Theriogenology 84 (2015) 681–686

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Theriogenology
journal homepage: www.theriojournal.com

In utero development of the fetal intestine: Sonographic

evaluation and correlation with gestational age and fetal
maturity in dogs
Elaine M.U. Gil*, Daniela A.A. Garcia, Tilde R. Froes
Department of Veterinary Medicine, School of Veterinary Medicine, Federal University of Paraná, Curitiba City, Paraná State, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Modern high-resolution ultrasound images enable earlier assessment of measures of fetal
Received 26 February 2015 development, including identification of the bowel. The aim of this study was to describe
Received in revised form 28 April 2015 the ultrasonographic development of fetal bowel and correlate this with gestational age;
Accepted 29 April 2015
define whether ultrasonographic visualization of fetal intestinal peristalsis in utero is
associated with fetal maturation and determine whether there is a difference in fetal in-
Keywords:
testinal peristalsis detection time between fetuses delivered by normal delivery and
Canine
cesarean. A cohort study was conducted in pregnant bitches presented to a veterinary
Pregnancy
Gestational ultrasound hospital, to assess fetal bowel development. Statistical analysis was used to establish the
Fetal bowel ultrasonography correlation of the stage of fetal bowel development, as recorded by ultrasound, with
Maturation outcomes of normal delivery and cesarean section. The study was broken down into three
stages: the first stage was a descriptive analysis of fetal bowel development by ultrasound;
the second stage compared time (in days) of bowel development between groups (normal
delivery vs. cesarean); and the third stage was correlated survival probability for fetuses
born on any day after detection of intestinal peristalsis with fetal maturity. All statistical
analyses were significant. It is possible to monitor pregnancy progression using ultraso-
nographic evaluation of bowel development and this can reliably identify the end of fetal
organogenesis. However, ultrasonographic detection of bowel segments with visualization
of wall layers and associated peristalsis should not be used as the sole indicator for
cesarean section planning because it is not possible to determine ultrasonographically
whether the bowel is functional (mature).
Ó 2015 Elsevier Inc. All rights reserved.

1. Introduction fetal maturity and appropriate timing of C-section can

Ultrasonography is the preferred method for early
diagnosis of pregnancy, evaluation of fetal viability, and
estimation of gestational age [1]. Early and accurate
determination of gestational age is useful for predicting
time and management of deliver, including planning
cesarean section (C-section) [2]. In some breeds of dogs in
which C-section is considered necessary, assessment of
* Corresponding author. Tel.: þ55 41 3350 5767; fax: þ55 41 3350 5725.
E-mail address: elainegil07@gmail.com (E.M.U. Gil).
reduce neonatal mortality [3].
As in human medicine, there are a variety of methods
for ultrasonographic estimation of fetal age in pregnant
bitches; these include calculation from crown–rump length
in early pregnancy, biparietal diameter, and assessment of
fetal organogenesis by serial examinations [2–7]. The
assessment of fetal organogenesis is an interesting model
for determination of fetal age in dogs. The bowel is the last
organ to be identified by ultrasonography as fetal dogs
develop [5,7].
According to some authors visualization of the bowel
and identification of peristalsis by ultrasound determines

0093-691X/$ – see front matter Ó 2015 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.theriogenology.2015.04.030
682 E.M.U. Gil et al. / Theriogenology 84 (2015) 681–686
the end of fetal organogenesis, indirectly indicating that the
fetus is full term. This happens around 57 to 63 days of
gestation [5,8,9]. Several authors [7–10] describe a range of
gestational ages for detection of peristalsis by ultrasonog-
raphy from 57 days after the peak of LH.
However, modern high-resolution ultrasound images
enable earlier assessment of measures of fetal development,
including identification of the bowel. There are no previous
studies describing the ultrasonographic assessment of bowel
development in canine fetuses. Our hypothesis is that ultra-
sonographic visualization of fetal bowel is possible at earlier
fetal ages than previously described. The purpose of this study
was threefold: (1) to describe the ultrasonographic develop-
ment of the fetal bowel and correlate this with gestational age;
(2) to define whether ultrasonographic visualization of fetal
intestinal peristalsis in utero is associated with fetal matura-
tion; (3) to determine whether there is a difference in fetal
intestinal peristalsis detection time (days before delivery)
between fetuses born by normal delivery and cesarean.
2. Materials and methods
2.1. Patient selection
A cohort study was conducted in pregnant bitches to
assess fetal bowel development. The sample population
consisted of bitches with confirmed pregnancy presented
to a veterinary hospital between May 2013 and April 2014.
All procedures were carried out in accordance with Animal
Use Committee guidelines. All owners provided informed
written consent to be included in the study. Exclusion
criteria were bitches with positive pregnancy unavailable
for serial examinations, late pregnancy (more than 30 days
of gestation), at time of the first presentation, date of de-
livery not reported by owners, and bitches presented with
concomitant disease.
2.2. Ultrasound imaging and equipment
Ultrasound scanning was performed with a high-
resolution linear multifrequency transducer (7.5–
12 MHz), model MyLab 30 (Esaote, Genova, Italy). The gain,
focus, and other adjustments were made during examina-
tion to obtain the best image for each fetus evaluated. All
pregnant bitches were prepared with hair clipped before
the examination and positioned in dorsal recumbency, and
ultrasound gel was used to optimize image acquisition.
The pregnant bitches were followed by ultrasono-
graphic examination from the 14th day after the first
mating and/or insemination. Ultrasonography examina-
tions were performed every 4 days until intense peristalsis
(movement every three seconds) of the fetal bowel was
visible. From that examination onward, daily assessments
were made until delivery.
Gestational age was confirmed after delivery, in days to
delivery, by counting backward (delivery as Day 0); normal
gestational length was considered to be 57 to 63 days
because of the variable proestrus and estrus periods in dogs
[11]. During ultrasound examination, gestational age was
estimated in days of gestation, using the descriptions of
Yeager et al. [5].
Each sonographer scanned all fetuses in each pregnant
bitch. Each bitch was scanned independently by two
experienced sonographer (one of whom is a member of the
Brazilian College of Veterinary Radiology) at each exami-
nation. However, both sonographers were in the room
during the examinations. The ultrasound interpretation
was achieved by consensus of the two sonographers. The
examination method followed a protocol to examine the
whole abdomen by scanning clockwise, starting with fe-
tuses in the left uterine horn (cranial to caudal) followed by
the right horn (caudal to cranial). In bitches with large
numbers of fetuses, at least four fetuses were examined at
all examinations, and in bitches with four or fewer fetuses,
all fetal abdomens were examined.
Intrauterine fetal abdomens were assessed in the longi-
tudinal and dorsal planes of each fetus. All fetal organogen-
esis was monitored; however, the priority was examination
of the bowel.
After data collection, pregnant females were classified
according to delivery method (C-section or natural)
and divided into two groups. The decision to perform a
C-section was based on ultrasound indications of fetal
distress [12]. Fetuses were considered to be distressed if
fetal heart rate remained low (between 160 and 190 beats
per minute), and without peaks of acceleration and decel-
eration as described by Gil et al. [13]. Fetal heart rate was
measured using M-mode for five minutes per fetus in all
pregnant bitches up to maximum four fetuses.
2.3. Experimental design
Statistical analysis was used to establish the correlation
of the stage of fetal bowel development, as recorded
by ultrasound, with outcomes of normal delivery and
C-section. The study was broken down into three stages.
The first stage was a descriptive analysis of fetal bowel
development by ultrasound. In the second and third stages,
a rating from one to four was used for various phases of
fetal bowel development. Phase 1 was defined as the first
time the bowel could be visualized and phase 4 was the last
phase, when intestinal peristalsis (movement every 3 sec-
onds) was identified. Once phase 4 had been identified, this
was used for statistical analysis of the second and third
stages of the experiment. For each phase (1–4) of intestinal
development, respective fetal age ranges were calculated.
The aim of the second stage was to compare time (in
days) of bowel development between groups (normal de-
livery vs. cesarean). For this, statistical testing was used: (1)
the Student t test which compared all phases (1/1, 2/2, 3/3,
and 4/4) between the two groups; (2) the semiparametric
regression Cox model [14] was used to specifically assess
phase 4 of bowel development, testing whether there was a
difference in time (days) of ultrasound visualization of
bowel between the two groups. In the Cox model, the group
of bitches with normal delivery was used as the control.
The aim of the third stage of the study was to correlate
survival probability for fetuses born on any day in phase 4,
at which time fetuses were assumed to be mature, and to
this end, a survival curve was generated. The survival curve
was constructed using the Kaplan–Meier method [15], and
statistical comparison between groups was performed by
 E.M.U. Gil et al. / Theriogenology 84 (2015) 681–686
the log-rank test and then identifying whether there were
differences between the survival probabilities of puppies
born by normal delivery or cesarean. In all analyzes, a P
value of a ¼ 0.05 was considered significant and the sig-
nificance was analyzed relative to the value set.
All statistical tests were selected and performed by one
author (Elaine Gil) and one statistical professional (Eliane
Coimbra). Data collation and analysis were performed using
Microsoft Office Excel (Microsoft Office 2007 for Windows,
Redmond, WA, USA) and R for Windows (version 3.1.1 Ri386,
R Foundation for Statistical Computing, Vienna, Austria,
2014) through packages “Survival”, “KMsurv” and “Coin”.
3. Results
Eighteen pregnant bitches were included in this study.
Several breeds were represented, and ages ranged from 1 to
6 years. Seventy-five fetuses were evaluated, and all were
born healthy, including those delivered by cesarean. The
litter size of each bitch was between two and nine pups
(Table 1).
After ultrasound monitoring of fetal organogenesis and
evaluation of development of fetal intrauterine bowel in all
females, four different phases of development were defined.
All fetuses displayed the same ultrasonographic patterns of
bowel development. The four phases were as follows.
 Phase 1. One uniform echogenic area caudal to the fetal
liver in the topographic region of bowel (Fig. 1A);
 Phase 2. In the same anterior region, some portions of
bowel segments were better defined allowing visuali-
zation of the intestinal wall i.e., anechoic areas inter-
mixed with multifocal normal intestinal wall. Peristalsis
was absent (Fig. 1B);
 Phase 3. Bowel segments had clearly defined intestinal
walls, and anechoic areas were fewer when compared to
phase 2; defined segments had mucosal intraluminal
content, with better definition of the mucosal surface
versus the intestinal wall. Peristalsis in some intestinal
portions (Fig. 1C);
Table 1
Description of breeds, age, and litter size of bitches classified according to
the type of delivery May 2013 to April 2014.
Type of delivery Age Breed
(y)
Normal delivery 2 Dog Chinese Crested
5 French Bulldog
5 Miniature Schnauzer
1 Siberian Husky
2 Pug
2 Pekingese
1 Maltese
2 Chihuahua
6 Miniature Schnauzer
Cesarean 2 Dog Chinese Crested
5 Yorkshire Terrier
3 American Staffordshire Terrier
2 English Bulldog
2 English Bulldog
1 English Bulldog
2 Pug
6 Miniature Schnauzer
3 Miniature Schnauzer
683
 Phase 4. Identification of complete intestinal wall, visual
distinction between the mucosal surface and the intes-
tinal wall, ultrasonographic determination of wall layers,
surface mucosadhyperechoic; mucosa, submucosa,
muscledhypoechoic; serousdhyperechoic. Segmental
dilatation of the bowel by intraluminal mucous and fluid
content. Peristalsis in all segments of the bowel (move-
ment every 3 seconds; Fig. 1D).
Table 2 shows gestational ages (days to delivery and
days of estimated gestation), mean, standard deviation, and
median of four phases of intrauterine fetal bowel devel-
opment by ultrasound according to the type of delivery.
Table 3 presents results of the Student t test for the four
phases of intrauterine fetal bowel development comparing
the type of delivery (normal or cesarean), showing a sig-
nificant (a ¼ 0.05) difference between groups only in phase
4 of bowel development.
Semiparametric COX model, coefficient value of the
reference group (normal delivery bitches) was 1.316,
resulting in exp(1.316) ¼ 0.268. This confirms that the
time of ultrasound visualization of the bowel in phase 4 (in
which there is peristalsis) is different in fetuses born by C-
section from those delivered naturally; in other words, the
duration of phase 4 is earlier in fetuses delivered by C-
section.
The probability of survival of fetuses born on any day
during phase 4 was different when comparing the puppies
born by normal delivery with those delivered by cesarean,
resulting in a Kaplan–Meier curve with a stairway shape
(Fig. 2). This difference in survival probability in phase 4
was tested by a log-rank test indicating that the duration of
phase 4 was different between groups.
4. Discussion
In view of the continuous technical improvements in
ultrasound equipment, it is essential to reconfirm data
previously published in the veterinary literature. In this
study, ultrasonographic description of the development of
the fetal bowel was studied because bowel is the organ
whose development is reported to terminate fetal organo-
genesis, indicating a fetal age of 57 days of gestation [5,8,9].
Litter Accurate determination of fetal age is important to
size
reduce the risk of premature birth and consequent fetal
2
deaths by informed decisions on timing of cesarean, if this
3
3 is indicated. Accurate fetal aging is particularly important
7 in brachiocephalic breeds, in which surgical intervention is
7 often necessary for delivery [16–21].
5 In this study, the first ultrasonographic identification of
3
3
the fetal bowel occurred around 39 to 44 days of gestation
4 (Table 2) period. At that time (phase 1), the fetal bowel has
3 ultrasonographic features not described in previous
4 studies. In phase 1, ultrasound characteristics correspond to
3
primitive intestine development, originating from the
9
3 dorsal mesenchymal layer (dorsal mesentery) and is
5 interposed between vascular supply, lymphatics, and neu-
3 rones. Phase 2 is accompanied by the formation of bowel
4 walls, which are derived from the endoderm (bowel inner
4
layer) and splanchnic mesoderm (outer layer) that will
684 E.M.U. Gil et al. / Theriogenology 84 (2015) 681–686

Fig. 1. Ultrasound image showing (A) phase 1: presence of echogenic and homogeneous areas (arrows) in the caudal region to the fetal liver. (B) Phase 2:
beginning of differentiation of wall layers in the fetal bowel (blue arrow), with intermixed anechoic areas (red arrow). No intestinal peristalsis. (C) Phase 3:
identification of intestinal wall segment intermixed with fewer anechoic areas (red arrow) when compared to phase 2. The defined segments showed intra-
luminal mucosal content (blue arrow), and there is a better definition of the mucosal surface versus the intestine wall. Intestinal peristalsis identified in some
bowel segments. (D) Phase 4: well-defined intestinal wall, mucosa versus intestinal wall clearly defined, ultrasonographic definition of bowel wall layers into the
mucosal surfacedhyperechoic; mucosa, submucosa, muscledhypoechoic; serosadhyperechoic; segmental dilatation of the bowel by intraluminal mucous
(arrow) [23]. Intestinal peristalsis in all bowel segments. (For interpretation of the references to color in this figure, the reader is referred to the Web version of
this article.)

develop into the connective muscle of the bowel wall and
will subsequently organize to form four layers of intestinal
wall and contribute to increased intestinal length [22].
The ability to see defined layers of the fetal intestinal
wall and lumen interface, associated with the first visuali-
zation of intestinal peristalsis, heralds the beginning of
phase 3, which occurs at approximately 48 to 54 days of
gestation (Table 2). In this phase, peristalsis is not constant,
and some regions of the bowel exhibit no peristaltic
movement (Fig. 1C). It is this intermittent peristalsis that
defines that the fetus is still in phase 3 of development and
has not completed organogenesis. Errors in interpretation
of peristaltic motion may result in inaccurate determina-
tion of fetal age and consequently inappropriate planning
of surgical intervention (C-section), whereas in fact in
phase 3, there are still approximately 8 to 15 days before
full term (Table 2).
Phase 4 coincides with an approximate fetal age of 57 to
62 days of gestation (Table 2) and probably corresponds with
the descriptions of the fetal intestine as reported in the
literature [5,8–10]. This is the last stage of fetal organogen-
esis. At this time, it is possible to recognize the bowel wall
and distinguish the surface mucosa versus the wall (Fig. 1D).
With high-resolution ultrasound equipment and appro-
priate adjustments to examine the fetus, three layers of in-
testinal wall (as in adult dogs) [23] can be identified.
However, ultrasonographic visualization of five wall layers
(as in the adult intestine) is not possible, presumably because
of the size of structures when compared to adult patients.
In phase 4, intraluminal contents are well defined, we
suggest that this finding is related to increased meconium
in the gastrointestinal tract, which in man correlates to
progression of pregnancy [24,25]. In human fetuses, it is
known that propulsion of meconium along the intestine
causes gut distension and sufficient peristalsis to move the
luminal contents [26], a finding also observed in our study.
Identification of anechoic intraluminal fluid is a char-
acteristic of intestinal maturation of human fetuses and
corresponds to meconium. Meconium accumulates in the
intestine partially distending the bowel and facilitating
identification of peristalsis. In human fetuses, this finding,
together with visualization of the stomach and bladder, is
some of ultrasonographic features that assist in deter-
mining progression of fetal organogenesis [27].
 E.M.U. Gil et al. / Theriogenology 84 (2015) 681–686 685

Table 2
Descriptive statistics of four phases of ultrasound visualization of fetal bowel development intrauterine correlated fetal age determined counting backward
considering delivery as Day 0, categorized according to the type of delivery (normal delivery or cesarean), May 2013 to April 2014.

US phases development Gestational age Median Average Standard deviation Estimated gestational age
of fetal bowel (days from delivery) (days of gestation)
Normal delivery
Phase 1 19–23 21 20.86 1.35 40–44
Phase 2 15–19 16 16.67 1.22 44–48
Phase 3 9–13 10 10.67 1.41 50–54
Phase 4 1–4 2 2.22 1.09 59–62
Cesarean
Phase 1 20–24 22 21.44 1.51 39–43
Phase 2 14–19 16 16.56 1.81 44–49
Phase 3 8–15 11.5 11.75 2.25 48–55
Phase 4 2–6 4 4.11 1.36 57–61

Phase 1: viewing an echogenic area in the topographic region of the bowel; phase 2: beginning visualization of definition intestinal wall without peristalsis;
phase 3: peristalsis visualization in some segments of the bowel; phase 4: peristalsis visualization in all segments (movement every 3 seconds).
Abbreviation: US, ultrasonographic.

Care should be taken during ultrasound examination
when differentiating phases 3 and 4 of intestinal develop-
ment as this distinction is subtle. Assessment of peristalsis is
the key point: in phase 4, intestinal peristalsis is visible
immediately, whereas in phase 3, identification of peristalsis
is only possible after one minute of observation. Another
important point for distinction between phases 3 and 4 is
that intraluminal fluid is more evident in phase 4. It is
essential that decisions with regard to planning cesarean are
not rushed as this could result in death of premature fetuses.
Phases 1, 2, and 3 of fetal bowel development occurred,
on average, at the same fetal ages (as determined by ul-
trasonography), in both groups of bitches (normal delivery
and C-section) (Table 2); reporting that development of
organs is equivalent in both groups. However, in this study,
we show that there were, on average, twice as many days
until delivery from the onset of phase 4 in bitches which
subsequently had cesarean deliveries compared to those
bitches which achieved normal delivery. The difference in
the duration of phase 4 (in days) was confirmed statistically
by the Student t test. It is likely that those bitches which
subsequently had cesarean deliveries went beyond full
term, whilst investigators waited for puppies to be born by
normal delivery. Cesareans were only requested once
normal delivery had failed to occur, and fetuses became
distressed. The Cox model of proportional hazards resulted
in a significant coefficient showing the differences in the
duration of phase 4 development stage between fetuses of
bitches born by cesarean deliveries compared to fetuses of
bitches which had a normal delivery.
The probability of survival for fetuses born on a partic-
ular day is illustrated by the Kaplan–Meier curve (Fig. 2)
and is correlated to the degree of fetal maturation on each
day of phase 4 in both groups of dogs i.e., once intestinal
peristalsis is consistently found ultrasonographically. Fe-
tuses born at this time had a 10% chance of survival if
delivered naturally and a 20% chance of survival if delivered
by C-section. This suggests that fetuses from both groups
were probably insufficiently mature to survive extra utero.
This shows that ultrasound detection of fetal intestinal
peristalsis on the first day of phase 4 is insufficient alone to
indicate fetal maturity. Natural delivery occurred 4 days
after the first detection of peristalsis and after 6 days in
bitches submitted to C-section. When intestinal peristalsis
is found on a single ultrasound examination, fetal matu-
ration should be confirmed by additional evaluation of
other organs.
The Kaplan–Meier curve (Fig. 2) shows a difference in the
probability of survival between fetuses of the two groups in

Table 3
Values obtained in the Student t test in which time (in days) of intestinal
development visualization is analyzed in four phases of development,
comparing the bitches that had normal delivery versus cesarean section.

US phases development 95% Confidence interval DF P value

of fetal bowel
Lower limit Higher limit
Phase 1 2.1248 0.9502 14 0.4257
Phase 2 1.451 1.6732 14 0.881
Phase 3 3.1085 0.9419 12 0.2653
Phase 4 3.1289 0.6489 15 0.0054a

Phase 1: viewing an echogenic area in the topographic region of the

bowel; phase 2: beginning visualization of definition intestinal wall
without peristalsis; phase 3: peristalsis visualization in some segments of
the bowel; phase 4: peristalsis visualization in all segments (movement
every 3 seconds).
Abbreviations: DF, degrees of freedom; US, ultrasonographic. Fig. 2. Kaplan–Meier curve showing the probability of survival for fetuses
a
Significant at 5%. born on any day during phase 4.
686 E.M.U. Gil et al. / Theriogenology 84 (2015) 681–686
stage 4. This difference between groups was tested by the
log-rank test which proved to be statistically significant
(P ¼ 0.05). The difference in probability of survival between
the groups is because there are more days of development
required for fetuses in the group of bitches undergoing
cesarean deliveries. Once again, these extra days are prob-
ably due to delays in delivery; normal delivery was expected
in the cesarean delivery group until such time as the fetus
became distressed [12,13], and surgery was indicated.
The limitations of this study are that all fetuses were born
healthy, despite indications for C-section, fetal distress was
based on ultrasound detection of variations in fetal heart
rate [13]. Another factor that must be considered is that
there was a wider than expected age at which bitches were
presented for examination because these were owned pets
and not experimental dogs. Other limitations of this study
were breed variations, the small number of animals
included and the absence of LH measurements.
Intestinal peristalsis is an important finding that pro-
vides evidence of completion of canine fetal organogenesis.
However, it should be noted that, even after complete
development of the bowel, ultrasonography cannot be
relied on to determine functionality (maturation) of this
organ. This was found in this study because even after ul-
trasonographic confirmation of fetal intestinal develop-
ment, up to a further 4 days elapsed before natural delivery
and up to 6 days before signs of fetal distress were evident.
Ultrasonographic evidence of completion of bowel
organogenesis should not be used as the sole parameter for
scheduling C-section. We suggest daily fetal monitoring by
ultrasound from phase 4 of intestinal development because
oscillations of fetal heart rate [13] begin at this time and
this may be a more reliable predictor of day of parturition.
4.1. Conclusions
Evaluation of the development of a pregnancy is possible
using ultrasonographic monitoring of intestinal development
and this can reliably identify the end of fetal organogenesis.
Ultrasonographic detection of intestinal segments with
visualization of wall layers and associated peristalsis should
not however be used as the sole indicator for C-section
planning because it is not possible to determine ultrasono-
graphically whether the bowel is functional (mature).
Acknowledgments
The authors thank Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior (CAPES) for the scholarship granted
and Eliane de Fátima Coimbra for statistical help. Our main
thanks go to the owners who agreed to cooperate with this
study.
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