animal
Animal (2016), 10:8, pp 1336–1341 © The Animal Consortium 2016
doi:10.1017/S175173111600029X
Embryonic survival at day 9, 21 and 35 of pregnancy in intact and
unilaterally oviduct ligated multiparous sows
P. Langendijk1†a, T. Y. Chen1, R. Z. Athorn2 and E. G. Bouwman1
1
South Australian Research and Development Institute, Roseworthy Campus, Roseworthy 5371, South Australia; 2School of Animal and Veterinary Sciences,
The University of Adelaide, Roseworthy Campus, Roseworthy 5371, South Australia
(Received 7 January 2015; Accepted 11 January 2016; First published online 1 March 2016)
To investigate the effect of uterine space on timing of embryonic mortality, multiparous sows were left intact (CTR; n = 42) or
subjected to unilateral oviduct ligation (LIG; n = 23), after their first post wean oestrus. Intact sows were killed at day 9 (n = 10),
day 21 (n = 15), or day 35 (n = 17), and LIG sows were killed at day 21 (n = 11) or day 35 (n = 12) of gestation. At day 9,
92% of ovulations were represented by an embryo. At day 21, embryonic mortality was 24% and was not altered by increasing
uterine space. At day 35, space per embryo was twice as large in LIG sows (30 ± 3 v. 16 ± 0.8 cm), and implantation length tended
to be larger (19.0 ± 1.2 v. 15.5 ± 1.3 cm). Between day 21 and day 35, CTR sows lost another 8% to 14% of their embryos,
whereas LIG sows lost none. Embryos tended to be heavier (4.9 ± 0.2 v. 4.3 ± 0.3 g) in LIG sows. In conclusion, embryonic loss in
multiparous sows is 24% by day 21 and is not related to space, whereas after day 21 limited space causes additional 8% to
14% embryonic mortality in intact sows only.
Keywords: sows, uterine, crowding, embryo, survival
Implications
In multiparous sows, embryonic mortality at day 21 of
gestation is already 24%, and is independent of space. This
means that either a percentage of embryos is intrinsically
unfit to survive, or there are interactions other than competition for space between embryos in a litter, direct or through
influences on the uterine environment, that limit the survival
of some embryos.
Introduction
Prenatal losses in the pig range between 30% to 50% in
commercial genetic lines (Pope et al., 1972; Geisert and
Schmitt, 2002). The majority of these losses occur during the
embryonic phase (before day 35), with 20% to 30% of
embryos lost by the 3rd week and another 10% to 15%
being lost by the end of the embryonic phase (Ford et al.,
2002). Experimental alteration of the available uterine
space per embryo, by using a range of techniques (e.g. Dziuk,
1968; Père et al., 1997; Town et al., 2004) has shown that by
day 30 to 35 of gestation more embryos are lost when
uterine space is limiting, hence the term uterine capacity.
a
Present address: Trouw Nutrition R&D, Veerstraat 38, 5830 AE Boxmeer, the
Netherlands.
†
E-mail: [email protected]
Even though uterine length is plastic and increases with the
number of occupying embryos, Chen and Dziuk (1993)
established that a minimum length of around 25 cm per
embryo is required at fertilisation to maximise survival.
It is not clear when exactly uterine space becomes limiting to
the survival of porcine embryos, since most of the experiments
mentioned above made observations between day 30 and 40 of
gestation. Most embryos survive until day 12 (93% to 96%;
Anderson et al., 1993). After that, elongation (day 11 to 13),
spacing, and implantation (day 15 to 17) occur, however there
are few reports of losses during these specific periods. The few
studies available before day 30, report losses to be 18% to
35%, and mostly independent of space. However, these reports
are all based on gilts, and in some studies there is no clear
description of stage of the embryos (Dziuk, 1968), controls were
super-ovulated (Pope et al., 1972; Webel and Dziuk, 1974), or
number of observations were limited (Knight et al., 1977).
Studies in multiparous sows have only been reported by King
and Williams (1984) and Town et al. (2004), for day 30 gestational age. Multiparous sows have a much higher ovulation rate
than gilts and the available area for each embryo is smaller than
in gilts, despite the greater uterine length. Therefore, the current
study was undertaken to provide data on embryonic survival in
multiparous sows rather than gilts, and to determine whether
space limits embryonic survival before day 30 in multiparous
sows specifically, using a unilateral oviduct ligation model.
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Uterine space and embryonic survival in multiparous sows
Material and methods
Multiparous sows (having had 2 to 11 litters) of a Large
White × Landrace cross were weaned and then either left
intact (CTR, n = 42) or subjected to unilateral oviduct
ligation (LIG, n = 23) after the first post weaning oestrus.
Oviduct ligated sows
Oviduct ligation was performed in LIG sows within 10 days
following the first oestrus and sows were mated and
ovulation was assessed as described below, at the second
oestrus.
Sows were fasted for 12 h before surgery. The animals
were anaesthetised by thiopentone sodium at a dose rate of
10 mg/kg of BW administered by injection via an ear vein.
Anaesthesia was maintained using a combination of
isoflurane and oxygen. Unilateral oviduct ligation was
performed by mid-ventral laparotomy. Randomly, either the
right or the left oviduct was looped and then tied off at the
base of the loop with one absorbable suture. The strictured
part of the loop was then excised. The operation wound was
closed using vicryl absorbable sutures. Animals were given
250 mg IM (intramuscular) of Flunixil (Flunixin-Meglumine,
Norbrook Laboratories, Northern Ireland) as an analgesic and
1050 mg IM of Moxylan (amoxicillin; Jurox, Rutherford,
NSW, Australia) as an antibiotic. Sows then received
1050 mg of IM per day of Moxylan for 2 days post-surgery.
The rationale for the unilateral oviduct ligation was to reduce
the number of embryos entering the uterus after fertilisation
by 50% on average, and as a result doubling the available
uterine space per embryo, compared with intact sows.
Heat detection and ultrasound
All sows received boar contact twice a day (morning and
afternoon) from 5 days before expected (second) oestrus, in a
detection-mating-area, until oestrus had ceased. Sows were
mated with 3 billion sperm cells from pooled semen at first
standing and then every 24 h until ovulation was detected.
Ovulation was assessed using trans-rectal ultrasound
(3.5 MHz sector probe; Aquila Vet, Pie Medical, the
Netherlands), once per day. Once the pre-ovulatory follicles
had disappeared, time of ovulation was estimated as having
occurred in the 24 h prior.
Reproductive tracts
Intact sows were slaughtered at day 9, day 21 or day 35 of
gestation (day 0 is day of ovulation), and LIG sows at day
21 and 35. The day 9 observations were included to
demonstrate that the heat detection and insemination
strategy resulted in >90% fertilisation in order to prove that
losses at later stages occurred after day 9. We assumed
that there would be no crowding before day 9, and more
importantly, that at this stage there is negligible mortality,
based on the observations by Anderson et al. (1993) and
earlier work from our lab, and that ovulations that are not
presented by an embryo probably reflect flushing inefficiency
or unfertilised oocytes. In LIG sows, the ligated oviduct was
double-checked for (non) patency by infusing saline into the
infidibulum. Reproductive tracts were collected to assess
ovulation rate, weight of individual corpora lutea after
excision, number of embryos, and gross morphological
characteristics of uterine horns, placentae and implantations
(day 21 and day 35). Length of implantations was measured
and embryos were weighed. Placentae were removed from
the implantation sites and then spread on wax paper and
traced. After drying the size of the traced area was calculated
by relating its weight to a standard size piece of wax paper.
Arbitrarely, the 10% of embryos lowest in weight were
considered as unviable. This included embryos that were
obviously unviable based on haemorrhagic appearance or
showing signs of disintegrating and a brownish colour.
For the day 9 gestational stage, uterine horns were flushed
using phosphate buffered saline, and subsequently embryos
were counted and dimensions were measured under a
dissecting microscope. Presence of unfertilised oocytes
was also recorded.
Embryonic survival was calculated as the percentage of
ovulations that were represented by an embryo. For LIG
sows, only the corpora lutea on the ovary with the intact
oviduct were counted.
Statistical analysis
Statistical analyses were performed using the SAS statistical
package (9.3 edition; SAS Institute Inc, Cary, NC, USA).
Differences between treatments (LIG v. controls) and
between stages of gestation were tested using the GLM
procedure. Regression analysis, for example between the
number of embryos and the number of ovulations, was
also performed using the GLM procedure.
Results
Overall, ovulation rate was 22 ± 0.9. Ovulation rate was
18.7 ± 0.7 (n = 18) for second litter sows, 20.5 ± 0.9
(n = 12) for third litter sows, 19.5 ± 2 (n = 7 for fourth litter
sows, and 22.8 ± 0.8 (n = 28) for older sows. Luteal tissue
mass was 14.6 ± 0.9 g per sow at day 9, 8.5 ± 0.3 g at
day 21 and 9.3 ± 0.4 g at day 35. At day 21 and day 35, the
distribution of embryos across horns in ligated sows was
even, with 52% of the embryos in the horn ipsilateral to
the patent oviduct (range 33% to 73%).
At day 9 of pregnancy almost every (92%) ovulation was
represented by an embryo, and, every extra ovulation resulted
in 0.9 extra embryos (r = 0.6; P < 0.01). At later stages too,
the number of embryos was correlated to the number of
ovulations (r = 0.78; P < 0.05), and each extra ovulation
resulted in 0.6 extra embryos at day 21 and 0.5 embryos at
day 35 of gestation (P < 0.05). Embryonic survival decreased
with ovulation rate (r = − 0.47; P < 0.01), by 0.6% for every
ovulation at day 21, and by 1.3% for every ovulation at day 35
(P < 0.01). The relationship between embryonic survival and
ovulation rate is reported in Figure 1.
In intact animals, the available space per embryo was
strongly negatively correlated (r = − 0.85) to the number of
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Langendijk, Chen, Athorn and Bouwman
Figure 1 Number of embryos surviving at day 21 (top panel) and at day
35 (bottom panel) of gestation in relation to ovulation rate for intact
sows (closed circles) and oviduct ligated sows (open circles). At day 21,
each extra ovulation resulted in 0.73 extra embryo (R 2 = 0.68). At day
35, each extra ovulation resulted in 0.8 extra embryo in ligated sows,
and 0.6 extra embryo in intact sows (R 2 = 0.52).
ovulations. At day 21, the length of the uterine horns was
unaffected, however, at day 35 the length of the uterine horn
increased by 6 cm with each extra embryo (r = 0.41;
P < 0.05). Nevertheless, at day 35 the available space per
ovulation in intact sows was half that in ligated sows, with
all intact sows having an average available space per
ovulation smaller than 25 cm (Figure 2). At day 21, the extra
space available due to ligation did not affect the area of the
placentas (67 ± 9 v. 84 ± 22 cm2, ns), however, at day 35
placentas in ligated animals spanned an 18% greater area
(600 ± 54 v. 709 ± 23 cm2). The crowding effect at day 35
was also evident from the length of the implantation sites in
intact animals (15.5 ± 1.3 cm) being almost similar to the
available space (16.1 ± 0.8 cm), whereas in ligated sows the
space taken up by implantation sites (19 ± 1 cm) was longer
than for intact sows but far smaller than the available
space (30 ± 2.9 cm) (Table 1; Figure 2).
The frequency distribution for area of individual placentas
followed a similar pattern for intact and ligated sows at day
21, which is reflected by the mean placenta area in Table 1.
At day 35 however, in ligated sows there was a shift towards
larger placentas (area), which is reflected in both mean placenta area and mean implantation length. For example,
placenta area was smaller than 500 cm2 in 45% of placentas
Figure 2 Top two panels: Available length (cm) of uterine horn per
ovulation (calculated) and actual mean area of placentation (cm2), in
relation to the number of available ovulations for intact sows (closed circles)
and sows with unilateral oviduct ligation (open circles). Bottom panel:
Embryo weight in relation to area of placentation. All data from day 35.
in intact animals, but only in 12% of ligated animals
(P < 0.01). The size of unoccupied areas of the uterine horns
showed a similar (normal) distribution across treatments,
although the mean length of unoccupied spaces was larger
for ligated sows at day 21 (Table 1). The size of unoccupied
spaces did not increase from day 21 to day 35, whereas that
of occupied spaces did.
By day 21 most embryonic mortality (~24%) had already
occurred and was not influenced by available space. In
ligated animals there was no more embryonic mortality after
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Uterine space and embryonic survival in multiparous sows
Table 1 Embryonic survival and characteristics of placentation and embryonic development at day 9, day 21 and day 35 of gestation
Day 9
n
Ovulations
Embryos (n)
Implantation rate** (%)
Embryonic survival (%)
(range)
Viable embryo survival (%)
Space (cm per ovulation)
Length of implantations (cm)
Length of unoccupied spaces (cm)
Size of detached placentae (cm2)
Embryo weight (g)
Efficiency (g/10 cm)
Efficiency (g/100 cm2)
Uterine weight full (g)
Uterine weight empty (g)
Uterine length (cm)
Luteal weight (g)
10
24.2 ± 1.5
22.0 ± 1.0
92 ± 3
(77 to 106)
Day 21
Day 21 oviduct ligated
Day 35
Day 35 oviduct ligated
15
20.9 ± 1.5a
15.7 ± 0.9a
82 ± 5
78 ± 4
11
11.6 ± 0.8b
9.0 ± 0.6b
83 ± 5
79 ± 5
17
20.3 ± 0.9a
13.0 ± 1.0a
69 ± 4a
64 ± 4*a
70 ± 3*a
(33 to 83)
59 ± 4
16.1 ± 0.8a
15.5 ± 1.3x
8.5 ± 1.7
600 ± 54x
4.3 ± 0.3x
3.2 ± 0.4
0.87 ± 0.08
3980 ± 279x
1920 ± 141
334 ± 15x
12
10.7 ± 0.9b
8.5 ± 0.8b
84 ± 4b
79 ± 3b
(50 to 100)
76 ± 5
14.3 ± 1.3a
9.9 ± 1.1
7.4 ± 1.3a
66.8 ± 9.3
0.22 ± 0.03
0.30 ± 0.06
0.42 ± 0.07
1459 ± 72
1133 ± 59
274 ± 16
14.6 ± 0.9
(57 to 100)
75 ± 5
22.7 ± 1.5b
11.4 ± 1.2
13.8 ± 2.1b
88.6 ± 23.0
0.25 ± 0.05
0.25 ± 0.05
0.37 ± 0.04
1330 ± 150
1110 ± 70
255 ± 14
8.5 ± 0.33
(60 to 100)
77 ± 3
30.0 ± 2.9b
19.0 ± 1.2y
13.8 ± 4.3
709 ± 23y
4.9 ± 0.2y
2.8 ± 0.3
0.71 ± 0.06
3272 ± 302y
1830 ± 103
296 ± 16y
9.3 ± 0.4
P < 0.05; x,yP < 0.10 within rows.
*70% survival when excluding outliers.
**Percentage of ovulations represented by an implantation mark, including ‘unoccupied’ implantations where there are visible marks of implantation but no embryos present.
a,b
day 21. In intact animals, however, another 8% to 14%
mortality occurred, depending on whether outliers were
included, bringing the viable embryonic survival by day 35
down to 59% in intact animals as opposed to 77% in ligated
sows. Although the reduced available space in intact
animals clearly reduced the placenta area, there was no
clear relationship between mean placenta area and
embryonic survival rate, at sow level. There was also no clear
relationship between mean placenta area and embryo
weight (Figure 2), however, in the ligated group the extra
available space tended to increase embryo weight.
Moreover, at the embryo level embryo weight increased
by 0.16 g per 100 cm2 placenta at day 21 (r = 0.6; P < 0.01),
and with 0.28 g per 100 cm2 placenta at day 35 (r = 0.4;
P < 0.01).
Discussion
In this study, two-thirds (24% out of 41%) of embryonic
mortality in multiparous sows occurred before day 21. The
mortality before day 21 was not due to space limitation.
This has not been reported before for multiparous sows.
Père et al. (1997) and Town et al. (2004) also used unilateral
oviduct ligation as a means to increase the available space
for embryos, but the earliest stage of gestation they reported
on was day 30 to 35. In gilts, oviduct ligation models have
been used to show that early embryonic mortality is not
related to space (Dziuk, 1968; Webel and Dziuk, 1974), and
Freking et al. (2007) showed that selection for uterine
capacity did not change early embryonic losses. However,
these studies did not investigate embryonic survival before
day 25 of gestation.
Assuming fertilisation rate is 90% to 95%, there was
minimal embryonic loss before day 9 and recovery rates
lower than 100% at this stage were presumably due to
efficiency of the flushing procedure. Since implantation rate
was 82% of the potential number of embryos, 18% did not
even implant, indicating that some of the early mortality
occurred during the period of spacing (after day 9 but before
implantation) and some around implantation. Implantation
rate includes those placentations that do not have an embryo
attached, and is therefore higher than embryonic survival
rate, which only includes ovulation represented by an
embryo. From our observations in this study and numerous
other studies we have performed, it appears that at
postmortem some implantation sites show an implantation
mark and remnants of the chorio-allantois, without the
presence of an embryo. This is evidence of embryos that have
commenced implantation but failed to survive, leaving an
‘unoccupied’ implantation site. These areas are generally
small. Embryos that would have implanted but later
been resorbed, would have left implantation marks on the
endometrium.
By doubling the available space in the LIG sows, embryonic mortality from day 21 to day 35 was eliminated. In intact
sows, embryo mortality between day 21 and day 35 was
14% when including all sows, and 8% when excluding
two sows that had embryo mortality lower than 40%.
This threshold was based on the distribution of embryonic
mortality which clearly showed that observations below
40% were well outside the normal distribution. It is
debatable whether the outliers should be included in the
analysis of mortality. On one hand, they may be a
consequence of crowding as they only occurred in the intact
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Langendijk, Chen, Athorn and Bouwman
animals. On the other hand, the outliers were animals with
ovulation rate below the mean, which would suggest that
factors other than crowding were a cause of the increased
embryonic mortality. Either way, embryonic mortality after
day 21 was only observed in intact animals with limited
space per embryo, and not in the ligated sows. Similarly,
studies by Town et al. (2004) and Père et al. (1997) show that
doubling the uterine space per embryo by ligation reduces
embryonic mortality at day 30 to 35. Clearly, at this stage the
area of the placenta becomes a limiting factor in facilitating
nutrient uptake, which was reflected by the smaller placentas
in intact sows, and by the fact that nearly all the available
space was occupied by implantations, leaving hardly any
space to increase physical area of the implantations.
The element of crowding was also reflected in the positive
relationship between implantation area and embryo weight,
and it may be speculated that the higher percentage of
smaller placentas in intact sows may cause additional
mortality of foetuses later in gestation. As a consequence,
sows with a high ovulation rate may not only suffer a higher
embryonic mortality post day 21, but also in the foetal stages
because of insufficient placental interface.
If embryonic mortality before day 21 is independent of
space, the question is what then causes embryonic mortality
around spacing and implantation. From day 8 to day 10,
embryos migrate through the uterine horns and some will
cross the bifurcation between the left and right horn.
Between day 10 and day 13, embryos elongate and space
along the uterine horns. Around day 12, embryos start to
secrete oestrogens, and at the same time they start the
process of spacing, in which they position themselves
throughout the uterine horns aligning themselves in
preparation for implantation at around day 15 (Dziuk, 1985).
The process of spacing is a co-ordinated mechanism, during
which the available uterine space is distributed fairly evenly
among the embryos. Studies with inert, oestrogen-soaked
beads have shown that this process may be facilitated by
mild contractile activity of the uterus, induced by oestrogens
originating from the embryos, with presence of embryos in
localised areas of the uterus inducing more or less uterine
contractility (Pope et al., 1986). Spacing is independent of
the number of embryos, and small and large litters both
migrate and space evenly (Dziuk, 1968). Whether there is
direct communication between embryos is not clear,
however, from our own observations implantation sites
hardly ever overlap, which would suggest that there is. In the
process of spacing and implantation, developmental stage of
the embryos and variation between embryos play a role
in determining which embryos survive (Geisert and Schmitt,
2002).
Before implantation, variation in embryonic development
may be such that advanced embryos influence the uterine
environment in a way that is detrimental to more delayed
embryos. Geisert et al. (2006) showed that treatment of sows
with oestrogens before day 12 had a negative impact on
embryonic survival. Embryos will still elongate, but not
survive to day 16 (Morgan et al., 1987). This suggests that
there is a window, before elongation, in which oestrogens
are detrimental to embryonic development through their
effect on the uterine environment relative to the developmental stage of the embryos. Treatment with oestrogens at a
later stage, when embryos start to secrete oestrogens
themselves, is not harmful to embryonic survival (Pope et al.,
1986). Advanced embryos may start to secrete oestrogens at
a stage when retarded embryos are compromised by the
same oestrogens, and this may be another mechanism
through which variation in embryonic development causes
embryonic mortality. In this respect, it is noteworthy that
Meishan embryos develop slower, are smaller in general and
secrete less oestrogens (Anderson et al., 1993). This would
reduce the variation between embryos once a litter reaches
the critical stage when the first embryos start elongating and
secreting oestrogens. The amount of oestrogen secreted in
white breeds is probably well above what is necessary for
embryonic development, since reduction of secretion with
aromatase inhibitors by 57% did not impede embryonic
development (O’Neill et al., 1991).
In conclusion, in multiparous sows around 24% of embryos
are lost during spacing and implantation, and this loss is not
related to uterine space, but probably due to intrinsic
embryonic quality or variation, interaction between embryos
and/or the uterine environment, or a combination of these
factors. After implantation, uterine space is limiting, and causes
another 10% mortality between day 21 and day 35.
Acknowledgements
The authors gratefully acknowledge the CRC for High Integrity
Australian Pork for their funding in this project.
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