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STANDARD ARTICLE
Association between life span and body condition in
neutered client-owned dogs
Carina Salt
1
| Penelope J. Morris
1
| Derek Wilson
1
| Elizabeth M. Lund
2
|
Alexander J. German
3
1
WALTHAM Centre for Pet Nutrition, Melton
Mowbray, United Kingdom
2
BANFIELD
®
Pet Hospitals, Vancouver,
WA, USA
3
Institute of Ageing and Chronic Disease,
University of Liverpool, Cheshire, United
Kingdom
Correspondence
Alexander J. German, Institute of Ageing and
Chronic Disease, University of Liverpool,
Leahurst Campus, Chester High Road, Neston,
CH64 7TE, United Kingdom.
Email: ajgerman@liverpool.ac.uk
Funding information
Royal Canin
Background: There is an association between overweight status and life span in kenneled dogs,
but a similar association has not been reported for pet dogs.
Objectives: To examine the effects of being overweight in middle age on the life span of neu-
tered client-owned dogs.
Animals: Fifty-thousand seven-hundred eighty seven middle-aged neutered client-owned dogs
attending a network of approximately 900 veterinary hospitals across North America.
Methods: Retrospective case-control study. For each of 12 breeds, groups of dogs aged between
6.5 and 8.5 years were identified as being in “overweight”or “normal”body condition. Within each
breed and sex, differences in life span between dogs in normal body condition and overweight body
condition in the 2 groups were then analyzed by Cox proportional hazards models.
Results: For all breeds, instantaneous risk of death for dogs in overweight body condition was
greater than those in normal body condition throughout the age range studied, with hazard
ratios ranging from 1.35 (99.79% confidence interval [CI] 1.05-1.73) for German Shepherd dog
to 2.86 (99.79% CI 2.14-3.83) for Yorkshire Terrier. In all breeds, median life span was shorter in
overweight compared with normal weight dogs, with the difference being greatest in Yorkshire
Terriers (overweight: 13.7 years, 99.79% CI 13.3-14.2; normal: 16.2 years, 99.79% CI
15.7-16.5) and least in German Shepherd dogs (overweight: 12.1 years, 99.79% CI 11.8-12.4;
normal: 12.5 years, 99.79% CI 12.2-12.9).
Conclusions and Clinical Importance: Veterinary professionals should consider promoting
healthy body condition for dogs, particularly from midlife onward.
KEYWORDS
canine, longevity, nutrition, obesity, survival
1|INTRODUCTION
Obesity is characterized by an expansion of white adipose tissue
(WAT)
1
and is now a major health concern in pet dogs,
1
with recent
evidence suggesting a rapidly increasing prevalence.
2
Dogs that are
overweight or have obesity are at increased risk of developing a range
of chronic diseases including orthopedic diseases, diabetes mellitus,
and certain types of neoplasia.
1,3
Metabolic derangements,
4,5
func-
tional impairment (most notably respiratory, cardiovascular, and renal
function),
6–8
and adverse effects on quality of life also occur.
9
Parallels
exist between canine and human obesity because both are outbred
species that share a similar environment,
1
and similar disease associa-
tions are seen including diabetes mellitus, cardiovascular disease, and
hypertension.
10
As such, both the international medical and veterinary
communities have advised formally classifying obesity as a disease.
11
The expansion of WAT causes secondary disease in 2 ways: through
the “mechanical”impact of increased tissue mass or volume on func-
tion and through the effects of perturbed endocrine function.
1
Both
Abbreviations: BCS, body condition score; CEM, coarsened exact matching; CI,
confidence interval; HR, hazard ratio; PH, proportional hazards; WAT, white adi-
pose tissue.
Received: 1 May 2018 Accepted: 24 October 2018
DOI: 10.1111/jvim.15367
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited and is not used for commercial purposes.
© 2018 The Authors. Journal of Veterinary Internal Medicine published by Wiley Periodicals, Inc. on behalf of the American College of Veterinary Internal Medicine.
J Vet Intern Med. 2019;33:89–99. wileyonlinelibrary.com/journal/jvim 89
pro-inflammatory cytokines and acute phase proteins are produced by
WAT, and both their tissue expression and circulating concentration
are altered by obesity in humans and dogs.
12,13
The chronic low-grade
systemic inflammation that results is thought to provide the link
among obesity, insulin resistance, and the metabolic syndrome.
12
In addition to increasing disease risk and causing functional
impairment, having an overweight body condition increases mortality
risk in humans worldwide.
14
All-cause mortality is least in adults with
a body mass index of 20.0-25.0 and increases significantly and incre-
mentally throughout the overweight range.
14
In veterinary studies,
there are negative associations between life span and both under-
weight and obese body condition in cats from a single veterinary prac-
tice in Sydney, Australia,
15
and evidence for overweight condition
having an adverse effect on life span effects in a lifelong feeding study
involving a colony of Labrador Retriever dogs.
16–19
In this latter study,
dogs were paired, with 1 dog in each pair being fed ad libitum,
whereas the other dog was fed 25% less food than its pair-mate from
8 weeks of age until death. Ad-libitum-fed dogs had a greater body
condition and a shorter median life span than dogs of the restricted-
feeding group.
17
Although this suggests a possible association
between overweight condition and shortened life span in dogs main-
tained in a controlled colony environment, to date, similar effects have
not been studied in client-owned domesticated dogs. Therefore, the
aim of the current study was to explore possible associations between
body condition and life span using a large database of veterinary
health records from pet dogs in North America.
2|METHODS
2.1 |Study design
This was a retrospective case-control study to investigate longevity in
dogs, utilizing demographic, geographic, and clinical data from dogs
registered with a North American veterinary hospital network
(BANFIELD Pet Hospitals).
2.2 |Data extraction and study population
The network comprised 900 veterinary hospitals located predomi-
nantly in the United States (BANFIELD Pet Hospitals), which have
electronic records dating back to 1994. All medical notes from these
records were anonymized by removing client-identifying details and
then stored in an object-related database management system (Oracle
11g release 2, Oracle Corporation, Redwood Shores, California), here-
after referred to as the “records database.”Available records included
those from April 1994 to September 2015. Data were extracted for
purebred individuals from 12 of the most popular breeds representing
the 5 size classes defined by similarities in patterns of growth.
20
The
breeds studied were American Cocker Spaniel, Beagle, Boxer, Chihua-
hua, Dachshund, German Shepherd dog, Golden Retriever, Labrador
Retriever, Pit Bull Terrier type, Pomeranian, Shih Tzu, and Yorkshire
Terrier. The data extracted included demographic (breed, sex, neuter
status, and date of birth) and geographic (latitude and longitude of the
owner's zip code) variables, plus data collected during in-clinic visits
(date of visit, bodyweight, and if available body condition), and date of
death. Pedigree status and date of birth are both owner-reported
parameters and were not verified by the veterinary staff.
2.3 |Eligibility criteria
Dogs were eligible for inclusion when they had at least 1 “in-clinic”
visit (defined as an appointment when both the owner and dog were
in attendance), were between 6.5 and 8.5 years, and whose veterinary
care had not ceased (eg, because of death or moving to a different
veterinary practice) before 9.5 years. In this respect, there had to be
some contact with the owner after this time, for example, an in-clinic
visit or a phone consultation about the dog. This was necessary so as
to minimize any possible influence of life-threatening disease on the
body condition assessment, as is customary in similar human studies
comparing the association between overweight status and mortality.
14
In addition, dogs had to be neutered and from 1 of the 12 most com-
mon breeds in the database (see above). Because most dogs were
neutered before 2 years, only data from visits after this age were used
in modeling studies to ensure that neuter status would not change
during follow-up. Furthermore, for the group-matching process (see
below), a single in-clinic visit was chosen for each dog as the represen-
tative visit, and this was the 1 that was closest to 7.5 year. This
ensured that each dog was only included once during matching.
2.4 |Age, date of birth, and date of death
The age of the dog at each visit was calculated from the visit date and
the date of birth of the dog. Date of birth is a field within the com-
puter electronic records and must be recorded for all dogs; the field is
completed at the time the dog is registered with the practice, based
on information provided by the owner. Date of death is also a field
within the computer electronic records and was completed when dogs
died or were euthanized, along with the reason for death. If the eutha-
nasia is conducted by a veterinarian at the practice, the field is manu-
ally completed. Neither the date of birth nor date of death fields are
verified for accuracy. For dogs with a recorded death date, life span
was calculated from date of birth to date of death; where no date of
death was not recorded, survival data were censored at the date of
the last contact (clinic visit or phone consultation).
2.5 |Body condition assessment
Before 2010, body condition was assessed by a subjective 3-category
classification (“thin,”“normal,”or “heavy”). After 2010, a 5-category
body condition score (BCS) was used, based on visual characteristics
and palpation as previously described.
3
To ensure consistency
between the pre-2010 body condition categories and post-2010 BCS
data, the 5 category BCS was mapped to the 3-category classification
with the same approach as that used in a previous study.
20
Briefly, the
“very thin”and ‘thin’categories were mapped to the pre-2010 “thin”
category, whereas the “overweight”and “markedly obese”categories
were mapped to the pre-2010 “heavy”category. In addition, the
records database contains weight-related diagnoses, which veterinar-
ians can use when classifying the nature of any consultation. The use
90 SALT ET AL.
of these diagnoses was also examined, and if it did not agree with the
body condition assessment (eg, dog assigned a normal body condition,
but given a diagnosis of “thin”), the body condition assessment was
altered to bring it in line with the stated diagnosis.
One further issue for pre-2013 data was that the body condition
field defaulted to “normal”if a body condition category was not
entered. An extrapolation process was used to correct errors arising
from this issue, where a non-default body condition assessment either
preceded or followed a default body condition assessment, the default
assessment was changed to the value of the non-default assessment
provided that the bodyweight of the dog had remained within 5%
between visits. The 5% rule was used because changes in body-
weight of >5% are typically required for changes in BCS to be seen.
21
Body condition data were used to produce 2 groups of dogs,
“normal body condition”and “overweight body condition,”that were
matched on sex, visit age, visit year, latitude, and longitude (see
below). The “overweight body condition”group comprised dogs with
a body condition category of “heavy”at every visit between 5.5 and
9.5 years. The “normal body condition”group comprised dogs whose
body condition was never classified as “thin”or “heavy,”and whose
body condition was classified as “normal”between 5.5 and 9.5 years.
2.6 |Data handling and statistical analysis
Six substantial data cleaning steps were used to ensure both eligibility
criteria were met and data were accurate and reliable (Figure 1). First,
dogs younger than 5.5 years or older than 9.5 years at their visit were
excluded to ensure the selection of middle-aged dogs and to maintain
a balance between numbers of dogs and knowing with certainty that
dogs were still alive at a specific age. Second, outlying visits with
extreme ages (which might have been keyed in by mistake) were
removed by a method based on box and whisker statistics for skewed
data.
22
Third, groups of dogs in overweight and normal body condition
were selected (as described above) to create a single dataset for
matching purposes. Fourth, dogs whose veterinary care ceased before
9.5 years, either because of death, euthanasia, or moving to a differ-
ent veterinary practice were excluded, and the in-clinic visit which
was closest to 7.5 years in age was chosen as the single representa-
tive visit for the subsequent matching process, ensuring that dogs
with multiple visits between 6.5 and 8.5 years were only included
once. Fifth, dogs listed as sexually intact were removed given their rel-
ative paucity within the dataset. Finally, to mitigate any possible lack
of balance between groups, a “statistical matching”technique was
applied to all 12 data subsets, whereby normal and overweight groups
were matched on sex, visit year, or visit age by the coarsened exact
matching (CEM) method,
23
using a bespoke package (Package “cem,”
version 1.1.17, Iacus SM) within an open-source statistical software
environment (R, version 3.2.0, R Foundation for Statistical Computing,
Vienna, Austria). This method temporarily coarsens the data and then
finds exact matches for dogs in the 2 groups. Each observed variable
is coarsened into meaningful groups (eg, using age groups instead of
exact birth dates). Then, visits with the same values for all the coars-
ened variables are placed in a single stratum. Strata without at least
1“normal”and 1 “overweight”visit are dropped. Only the original un-
coarsened values of the matched data are retained. It should be
emphasized that the exact matching procedure is applied to the coars-
ened data to find the matches and discard unmatched units before the
un-coarsened values of the matched data are returned. Therefore, simi-
lar to other matching techniques, CEM does not produce a 1:1 ratio of
normal to overweight dogs; to do so might lead to a large number of
observations being discarded, leading to reduced statistical power. Sup-
porting Information Table S1 outlines the improvement in balance,
using the L1 norm for each of the breeds.
24
After matching, the median
number of dogs with a death date was 911 across the 12 breeds.
Given that the records database did not include death dates for
all dogs, the data were right censored. As a result, comparisons of sur-
vival between normal and overweight dogs were made by generating
Cox proportional hazards (PH) models given their ability to deal with
left and right censored data. A bespoke package (Package “survival,”
version 2.38-3, Therneu TM) of a statistical software environment (R,
version 3.2.0) was used to produce models for male and female dogs,
and survival predictions from the Cox PH models were used to com-
pare the median life span of normal and overweight dogs. The PH
assumption holds if the hazard functions for 2 individuals remain pro-
portional over time, that is, constant relative hazard. This assumption
was tested for all explanatory variables (sex, BCS, visit year, and
visit age) using weighted residuals.
25
When body condition violated
the PH assumption, it was managed by adding a time-dependent body
condition variable. This indicator variable depended on the visit age at
which the PH assumption failed, specifically 10.5 (when violation of
PH could not be mitigated), 12.5, or 14.5 years. Stratification was
FIGURE 1 Summary of the data cleaning process. Flow diagram
illustrating the data cleaning process to create the final study
population. The number of dogs eligible at each stage is depicted,
where m denotes million(s) and k denotes thousand(s)
SALT ET AL.91
used for instances for which the PH assumption did not hold for sex,
visit year, or visit age. Hazard ratios (HR) and 99.79% confidence
intervals (CI) were calculated for the body condition term in each Cox
PH model. For each HR, the “hazard”was the instantaneous event
rate in an overweight dog compared with a dog in normal body condi-
tion, with the event in question being death. Binomial tests were used
to assess propensity in the direction of any association between body
condition and risk change in all 12 breeds. A Bonferroni adjustment
was used to correct for the effects of multiple testing, with the
adjusted significance level being P= .002 (eg, 0.05/24) for 2-sided
analyses.
Median life span was calculated for each breed using predictions
from the Cox PH models, and these were stratified both by sex (male
versus female) and for both normal and overweight groups stratified by
sex. We tested the hypothesis that there would be a difference in
median life span between dogs with normal body condition and over-
weight body condition. The percentage difference in median life span for
the overweight group relative to the normal group was compared for all
12breedsandbothmaleandfemale.The effect of body condition on life
span was tested by the Cox PH model for each of the 12 breeds by the
same open-source statistical software environment (R, version 3.2.0). A
Bonferroni adjustment was again used to correct for the effects of multi-
ple testing, with the adjusted significance level being P= .002 (eg,
0.05/24) for 2-sided analyses. Binomial tests were again used to assess
trends in the direction of any association between body condition and
survival across all 12 breeds. For example, where no underlying trend
existed, the overweight group would be expected to have a 50% chance
of having a longer median life span than the normal group and a 50%
chance of having a shorter median life span.
3|RESULTS
3.1 |Final study population
Before applying eligibility criteria and performing matching, the
records database contained 5.4 ×10
6
visits available from 1.2 ×10
6
dogs (Figure 1). After filtering the dataset and matching, the total
number of dogs available was 50 787, and date of death was recorded
in 14 316 of these (28.2%). The number of dogs available for each
breed is shown in Table 1. After data cleaning, the median number of
dogs available per breed was 3865 (range 1273-11 867), whereas the
median number of dogs with a known death date was 911 (range
328-4520).
3.2 |Survival predictions and hazards ratios
Body condition score violated the PH assumption and required the
introduction of a time-dependent body condition variable for 8 of
12 breeds (American Cocker Spaniel, Beagle, Chihuahua, Dachshund,
Labrador Retriever, Pomeranian, Shih Tzu, and Yorkshire Terrier). For
Labrador Retriever and Shih Tzu, the PH violation occurred at 12.5
and 10.5 years, respectively. The PH violation could not be reduced
for Shih Tzu. For other breeds, violation occurred at 14.5 years. Sur-
vival probability predictions for male and female dogs of all 12 breeds
TABLE 1 Details of the final study population, stratified according to breed, sex, and body condition status
All dogs Male dogs Female dogs
Breed Size class Total Normal
1
Overweight
2
Total Normal
1
Overweight
2
Total Normal
1
Overweight
2
Chihuahua I 6306 (1098) 2460 (210) 3846 (888) 2977 (524) 1227 (109) 1750 (415) 3329 (574) 1233 (101) 2096 (473)
Pomeranian I 2297 (515) 1123 (140) 1174 (375) 1280 (281) 623 (76) 657 (205) 1017 (234) 500 (64) 517 (170)
Yorkshire Terrier I 4065 (574) 2540 (212) 1525 (362) 2287 (313) 1447 (112) 840 (201) 1778 (261) 1093 (100) 685 (161)
Shih Tzu II 5488 (873) 3329 (355) 2159 (518) 2915 (469) 1733 (179) 1182 (290) 2573 (404) 1596 (176) 977 (228)
American
Cocker Spaniel
III 2997 (949) 927 (179) 2070 (770) 1398 (402) 452 (85) 946 (317) 1599 (547) 475 (94) 1124 (453)
Beagle III 3665 (1095) 703 (106) 2962 (989) 1756 (518) 342 (55) 1414 (463) 1909 (577) 361 (51) 1548 (526)
Dachshund III 4799 (984) 1538 (152) 3261 (832) 2396 (491) 765 (76) 1631 (415) 2403 (493) 773 (76) 1630 (417)
Boxer IV 1659 (718) 807 (264) 852 (454) 740 (315) 348 (109) 392 (206) 919 (403) 459 (155) 460 (248)
Pit Bull IV 1273 (328) 530 (99) 743 (229) 484 (119) 215 (46) 269 (73) 789 (209) 315 (53) 474 (156)
German Shepherd dog V 1811 (729) 833 (262) 978 (467) 777 (309) 383 (122) 394 (187) 1034 (420) 450 (140) 584 (280)
Golden Retriever V 4560 (1933) 876 (242) 3684 (1691) 2166 (940) 407 (117) 1759 (823) 2394 (993) 469 (125) 1925 (868)
Labrador Retriever V 11 867 (4520) 2672 (598) 9195 (3922) 5511 (2194) 1238 (299) 4273 (1895) 6356 (2326) 1434 (299) 4922 (2027)
Total …50 787 (14316) 18 338 (2819) 32 449 (11497) 24 687 (6875) 32 449 (1385) 15 507 (5490) 26 100 (7441) 9158 (1434) 16 942 (6007)
Data reported are total numbers of dogs and dogs with a recorded death age in brackets.
1
Dogs were classified as “normal”when their body condition was recorded as “normal”between 5.5 and 9.5 years and if they
were never recorded as “thin”or “heavy”at any age
2
; dogs were classified as “overweight”when their body condition was recorded as “heavy”at every visit between 5.5 and 9.5 years.
92 SALT ET AL.
FIGURE 2 Survival probability models for male neutered (A) and female spayed (B) Yorkshire Terriers. Middle lines depict the probability of
survival for a dog at 7.5 years age in 2003 (assuming survival to at least 9.5 years), with the upper and lower lines depicting 99.79%
confidence intervals. The survival of dogs in the normal body condition group is shown in red, whereas that of the overweight group is show
in blue
FIGURE 3 Survival probability models for male neutered (A) and female spayed (B) Shih Tzus. Middle lines depict the probability of survival for a
dog at 7.5 years age in 2003 (assuming survival to at least 9.5 years), with the upper and lower lines depicting 99.79% confidence intervals. The
survival of dogs in the normal body condition group is shown in red, whereas that of the overweight group is show in blue
SALT ET AL.93
FIGURE 4 Survival probability models for male neutered (A) and female spayed (B) Dachshunds. Middle lines depict the probability of survival for
a dog at 7.5 years age in 2003 (assuming survival to at least 9.5 years), with the upper and lower lines depicting 99.79% confidence intervals. The
survival of dogs in the normal body condition group is shown in red, whereas that of the overweight group is show in blue
FIGURE 5 Survival probability models for male neutered (A) and female spayed (B) Boxers. Middle lines depict the probability of survival for a
dog at 7.5 years age in 2003 (assuming survival to at least 9.5 years), with the upper and lower lines depicting 99.79% confidence intervals. The
survival of dogs in the normal body condition group is shown in red, whereas that of the overweight group is show in blue
94 SALT ET AL.
were then produced from the Cox PH models; examples for 5 breeds
(Yorkshire Terrier, Shih Tzu, Dachshund, Boxer, and German Shepherd
dog) are depicted in Figures 2–6, whereas survival curves for all other
breeds are included in Supporting Information (Figures S1-S7). For all
12 breeds, the survival probability for dogs in overweight body condi-
tion was less than for dogs in ideal body condition throughout the age
range studied.
Hazard ratios and 99.79% CIs for the body condition term (over-
weight condition relative to normal condition) from the Cox PH
models produced for all 12 breeds are shown in Table 2. The body
condition HRs ranged from 1.35 (99.79% CI 1.05-1.73) for German
Shepherd dog to 2.86 (99.79% CI 2.14-3.83) for Yorkshire Terrier.
Binomial testing confirmed an increase in relative risk of dying for
overweight dogs compared to normal body condition dogs across all
12 breeds (P< .001 for all) at the Bonferroni-corrected 2-sided test
level.
3.3 |Life span of dogs in ideal and overweight body
condition
Median life spans (with multiple testing adjusted CIs) for dogs in over-
weight and normal body condition from the 12 breeds are shown in
Table 3, whereas Figure 7 illustrates the reduction in median life span
for all 12 breeds and both male and female dogs. Binomial testing con-
firmed a shorter survival for overweight dogs of all 12 breeds would
not be expected by chance, indicating the presence of a nonrandom
directional trend (P< .001). The estimated reduction in median life
span for the overweight group relative to the normal group ranged
from 5 months, for male German Shepherd dogs, to 2 years 6 months
for male Yorkshire Terriers (Table 3).
4|DISCUSSION
Our study demonstrates an adverse effect of overweight body condi-
tion on life span in client-owned dogs of a range of breeds, thereby
FIGURE 6 Survival probability models for male neutered (A) and female spayed (B) German Shepherd dogs. Middle lines depict the probability of
survival for a dog at 7.5 years age in 2003 (assuming survival to at least 9.5 years), with the upper and lower lines depicting 99.79% confidence
intervals. The survival of dogs in the normal body condition group is shown in red, whereas that of the overweight group is show in blue
TABLE 2 Hazard ratios for the effect of overweight body condition
on risk of death in pet dogs
Breed Size class
Hazard
ratio 99.79% CI Pvalue
Chihuahua I 2.42 1.87-3.13 <.001
Pomeranian I 2.25 1.62-3.12 <.001
Yorkshire Terrier I 2.86 2.14-3.83 <.001
Shih Tzu II 2.19 1.39-3.45 <.001
American
Cocker Spaniel
III 2.21 1.66-2.93 <.001
Beagle III 2.40 1.69-3.43 <.001
Dachshund III 2.77 2.03-3.79 <.001
Boxer IV 1.62 1.27-2.07 <.001
Pit Bull IV 1.57 1.08-2.29 <.001
German Shepherd V 1.35 1.05-1.73 <.001
Golden Retriever V 1.56 1.26-1.94 <.001
Labrador Retriever V 1.83 1.54-2.17 <.001
Data reported are hazard ratios, 99.79% confidence interval (CI), and asso-
ciated Pvalues for risk of death for dogs in overweight body condition rel-
ative to dogs in normal body condition.
SALT ET AL.95
TABLE 3 Differences in life span between dogs in normal and overweight body condition
Breed Size class
Male dogs Female dogs
Normal
1
Overweight
2
Normal
1
Overweight
2
Chihuahua I 16.0 (15.6, 16.4) 13.9 (13.5, 14.2) 16.1 (15.7, 16.7) 14.0 (13.6, 14.3)
Pomeranian I 15.5 (15.2, 16.3) 13.7 (13.3, 14.1) 15.5 (15.0, 15.9) 13.6 (13.2, 14.0)
Yorkshire Terrier I 16.2 (15.7, 16.5) 13.7 (13.3, 14.2) 15.5 (15.3, 15.7) 13.5 (13.2, 14.0)
Shih Tzu II 14.5 (14.5, 15.3) 13.8 (13.6, 14.3) 14.5 (14.5, 15.4) 13.9 (13.6, 14.3)
American Cocker Spaniel III 14.9 (14.4, 15.6) 13.4 (13.2, 13.6) 14.8 (14.3, 15.4) 13.3 (13.0, 13.4)
Beagle III 15.2 (14.5, 16.1) 13.2 (13.0, 13.5) 15.3 (14.6, 16.2) 13.3 (13.1, 13.6)
Dachshund III 16.4 (15.8, 16.8) 14.1 (13.8, 14.4) 16.4 (15.9, 16.8) 14.1 (13.8, 14.4)
Boxer IV 12.4 (12.2, 12.6) 11.8 (11.5, 12.0) 12.3 (12.1, 12.6) 11.7 (11.4, 11.9)
Pit Bull IV 13.8 (13.3, 14.5) 13.0 (12.5, 13.5) 13.8 (13.3, 14.3) 12.9 (12.6, 13.4)
German Shepherd dog V 12.5 (12.2, 12.9) 12.1 (11.8, 12.4) 13.1 (12.7, 13.5) 12.5 (12.3, 12.8)
Golden Retriever V 13.3 (13.0, 13.6) 12.5 (12.4, 12.7) 13.5 (13.1, 13.8) 12.7 (12.6, 12.9)
Labrador Retriever V 13.3 (12.8, 13.6) 12.7 (12.6, 12.8) 13.6 (13.2, 14.0) 13.0 (12.9, 13.2)
Data reported are median (99.79% confidence interval) life span for male and female dogs of the 12 breeds in the study.
1
Dogs were classified as ‘normal’
when their body condition was recorded as “normal”between 5.5 and 9.5 years and if they were never recorded as “thin”or “heavy”at any age
2
; dogs
were classified as “overweight”when their body condition was recorded as “heavy”at every visit between 5.5 and 9.5 years.
FIGURE 7 Estimated effect of overweight body condition on life span in male (A) and female (B) dogs. The 12 breeds studied have been ordered
by size class,
20
with columns representing the median, for overweight dogs compared with dogs in normal body condition. The columns indicate
medians of 12 breeds and both sexes (MN, male neutered; FS, female spayed). Breeds have been ordered by size class, starting with small breeds
96 SALT ET AL.
extending the findings from an earlier colony study in Labrador
Retrievers.
16–19
These results emphasize the need for veterinarians to
implement steps to prevent the development of obesity in dogs under
their care. Specifically, veterinarians could use the study findings in
discussions with owners of new puppies, to highlight the risk that
overweight status poses to health and the need for prevention. The
findings could also be used in discussions with owners of already-
obese dogs to convince them of the need to implement a controlled
weight loss program.
Overweight body condition was associated with a shorter life
span in all 12 breeds studied, but the magnitude of the effect varied
being least for large-breed dogs (eg, 5 months) and greatest for dogs
of the smallest breed (eg, greater than 2 years in dogs from size
class I). Hazards ratios for estimated risk of death in overweight dogs
relative to those in normal body condition mirrored these findings.
The reason for these results is unclear, but 1 possibility would be a
difference in natural prevalence of the various obesity-associated dis-
eases among the breeds studied. For example, orthopedic diseases
such as osteoarthritis are more common in larger breeds.
26
Alterna-
tively, individual breed characteristics might influence the impact of
any functional impairments that arise from obesity, for example,
metabolic dysfunction or impaired quality of life.
5–9,18
Whatever the
reasons, the importance of this life span effect should not be ignored.
Indeed, even in the breeds for which the effect was least pronounced,
such shortening is likely to be important because most owners would
wish to ensure that their dog lives a long and healthy life.
In the authors' opinion, although only 12 breeds were studied, the
fact that the negative association between overweight status and life
span was apparent in all breeds implies that this same effect is likely
to be present in any breed. Nonetheless, such extrapolations should
be made cautiously until studies including a wider breed range are
undertaken. In a similar manner, the inclusion of neutered dogs only
and of dogs between 5.5 and 9.5 years means that extrapolation to
sexually intact or younger dogs should also be made cautiously.
Given that the study was retrospective and observational, it was
not possible to determine the reasons for the association between
overweight body condition and life span, and causality cannot neces-
sarily be assumed. One possibility is that overweight status is only
indirectly associated with life span, for example, by predisposing to
diseases that are themselves fatal (eg, neoplasia).
3,27,28
Alternatively,
overweight body condition might exacerbate other diseases that have
a negative impact on health (eg, osteoarthritis), thereby prompting a
decision for euthanasia. Indeed, in the previous lifelong feeding study
of dogs, chronic diseases including various types of neoplasia and
osteoarthritis were diagnosed at an earlier age in the ad libitum-fed
group that were overweight, compared with the calorie-restricted
group that remained in ideal body condition.
17
Furthermore, obese
dogs have a poorer quality of life than dogs in ideal condition.
9
A 2nd
possibility for the life span difference between overweight and ideal
weight dogs is that weight status is a proxy measure for caloric intake.
In this respect, calorie restriction without malnutrition can increase
longevity in a wide variety of species including spiders, fish, inverte-
brates, and rodents.
29,30
Furthermore, biomarkers associated with lon-
gevity (eg, fasting insulin concentration and body temperature) were
decreased by prolonged calorie restriction in human beings.
31
Given
that, in our study, information on concurrent disease, diet, and energy
intake were not assessed, further work would be required to deter-
mine the reason for the difference in life span between overweight
dogs and those in ideal condition.
In analyzing study data, we chose an approach involving matching
rather than, for example, using PH models with weight status as the
variable of interest, and all other covariates considered as potential
confounders. The main disadvantage of using matching methods is
that they can be less “powerful”and, therefore, might increase the
chances of type II statistical error.
32
However, this was arguably not a
concern in the current study because significant effects were demon-
strated even after applying a Bonferroni correction. The main advan-
tage of using a matching method is that it can better deal with
observational data that are unbalanced in one or more covariates that
themselves might be associated with the dependent variable of inter-
est. For example, in a situation where 1 of the covariates is a causal
variable in its own right but is also correlated with the independent
variable of interest, a model without matching can struggle to sepa-
rate the effect of the independent variable of interest from that of the
covariate. Furthermore, even when a significant effect of the indepen-
dent variable of interest is found, it might simply be related to its asso-
ciation with the covariate. Matching methods can separate these
effects thereby avoiding a “second-hand”association of the indepen-
dent variable of interest with a noise variable.
33
Therefore, although
other methods could have been considered, the advantages of the
method chosen outweighed the disadvantages.
A strength of our study is its size in that, by using a large veterinary
hospital network, data from over 50 000 dogs were available for assess-
ment even after data cleaning. This enabled differences in life span to be
identified in male and female neutered dogs in all 12 breeds. A further
advantage of the approach taken was the fact that client-owned dogs
living in a home environment could be studied and, as such, results are
likely to be generalizable to the general pet dog population. However, a
disadvantage of the approach is the fact that data were collected by
many veterinary professionals in many locations, meaning potential dis-
crepancies in assessment of body condition. Furthermore, data were not
specifically collected for this scientific study, rather data were gathered
by many veterinarians for clinical reasons, and there might have been
errors or omissions in terms of data inputting.
Several other study limitations should also be acknowledged.
First, the study was retrospective with data collected over a period of
20 years. As well as both the prevalence and awareness of body con-
dition during this time frame, it is likely that there were numerous
changes in practice protocols, expertise, technology, and data record-
ing. Such factors are likely to impact on the reliability of the study
data. Moreover, some information that owners provided, such as
breed and date of birth, were not verified for accuracy at the time it
was recorded, for instance by examining pedigree records. Further-
more, owners might not have known the exact date of birth for their
dog, for example, if it had been re-homed. There might also have been
inaccuracies with date of death when this was owner-reported (if the
dog died at home), because some owners might understandably have
delayed informing the practice until a time that they could cope with
such a difficult conversation. It is also possible that veterinary
practice staff might have made errors when entering data into the
SALT ET AL.97
records database. To mitigate such limitations, extensive data cleaning
was undertaken, with exclusion of any data thought to be unreliable.
One consequence of this cautious approach is the reduction of avail-
able data (Figure 1), meaning that the final dataset might be less repre-
sentative of the original study population, and the number of breeds
where sufficient data were available for analysis is reduced. That said,
the original datasets were large enough to accommodate this.
A 2nd limitation is that we cannot be certain whether or not the
association between body condition and survival is truly related to a
shortened natural life span. Survival studies are difficult to conduct in
companion animals because, unlike in humans, pet dogs can be eutha-
nized rather than allowed to die from natural causes. The reasons for
euthanasia and the timing of the decision are variable with many fac-
tors involved. Decisions might relate to animal factors such as the
development of disease (not least if the disease is a terminal one),
presence of multiple concurrent diseases, perceived poor quality of
life, aggression, or other behavioral disorders. A final possible reason
for euthanasia is financial, whereby the costs of pet ownership and,
sometimes, costs of treatment might sway the decision for euthanasia.
In a recent review, the financial impact of a dog having obesity and
obesity-related disease was estimated to be approximately $2000 per
year.
34
Given that the current study was retrospective, the reasons
for death or euthanasia were not always recorded.
A 3rd study limitation was the fact that a different approach was
used to assess body condition at the start of the study compared with
the end. Initially, a 3-category system was used, which was replaced by
a more conventional 5-category system in 2010. To maximize the avail-
able study data, 5-point scores used after 2010 were mapped onto the
3-category scores used before 2010. This approach has been used in a
previous study,
20
and because it was straightforward (involving merg-
ing categories), it is unlikely that errors arose at this stage. That said, it
is unclear whether the categories were truly equivalent. A 2nd concern
regarding body condition was that it was not a mandatory field within
the computer records and, if not completed, the system automatically
recorded the body condition as “normal.”It could be argued that failure
to complete this field is more likely to occur when the dog already has
a normal body condition than when the body condition is abnormal
(overweight or underweight). It cannot be guaranteed that this would
always be the case given the relative infrequency with which veterinar-
ians spontaneously record body condition
35
or use the terms over-
weight and obese
36
in electronic records. Therefore, to mitigate errors
arising at this stage, an extrapolation process was used whereby all
default values were compared with assessments that immediately pre-
ceded or followed them. Furthermore, body condition assessments
were cross-checked for consistency against diagnosis categories that
the veterinarian had recorded (eg, when the veterinarian recorded the
diagnosis as underweight, overweight, or obesity) and corrected if they
deviated. Although it is likely that these stringent data cleaning
methods improved the accuracy of the final dataset, some uncertainty
over accuracy remains. That said, because most errors would involve
dogs with abnormal body condition being erroneously classified as nor-
mal rather than the other way around, the effect would be to decrease
differences between groups rather than increase them. Further studies
should be considered, involving similarly large datasets to confirm the
findings of the current study.
A 4th study limitation was the fact that the decision about whether
dogs were selected for the overweight and normal groups was made
when dogs were middle aged (between 5.5 and 9.5 years), rather than
earlier in life. As a result, the kinetics of weight change throughout life
could not be assessed, as they had been in a previous cohort study.
16–19
This was necessary because selecting dogs earlier would have meant
fewer dogs with usable data for the study. First, younger dogs are gener-
ally healthier than middle-aged dogs (because chronic diseases typically
manifest later in life), hence they visit the veterinarian less frequently.
Second, it is common to have notable attrition from owners moving
practices, meaning far fewer selected dogs would have had a recorded
death dates available for analysis. However, the disadvantage of this
approach is that the impact of timing, speed, and duration of weight gain
could not be examined; for example, whether weight gain early in life
has more impact than weight gain later in life. Likewise, we did not
examine the effect of any methods used to achieve weight loss or pre-
vent weight gain on life span. Moreover, as only 2 groups were com-
pared (normal condition and overweight condition), we did not consider
the impact of magnitude of excess weight. Therefore, additional studies
would be required to examine these aspects in more detail.
5|CONCLUSIONS
There is a negative association between overweight body condition
and life span in client-owned dogs from 12 common breeds. These
findings emphasize the need for veterinary professionals to promote a
healthy body condition for dogs, particularly in midlife onward.
ACKNOWLEDGMENTS
The authors acknowledge the assistance of Emi Saito (BANFIELD Pet
Hospitals) for help with veterinary interpretation and provision of
information regarding clinical practices at BANFIELD Pet Hospitals.
The data used in the study were gathered from the BANFIELD Pet
Hospitals, and data analysis was conducted at the WALTHAM Centre
for Pet Nutrition, Melton Mowbray, United Kingdom. Preliminary
findings for part of the dataset used in this study were presented at
the WALTHAM International Nutritional Sciences Symposium 2013,
October 1-4, Portland.
CONFLICT OF INTEREST DECLARATION
Carina Salt, Penelope J. Morris, and Derek Wilson are employees of
WALTHAM, whereas Elizabeth M. Lund was an employee of BAN-
FIELD Pet Hospitals at the time the study was conducted. Both com-
panies both are owned by Mars Inc. Alexander J. German is an
employee of the University of Liverpool, but his post is financially sup-
ported by Royal Canin, which is also owned by Mars Petcare.
Alexander J. German has also received financial remuneration for pro-
viding educational material, speaking at conferences, and consultancy
work for Mars Petcare; all such remuneration has been for projects
unrelated to the work reported in this article. The funder, Mars, did
not have any role in the study design, data collection, data analysis,
results, or preparation of the manuscript.
98 SALT ET AL.
OFF-LABEL ANTIMICROBIAL DECLARATION
Authors declare no off-label use of antimicrobials.
INSTITUTIONAL ANIMAL CARE AND USE COMMITTEE
(IACUC) OR OTHER APPROVAL DECLARATION
The study protocol was approved by the WALTHAM ethical review
committee, and owners of all participating dogs gave consent for data
to be used.
HUMAN ETHICS APPROVAL DECLARATION
The study protocol was approved by the WALTHAM ethical review
committee, and all owners gave consent for data to be used.
ORCID
Alexander J. German https://orcid.org/0000-0002-3017-7988
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SUPPORTING INFORMATION
Additional supporting information may be found online in the Sup-
porting Information section at the end of the article.
How to cite this article: Salt C, Morris PJ, Wilson D,
Lund EM, German AJ. Association between life span and body
condition in neutered client-owned dogs. J Vet Intern Med.
2019;33:89–99. https://doi.org/10.1111/jvim.15367
SALT ET AL.99
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