ISSN 1916-6958

2010; Volume 1 (Number 1):
Pages 21-26

ORIGINAL RESEARCH

Perinatal outcomes to uterine
stimulation with breast massage alone or in combination with oxytocin in
dystocic sows

Miguel
GONZÁLEZ-LOZANOa, Daniel MOTA-ROJASb,*, Alejandro A. NAVA-OCAMPOc,d, María ALONSO-SPILSBURYb, E. Yadira
VELÁZQUEZ-ARMENTAd, Rafael HERNÁNDEZ-GONZÁLEZe, Ramiro RAMÍREZ-NECOECHEAb, María E.
TRUJILLO-ORTEGAf

aPostgraduate Div. of Animal Science and Health,
School of Veterinary and Animal Production, UNAM, México DF, México, bDept.
of Animal Production & Agriculture, Research Area: Ecodesarrollo de la
Producción Animal, UAM-Xochimilco, México DF, México, cDepartment of
Pharmacology & Toxicology, Faculty of Medicine, University of Toronto,
Toronto, Canada, dPharmaReasons, Toronto, Canada, eDepartment
of Experimental Research & Animal Resources, Instituto Nacional de Ciencias
Médicas y  Nutrición ‘Salvador Zubirán’,
and fDepartment of Animal Medicine and Production: Swine, School of
Veterinary and Animal Production, UNAM, México DF, México.

*Corresponding author:
[email-masked]

ABSTRACT

Objective:
Our goal was to evaluate the obstetric and fetal
outcomes in dystocic sows receiving udder massage stimulation alone or in combination
with oxytocin. Methods: 120 sows
with maternal or fetal dystocia were randomly allocated to receive either
intravulvar (I-Vu) saline (control group), udder massage followed by I-Vu
saline, or udder massage followed by I-Vu oxytocin 10 IU (groups 1, 2 and 3,
respectively). Udder massage consisted in the application of natural oil while
rubbing the udder in a cephalic-to-caudal direction. Obstetric and fetal outcomes
were obtained and compared among the three groups. The statistically significant
limit was fixed to a two-tailed P < 0.05 in every test. Results: Intensity of uterine contractions decreased from 18.1 ±
3.6 mmHg in the control group to 14.1 ± 3.8 mmHg (P < 0.001) in group 2.
Compared to the control group, there was an approximately 3.3-fold reduction in
the number of moderate-to-severe meconium stained live-born piglets and 50%
reduction of intrapartum deaths in group 2. In group 3, the reduction in these
two outcomes was less evident but remained statistically significant. Conclusions: Dystocic sows that
received udder massage had better obstetric and fetal outcomes than control
sows. However, co-administration of oxytocin might reverse the advantages of
udder massage.

Key words

Dystocia; Experimental animal models;
Neuroendocrine system; Uterine stimulants

RÉSUMÉ

Objectif: Les effets obstétricaux et fœtaux de la
stimulation mammaire seule ou associée à l’ocytocine ont été évalués chez des
truies avec mise-bas dystocique. Méthodes:
120 truies avec dystocie maternelle ou fœtale ont été randomisées à un des
trois groupes suivants: administration de sérum physiologique intravulvaire
(I-Vu) (groupe témoin), stimulation mammaire suivie d’une administration de
sérum physiologique I-Vu, ou stimulation mammaire suivie d’une administration
de 10 UI d’ocytocine I-Vu (groupes 1, 2 et 3). La stimulation mammaire a
consisté en l’application d’huile naturelle avec massage des mamelles en
direction céphalocaudale. Les effets obstétricaux et fœtaux ont été enregistrés
et comparés entre les trois groupes. Une valeur de P < 0,05 en
bidirectionnel a été considérée comme statistiquement significative. Résultats: Une diminution de
l’intensité des contractions utérines de 18,1 ± 3,6 mmHg dans le groupe témoin
à 14,1 ± 3,8 mmHg est observée dans le groupe 2 (P < 0,001). De même, le
nombre de porcelets nés vivants avec liquide amniotique modérément à sévèrement
méconial est réduit de 3,3 fois et la mortalité périnatale est réduite de 50 %
dans le groupe 2. Dans le groupe 3, la réduction de ces paramètres est moins
marquée, la différence vis-à-vis du groupe témoin restant cependant
statistiquement significative. Conclusions:
La stimulation mammaire procure des avantages obstétricaux et fœtaux chez les
truies dystociques. L’administration concomitante d’ocytocine pourrait en
diminuer les avantages.

Mots clés

Dystocie; Modèles
expérimentaux animaux; Système neuroendocrinien; Stimulants utérins

RESUMEN

Objetivo: Evaluar los efectos obstétricos y fetales en
cerdas distócicas que recibieron estimulación con masaje mamario solo o en
combinación con oxitocina. Métodos:
120 cerdas con distocia materna y fetal fueron asignadas en forma aleatoria a
cualquiera de los siguientes tres grupos: solución salina intravulvar (I-Vu)
(grupo control); masaje mamario y solución salina I-Vu; o masaje mamario y
oxitocina 10 UI (grupos 1, 2 y 3, respectivamente). El masaje mamario consistió
en la aplicación de aceite natural mientras se masajeaba a la ubre en dirección
cefálico-caudal. Los resultados obstétricos y fetales observados se
compararon  entre los tres grupos. El
límite de significancia estadística fue de P < 0.05 de dos colas en todos
los análisis realizados.  Resultados: La intensidad de las
contracciones uterinas disminuyó de 18.1 ± 3.6 mmHg en el grupo control a 14.1
± 3.8 mmHg (P < 0.001) en el grupo 2. En comparación con el grupo control,
en el grupo 2, el número de lechones nacidos vivos y con tinción de meconio de
moderada a severa se redujo 3.3 veces mientras que el número de lechones
muertos intraparto se redujo un 50%. La reducción de estos dos parámetros fue
menos evidente en el grupo 3, aunque la diferencia resultó estadísticamente
significativa. Conclusiones: Las
cerdas distócicas sometidas a masaje mamario tuvieron mejores resultados
obstétricos y fetales que las cerdas controles. Sin embargo, la
coadministración de oxitocina revertió parcialmente las ventajas del masaje
mamario.

Palabras clave

Distocia;
Modelos animales experimentales; Sistema neuroendócrino; Estimulantes uterinos

INTRODUCTION

Dystocia is a common obstetric and public
health problem because of the increased risk of intrauterine asphyxia,
operative delivery, and maternal morbidity [1]. In pregnant women, breast stimulation may result in
labor induction and reduction of rates of postpartum hemorrhage [2] [3]. However, breast stimulation may fail to enhance
uterine response in 50% of parturient women [4], requiring the subsequent administration of oxytocin.
Despite its technical simplicity, a number of problems have been recognized for
developing appropriate trials to evaluate labor augmentation by breast
stimulation in parturient women [5] [6]. This is probably the reason why insufficient
information is available in the literature on this topic [3].

Pregnant sows appear to be a relevant animal
model for studying uterine stimulation. In sows, low plasma levels of oxytocin
are associated with prolonged parturition [7]. Conversely, udder stimulation has been associated
with increased plasma levels of oxytocin in ewes [8]. However, few studies have focused on the uterotonic
activity of teat massage during parturition, as breast massage had shown very
strong effects, similar to the use of oxytocin.

The objective of the present study was to
evaluate the obstetric and fetal outcomes in dystocic sows receiving udder
massage stimulation alone or in combination with oxytocin.

METHODS

Animals

Previous approval by the Institutional Review
Board of the Universidad Autónoma Metropolitana-Xochimilco, México DF, Mexico,
and in accordance with the guidelines of the ethical use of animals in applied
ethologic studies [9], the study was performed at a commercial farm of
Yorkshire-Landrace sows located in the State of Hidalgo, Mexico. Approximately 120 sows
deliver per month at this farm, and 2% to 4% have dystocia. The animals were
artificially inseminated and received prenatal care throughout pregnancy
including a diagnostic ultrasound (Renco Pregnant-Alert, Minneapolis MN, USA) at 5 weeks of pregnancy.
Parturition was induced with an intramuscular prostaglandin injection
(dinoprost tromethamine 10 mg; Lutalyse, Pharmacia
& Upjohn,
Mexico DF, Mexico) 24 hours prior to the
expected delivery date, at 114 days of gestation, according to the farm’s
breeding-farrowing records. Animals were housed in individual crates of 1.76 m ´ 1.0 m for 5 days prior to the expected delivery date and for
21 days after delivery until complete weaning occurred in all the litters. The
sows were in their first to fifth pregnancy.

Treatments

By means of a predesigned table of random
numbers, at the time of delivery, 120 sows with maternal or fetal dystocia were
allocated to one of the following 3 groups. In group 1 (controls), saline was
injected by intravulvar route. In group 2, animals received an udder massage
for 5 min starting after maternal or fetal dystocia was identified, followed by
an intravulvar injection of saline. In group 3, sows received udder massage for
5 min starting after maternal or fetal dystocia was identified, followed by
intravulvar administration of 10 IU of oxytocin. Udder massage involved the
application of natural oil while rubbing the udder in a cephalic-to-caudal
direction; this procedure was performed by the same investigator in all
occasions.

For purpose of the study, fetal dystocia was
considered as present when a sow delivered one or two consecutive intrapartum
stillbirths prior to the inclusion of the animal into the study. Maternal
dystocia was defined as a 40-min period of uterine quiescence that occurred in
the parturient sow after the delivery of any of the piglets. Parturition was
manually assisted by two of the investigators when the interval of time between
piglets was longer than 1 hour.

Study outcomes

As obstetric outcomes, the number, intensity
(mmHg) and duration (seconds) of uterine contractions were monitored by means
of an electronic digital cardiotocograph (Fetal Monitor Coriometric, Medical
Systems Inc. Co., Connecticut, CN, USA).
Duration of parturition (min) was registered starting from the first
tocographic evidence of consistent uterine activity until the delivery of the
placenta. The time to deliver each piglet (time interval between piglets; min)
was measured and averaged for each sow.
The number of manual obstetric interventions per sow, performed by one
of the investigators, was also registered.

As fetal outcomes, the number of live-born
and stillborn piglets was registered. Stillbirths were classified into type I
or type II, according to the classification criteria previously described in
detail elsewhere [10] [11]. Type I or ante-partum
stillbirths had a characteristic edematous and hemorrhagic appearance, a
grayish-brown discoloration because of beginning mummification; if the process
was advanced then the fetuses were dehydrated and started to lose hair. Type II
or intra-partum stillbirths had the exact appearance of their normal
littermates with the exception that they did not breathe. Finally, based on
the degree of meconium staining at birth, life-born piglets were classified as
unstained-to-mildly and moderate-to-severely stained [11].

Statistical analysis

The number of piglets born per sow was
compared among groups by means of the Kruskal-Wallis test followed by the
Mann-Whitney test in order to distinguish the differences between group 1
(controls) and either group 2 (udder massage) or 3 (udder massage and
oxytocin). The other continuous variables were compared among groups by an
Analysis of Variance (ANOVA) followed by a Dunnett test to distinguish the
differences between group 1 and either group 2 or 3. Categorical variables were
compared among the three groups by a ‘2 by k’ X2 test followed by a comparison between group 1 and
either group 2 or 3 by a ‘2 by 2’ X2
test. The statistically significant limit was fixed to a two-tailed P < 0.05 in every test.

RESULTS

Udder massage alone or in combination with
oxytocin did not increase the number of uterine contractions in comparison to
the control group (Table
1). However, the duration of uterine contractions and the overall
duration of parturition were decreased by approximately 9 s and 20 min by udder
massage, respectively; as expected, the reduction was more evident in group 3
(approximately 12 s and 50 min, respectively). Paradoxically, the intensity of
uterine contractions decreased from 18.1 ± 3.6 mmHg in
group 1 to 14.1 ± 3.8 mmHg in group 2 (P < 0.001) (Table 1).

In group 3, however, the intensity of uterine
contractions increased approximately 3 mmHg above that observed in the control
group (P ≤ 0.0025). Piglets were delivered at intervals of approximately
16 min in the control group and 15 min in the group treated with udder massage;
time interval between piglets was reduced by 3 min (P < 0.001) in group 3
compared to the control. The number of manual obstetric interventions
significantly decreased in sows in group 2 compared to the control group; this
reduction was more evident in group 3.

Table
1

Obstetric
outcomes of dystocic sows treated with udder massage alone or in combination
with oxytocin

Group
1

(controls)

n
= 40

Group
2

(udder
massage)

n
= 40

Group
3

(udder
massage + oxytocin)

n
= 40

P
value

Uterine
contractions per piglet (n)

3.8
± 1.2

3.7
± 0.7

4.3
± 1.8

0.08

Intensity
of uterine contraction (mmHg)

18.1
± 3.6

14.1
± 3.8*

21.1
±  4.1*

<
0.01

Duration of
uterine contraction (s)

25.6
± 5.7

16.7
± 4.5*

13.1
± 2.8*

<
0.001

Duration
of parturition (min)

205.2
± 33.1

185.2
± 36.6*

156.3
± 37.3*

<
0.001

Time
interval between piglets (min)

16.9
± 3.3

15.4
± 3.3

13.1
± 3.6*

<
0.001

Manual
obstetrics interventions

[n (% of piglets)]

76
(14.9)

49
(10.1)*

30
(6.2)*

<
0.001

*P < 0.05, control group
versus either udder massage or udder massage followed by oxytocin
administration.

Data are mean ± SD or where
specified n (%).

Table
2

Fetal
outcomes of dystocic sows treated with udder massage alone or in combination
with oxytocin

Group
1

(controls)

n
= 40

Group
2

(udder
massage)

n
= 40

Group
3

(udder
massage + oxytocin)

n
= 40

P
value

Piglets
per sow [median (range)]

13
(11 – 15)

12
(10 -16)*

12
(8 -15)

0.048

Live
born piglets [n (%)]

407
(79.6)

433
(89.1)*

398
(82.2)

< 0.001

Antepartum
deaths [n (%)]

6
(1.2)

4
(0.8)

10
(2.0)

0.2

Intrapartum
deaths [n (%)]

98
(19.2)

49
(10.1)*

76
(15.7)

<
0.001

Moderate-to-severe
meconium stained piglets [n (% of live-born piglets)]

117
(28.7)

36
(8.8)*

58
(17.2)*

<
0.001

*P < 0.05, control group
versus either udder massage or udder massage followed by oxytocin administration

The number of piglets born per sow was
similar between groups 1 and 3; it was slightly, but significantly, lower in
group 2 (Table
2). The number of live born piglets was significantly higher in
group 2 than in the control group, whereas no differences were observed between
groups 1 and 3. There was an approximately 3.3-fold reduction in the number of
moderate-to-severe meconium stained piglets born to dystocic sows treated with
udder massage (P < 0.001). In group 3, there was a 1.7-fold reduction (P
< 0.001). Although the number of antepartum-death piglets was similar among
the three groups, there was a reduction of approximately 50% in the number of
intrapartum deaths in group 2 whereas the difference was not significant
between groups 1 and 3 (Table
2).

DISCUSSION

The current study showed that udder massage applied
to dystocic sows resulted in better obstetric and fetal outcomes than sows
without any intervention. The demonstration that breast stimulation can
successfully be used for ripening the cervix and labor induction was described
as early as in the 18th and 19th centuries [5]. However, few advances to study the uterotonic
effects, produced in response to breast stimulation, have been performed.

The uterotonic effect of udder massage in
parturient sows can be enhanced by the subsequent administration of oxytocin.
However, the rate of adverse obstetric and fetal outcomes also increased with
the co-administration of oxytocin. Gestation-related changes in uterine
activity include alterations in hormonal, metabolic, and neural inputs to the
uterus, changes in the responsiveness of the myometrium to bioactive substances
through alterations in receptors, and coupled signal transduction mechanisms
resulting in myometrial layer-dependent differences in responsiveness to
bioactive substances less marked than that observed in non-pregnant sows [12].

Uterine response to breast stimulation has
not shown any correlation with oxytocin levels [13], and the effects observed in the present study further
support that breast stimulation may act through a different mechanism to oxytocin.
For example, udder massage in dystocic sows significantly decreased uterine
activity whereas oxytocin administration evidently enhanced it. In contrast,
either udder massage alone or followed by oxytocin administration resulted in
shorter duration of uterine contractions and parturition. In pregnant mammals,
including humans, an abrupt increase in oxytocin binding sites in the uterus
may occur at approximately 24 h before the onset of labor, reaching the
greatest levels during labor and sharply decreasing after parturition to reach
baseline levels 2-5 days postpartum [14] [15] [16]. These physiological changes explain the
participation of endogenous oxytocin during parturition as well as the efficacy
of this hormone when exogenously administered. Breast stimulation may
facilitate the oxytocin-induced uterine stimulation by other pathways involved
in the parturition process.

In our study, a 50% reduction in the rates of
meconium-stained live-born piglets was observed in the group of dystocic sows
that received udder massage in comparison to the control group. Similar
significant, though less evident, results were previously reported in studies
performed in parturient women [3]. In this study, however, the positive effect of udder
massage was partially reversed by the administration of oxytocin. The adverse
fetal and obstetric outcomes to oxytocin could be related to uterine hyperstimulation
[17]. However, dystocia may not only result from uterine
hyperstimulation but also from the lack of uterine response to oxytocin
administration [18]. In a study on breast stimulation in parturient
women, this maneuver failed to produce adequate uterine stimulation in 50% of
cases, but there was no case of uterine hyperstimulation in those patients who
subsequently received oxytocin [4]. The dose and the rate at which oxytocin is
administered might define whether it may or may not produce uterine
hyperstimulation. However, the current evidence points to a mechanism of action
different to that produced by breast stimulation in mammals.

In conclusion, udder massage applied to
dystocic sows resulted in better obstetric and fetal outcome than sows without
any intervention. The mechanism of action of udder massage appears to be
different to oxytocin. However, the subsequent administration of oxytocin
partially reversed the benefits of udder massage.

AUTHORS’ PARTICIPATION

D MR, M AS, R RN, M GL, and ME TO conceived
the idea, drafted the protocol and proposed the study design. D MR, MGL, and M
Z were responsible for the experimental part of the study. AA NO, and EY VA
performed the data analysis. D MR, M AS, R RN, and ME TO drafted the manuscript.
All participated in the discussion of the results and contributed to the final
version of the manuscript.

ACKNOWLEDGEMENTS

The study was supported by a grant from the
Programa de Mejoramiento del
Profesorado (PROMEP) No. UAM-PTC-028 to the Academic Staff of Etología,
Producción Porcina y Fauna Silvestre. D Mota-Rojas, M Alonso-Spilsbury, R
Ramírez-Necoechea and ME Trujillo-Ortega, were supported, as members, by the
Sistema Nacional de Investigadores. The authors are grateful to Pedro Sánchez
Aparicio, Gloria González Hernández and Adriana Olmos, for the animal husbandry
and technical assistance throughout the study.

CONFLICT OF INTERESTS/DISCLAIMERS

M GL, D MR, AA NO, M AS, EY VA, and R
RN are members of the Editorial Board of the journal.

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