Latest Shock Collar Research

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https://www.thebark.com/print/6656?page=show
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Study looks at stress behavior associated with different training methods.
JoAnna Lou [3]
|
September 20, 2014
A study published earlier this month showed that shock collars can lead to an increase in
stress behaviors in dogs [4]. This may seem like stating the obvious, but these type of
training devices continue to be popular despite the risks. The research by the University
of Lincoln was commissioned by the U.K.'s Department for Environment, Food, and
Rural Affairs to provide scientific evidence on which to base their animal welfare policy
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8/25/15, 1:05 PM
https://www.thebark.com/print/6656?page=show
(pretty cool!).
The study was made up of 63 dogs that were identified as having poor recall skills and
related problems, such as attacking livestock, a main reason for the shock collar's use in
the U.K. The canine subjects were divided into three groups: Group A used a shock
collar under the direction of trainers nominated by the Electronic Collar Manufacturers
Association (ECMA). Groups B and C trained without a shock collar. One group under
the direction of the same ECMA trainers and the other with trainers from the Association
of Pet Dog Trainers, a group committed to reinforcement based methods.
The trainers worked with each dog for two 15-minute sessions a day, for five days. The
interactions were videotaped to analyze behavior, and saliva and urine samples were
collected to measure cortisol levels (a hormone associated with stress).
The researchers found that the dogs in the shock collar group showed significantly more
stress behaviors, such as tense body language, yawning, and disengaging with the
environment. Although a smaller preliminary study found higher cortisol levels associated
with the shock collar, there wasn't a significant difference in cortisol levels in the larger
research.
Furthermore, following the five days of training, 92 percent of owners reported
improvements in their dog's behavior. There was no significant difference in reported
efficacy across the three groups.
Some people say that there are certain behaviors, like a reliable recall, that can't be
taught without a shock collar. And that is simply not true. I've seen people train rock solid
recalls using only reinforcement based methods. It's nice to have this scientific research
to back up that claim. I was also impressed that the U.K. government commissioned this
research to inform their policy.
Of course training using reinforcement based methods doesn't come without dedication.
Unfortunately there are no shortcuts in dog training! However, a key learning from this
study is around the consistency in results across groups (as a side note, while results
seemed consistent in the short term, I believe that punishment tools, like shock collars,
can often develop unintended consequences in the long term). The short training
sessions repeated every day was the primary diver for getting results. Even if you only
train for five minutes a day, if you stick to it, you'll see progress in your training
challenges.
Print [1]|Email [2]
JoAnna Lou is a New York City-based researcher, writer and agility enthusiast.
Source URL (retrieved on 8/25/2015): https://www.thebark.com/content/latest-shock-collarresearch?page=show
Links:
[1] https://www.thebark.com/print/6656?page=show
[2] https://www.thebark.com/printmail/6656?page=show
[3] https://www.thebark.com/category/author/joanna-lou
[4] http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0102722
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8/25/15, 1:05 PM
The Welfare Consequences and Efficacy of Training Pet
Dogs with Remote Electronic Training Collars in
Comparison to Reward Based Training
Jonathan J. Cooper*, Nina Cracknell, Jessica Hardiman, Hannah Wright, Daniel Mills
Animal Behaviour, Cognition and Welfare Research Group, School of Life Sciences, University of Lincoln, Lincoln, United Kingdom
Abstract
This study investigated the welfare consequences of training dogs in the field with manually operated electronic devices (ecollars). Following a preliminary study on 9 dogs, 63 pet dogs referred for recall related problems were assigned to one of
three Groups: Treatment Group A were trained by industry approved trainers using e-collars; Control Group B trained by the
same trainers but without use of e-collars; and Group C trained by members of the Association of Pet Dog Trainers, UK again
without e-collar stimulation (n = 21 for each Group). Dogs received two 15 minute training sessions per day for 4–5 days.
Training sessions were recorded on video for behavioural analysis. Saliva and urine were collected to assay for cortisol over
the training period. During preliminary studies there were negative changes in dogs’ behaviour on application of electric
stimuli, and elevated cortisol post-stimulation. These dogs had generally experienced high intensity stimuli without prewarning cues during training. In contrast, in the subsequent larger, controlled study, trainers used lower settings with a prewarning function and behavioural responses were less marked. Nevertheless, Group A dogs spent significantly more time
tense, yawned more often and engaged in less environmental interaction than Group C dogs. There was no difference in
urinary corticosteroids between Groups. Salivary cortisol in Group A dogs was not significantly different from that in Group
B or Group C, though Group C dogs showed higher measures than Group B throughout sampling. Following training 92% of
owners reported improvements in their dog’s referred behaviour, and there was no significant difference in reported
efficacy across Groups. Owners of dogs trained using e-collars were less confident of applying the training approach
demonstrated. These findings suggest that there is no consistent benefit to be gained from e-collar training but greater
welfare concerns compared with positive reward based training.
Citation: Cooper JJ, Cracknell N, Hardiman J, Wright H, Mills D (2014) The Welfare Consequences and Efficacy of Training Pet Dogs with Remote Electronic
Training Collars in Comparison to Reward Based Training. PLoS ONE 9(9): e102722. doi:10.1371/journal.pone.0102722
Editor: Odile Petit, CNRS (National Center for Scientific Research), France
Received September 9, 2013; Accepted June 24, 2014; Published September 3, 2014
Copyright: ß 2014 Cooper et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The research project was commissioned and funded by defra of UK government AW1402 and AW1402a to provide scientific evidence on which to base
animal welfare policy (url: http://www.defra.gov.uk/). The project team did receive input from defra regarding project design and timescales, but ultimately the
project team was responsible for design of study. Defra also provided feedback on project reports from an independent anonymous review panel, and this
feedback has been taken into account in the final project report, from which this paper has been derived. The authors have support of the funding body to
publish findings of study following independent peer review.
Competing Interests: The authors have declared that no competing interests exist.
* Email: [email protected]
to precede the electric stimulus. These in combination with other
cues, such as verbal commands, offer the potential for avoidance
learning by dogs [6] which potentially allows the handler to train
more desirable behaviour in a given situation.
The arguments for and against their use have recently been
reviewed by the Companion Animal Welfare Council [1], which
also highlighted the emotional level of argument used and lack of
scientific evidence to draw solid scientific conclusions for welfarebased policy decisions on this matter. The emotion of the
argument is reinforced by spectacular public demonstrations of
the misuse of these devices on sites like YouTube (e.g. http://
www.youtube.com/watch?v = _T9qiGCq5sk, the first video to
come up on this site when the term ‘‘shock collar’’ was entered as a
search term on this site 19/8/13). There is, however, a lack of
description of the immediate responses of animals to the use of
these devices in the scientific literature, on which to base scientific
and practical considerations. There are some clear theoretical
welfare risks, such as the failure to link delivery of the e-collar
stimulus with clear conditioning stimuli, or poor timing of response
Introduction
The use of collar mounted electronic training aids, such as radio
fence systems to deter roaming, anti-bark devices and manually
operated remote training devices is controversial and their use has
been banned in some countries, whilst being the focus of
considerable political debate in others [1]. For critics of these
devices (often called shock collars or, less emotively, e-collars), they
represent an unacceptable means of correcting undesirable
behaviours [2], whilst others claim they can be useful tools for
addressing behavioural problems in pet dogs [3,4].
The technical features of manually operated e-collar systems has
recently been described by Lines et al [5], but broadly speaking
they consist of a collar mounted device capable of delivering a
short electric stimulus to the neck of a dog via two protruding
blunt electrodes. The device is controlled by a hand set, which
typically provides a number of settings governing the intensity and
duration of stimulus. Most modern devices also allow handleroperated pre-warning cues such as an auditory or vibration signal
PLOS ONE | www.plosone.org
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September 2014 | Volume 9 | Issue 9 | e102722
Welfare of Dogs Trained with E-Collars
and reinforcement [3,6,7], which have been investigated experimentally [8–10]. These studies show that these devices have the
potential to cause distress and pain, but do not address the
question of whether the use of these devices necessarily causes
distress; i.e. when used in accordance with best practice by trainers
experienced in their use. Indeed it has been suggested that from a
theoretical perspective, efficient avoidance conditioning may not
always be a significant cause for welfare concern [1].
Although organisations such as the British Veterinary Behaviour Association (formerly Companion Animal Behaviour Therapy Study Group, who advise the veterinary profession in the UK
on related policy especially towards pets) state that other reward
based methods are similarly effective without the associated
welfare risks [11], there do not appear to be any scientific studies
to corroborate this statement, especially in relation to efficacy
equivalence. Indeed, an experimental study examining the effect of
rewards and punishment in the control of ‘‘instinctive’’ behaviour
by dogs, concluded that ‘‘negative reinforcement and punishment
may be desirable and necessary additions to positive reinforcement
techniques’’ [12]. Advocates of such devices suggest they are
particularly useful for correcting behaviour at a distance from the
operator during off lead activity, such as poor recall, or livestock
chasing, when, for example, a food reward cannot be delivered
remotely; and in previous studies, these indications were reported
to be the two commonest reasons for using such devices in the UK
[13,14].
Studies of dogs undergoing e-collar training have also tended to
focus on sub-populations of dogs such as those trained for police
work [10], hunting [15] or model populations of laboratory dogs
[9]. These populations do not, however, represent the context of
their most common use, i.e. with the companion/pet dog
population [13]. Furthermore, where studies used older devices,
it is possible they are not representative of more modern devices.
Retrospective studies, such as Blackwell et al. [13], have been
undertaken on pets and found that the use of rewards was
associated with a higher rate of success compared to the use of an
e-collar for controlling chasing, but, as the authors acknowledge,
this may simply reflect differences in severity of the problem
between the two sets of respondents. When considering the
necessity of a procedure which has the potential to cause harm, it
is essential to consider both efficacy and welfare impact of best
practice in situ, and to date no study has addressed both of these
factors in relation to the use of e-collars in training.
In this study, we aimed to fill three important gaps in our
knowledge of the use of e-collars for training pet dogs. Firstly, we
described the responses of dogs in the field to training with an ecollar. Secondly, we investigated whether the welfare of dogs
trained with an e-collar was necessarily compromised in comparison to approaches which did not rely on use of e-collars, when
trying to address the most common problems for which e-collars
are often advocated. Finally we investigated the efficacy of e-collar
training in addressing these problems in comparison to other
approaches. In the first study, which also acted as a preliminary for
the main experimental study, we used largely qualitative
observational methods to describe the responses of dogs being
routinely trained with e-collars, since accurate information from
the everyday use of these devices has been missing from the
scientific literature [1]. In the main experimental study we used
the information gained from this initial work to execute a
quantitative assessment of the behavioural and physiological
effects of different training regimes on animals exhibiting typical
problems for which e-collars are advocated. By controlling for
trainer and method of training, we were able to evaluate whether
the use of an e-collar produced a significantly different result
compared to a regime that did not use an e-collar, both in terms of
the welfare of the subject being trained and the resolution of the
problem for which the owner was seeking help. This latter study
was conducted using e-collar training protocols that were
consistent with the published recommendations advocated by
collar manufacturers [16–19] and delivered by trainers with
considerable experience of training with and without e-collars.
Data from these dogs were compared with data from dogs trained
by the same trainers but without e-collars and by trainers who
were members of the APDT (UK), an organisation that does not
advocate the use of e-collars. By doing this we could control for the
risk of any potential bias towards the use of the e-collar.
Study Design
The paper presents findings of two studies; a preliminary study
involving nine dogs was used to generate initial qualitative data on
the use of these devices under typical conditions and refine data
collection techniques in the field. This was followed by a larger,
controlled study which involved 63 dogs. For this, volunteered
subjects who had been referred for problems commonly addressed
using e-collars such as recall problems and livestock worrying [13]
were allocated with the informed consent of owners to one of three
Groups; one using e-collars and two control populations where
dogs were not exposed to e-collars (Table S3 in File S2). The ecollar treatment Group (Group A) consisted of dogs referred to
professional trainers who were experienced in the use of e-collars
to improve off lead recall. Control Group B were dogs referred to
the same trainers but trained without the use of e-collars, whilst
Control Group C included dogs with similar behavioural problems
to those in Group A, but referred to professional trainers who were
members of a professional training association focused on reward
based training, that do not allow use of e-collars (or other
potentially aversive techniques or equipment) by their members
(Association of Pet Dog Trainers, UK). Dogs in Groups B and C
were subject to the same protocols as those in Group A but with no
use of e-collars. Training focussed on improving off lead recall
when dogs were exposed to livestock (sheep, poultry) and other
dogs. Behavioural and physiological data that related to dog’s
emotional state [8,20] were collected during training to assess the
immediate impact of exposure to e-collar stimulus in comparison
to control Groups, as well as adaptation to training protocols.
Dogs were allocated to treatment Group A and control Groups B
and C using owner’s pre-training assessment of the nature of the
referred problem and its severity in order to balance these factors
across the three Groups, and owners were surveyed following
training to assess the efficacy of training.
Methods
Ethical Statement: Ethical approval was provided by University
of Lincoln Research Ethics Committee following discussion with
Home Office Inspectorate in September 2008 for the preliminary
study and September 2010 for the main study. Ethical approval
was granted as the devices were legal in participating countries and
the research team were not modifying trainers’ normal use of ecollars. As part of the ethical considerations relating to this project,
only adult dogs (over 6 months of age) with no previous experience
of e-collars were used, and only subjects that had been voluntarily
referred by their owners to trainers who would normally consider
the use of e-collars for managing the behavioural problem for
which they were referred were enrolled in the study. Owner
consent forms were provided to owners prior to the recruitment of
their dogs and all the owners of the dogs gave permission for their
animals to be used in this study.
2
effective, involved minimal restraint and could be employed
without interfering with training. All dogs readily supplied
adequate saliva with cheese used as a lure to stimulate interest
and salivation.
Behavioural data were collected by the research team on hand
held video cameras before, during and after the exposure to the
electric stimulation. Six of the 8 dogs referred for sheep chasing
only engaged in one or two approaches, and received a single
application of the electric stimulus each time they approached
sheep, which led to a cessation of approach. One dog referred for
sheep chasing did not approach sheep during the training sessions,
but received two stimuli at points when it was orientated towards
nearby sheep. One dog received 5 exposures to e-collar stimuli
before approaches ceased. As dogs were relatively free to roam
open fields during training, video operators chose to position
themselves where they could have best view of dogs when in
proximity to sheep. As a consequence, it was not possible to have
full video records of the entire training period, but good records
were made of the period immediately before and immediately
after approach to sheep and exposure to electronic stimulation.
For analysis of behaviour before and after exposure to e-collar
stimuli, periods of up to 30 seconds prior to and after each
exposure based on known times of application were used. Video
analysis was conducted by a trained video observer who was
independent of the research team in the field and blind to the
purpose of the study. The draft ethogram included: time spent in
postures such as sit, stand, walk and run; tail position and
movement; panting; overall behavioural state including excited,
relaxed, tense; and the frequency of number of activities drawn
from studies of training in dogs, as well as studies of aversion or
anxiety [8,29–31]. These included vocalisations, lip-licking,
yawning, paw-lifts and body-shakes. Finally the video observer
was asked to note any unusual changes in behaviour during the
observations.
As the length of time in view during data collection varied
between samples, data for behavioural states and postures were
converted into percentage of observation time. These provide
useful, independently documented field observations of pet dogs’
responses to e-collar use in the field. Descriptive statistics only are
presented for these behavioural data. As saliva samples could be
sampled consistently, these data were analysed using a repeated
measure ANOVA on log transformed cortisol concentrations, with
post-ANOVA Tukey test used to identify differences between
sample periods.
Preliminary Study
A preliminary study was used to generate initial qualitative data
on the use of these devices under typical conditions and refine data
collection techniques in the field for the subsequent more
controlled study. This included: assessing if saliva could be reliably
collected in the training context without interfering with the
training programme; evaluating the use of video data collection in
the field; and developing an ethogram of behavioural responses to
training for the main study. Data collection was focussed around
the initial exposure to e-collar stimuli, when used to resolve the
behavioural problem that was the basis of referral. For this
preliminary study, trainer contact details were obtained from
publically available marketing (e.g. websites, magazine advertisements) or through collar manufacturers. Nine visits were
conducted with four trainers who had 1 dog, 1 dog, 2 dogs and
5 dogs booked for e-collar training respectively; all were willing to
allow video recording of the training. 8 dogs had been referred for
sheep chasing and 1 for poor recall. Each dog received training
over short periods on a single day. Training occurred in rural
locations (i.e. farm yards and fields).
One trainer, who was training a single dog for improved recall,
followed a protocol that was broadly similar to that advocated by
collar manufacturers [16], in that the trainer initially established
the intensity of collar setting that caused a mild response in the
dog, and used this setting in combination with pre-warning cues to
train the dog to return or recall on command. The remaining 3
trainers were training 8 dogs referred for sheep chasing and they
adopted a different approach. The collar was fitted prior to
exposure to sheep and there was either no assessment of dog’s
sensitivity to electric stimulation prior to training (two trainers of 3
dogs) or the dogs received a single low intensity stimulation to
check the collar was working (1 trainer of 5 dogs). Thereafter, for
all but one dog (which was exposed to a setting at the higher end of
available range) the trainers selected the highest setting available
on the device and dogs were allowed to roam off-lead in a field,
where sheep were present. If dogs approached sheep, then the
trainer would apply an e-collar stimulus using the high setting with
timings of their choice. These trainers stated that they aimed to
associate proximity to or orientation towards sheep with the estimulus, and consequently did not plan to use pre warning cues
such as the collar mounted tone or vibration stimuli as a predictor
of electric stimulation.
Saliva was collected at 4 sample periods to allow assay of
salivary cortisol [21–23]. These were on first arrival at the training
location (Sample0), about 15 minutes after the e-collar had been
fitted to the dog where it was allowed to engage in moderate
exercise, but where no electrical stimuli had been applied
(Sample1), about 15 minutes following final exposure to electronic
stimulus during training (Sample2), and about 40 minutes
following training (Sample3). These timings had been drawn from
relevant research into dog’s responses to potentially arousing
stimuli [24] and verified by the research team [25] in a training
context. In this part of the study we did not control for time of day,
as we were dependent on availability of trainers, with training
sessions normally occurring between 10am and 2pm on each day.
However studies of patterns of cortisol secretion in owned dogs
rarely find evidence of circadian patterns and any temporal
patterns are best described as episodic, relating to key events in the
day, rather than light dark cycles [26–28]. For this, a large cotton
bud was placed towards the back of the dog’s mouth, and the
saliva extracted before being immediately stored on ice, prior to
storage at 240uC. At the end of the preliminary study samples
were assayed by Food and Environment Research Agency (FERA)
using standard protocols. The sampling technique was simple and
Results: Preliminary Study
Video analysis of the preliminary study noted some variation in
the immediate reaction of dogs to each application of stimulus, but
stimulus reaction could be broadly described as an abrupt change
in locomotor activity, normally from walking or running to abrupt
halt, or other distinct change in direction of travel and gait. The
one exception was the dog trained for recall alone with a warning
stimulus and on a lower setting than the sheep chasers, and whilst
an apparent response to e-collar stimulus was detected in terms of
change in orientation and posture, this appeared less pronounced
than that observed in sheep chasers.
Dogs showed a number of additional changes in behaviour in
the period following electric stimulus presentation, compared with
behaviour prior to stimulus presentation. Dogs showed an increase
in vocalisation, with none recorded prior to first stimulus
compared to a total of 13 ‘‘yelps’’ and 5 ‘‘whines’’ after exposure.
There was a change in tail carriage from principally an elevated
carriage prior to exposure (with only 2% of time was the tail
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between legs) to the tail being between legs 20% of the time
following exposure. Prior to stimulus application the dogs were
generally described as being in a neutral (40% of time) or
investigatory (20%) state with only 10% of time described as tense;
whereas afterwards, dogs were tense for 50% of the time and spent
only 5% of their time engaged in investigatory behaviour. A small
number of yawns and paw lifts were observed after stimuli, but
none seen before exposure. Bouts of lip licking and body shaking
were recorded before and after exposure at approximately the
same rate. Finally there was an increase in owner interaction by
the dogs after exposure to the stimuli (56% of time compared with
14% prior to stimuli), with several dogs looking towards or
returning to their owners soon after application of stimulus. On
returning to owners, dogs received praise and attention.
There were individual differences between dogs in salivary
cortisol output, F8,23 = 3.44, p = 0.009, and also sample time effect
(F1,7 = 3.29, p = 0.041) with post-hoc Tukey test indicating a
difference between Sample1 prior to training and Sample2
following exposure to e-collar stimulation (T = 2.89, p = 0.042),
suggesting that salivary cortisol following exposure to sheep and
training involving e-collar stimuli was elevated in comparison to
the pre-training sample (Figure 1).
developed to accommodate this in statistical analysis and
interpretation of results.
Prior to allocation to Groups a questionnaire was used to collect
data on the general characteristics of dogs, their past training
history and information on why owners were referring dogs for
training. Owners were asked to broadly rate the intensity of the
main referred problem as; 1 ‘‘Always displayed’’, 2 ‘‘Frequently
displayed’’, 3 ‘‘Occasionally displayed’’, 4 ‘‘Rarely displayed’’ and
5 ‘‘Never displayed’’. Recruited dogs were primarily selected on
the basis of attention and recall related problems (including
livestock worrying and wildlife chasing) and the need to train a
recall task at distance. Reason for referral was the main selection
criterion as it was important that the control dogs presented
similar behavioural problems and similar levels of severity as those
dogs exposed to e-collars. Dogs younger than 6 months of age or
with prior experience of electronic training devices were excluded.
Two experienced dog trainers were nominated by The
Electronic Collar Manufacturers Association (ECMA) to train
dogs in Groups A and B, with equal numbers of dogs allocated to
each Group and each trainer working with half the dogs in each
Group. The trainers used in Groups A and B commonly used ecollars to address these problems, but did not use these collars
exclusively or with every case referred to them. Dogs were
allocated to either Group A or B by the research team, based on
information provided by owners prior to training on the nature of
the referral and severity of problem. The ECMA nominated
trainers had no influence on allocation to Group, but if following
interview by the research team, owners expressed a preference for
or a concern against training with e-collars, they were swapped
between Groups with a dog with equivalent training problem and
severity. This represented a small number of owners (2 pairs i.e. 4
dogs swapped).
For Control Group C, two trainers with a similar amount of
dog-training experience to the trainers used for Groups A and B
and who belonged to a professional training organisation
(Association of Pet Dog Trainers, UK; APDT, UK) which is
opposed to the use of e-collars were recruited to train the same
number of dogs presenting with similar problems. Dogs were
selected for this Group from volunteers to match dogs studied in
Treatment Group A based on reason for referral and severity of
problem. Volunteered dogs therefore were allocated to one of
three Groups (Table S3 in File S2). The average age of dogs used
in the study was 46 months and there was no significant difference
Main Study
The study investigated the immediate effects of exposure to ecollars in a pet dog training context, using experienced e-collar
trainers (Group A) and compared their responses with a
population presenting to the same trainers with similar behaviour
problems for training without the use of an e-collar (Group B) and
a similar population presented to trainers who do not advocate the
use of e-collars in training (Group C). Data collection focused on
behavioural and physiological measures of emotional state before,
during and after training as well as efficacy. The choice of sample
size (21 in each Group) considered the population sizes used in
previous between-subject design studies examining the effect of ecollars in more extreme situations (15–16 subjects in Schilder and
van der Borg) [10] with an additional 40% to increase sensitivity,
given an anticipated smaller effect size. Differences detected at this
level, would be substantial enough to be considered practically
important, while reducing the risk of Type I errors which might
confuse the interpretation of main effects. However, it is
recognised that other potentially valuable effects may not be
detected as significant using this sample size and so a strategy was
Figure 1. Log10 salivary cortisol (mean ± SE) on arrival at training centre (Sample 0), following training without e-collar when dogs
were allowed free exercise (Sample 1), 15 minutes following training with an activated e-collar (Sample 2) and 40 minutes
following training with e-collars (Sample 3).
doi:10.1371/journal.pone.0102722.g001
4
Dogs were trained at one of two training centres. Dogs in
Groups A and B were trained at a farm location near to
Edinburgh during Autumn-Winter 2010. Dog training initially
occurred in a field setting with a small flock of sheep and small
flock of poultry penned in the training field. When weather
conditions were not conducive to outdoor training, the training
was relocated to a yard on the same farm with similarly penned
animals. Dogs in Control Group C were trained at Riseholme near
Lincoln in Spring 2011, with a field set up to replicate conditions
originally used in the Edinburgh training centre. The timing of
data collection was related to the availability of professional
trainers, and the consequences of this will be discussed in light of
findings of the study. Each training session lasted approximately
15 minutes and each dog received two training sessions per day,
one in the morning and one in the afternoon. Behavioural data
were collected by video recording for the full duration of each
training session, on days 1, 2, 3, 4 and 5 as applicable.
Behavioural Data - Video Analysis. An ethogram based on
review of the preliminary study, and with input from a related
study on long term effects of e-collar training [14], was developed
to cover time spent in different postures, in different qualitative
behavioural states, tail positions and panting and the frequency of
activities (Tables S1 and S2 in File S1). Video analysis was
conducted by four observers with experience of behavioural
recording who were blind to Groups and the objectives of the
study. Each observer received training to become familiar with the
ethogram developed for this study and the data collection
protocols, and to allow assessment of inter-observer reliability.
Inter-observer reliability was tested by allocating four videos to
different observers at an early stage of analysis. Consistency in
scoring was assessed by calculating the correlation co-efficient r for
the behavioural categories. Where r.0.8, it was assumed there
was good agreement between observers’ scores and they were
reliably following the sampling method. Where there was poor
agreement (r,0.8), observers received further training to address
inconsistencies. This was only necessary for one observer, who
following retraining and re-analysis of early tapes was in good
agreement with all other observers for the rest of data collection.
Training videos were allocated so that each observer had similar
numbers of dogs from each Group, although they were also blind
to this partition.
Data from training videos were extracted from video tapes using
a Microsoft Excel based check-sheet with each video having two
sets of observations recorded. The first observation used an
instantaneous scan sample technique where videos were sampled
once per minute (up to 15 scans per video). At each sampling point
the dog’s posture (sit, stand, walk, run), overall behavioural state
(relaxed, tense, excited, neutral), distance to trainer and distance to
owner, tail carriage and movement, and panting were recorded. If
dogs were out of sight or behaviour could not be determined at the
sampling point then each category of behaviour was recorded as
unknown. The second observation consisted of a continuous
sample of the frequencies of key behavioural events. These
included oral activities (yawn, lip licks (with or without food)) and
vocalisations. In addition, any time out of view was recorded. This
allowed calculation of the frequency of events per minute of time
in view for analysis. Categories used in these ethograms were
derived from previous studies investigating anxiety and arousal in
dogs [8,29–31] as well as the experience of data collection during
the preliminary study and project AW1402 [14].
Efficacy of training was assessed by questionnaire distributed to
owners one week following training. Where owners did not return
this questionnaire, the questionnaire was resent. This resulted in
responses from all 21 owners whose dogs joined Groups A and C,
in age of dogs between the three Groups. Thirty four out of the
sixty three dogs were female (54% of sample), with similar
numbers of female dogs in Groups A (n = 13) and C (n = 12), but
slightly less in Group B (n = 9), but this difference was not
significant (X2 = 1.661, df = 2, p = 0.436). Gundogs and cross
breeds were the most commonly referred breed-types, represented
by 16 dogs each (51% of the sample in total). The remaining dogs
were pastoral breeds (n = 11, 17%), terriers (n = 8, 13%), hounds
and working breeds (both n = 6, 10% each). There were no
representatives of toy or utility breeds as defined by The Kennel
Club in the UK (Table S3 in File S2).
There was, therefore, no difference in age profile, sex ratios or
breed prevalence between the three Groups. The primary
justification for the inclusion of the three Groups used was as
follows: any significant differences between Group A versus B and
C would most likely reflect the effect of the use of an e-collar in
training; whereas differences between Groups A and B versus C
would most likely reflect either trainer or environmental effects. As
previously mentioned, the inclusion of Group C, ensured that we
matched for trainer experience and familiarity with preferred
training techniques (including their choice to include or exclude ecollar use). Therefore differences between A and C can be
considered to reflect differences between best practice use of the ecollar and best practice which excluded the use of an e-collar.
When trying to draw conclusions about the welfare implications of
an intervention it is important to triangulate the available evidence
in order to make the most robust inferences. Accordingly in the
discussion below, we consider the significant effects after
correction for false discovery and then evaluate these in light of
the more marginal effects (i.e. effects that would have been
significant if the difference observed had been replicated in a
sample size twice that used).
Dog Training protocols. During training, data were collected over a period of up to 5 days covering introduction to ecollar and other training stimuli and the period of initial
modification of behaviour. For Group A the choice of collars
and precise training regime were determined by the trainers, using
e-collars with a variable setting to allow the operator the
opportunity to determine the level at which the e-collar stimulus
was to be delivered, and a pre-warning cue which might allow
dogs over time to modify behaviour prior to exposure to e-collar
stimulus. Trainers only worked with their preferred make and
model of device, which were Sportdog SD-1825E (n = 11) and
Dogtra 1210 NCP (n = 10). E-collars were chosen that had both
tone and vibration pre-warning cues, however, with the agreement
of the trainers, only vibration cues were used during training to
ensure video analysis was blind to treatment.
Dogs’ individual training regime was determined by the trainer
and followed typical good practice for resolving the problem under
referral given the chosen method. Dogs in Group A were to have
the working level of e-stimulus determined on day 1 of training,
whilst on subsequent days non-compliance with trainer given cues
would be associated with potential exposure to the e-stimulus, with
the pre-warning stimulus used as desired by the trainer. Dogs in
this Group were also exposed to positive reinforcement such as
food, play and/or praise for compliance. Dogs in control Groups B
and C wore a dummy collar (de-activated e-collar) to control for
collar wearing and ensure observers of video tapes were blind to
treatment. On the final training day (normally day 5), all dog
owners conducted training under instruction from the trainers. For
a small number of dogs, where trainers felt training had progressed
sufficiently, this final owner training day was day 4, and the dogs
did not return for a 5th day of training. This represented one dog
from Group A and one dog from Group B.
5
and 19 returned questionnaires for Group B. Questions related to
the owner’s perception of improvement in both their dog’s
behaviour, whether they were continuing to use the training
techniques they had learnt during the sessions, and their
confidence in using these techniques. Responses were scored
using a five point semantic differential scale for each item, for
example from very confident to not confident, or from very
satisfied to very dissatisfied, which were then allocated numerical
scores from 1 to 5 for analysis.
Statistical Analysis. Data analysis was completed in Minitab
15.0 using parametric approaches where appropriate on raw data
or following transformation. Rare behaviours seen in less than
10% of dogs were removed from analysis, as were distance to
owner and distance to trainer as these could not be reliably
assessed for many videos as human subjects were out of frame for
long periods. Where data were collected over several phases of
study, then a repeated measure design was conducted with dogs
nested within Group used as the between subject variable, or
where data did not meet requirements of parametric analysis
sampling period effects were assessed using Friedman ANOVA on
each Group.
This approach, however, resulted in some loss of dogs from
analysis where data were not recorded over all sampling periods.
For example where dogs ceased training on day 4, but more
particularly with sampling of urine where some owners (n = 23)
were not able to extract first passage urine from their dogs on
every training day. As no sampling order effects were found during
preliminary analysis, the data for each dog were averaged across
sampling periods in order to provide data on every dog in each
Group. These were analysed with a one way ANOVA for
parametric data or Kruskal-Wallis test for non-parametric data. A
post-hoc Tukey test was employed to test for differences between
Groups where Group effects were identified from ANOVAs (or
pair wise Mann-Whitney for non-parametric data). Finally for
dogs in Group A, although it was not possible to determine the
number of applications of electronic stimulus during training, data
were available for the device setting during each training session,
which allowed analysis of co-variance between behavioural
responses and collar settings (controlling for trainer/collar brand)
for parametric data and Spearman rank correlation for nonparametric data.
As the behavioural data analysis included multiple comparisons
of related data, correction factors were used to control for Type I
errors. For this the False Discovery Rate method developed by
Benjamini & Hochberg [32,33] was used to take into account the
analysis of a large number of behavioural measures. Variables that
met these corrected criteria are presented in bold in Tables S4 and
S5 in File S2 and described in text as being a significant effect.
had wanted further advice on addressing off-lead problems. A
numerically higher proportion of dogs in Group C were described
as always showing the referred problem (67% of Group) compared
with 48% of Group A and 33% of Group B, but this difference was
not statistically significant (X2 = 4.79, df = 2, p = 0.091).
Behavioural Measures During Training
There were no day effects on dog activity, panting, behavioural
state or tail carriage over the five training days. Dogs in Groups A
and B were recorded as spending roughly half of their time
walking during training, which was significantly more than dogs in
Group C, who were observed significantly more often to be
standing during the training sessions (Table S4 in File S2). There
were also significant differences between Groups in sitting which
was most common in Group A and least common in Group C. No
differences were found in tail carriage or movement between
Groups.
Panting appeared to be twice as common in Group A dogs
(20% of scans) as Groups B and C (both about 10%), however, this
was not a significant effect. Close examination of the data
indicated that a small number of dogs in Group A showed elevated
rates of panting; 4 dogs were panting in over 50% of scans,
compared with none in Groups B and C. There was no evidence
of a difference in percentage of scans in the behavioural states
relaxed, ambiguous or excited (Table S4 in File S2) between the
three Groups. There was a difference in time spent in a tense state,
as dogs in Group C spent less time tense than dogs in Group A
(Tukey, t = 3.14, p = 0.007), but no difference between Groups A
and B or B and C (t,1.87, p.0.16).
There were no day effects on continuous recorded activities.
There were differences between the Groups in the rates of a
number of activities (Table S5 in File S2) Overall, lip-licking was
similar between the three training approaches, however, when this
was separated between lip-licking in association with food, then
Group C dogs showed more food related lip-licking than dogs in
either Group A or B. In contrast, differences in lip licking in
absence of food were not significant at the sample sizes in this
study.
Dogs from Group A showed more yawning than dogs in Group
C (Table S5 in File S2). Sudden movements away from trainer,
including rapid turning away of head or body movements,
appeared to be least common in Group C, though this was not
significant at the sample size of the study. Dogs in Group A
appeared to engage in most yelping, though yelping was rare in all
Groups and most dogs were not recorded yelping in any training
session. It appeared to be about 5 times more common in Group A
than in either Group B or C, but this apparent difference was not
significant. As with panting, yelps appeared to be primarily
observed in a small number of dogs in Group A; the majority of
dogs in that Group showed no yelping. There was, however,
evidence of a relationship between vocalisations and collar settings
for Group A dogs, with yelping (F1,17 = 7.58, p = 0.014) and all
vocalisations (F1,17 = 10.7, p = 0.004) increasing with average
collar stimulus intensity setting across training days. These
differences appear to largely relate to a small number of dogs
trained at higher settings showing high frequencies of vocalisations
with most dogs in Group A showing no or few vocalisations during
training sessions (Figure 2).
Two further aspects of training were found to differ between
Group C and both Groups A and B. These were the number of
commands given, where dogs in Groups A and B appeared to
receive about twice as many commands per training sessions than
dogs in Group C (Table S5 in File S2) and sniffing or
Results: Experimental Study
Reasons for Referral in Sample Population
The majority of dogs referred had chasing or worrying as their
owner’s primary concern (51 dogs or 81% of sample), involving
chasing sheep/lambs, horses, rabbits, joggers and cars, or a
combination of these. These were similarly represented in the
three Groups. Nine dogs (14%) were referred for general recall
problems without the owners reporting any issues with chasing or
worrying, whilst three dogs (5%) had owners whose primary
concern was aggressive encounters with other dogs whilst off lead
(Table S3 in File S2). The majority of owners rated the problems
as either 1 (‘‘always displayed’’, 31 dogs or 49% of sample) or 2
(‘‘frequently displayed’’, 24 dogs; 38%). Six dogs were rated as
occasionally displaying the problem, two as rarely, but the owners
6
Figure 2. Scatter plot of rate of vocalisations per minute against average collar settings (Stimulus intensity) used during training
for the two collars (W being Sportdog SD-1825E (n = 11) and X being Dogtra 1210 NCP (n = 10)) used with Group A dogs.
environmental interactions, which occurred at about half the rate
in Groups A and B, then in dogs in Group C.
Owner Perception of Efficacy
Overall, owners were generally satisfied with the training
programmes in which they had participated. 88.5% of owners
reported they had seen an improvement in their dog’s general
behaviour and 91.8% reported that there had been an improvement in the obedience problem for which their dog had been
referred (Figure 3). There were no significant differences in the
responses of owners from the 3 Groups. 18 out of 19 owners
(94.7%) from Group B reporting improvement in both measures,
whereas 18 out of 21 owners (88.5%) of owners who had
participated in both Groups A and Group C, considered that their
dog’s general behaviour had improved. 19 out of 21 owners
(90.5%) from both Groups A and C also considered obedience
with respect to the referred behaviour had improved. 90.2% of
owners reported they were satisfied with the training advice they
received (Figure 4) and 88.5% indicated that they were continuing
to use the trainers’ advice both for general dog behaviour and in
relation to the problem that was the reason for referral (Figure 5).
There was no evidence of differences between the three training
Groups in these measures of satisfaction.
The majority of owners (91.8%) reported they were confident of
being able to continue to apply the training techniques. All 21
owners (100%) from Group C, and 18 out of 19 respondents
(94.7%) from Group B stated they were confident of continuing to
effectively use the training programme, compared with only 16 out
of the 21 owners (76.2%) in Group A (Figure 6). Chi squared
analysis suggests there was a significant differences in confidence
between these three Groups (X2 = 8.33, df = 2, p = 0.016), though
the size of each of the non-confident cells was small. Investigation
using a Fisher’s exact test indicated that there was a difference in
confidence with training approach between Group A and Group
Physiological Measures During Training
Overall there were no consistent differences between sampling
periods in salivary cortisol, and no evidence of interaction between
sampling period and Group, but there was a Group effect on
salivary cortisol (F2, 59, = 6.11, p = 0.004), with dogs in Group C
(logCort = 3.1060.016) having higher levels during the study than
those in Group B (logCort = 2.9260.022; LSD, p = 0.001). Values
from Group A (logCort = 3.0260.023) did not differ from those of
Group B (LSD, p = 0.08) or Group C (LSD, p = 0.066). These
Group differences were found in both the pre-training samples on
day 1 and day 5 (F2, 59, = 3.35, p = 0.042) and the post training
samples on days 1 through to 5 of training (F2, 59, = 5.32,
p = 0.008). Furthermore, when the average pre-training sample
measures were subtracted from average post-training sample
measures, there was neither an overall difference (Paired t-test,
n = 62, t = 0.18, p = 0.85) nor a Group effect (F2, 59 = 0.03,
p = 0.96).
Overall there was no significant difference in urinary cortisol to
creatinine ratios between Groups before (F2,59 = 0.91, p = 0.41) or
after training (F2,59 = 0.03, p = 0.97) with average values of
1.6560.11 for Group A, 1.6960.23 for Group B, and
1.6460.14 for Group C in the four samples taken after training
sessions had been experienced. There were also no changes in
concentration ratios over the five days of training for any Group.
There was no effect of collar setting on any physiological measures
in Group A.
7
Figure 3. Percentage of owners in each response category indicating that training was effective at improving dog’s referred
behaviour.
Figure 4. Percentage of owners in each response category who were satisfied with the training methods used.
8
Figure 5. Percentage of owners in each response category who would continue to use the training methods to address the referred
behaviour.
C (p = 0.048) and between Group A versus Groups B and C
combined (p = 0.015), whereas no other combinations were
significant, suggesting that owners of dogs who experienced ecollar training (Group A) were less confident in applying the
training approaches seen than those whose dogs were not trained
with an e-collar.
experience. This approach to controlling behaviour around prey
species requires good timing on the part of the handler, as poor
association between the stimulus and related cues has been found
not only to be ineffective in changing behaviour [34], but also to
result in prolonged elevation of corticosteroids [9].
In our preliminary study, we observed distinct changes in
behaviour, including sudden changes in posture, tail position and
vocalisations that are consistent with pain and/or aversion in dogs
[8,10]. The significant elevation in salivary cortisol recorded in
these dogs after e-collar training, may be due to the e-collar
stimulation, and/or the arousal resulting from exposure to prey
stimuli in the form of sheep and/or associated chase behaviour
prior to stimulation. Nonetheless, the elevation is comparable to
those found by Beerda et al [8], and Schalke et al [9] when dogs
were exposed to e-collar stimulation without exposure to a
potential prey species. Taken together, these results are consistent
with exposure to a significant short term stressor in the form of an
aversive and probably painful stimulus during training.
The aim of this second study was to assess the efficacy and
welfare implications of best practice with respect to a behaviour
modification programme including the use of e-collars versus best
practice for the same problem while excluding their use. The
rationale was that if, under these conditions, we could bring
scientific evidence to the discussion of the costs and benefits of
these devices in society. In contrast to the field observations of the
preliminary study, in this experimental study the trainers using ecollars were observed consistently to undertake an assessment of
the dog’s sensitivity to e-collar stimulus. Furthermore, a prewarning cue was paired with exposure to e-stimulus as a
conditional stimulus with the aim of allowing dog’s to learn to
avoid the e-stimulus. Although this ‘‘idealised’’ use of e-collars may
Discussion
In the preliminary study, only 1 dog trained for improved recall
experienced an approach that was similar to that advocated by
collar manufacturers in the UK [16], where the dog’s sensitivity to
e-collar stimulus was assessed prior to training, and where, during
training, this level of stimulation was associated with a pre-warning
cue or conditioning stimulus. Under these conditions, the trainer
(and dog) had the potential to gain greater control over the
situation, since higher order conditioning can be used to build an
association between the conditioned stimulus (pre-warning cue)
and a verbal command to interrupt ongoing behaviour. Although
the application of stimulus was discernable in this dog, its response
was mild in comparison to the other dogs observed in the
preliminary study.
In contrast, trainers aimed to develop an association between
the electric stimulus alone and proximity to sheep in the 8 other
cases. The development of an aversion response in this way has
also been studied in hunting dogs exposed to stuffed or frozen kiwi
or kiwi feathers [15], where dogs showed long term aversion to
these models (though the study does not present evidence of
efficacy with live kiwis). Furthermore, whilst the authors considered the welfare implications of the aversion based training, they
did not record the response of these dogs to the electrical stimulus
or other measures of the welfare impact on the dog of this
9
Figure 6. Percentage of owners in each response category who reported they were confident of continuing to use the training
methods.
represent the way some dogs are trained, it does not represent the
methods used for all dogs, as evidenced by our preliminary study.
Trainers of Groups A and B used more commands than those in
Group C and encouraged sitting and walking rather than standing.
Dogs in Groups A and B also spent less time sniffing and engaging
in environmental interactions during training. There was also
some evidence (Table S4 in File S2) that dogs in Group B, and
particularly Group A spent more time with a lower tail carriage
than those in Group C, as well as performing more sudden
movements away from the trainer. These results are most
parsimoniously explained by differences in training approach
since it is unclear how these differences could be consistently
associated with the geographical differences between the two
training sites or the time of year of data collection. Lower tail
carriage is often associated with stress [20], and sniffing might be a
displacement behaviour associated with anxiety [10], or may be
associated with the use of food rewards by the trainers in Group C,
or their willingness to allow dogs to engage in more environmental
interactions during training. These trainer based differences would
be worth further investigation, to examine if they are simply
individual differences, or reflect a more general difference in style
associated with training philosophy, since trainers of Groups A
and B were recommended by ECMA, and the trainers of Group C
were assessed members of the APDT, UK. However, no
conclusions should be drawn at this time given that only 4 trainers
were observed out of a much larger population who may vary
considerably in their interpretation and application of different
training approaches
When considering the welfare implications of the inclusion of
the e-collar in training, there were significant differences between
Groups A and C. Specifically, dogs in Group A were more
frequently described as tense and yawned more. Yawning has been
identified as a behavioural sign of conflict or mild stress in a
number of studies (e.g. 8, [35]). Other marginal differences
support the inference that some dogs in Group A were
experiencing welfare compromises during training including the
incidence of panting and yelping. Closer inspection of the data
revealed that the higher levels of yelping and panting in Group A
appeared to arise from a small number of dogs. Yelping may be
interpreted as a response to pain and was reported as such in
Schilder and van der Borg’s study [10] and the preliminary study
presented above, where dogs were exposed to higher intensity ecollar stimuli. However most dogs in Group A yelped at a much
lower rate than reported in the above studies, equivalent to
roughly half a yelp per fifteen minute training session, during
which time dogs could have received several e-stimuli per session.
In Group A, the highest frequencies of vocalisations were
associated with the highest settings used on each of the designs
of collar.
Panting is normally associated with thermo-regulation in dogs,
but appeared to be rarer in the dogs trained in the warmer spring
collection period. Panting has also been associated with acute
stress in dogs [35] and again there was some evidence to suggest
that a sub-population in Group A engaged in most panting during
training. These were no clear associations between this behaviour
and activity level or collar setting, so it is not possible in the current
sample to establish if these dogs were panting as a consequence of
the training programme. Finally there was some evidence of more
whining in Group C dogs. This vocalisation has been associated
with social solicitation [36], attention seeking and/or food begging
behaviour [37] in dogs.
There was no significant difference between the three Groups in
cortisol levels measured in the medium (urinary) term. However
dogs from Group C consistently showed elevated salivary cortisol
10
practice as advocated by collar manufacturers mediates the
behavioural and physiological indicators of poor welfare detected
in the preliminary study, there are still behavioural differences that
are consistent with a more negative experience for dogs trained
with e-collars, although there was no evidence of physiological
disturbance. E-collar training did not result in a substantially
superior response to training in comparison to similarly experienced trainers who do not use e-collars to improve recall and
control chasing behaviour. Accordingly, it seems that the routine
use of e-collars even in accordance with best practice (as suggested
by collar manufacturers) presents a risk to the well-being of pet
dogs. The scale of this risk would be expected to be increased
when practice falls outside of this ideal.
compared with dogs in Group B, with Group A dogs at an
intermediate level but closer to measures of Group B. These
differences were found in both the pre-training and post-training
samples which suggest that the findings do not relate to the use of
e-collars in training protocol. Whilst elevated cortisol can be
interpreted as evidence of distress in response to environmental
challenges, this is not a uni-valent state, as high arousal associated
with positive emotional states can also elevate cortisol as well as
there being associations with the level of physical activity [23]. It is
therefore important to evaluate differences in cortisol in light of
other measures of environmental response such as behaviour. In
the preliminary study, the elevated cortisol found post training in
the preliminary study is consistent with the negative behavioural
responses observed and an interpretation of pain or aversion
during training [8,10], (though as discussed we cannot without
potentially unethical controls rule out the potential of enhanced
arousal related to exercise and exposure to sheep alone). In the
second study, it is harder to explain the differences in cortisol as
the behavioural measures were consistent with a negative (albeit
less severe) response to stimuli experienced by treatment Group A.
Furthermore there was no evidence of differences in cortisol levels
between pre-training and post-training samples for any Group.
Overall the physiological data from the main study suggest two
things: firstly that once the dogs entered training, none of the
treatments resulted in large increases in cortisol secretion and by
inference arousal or stress; and secondly the differences in salivary
cortisol between treatment Groups appear to represent some
underlying difference in arousal, perhaps related to time of year,
rather than a difference in arousal due to the training
programmes.
A common claim by advocates of the use of e-collars is that they
are the most effective way to reliably reduce some potentially
dangerous behavioural problems, in particular failure to recall or
worrying other animals including livestock and other dogs when
off lead. Indeed off lead problems have been found to be the most
common reasons for using manually operated devices in the UK
[13,14]. For this reason we controlled for reason for referral
(behavioural problem) and owner assessment of severity in
allocating dogs to Groups, and we conducted follow up
questionnaires to assess owner’s satisfaction with the training
programme and improvements in dog’s referred behaviour. The
treatment Group and two control Groups were well balanced in
terms of reason for referral, with no significant difference between
Groups in reason for referral or owner assessment of severity.
Owners were generally satisfied with the advice they received from
trainers, and on the whole saw improvements in both the referred
problem and their dog’s general behaviour. Whilst there is the
potential for bias in the owners reporting of behaviour, there is no
reason to anticipate that this would differ between the three
Groups and findings such as these are entirely consistent with
owners having the opportunity to work closely with experienced
professional trainers over several training sessions. Apart from
their being some evidence that Group C owners were more
confident of applying the approaches they had been shown, there
were no differences in owner satisfaction between the training
programmes, or in dog’s improvement in behaviour. This suggests
that the use of e-collars is no more effective than the use of mainly
reward based training to improve off lead obedience.
Supporting Information
Table S1, Ethogram of behavioural categories sampled
by fixed interval scan sampling. Table S2, Ethogram of
behavioural categories counted by continuous behavioural sampling.
(DOC)
File S1
File S2 Table S3, Treatment Groups in Main Study. These
include the numbers of dogs belonging to UK Kennel Club breed
types, gender, age, reasons for referral and owner’s assessment of
severity of referred behaviour. Table S4, Mean (SE) percentage of
scans in posture/activity, panting, behavioural state, tail movement and position. F-statistic and p value from one way ANOVA.
Group differences identified by post-hoc Tukey t-test; a and b
indicate that there are significant differences between groups.
Where data did not conform to requirements of parametric
analysis, a Kruskall-Wallis test was applied followed by MannWhitney test to identify group differences. These measures are
marked with an asterisk*. To correct for Type I errors due to
multiple comparisons, the False Discovery Rate control (Benjamini
& Hochberg 1995, 2000) was applied. Variables in bold showed
significant effects based on this adjusted criteria. To correct for
Type I errors due to multiple comparisons, the False Discovery
Rate control (Benjamini & Hochberg 1995, 2000) was applied. To
take into account Type II errors, power tests were applied to the
sampled data. Variables in italics did not meet the False Discovery
Rate criteria but application of power tests, suggest that if the
pattern of group variation had been found in a sample size
approximately twice that of this study (n = 120), then the data
would also have met this criteria. Table S5, Frequencies of
activities presented as mean counts (SE) events per training session.
F-statistic and p value from one way ANOVA. Group differences
identified by post-hoc Tukey t-test; a and b indicate that there are
significant differences between groups. Where data did not
conform to requirements of parametric analysis, a Kruskall-Wallis
test was applied followed by Mann-Whitney test to identify group
differences. These measures are marked with an asterisk*. To
correct for Type I errors due to multiple comparisons, the False
Discovery Rate control (Benjamini & Hochberg 1995, 2000) was
applied. Variables in bold showed significant effects based on this
adjusted criteria. To take into account Type II errors, power tests
were applied to the sampled data. Variables in italics did not meet
the False Discovery Rate criteria but application of power tests,
suggest that if the pattern of group variation had been found in a
sample size approximately twice that of this study (n = 120), then
the data would also have met this criteria.
(DOC)
Conclusions
Our results indicate that the immediate effects of training with
an e-collar give rise to behavioural signs of distress in pet dogs,
particularly when used at high settings. Furthermore, whilst best
11
Acknowledgments
Author Contributions
The project team would also like to thank colleagues from University of
Bristol, School of Veterinary Medicine (Rachel Casey, Emily Blackwall,
Gill, Jane Murray, Mike Mendl, Oliver Burman), Food and Environment
Research Agency (Katja van Driel, Fiona Bellamy), Silsoe Livestock
Systems (Jeff Lines) for their help in development of methods which
informed design and interpretation of this project.
Conceived and designed the experiments: JC NC JH HW DM. Performed
the experiments: JC NC JH HW. Analyzed the data: JC. Wrote the paper:
JC HW DM.
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Published in final edited form as:
Appl Anim Behav Sci. 2012 November ; 141(3-4): . doi:10.1016/j.applanim.2012.08.007.
Salivary cortisol concentrations and behavior in a population of
healthy dogs hospitalized for elective procedures
Jessica P. Hekmana,1, Alicia Z. Karasa, and Nancy A. Dreschelb
aDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University,
North Grafton, MA, USA 01536
bDepartment
of Animal Science, Pennsylvania State University, University Park, PA, USA 16802
Abstract
Identification of severe stress in hospitalized veterinary patients may improve treatment outcomes
and welfare. To assess stress levels, in Study 1, we collected salivary cortisol samples and
behavioral parameters in 28 healthy dogs hospitalized prior to elective procedures. Dogs were
categorized into two groups; low cortisol (LC) and high cortisol (HC), based on the distribution of
cortisol concentrations (< or ≥ 0.6 µg/dL). We constructed a stress research tool (SRT) based on
three behaviors, (head resting, panting and lip licking) that were most strongly related to salivary
cortisol concentrations. In Study 2, we collected salivary cortisol samples from 39 additional dogs,
evaluated behavior/cortisol relationships, assigned each dog to an LC or HC group, and tested the
ability of the SRT to predict salivary cortisol. Median (interquartile range) salivary cortisol
concentrations were not different between Study 1 (0.43 µg/dL, 0.33 to 1.00 µg/dL) and Study 2
dogs (0.41 µg/dL, 0.28 to 0.52 µg/dL). The median salivary cortisol concentration was
significantly lower (P ≤ 0.001) in LC versus HC dogs in each study; (Study 1 LC: 0.38 µg/dL,
(0.19 to 0.44), n = 19, HC: 2.0 µg/dL, (1.0 to 2.8), n = 9, and Study 2 LC: 0.35 µg/dL, (0.25 to
0.48), n = 28, HC: 0.89 µg/dL, (0.66 to 1.4), n = 7). In Study 1, three behaviors were found to be
associated with salivary cortisol concentrations. Duration of head resting was negatively
associated with salivary cortisol (ρ = −0.60, P = 0.001), panting and lip licking were positively
associated with cortisol (ρ = 0.39, P = 0.04, and 0.30, P = 0.05, respectively), Head resting (p =
0.001) and panting (p = 0.003) were also associated with LC/HC group assignment. In Study 2
dogs, the three behaviors correlated (but not significantly) with salivary cortisol concentration; of
the three, only head resting was significantly associated with LC/HC group assignment (P = 0.03).
The SRT derived from Study 1 was effective at prediction of salivary cortisol concentrations when
applied to 20 min but not 2 min of behavioral data from Study 2. Additionally, we note that
dexmedetomidine and butorphanol sedation more than 6 h prior to measurement was found to be
significantly (P = 0.05) associated with lower salivary cortisol concentrations when compared to
unsedated dogs. Our work offers support for eventual construction of a rating tool that utilizes the
presence or absence of specific behaviors to identify higher salivary cortisol concentrations in
dogs subjected to hospitalization, which may be tied to greater psychogenic stress levels. Future
work to investigate the effects of stress on dogs and its mitigation in clinical situations may be
© 2012 Elsevier B.V. All rights reserved.
Corresponding author: [email protected], Cummings School of Veterinary Medicine, 200 Westboro Road, North Grafton, MA,
01536, ph 01-508 -887-4638, fax 01-508- 839-7922.
1Current address: Maddie’s Shelter Medicine Program, College of Veterinary Medicine, 2015 SW 16th Avenue, Gainesville, FL
32610, USA
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Hekman et al.
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approached by studying a combination o f parameters, and should consider the possible beneficial
effects of sedatives.
Keywords
Salivary cortisol; hospitalization; stress; dogs; dexmedetomidine; butorphanol
1. Introduction
Evidence from laboratory, clinical, and epidemiological trials suggests that acute and
chronic psychogenic stress has health implications for animals and people, including
susceptibility to infection (Glaser and Kiecolt-Glaser, 2005; Kemeny and Schedlowski,
2007) and slowed wound healing (Detillion et al., 2004; Vitalo et al., 2009). The signs and
effects of stress in populations of dogs in various environments have been investigated:
shelter, (Bergamasco et al., 2010 ; Hennessy et al., 2001;) working, (Haverbeke et al., 2008)
laboratory, (Spangenberg et al., 2006) and in a veterinary hospital for medical care or
surgery (hospitalized dogs) (Kim et al., 2010; Siracusa et al., 2008; Väisänen et al., 2005).
Hospitalized dogs may experience acute and/or chronic psychogenic stress, as a result of
exposure to a novel environment and invasive procedures, particularly in the absence of
familiar caretakers.
Excessive or prolonged stress, especially when associated with negative health outcomes, is
known as distress (Committee on Recognition and Alleviation of Distress in Laboratory
Animals, National Research Council, 2008). Methods of evaluating stress levels in canine
and human patients include the measurement of elements of the hypothalamic-pituitaryadrenal (HPA) axis or sympatho-medullary-adrenal (SAM) axis; most commonly, cortisol
concentrations are examined (Castillo et al., 2009; Kobelt et al., 2003). Salivary cortisol
concentrations have been shown to closely parallel plasma cortisol concentrations, and can
be collected less invasively (Beerda et al., 1996; Hellhammer et al., 2009). At present, the
salivary cortisol concentrations which mark distress or undesirable outcomes in dogs are not
known. Behavioral correlates to physiologic stress measurements could provide a practical
alternative parameter to use for identification of stress. Clinical and research tools have been
developed and validated to assess a number of states in dogs: pain (Brown et al., 2007;
Hudson et al., 2004; Morton et al., 2005) quality of life, (Mullan and Main, 2007; WisemanOrr et al., 2004) and temperament (Hsu and Serpell, 2003). An ability to quantify stress is
central to the investigation of the degree to which distress affects health and well-being, as
well as to the development and assessment of strategies to reduce distress. Thus the
development of specialized tools for evaluation of stress in hospitalized dogs would be
useful for the clinical management setting. Newly developed tools should undergo a
rigorous validation process before being recommended for clinical or research use.
Researchers have attempted to relate behavior to HPA axis variables in a number of settings,
but we were aware of no study looking at the predictive relationship of behavior to salivary
cortisol concentration in dogs in a veterinary hospital setting. We therefore attempted to
characterize stress levels and behavioral signs that might be associated with high stress in a
population of healthy hospitalized dogs, to develop a stress research tool (SRT) and to
validate the behavior/cortisol relationships and SRT in a second population of dogs.
Hekman et al.
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2. Materials and methods
2.1 Subjects
All animal procedures were approved by the institutional Clinical Studies Review
Committee. Owner consent was obtained prior to any procedure. Dogs were recruited for all
studies described here from a population of healthy canine patients admitted for an elective
procedure to the Foster Hospital for Small Animals (FHSA) at the Tufts Cummings School
of Veterinary Medicine, North Grafton, MA, USA. The following criteria for enrollment
were used: at least 7 months of age; large or medium breed; not systemically ill; no
neurologic abnormalities; ambulatory; sighted; not aggressive to humans; no recent history
of corticosteroid administration. The enrollment criteria permitted inclusion of dogs that had
been sedated with dexmedetomidine and butorphanol earlier in the day for noninvasive
procedures such as radiographs, but all dogs were reversed with atipamezole and allowed at
least 6 h to recover from sedation prior to enrollment. Medium to large size dogs were
chosen because large runs were used to house dogs for the study and to ensure collection of
an adequate volume of saliva. The estrous cycle status of intact female dogs was not
recorded.
For Study 1, a total of 42 dogs were enrolled. Eleven dogs were excluded from analysis due
to problems with sample collection (insufficient saliva volume, blood contamination,
suspicion of aggression, researcher error, and interruption of video recording). One dog was
excluded from analysis due to subsequent diagnosis with hypoadrenocorticism. Data from
two dogs were excluded from analysis due to salivary cortisol concentrations above two
deviations from the sample mean. Therefore, data from 28 dogs were included in the
subsequent analyses. Subject age ranged from 0.8 to 11.4 years (median 2.5), and body
weight ranged from 17.2 to 67.6 kg (median 34.9 kg). Thirteen different breeds were
represented, predominantly retrievers and retriever mixes (See Table 1). Six subjects were
awaiting elective spaying and neutering, 17 were hospitalized for orthopedic procedures
(cruciate ligament repair, arthroscopy, tibial tuberosity advancement, corrective ostectomy,
and triple pelvic osteotomy), and seven were to undergo soft tissue surgery (mass and cyst
removal, hernia repair, seroma drainage and arytenoid lateralization). A single subject was
sedated with dexmedetomidine and butorphanol and reversed with atipamezole for presurgical radiographs, at least 6 h before video recording.
For Study 2, a total of 39 dogs were enrolled. Four dogs were excluded from analysis due to
insufficient saliva volume collected or sample contamination with blood. Therefore, data
from 35 dogs were analyzed. Subject age ranged from 0.6 to 11.2 years, median 3.3 years,
and body weights ranged from 15.7 kg to 102.0 kg (median 35.2 kg). Breed distribution was
similar to that of Study 1 (See Table 2). Seven subjects were awaiting elective spaying and
neutering, 33 were hospitalized for orthopedic procedures (cruciate ligament repair,
arthroscopy, tibial tuberosity advancement, corrective ostectomy, total hip replacement, and
triple pelvic osteotomy), three were to undergo soft tissue surgery (mass or hematoma
removal), and one was scheduled for a radiographic recheck of spinal meningioma. A subset
of subjects (n = 15) were sedated for radiographs with dexmedetomidine and butorphanol,
and reversed with atipamezole, before enrollment. All dogs were allowed a minimum of 6 h
to recover from sedation prior to video recording.
2.2 Video recording and ethogram logging
Ethogram logging was used to record all behaviors which might be significant as markers of
stress in Study 1 and Study 2. All measurements for both studies took place between 18:00 h
and 21:00 h, to avoid confounding by diurnal variation, over a period of 10 months. Dogs
were placed in a 1.2 m × 2.4 m run in a hospital ward with a padded blanket. Ambient
Hekman et al.
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temperatures in the ward were controlled between 20°C – 22°C. A video recording of
behaviors was collected for each dog for a minimum of 25 min with a standard black and
white video surveillance camera (Lorex Technology Inc., Markham, Ontario, Canada), and a
DVD recorder (Sony Corporation, Tokyo, Japan) in real time at 24 frames/s. Video data
were subsequently analyzed by a single observer (JPH) in a random order with respect to
collection date, using the first 20 min of video recording. Behaviors were logged using a
purpose-developed application written in the PHP scripting language (The PHP Group,
www.php.net).
Six behaviors were logged with units of duration (percentage of total time), as described in
Table 3. Six others (“barks,” “whines,” “lip licks,” “yawns,” “pawing at or manipulating the
door,” and “tail wagging”) were logged as the number of events per 20 min.
2.3 Salivary cortisol collection and measurement
Saliva samples were collected and salivary cortisol concentrations measured from all dogs in
Study 1 and Study 2. At the end of each video recording period, saliva was collected from
each dog by means of two to four Sorbettes (Salimetrics, State College, PA, USA) placed in
the animal’s mouth for 2 to 3 min. Saliva collection was completed in less than 4 min to
prevent the stress of restraint from elevating salivary cortisol concentrations (Kobelt et al.,
2003). Sorbettes we re centrifuged (3250 rpm, 15 min, 4° C), and saliva was pipetted into
cryovials and stored at −80°C. Saliva samples were assayed for cortisol concentrations using
a high-sensitivity salivary cortisol enzyme immunoassay kit from Salimetrics (State College,
PA, USA). Samples were assayed in triplicate, using 25 µL of sample per well. Samples
with visible blood contamination were discarded so that cortisol from plasma would not
artifactually elevate the measured salivary cortisol level. Samples with insufficient volume
were diluted by 50% with assay diluent. The kit’s lower limit of sensitivity is 0.003 µg/dL.
Average intra- and inter-assay coefficients of variation were less than 15% and 10%,
respectively.
2.4 Division into HC and LC groups and SRT construction
When dogs in Study 1 were ranked by salivary cortisol concentration and the data plotted,
an inflection point could be seen, with approximately one-third of the dogs having higher
cortisol levels than the others. Based on this inflection point, dogs were designated as LC
(for lower salivary cortisols) or as HC (for highest salivary cortisols) for subsequent
analysis. The unequal grouping was chosen in an attempt to develop a method capable of
identification of the subgroup of dogs putatively experiencing the highest level of stress.
Associations were sought using correlation between behavior frequency or duration and
salivary cortisol concentration, occurrence of behaviors in dogs assigned to the HC group
versus dogs in the LC group, and the odds of being in either group, (evaluated for every
possible behavior frequency) to determine the likelihood of a dog falling into the HC or LC
group based on that behavioral “break point”. A behavior-based stress research tool (SRT)
was constructed based on behaviors with the strongest associations to salivary cortisol
concentrations in the discovery group. The tool employed continuous numeric scoring, with
a larger positive score implying greater stress levels (Table 4). This tool was designed to be
applied over 1 min periods and averaged over multiple min. Scores may range from −12 to a
theoretically unbounded positive number.
2.5 Study 2: Validation of the ability of behavior to predict salivary cortisol
The purpose of Study 2 was: to evaluate the previously identified relationships of behaviors
to salivary cortisol concentrations; to test the construct validity of the SRT (its ability to
measure a hypothetical construct such as distress (Streiner and Norman, 2008)) on this new
group of dogs by comparison of scores with salivary cortisol concentration; and to determine
Hekman et al.
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whether the SRT is more effective when derived from behavioral data collected over a
longer (20 min) versus a shorter (2 min) period of time. A validation population of dogs
distinct from those enrolled in Study 1 was enrolled for Study 2. Comparisons of salivary
cortisol to behavior frequency were made as in Study 1. We subsequently compared the SRT
scores of the HC group vs the SRT scores of the LC group, and compared the cortisol
concentrations of dogs with positive SRT scores to the cortisol concentrations of dogs with
negative SRT scores. Lastly, to compare the effectiveness of different observation durations,
the SRT was applied to video segments of dogs observed for lengths of 2 min and 20 min.
The 2 min segment was always taken from min 8 and 9 after the start of the video recording,
and the 20 min segment was taken from the first 20 min after the start of the video
recording. Each dog was assigned two numeric scores: one based on the SRT using 2 min of
video observation (SRT2 score), and the other based on the same tool using 20 min of video
observation (SRT20 score).
2.6 Statistical analysis
The minimum sample size necessary for a sufficiently powered study was calculated using
mean and SD of baseline salivary cortisol values in dogs from Kobelt et al., 2003.
Correlations between behaviors and salivary cortisol level were examined by means of
Spearman’s correlation. Further exploration of the relationships of behaviors to salivary
cortisol levels was sought by inspection of scatter plots, and relationships to “low cortisol”
(LC) and “high cortisol” (HC) groups. Odds ratio analyses were used to calculate whether
the frequency of displaying a behavior versus LC or HC categorization was useful for
inclusion in the SRT. Because of the possibility of encountering Type I errors after a large
number of statistical calculations, behaviors that did not appear significant after multiple
testing methods were discarded. As data values were not normally distributed, differences
between frequencies of behaviors, salivary cortisol concentrations, and SRT scores were
tested using non-parametric Mann-Whitney U tests. (Gnumeric Spreadsheet 1.10.7, SPSS
16.0 and 19.0) All data are presented as median (interquartile range), unless otherwise noted.
Some actual ranges and mean values are given when these are of use in interpreting data.
3. Results
3.1 Subject characteristic comparisons between populations
Breed distributions between Study 1 and Study 2 populations were comparable, with the
most common breed being Labrador retriever. Distribution of dogs by sex indicated that
Study1 and Study2 frequencies, respectively, were: castrated male, 43% and 51%; intact
male, 18% and 11%; spayed female, 25% and 34%; and intact female, 14% and 3%. Thus
sex distribution was not equivalent between groups because of the higher percentages of
intact male and female dogs in Study 1. Age distribution of dogs between the two studies
were similar (Study 1: 9 – 137 m, median 30 m; Study 2: 7–134 m, median 39 m), as was
weight distribution (Study 1: 17.2 – 67.6 kg, median 35.8 kg; Study 2: 15.7 – 102 kg,
median 37.4 kg).
3.1.1 Study 1 Salivary cortisol values—Fig. 1 shows the salivary cortisol
concentrations in the 28 dogs which were used for analysis. Median salivary cortisol was
0.43 µg/dL (0.33 to 1.00 µg/dL); however, we note that the mean value was 0.87 µg/dL. An
inflection point in Fig. 1 appears between 0.5–1.0 µg/dL. Therefore, we assigned a salivary
cortisol concentration “break point” value of 0.6 µg/dL, and dogs were assigned to LC
(salivary cortisol < 0.6) and HC (salivary cortisol ≥ 0.6 g/dl) groups. Median (interquartile
range) values for LC dogs were 0.38 µg/dL (0.19 to 0.44), n = 19, and for HC dogs were 2.0
µg/dL (1.0 to 2.8), n = 9 (P≤ 0.001). Thus 32.1% of dogs had salivary cortisol concentrations
≥ 0.6 µg/dL.
Hekman et al.
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3.1.2 Relationships between behavior, salivary cortisol and LC/HC group in
Study 1 dogs—Of the behaviors scored, those with the strongest correlations with salivary
cortisol concentration were used for subsequent analysis. Initially, three behaviors were
identified as useful markers of dogs in the LC or HC group. These were “head resting,”
“panting,” and “lip licking”. “Head resting” had a negative correlation with salivary cortisol
(ρ = −0.60, P = 0.001). Only one of nine HC dogs (11%) ever rested its head on the ground
or its paws, and the median time spent with head resting was 0%, and ranged from 0 to 0.8%
(interquartile range 0 to 0%). Fifteen of 19 LC dogs (79%) rested their heads and four did
not, with a median duration of 15.5% of the observation time spent resting (range 0 to
99.2%, interquartile range 0.42 to 60.2%, Mann-Whitney U = 22.5, P = 0.001). “Panting”
had a positive correlation with salivary cortisol (ρ = 0.39, P = 0.04). All of the HC dogs
(100%) were observed panting for some of the time, and these dogs panted for a median of
79.8% of the observation time, (range 49 to 95%, interquartile range 62.8 to 90.5%). Twelve
LC dogs (63%) panted, for a median of 38.5% of the observation time (range 0 to 92%,
interquartile range 0 to 57.1%, Mann-Whitney U = 26.0, P = 0.003). “Lip licking” had a
positive correlation with salivary cortisol (ρ = 0.30, P = 0.05). Eight HC dogs (89%)
exhibited lip licking and in the 20 min of observation, there was a median of 24 licks, (range
0 to 47, interquartile range 13 to 42 times). Fourteen LC dogs (74%) exhibited lip-licking,
and there were a median of eight licks (range 0 to 51, interquartile range 0.5 to 18.5 times,
Mann-Whitney U = 49.0, P = 0.08).
3.2 Study 2
3.2.1 Salivary cortisol values—The salivary cortisol concentrations from the 35 Study 2
dogs showed a similar pattern to those in Study 1 (Fig. 2). Note that some points represent
multiple dogs with identical salivary cortisol concentration. Median salivary cortisol
concentration was 0.41 µg/dL (0.28 to 0.52 µg/dL), and we additionally note that the mean
value was 0.48 µg/dL. The break point between the two groups was set at the same value as
in Study 1 (0.6 µg/dL) to allow meaningful comparisons between the two studies. The
median salivary cortisol concentration in Study 2 was 0.35 µg/dL (0.25 to 0.48), n = 28 for
LC dogs, and 0.89 µg/dL (0.66 to 1.4), n = 7 for HC dogs (P<0.001). Thus 20% of Study 2
dogs had salivary cortisol concentrations ≥ 0.6 µg/dL.
3.2.2 Relationships between behavior, salivary cortisol and LC/HC group in
Study 2 dogs—When behaviors were examined for correlation with salivary cortisol, the
three with the highest correlations were “lip licking,” “head resting,” and “panting”, but
these trends towards associations did not achieve a level of significance at P ≤ 0.05. “Head
resting” had a negative, but non significant correlation with salivary cortisol (ρ = −0.28, P =
0.105); and was significantly associated with assignment to LC/HC group. Three of the
seven HC dogs (43%) rested their heads on the ground or paws, and the median time spent
with head resting was 0%, and ranged from 0 to 27.5% (interquartile range 0 to 4.38%).
Twenty-one LC dogs (75%) rested their heads and seven did not, with a median duration of
18.54% of observation time spent resting (range 0 to 93.75%, interquartile range 1.88% to
39.38%, Mann-Whitney U = 46.5, P = 0.03). “Panting” had a positive, but non significant
correlation with salivary cortisol (ρ = 0.33, P = 0.056). Six HC dogs (86%) were observed
panting for some of the time, and these dogs panted for a median of 82.08%, of the
observation time (range 0 to 98.75%, interquartile range 50.51% to 89.80%). Twenty-five
LC dogs (89%) panted, and they panted for a median of 35.42% of the observation time
(range 0 to 99.17%, interquartile range 8.75% to 57.57%, Mann-Whitney U = 55, P = 0.08).
“Lip licking” had a positive, but non significant correlation with salivary cortisol (ρ = 0.17,
P = 0.322). Six of the HC dogs (86%) exhibited lip licking and in the 20 min of observation,
there was a median of 22 licks, (range 0 to 50, interquartile range 8.00 to 32.00 times).
Hekman et al.
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Twenty-four LC dogs (86%) exhibited lip-licking, and there were a median of 8.5 licks
(range 0 to 86, interquartile range 3.75 to 27.5 times, Mann-Whitney U = 82.5, P = 0.54).
3.2.3 Validation of stress research tool over 2 min (SRT2) in Study 2 dogs—
The median salivary cortisol concentration of dogs with an SRT2 score < 0 (median 0.44 µg/
dL, (0.35 to 0.50 µg/dL), n = 9) was not significantly different (Mann-Whitney U = 115, P =
0.94) to the median salivary cortisol concentration of dogs with an SRT2 score ≥ 0 (median
0.40 µg/dL, (0.27 to 0.56 µg/dL), n = 26). Similarly, there was no significant difference
(Mann-Whitney U = 74.0, P = 0.33) between the SRT2 scores of the LC group (median 4.0,
(−1.0 to 10.25), n = 28) and the SRT2 scores of the HC group (median 9.5, (4.25 to 11), n =
7).
3.2.5 Sedation—Although the median salivary cortisol concentrations of dogs in Study 1
and Study 2 were not significantly different, the mean salivary cortisol level of dogs in
Study 1 was 0.39 µg/dL greater than that of dogs in Study 2. The distribution of sedated and
unsedated dogs differed between Study 1 (sedated n = 1, unsedated n = 27, 3.6% of
population sedated) and Study 2 (sedated n = 14, unsedated n = 21, 40% of population
sedated). As the salivary cortisol concentrations of unsedated dogs in the Study 1 and Study
2 were not significantly different (Mann-Whitney U = 277.0, P = 0.69), the difference in
salivary cortisol concentrations between the two studies was likely attributable to the greater
number of dogs sedated in Study 2. The median salivary cortisol values of sedated dog s
combined from both studies, 0.35 µg/dL, 0.22 to 0.43 µg/dL), n=15, was significantly lower
than the median salivary cortisol concentrations of unsedated dogs from both studies, 0.46
µg/dL, (0.33 to 0.72 µg/dL), n=49, (Mann-Whitney U = 231.5, P 0.05). All of the sedated
dogs fell into the LC group. When we examined correlations of salivary cortisol
concentration with behavior in only unsedated Study 2 dogs, the ρ values improved but
continued be non significant. When we examined correlations of salivary cortisol
concentration with behavior in only the unsedated Study 2 dogs, the ρ values improved, and
the trends regarding head resting and panting remained, but were non-significant, and there
was no significant association with lip licking.
3.2.4 Validation of stress research tool over 20 min (SRT20)—The salivary
cortisol concentration of dogs with an SRT20 score < 0 (median 0.31 µg/dL, (0.25 to 0.44
µg/dL), n = 13) was significantly different (Mann-Whitney U = 86.0, P = 0.05) to that of
dogs with an SRT20 score ≥ 0 (median 0.47 µg/dL, (0.35 to 0.62 µg/dL), n = 22. A
significant difference (Mann-Whitney U = 51.0, P = 0.05) between the SRT20 scores of the
LC group (median 1.63, (1.11 to 4.01), n = 28) and HC group (median 4.41, (3.40 to 5.79), n
= 7) was also was found.
4. Discussion
The goal of this work was to characterize stress levels in healthy dogs hospitalized for
elective procedures, and to attempt to relate spontaneous behavioral manifestations to an
objective marker of stress, salivary cortisol concentration. Because it was not expected that
all dogs would show one common and significant behavior indicative of their stress level,
we attempted to construct and validate a scale or assessment tool that would allow
prediction of salivary cortisol concentration. In these two populations of medium to large
breed dogs exposed to the stimuli of a veterinary hospital ward, analysis of ethograms
showed only modest correlations of certain individual behavioral frequencies or durations
with salivary cortisol concentration. These were “head resting”, “panting” and “lip licking”.
Salivary cortisol concentration measurements showed a pattern where approximately 30%
(Study 1) and 20% (Study 2) of dogs had significantly higher values than the others in the
group. When Study 1 dogs were designated as highest cortisol” or HC, and “lower cortisol”
Hekman et al.
Page 8
or LC according to an inflection point demonstrated in the graph of salivary cortisol
concentration distribution, only “head resting” and “panting” were significantly associated
with HC or LC status. The SRT that was s ubsequently developed was tested in a second
population of dogs. In the Study 2 dogs, the relationship of salivary cortisol concentration to
head resting and panting showed a similar trend as in Study 1. Although none of the specific
behaviors in Study 2 were significantly correlated with salivary cortisol concentration, head
resting remained significantly associated with HC or LC status. In Study 2 as in Study 1, lip
licking was not significantly associated with assignment to LC or HC status. Finally, in
Study 2, a dog’s SRT score (using the SRT that included all three behaviors), was
significantly associated with salivary cortisol concentration and with HC or LC status, when
the behaviors are observed over a 20-min period (SRT20), but not when observed over a
shorter 2-min period (SRT2).
A number of limitations of our work bear discussion. First, there may have been differences
introduced by virtue of the fact that the populations in Study 1 vs. Study 2 varied to some
extent in terms of the breed and sex distributions of dogs. While we attempted to control for
status (healthy), size (medium to large breed), and time of day (evening), few clinical studies
in veterinary populations can be completely standardized with respect to patient
characteristic.
Secondly, we realized that more of the dogs in Study 2 had received sedation earlier in the
day than those in Study 1. At our hospital, the sedative-analgesic combination of
dexmedetomidine and butorphanol is given intravenously to facilitate a procedure such as
radiography which would otherwise not by possible. We pre-specified that this sedation
protocol (as opposed to any longer lasting drug regimen) was acceptable if sedation and the
standard antagonism of the dexmedetomidine component took place at least 6 h prior to
sample collection for our study. While we were generally aware of the potential effect of
sedatives, specifically the alpha-2-agonist class of drug, on HPA axis elements, we elected
to allow this sedation paradigm, because in reports of the effect of alpha-2-agonists on
plasma cortisol in dogs, the difference between treated and untreated individuals who were
exposed to a painful or general anesthetic stimulus appears to wane at 3 to 4 h (Ko et al.,
2000; Kuusela et al., 2003; Väisänen et al., 2002). In retrospect, we noted serendipitously
that dogs who were sedated more than 6 h prior to sample collection had significantly lower
salivary cortisol concentrations than unsedated dogs. The fact that correlations and
associations with salivary cortisol levels were less significantly related in Study 2 may well
be due to the fact that the sample size of non sedated dogs was smaller than in Study 1.
While this may have affected both the relationships of behaviors to salivary cortisol
concentrations and our SRT validation efforts, it does at least open the intriguing possibility
that use of sedation may help dogs cope with hospitalization. While we recommend that
future studies take into account the potential confounding effects of sedation, we also
suggest that it would be useful to study the effects of sedation on hospitalized dog behavior
and stress physiology.
Thirdly, based on the distribution of salivary cortisol concentrations, we divided the subjects
into lower and highest cortisol groups based on the assumption that some dogs were
experiencing more stress than others. The groups represent relative categories and as such
they are not intended to be interpreted as strict divisions between basal cortisol
concentrations and concentrations at which distress is manifest. As there is no possibility of
verbal “stress self-report” in dogs, future studies might attempt to correlate other measures
of the stress response, such as salivary IgA (Kikkawa et al., 2003; Skandakumar et al.,
1995), neutrophil to lymphocyte (N:L) ratios (Beerda et al., 1999), or heart rate variability
(HRV) (Väisänen et al., 2005), with salivary cortisol concentrations and to compare them
with behavioral data.
Hekman et al.
Page 9
While it is important to be reserved in terms of concluding that behavior can indicate stress
level, the fact that a small cluster of individual behaviors, which correlated to some degree
with salivary cortisol concentration or a range of salivary cortisol concentrations, is of
potential interest. Until some gold standard measure of stress or distress is developed,
behavior will remain an important means to evaluate dogs in a given setting. Even allowing
for the potentially mitigating effect of sedation on cortisol concentrations, our values were
substantially greater than those measured in other populations of dogs exposed to stressors.
Salivary cortisol concentrations measured in dogs under “basal” conditions generally are
reported to fall in to the range of 0.02 – 0.3 µg/dL (Bennett and Hayssen, 2010, WengerRiggenback et al., 2010, both in pet dogs measured at home). In studies using the same
immunoassay kit (Salimetrics, State College, PA, USA), the mean salivary cortisol
concentration of dogs accompanied by their owners a veterinary clinic was 0.17 µg/dL,
(Dreschel and Granger, 2009) while the salivary cortisol concentrations of thunderstorm
phobic dogs increased during thunderstorms from a basal mean of 0.1 µg/dL to a stressor
mean of 0.2 µg/dL (Dreschel and Granger, 2005). There are a number of potential
explanations for this discrepancy between our studies and previous work. One is that the
performance of the assay is laboratory specific, in which case any conclusions derived from
cortisol concentrations should be referenced to that laboratory setting only (Briegel et al.,
2009). The second possibility is that our findings were due to a Type I error resulting from
small sample size. Thirdly, breed and sex differences between canine populations may play
a large role. Finally, hospitalization may represent a much greater stressor for dogs than
previously reported types of stressors. Belpedio et al., (2010) found that, using the same
immunoassay kit (Salimetrics), the mean salivary cortisol concentrations in dogs initially
placed in shelters ranged from 0.19– 1.09 µg /dL. Future work might attempt to correlate
measurements of salivary cortisol and behavior in the same individuals during low (resting
at home), intermediate (in the clinic with the owner present), and high (during
hospitalization with the owner absent) conditions of stress. The finding of elevated salivary
cortisol concentrations in dogs in the current study populations remains of unknown
significance.
It should also be emphasized that the use of behaviors to identify highly stressed dogs was
evaluated in the controlled context of our experimental conditions. Both panting and head
resting may occur for reasons other than underlying emotional stress. Panting in dogs clearly
occurs during thermoregulation and during situations of increased oxygen demand, and the
general expectation is that they also pant when they are stressed. Thus, dogs who are panting
may be doing so for purposes of evaporative cooling and oxygen exchange, but if neither of
those conditions is likely, then panting may have significance in detecting emotional state.
Similarly, dogs who are observed resting their heads may be doing so because of weakness,
sedation, or during sleep; alternatively, they may be experiencing a low state of arousal and
stress. We were unable to detect other behaviors that are suggested to be altered in stressed
dogs, such as blink rate, because of limitations with our video technology. Additionally, all
behavioral data was collected by video recording, so dog behavior may be different in the
actual presence of an observer. Future work may elucidate the usefulness of behavior in
different environments.
The SRT itself is only a preliminary construct, and will require further investigation and
modification in order to prove useful in investigations into the health effects of stress and/or
the effectiveness of stress reduction interventions. For clinical purposes, a stress assessment
tool would be valuable for practical detection and management of distressed hospitalized
dogs. However, our SRT is unlikely to be useful in a clinical setting, as it may require as
much as 20 min of detailed observation for effectiveness.
Hekman et al.
Page 10
5. Conclusion
Identification of dogs with moderate to severe stress in veterinary medical settings is
potentially useful in order to study the effects of stress on healthcare outcomes; as well, it
may allow the development of effective methods to ameliorate stress. Our studies indicated
that a proportion of healthy dogs in a hospital setting had significantly higher salivary
cortisol concentrations than the rest of the population studied, and that behaviors,
specifically head resting, panting and lip licking, may prove useful for evaluation of stress
levels in hospitalized dogs. Further, sedation with dexmedetomidine and butorphanol
appears to depress salivary cortisol concentrations in dogs in the short-term and warrants
consideration in future studies.
Acknowledgments
This manuscript represents a portion of a thesis submitted by Jessica Hekman to the Tufts University Cummings
School of Veterinary Medicine Department of Comparative Biomedical Sciences as partial fulfillment of the
requirements for a Master of Science degree.
This project was supported by the National Center for Research Resources and the Office of Research Infrastructure
Programs (ORIP) of the National Institutes of Health through Grant Number T32 RR018267
This publication was also supported by Grant Number UL1 RR025752 from the National Center for Research
Resources. Its contents are solely the responsibility of the authors and do not necessarily represent the official views
of the NCRR.
Supported in part by the National Institute of Health and the U.S. Army.
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Page 13
Fig.1.
Salivary cortisol values ranked in order of increasing concentration, of 28 dogs in Study 1.
Hekman et al.
Page 14
Fig.2.
Salivary cortisol values ranked in order of increasing concentration, of 35 dogs in Study 2.
Hekman et al.
Page 15
Table 1
Breed and sex distribution of dogs in Study 1.
Breed
Number of
dogs
Labrador retriever
Sex of dogs
(CM/M/SF/F)
11
3/4/3/1
Golden retriever
3
2/0/1/0
Labrador mix
3
3/0/0/0
Greater Swiss mountain dog
2
0/0/0/2
Australian cattle dog
1
0/0/0/1
Australian shepherd mix
1
0/0/1/0
Basset hound
1
1/0/0/0
Beagle mix
1
1/0/0/0
German shepherd
1
1/0/0/0
Mastiff
1
0/0/1/0
Newfoundland
1
0/0/1/0
Polish lowland sheepdog
1
1/0/0/0
Springer spaniel
1
0/1/0/0
28
12/5/7/4
Total
CM= castrated male, M= male, SF = spayed female, F = female
Hekman et al.
Page 16
Table 2
Breed and sex distribution of dogs in Study 2.
Breed
Number of
dogs
Sex of dogs
(CM/M/SF/F)
Labrador retriever
9
5/0/3/1
Golden retriever
5
2/1/2/0
Mixed breed
2
2/0/0/0
Labrador retriever mix
2
1/0/1/0
Great Pyrenees
1
1/0/0/0
Bernese mountain dog
1
0/0/1/0
Beagle mix
1
0/0/1/0
Border collie mix
1
1/0/0/0
Cocker spaniel
1
0/0/1/0
Doberman pinscher
1
1/0/0/0
Golden retriever mix
1
1/0/0/0
Great Dane
1
0/1/0/0
German shepherd dog
1
0/0/1/0
German shepherd mix
1
0/1/0/0
Greater Swiss mountain dog
1
1/0/0/0
Mastiff
1
0/1/0/0
Pit bull
1
0/0/1/0
Rottweiler
1
0/0/1/0
Saint Bernard
1
1/0/0/0
Saint Bernard mix
1
1/0/0/0
Shetland sheepdog
1
1/0/0/0
Total
35
18/4/12/1
CM= castrated male, M= male, SF = spayed female, F = female
Hekman et al.
Page 17
Table 3
A list of behavioral states observed for dogs and which were scored as percentage of total observation time.
Behavior
Possible scores
Pant
Indiscernable (cannot tell)
Pant
No pant
Position
Lateral
Half sternal (on one hip)
Full sternal
Sitting
Standing
Walking
Jumping
Changing position
Location in run
Front
Middle
Back
Sniffing
Sniffing (air or object)
Not sniffing
Head
Up
Resting (on paws or ground)
Facing
Front of run
Side of run
Rear of run
Hekman et al.
Page 18
Table 4
The stress research tool (SRT).
Score the dog for each min that it is observed. Average the scores from multiple min.
Initial score: 0
For each time that the dog rested its head on the ground or its paws for at least 5 s, subtract a point. For example, if it rests its head for 13 s,
subtract 2 points.
For each time that the dog panted for at least 5 s, add a point. For example, if it pants for 21 s, add 4 points.
For each time the dog licks its lips, add a point.
Demystifying the Scientific Paper
Jessica Hekman, DVM, MS
APDT Conference 2015, Dallas, TX
Long term goal:
Be comfortable with your
ability to read a scientific
paper thoughtfully.
2
It is possible to learn to read
scientific papers without an advanced science
degree.
3
Stay critical!
4
Tolerate ambiguity!
5
Practice,
practice,
practice!
6
1. Study Design
7
There are no
perfect studies in
the real world.
Image: Reddit (HerpDerpCrabMan)
8
Independent
variable
9
Dependent
variable
Which is independent? Which is dependent?
Spay/neuter status
Cancer diagnosis
Image: wearethecure.org
10
Correlation does not equal causation
11
Spay/neuter status correlates with cancer
diagnosis.
What are other explanations?
Image: wearethecure.org
12
Prospective studies watch to see what will
happen.
Retrospective studies look at records to see
what did happen.
13
Are cancer studies probably mostly prospective
or retrospective?
Consequences of that study design?
14
Blinded study: subject (or
owner) doesn’t know if
they’re getting treatment
or control.
Double blinded study:
researcher doesn’t know
either!
15
How would you blind a study about effects of
spay/neuter?
16
Randomizing which subject goes into which group can
be difficult, but is extremely important.
17
How best to randomize a spay/neuter study?
18
A case study describes just one subject.
19
2. Anatomy of a scientific paper
20
Was the paper published in a “big name” journal?
21
How old is the paper?
Does it use modern methods and information?
22
You can search for papers by date with Google Scholar.
23
Parts of a Scientific Article
Abstract
Materials and Methods
Results
Discussion
All example screenshots from:
Hekman, Jessica P., Alicia Z. Karas, and Nancy A. Dreschel. “Salivary cortisol
concentrations and behavior in a population of healthy dogs hospitalized for elective
procedures.” Applied Animal Behaviour Science 141.3 (2012): 149-157.
The abstract can help you decide whether a paper has
the information you’re looking for.
But don’t depend on its conclusions.
The introduction can provide useful background
about a particular area.
The materials and methods section
provides detailed information about how the
study was designed.
The results section can
seem like an
overwhelming mass of
numbers.
But it contains vital
information.
The discussion section puts everything in context.
Don’t believe all the authors’ conclusions just
because they’re in print!
Review papers can be great sources of lots of
information on a single topic, all in one paper.
Free versions of papers can often be found using
Google scholar’s “all n versions” link.
Twitter users can ask for a copy of a paper using
#icanhazpdf.
You can “rent” a copy of a paper for a short time
for a fee at DeepDyve.com.
3. A tiny bit of statistics
34
Statistics helps us decide if a particular result may
be just due to chance.
Null hypothesis testing is one way to approach this
problem.
The “null” hypothesis is that nothing is going on –
our treatment doesn’t work.
The p value is a number which tells
us how likely a particular result is to
be due just to chance.
p = 0.12
A p value of 0.12 means that if you
ran this same test many times, then
in 12% or more cases, you would
see a difference this big (or larger).
Just by chance.
p = 0.04
We usually say a result is
“significant” if its p value is less than
0.05.
Only 5% of the time will you see
results like this due just to chance.
Statistical significance is not the same as biological
significance.
Biological significance: is the difference I found big
enough to matter in the real world?
With enough subjects, you may get a small
(significant) p value…
…but will you find a biologically significant
result?
What the p value does not tell you
Are these results meaningful in the real world?
Is there a true correlation between our
treatment and our results?
Does our treatment cause any differences in
our results?
Because correlation does not equal causation…
42
The p value is flawed, but still
widely used.
Always look at the actual results,
not just the p values!
We gain confidence in outcomes
through replication.
Be careful not to fall
prey to confirmation
bias.
4. What to do when you don’t
understand a paper
47
Recognize when you’re starting to get
overwhelmed and take a step back.
Look stuff up (on Wikipedia, YouTube…)
Make yourself write
out a detailed
summary with your
conclusions.
Take a class on the subject.
If you don’t read a paper in detail,
remember that you don’t have enough
information about whether or not to accept
its conclusions!
5. Applying what you’ve learned
53
Popular press story
+
The paper it refers to
Read the popular press story first.
What do you expect to find in the paper?
Do you expect yourself to have confirmation
bias?
Read the paper next.
What kind of study design?
Blinded?
Randomized?
What results did they find?
Your conclusions?
Stay critical!
Tolerate ambiguity!
Practice!
Thank you!
[email protected]
@dogzombieblog (Twitter)

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