentalised
Intermale Intermale/ Intermale Intermale Intrasexual Intercanine
interfemale
Learned Learned
Medical .

Pain-induced Pain-induced Pain-induced Pain-induced

Play Play
Redirected Redirected Redirected
Sex related
Idiopathic Idiopathic Idopathic
Sibling rivalry
Possesive - Possesive
Punishment-elicited
Competitive
- Food related

dogs that most likely exhibit a pathological form
of aggression, defined as a form that does not
comply with the normal behaviour code. To
determine the pathological state of the aggression a
specific set of criteria should be applied for each
subpopulation. For example, aggression of a dog
belonging to a more aggressive breed or strain
may not be evaluated with equal measures as the
same degree of aggression performed by a dog
from a less aggressive breed or strain.
Therefore numerous factors such as breed, gender,
early experience and the ability to perform breed
specific tasks need to be taken into account for
each individual dog. For example, aggression by a
hunting dog should be considered less severe when
the dog is not used for this purpose.
Another issue is the appropriateness of the
aggression in relation to the context. The tolerance
for a certain aggressive behaviour pattern is
strongly dependent on public opinion and on the
extent to which the environment is familiar with
the behavioural patterns of dogs in general. This
perception is liable to a subjectivity that needs to
be avoided in scientific research. This does not
exclude the fact that functional classification
schemes are highly valuable in this context for
-
practical diagnostics where therapy and prognosis
are of prior interest.
It is obvious that the predictability of aggressive
behaviour, which is suggested as a criterion for the
classification of aggression by Reisher et al. (25),
suffers from the same shortcomings as mentioned
for the appropriateness of aggressive behaviour.
Aggression will be more predictable to a person
who is familiar with canine behaviour patterns in
general and who can distinguish subtle signals.
The considerable amount of subjectivity undermi-
nes the reliability of this parameter.
 59
The severity of the caused injury as proposed by
Reisner (26) and Sacks et al. (28) is also a dubious
parameter for assessing the pathological extent of
aggressive behaviour, because it is strongly
influenced by various additional factors such as the
strength of the attacking dog and of the victim, the
predictability of the assault, the relative degree of
inhibition or disinhibition of the dog, and the
duration of the attack.
The descriptive classification is essential for an
unbiased evaluation of animal behaviour in order
to avoid false determination of different behaviour
patterns as aggression. It forces the evaluator to
set up a clear and objective description of the
behaviour patterns before any interpretation is
made. Therefore this classification should be
included in every evaluation protocol.
There is also a strong motivation for determining
the function of aggressive behaviour using a
functional classification because the various
functional aggression types are suggested to have a
specific neurological and/or endocrine basis (18).
Because many factors affect
aggression, a
simplified approach is desired for the practical
evaluation of the pathological extent of aggressive
behaviour. A suitable method is given by Beata (5)
who describes a functional classification system
combined with a descriptive class of
instrumentalised aggression which is characterised
by the absence of a warning phase and/or stop
signal. Each functional class can evolve to this
instrumentalised aggression. A major advantage of
this approach is the fact that it offers for all the
functional classes a general threshold, namely the
loss of the aggression sequence integrity, by which
the pathological level of the aggression can be
determined and a prognosis can be made.
The aggression sequence can be altered either at
the first aggressive assault or after an evolutionary
process in which a dog that previously exhibited a
normal aggression sequence undergoes a gradual
reduction of the warning phase and/or the stop
signal over a certain period of time until these
phases become absent.
The approach of Beata (5) has the additional
advantage that canine aggressiveness can be
assessed under various conditions (different
breeds, sexes, environmental factors), since dogs
with a high intrinsic aggressiveness are still
expected to exhibit the normal aggression
sequence.
It is important, however, that the classification of
dogs with instrumentalised aggression is performed
by experts who are familiar with the normal canine
behaviour repertory and are capable to correctly
interpret subtle signals. This is in particular the
case for fear-induced aggression which is
characterised by a limited warning phase and could
therefore be falsely defined as instrumentalised
aggression. However, the warning phase of
fear-induced aggression can be recognised by
facial and/or postural expressions and autonomic
nervous reactions.
The number of bites per attack as suggested by
Reisner et al. (25) could be a reliable parameter
because it yields information about the relative
degree of bite inhibition of the dog. Since some
dog strains are genetically selected for a reduced
bite inhibition, one may assume a considerable
genetical determination of this parameter.
Other factors, such as the duration of the attack as
mentioned by Reisner (26) and the frequency of
aggressive behaviour as suggested by Blackshaw
(7) and Reisner et al. (25), could also be related to
the pathological extent of aggressive behaviour and
should therefore be taken into account for research
purposes. However, the frequency of the assaults
is often difficult to determine because some dogs
are euthanised after the first aggressive incident
while in other cases attempts are made to solve the
problem by behaviour therapy and/or medication.
Conclusion
Several criteria described in the literature are
suitable for the practical classification of
aggressive behaviour. Some of these parameters
could give information about the pathological
extent of this behaviour. They include the objecti-
ve description of the behaviour pattern, the deter-
mination of the function of the aggression, the eva-
luation of the presence of the three phases of the
normal aggression sequence, and the assessment of
the degree of inhibition or disinhibition. Additional
parameters include the duration of the attack and
the frequency of the aggressive behaviour.
The presence of a normal aggression sequence is
the only parameter of which a direct link to the
pathological level of the aggression is mentioned.
Other features such as the appropriateness of the
aggression in relation to the context, the
predictability of the aggressive assaults and the
severity of the caused injury interfere with a
uniform classification because they are strongly
dependent on several external factors.
Further neurochemical research is planned for
studying the link between the various parameters
and the pathological extent of aggressive behaviour
in dogs.
 60
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