Accepted Manuscript Canine fetal heart rate: Do accelerations or decelerations predict the parturition day in bitches? E.M.U. Gil, D.A.A. Garcia, A.T. Giannico, T.R. Froes PII:
S0093-691X(14)00205-2
DOI:
10.1016/j.theriogenology.2014.04.025
Reference:
THE 12790
To appear in:
Theriogenology
Received Date: 5 February 2014 Revised Date:
22 April 2014
Accepted Date: 30 April 2014
Please cite this article as: Gil EMU, Garcia DAA, Giannico AT, Froes TR, Canine fetal heart rate: Do accelerations or decelerations predict the parturition day in bitches?, Theriogenology (2014), doi: 10.1016/j.theriogenology.2014.04.025. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
REVISED
ACCEPTED MANUSCRIPT 1
Canine fetal heart rate: Do accelerations or decelerations predict
2
the parturition day in bitches?
3
E.M.U. Gila, D.A.A. Garciaa, A.T. Giannicoa, T.R. Froesa*
5
a
RI PT
4 Federal University of Paraná
*Address correspondence to: T.R. Froes
8
Federal University of Paraná
9
Rua dos Funcionários 1540. Juvevê. Zip Code 80035-050
M AN U
7
SC
6
Curitiba City, Paraná State, Brazil
11
Phone: 55 (41) 3350-5616, Fax: 55 (41) 3350-5725
AC C
EP
TE D
10
1
REVISED
ACCEPTED MANUSCRIPT Abstract
13
Ultrasonography is a safe and efficient technique for monitoring fetal development and
14
viability. One of the most important and widely used parameters to verify fetal viability
15
is the fetal heart rate (HR). In human medicine, the fetal HR normally oscillates during
16
labor in transient accelerations and decelerations associated with uterine contractions.
17
The present study investigated whether these variations also occur in canine fetuses and
18
its relationship to parturition. A cohort study was conducted in 15 pregnant bitches
19
undergoing two-dimensional high-resolution ultrasonographic examination during the
20
8th week of gestation. Fetal HR was assessed in M-mode for 5 min in each fetus in all
21
bitches. In addition, the bitches were monitored for clinical signs of imminent
22
parturition. Associations between the HR, antepartum time, and delivery characteristics
23
were evaluated with a Poisson regression model. Fetal HR acceleration and deceleration
24
occurred in canine fetuses and predicted the optimal time of parturition. These findings
25
can help veterinarians and sonographers better understand this phenomenon in canine
26
fetuses.
27
Keywords:
fetal
ultrasonography,
pregnancy,
gestational
ultrasound
AC C
EP
canine,
TE D
M AN U
SC
RI PT
12
2
REVISED
ACCEPTED MANUSCRIPT 28
1. Introduction Canine gestation lasts 64–66 days based on the pre-ovulatory serum luteinizing
30
hormone peak [1]. However, full-term gestation ranges from 57 to 72 days post-
31
breeding, depending on the breed, litter size, and the individual proestrus and estrus
32
duration [2,3,4,5]. It is difficult to predict the exact day of partum in bitches. An
33
accurate method predicting the precise time of parturition in bitches would prove useful
34
by allowing timely intervention to minimize or prevent reproductive losses.
SC
RI PT
29
Ultrasonography is a safe and effective method for monitoring fetal development
36
and viability [6]. One of the most important and widely used parameters to verify fetal
37
viability is fetal heart rate (HR). Fetal stress resulting from hypoxia can occur during
38
dystocia and manifests as a decreased HR [7]. Fetal HR should be greater than 220
39
beats per min (bpm); HRs between 180 and 220 bpm indicate moderate fetal distress,
40
while values less than 180 bpm indicate severe fetal distress [8].
TE D
M AN U
35
In human medicine, Hon [9] and Caldeyro-Barcia et al. [10] reported that fetal
42
HR oscillated during phase I of labor. They observed transient accelerations and
43
decelerations in the normal fetal cardiac activity resulting from uterine contractions.
44
Such events have not been described in veterinary medicine. Therefore, the present
45
study assessed whether these changes occur in dogs, their relationship to parturition,
46
and their utility in predicting a suitable time for a Caesarean section.
48
AC C
47
EP
41
2. Materials and Methods
49
This cohort study was conducted on 15 pregnant bitches that underwent an
50
ultrasonographic examination during the 8th week of gestation. All procedures were
51
conducted in accordance with the Animal Use Committee guidelines. In all bitches, the 3
REVISED
ACCEPTED MANUSCRIPT examination was performed using two-dimensional ultrasonographic equipment and
53
high-resolution imaging (Ultrasonix [SONIX OP, Ultrasonix Ltd., Richmond, BC,
54
Canada], Esaote [MyLab 30, Genova, Italy], and General Electric [Logic 3 Expert, GE
55
Healthcare, Wauwatosa, WI, USA]). Electronic convex and linear multifrequency
56
transducers ranging from 2.5 to 14.0 MHz frequencies were selected according to the
57
size of the animal. Abdominal hair was clipped to optimize ultrasonographic image
58
acquisition.
SC
RI PT
52
Fetal HR was evaluated using M-mode for 5 min per fetus in all pregnant bitches
60
up to a maximum four fetuses. When more than four fetuses were present, we evaluated
61
at least five fetuses in different positions. Fetal distress was defined as a HR
62
consistently within a 160- to 190-bpm range. HR was measured at 72, 48, 24, 12, and
63
between 6–1h before parturition. Fetal HR measurement during the final antepartum
64
period (6–1h) varied depending on the delivery method; in bitches undergoing
65
caesarean surgery, the fetal HR was assessed 1 h preoperatively, while in those
66
undergoing normal labor, the final ultrasound examination was performed within 6 h
67
antepartum.
EP
TE D
M AN U
59
Sonographic examinations were performed in all dogs by two sonographers, one a
69
member of the Brazilian College of Veterinary Radiology and the other an
70
echocardiographer who assessed all HR-related sonographic findings during the
71
examination.
AC C
68
72
In addition to sonographic monitoring, the bitches were tracked clinically for
73
signs of imminent delivery including decreased rectal temperature (less than 37.2°C),
74
milk yield, nesting behavior, and vulvar discharge.
4
REVISED
ACCEPTED MANUSCRIPT Data collation and analysis were conducted using Microsoft Office Excel
76
(Microsoft® Office 2007 for Windows, Redmond, WA, USA) and R for Windows
77
(version 3.0.1, R Foundation for Statistical Computing, Vienna, Austria, 2013). To
78
evaluate the association between HR, time, and delivery characteristics, a Poisson
79
regression model was used. A descriptive statistical analysis was performed and
80
adjusted for generalized linear model categorical data before implementing the Poisson
81
regression. The following variables were assessed: variable fetal HR response (bpm),
82
the explanatory variables (group of animals), and the antepartum period (6–1h). A
83
Poisson distribution was modeled for the HR counts, and a Poisson regression analysis
84
estimated the effect of HR acceleration and deceleration antepartum The Poisson
85
regression was fitted to the fetal HR data in the 15 cases according to the experimental
86
group and antepartum duration. The estimate for Group 1 (normal parturition) was
87
compared to other group estimates. A P-value of α = 5% was considered significant,
88
and the significance of each parameter was analyzed relative to the value set. The
89
groups were established according to the clinical findings.
TE D
M AN U
SC
RI PT
75
91
3. Results
EP
90
Fifteen bitches were included in the study and ranged from 1 to 7 years of age.
93
Of these, 3 had normal deliveries, and 12 underwent Caesarean section (Table 1). They
94
were categorized into 3 groups: Group 1 comprised bitches undergoing normal
95
parturition (bitches 1–3); Group 2 comprised bitches that were referred for a Caesarean
96
section with one or more (but not all) fetuses in distress (bitches 4–12); and Group 3
97
comprised bitches that were referred for a Caesarean section with all fetuses in distress
98
(bitches 13–15) (Figure 1).
AC C
92
5
REVISED
ACCEPTED MANUSCRIPT The fetal HR variability was measured and found to be consistent with
100
accelerations and decelerations. These changes occurred during the entire study period
101
from 72 h until 6–1 h antepartum. Initially, HR variations occurred only in select
102
fetuses, but as parturition approached, all fetuses presented these variations. HR
103
acceleration and deceleration variations alternated and became extreme as parturition
104
approached. HR extremes of 143 to 205 bpm were observed over a 4 s period and
105
analyzed by M-mode, as shown in Figure 2.
SC
107
Figure 3 summarizes the variable fetal HR (bpm) distribution by bitch between 6 and 1 h antepartum.
M AN U
106
RI PT
99
108
The fetal HR dispersion during the antepartum period for bitches in Groups 1
109
and 2 is shown in Figure 4. As parturition approached, the fetal HR decelerations
110
reached a 103 bpm minimum and sustained maximum values above 200 bpm. All fetuses in Group 1 (3/3) had HR acceleration
TE D
111
and deceleration 6–1 h antepartum ranging from 119 to 242 bpm. In bitch 1, the fetal
113
HR accelerations and decelerations began within 12 h antepartum in all fetuses. In bitch
114
2, fetal HR changes were observed in just a few fetuses 48 h antepartum. In bitch 3,
115
acceleration and deceleration was observed in select fetuses within 72 h antepartum, but
116
as parturition approached, additional and eventually all fetuses presented HR
117
accelerations and decelerations (Figure 5).
AC C
118
EP
112
Fetuses in two English Bulldogs in Group 2 (2/9) (bitches 4 and 5) had fetal
119
distress antepartum. HR acceleration and deceleration began 12 h before the Caesarean
120
section; this variation persisted during the 1–6 h antepartum period. On the basis of the
121
on the HR variations and signs of impending parturition, the bitches underwent
122
Caesarean sections (Tables 1 and 2). 6
REVISED
ACCEPTED MANUSCRIPT In Group 2 (6/9) (bitches 6 to 11), one or more, but not all, fetuses presented
124
signs of fetal distress (HR consistently between 160 and 190 bpm) 1 to 6 h
125
preoperatively. The remaining fetuses within each litter showed HR decelerations and
126
accelerations (Figure 2). On the basis of these fetal observations and other indications,
127
Caesarean section was performed (Table 2). In all bitches, decreased rectal temperature,
128
lactation, and nesting behavior was detected without any other sign of delivery. In bitch
129
6, antepartum uterine prolapse was observed. Bitch 10 whelped three fetuses each with
130
a different HR 1 to 6 h antepartum. Of the 3 fetuses, one was in fetal distress with an
131
HR between 160 and 185 bpm, another had HR accelerations and decelerations between
132
185 and 236 bpm, and the third had HR accelerations and decelerations between 138
133
and 225 bpm. Bitch 11 was diagnosed with cystic endometrial hyperplasia throughout
134
the uterine extension.
M AN U
SC
RI PT
123
In bitch 12 (Group 2, 1/9), periods of increased HR acceleration and
136
deceleration were initially observed in the fetuses (48 and 24 h preoperatively, Figure 6)
137
and several signs of parturition occurred, but these changes ceased 6–1 h antepartum;
138
the fetal HRs no longer decelerated and remained above 200 bpm (Figure 6); in
139
addition, the bitch showed no signs of delivery and became lethargic. Hence, a
140
Caesarean section was indicated (Table 2).
EP
AC C
141
TE D
135
During the antepartum period, the greatest fetal HR decline is observed in the
142
Group 1 (normal parturition) fetuses (Figure 5). The same fetal HR trend occurred in
143
Group 2 (Caesarean section, Figure 6), except in bitch 12, in which the fetal HR
144
returned to greater than 200 bpm during the 6–1 h antepartum period.
145
In Group 3 (3/3) (bitches 13, 14, and 15), all fetuses were in distress 6 to 1 h
146
antepartum, and Caesareans were indicated (Table 2). Bitches 13 and 14 (2/3) had no 7
REVISED
ACCEPTED MANUSCRIPT signs of labor; their rectal temperatures did decrease over the previous 2 days but
148
returned to normal on the day of the surgery. In one (bitch 14), the signs of uterine
149
rupture were observed intraoperatively. Bitch 15 showed only lactation as an
150
antepartum sign, and a macerated fetus was observed, which was previously visualized
151
and monitored ultrasonographically during pregnancy.
RI PT
147
In Group 3 (all fetuses in distress), fetal HR decelerations were observed during
153
the 12 h antepartum period; however, during the 6–1 h antepartum period, the HR did
154
not exceed 200 bpm, showed no marked decelerations, and remained in a consistent
155
range (Figure 7).
M AN U
SC
152
Poisson model estimates are summarized in Table 3. The deviation from the
157
model was 3612.40 with 1206 degrees of freedom, showing that the adjustment was
158
adequate. Furthermore, there were significant estimates in Groups 2 (Caesarean
159
delivery) and 3 (Caesarean delivery with all fetuses in distress). Considering the P
S0093-691X(14)00205-2
DOI:
10.1016/j.theriogenology.2014.04.025
Reference:
THE 12790
To appear in:
Theriogenology
Received Date: 5 February 2014 Revised Date:
22 April 2014
Accepted Date: 30 April 2014
Please cite this article as: Gil EMU, Garcia DAA, Giannico AT, Froes TR, Canine fetal heart rate: Do accelerations or decelerations predict the parturition day in bitches?, Theriogenology (2014), doi: 10.1016/j.theriogenology.2014.04.025. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
REVISED
ACCEPTED MANUSCRIPT 1
Canine fetal heart rate: Do accelerations or decelerations predict
2
the parturition day in bitches?
3
E.M.U. Gila, D.A.A. Garciaa, A.T. Giannicoa, T.R. Froesa*
5
a
RI PT
4 Federal University of Paraná
*Address correspondence to: T.R. Froes
8
Federal University of Paraná
9
Rua dos Funcionários 1540. Juvevê. Zip Code 80035-050
M AN U
7
SC
6
Curitiba City, Paraná State, Brazil
11
Phone: 55 (41) 3350-5616, Fax: 55 (41) 3350-5725
AC C
EP
TE D
10
1
REVISED
ACCEPTED MANUSCRIPT Abstract
13
Ultrasonography is a safe and efficient technique for monitoring fetal development and
14
viability. One of the most important and widely used parameters to verify fetal viability
15
is the fetal heart rate (HR). In human medicine, the fetal HR normally oscillates during
16
labor in transient accelerations and decelerations associated with uterine contractions.
17
The present study investigated whether these variations also occur in canine fetuses and
18
its relationship to parturition. A cohort study was conducted in 15 pregnant bitches
19
undergoing two-dimensional high-resolution ultrasonographic examination during the
20
8th week of gestation. Fetal HR was assessed in M-mode for 5 min in each fetus in all
21
bitches. In addition, the bitches were monitored for clinical signs of imminent
22
parturition. Associations between the HR, antepartum time, and delivery characteristics
23
were evaluated with a Poisson regression model. Fetal HR acceleration and deceleration
24
occurred in canine fetuses and predicted the optimal time of parturition. These findings
25
can help veterinarians and sonographers better understand this phenomenon in canine
26
fetuses.
27
Keywords:
fetal
ultrasonography,
pregnancy,
gestational
ultrasound
AC C
EP
canine,
TE D
M AN U
SC
RI PT
12
2
REVISED
ACCEPTED MANUSCRIPT 28
1. Introduction Canine gestation lasts 64–66 days based on the pre-ovulatory serum luteinizing
30
hormone peak [1]. However, full-term gestation ranges from 57 to 72 days post-
31
breeding, depending on the breed, litter size, and the individual proestrus and estrus
32
duration [2,3,4,5]. It is difficult to predict the exact day of partum in bitches. An
33
accurate method predicting the precise time of parturition in bitches would prove useful
34
by allowing timely intervention to minimize or prevent reproductive losses.
SC
RI PT
29
Ultrasonography is a safe and effective method for monitoring fetal development
36
and viability [6]. One of the most important and widely used parameters to verify fetal
37
viability is fetal heart rate (HR). Fetal stress resulting from hypoxia can occur during
38
dystocia and manifests as a decreased HR [7]. Fetal HR should be greater than 220
39
beats per min (bpm); HRs between 180 and 220 bpm indicate moderate fetal distress,
40
while values less than 180 bpm indicate severe fetal distress [8].
TE D
M AN U
35
In human medicine, Hon [9] and Caldeyro-Barcia et al. [10] reported that fetal
42
HR oscillated during phase I of labor. They observed transient accelerations and
43
decelerations in the normal fetal cardiac activity resulting from uterine contractions.
44
Such events have not been described in veterinary medicine. Therefore, the present
45
study assessed whether these changes occur in dogs, their relationship to parturition,
46
and their utility in predicting a suitable time for a Caesarean section.
48
AC C
47
EP
41
2. Materials and Methods
49
This cohort study was conducted on 15 pregnant bitches that underwent an
50
ultrasonographic examination during the 8th week of gestation. All procedures were
51
conducted in accordance with the Animal Use Committee guidelines. In all bitches, the 3
REVISED
ACCEPTED MANUSCRIPT examination was performed using two-dimensional ultrasonographic equipment and
53
high-resolution imaging (Ultrasonix [SONIX OP, Ultrasonix Ltd., Richmond, BC,
54
Canada], Esaote [MyLab 30, Genova, Italy], and General Electric [Logic 3 Expert, GE
55
Healthcare, Wauwatosa, WI, USA]). Electronic convex and linear multifrequency
56
transducers ranging from 2.5 to 14.0 MHz frequencies were selected according to the
57
size of the animal. Abdominal hair was clipped to optimize ultrasonographic image
58
acquisition.
SC
RI PT
52
Fetal HR was evaluated using M-mode for 5 min per fetus in all pregnant bitches
60
up to a maximum four fetuses. When more than four fetuses were present, we evaluated
61
at least five fetuses in different positions. Fetal distress was defined as a HR
62
consistently within a 160- to 190-bpm range. HR was measured at 72, 48, 24, 12, and
63
between 6–1h before parturition. Fetal HR measurement during the final antepartum
64
period (6–1h) varied depending on the delivery method; in bitches undergoing
65
caesarean surgery, the fetal HR was assessed 1 h preoperatively, while in those
66
undergoing normal labor, the final ultrasound examination was performed within 6 h
67
antepartum.
EP
TE D
M AN U
59
Sonographic examinations were performed in all dogs by two sonographers, one a
69
member of the Brazilian College of Veterinary Radiology and the other an
70
echocardiographer who assessed all HR-related sonographic findings during the
71
examination.
AC C
68
72
In addition to sonographic monitoring, the bitches were tracked clinically for
73
signs of imminent delivery including decreased rectal temperature (less than 37.2°C),
74
milk yield, nesting behavior, and vulvar discharge.
4
REVISED
ACCEPTED MANUSCRIPT Data collation and analysis were conducted using Microsoft Office Excel
76
(Microsoft® Office 2007 for Windows, Redmond, WA, USA) and R for Windows
77
(version 3.0.1, R Foundation for Statistical Computing, Vienna, Austria, 2013). To
78
evaluate the association between HR, time, and delivery characteristics, a Poisson
79
regression model was used. A descriptive statistical analysis was performed and
80
adjusted for generalized linear model categorical data before implementing the Poisson
81
regression. The following variables were assessed: variable fetal HR response (bpm),
82
the explanatory variables (group of animals), and the antepartum period (6–1h). A
83
Poisson distribution was modeled for the HR counts, and a Poisson regression analysis
84
estimated the effect of HR acceleration and deceleration antepartum The Poisson
85
regression was fitted to the fetal HR data in the 15 cases according to the experimental
86
group and antepartum duration. The estimate for Group 1 (normal parturition) was
87
compared to other group estimates. A P-value of α = 5% was considered significant,
88
and the significance of each parameter was analyzed relative to the value set. The
89
groups were established according to the clinical findings.
TE D
M AN U
SC
RI PT
75
91
3. Results
EP
90
Fifteen bitches were included in the study and ranged from 1 to 7 years of age.
93
Of these, 3 had normal deliveries, and 12 underwent Caesarean section (Table 1). They
94
were categorized into 3 groups: Group 1 comprised bitches undergoing normal
95
parturition (bitches 1–3); Group 2 comprised bitches that were referred for a Caesarean
96
section with one or more (but not all) fetuses in distress (bitches 4–12); and Group 3
97
comprised bitches that were referred for a Caesarean section with all fetuses in distress
98
(bitches 13–15) (Figure 1).
AC C
92
5
REVISED
ACCEPTED MANUSCRIPT The fetal HR variability was measured and found to be consistent with
100
accelerations and decelerations. These changes occurred during the entire study period
101
from 72 h until 6–1 h antepartum. Initially, HR variations occurred only in select
102
fetuses, but as parturition approached, all fetuses presented these variations. HR
103
acceleration and deceleration variations alternated and became extreme as parturition
104
approached. HR extremes of 143 to 205 bpm were observed over a 4 s period and
105
analyzed by M-mode, as shown in Figure 2.
SC
107
Figure 3 summarizes the variable fetal HR (bpm) distribution by bitch between 6 and 1 h antepartum.
M AN U
106
RI PT
99
108
The fetal HR dispersion during the antepartum period for bitches in Groups 1
109
and 2 is shown in Figure 4. As parturition approached, the fetal HR decelerations
110
reached a 103 bpm minimum and sustained maximum values above 200 bpm. All fetuses in Group 1 (3/3) had HR acceleration
TE D
111
and deceleration 6–1 h antepartum ranging from 119 to 242 bpm. In bitch 1, the fetal
113
HR accelerations and decelerations began within 12 h antepartum in all fetuses. In bitch
114
2, fetal HR changes were observed in just a few fetuses 48 h antepartum. In bitch 3,
115
acceleration and deceleration was observed in select fetuses within 72 h antepartum, but
116
as parturition approached, additional and eventually all fetuses presented HR
117
accelerations and decelerations (Figure 5).
AC C
118
EP
112
Fetuses in two English Bulldogs in Group 2 (2/9) (bitches 4 and 5) had fetal
119
distress antepartum. HR acceleration and deceleration began 12 h before the Caesarean
120
section; this variation persisted during the 1–6 h antepartum period. On the basis of the
121
on the HR variations and signs of impending parturition, the bitches underwent
122
Caesarean sections (Tables 1 and 2). 6
REVISED
ACCEPTED MANUSCRIPT In Group 2 (6/9) (bitches 6 to 11), one or more, but not all, fetuses presented
124
signs of fetal distress (HR consistently between 160 and 190 bpm) 1 to 6 h
125
preoperatively. The remaining fetuses within each litter showed HR decelerations and
126
accelerations (Figure 2). On the basis of these fetal observations and other indications,
127
Caesarean section was performed (Table 2). In all bitches, decreased rectal temperature,
128
lactation, and nesting behavior was detected without any other sign of delivery. In bitch
129
6, antepartum uterine prolapse was observed. Bitch 10 whelped three fetuses each with
130
a different HR 1 to 6 h antepartum. Of the 3 fetuses, one was in fetal distress with an
131
HR between 160 and 185 bpm, another had HR accelerations and decelerations between
132
185 and 236 bpm, and the third had HR accelerations and decelerations between 138
133
and 225 bpm. Bitch 11 was diagnosed with cystic endometrial hyperplasia throughout
134
the uterine extension.
M AN U
SC
RI PT
123
In bitch 12 (Group 2, 1/9), periods of increased HR acceleration and
136
deceleration were initially observed in the fetuses (48 and 24 h preoperatively, Figure 6)
137
and several signs of parturition occurred, but these changes ceased 6–1 h antepartum;
138
the fetal HRs no longer decelerated and remained above 200 bpm (Figure 6); in
139
addition, the bitch showed no signs of delivery and became lethargic. Hence, a
140
Caesarean section was indicated (Table 2).
EP
AC C
141
TE D
135
During the antepartum period, the greatest fetal HR decline is observed in the
142
Group 1 (normal parturition) fetuses (Figure 5). The same fetal HR trend occurred in
143
Group 2 (Caesarean section, Figure 6), except in bitch 12, in which the fetal HR
144
returned to greater than 200 bpm during the 6–1 h antepartum period.
145
In Group 3 (3/3) (bitches 13, 14, and 15), all fetuses were in distress 6 to 1 h
146
antepartum, and Caesareans were indicated (Table 2). Bitches 13 and 14 (2/3) had no 7
REVISED
ACCEPTED MANUSCRIPT signs of labor; their rectal temperatures did decrease over the previous 2 days but
148
returned to normal on the day of the surgery. In one (bitch 14), the signs of uterine
149
rupture were observed intraoperatively. Bitch 15 showed only lactation as an
150
antepartum sign, and a macerated fetus was observed, which was previously visualized
151
and monitored ultrasonographically during pregnancy.
RI PT
147
In Group 3 (all fetuses in distress), fetal HR decelerations were observed during
153
the 12 h antepartum period; however, during the 6–1 h antepartum period, the HR did
154
not exceed 200 bpm, showed no marked decelerations, and remained in a consistent
155
range (Figure 7).
M AN U
SC
152
Poisson model estimates are summarized in Table 3. The deviation from the
157
model was 3612.40 with 1206 degrees of freedom, showing that the adjustment was
158
adequate. Furthermore, there were significant estimates in Groups 2 (Caesarean
159
delivery) and 3 (Caesarean delivery with all fetuses in distress). Considering the P
