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Understanding the genetic basis of canine anxiety: Phenotyping dogs for behavioral, neurochemical, and genetic assessment

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IN BRIEF: PRACTICE AND PROCESS
Understanding the genetic basis of canine anxiety:
phenotyping dogs for behavioral, neurochemical, and
genetic assessment
Karen L. Overall, MA, VMD, PhD,
a
Steven P. Hamilton, MD, PhD,
b
Melanie Lee Chang, PhD
b
a
From the Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania; and the
b
Department of Psychiatry, University of California, San Francisco, California.
Introduction: the Canine Behavioral Genetics
Project (CBGP)
Behavioral problems account for the death, relinquishment,
or the end of breeding careers of more dogs than does any
other set of problems (Miller et al., 1996; Patronek et al.,
1996; Salman et al., 1998, 2000; Scarlett et al., 1999; Shore
et al, 2003; Mondelli et al., 2004; Shore, 2005). Whereas
many behavioral complaints involve management-related
issues or dog-human temperament mismatches, the behav-
ioral concerns that are most interesting to scientists and
breeders alike are those with familial patterns.
A number of conditions have been identified as run-
ning in family lines of a number of breeds including, but
not restricted to, generalized anxiety/fear, noise phobia,
impulse/control aggression, conspecific aggression, pred-
atory aggression, and obsessive-compulsive disorder
(Overall, 1994; Overall and Dunham, 2002; Overall,
2005). Most of these conditions appear sometime be-
tween one and two years of age, the social maturity
period, during which neural systems are undergoing ex-
tensive developmental changes. The potential benefit of
genetic counseling is clear, and the potential to make
dogs “safer” and happier is substantial. Understanding
the genetic bases of behavioral problems will lead to
more humane treatment of dogs, fewer public health
risks, an improved public perception of dogs as pets, and
a considerable lessening in the recycled pet problem.
Additionally, elucidation of the biological systems un-
derlying pathological behavior will heighten our general
understanding of the underlying molecular biology of
behavior, allowing the dog to contribute to this rapidly
evolving field.
Over 50 breeds across all seven AKC groups have family
lines in which “fear/shyness/nervousness/panic/anxiety” is a
major breeder-reported concern (Overall, unpublished).
Within these breeds, this “trait” often follows familial lines,
suggesting a heritable basis. This pattern has been noted for
many physical conditions in dogs (Sutter et al., 2004; Lark
et al., 2006), but little emphasis has been placed on behav-
ioral conditions because of the difficulty in defining a clear
phenotype. Although recognition of other genetically medi-
ated conditions is often straightforward, based on easily
observable clinical phenomena that are defined by consen-
sus (e.g., cancer, retinopathies, narcolepsy), assignment of
behavioral phenotypes can be open to misclassification or
misinterpretation (Overall, 2005; Overall and Burghardt,
2006).
The broad goal of the CBGP is to explore the genetic
background of anxiety-related behavioral problems in dogs.
To do so, we must: (1) solicit the participation of owners of
candidate dogs possibly affected by anxiety-related behav-
ioral problems; (2) identify affected and unaffected dogs,
Address reprint requests and correspondence: Karen L. Overall, Center
for Neurobiology and Behavior, Psychiatry Dept Translational Research
Laboratory School of Medicine, University of Pennsylvania, 125 South
30th Street, Philadelphia, PA 19104.
E-mail: overall@mail.med.upenn.edu
1558-7878/$ -see front matter © 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.jveb.2006.09.004
Journal of Veterinary Behavior (2006) 1, 124-141
using the necessary and specific diagnostic criteria to make
a diagnosis of the condition; (3) confirm the presence of the
relevant diagnosis in these dogs and if possible in their
family lines, using reliable, repeatable, and validated behav-
ioral measures involving questionnaires and videos; and (4)
obtain DNA samples for genetic linkage and association
analyses, along with the relevant pedigrees. In this article,
we discuss the distinction between diagnosis and pheno-
type, and we describe our protocol for assessing behavioral
phenotypes in dogs, addressing the second and third aspects
of our project just discussed.
Diagnosis vs. phenotype
The questions we are most commonly asked are: (1) “What
behaviors are you interested in?” and (2) “How do you
phenotype canine behavior?” Both of these questions are
important and more complex than they appear, and each is
related to the other and to the methodology used in the
study.
In biomedically oriented genetic investigations, pheno-
types are often defined by the diagnoses under study. Thus,
phenotypes such as hip dysplasia, diabetes, hypothyroidism,
or noise phobia are defined by consensus clinical criteria.
The use of such consensus criteria means that not every
subject who has received a diagnosis of the condition is
necessarily considered a candidate for genetic investigation;
only those meeting the consensus criteria— often more re-
strictive than broad, clinical, diagnostic criteria—are con-
sidered on the basis of phenotype for further genotypic
examination. If the diagnostic criteria are sufficiently clear
and well defined, those meeting them should at least share
overlapping or clusters of phenotypes, even if one, overrid-
ing phenotype does not emerge. For example, in human
panic disorder, patients experience panic attacks, which are
discrete episodes of extreme fear accompanied by a set of
physiological and psychological symptoms. One person ex-
periencing palpitations, chest pain, sweating, and a choking
sensation may not share these same symptoms with another
person whose panic attack is characterized by tremor, diz-
ziness, chills, and nausea, yet both have panic disorder
based on longitudinal research.
It is also possible to extend these definitions beyond the
discrete disease diagnoses to produce a broader phenotype,
either as a spectrum of pathology or to include other phe-
nomena that overlap with the target phenotype. For exam-
ple, it has been proposed that particular behaviors that occur
across the population, but appear to be enriched in human
patients with a behavioral disorder, may provide a more
focused biological pathway for the study of that disorder.
These so-called “endophenotypes” (Gottesman and Gould,
2003) have led to interesting hypotheses about the patho-
physiology and genetics of disorders such as
schizophrenia and mood disorders (Hariri et al., 2005; Pe-
zawas et al., 2005; Tunbridge et al., 2006). This approach
also allows clusters of behavioral responses to be compared
with clusters of neurochemical or physiological responses
that occur with the discrete groups examined (Overall,
2005).
The use of additional, seemingly “unrelated” clinical
information allows the investigator to extend his or her
definition of phenotype far beyond the particular disorder
under study. For example, in one study of human panic
disorder, a constellation of medical symptoms, including
renal and bladder conditions, thyroid disorders, headaches,
and mitral valve prolapse, helped to genetically define a
subset of persons with panic disorder (Weissman et al.,
2000; Hamilton et al., 2003). Indeed, when subjects with a
common bladder condition called interstitial cystitis were
examined, panic disorder was highly enriched in the sub-
jects and their families when compared to controls (Weiss-
man et al., 2004). These types of approaches allow us to ask
questions about underlying genetic and neurochemical as-
sociations for conditions that may not appear to be related at
first glance.
In previous work, we distinguished between noise phobia
and separation anxiety in dogs in a clinical population,
although there exists an overlap between these disorders
(Overall et al., 2001). Whether this overlap is caused by an
overlap in definitions of the disorder, comorbidity between
common disorders, or pleiotropic expression of a broader
behavioral phenotype is currently unknown, but this is ex-
actly the sort of question our study tools are intended to
address. The starting point of our study lies in its definition
and assessment of phenotype using objective criteria based
on observable phenomena. This approach is to be distin-
guished from attempts to attribute motivations to a behavior
or define a behavior purely on its context.
Methods and tools of assessment
Participating dogs and owners in the CBGP are recruited
from active owners, trainers, breeders, handlers, and the
general pet-owning public. We are particularly interested in
anxiety-related disorders, including many aggressions, and
in families or households of dogs in which some dogs are
affected, and some dogs are not affected. By using unaf-
fected and affected dogs we can conduct a case-control
analysis, which speeds the rate at which suspect genetic
contributions can be readily identified. These types of stud-
ies are traditionally performed in laboratory environments,
where context and breeding can be tightly controlled. For
general questions about patterns of expressed phenotype
and potential heritability, laboratory studies are almost al-
ways too tightly constrained. Laboratory studies are at their
best for the examination of a single complex condition
which can be elucidated by crossing at least two different
breeds that are affected, and for in-depth studies of the
125Overall et al Understanding the Genetic Basis of Canine Anxiety
neurochemical and molecular pathology and interventions
that can manipulate it (see Parker and Ostrander, 2005 for
examples). By moving our studies from the laboratory (after
Scott and Fuller, 1965) to the home, we have sacrificed a
controlled environment for a more naturalistic one, but with
the benefit that it is in the latter in which dogs are expected
to live. Using dogs in the home environment also has the
advantage of allowing a full evaluation of a range of phe-
notypes that would likely not be expressed in controlled
circumstances. It is also true that by considering the envi-
ronment in which the dog is living, useful intervention may
be suggested.
All participating owners are required to: (1) complete an
extensive assessment questionnaire (24 pages; see Appen-
dix) for each dog, (2) submit all biological samples re-
quested (buccal swabs and/or blood for DNA extraction),
and if possible (3) provide an accurate pedigree. An exam-
ple of how the questionnaires for behavioral assessment will
be analyzed follows.
The use of a standardized methodology and defining
criteria (Overall, 1991, 1997, 2001, 2005) for this project
removes the need to rely on personal judgments (e.g., “the
dog is aggressive”) and on nonspecific signs, and instead
allows us to use these nonspecific signs (e.g., response when
pushed from the bed, response when verbally reprimanded)
and the type of reaction within each contextual category
evaluated (e.g., bark, growl, snarl, lift lip, snap, bite, with-
draw) to gauge the reactivity, severity, and intensity of the
reaction in an unambiguous manner. In the case of our
aggression questionnaire (CBGP: AGG), reactivity is de-
fined as the number of categories in which the dog reacts
inappropriately as a proportion of the total number of cat-
egories, severity is the score of how much the dog reacts
given the total number of points available if the dog exhib-
ited all reactions in all categories, and intensity can be
considered the total number of points accrued for all reac-
tions divided by the number of categories in which the dog
reacts.
Such an approach also allows the use of repeated mea-
sures for (a) stability of behavior; (b) treatment assessment;
and (c) for comparisons within or across families, age
groups, sexes, or breeds. Responses for different popula-
tions of dogs (e.g., families within breeds, breeds within
related groups, or across related vs. unrelated breeds) can
then be compared for age and sex. This approach also
allows us to gauge reliability and validity, measures that are
too often missing from veterinary behavioral studies (Mar-
tin and Bateson, 1986).
If we hope to understand the genetic bases of these
behaviors and behavioral pathologies, it is essential that
we use measurements or assessments that are repeatable
and consistent, and as free as possible from random
errors (in other words, that the behavioral assessments
are reliable), and that we are measuring what we think we
are measuring, not someone’s biased opinion of a com-
plex process (that is to say that the behavioral assess-
ments are valid). Achieving this goal is not possible if we
ask about people’s impressions of the behaviors rather
than assessing the behaviors themselves (see Taylor and
Mills, 2006, this volume).
Even in situations of complex inheritance, our under-
standing of heritable canine somatic conditions (Todhunter
et al., 2003; Carrier et al., 2005; Chase et al., 2005) is more
advanced than our understanding of putative, heritable ca-
nine behavioral conditions. One major reason for this dif-
ference is that behavioral assessments have historically
lacked rigor because of a lack of reliable and valid measures
or procedures. The CBGP approach is designed to redress
such concerns and to provide much needed data about
behavioral phenotypes and their underlying genetic associ-
ations.
The solicitation approach is two-tiered: owners complete
a short questionnaire online (see Appendix A) to submit
their colntact information and limited demographic and be-
havioral information about their dog(s). We then send a
participation kit including buccal swabs (adequate for small
searches of microsatellite markers) (Figure), and, if the dog,
condition, or initial findings are of interest, the longer, more
detailed CBGP questionnaire packet. Owners return the
questionnaire and biological samples along with a pedigree
(if available). Subsequently, a blood sample (needed for
larger SNP-based whole genome screens) and a video of
suites of specific behaviors may be requested. If interested
owners do not have access to the Internet, they may com-
municate with us by phone or mail.
The CBGP questionnaire packet (Appendix B) is derived
from continually updated, previously published question-
naires (Overall, 1991, 1997, 2001, 2007) that have been
tested in numerous clinical situations (Overall et al., 2001;
Overall and Dunham, 2002). Diagnostic definitions follow
those of Overall (1997, 2005, 2007).
The current complete version of the CBGP question-
naire packet follows. The authors welcome distribution
of this packet, participation and questions from clients
with potentially interesting dogs, and participation and
questions from breeders. More complete information
Figure Contents of kits sent to dog owners.
126 Journal of Veterinary Behavior, Vol 1, No 3, November/December 2006
about the mission and aims of the CBGP is available on the
Web site: http://psych.ucsf.edu/K9BehavioralGenetics/.
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127Overall et al Understanding the Genetic Basis of Canine Anxiety
Appendix A: Canine Behavioral Genetics Project (CBGP)- Initial Short Survey Questionnaire
This questionnaire is designed to collect data on the owner/client’s experience with their dog breed and any behavioral/medical
history for each participating dog. The data collected will be confidential and will NOT be sold or shared to outside parties.
Answering questions:
For YES/NO answers please mark an “X” for the appropriate answer. If there is not enough room to answer a question, continue in
the available space provided in the “Comments or additional answers to questions” space or on another piece of blank paper, with
the appropriate question number.
If you have more then one dog, please fill out one questionnaire for each participating dog.
For any questions or concerns, email K9BehavioralGenetics@lppi.ucsf.edu
Thank you!
A FEW EXAMPLES:
OWNER/CLIENT EXAMPLE
YES NO
1. How did you learn about the CBGP? (E.g., email, friend [Name the contact], online group/Web site) Online Yahoo group
2. Are you currently a dog breeder? X
3. If you said NO to #2 but were a dog breeder in the past, then what year(s)?
4. List present and past breeds you have bred: German Shepherd Dogs
5. Do you show your dog(s) in competition? X
6. Are you involved in dog breed groups (i.e. dog clubs, online groups, etc.)? X
7. Have you assisted in the development of a questionnaire pertaining to your dog’s breed? X
8. If yes, name of the group or association who developed the questionnaire:
DOG HISTORY EXAMPLE
Name of Dog: MAX
Questions #1 and #2 refer to MALE dogs only. For Female dogs, proceed to Question 3.
Regarding Only MALE dogs (#1 & #2): YES NO
1. Are they neutered? X
2. If yes, has their semen been saved? X
3. Does this dog have pedigree paperwork (with at least 3-4 generations)? X
4. Is there any behavioral information available for the previous 3-4 generations? X
5. Name of your dog’s breeder (if known, provide name, email or mailing address, and/or phone number):
Best Dog Breeder Inc., 123 Street St., Anytown, CA, 98765
CBGP- Initial Short Survey Questionnaire
OWNER/CLIENT
YES NO
1. How did you learn about the CBGP? (e.g. email, friend [Name the contact], online group/Web site)
2. Are you currently a dog breeder?
3. If you said NO to #2 but were a dog breeder in the past, then what year(s)?
4. List present and past breeds you have bred:
5. Do you show your dog(s) in competition?
6. Are you involved in dog breed groups (i.e. dog clubs, online groups, etc.)?
7. Have you assisted in the development of a questionnaire pertaining to your dog’s breed?
8. If yes, name of the group or association who developed the questionnaire:
128 Journal of Veterinary Behavior, Vol 1, No 3, November/December 2006
CBGP- Initial Short Survey Questionnaire
DOG
You are welcome to make as many copies of this form as needed.
This section regards your dog(s). If you have more then one dog, please fill out one dog questionnaire for each dog.
Name of Dog: ________________________________________
Questions #1 and #2 regard to MALE dogs only. For Female dogs, proceed to Question 3.
Regarding Only MALE dogs (#1 & #2): YES NO
1. Is HE neutered?
2. If yes, has his semen been saved?
3. Does this dog have pedigree paperwork (with at least 3-4 generations)?
a. If yes, can you provide a pedigree copy to this project? (Enclose a copy with swab samples)
b. If you are unable to provide a copy, then state a reason why:
4. Is there any behavioral information available for the previous 3-4 generations?
(Do you know if there are/were any BEHAVIORAL concerns with related family members?)
5. Name of your dog’s breeder (if known, provide name, email or mailing address, and/or phone number):
6. Does this dog have any BEHAVIORAL concerns?
7. If yes, what type of BEHAVIOR problem (e.g. panic, anxiety, separation anxiety, aggression to dogs, shy with humans, et cetera)?
8. Does this BEHAVIORAL concern run through their pedigree line?
a. Do you know of the same or similar BEHAVIORAL concerns in his or her siblings, parents, and/or other
related members?
b. Can you list which members and their BEHAVIORAL concerns (e.g., half-brother – separation anxiety)?
9. List medication(s) for the diagnosed BEHAVIORAL problem, if available:
10. List any MEDICAL concerns that run through their pedigree line (e.g., deafness, epilepsy, blindness):
11. Are you aware of any other dogs related to this one that are participating in this project?
(If known, please state the name of relative and relationship. e.g., Mariah – sister)
12. Coat and color markings:
13. Comments or additional answers to questions:
If you have another dog to submit, please continue onto the other side of this sheet or to another copy of this questionnaire.
Appendix B: Canine Behavioral Genetics Project (CBGP)
Instructions for completion of the history packet for canine behavioral genetics study:
The basic questionnaire—that must be completed for all dogs—has 4 parts: (1) a short questionnaire about you and your
household (DEMO & DOGH), (2) a screen for distress responses when left alone or when exposed to noise that has become a
uniform, validated tool for assessing specific types of canine anxiety (SANP), (3) a screen for aggressive responses that has become
a uniform, validated tool for assessing canine aggression (AGG), and (4) a screen for previous treatments / experiences / exposures
(PRT). If you have a dog who exhibits repetitive, stereotypic behavior, there is a 5th questionnaire for you to complete: Stereotypic
and Ritualistic Behavior History (SRBH).
Most of the responses called for are ticks in appropriate places, so it will take you about
1
2
hour per dog to complete the
questionnaires if the dog for whom you are completing the forms is problematic. If the dog has no problems, completion times will
be short.
129Overall et al Understanding the Genetic Basis of Canine Anxiety
Please complete 1 survey for each dog for whom you are submitting a DNA sample. If you are completing the questionnaires for
more than one pup in the same litter, you only need to complete the basic info about you, et cetera, once, as long as you indicate
that the pups are all from the same litter. If you are submitting forms for multiple adults, you do not need to repeat all of the
demographic information, but you do need to identify yourself, and the dog being evaluated, on each sheet. If you need more
sheets or lines on tables, please attach them with a clear indication of the section and question number to which they belong.
Many of these questions will not be directly relevant to your dog. In fact, we are not wholly sure which questions will be most
useful in identifying specific behaviors we will want to further analyze, so PLEASE send us your ideas. We are customizing these
surveys for factors that may be important in different breeds (e.g., eye color, hip evaluation, height), but we have to ask everyone
all of the same questions even if there is no response. Although all your specific data will be kept anonymous, the answers from the
questionnaires will be entered into the master database so that we can compare behaviors of your dogs with the large bank of
response about other dogs.
Also, because so many behavioral problems have been attributed to early environments, infections, exposures to toxins, diet,
medication, et cetera, it is very important that we ensure that we ask the same questions for each dog to learn about the more rare
early associations.
This bank of questions is lengthy, but no more lengthy than for similar studies on humans. Follow-up questionnaires and videos
may be desired for some dogs, and, if so, we’ll be contacting you again. Please remember that all data provided, even your identity,
is confidential. If you would like to be acknowledged in any specific way for participation at any level, please let us know.
When completed, please send the forms to:
Canine Behavioral Genetics Project
Steve Hamilton Lab - LPPI
401 Parnassus Ave. – Box 0984-NGL
San Francisco, CA 94143 U.S.A.
Or
Email forms to: K9BehavioralGenetics@lppi.ucsf.edu
Owner / client’s name: __________________________________________________
CLIENT: Demographics(DEMO)
Please fill out general information about the owner / client, your household, and all animals.
1. Owner or client’s name (first and last names):
2. Owner or client’s kennel name (if applicable):
3. Owner’s / client’s address:
4. Owner’s / client’s HOME phone no.:
5. Owner’s / client’s OFFICE phone no.:
6. Owner’s / client’s fax no.:
7. Owner’s / client’s e-mail address:
8. Please list the people, including yourself, currently living in the household now.
Name Sex (M/F) Age (yrs) Relationship to you (e.g. husband)
Self
9. Please list all the animals in the household.
KEY:
Pet’s Name Common or registered name
Order obtained The numerical order in which you acquired your pets
Sex M (Intact/Entire Male), MC (Male Castrated/Neutered/Altered), F (Intact/Entire or Unspayed Female),
FS (Spayed/Neutered/Altered Female)
Age obtained At what age (in months) was your animal when you received it?
Age now Current age (in months) of the animal
Any medical illness? Regarding present medical illness
Any behavioral illness? Regarding present behavioral illness
YYes
NNo
130 Journal of Veterinary Behavior, Vol 1, No 3, November/December 2006
Example:
Pet’s Name
Order
Obtained Breed
Sex
(M, MC, F, FS)
Age Obtained
(months)
Age Now
(months)
Any Medical
Illness?
Any Behavioral
Illness?
Rizzo 2 Beagle MC 24 60 (X)Y ()N ()Y (X)N
Max 1 German
Shepherd
MC 12 48 ()Y (X)N (X)Y ()N
Please complete:
Pet’s Name
Order
Obtained Breed
Sex
(M, MC, F, FS)
Age Obtained
(months)
Age Now
(months)
Any Medical
Illness?
Any Behavioral
Illness?
()Y ()N ()Y ()N
()Y ()N ()Y ()N
()Y ()N ()Y ()N
()Y ()N ()Y ()N
()Y ()N ()Y ()N
()Y ()N ()Y ()N
()Y ()N ()Y ()N
()Y ()N ()Y ()N
()Y ()N ()Y ()N
()Y ()N ()Y ()N
Owner / client’s name: __________________________________________________
CBGP: Dog History (DOGH)
The rest of the questionnaire will reflect information about the dogs participating in this study.
Please answer all questions to the best of your ability.
To continue, please complete all CBGP forms (pages 4–24) for one of the following:
a. One set of forms for EACH dog (single or multiple adults, related and unrelated).
OR
b. One set of forms for each LITTER (pups in the same litter).
Make as many copies of the CBGP forms as needed.
10. Dog’s Name (Registered name and Call name, if applicable):
11. Breed of Dog:
12. Sex of Dog: ( ) Male ( ) Castrated? ( ) Female ( ) Spayed?
13. How old was the dog when neutered? _______________ months old
14. Has this dog been bred? ( ) Yes ( ) No
15. If you have not yet bred this dog, do you plan on breeding him or her? ( ) Yes ( ) No
16. How tall is your dog (from shoulder to floor)? _______________ inches tall
17. Your dog’s weight? _______________ kg
18. What color is your dog? (e.g. Black, Brindle, Black/Tan, etc.)
19. What is the EYE color of your dog? Left eye: Right eye:
20. What is the NOSE color of your dog?
21. Dog’s date of birth: Day _______________ Month _______________ Year _______________
22. Has this pet had other owners (besides you)? ( ) Yes ( ) No
a. If YES, how many? ()1()2()3()4()Unknown
b. Reason for previous owner(s) relinquishment of this animal:
23. Where did you get this dog? Check the best appropriate answer.
c. ( ) Stray / found
e. ( ) Breeder - backyard breeder
g. ( ) Breed rescue service
i. ( ) Pet store
k. ( ) From your own breeding
l. ( ) Other (Please explain):
d. ( ) Breeder - serious show / performance
breeder
f. ( ) SPCA / Humane shelter
h. ( ) Newspaper adoption ad (not breeder)
j. ( ) Friend
131Overall et al Understanding the Genetic Basis of Canine Anxiety
YES
If YES, indicate under what
circumstances: NO
24. Does the dog for whom this questionnaire is being
completed have any recurrent, sporadic, or periodic
bouts of vomiting?
() ()
25. Does the dog for whom this questionnaire is being
completed have any recurrent, sporadic, or periodic
bouts of diarrhea / loose stool?
() ()
26. Has your dog been evaluated for any of the following
problems, and if so, what was the outcome?
YES NO OUTCOME?
a. Thyroidal Illness ( ) ( )
b. Addison’s Disease ( ) ( )
c. Cushing’s Disease ( ) ( )
d. Hip Dysplasia ( ) ( )
If YES, what method was used to evaluate the hips? ( ) OFA ( ) PennHIP ( ) Other
e. Elbow Dysplasia ( ) ( )
f. Hearing (BAER testing) ( ) ( )
g. Vision (CERF testing) ( ) ( )
h. Cardiac screened / assessed (e.g. for PDA, et cetera) ( ) ( )
27. Does this dog have any other physical or medical
problems – including any concerns about skin, joints,
digestion, reproduction, nervous system function (e.g.
epilepsy), long-term / serious infections (e.g. Lyme
disease), et cetera - that your veterinarian has noted?
() ()
28. Is your dog taking any medication for any medical or
behavioral problems?
() ()
29. What foods, including treats, is your dog fed (brand names, please)?
30. How is your dog exercised / maintained? Check all that apply.
m. ( ) Allowed to run free, unsupervised
o. ( ) Leash walked
q. ( ) Indoors only
n. ( ) Fenced/Kenneled/Run
p. ( ) Outside, unleashed but supervised
r. ( ) Outdoors only
31. How is your dog kept when you leave him or her alone?
b. ( ) Free in house
d. ( ) Indoors kennel / run
f. ( ) Crate indoors
h. ( ) Behind a gate or door in house
i. ( ) Other (please specify):
c. ( ) Free outdoors
e. ( ) Outdoor kennel / run
g. ( ) Crate outdoors or garage
32. What kind of living situation do you have?
a. ( ) Apartment
c. ( ) House with small yard
e. ( ) Farm
b. ( ) Townhouse / Condominium
d. ( ) House with large yard
33. Do you know how many animals were in this pet’s litter? ( ) YES()NO
# __________ Females # __________ Males
YES Specify Problem: NO DON’T KNOW
34. Are any litter mates who were / are affected
with any medical problems?
() () ()
35. Are any litter mates who were / are affected
with any behavioral problems?
() () ()
132 Journal of Veterinary Behavior, Vol 1, No 3, November/December 2006
36. Where does your pet sleep? Check all that apply; we know pets move at night.
a. ( ) In or on your bed
c. ( ) In its crate in your bedroom
e. ( ) In a crate in another room
g. ( ) In another room, voluntarily, chooses another
location elsewhere.
b. ( ) On its own bed in your bedroom
d. ( ) On its own bed in another room
f. ( ) On the floor next to your bed
h. ( ) In another room, (locked out of your bedroom),
chooses another location elsewhere.
37. What is your dog’s obedience school / training history?
a. ( ) No school
c. ( ) Puppy kindergarten
e. ( ) Group lessons - advanced
b. ( ) Trained yourself
d. ( ) Group lessons - basic
f. ( ) Private trainer at house or with you at their office – Specify:
( ) Private trainer - sent to trainer ( ) Agility
( ) Flyball
( ) Specialty training (hunting, herding, et cetera), please specify:
YES Specify Titles: NO
38. Does the dog have any titles? ( ) ( )
39. How well does this dog do with the following commands / requests: Perfectly OK, Needs work Badly
Sit () () ()
Stay ( ) ( ) ( )
Down / lie down ( ) ( ) ( )
Wait ( ) ( ) ( )
Heel ( ) ( ) ( )
Fetch ( ) ( ) ( )
Leave it / drop it ( ) ( ) ( )
Take it ( ) ( ) ( )
Other (Please specify): ( ) ( ) ( )
012345>5
40. How many total bites has your dog inflicted on any human?()()()()()()()
41. How many bites to humans broke the skin? ( ) ( ) ( ) ( ) ( ) ( ) ( )
42. How many total bites has your dog inflicted on any dog? ()()()()()()()
43. How many bites to dogs broke the skin? ( ) ( ) ( ) ( ) ( ) ( ) ( )
a. For dogs that have bitten HUMANS, which category best describes your dog’s orientation to the person bitten?
( ) Dog bites only when the victim’s back is turned (bites from behind).
( ) Dog bites only from the front of the victim.
( ) Dog bites from any direction.
b. For dogs that have bitten DOGS, which category best describes your dog’s orientation to the dog bitten?
( ) Dog bites only when the victim’s back is turned (bites from behind).
( ) Dog bites only from the front of the victim.
( ) Dog bites from any direction.
Owner / client’s name: __________________________________________________
CBGP: Separation Anxiety and Noise Phobias (SANP)
Please answer the following questions to the best of your ability.
The first set of these questions deals with an “actual absence”—i.e., the client actually leaves the house and the dog is either
alone or totally without the client. The second set deals with “virtual absence”— i.e., the client is home, but not accessible
because the door is closed or the dog is barricaded in another room. The questions are the same for each, but please answer both.
To answer questions:
Check NO if the dog on whom you are reporting does not react in the listed circumstance.
Check UNKNOWN if you don’t know.
Check YES if the dog reacts. Please evaluate the extent of the reaction from the accompanying list below.
IF YES: 0 100% of time (always)
1⫽⬍100% of time but 60% (more often than not)
240-60% of time (about equally)
3⫽⬎0% of time but 40% (less often than not)
133Overall et al Understanding the Genetic Basis of Canine Anxiety
FORMER BEHAVIOR?
Check THEN if your dog formerly exhibited the behaviors but has changed. Then write what he or she currently does in the
NOW column.
EXAMPLE ANSWERS:
Behaviors during an ACTUAL absence:
YES UNKNOWN NO BEHAVIOR
FORMER BEHAVIOR?
THEN NOW (Specify behavior)
()0(x)1()2()3 1.Destructive behavior when separated from owner/client.
()0()1()2()3 X2. Urination when separated from owner/client. x Hides under the table.
()0()1()2(x) 3 3. Defecation when separated from owner/client.
()0()1()2()3 x4. Vocalization when separated from owner/client.
()0()1()2()3 x5. Salivation when separated from owner/client.
Behaviors during an ACTUAL absence:
YES UNKNOWN NO BEHAVIOR
FORMER BEHAVIOR?
THEN NOW (Specify behavior)
1.()0()1()2()3 1.Destructive behavior when separated from owner/client.
2.()0()1()2()3 2.Urination when separated from owner/client.
3.()0()1()2()3 3.Defecation when separated from owner/client.
4.()0()1()2()3 4.Vocalization when separated from owner/client.
5.()0()1()2()3 5.Salivation when separated from owner/client.
Behaviors during a VIRTUAL absence:
YES UNKNOWN NO BEHAVIOR
FORMER BEHAVIOR?
THEN NOW (Specify behavior)
6. ( )0 ( )1 ( )2 ( )3 6. Destructive behavior when separated from owner/client.
7. ( )0 ( )1 ( )2 ( )3 7. Urination when separated from owner/client.
8. ( )0 ( )1 ( )2 ( )3 8. Defecation when separated from owner/client.
9. ( )0 ( )1 ( )2 ( )3 9. Vocalization when separated from owner/client.
10. ( )0 ( )1 ( )2 ( )3 10. Salivation when separated from owner/client.
11. ( )0 ( )1 ( )2 ( )3 11. Reaction during thunderstorms:
Type of response - please check all that apply:
( ) salivate
( ) defecate
( ) urinate
( ) destroy
( ) escape
( ) hide
( ) tremble
( ) vocalize
( ) pace
( ) freeze
( ) other; specify what, please
134 Journal of Veterinary Behavior, Vol 1, No 3, November/December 2006
12. ( )0 ( )1 ( )2 ( )3 12. Reaction to fireworks:
Type of response - please check all that apply:
( ) salivate
( ) defecate
( ) urinate
( ) destroy
( ) escape
( ) hide
( ) tremble
( ) vocalize
( ) pace
( ) freeze
( ) other; specify what, please
13. ( )0 ( )1 ( )2 ( )3 13. Reaction to other noises
Type(s) of Noise(s): (e.g. vacuum cleaners, leaf
blowers, weed whackers, dump trucks, sirens,
alarm systems, et cetera):
Type of response - please check all that apply:
( ) salivate
( ) defecate
( ) urinate
( ) destroy
( ) escape
( ) hide
( ) tremble
( ) vocalize
( ) pace
( ) freeze
( ) other; specify what, please
Behaviors for Noise Phobia:
If you noted any noise reactions in your answers for questions 1 through 13 of CBGP: Separation Anxiety and Noise Phobias (SANP),
please answer the following questions as relevant:
14. If your dog reacts in any of the ways described above to noises, and this is a working dog (meaning the ACTUAL work for which
the dog was bred, such as livestock work for Border Collies, retrieving fowl for Labrador Retrievers—not “herding” the cats or
retrieving balls), is the intensity of the dog’s reaction to noise different while working?
a. ( ) Yes, it is non-existent.
b. ( ) Yes, it is less severe.
c. ( ) No, it is the same.
d. ( ) Yes, it is more severe.
Please describe:
15. If you engage your dog in an organized activity (a dog sport such as agility or flyball, obedience, etc.), is the dog’s intensity of
reaction to noise different while engaged in that activity?
a. ( ) Yes, it is non-existent.
b. ( ) Yes, it is less severe.
c. ( ) No, it is the same.
d. ( ) Yes, it is more severe.
Please describe:
135Overall et al Understanding the Genetic Basis of Canine Anxiety
16. How frequently do noise events such as thunder, fireworks, or gunshots occur in the dog’s environment?
a. ( ) Never
b. ( ) Infrequently (only a few times a year)
c. ( ) Regular (averaging once a month or so)
d. ( ) Frequently (a few times a month or more)
What are these noises?
If the dog has undergone a change of environment, or is in more than one environment (as a result of travel, multiple homes,
away for training, etc.) and this situation is relevant, explain below:
17. Has this dog ever been treated for noise sensitivities or phobias? Please circle all relevant choices below:
a. ( ) Acepromazine (“Ace”)
b. ( ) Rescue Remedy
c. ( ) Benzodiazepines (i.e., Valium, Xanax)
d. ( ) Other medications (please describe)
e. ( ) Other “natural” or holistic remedies (please describe)
f. ( ) Desensitization (tapes, CDs, videos)
g. ( ) Other (please describe)
18. Do you have additional comments about your dog’s reaction to noise, or is there anything else about his or her behavior when
exposed to noise that you think we should know?
Owner / client’s name: __________________________________________________
CBGP: Aggression (AGG)
This part of the questionnaire looks at your dog’s response to various situations (stimuli).
Please read through each item and check the relevant column. Feel free to add comments or additional explanations where
you think it is appropriate (see example). This part of the questionnaire will take 5-10 minutes to complete.
To answer:
As you evaluate your dog, check the appropriate reaction from the accompanying list below.
KEY:
NR no reaction
SL snarl (noise)
Llift lip (can see corner teeth)
BK bark (aggressive, not an alerting bark)
Ggrowl (not a play growl)
SP snap (no connection with skin)
BT bite (connects with skin, regardless of damage)
WD withdraw from or avoid situation
NA not applicable (animal has never been in that situation)
FORMER BEHAVIOR?
Check THEN if your dog formerly exhibited the behaviors but has since changed his or her response. Then, in the NOW column,
write what he or she currently does as a response.
*For any of the categories marked with an asterisk, please note the dog’s other body postures, including position and activity of
tail, position of ears, position of body, whether hair is up and where, and any other information you think is important. For
additional comments, write on a blank sheet of paper any observations with the corresponding questionnaire section and action
number.
If you notice that your dog reacted to categories 29, 30, 33, 34, or 35, does he or she react only as a last resort?
136 Journal of Veterinary Behavior, Vol 1, No 3, November/December 2006
For Example:
ACTION NR SL L BK G SP BT WD NA
FORMER BEHAVIOR?
THEN NOW (Specify behavior)
1. Take dog’s food dish with food X
2. Dog approaches dog while eating* X
3. Dog on leash approached by known dog on street*
X
Additional answers/information provided by owner/client:
Aggression (AGG)
(2) His ears are pointing up, and his tail is up too. He looks like he will charge the other dog.
(3) He reacts as soon as the known dog approaches him.
Owner / client’s name: __________________________________________________
CBGP: Aggression (AGG)
ACTION NR SL L BK G SP BT WD NA
FORMER BEHAVIOR?
THEN NOW (Specify behavior)
1. Take dog’s food dish with food
2. Take dog’s empty food dish
3. Take dog’s water dish
4. Take food (human) that falls on floor
5. Take rawhide
6. Take real bone
7. Take biscuit
8. Take toy
9. Human approaches dog while eating*
10. Dog approaches dog while eating*
11. Person approaches dog while playing with toys*
12. Dog approaches dog while playing with toys*
13. Person approaches/disturbs dog while sleeping*
14. Dog approaches/disturbs dog while sleeping*
15. Step over dog
16. Push dog off bed/couch
17. Reach toward dog*
18. Reach over head*
19. Put on leash*
20. Push on shoulders
21. Push on rump
22. Towel feet when wet
23. Bathe dog
24. Groom dog’s head*
25. Groom dog’s body*
26. Stare at
27. Take muzzle in hands and shake*
28. Push dog over onto back*
29. Stranger knocks on door
30. Stranger enters room*
31. Dog in car at toll booth*
32. Dog in car at gas station*
33. Dog on leash approached by known dog on street*
34. Dog on leash approached by unknown dog on
street*
35. Dog on leash approached by person on street*
36. Dog in yard—person passes*
37. Dog in yard—unknown dog passes*
38. Dog in yard—known dog passes*
39. Dog in vet’s office*
40. Dog in boarding kennel*
41. Dog at groomer*
42. Dog yelled at*
43. Dog corrected with leash* (Please define what you
mean by a “correction”)
137Overall et al Understanding the Genetic Basis of Canine Anxiety
44. Someone raised voice to owner in presence of dog
45. Someone hugs or touches owner in presence of dog*
46. Squirrels, cats, small animals approach dog
47. Bicycles, skateboards
48. Crying infant*
49. Playing with 2-year-old children*
50. Playing with 5-7-year-old children*
51. Playing with 8-11-year-old children*
52. Playing with 12-16-year-old children*
Additional answers/information provided by client/owner
Owner / client’s name: __________________________________________________
CBGP: Previous Treatments (PRT)
This portion of the questionnaire investigates types of manipulations used on the dog as a behavioral modifier.
In the “ACTIVITY TRIED?” column, please check the items below according to which treatment your dog has experienced, and
indicate the outcome. If your dog is a rescue dog and/or someone else (besides you) has formerly tried any of these activities,
please check the asterik* column and indicate the response, if known.
FOR EXAMPLE:
Activity tried? *Outcome (Dog’s Response)
1. Stare at or “stare down” XDog growled.
2. Grab by jowls and shake XDog bit hand. Broke skin on hand of owner.
Previous Treatments
Activity tried? *Outcome (Dog’s response)
1. Stare at or “stare down”
2. Grab by jowls and shake
3. Get an additional dog as a companion for this one
4. Step on leash or choke collar and force down
5. Blow in nose or face
6. Buy different types of dog toys (ex: Kongs, etc.)
7. Metal choke collar
8. Prong collar
9. Halti, head collar, or Gentle Leader
10. Harness
11. No-pull or Sporn harness
12. Martingale collar
13. Scruffy Guider
14. Fabric choke collar
15. Electronic or shock collar controlled by owner
16. Electronic or shock collar controlled by trainer
17. Electronic or shock collar—remote-control or bark-activated
18. Citronella collar
19. Citronella spray
20. Throw a tin or can of pennies
21. Water pistol
22. Whistle
23. Foghorn
24. Hit dog with hand
25. Hit dog with leash
26. Hit dog with empty plastic soda bottle
27. Hit dog with whiffle ball bat
28. Hit dog with chain
29. Hit dog with board, plank, or baseball bat
30. Hit dog under chin
31. Step on dog’s toes
32. Knee dog in chest / belly
33. Kick dog
34. Bite dog
138 Journal of Veterinary Behavior, Vol 1, No 3, November/December 2006
35. “Alpha roll” [Hold dog in a spread eagle position on back]
36. “Dominance down” [Hold dog down on side, legs extended,
head flat]
37. Growl at dog
38. Yell or scream at dog
39. Long down
40. Sit and wait
41. “Time out” [If YES, indicate where, how, and length of time]
42. Praise for good behavior
43. Crate
44. Kennel outdoors
45. Fenced yard
46. Invisible fence
47. Isolate somewhere in house [if YES, indicate where in the
house and length of time]
48. Board at vet’s or kennel (indicate establishment)
49. Use whip on dog
50. Cattle prod
51. “String up” or hang by leash and collar (all 4 paws off
ground)
52. “String up” or hang by leash and collar (only front paws off
ground)
53. Pop and jerk leash
54. Yank or pull on leash
55. Tie up—physically
56. Tie out or stake on very short lead hooked to wall or floor
57. Muzzle
58. Increase exercise
59. Increase play
60. Give treats for good behavior
61. Deprive of food
62. Thrown against wall
63. Beat with your fists
64. Shove dog’s nose / face into urine, feces, or destruction
65. Use blow torch on dog
66. List any other technique recommended or not listed:
Owner / client’s name: __________________________________________________
CBGP: Stereotypic and Ritualistic Behavior History (SRBH)
Please complete this form ONLY if your pet is showing any repetitive, ritualistic behaviors that you find troublesome or
about which you are concerned. If not, please go to the LAST PAGE.
1. Which of the following category/categories below fits your dog’s behavior? (Check as many categories that apply to the dog’s
behavior. Then check the best description that relates to the selected behavior.)
a. ( ) Grooming ( ) Chewing
( ) Biting
( ) Licking
( ) Plucking
( ) Barbering
( ) Sucking self
b. ( ) Hallucinatory ( ) Staring
( ) Tracking
( ) Attacking
( ) “Invisible prey”
139Overall et al Understanding the Genetic Basis of Canine Anxiety
c. ( ) Consumptive ( ) Consuming rocks
( ) Dirt
( ) Other objects
( ) Wool-fabric chewing or sucking
( ) Licking or gulping air
d. ( ) Locomotory ( ) Circling
( ) Tail-chasing
( ) Freezing
( ) Scratching
e. ( ) Vocalization ( ) Rhythmic barking
( ) Barking
( ) Howling
( ) Growling
Owner / client’s name: __________________________________________________
CBGP: Stereotypic and Ritualistic Behavior History (SRBH)
Check the appropriate answer (YES/NO/UNCERTAIN) for each of the following questions. Some of the answers may need more
detailed explanations. If so, please write the answer on a blank piece of paper, indicating the questionnaire section and appropriate
question number.
FOR EXAMPLE:
YES NO UNCERTAIN
2. Was there a change in the household or an event
that was associated with the development of the
behavior?
If so, please describe in detail.
(X)
() UNCERTAIN – There may have been.
Please explain. ()
2. YES – Our dog’s behavior changed after we introduced him to our new baby.
CONTINUE WITH QUESTIONNAIRE:
YES NO UNCERTAIN
2. Was there a change in the household or an
event that was associated with the development
of the behavior?
If so, please describe in detail.
()
() UNCERTAIN – There may have been.
Please explain. ()
3. Is there any time of day when the behavior
seems more or less intense?
If so, please describe in detail
what is usually going on at
that time of day. ()
() No one is home long enough to
know. ()
4. Is there a person/another pet in the presence
of whom the behavior seems more intense?
If so, who is this and what is
their association to the pet?
()
() No one is home long enough to
know. ()
5. What is the attitude of the pet while performing the behavior (e.g., distressed, self-absorbed, fearful, frantic)?
6. Does the animal respond to its name or seem
aware of its surroundings while in the midst of
the behavior?
() () ()
7. Is the dog aware that you are calling him or
her?
If so, how can you tell? () () No one is home long enough to
know. ()
8. Can you convince the pet to stop the behavior by either of the following:
a. Calling him or her. ( ) ( ) ( )
b. Using physical restraint. ( ) ( ) ( )
9. List what kinds of things (e.g., noises, treats, toys), if any, will interrupt the behavior once it has started:
10. Is there a location in which the animal prefers
to perform the behavior?
If so, where? () () ()
140 Journal of Veterinary Behavior, Vol 1, No 3, November/December 2006
11. For ingestion, list what types of objects are consumed: (Please be as specific as possible–what type of rug, fabric, of sweater?)
12. Does any event or behavior routinely occur
immediately before the behavior begins?
If so, what? () () ()
13. Does any event or behavior routinely occur
immediately after the behavior ceases?
If so, what? () () ()
14. Has the pet’s general behavior changed in any
way since the onset of the atypical behavior
(e.g., the dog is more aloof, more aggressive,
more withdrawn, more or less playful)?
If so, please specify? () () ()
15. Has the pet’s diet recently been changed? If so, what—specifically—was
the change? ()
() ()
16. Regarding your concerns, how old do you think your pet was when its ritualistic
behavior began?
_______________ months
17. Did anyone else in the dog’s family exhibit
these or similar behaviors?
() () ()
If YES, please check all relatives known to be affected, and if they exhibited different forms of ritualistic behaviors, please specify:
RELATIVE PLEASE SPECIFY IF THE RELATIVE EXHIBITED A DIFFERENT FORM OF
RITUALISTIC BEHAVIOR
a. Mother
b. Father
c. Sister
d. Brother
e. Grandmother
f. Grandfather
g. Cousin
h. Son
i. Daughter
j. Other (Unsure if a relative exhibited behavior, or
they are distantly related.)
Finally, here are the last few questions!!!!
YES NO
1. Are these questionnaires accompanied by a PEDIGREE
for each participating dog?
() ()
**PLEASE do not forget to provide a pedigree for each
participating dog, if possible.
If you know or think you have a FAMILIAL
BEHAVIORAL PROBLEM, please assign a CODE for each
family member on the pedigree. Below is the list of
the codes to be used:
KA Affected
KU Known to be unaffected
TA Thought to be affected
TU Thought to be unaffected
NA Information is not available
2. Can you provide a video of the dog if we request
one?
() ()
3. Is there anything else you’d like us to know? ( ) ( )
Your confidentiality will be respected. Also, please help us to improve these questionnaires. We’d love to hear your ideas.
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141Overall et al Understanding the Genetic Basis of Canine Anxiety
... It is based on the established and widely accepted content of the instrument used to determine noise phobia [Lincoln Sound-Sensitivity Scale) in the main clinical behavioral study (18)]. The states referred to in this instrument have been used in several clinical trials on noise phobia and other anxiety problems with success (19,20), and also used in other assessments with a similar goal (21) and the Anxiety Intensity Rank scale (22). However, we did not include the behavior "Exaggerated response when startled, " from the Lincoln Sound-Sensitivity Scale, because it is rare and previous experience of one of the authors and originators of the scale (DSM,) indicate that it is difficult for the owners to judge. ...
... The behaviors used LCAS are a widely accepted representation of canine anxiety-related behaviors (16,(21)(22)(23). ...
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Introduction: Anxiety in dogs, especially in relation to certain noises, is a common issue which can lead to clinically significant problems like noise phobias. While several scales have been used to assess sound sensitivity and reactivity, clinical monitoring has tended to depend on unvalidated methods, general assessment, and/or historical comparison with owners' recall of previous episodes. Therefore, we aimed to develop and validate a scale to assess canine anxiety. Materials and Methods: We used the data from 226 dogs from a previously reported double blind placebo controlled study in order to determine the validity of the 16 item “Lincoln Canine Anxiety Scale.” Unidimensionality was assessed through correlation between individual item scores and total score, with internal consistency assessed using Cronbach's alpha. Factor analysis was used to determine the dimensionality of the scale. Item response theory (IRT) was used to gain insight into the value of single items to the overall scale scores. To characterize the score characteristics in an anxiety-eliciting context we analyzed the behaviors of placebo treated dogs assessed at 00:20 h, the time point of maximum noise stimulus during New Year's Eve fireworks. Sensitivity of the scale to treatment effects was determined from its performance in the wider study. Results: The majority of correlations between individual items and total score were >0.48, with Cronbach's alpha equalling 0.88, indicating good internal consistency. Principal Component Analysis (PCA) confirmed a unidimensional structure. IRT indicated that the scale could be reduced to 11 items without significantly reducing its value. The scale showed good treatment and stimulus sensitivity, with a score change of ~20 points differentiating “no/worse” effect from an “excellent” effect and a 30% difference between treatment (imepitoin) and placebo. Conclusion: In our initial validation the Lincoln Canine Anxiety Scale appears to provide a reliable method for determining anxiety and fear responses by dogs and monitoring the effects of treatment.
... Although high levels of fear may be a consequence of poor or absent socialization practices in the kennels, it is important to note that a range of different factors may play a role in shaping fear responses. These include genetics, physical health, handling and breeding practices, exercise, conspecific interactions, parity, breed and more [6,[27][28][29][30]. In this study, no significant differences were found between the behavioral reactions of males and females to any of the three stimuli. ...
... However, there is evidence from previous work that breed may have a significant effect on fear levels. More than 50 breeds have been determined to show potentially heritable fear/anxiety [29]. Additionally, Morrow et al. [30] found significant differences in the percentage of subjects demonstrating fear-related avoidance behaviors and the age of onset of these behaviors between three various breeds. ...
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Understanding the behavioral welfare of dogs in commercial breeding kennels (CBKs) is important for improving breeders’ management practices as well as dog welfare. In the current study, breeding dogs from CBKs were exposed to novel stimuli to evaluate their behavioral responses, with emphasis on indicators of fear. Subjects were presented with a standard stranger-approach test, a traffic cone, and a realistic dog statue. Sixty dogs were exposed to the three stimuli and behavioral responses were scored using an ethogram developed for this study. Dogs spent significantly more time investigating the environment, staying further away from the stimulus, and they took longer to approach and investigate when presented with the cone than with the dog statue or stranger (p < 0.01). These findings suggest that the cone elicited more fear-related behaviors than the dog statue and stranger. Given these results, in addition to socializing their dogs to unfamiliar people and other dogs within their kennels, commercial breeders should be encouraged to increase the exposure of their dogs to more diverse novel stimuli to reduce non-social fear and support the welfare of dogs while they reside in the kennel and when they transition to new homes.
... All dogs had anxiety intensity ranks (AIRs scores) for noise calculated based a section of a much longer behavior and life-style questionnaire (WDQ-PET), completed by owners of all study dogs (Overall et al., 2006). We used this questionnaire to classify dogs as noise phobic or reactive or not reactive. ...
... In this study AIR scores were calculated based on client reports using a standardized and validated noise questionnaire embedded in the WDQ-PET (Overall et al., 2006Tiira and Lohi, 2016;Bellamy et al., 2018). It is notable that two clients (∼10%) who responded 'no' to a 'yes/no/unknown' question, changed to 'yes' when they could reflect on the affiliated behaviors and their frequencies across the contexts of noises queried. ...
Article
As part of a larger problem solving study, 22 dogs who were identified by owners/clients as reacting to noise and 13 identified by owners/clients as not reacting to noise that had been previously compared for auditory function were compared with respect to their reported noise reactions, performance on a puzzle box test, response to a provocative noise recording, and movement. Each dog was evaluated using a standardized, validated, semi-quantitative objective questionnaire from which an Anxiety Intensity Rank (AIR) score was calculated. AIR score calculations reflect the number of categories of noise to which the dog reacts, the behaviors exhibited, and the intensity of the reaction. Each dog underwent a 13 item problem-solving test (The Canine Intelligence Test Protocol; CITP) designed to evaluate 4 standardly evaluated cognitive domains. We report on two of the 13 tests – the puzzle box test and the provocative noise test – for this group of dogs. During testing most dogs wore collars containing accelerometers using custom firmware which provided second-by-second 3D movement data. AIR scores for the 2 groups differed significantly (Welch’s t tests; t = 4.34, df = 19.23, P < 0.0004), although the affected group was only mildly affected. Affected dogs took longer to solve the tasks and, overall, did more poorly (P < 0.5). Accelerometry revealed that during testing, movements of affected dogs were more erratic, less continuous and subject to greater extreme deviations and longer pauses than were the movements of unaffected dogs. Even dogs mildly affected with fear of noises differed from unaffected dogs, and performed more poorly on problem-solving tests possibly, in part, because their movements were characterized by a high degree of physical and behavioral/emotional reactivity. Reactions to noise affect how these dogs move, which may affect every investigatory and interactive aspect of their lives. Combining AIR scores with movement measures may be a useful method to assess welfare in pet dogs.
... A dog's behavior is a function of genetic, epigenetic, and environmental factors [1,2]. The endocrine balance reflected in the level of neuromodulators such as dopamine and serotonin as well as cortisol or noradrenaline is necessary for maintaining homeostasis and facilitates adaptation to stressful conditions [3,4]. ...
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It has been assumed that stroking relieves stress responses in dogs, and dogs with the activation of the left-brain hemisphere (right-pawed) may show better adaptation to stress conditions. The aim of the study was to determine whether the stroking stimulus induced changes in the level of selected neuroregulators in dogs’ blood and whether these changes depended on the sex and the predominance of the activity of one of the brain hemispheres. The study involved 40 dogs of various breeds and both sexes. The experimental animals were subjected to a behavioral tests (Kong test), and the levels of noradrenaline, serotonin, and cortisol were determined in their blood plasma. The results of the behavioral test revealed that most dogs exhibited increased activity of the left hemisphere. Furthermore, irrespective of the sex and paw preference, stroking the animal was found to alleviate the stress response, which was reflected in reduced cortisol levels and increased serotonin levels. It was found that the plasma noradrenaline, cortisol, and serotonin levels were lower in the female dogs than in the males. Additionally, the plasma noradrenaline and serotonin levels were higher in the right-pawed dogs than in the left-pawed dogs. The present results confirm the assumption that right-pawed dogs adapt to stressful conditions more readily.
... Even in studies where clients have received information defining specific behavioural patterns, some behavioral signs used by researchers are simply less apparent than others if constant monitoring of the dog does not occur. If dogs are not exposed to certain provocative stimuli, or not observed to react in any given context, false negatives can be reported, a sequela that can be minimized by behavioural testing and rigorous, objective quantitative or semiquantitative questionnaires (Overall et al., 2006;Tiira and Lohi, 2014;Overall et al., 2016;Bellamy et al., 2018). Furthermore, dogs may change with age, exposure, and level and type of provocative stimulus, all of which may have affected how the owner evaluated the dog the day any survey was completed. ...
... Although SRD is one of the most studied behavioural problems in dogs, its etiology is still obscure (Ogata, 2016). The potential causes mentioned in the literature include negative early experiences such as being separated too early from the mother, traumatic experiences occurring while left alone, changes in family circumstances (for details see Flannigan and Dodman (2001)) or heritable factors (Overall et al., 2006;van Rooy et al., 2016). McCrave (1991) also reported an increased prevalence of SRD in mixed breed dogs. ...
Article
Anxiety tends to aggregate in families, and families increasingly include companion animals, such as dogs. Based on previous research pointing to a 'personality fit' between humans and their companion dogs, this study explored the potential association between owners' trait anxiety and dogs' fear and anxiety-related behavior problems, while also testing for mediating and moderating factors. Two hypotheses previously proposed in the literature were here tested: that dogs may respond to their owners' anxiety directly through emotional contagion, or that owners' anxiety may affect dogs' indirectly via (a) owners' over-protectiveness-thereby restricting the dog's ability to familiarize itself with novel situations-or (b) their use of coercive dog-training methods. A cross-sectional approach was followed with use of an on-line questionnaire designed to measure owners' trait anxiety and dogs' fear and anxiety-related behavior problems, as well as owners' protective behavior, and dogs' emotional reactions to their owners' emotions (i.e., 'empathic trait'). Data were obtained from 1,172 self-identified dog owners. Results showed a significant positive correlation between owners' trait anxiety and the severity of their dogs' fear and anxiety-related behavior. No evidence was found for mediation of this relationship by owners' protective behavior or their use of coercive training methods. However, the results showed a marginally significant moderation effect above a particular score in dogs' 'empathic trait'. This study suggests that owners' trait anxiety is associated, to some extent, with the occurrence of dogs' fear and anxiety related behavior problems. The extent to which dogs exhibit an 'empathic trait' may explain the strength of this association.
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Canine separation anxiety is a common problem behavior with little known about the factors that lead to its development. This study investigated whether high arousal/excited departures and greetings with a dog may lead to the development of increased frequency of separation-related behavior in newly adopted dogs. In Experiment 1, we exposed two groups of dogs to a series of either high or low arousal human experimenter interactions. We hypothesized there would be an increase in activity, vocalizations, and time in proximity to door for the dogs in the high arousal condition compared to the low arousal condition, when left alone, and that these behaviors would increase across 10 sessions. Our results did not show this, indicating high arousal departures and arrivals may not play a role in the development of increased separation-related behavior. In Experiment 2, we utilized a survey to ask owners of dogs with, and without, canine separation anxiety about their arousal levels during arrivals and departures at home with their pet dog. We hypothesized dogs with reported canine separation anxiety would have been exposed to higher arousal levels during departures and arrivals. Our results showed a small difference between the groups, in the opposite direction of our hypothesis, where the dogs with reported canine separation anxiety were exposed to slightly lower arousal levels than dogs without, but the difference was small. From both Experiment 1 and 2, our results indicate that high excitement and playful levels of owners during departures and arrivals is not associated with the development of increased separation-related behavior in newly adopted dogs. It is important to make the distinction however, that low arousal departures and arrivals are a well-documented treatment for separation-related behavior, and our results only reflect that these arousal levels do not appear to play a causal role in the development of an increased frequency of them.
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Behavioral problems occur frequently in dogs and represent a significant threat to dog welfare. Anxiety, phobias, and fears comprise most of the canine behavioral conditions. The identification of an association between specific behavioral phenotypes and genetic variants of candidate genes would be a valuable tool in selection for dogs less susceptible to anxiety and fear, which may improve animal welfare. The DRD2 gene encodes the dopamine receptor 2. In this study, we found 8 SNPs in the DRD2 gene of the Havanese, a breed that shows large variation in a behavioral phenotype that manifests itself as a tendency to react fearfully by withdrawing in social situations. Significant associations were detected between 2 SNPs in exon 2 of the DRD2 gene and increased social fear in Havanese dogs (n = 158), as evaluated through observation by an external evaluator (respective allelic odds ratio: 4.35, 4.07) and through owner questionnaires (respective allelic odds ratio: 1.96, 2.2). Because different types of fear-related behavioral disorders commonly co-occur, the SNPs in exon 2 were also investigated for possible association to noise reactivity in 5 breeds: Havanese (n = 121), collie (n = 94), Irish soft-coated wheaten terrier (n = 44), Nova Scotia duck tolling retriever (n = 33), and standard poodle (n = 29). Significant associations were detected between SNPs in exon 2 of the DRD2 gene and noise reactivity in the Irish soft-coated wheaten terrier (respective allelic odds ratio: 2.64, 2.88) and collie (allelic odds ratio: 3.03). The same SNP alleles were associated with the beneficial phenotypes in the 3 breeds.
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This paper reports evidence for a possible “chromosome 13 syndrome,” which includes panic disorder, kidney or bladder problems, serious headaches, thyroid problems (usually hypothyroid), and/or mitral valve prolapse (MVP). In the course of a genetic linkage study of panic disorder, we noted these medical conditions in individual family members. (We were blind to family relationships and marker data.) We hypothesized that there may exist a subgroup of panic families with these medical conditions, which for simplicity we called it the “syndrome.” Subsequently we reclassified the families as with or without the “syndrome” and extended the phenotype for analysis to include the above medical conditions. All these classifications were also done before the analysis and blind to marker data. We then examined our linkage results, looking for significant differences between families with and without the “syndrome” (using several definitions of the “syndrome”)—i.e., testing for genetic heterogeneity. When the families with and without bladder/kidney problems were separated from each other, one marker—D13S779 (ATA26D07)—yielded a lod score of over 3 in the families with bladder/kidney problems. This lod score went up to 4.2 in these families when we diagnosed any individual with any one of the “syndrome” conditions as affected. These results were statistically significant even after applying an extremely overconservative Bonferroni correction for multiple tests. We present these results in order to alert other investigators working on panic disorder, for replication. If replicated, one may hypothesize that a candidate gene for the syndrome should be expressed in CNS, kidney, gut, thyroid, etc. We also noted that two independent studies report recent linkage findings between schizophrenia and the same region on chromosome 13. No connection between schizophrenia and panic disorder has ever been reported. Finally, we suggest that genetic studies of psychiatric disorders might prove more fruitful if phenotypes were expanded to include possible manifestations of the disorder in medical (non-mental) symptoms. Am. J. Med. Genet.(Neuropsychiatr. Genet.) 96:24–35, 2000. © 2000 Wiley-Liss, Inc.
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The Regional Shelter Relinquishment Study sponsored by the National Council on Pet Population Study and Policy (NCPPSP) is a US research project designed to explore the characteristics of relinquished dogs and cats, their owners, and the reasons for relinquishment. The NCPPSP Regional Shelter Study, which was conducted between February 1995 and April 1996, found that behavioural problems, including aggression toward people or non-human animals, were the most frequently given reasons for canine relinquishment and the second most frequently given reasons for feline relinquishment. No association was found between category of relinquishment (behavioural, mixed, non-behavioural) and gender, number of times mated (males), number of litters (females), purebred status, declaw status, and number of visits to the veterinarian within the past year, for either dogs or cats. Associations were found between category of relinquishment and number of pets in the household, number of pets added to the household, neuter status of female dogs and cats , neuter status of male dogs, training level, age of pet relinquished, length of ownership, and pets acquired from shelters. Associations also were found between the state in which the pet was relinquished and income level of owner.
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Although these more divergent views show how different theoretical foci shape the approach and point of departure for discussion and diagnosis, what is clear from the above is the agreement on the need to vigorously pursue areas of behavior often considered only tangential to the actual daily practice of veterinary behavioral medicine (eg, ethograms, normal behavior and effects of ontogeny, behavioral neurogenetics, sensory assessments, etc.). As part of this discussion section, participants were asked to further discuss the issues they felt were important. The contributions of Sharon Crowell-Davis, Joel Dehasse, Jaume Fatjo, Kathe Houpt, Daniel Mills, and Clara Palestrini follow in this volume.
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Temperament tests have been created by a range of organizations and individuals in order to assess useful, predictable behavioral tendencies in working dogs and, increasingly, in companion dogs. For the latter group, such tests may help to select suitable pets from rescue centers or to identify those already in the population that are, or are likely to be, unsuitable as pets (e.g., those with behavior problems involving aggression). Unfortunately, many of these tests seem to have been developed without a systematic scientific approach. Perhaps as a result there are few reports of these tests in the scientific literature and even fewer that fully report their reliability and specific aspects of validity. This pattern is unfortunate, because the outcome of tests for companion dogs may have the potential to affect their welfare and survival. This paper attempts to encourage a more scientific approach to the development, conduct, and evaluation of temperament tests for adult companion dogs. Five key measures of the quality of a temperament test (purpose, standardization, reliability, validity, and practicality) are identified and explained in detail. Methods for the assessment of these qualities are given together with discussion of their limitations.
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New areas of endeavour succeed either because they make a compelling case for their worth within an existing paradigm or because a new generation is raised for whom a once heretical paradigm is now the norm. It is difficult to tell which route will lead to the acceptance and growth of veterinary behavioural medicine, but the latter seems likely and, perhaps, necessary. As one of the newest specialities in veterinary medicine, behavioural medicine may suffer more than other specialities from an unclear identity because so many disparate groups who are not rooted in veterinary medicine have participated in its evolution.
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The domestication of the dog from its wolf ancestors is perhaps the most complex genetic experiment in history, and certainly the most extensive. Beginning with the wolf, man has created dog breeds that are hunters or herders, big or small, lean or squat, and independent or loyal. Most breeds were established in the 1800s by dog fanciers, using a small number of founders that featured traits of particular interest. Popular sire effects, population bottlenecks, and strict breeding programs designed to expand populations with desirable traits led to the development of what are now closed breeding populations, with limited phenotypic and genetic heterogeneity, but which are ideal for genetic dissection of complex traits. In this review, we first discuss the advances in mapping and sequencing that accelerated the field in recent years. We then highlight findings of interest related to disease gene mapping and population structure. Finally, we summarize novel results on the genetics of morphologic variation.