Prevalence of mortality during the rst 3 wk after
birth in the canine species is one of the highest among
domestic animals: around 17% of puppies die during
this perinatal period (stillbirth and neonatal mortal-
ity; Potkay and Bacher, 1977; Gill, 2001; Nielen et al.,
2001; Indrebø et al., 2007). Mortality risk rst depends
on intrauterine growth, with puppies of the lowest
weight at birth being at higher risk of neonatal death
compared with littermates (Grundy, 2006), as ob-
served in kittens and piglets (Lawler, 2008; Devillers
et al., 2011). In large-sized breeds, puppies dying dur-
ing the rst week after birth had over 100 g lower birth
weight than puppies still alive at 8 wk (Indrebø et al.,
2007). However, birth weight thresholds for the differ-
ent breed sizes dening puppies at risk of death, requir-
ing more intensive nursing, as well as factors impact-
ing birth weight are not dened to date.
After birth, at an early stage of life, canine new-
borns depend entirely on colostrum intake. This spe-
cic mammary secretion provides puppies with not
Differential impact of birth weight and early growth on
neonatal mortality in puppies1,2
H. Mila,*†‡ A. Grellet,‡ A. Feugier,‡ and S. Chastant-Maillard*†3
*Université de Toulouse, INP, ENVT, UMR 1225, IHAP, F-31076, 23 Chemin des Capelles,
31300 Toulouse, France; †INRA, UMR1225, IHAP, F-31076, 23 Chemin des Capelles,
31300 Toulouse, France; and ‡Royal Canin, 650 Avenue de la Petite Camargue, Aimargues, France
ABSTRACT: Breeding kennels face a high rate of
neonatal mortality, on which the impact of nutrition
remains to be determined. This study was designed
to evaluate the impact of birth weight (reecting
intrauterine growth) and early growth rate (reecting
colostrum intake) on risk of neonatal mortality in pup-
pies and to determine the critical thresholds of both
parameters. Puppies from various breeds were weighed
at birth (n = 514) and at 2 d of age, and the growth rate
over that period (early growth rate) was calculated for
all survivors (n = 477). Linear mixed models evalu-
ated the effect of birth weight on mortality between
birth and 2 d of age and the effect of both birth weight
and early growth rate on mortality between 2 and 21 d
of age. Birth weight was inuenced by litter size (P =
0.003), with more low-birth-weight puppies (the light-
est 25% within a breed size) in large litters compared
with smaller litters. Mortality over the rst 2 d after
birth was associated with birth weight (P < 0.001),
with 81.1% of dying puppies characterized by a low
birth weight. Mortality between 2 and 21 d of age was
not related to birth weight but was found to be associ-
ated with early growth rate (P < 0.001), with higher
risk of death in puppies with growth rate at or below
–4% after the rst 2 d of life. This study demonstrates
the differential effect of intrauterine nutrition impact-
ing mortality during the rst 2 d of life and that of
colostrum intake impacting mortality until 21 d of life.
Birth weight and early growth rate thresholds provid-
ed in this study allow identication of puppies at risk,
whereby provision can be made for adequate nursing
to increase their chances to survive.
Key words: birth weight, colostrum intake, litter size, mortality, puppy, weight change
© 2015 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2015.93:4436–4442
1This study was partially funded by Royal Canin SAS (grant
number R3789 1/02/2012). We would like to thank the owner of
the kennel for his contribution to this work and Mr. Adrian Watson
for the English revision of the manuscript. Our thanks extend to
graduate and undergraduate students of Ecole Nationale Vétérinaire
de Toulouse for the crucial help in data collection.
H.M., A.G., and A.F. are employees of Royal Canin SAS.
S.C.M. has no conicts of interest to declare.
3Corresponding author: email@example.com
Received January 30, 2015.
Accepted March 17, 2015.
Published September 8, 2015
Birth weight and early growth in puppies 4437
only nutrients but also hormones, growth factors, and
passive immunity. All of mentioned components are
indispensable for the puppy’s life, as hypoglycemia
and hypothermia, together with infectious diseases,
are recognized as the major causes of neonatal mor-
tality in puppies (Indrebø et al., 2007; Münnich and
Küchenmeister, 2014). Whereas energy intake covers
the basal metabolic needs, ensuring thermoregulation
and body growth, immunoglobulin acquisition early af-
ter birth provides the only immune protection during
the rst weeks. In piglets, early weight gain is used to
evaluate the amount of colostrum ingested and eventual
risk of neonatal death, as piglets dying before wean-
ing gained less weight between birth and 24 h of life
(Devillers et al., 2011). Although a 10% loss of birth
weight is commonly considered to be physiological in
2-d-old puppies (Grundy, 2006), the real impact of early
weight change on canine neonatal mortality is unknown.
The aim of this study was to evaluate the relation-
ship between neonatal mortality in puppies and both
birth weight and growth rate during the rst 2 d of
life (early growth rate). The critical thresholds of birth
weight and early growth rate dening puppies at high-
er risk of death were also determined.
MATERIALS AND METHODS
The protocol was reviewed and approved by the
Royal Canin Internal Ethics Committee (AF/20140704).
The experiment was performed on all puppies
born alive from 100 bitches within 1 breeding ken-
nel. Ninety-eight bitches were multiparous. Between 1
wk before parturition and the end of lactation, bitches
were housed in a single box (2–4 m2) and fed a dry
balanced diet for growing dogs (Starter; Royal Canin,
Aimargues, France) ad libitum. Whelping boxes
were heated (continuous under oor heating plus a
heat infrared lamp during the rst 3–5 d after whelp-
ing), so that the stable temperature of 28 to 30°C at
the ground level was assured. None of the whelpings
were assisted, no cesarean section was performed, and
no puppies were hand reared during the experiment.
After whelping, the total number of puppies born
within a litter (born alive or dead [stillborn]), den-
ing litter size, was recorded. Each puppy was identi-
ed by a colored woolen collar and its sex, breed, and
the age of its dam were recorded. Within the rst 8 h
after birth, puppies were weighed using a calibrated
analytical scale in 1-g increments (Fisher Scientic
International Inc., Hampton, NH). At 48 h of life, mor-
tality was registered and all surviving puppies were
weighed again. Their growth rate over the rst 2 d of
life was calculated [(weight at 2 d – weight at birth)/
weight at birth × 100%]. Mortality between 2 and 21 d
was then registered.
Statistical analyses were performed with the
Statistical Analysis Systems statistical software pack-
age version 9.3 (SAS Inst. Inc., Cary, NC). The nor-
mality was evaluated with the Shapiro–Wilk test.
Univariable statistical analyses were performed with
the Kruskal–Wallis test.
Dams were classied into young (≤6 yr of age)
and old (>6 yr of age). Depending on adult weight,
neonates and their dams were classied into small
breed dogs (<15 kg), medium breed dogs (15–25 kg),
and large breed dogs (>25 kg; Table 1). Because birth
weight and litter size vary among breeds (Grundy,
2006), birth weight and litter size values were classi-
ed into quartiles, separately, for small, medium, and
large breed puppies (Table 2). The rst quartile (Q1)
represents the lowest 25% of registered values, the
second and third quartiles (Q2 and Q3, respectively)
represent 25% of values below and above the median,
and fourth quartile (Q4) represents the highest 25% of
First, a generalized linear mixed model (GLIMMIX
procedure) with birth weight as an outcome (trans-
Table 1. Breed size classication according to the
adult BW and numbers of litters and puppies included
in the study
Breed size Breed
Small, <15 kg Bichon Frise 4 15
Bichon Maltese 7 40
Jack Russell Terrier 4 12
Lhasa Apso 11 50
Pomeranian 1 4
Poodle 8 28
Shih Tzu 6 32
German Spitz 3 11
Scottish Terrier 1 1
West Highland White
Yorkshire Terrier 2 15
Medium, 15–25 kg Cocker Spaniel 17 90
Large, >25 kg Boxer 1 8
Labrador 11 58
German Shepherd 2 11
Golden Retriever 15 104
Total 100 514
Mila et al.
formation in ordinal outcome) was used to assess the
following xed effects: sex of the puppy (male or fe-
male), litter size, and age of the dam (young or old).
Subsequently, a GLIMMIX procedure with mortality
between birth and 2 d of age as a binary outcome (logit
transformation) was used to assess the following xed
effects: sex of the puppy, litter size, age of the dam,
breed size, and birth weight.
Second, a linear mixed model (MIXED proce-
dure) was performed to determine the variables affect-
ing growth rate between birth and 2 d of age. As re-
siduals of this multivariable model were not normally
distributed, a nonparametric analysis was performed
(rank transformation of the outcome). This model in-
cluded, as xed effects, sex, litter size, age of the dam,
breed size (small, medium, or large), and birth weight.
Subsequently, a GLIMMIX procedure with mortality
between 2 and 21 d of age as a binary outcome (logit
transformation) was used to assess the following xed
effects: sex, litter size, age of the dam, breed size, and
birth weight. Moreover, the effect of growth rate was
added as a covariate. In all multivariable models, litter
was modeled as a random effect.
A receiver operating characteristic curve was drawn
based on the result of the logistic model on mortality
between 2 and 21 d of age. The Hosmer and Lemeshow
goodness-of-t test permitted assessment of the quality
of this model. The best cutoff from the model for high
and low mortality risk populations was dened based
on Youden’s index. Differences were considered sig-
nicant at P < 0.05. Quantitative data are presented as
medians with interquartile range (IQR).
The median age of the 100 bitches included in the
study was 6 yr (IQR: 4 to 7 yr) and median number
of puppies born per litter (litter size) was 5 (IQR: 4 to
7). From a total of 532 puppies born, 18 were stillborn
(3.4%). The sex ratio in 514 puppies born alive was 1.2
(280 males and 234 females). Birth weight varied from
80 to 604 g. Both birth weight and litter size were sig-
nicantly different between small, medium, and large
breeds (P < 0.001 in both models; Table 2). Weight
at birth was signicantly inuenced by litter size (P =
0.003) and litter effect (P < 0.001; Fig. 1). Among all
puppies belonging to large litters (quartile 4), 37.1%
(36/97) were of low birth weight (quartile 1) and 12.4%
(12/97) of high birth weight (quartile 4), whereas pro-
portions in small-sized litters (quartile 1) were 8.6%
(7/81) of low birth weight and 50.6% (41/81) of high
birth weight puppies. None of the other factors tested
in this model (sex of the puppy and age of the dam) has
any inuence on puppy birth weight.
A total of 20.6% (106/514) of live-born pup-
pies died between birth and 21 d of age, with 34.9%
(37/106) of deaths occurring during the rst 2 d after
birth. Mortality between birth and 2 d of age was in-
uenced by birth weight (P < 0.001; Table 3; Fig. 2)
and tended to be inuenced by breed size and litter ef-
fect (P = 0.09 and P = 0.06, respectively). Among all
puppies dying within the rst 48 h after birth, 81.1%
(30/37) were of low birth weight (quartile 1). None of
the other factors tested (such as litter size, sex of the
puppy, or age of the dam) had any inuence on mortal-
ity between birth and 2 d of age.
Median growth rate during the rst 48 h of life cal-
culated for 477 puppies still alive at Day 2 was 3.3%
Table 2. Classication of puppies according to birth weight and litter size (514 puppies) depending on breed size
Quartiles of birth weight,1 g Median
Quartiles of litter size,
number of puppies per litter
Q1 Q2 Q3 Q4 Q1 Q2 Q3 Q4
Small 243 185a<151 151–185 186–219 >219 4a<4 4 5 >5
Medium 90 267b<225 225–267 268–309 >309 5b<5 5 6 >6
Large 181 377c<330 330–377 378–428 >428 7c<6 6–7 8–9 >9
a–cMedian values within a column with different superscripts were signicantly different (P < 0.05).
1Q1 = lowest 25% registered values; Q2 = 25% of values below the median; Q3 = 25% of values above the median; Q4 = highest 25% registered values.
Figure 1. Correlation between litter size and mean quartile of birth
weights in puppies from 1 given litter (100 litters and 514 puppies). Both
variables are expressed in quartiles according to Table 2.
Birth weight and early growth in puppies 4439
(IQR: –4.9 to 13.2%). No inuence of birth weight on
early growth rate was evidenced (Fig. 3). No effect
of breed size, litter size, age of the dam, or sex of the
puppy was observed on growth rate, but an effect of
litter was evidenced as a random term (P < 0.001).
Mortality rate between 2 and 21 d of age was in-
uenced by growth rate within the rst 2 d of life and
litter effect (P < 0.001 and P < 0.001, respectively;
Table 3; Fig. 4). Median growth rate in puppies dying
between 2 and 21 d of age was –11.3% (IQR: –16.7
to –4%) compared with 5.1% (IQR: –2.2 to 13.2%) in
puppies still alive at Day 21. The optimal cutoff value
of growth rate within the rst 48 h of life to assess pre-
dictive likelihood of mortality between 2 and 21 d of
age was –4% with a sensitivity of 75.4% and specici-
ty of 79.7%. Among all puppies that survived until Day
2, 28.3% (135/477) had an early growth rate below or
equal to –4%. Mortality rate was 38.5% (52/135) for
puppies with early growth rate below this threshold vs.
5.0% (17/342) for puppies with higher growth rate val-
ues (P < 0.001). Neither an effect of the birth weight
on mortality between 2 and 21 d of age nor of any other
Table 3. Predictive factors for neonatal mortality in
puppies (514 puppies; 100 litters)
Mortality 0–2 d Mortality 2–21 d
P-value OR195% CI2P-value OR 95% CI
Age of dam 0.15 0.5 0.2, 1.3 0.68 0.8 0.3, 2.3
Breed size 0.09 0.25
Medium 0.6 0.1, 2.4 0.3 0.1, 1.3
Large 0.3 0.1, 0.9 1.1 0.4, 2.9
Sex 0.75 1.14 0.5, 2.6 0.75 0.9 0.4, 1.8
Litter size50.65 0.50
Q1 1.03– 1.03–
Q2 0.6 0.1, 2.6 1.0 0.2, 4.0
Q3 0.4 0.1, 1.8 0.5 0.1, 1.7
Q4 0.5 0.1, 2.6 0.6 0.1, 2.8
Birth weight <0.001 0.53
Q1 1.03– 1.03–
Q2 22.7 5.0, 102.9 1.0 0.4, 2.5
Q3 59.4 7.3, 481.5 1.4 0.5, 4.0
Q4 16.4 4.7, 57.3 2.1 0.7, 6.7
G rowth rate
– – – <0.001 0.9 0.8, 0.9
Litter effect 0.06 – – <0.001 – –
1OR = odd ratio.
2CI = condence interval.
4– = data not available.
5Q1 = lowest 25% registered values; Q2 = 25% of values below the
median; Q3 = 25% of values above the median; Q4 = highest 25% regis-
Figure 2. Relationship between mortality from birth until 2 d of age
and birth weight (observations for 514 puppies; P < 0.001). Birth weight is
expressed in quartiles as dened in Table 2.
Figure 3. Relationship between birth weight and growth rate after
the rst 2 d of life (observations for 477 puppies; P = 0.20). Birth weight
is expressed in quartiles as dened in Table 2. Growth rate is dened as
(weight at 2 d – weight at birth)/weight at birth × 100%.
Figure 4. Correlation between early growth and neonatal mortality
at a litter level (observations for 100 litters; P < 0.001). Early growth is
expressed as the mean growth rate in puppies between 0 and 2 d of life
from 1 litter. Mortality rate is the proportion of puppies dying between 2
and 21 d of age within 1 litter.
Mila et al.
factor tested in that model (breed size, litter size, sex of
the puppy, or age of the dam) was evidenced.
Canine neonates are born with very low body fat
content (1.3% of the body; Kienzle et al., 1998) with
most energy being provided by glycogenolysis. The
decline in muscle and liver glycogen concentrations
after birth is rapid (Kliegman and Morton, 1987), and
gluconeogenesis is very limited due to immature liver
(Miettinen and Kliegman, 1983). In parallel, shiver-
ing thermogenesis is absent up to 6 d (Münnich and
Küchenmeister, 2014), which, taken together, make
newborn puppies susceptible to hypoglycemia and
hypothermia and, as a consequence, death. The total
perinatal mortality (stillbirths and mortality during the
rst 3 wk of age) in our study was 23.3%, with over
one-third of live-born puppies dying during the rst 2
d after birth. This mortality rate is higher than those
reported in other studies, ranging between 13.6 and
20.2% (Potkay and Bacher, 1977; Gill, 2001; Nielen et
al., 2001; Indrebø et al., 2007). No additional nursing or
hand rearing was performed in the present study, which
could explain a higher mortality rate. The majority of
the puppies (81.1%) dying within the rst 48 h after
birth were characterized by a low birth weight, previ-
ously showed in newborn infants and piglets as a risk
factor for hypoglycemia and hypothermia (Williams,
1997; Laptook and Watkinson, 2008; Devillers et al.,
2011). Low-birth-weight puppies, with a higher ratio
between body surface and body mass than littermates,
have a decreased ability to maintain stable blood glu-
cose concentration and body temperature as well as
lower ability to suckle. These factors, taken together,
increase their risk of neonatal death (Grundy, 2006).
In our study, birth weight was negatively affected
by litter size. A similar effect has been demonstrated
in kittens, in which each additional kitten in a litter de-
creased mean BW by 2.2 g (mean kitten birth weight
= 100 g; Sparkes et al., 2006; Gatel et al., 2011). No
effect of dam age or parity has been shown in kittens
or in the puppies in our study, although in foals, birth
weight increases by 0.5 kg for every extra year of age
of the mare (Elliott et al., 2009). Other effects com-
mon for all puppies coming from 1 litter (litter effect)
had an impact on the puppy’s birth weight in our study.
In pigs, intrauterine growth retardation, associated
with reduced birth weight, is caused not by a limited
uterine space but by a smaller size of placenta and so
limited transport of inter alia AA from dam to the fetus
(Ashworth et al., 2001). In women, fetal growth retar-
dation is due to insufcient concentration of nutrients
in the dam’s bloodstream and due to maternal vascu-
lar diseases in as many as 35% of the cases (Howie,
1982). To date, the impact of canine placental disor-
ders on birth weight in puppies remains unknown.
To identify puppies at higher risk of death due to a
low birth weight, a cutoff value has to be dened dif-
ferentially according to breed size, because this factor
determines weight at birth. Low birth weight values for
small-, medium-, and large-sized dogs were provided
in this study (Table 2), dened by the 25% owest birth
weights, as puppies from the rst quartile . Such pup-
pies were proven to be at signicantly higher risk of
death. However, birth weights vary not only between
different breed sizes (Grundy, 2006; our study) but
also between breeds of the same size (Trangerud et al.,
2007). Therefore, building a multibreed database with
puppies’ birth weights and their mortality could lead
to an even better estimate of the chances of a just born
puppy to survive and to provide it an adequate care if
In contrast to a dramatic impact on mortality with-
in the rst 2 d after birth, birth weight was not associ-
ated with mortality between 2 and 21 d of age. A major
risk factor for mortality during that period was growth
rate during the rst 2 d of life. This relationship could
be explained by colostrum intake and the nutritional
and/or immunological value of the colostrum (GE at
Day 1 of lactation: 548 kJ/100 g [unpublished data];
IgG: 19.4 g/L [Mila et al., 2014]). Due to the endo-
theliochorial placenta, the transfer of immunoglobu-
lins from dam to fetus is very limited in dogs. Puppies
acquire 90% of their passive immunity via colostrum
ingested within the rst 12 to 16 h of life (Chastant-
Maillard et al., 2012). Indeed, serum IgG concentra-
tion at 2 d of age (as a marker of passive immune
transfer) has been demonstrated to be strongly associ-
ated with growth rate within the rst 2 d of life as well
as with neonatal mortality. Over 44% of puppies with
an IgG concentration at Day 2 at or below 2.3 g/L,
dened as passive immune decit in dogs, died during
the neonatal period compared with only 5% in puppies
with higher IgG concentrations (Mila et al., 2014).
Energy provided by the colostrum can also ex-
plain the link between early growth and neonatal mor-
tality. In 2-d-old piglets, colostrum intake, evaluated
through weight gain after the rst 24 h of life, was
positively associated with rectal temperature and glu-
cose concentration, showing the important role of co-
lostrum in thermoregulation and glucose homeostasis
(Devillers et al., 2011). The ability to maintain stable
body temperature as well as blood glucose level is
very limited in canine newborns, and hypothermia and
hypoglycemia may have fatal consequences for pup-
pies (Münnich and Küchenmeister, 2014). The early
growth rate threshold, below which risk of mortality
Birth weight and early growth in puppies 4441
is signicantly increased, was calculated at or below
–4% in this study. Weight monitoring, together with
the cutoff value calculated in our study, provide an
easy tool to detect and nurse puppies at increased risk
of hypoglycemia or hypothermia and, by consequence,
risk of neonatal mortality.
The positive effect of colostrum on survival might
be also related to its bioactive compounds, such as
prolactin, steroids, insulin, leptin, and many growth
factors, essential for correct organ development and
maturation (Hamosh, 2001; Farmer et al., 2006).
Amino acids together with Insulin-like Growth Factors,
highly concentrated in swine colostrum (Donovan et
al., 1994), have a stimulatory effect on protein synthe-
sis in the piglet intestinal tract 50-fold stronger than
mature milk (Burrin et al., 1992). In puppies, a large
increase in intestinal dimensions (i.e., 42% in mucosal
weight) occurs within the rst 24 h of life, dramatically
improving food intake, digestion, and nutrients absorp-
tion (Paulsen et al., 2003). Insufcient colostrum in-
take, as evidenced by reduced growth over the rst 2 d
of life, may, therefore, reduce nutrient absorption later
in life, leading to higher mortality rates in puppies.
Although differences in postweaning growth
curves and adult weights between females and males
have been demonstrated in dogs (Helmink et al., 2000)
and in cats (Moik and Kienzle, 2011), no sexual di-
morphism in birth weights or early growth was evi-
denced in our study. Interestingly, growth during the
rst 2 d of life was not found to be associated with birth
weight, whereas in many other species an accelerated
growth occurs, compensating the lower weight at birth
(Binkin et al., 1988; Moik and Kienzle, 2011). In rab-
bits and rats, litter size, negatively correlated with pup
growth, explains most of the preweaning growth vari-
ation (Rödel et al., 2008). In our study, not litter size
but litter effect as a random term for all littermates had
an inuence on early growth rate. Insufcient milk
yield, as shown previously in pigs (Marshall et al.,
2006), together with poor maternal behavior and other
circumstances precluding colostrum intake, could be
responsible for decreased growth in some litters.
This study illustrates the differential impact of
birth weight and early growth rate on neonatal mortal-
ity, either mortality during the rst 2 d after birth or
mortality between 2 d and 3 wk of age. It also provides
critical thresholds allowing identication of puppies
with particular need of monitoring and nursing dur-
ing the neonatal period. However, these values remain
to be rened for various dog breeds as well as differ-
ent kennels. This study highlights the need for further
investigation on intrauterine growth (to decrease the
incidence of low birth weights) and on colostrum in-
take (to optimize early growth) to reduce the high inci-
dence of neonatal mortality in the canine species.
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