Evaluación de La Viabilidad Neonatal Canina La Puntuación de Apgar

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DOI: 10.1111/rda.

12787

ORIGINAL ARTICLE

Assessment of canine neonatal viability—the Apgar score

MC Veronesi

Department of Veterinary
Medicine, Università degli Studi di Milano, Contents
Milan, Italy Perinatal mortality is relatively high in dogs, with deaths peaking around the time of
birth and during the first week of age. Among the several causes of canine perinatal
Correspondence
Maria Cristina Veronesi, Department of mortality, whelping is the greatest cause. Therefore, early neonatal assistance at birth
Veterinary Medicine, Università degli Studi
should be mandatory with dogs. In comparison with human neonatology, knowledge
di Milano , Milan, Italy.
Email: maria.veronesi@unimi.it and technological ability in canine neonatology is tremendously scarce. The Apgar
score for the newborn viability assessment at birth represents a feasible method for
the prompt recognition of newborns that will need special assistance immediately
after birth. The five parameters of the Apgar score were adapted to the canine species
by different studies. Advantages and limits, as well as clinical applications, are pre-
sented and discussed in further detail. It was concluded that the Apgar score repre-
sents the easiest and simplest, non-­invasive and reliable method, that could be
performed under every clinical and practical condition, for newborn puppies viability
evaluations and short-­term survival prognosis.

1 | BACKGRO UND ON In comparison with human neonatology, knowledge and techno-


CANINE NEONATOLOGY logical ability in canine neonatology is tremendously scarce (Lucio,
Silva, Rodrigues, Veiga, & Vannucchi, 2009), leading to difficulties to
In mammals, the reproductive process is considered to be successful recognize the newborns who are in need of assistance to limit the
when a pregnant female has a normal pregnancy and gives birth to live number of neonatal deaths. This could be due to the difficulty to
and viable offspring. The majority of offspring deaths can be attributed obtain biological samples for analysis, which are easily performed in
to the puppy losses occurring during the perinatal period. In dogs, peri- human neonates, such as blood sampling, but also to adapt to the dif-
natal mortality is considered as the sum of deaths related to stillborn, ferent general practical conditions of veterinary assistance in compar-
plus the puppies are dying within the neonatal period. Canine perina- ison with human hospitals (Lucio et al., 2009).
tal mortality is relatively high, reaching values up to 40%, with death
rates peaking around birth and during the first week of age (Tønnessen,
Sverdrup Borge, Nødtvedt, & Indrebø, 2012). Among the causes re- 2 | THE FOETAL-­T O-­N EONATAL
sponsible for such a high perinatal death percentage is the birth pro- ADAPTATION AND NEONATAL ASSESSMENT
cess which is the largest factor in this high death rate for puppies. In
dogs, the process of parturition is a relatively long process, even under The transition from the foetal to the neonatal life involves an efficient
the best physiological conditions, and it could become even longer in multisystemic adaptation process of the organism. The most critical
the case of dystocia. Thus, foetal asphyxia is thought to be one of the change is related to the beginning of respiration that influences the
most common causes of perinatal puppy death (Grundy, 2006; Moon, early survival of the neonate. Breathing is the key function for the
Erb, Ludders, Gleed, & Pascoe, 1998, 2000). As in other mammals, the immediate neonate’s survival. When the foetus is mature and ready
process of birth is challenging, and the first minutes after birth are the for birth, the passage through the birth canal, the blood oxygen to nitric
most life-­threatening. The efficiency of these first few minutes after oxide ratio and the umbilical cord detachment are the first stimuli to
birth has pivotal and long-­term consequences on the newborn’s life. start the puppy’s first breath. As a consequence of the first breath, the
Therefore, the assistance and care to each and every single newborn is lung inflates, and a number of other changes to the respiratory and
mandatory, in veterinary medicine as it is in human medicine. circulatory systems occur, first line the occlusion of the foetal blood

46 | © 2016 Blackwell Verlag GmbH wileyonlinelibrary.com/journal/rda Reprod Dom Anim 2016; 51 (Suppl. 1): 46–50
14390531, 2016, S1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rda.12787 by Cochrane Colombia, Wiley Online Library on [20/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Veronesi | 47

ways. As a consequence, a cascade of physiological changes leading


4 | THE APGAR SCORE SYSTEMS IN
to the first hours of neonatal adaptation is necessary for foetal-­to-­
CANINE NEONATOLOGY
neonatal viability and survival (Grundy, 2006).
The neonatal viability, which is the potential of the neonate to sur-
In two studies (Lucio et al., 2009; Silva, Lucio, Veiga, Rodrigues, &
vive outside the uterus after birth, depends largely on foetal organ
Vannucchi, 2009), the use of the Apgar score in the evaluation of
maturity, environmental conditions and neonatal care. In comparison
canine neonatal viability at birth, at 5 min and 60 min after delivery,
with foals, calves or piglets, puppies and kittens are largely imma-
was mentioned; unfortunately, the details about the method of evalu-
ture at birth, making them extremely vulnerable. Unlike humans, in
ation or reference were not reported.
most instances, dogs and cats give birth under field conditions and
In 2009, Veronesi and co-­authors proposed an Apgar score
rarely in veterinary facilities, so the techniques for neonatal evalua-
adapted for the neonatal viability assessment in canines, using the
tion and assistance should be adapted to every kind of environmental
same five parameters proposed by Dr. Virginia Apgar in babies, but
condition.
with modifications according to canine neonatal physiology (Table 1).
The veterinary assistance to the parturient bitch is recently highly
Appearance was assessed by the evaluation of the mucous mem-
requested from both pet owners and especially breeders, because of
branes colour as follows: pink rated as 2, pale rated as 1, and cyanotic
the high economic values of dams and litters (Smith, 2007). The sur-
rated as zero. Pulse, referring to heart rate, was rated as 2 when it
vival of a number as much higher as possible of newborns is therefore
was >220 beats per minute (bpm), rated as 1 when it was between
wanted not only from an ethical perspective, but also from an eco-
180 and 220 bpm and rated as zero when it was <180 bpm. Grimace,
nomic point of view (Veronesi, Panzani, Faustini, & Rota, 2009).
indicating the reaction of the neonate to irritability, was assessed by
The prerequisite for a prompt recognition of newborns that are in
the gentle compression of the tip of a paw, and evaluating the puppies
need of special assistance immediately after birth is the availability of
reaction: rated as 2 when the puppy reacted with crying and quick
a simple method for newborn viability assessment.
leg retraction, rated as 1 when the leg was weakly retracted in asso-
ciation to weak or none vocalization and rated as zero when no leg
retraction and no vocalization was stimulated. Attitude was evaluated
3 | THE APGA R SCORE
by neonatal motion as follows: rated as 2 when strength spontaneous
movements of the neonate were observed, rated as 1 when mild
Since the 1950s, the Apgar score, proposed by Virginia Apgar for the
movements were detected and rated as zero for the absence of neo-
quick assessment of neonatal viability in humans, was widely used
natal movements. Respiration was assessed by taking in consideration
all over the world and still remains the most suitable method for the
of both the respiratory rate (rr) and vocalization: respiratory efforts
viability assessment and short-­term survival prognosis in babies.
were rated as 2 when clear crying was associated to >15 rr, rated as
In humans, the Apgar score encompasses five parameters, easy to
1 when mild crying was associated to 6–15 rr and rated as zero when
assess, for the clinical evaluation of the infant soon after birth, usu-
no crying was associated to <6 rr.
ally within 1 min after birth and again at 5 min after birth, and may be
The same Apgar score system was subsequently used by Doebeli
repeated later for newborns with low scores. These five parameters
et al. (2013) for the evaluation of the effect on newborn puppy via-
are resumed in an acronym built on the surname of its creator, so that
bility of two different anaesthetic protocols with canine caesarean
APGAR recall easily the initials of the five parameters to be assessed:
section, and by Vassalo et al. (2015) for the routine assessment of
A, as appearance, P as pulse, G as grimace, A as attitude and R as respi-
newborn puppies’ viability.
ration. To each one of these parameters, a score ranging from zero to
Recently, Batista et al. (2014) used the same Apgar score pro-
two is assigned, for a total sum ranging between zero and ten. On the
posed by Veronesi et al. (2009), with some modifications adapted
base of the final sum, three classes of neonatal viability were defined:
to two brachycephalic dog breeds (English and French Bulldog) for
when the score is less than 3, the neonatal condition is considered
as critical and the newborn need medical assistance; when the score
T A B L E 1 Apgar score for canine newborn viability evaluation
is between 4 and 6, the condition of the newborn is considered as
(Veronesi et al., 2009)
low, and the newborn should be supervised or submitted to medical
assistance; when the score is 7 to 10, the newborn clinical condition is Score
normal, and the newborn need only routine care.
Parameter 0 1 2
Because of its feasibility, the Apgar score was thereafter intro-
Mucus colour Cyanotic Pale Pink
duced in veterinary medicine, and, after adaptation according to the
Heart rate (bpm) <180 180–220 >220
specific physiological features, used for the neonatal evaluation of
foals, calves and piglets. The Apgar score was not widely used with Reflex irritability Absent Grimace Vigorous

canines until recently. However, thanks to its feasibility of execution Motility Flaccid Some flexions Active motion

and the limited use of instruments (only a stethoscope is needed), this Respiratory No crying/<6 Mild crying/6 Clear
method has proved to be useful for the neonatal evaluation under efforts* to 15 crying/>15

every clinical condition in dogs (Veronesi et al., 2009). *vocalization and rr.
14390531, 2016, S1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rda.12787 by Cochrane Colombia, Wiley Online Library on [20/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
48 | Veronesi

the clinical evaluation of puppies born by caesarean section. The


6 | NEONATAL VIABILITY, CLINICAL
slight variations included a lower heart rate considered as normal:
MANAGEMENT AND SURVIVAL RATE
>180 bpm rated as 2, between 120 and 180 bpm rated as 1 and
<120 bpm was rated as zero. Respiration was evaluated considering
The viability assessment allowed the recognition of puppies with a low
only the respiratory rate, and the mucous membrane colour was rated
Apgar score, requiring different degrees of medical assistance. Some
as 2 when reddish, rated as 1 when pink and rated as zero when cya-
studies (Veronesi et al., 2009; Doebeli et al. 2013) provided assistance
notic or pale.
to all the newborns with an Apgar score <7, while Vassalo et al. (2015)
The Apgar score proposed by Veronesi et al. (2009) was also used
used the limit of Apgar score <6, and Batista et al. (2014) used the
by Cunto, Zambelli, Castagnetti, Linta, and Bini (2014) for newborn
Apgar score <5 to initiate protocols of intensive care and neonatal
puppy evaluations in a case report on diagnosis and treatment of foe-
resuscitation. Although the survival rate after neonatal assistance
tal anasarca in an English Bulldog litter.
was higher for newborns classified in the intermediate class of viabil-
In another study by Groppetti et al. (2010), a different Apgar score
ity as compared to the lowest class, the overall survival after assis-
was used, which considered seven parameters, including the mucous
tance was 43%–91% of the severely depressed/critical neonates, and
membrane colour, heart and respiratory rates measurement, reflex irri-
88%–100% of the moderately depressed/moderate vitality newborns
tability and mobility evaluation, suckling and vocalization assessment,
(Table 2). These results are very interesting, because the main goal of
instead of the traditional five parameters for newborn puppies viability
the neonatologists is the as high as possible survival rate of neonates.
evaluation.
Survival rate was checked again at different time points after birth.
Except for the score system proposed by Groppetti et al. (2010),
Doebeli et al. (2013) evaluated the survival rate at 1 and 24 hr after
all the other studies (Veronesi et al., 2009; Doebeli et al. 2013; Batista
birth; Veronesi et al. (2009) at 2 and 24 hr after birth; Batista et al.
et al., 2014; Vassalo et al., 2015) on the base of their final summa-
(2014) at 2, 12 and 24 hr after birth, while Vassalo et al. (2015) checked
rizations identified three classes of neonatal viability, similar to the
the survival rate at 2 and 24 hr, and then 30 days after birth; Groppetti
classification used for humans. Newborns rated as 0 to 3 were consid-
et al. (2010) checked the survival rate only once at 48 hr after birth. In
ered as severely distressed, or critical neonates; those rated as 4 to 6
these four studies, survival rates recorded at 1, 2 or 12 hr after birth
were moderately distressed, or moderate viability neonates; newborns
were the same as those recorded at 24 hr, except for the puppies rated
rated as 7 to 10 were considered as normal newborns with no distress,
an Apgar score of 3 to 0 in the study from Batista et al. (2014), in which
or normal viability neonates.
the survival rate decreased from 69% at 12 hr after birth to 55% at
24 hr after birth. Taken together, these results suggest that the Apgar
score was highly positively correlated to survival of puppies early after
5 | TIMETABLE FOR APGAR SCORE
birth and that the mortality rate was concentrated in puppies with a
MEASUREMENT IN CANINES
low Apgar score (0–3). Only Groppetti et al. (2010) reported that no
relation was found between the Apgar score and neonatal survival
In humans, the Apgar score is routinely measured at 1 min and at
checked only at 48 hr after birth.
5 min after birth (Finster & Wood, 2005). In dogs, Veronesi et al.
(2009) reported that the Apgar score routinely measured at 5 min
after birth interferes neither with the initial maternal care to the
7 | THE APGAR SCORE AND OTHER PUPPY
puppy during spontaneous or assisted parturition, nor with the first
VIGOUR PARAMETERS
neonatal care provided by human assistance in case of caesarean
section deliveries. Doebeli et al. (2013) and Batista et al. (2014) also
Puppy vigour can also be evaluated by some behavioural parameters
recorded the first measurement at 5 min after birth and reassessed
and neonatal reflexes, such as the mammary gland searching activity,
the puppies at 15 min and 60 min after birth (Doebeli et al. 2013), or
the suckling/swallowing reflexes, the rooting and righting reflexes.
60 min after birth (Batista et al., 2014). Other authors (Lucio et al.,
The concomitant measurement of Apgar score and neonatal reflexes
2009; Silva et al., 2009; Vassalo et al., 2015) measured the initial
is rational because both scores evaluate the neonatal viability (Vassalo
Apgar score at birth, with a second measurement at 5 min after birth
(Lucio et al., 2009; Silva et al., 2009), and a third measurement at
60 min after delivery (Lucio et al., 2009; Silva et al., 2009; Vassalo T A B L E 2 Survival rate after neonatal assistance in neonates with
Apgar scores between 3–0 and 6–4. Data are expressed as the
et al., 2015) during a normal parturition, after obstetrical assistance
number of subjects on the total, and percentage
or a caesarean section, and on puppies born following the oxytocin
administration (Silva et al., 2009). Lucio et al. (2009) reported a low Survival rate
Apgar score in all the puppies at births, associated to a mixed acido- Reference Apgar score 3–0 Apgar score 6–4
sis; the Apgar score improved in all newborns after 5 min of birth, and
Veronesi et al., 2009 3/7 (43%) 15/17 (88%)
carbon dioxide tension, base excess and venous blood pH improved
Doebeli et al., 2013 21/23 (91%) 16/16 (100%)
at 60 min after birth, although a metabolic acidosis persisted.
Batista et al., 2014 29/42 (69%) 138/139 (99%)
14390531, 2016, S1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rda.12787 by Cochrane Colombia, Wiley Online Library on [20/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Veronesi | 49

et al., 2015). The Apgar score resulted positively associated to mam- the Apgar score could facilitate the development of a strategy for a
mary gland searching and to suckling/swallowing reflexes (Veronesi proper puppy neonatal resuscitation and intensive care early after
et al., 2009). Suckle, rooting and righting reflexes improved at 60 min delivery (Batista et al., 2014). The Apgar measurement after assistance
after birth, as did the Apgar score (Vassalo et al., 2015). of depressed newborns could in some way allow the clinician to evalu-
ate the puppy’s response to resuscitation (Vassalo et al., 2015).
The Apgar score was very suitable also for the repeated evalu-
8 | THE APGA R SCORE AND ations during the first hour of life to assess individual spontaneous
TYPE OF DELIVERY improvement, or the response to assistance or resuscitation (Vassalo
et al., 2015; Veronesi et al., 2009).
The type of delivery seems to influence the neonatal Apgar score in According to survival prognosis, the Apgar evaluation of newborn
dogs. Some studies (Batista et al., 2014; Silva et al., 2009; Vassalo dogs was reliable for determining survival short-­term prognosis, with
et al., 2015) found lower Apgar scores in puppies born by caesarean some limitations (Batista et al., 2014; Veronesi et al., 2009). In fact,
section compared to those born by vaginal delivery, while Veronesi there is no guarantee that all those pups showing higher Apgar scores
et al. (2009) reported lower Apgar scores for puppies born by manual will automatically survive, but high Apgar scored puppies are more
or pharmacologically assisted delivery, as compared to vaginal sponta- likely to survive (Batista et al., 2014). Moreover, neonatal mortality
neous parturition deliveries or caesarean sections. Doebeli et al. (2013) was reported to be concentrated in those pups with the lowest Apgar
found good neonatal vitality rates in puppies born after emergency scores (0–3) (Batista et al., 2014).
caesarean sections. Lucio et al. (2009) reported a more severe Apgar Beside the strong points of the studies, some questions require
score at birth in neonates born from bitches with dystocia requiring elucidation.
obstetrical assistance in comparison with puppies born by normal First of all, none of the studies performed on dogs evaluated the
delivery or from bitches where only oxytocin was administered. relationship between the Apgar score at birth and long-­term survival
Where caesarean section is concerned, two main factors should or developmental, behavioural and neurological outcome in survivors.
be considered. The first relates to the different conditions of the foe- Several studies in humans demonstrated that the Apgar score is suit-
tuses when caesarean section is performed as a veterinary emergency able neither for long-­term neonatal survival prognosis nor for long-­
in comparison with an elective caesarean section. The second factor term neurological or mental impairment.
relates to the different anaesthesia protocols used. Regarding caesar- In addition, the real Apgar score cut-­off for spontaneous sur-
ean section, Batista et al. (2014) reported data obtained on elective vival should be further investigated. Data available from the studies
caesarean sections only, while in the other studies, data were obtained on dogs reported different scores to define normal viable newborn
from both emergency and elective caesarean sections. Doebeli, puppies: >7 (Veronesi et al., 2009; Doebeli et al. 2013), >6 (Vassalo
Michel, Bettschart, Hartnack, and Reichler (2013) evaluated the effect et al., 2015) and ≥5 (Batista et al., 2014). These data are not negligi-
of two different drugs for induction of anaesthesia during emergency ble, whether the correct cut-­off for spontaneous survival should be
caesarean section in dogs. The neonatal vitality, assessed by the Apgar identified in puppies rated as ≥5, and the puppies scored between 5
score at 5, 15 and 60 min after delivery was significantly higher when and 7 were presumably submitted unnecessarily to neonatal assis-
induction of anaesthesia was obtained with alfaxalone as compared tance. Consequently, the effect of neonatal assistance on survival of
to anaesthesia obtained with propofol, while the proportion of surviv- “low-­scored” puppies should be questionable. The real impact of neo-
ing puppies 60 min after delivery was not different between the two natal assistance in low viable neonates should also imply the enrol-
groups. Therefore, the impact of different drugs used for induction ment of a control, non-­treated group. Unfortunately, this is difficult to
of anaesthesia in dogs submitted to emergency caesarean section on obtain, mainly because of ethical reasons, but also from an economical
neonatal viability was demonstrated. standpoint, as even a single surviving puppy allows for a profit for the
breeder (Veronesi et al., 2009).
When more technical topics are concerned, the effect of type of
9 | STRENGTHS AND WEAKNESS OF THE delivery of the anaesthetic protocol and the effect played by both
APGAR SCORE IN CANINE NEONATOLOGY these parameters on puppy’s viability should be better investigated.
At last, since Batista et al. (2014) highlighted some breed-­specific
Data available from the few studies conducted on dogs highlight that differences in the parameters used in the score system, other breed-­
the Apgar score is an inexpensive, simple and practical method to specific changes to the former system of evaluation could be neces-
evaluate the condition of a newborn puppy, also under clinical prac- sary for a more correct evaluation of each canine breed.
tices (Vassalo et al., 2015; Veronesi et al., 2009). The Apgar score was
very suitable for assessing neonatal vitality in puppies, and the system-
atic use of the Apgar evaluation allowed the prompt identification of 10 | CONCLUSIONS
puppies requiring neonatal care and to choose the more appropriate
resuscitation procedure intensity in relation to the degree of puppy In conclusion, all the studies demonstrated the suitability of the use of
viability, minimizing neonatal losses (Veronesi et al., 2009). Therefore, the Apgar score in the neonatal viability assessment immediately after
14390531, 2016, S1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rda.12787 by Cochrane Colombia, Wiley Online Library on [20/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
50 | Veronesi

birth and in the first hours of life, especially for those born after cae- Doebeli, A., Michel, E., Bettschart, R., Hartnack, S., & Reichler, I. M. (2013).
sarean section or dystocia, or for breeds such as the brachycephalic, Apgar score after induction of anesthesia for canine caesarean section
with alfaxalone versus propofol. Theriogenology, 80, 850–854.
characterized by higher risk of mortality and low vitality at birth. The
Finster, M., & Wood, M. (2005). The Apgar score has survived the test of
value of the Apgar score to predict the short-­term survival rate of time. Anesthesiology, 102, 855–857.
puppies remains to be clarified, even if in some studies a close rela- Groppetti, D., Pecile, A., Del Carro, A. P., Copley, K., Minero, M., &
tionship between a high Apgar score and survival at 24 hr after birth Cremonesi, F. (2010). Evaluation of newborn canine viability by means
of umbilical vein lactate measurement, apgar score and uterine tocody-
was found. Although there is no guarantee that all puppies showing
namometry. Theriogenology, 74, 1187–1196.
a high Apgar score will surely survive, survival is more likely in high-­ Grundy, S. A. (2006). Clinically relevant physiology of the neonate. The
scored neonates than it is in low-­scoring neonates. The type of deliv- Veterinary Clinics of North America. Small Animal Practice, 36, 443–459.
ery has a significant impact on Apgar score, as well as the type of Lucio, C. F., Silva, L. C. G., Rodrigues, J. A., Veiga, G. A. L., & Vannucchi, C.
I. (2009). Acid-­base changes in canine neonates following normal birth
drug used for the induction of anaesthesia. Further studies are also
or dystocia. Reproduction in Domestic Animals = Zuchthygiene, 44(2),
required to define, if any, other breed-­specific parameters for the cor- 208–210.
rect Apgar score neonatal viability assessment in all the canine breeds. Moon, P. F., Erb, H. N., Ludders, J. W., Gleed, R. D., & Pascoe, P. J. (1998).
Similarly, also the real cut-­off Apgar score for spontaneous survival Perioperative management and mortality rates of dogs undergoing ce-
sarean section in the United States and Canada. Journal of the American
and the effect of intensive care and resuscitation on survival of low
Veterinary Medical Association, 213, 365–369.
viable neonates should be better elucidated. However, the Apgar
Moon, P. F., Erb, H. N., Ludders, J. W., Gleed, R. D., & Pascoe, P. J. (2000).
score, at present, represents the easiest and simplest, non-­invasive, Perioperative risk factors for puppies delivered by cesarean section in
less instrumental and reliable method, performable under every clini- the United States and Canada. Journal of the American Animal Hospital
cal practice condition, for newborn puppies viability evaluation and Association, 36, 359–368.
Silva, L. C. G., Lucio, C. F., Veiga, G. A. L., Rodrigues, J. A., & Vannucchi,
short-­term survival prognosis, in dogs as well as in humans.
C. I. (2009). Neonatal clinical evaluation, blood gas and radiographic
assessment after normal birth, vaginal dystocia or caesaeran sec-
tion in dogs. Reproduction in Domestic Animals = Zuchthygiene, 44,
CO NFLI CT OF I NTE RE ST 160–163.
Smith, F. O. (2007). Challenges in small animal parturition—Timing elective
There are no conflict of interests and no founding sources.
and emergency cesarean sections. Theriogenology, 68, 348–353.
Tønnessen, R., Sverdrup Borge, K., Nødtvedt, A., & Indrebø, A. (2012). Canine
perinatal mortality: A cohort study of 224 breeds. Theriogenology, 77,
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