AABArchives Animal BreedingAABArch. Anim. Breed.2363-9822Copernicus PublicationsGöttingen, Germany10.5194/aab-59-201-2016Physiological differences between twin and single-born lambs and kids during
the first month of lifeFazioFrancescofrancesco.fazio@unime.itArfusoFrancescaGiudiceElisabettaGiannettoClaudiaPiccioneGiuseppeDepartment of Veterinary Sciences, Polo Universitario Annunziata, University of Messina, 98168 Messina, ItalyDepartment of Chemical, Biological, Pharmaceutical and Environmental Sciences,
University of Messina, Viale Ferdinando Stagno d'Alcontres 31, 98166 Sant'Agata, Messina, ItalyFrancesco Fazio (francesco.fazio@unime.it)4May20165922012072March201618April201628April2016This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://aab.copernicus.org/articles/59/201/2016/aab-59-201-2016.htmlThe full text article is available as a PDF file from https://aab.copernicus.org/articles/59/201/2016/aab-59-201-2016.pdf
The effects of time after birth and of twinning on rectal temperature (RT),
heart rate (HR), respiratory rate (RR) and body weight (BW) values were
evaluated in five singleton Comisana lambs (three males and two females), five singleton
Maltese Kids (three males and two females), four couples of twin Comisana lambs (four
males and four females) and four couples of twin Maltese kids (four males and four
females) during the first month of life. For all kids and lambs, RT, HR, RR
and BW were recorded after 1 and 24 h from birth and every 2 days
until the 30th day of life. The application of two-way repeated
measures analysis of variance (ANOVA) showed a statistically significant
effect of time (P< 0.0001) on RT, HR, RR and BW values in all
lambs and kids during the first month of life. Any significant effect of
twinning (P> 0.05) on all studied parameters was found in lambs,
whereas statistically significant differences in BW, RT and HR values (P< 0.01)
were found between twin and singleton kids throughout the
first month of life. The results obtained in this study make a contribution
to the knowledge of homeostatic, cardiorespiratory and thermoregulatory
adaptations occurring in singleton lambs and kids and in twin lambs and kids
during the first 30 days of life. Our findings indicate that the BW, RT, HR
and RR values, whose homeostasis is still evolving in newborn, should be
interpreted dynamically as a function of the period of postnatal adaptation
and also of twinning.
Introduction
The management of newborn livestock species from birth until weaning has an
impact on herd productivity, and the economic return will depend on the
survival of the offspring. Physiological immaturity is considered the
major determinant of mortality and morbidity in newborn resulting in
economic losses in livestock production (Dwyer et al., 2005; Stafford et
al., 2007; Piccione et al., 2008, 2009, 2010). A substantial proportion of postnatal diseases or death could be
prevented by good management and by early intervention and by diagnosis and
treatment of situations that involve a high-risk newborn. The postnatal
period, known as the adaptative period, is a critical life stage that begins at birth and extends
until the 30th day of life and that reflects the ability of newborn to complete
their maturation with the animal's adaptation to extrauterine life
(Piccione et al., 2007; Vannucchi et al., 2012). At birth and during the
subsequent days of extrauterine life, the thermoregulatory, cardiovascular,
respiratory and homeostatic mechanisms complete newborn maturation (Chniter et
al., 2013).
Studies carried out on newborn calves, lambs and kids demonstrated that the
respiratory, cardiovascular and thermoregulatory function of these livestock
species is subjected to several adjustments following the transition from
the controlled uterine environment to the free-living state (Nowak and Poindron,
2006; Al-Tamimi, 2007; Ocak et al., 2009; Piccione et al., 2010, 2013; Davey
et al., 1998). These physiological functions are also influenced by the birth
weight of the animal (De Matteo et al., 2008; Chniter et al., 2013), which in
turn depends on fetal physiological adaptations made in response to the
intrauterine conditions (De Matteo et al., 2008). In this regard, multiple
gestation is recognized as a natural cause of intrauterine growth
restriction leading to a decrease in birth weight of twin births compared to
singleton births (de Geus et al., 2001). Although many authors have studied
the differences in several physiological functions between singleton and
twin offspring in human, ovine and caprine species, conflicting results were
obtained (Poulter et al., 1999; Baird et al., 2001; Aleksiev, 2009). Several
studies showed that triplet-born lambs have lighter birth weights, a lower
body temperature and some lower plasma parameter levels than twin-born
lambs, resulting in a poor thermoregulatory function during the postnatal
period (Morris and Kenyon, 2004; Stafford et al., 2007). Studies comparing
blood pressure or heart rate (HR) in singletons and twins have shown either no effect (de
Geus et al., 2001), higher values in twins (Dwyer et al., 1999) or lower
values in twin (De Matteo et al., 2008). These discordant results are likely
due to uncontrolled factors between groups, including dam or offspring
nutrition and a lack of differentiation between monozygotic and dizygotic
twins (De Matteo et al., 2008).
Because of the importance of deepening the knowledge on adaptation processes
occurring during the postnatal period in order to improve management techniques and
to prevent postnatal diseases or death, this study aimed to evaluate the
effect of time after birth and of twinning on rectal temperature, heart
rate, respiratory rate and body weight in lambs and kids during the first
month of life.
Material and methodsAnimals
This study was carried out on five singleton (three males and two
females) and eight twin (four males and four females) Comisana lambs, on the one hand, and five singleton (three males and two females) and eight twin Maltese kids (four males and four
females), on the other hand, born from multiparous Comisana sheep and Maltese goats, respectively, on the
same farm, situated in northeast Sicily (37∘43′24′′ N, 13∘26′05′′ E; 966 m above sea level).
All dams, aged 4–5 years old, were fed with a constant diet composed of a
concentrate mixture which consisted of the following ingredients: oats (12 %), faba bean (15 %), barley (25 %), pea (10 %), sugar beet pulp (20 %),
molasses (5 %), and mineral and vitamins supplements (3 %). Forage-based
diets were alfalfa (Medicago sativa L.) hay. About 250 g animal-1 of concentrate was
distributed twice a day and water was available ad libitum. Every day the dams were
herded out and grazed on an improved natural pasture from 10:00 to 18:00 LT.
All lambs and kids were born at term in spring (sunrise: 05:15; sunset: 21:02) at similar gestational age (singleton lamb: 148±1 days; twin
lambs: 146±1 days; singleton kids: 152±2 days; twin kids: 153±1 days). They were kept in boxes with their dam in order to
guarantee adequate mothering and to minimize disruption. Thermal and
hygrometric measurements were carried out inside the box for the whole study by
means of a data logger (Gemini, UK), and they agreed with the normal seasonal
pattern for the location (minimum and maximum temperature between
13.6 and 22.8∘ C, mean relative humidity of 57 %).
The newborn lambs and kids were considered clinically healthy. Their health
status was evaluated at birth based on behavior, rectal temperature,
heart and respiratory profile, cough, nasal discharge, ocular discharge,
appetite, faecal consistency, navel examination, and haematological profile
(data not shown). Lambs and kids were fed only with colostrum and maternal
milk. Each day the lambs and kids were herded out and grazed on an improved
natural pasture with their dams. At pasture they suckled freely.
Data collection
Once the lambs and kids were born, their birth data, type of birth and sex
were recorded and they were allowed to suckle successfully unaided.
For all lambs and kids, rectal temperature (RT), HR, respiratory
rate (RR) and body weight (BW) were recorded by the same operator after 1
(T0) and 24 (T1) h from birth and every 2 days until the 30th day of
life (T2, T4, T6, T8, T10, T12, T14, T16, T18, T20, T22, T24, T26, T28 and
T30).
The RT was recorded using a digital thermometer (model HI92704, Hanna
Instruments, Bedfordshire, UK) with the probe being inserted to a depth of
4 cm. The HR was measured by means of an oscillometric apparatus (Argus TM-7;
Schiller, Barr, Switzerland). The RR was assessed visually by observation of
chest and abdomen movements and auscultation with a stethoscope over a 5 min
period. The BW was measured by a means of a weighing platform
(PS1000 Livestock Scale, Brecknell, UK).
In our study, protocols of animal husbandry and experimentation were
reviewed and approved in accordance with the standards recommended by the
Guide for the Care and Use of Laboratory Animals and Directive 2010/63/EU
for animal experiments.
Mean ± standard deviation of body weight (BW), rectal
temperature (TR), respiratory rate (RR) and heart rate (HR) values measured
in twin and singleton lambs at each time point (T0–T30) of experimental
period.
Significance of the effect of (P< 0.0001):
a vs. T1–T30;
b vs. T6–T30;
c vs. T10–T30;
d vs. T14–T30;
e vs. T18–T30;
f vs. T20–T30;
g vs. T22–T30;
h vs. T24–T30;
i vs. T12–T30;
j vs. T28–T30;
k vs. T30;
l vs. T2–T30;
m vs. T8–T30;
n vs. T16–T30;
o vs. T26–T30;
p vs. T4–T30;
q vs. T28;
r vs. T10;
s vs. T14.
Statistical analysis
All data were tested for normality of distribution using the Kolmogorov–Smirnov
test. All data were normally distributed (P> 0.05), and
statistical analysis was performed. Two-way repeated measures analysis of
variance (ANOVA) was applied to assess the statistically significant effect of
time (days of life) and of twinning on BW, RT, HR and RR values measured in
lambs and kids during the first month of life. Duncan's multiple comparison
test was applied for post hoc comparison. P values < 0.05 were
considered statistically significant.
Statistical analysis was performed using the STATISTICA software package
(STATISTICA 7 Stat Software Inc., Tulsa, Oklahoma, USA).
Results and discussion
All the results were expressed as means ± standard deviation
(M ± SD).
Mean ± standard deviation of body weight (BW), rectal
temperature (TR), respiratory rate (RR) and heart rate (HR) values measured
in twin and singleton kids at each time points (T0–T30) of experimental
period.
Significances (Effect of time P< 0.0001):
a vs. T1–T30;
b vs. T6–T30;
c vs. T10–T30;
d vs. T14–T30;
e vs. T18–T30;
f vs. T20–T30;
g vs. T22–T30;
h vs. T24–T30;
i vs. T12–T30;
j vs. T28–T30;
k vs. T30;
l vs. T2–T30;
m vs. T8–T30;
n vs. T16–T30;
o vs. T26–T30;
p vs. T4–T30;
q vs. T28;
r vs. T10;
s vs. T14.
The application of two-way ANOVA showed a statistically significant effect of
time (P< 0.0001) on BW, RT, HR and RR values measured in both
singleton and twin lambs and in both singleton and twin kids during the
first month of life. In particular, all lambs and kids showed a
statistically significant increase in BW values (P< 0.0001) from
birth until the end of the monitoring period and a statistically significant
decrease in RT, HR and RR values (P< 0.0001) from birth until the
end of the monitoring period (Tables 1 and 2). These changes reflect the
physiological adjustments likely to occur in a newborn animal following
transition from the controlled uterine environment to the free-living state. It
has been stated that ovine and caprine newborns have high metabolic rates
immediately after the birth, which may increase their body temperatures at
this time (Vannucchi et al., 2012). The decrease in the RT values observed
24 h after birth may be due to a reduction in heat generation for body
temperature maintenance. The observed RT fluctuations may indicate either
that the thermoregulatory set point was not specified yet by the central
nervous system or that the thermoregulatory mechanisms were not mature
enough to maintain RT values within the already fixed set point (Aleksiev,
2009). The subsequent decrease in the RT values found in lambs and kids
until day 30 of life may be related to the withdrawal of the placental
inhibitors from the circulation and the initiation of nonshivering
thermogenesis in brown adipose tissue (Aleksiev, 2009; Plush et al., 2016).
Similar patterns of RT dynamics were established in a previous study on
newborn lambs and kids during the first day after delivery (Aleksiev, 2009).
This similarity in RT behavior in the newborn of the two species strongly
supports the concept of genetic control of the homeothermy development in
newborn (Aleksiev, 2009; Plush et al., 2015). The HR and RR in all lambs and
kids observed in this study showed higher values with respect to the reported
range in adult sheep and goats (Hemingway and Hemingway, 1966; Miller and
West, 1972). It has been stated that younger animals have higher heart rates (Mir
et al., 2000) and, owing to a higher surface area, also have higher respiration
rates (Mir et al., 2000). Decreases in HR and RR values were
found in both species throughout the monitoring period. These changes
highlighted the morphofunctional modifications of the cardiovascular and
respiratory system, leading the organism to adapt to the extrauterine
environment with a well-defined homeostatic ability (Piccione et al., 2007).
The heart is forced to pump the blood through a vascular system that
presents strong elastic, peripheral resistance and, since the organism of
the newborn is not yet able to vary cardiac output, it compensates the
limited systolic volume by increasing the heart rate. The decrease observed
in RR values highlights the irregularity of the respiratory activity of the
offspring during the postnatal period (Davey et al., 1998; Abu-Shaweesh
2004). With the first breath, three major changes that characterize the
respiratory adaptation of mammals at birth (onset of external ventilation,
clearing of the fetal pulmonary fluid and establishment of a functional
residual capacity) occur. In newborn, respiratory system compliance is low
and the resistance is high in the first minutes after birth. During the next
few days, the former increases by 80 % and the latter decreases by 20 %. Both
changes (i.e., the increase in lung compliance and the drop in total
pulmonary resistance) mainly reflect the changes in mechanical properties of
the lung that come with the progressive clearing of the pulmonary fluid and the
expansion of the lungs (Mortola, 2001).
Mean values of body weight (BW), rectal temperature (RT), heart
rate (HR) and respiratory rate (RR) obtained from singleton and twin lambs
during the first month of life. Vertical bars denote ±95 %
confidence intervals.
Mean values of body weight (BW), rectal temperature (RT), heart
rate (HR) and respiratory rate (RR) obtained from singleton and twin kids
during the first month of life. Vertical bars denote ±95 %
confidence intervals.
The values of BW, RT, HR and RR showed no effect of twinning (P> 0.05)
in lambs (Fig. 1), whereas twin kids showed statistically
significantly lower BW and higher RT and HR values (P< 0.01) compared to
singletons at most of the considered data points (Fig. 2).
Both twin lambs and kids showed lower birth BW values compared to singletons
and their postnatal growth rates were relatively constant throughout the
monitoring period, such that the newborn twins were lighter than singletons
until day 30 of life. However, no statistically significant difference
in BW values between twin and singleton lambs was observed during the
monitoring period, whereas twin kids were statistically lighter than
singletons from birth until day 8 of life. This difference could be
due to a greater degree of intrauterine growth restriction in twin kids
with respect to twin lambs, possibly because of species differences (De Matteo et
al., 2008). It was demonstrated that twins are growth restricted in utero
compared with singletons because of the reduced placental oxygen and
nutrient availability (Aleksiev, 2009). Although an increase in litter size
is known to be associated with an increase in placental weight and exchange
surface area of cotyledons (Kaulfuss et al., 2000), this compensatory
mechanism is insufficient to meet all fetal requirements and the surface
area of cotyledons for each lamb decrease with increased litter size (Dwyer,
2003). The growth restriction in utero likely to occur in twins (De Matteo
et al., 2008) could also explain the statistically significant effect of
twinning on HR values observed in kids at birth and at most of the other
considered data points. In particular, twin kids showed higher HR values
with respect to singletons suggesting an altered nutritional or fluid homeostatic
status of twins (De Matteo et al., 2008) that is probably the result of the small size of the heart of twins compared to that of singletons. Effectively,
catch-up growth likely to occur in twins during intrauterine life has
significant implications for later health, as organs that have terminally
developed in proportion to body size in utero may be reduced in size or
complexity relative to body size after catch-up growth (Mitchel et al.,
2004; De Matteo et al., 2008). The RT values measured in twin kids were
statistically higher than in singleton kids during the first week of life. This
difference might indicate a different degree of physiological maturation of
homoeothermic mechanisms in singleton and twin kids at birth and of their
ability to activate heat-producing and/or heat-preserving mechanisms, which
ultimately influence body heat (Aleksiev, 2009). Twin kids
showed a more marked decrease in RT within 24 h after birth with respect to
singletons. This suggests that twins cooled to a greater extent than
singletons, which may partly reflect the effect of body weight (Aleksiev,
2009). It has been stated that light newborns have a greater surface area to body
mass ratio, which results in an increased body heat loss to the environment
(Stafford et al., 2007). The heavier singletons had lower RT values after
delivery compared to the lighter twins. It could be assumed that singletons
made use of shivering thermogenesis to a lesser extent than the twins with
lower birth weight and there may also be insufficient cold stimuli to cause a metabolic overreaction and RT increase.
Conclusions
Under the conditions of this study, despite the observed changes, all
newborn kids and lambs exhibited good homeostatic ability and were able to
maintain the assessed parameters within the physiological limits. The
results obtained in this study make a contribution to the knowledge of
homeostatic, cardiorespiratory and thermoregulatory adaptations occurring
both in singleton and in twin lambs and kids during the first 30 days of
life. Moreover, our findings indicate that the BW, RT, HR and RR values,
whose homeostasis is still evolving in newborn, should be interpreted
dynamically as a function of the period of postnatal adaptation and also of the type
of birth.
Further aspects of homeostatic, cardiorespiratory and thermoregulatory
adaptations in a greater number of twin and single-born lambs and kids are
worth exploring.
All authors have made substantial contributions to each step of the experimental
procedure and manuscript preparation. In particular,
Francesco Fazio designed the experiment and performed the sampling, Francesca Arfuso performed
the laboratory analysis and Claudia Giannetto analyzed the data. Francesca Arfuso and Elisabetta Giudice
prepared the paper. Giuseppe Piccione supervised all stages of the experimental study. Edited by: S. Maak Reviewed by: V. Nagyova and two anonymous referees
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