This study aimed to investigate relations between
insulin-like growth factor-1 (IGF-1) concentrations and some body trait
measurements (body weight, withers height, rump height, body length, chest depth, chest
width, chest girth and cannon bone circumference) and climatic factors in
prepubertal male and female White (75 % Saanen and 25 %
Kilis goat) and Angora goat kids. For this purpose,
blood samples were regularly taken from the vena jugularis, and body trait
measurements were regularly carried out (every 15 d for 5 months) on each kid. The IGF-1
analysis on the blood serum was performed using the enzyme immunoassay (EIA)
method. Climatic values and the length of the photoperiod were obtained from the Turkish State
Meteorological Service for the experimental period, and the temperature–humidity
index (THI) was calculated using these values. Statistical
analysis showed that the IGF-1 concentrations were higher (P<0.05) in female White
goat kids. Furthermore, differences in IGF-1 concentrations were found (P<0.05) between
periods and between the gender groups for both the White and the Angora
goat kids. Moreover, the difference between the IGF-1 concentrations between genders
was higher (P<0.05) in White goat kids. Additionally, positive and significant correlations were found between IGF-1
concentrations and some body trait measurements in prepubertal kids, except for in female
White goat kids. In summary, it was found that there was a significant
relationship between IGF-1 concentrations and growth characteristics of the
goat kids. Furthermore, IGF-1 concentrations in the goat kids were significantly
influenced by climatic factors such as photoperiod, temperature and the
temperature–humidity index, with the release of IGF-1 increasing due to
increases in the photoperiod and the environmental temperature.
Introduction
Insulin-like growth factors (IGFs) are one of the most important compounds that
influence metabolism in animals. IGFs are a family of polypeptides
that carry out metabolic and mitogenic activities. The most potent mitogenic IGF
peptide is insulin-like growth factor-1 (IGF-1), a basic polypeptide of 70 amino acids directed by growth
hormone under normal physiological conditions (Buonomo et al., 1988). IGF-1
is mainly produced in the liver in addition to being produced by the environmental
tissues such as the skin, ovary, placenta, breast and bone as
autocrine/paracrine (Hashizume et al., 2000; Basturk, 2007). The bioactivity
of IGF-1 is achieved by specific insulin-like growth factor binding proteins
(IGFBPs) with high affinity (Obese et al., 2008).
IGF-1 plays an important role in various physiological processes such as
reproduction, growth, lactation and the health of the organism (McGuire et al.,
1992). IGF-1 is involved in the growth and function of almost every organ
in the body (Rasouli et al., 2017). The predominant physiological effect of
IGF-1 is the stimulation of postnatal body growth. In addition, IGF-1 can
regulate the synthesis of whole body protein, the uptake of glucose by
peripheral tissues and the regulation of lipid metabolism (Hadsell et al.,
2002).
IGF-1 is secreted nonpulsatile, and the secretion level of IGF-1 is
phenotypically correlated with the live weight and growth rate in cattle, pigs,
sheep and chickens (Bishop et al., 1989). In addition, it has been reported
that IGF-1 concentrations in farm animals are significantly affected by
environmental factors (Sarko et al., 1994). As a matter of fact, Spicer et
al. (1994) and Dahl et al. (1997) reported that photoperiod and IGF-1
concentration were positively correlated, Richards et al. (1995) reported a
negative correlation between environmental temperature and IGF-1
concentration, Moyes et al. (2003) reported that plasma IGF-1 concentrations
decreased when animals were in negative energy balance during the postpartum
period, Squires (2003) reported that short-term stress reduced IGF-1
secretion, and Magistrelli et al. (2005) reported that energy and protein
contents of rations are directly related to the plasma IGF-1 concentration.
However, studies regarding the association of IGF-1 concentrations with growth
traits and climatic factors have mainly been carried out on farm animal
species other than goats. From this point on, in this study,
the relationship between IGF-1 concentrations and some body trait
measurements and environmental factors such as temperature and photoperiod
are investigated in prepuberty period in male and female kids from two goat breeds that have different growth rates
(Cengiz et al., 1995; Erol et al., 2014); this difference is due to the fact that the Angora
goat is a fiber goat and the White goat is a milk goat.
Materials and methodsExperimental animals, location and management
This study was carried out on 13 White goat (75 % Saanen and 25 %
Kilis goat) kids and 12 Angora goat kids raised in the Animal Husbandry
Station (39∘57′42.5′′ N, 32∘51′56.2′′ E)
at the Ankara University, Faculty of Agriculture, Department of
Animal Science. All of the goat kids were clinically healthy. The animals were housed
in shaded pens with their dams, and natural light from windows and a door was allowed to pass through
to the pens. The goat kids were allowed to receive milk
from their dams during the experimental period, and from 2 weeks
old they were they were fed concentrate feed and alfalfa hay ad libitum. Experimental
feeds were collected during the experimental period and analyzed for chemical composition.
Dry matter, crude protein, crude fiber, crude ash and crude fat in
feeds were analyzed according to the AOAC Official Methods of Analysis (AOAC,
2000). Neutral detergent fibre (NDF) and acid detergent fibre (ADF) were
measured according to the methods described by Van Soest et al. (1991).
The metabolizable energy (ME) of forage and concentrate mix was calculated according
to the Turkish Standards Institute (TSE, 1991). The concentrated feed
composition and ME was as follows: dry matter (DM) comprised 91 %, crude protein (CP)
comprised 18.05 %, crude fiber (CF) comprised 8 %, crude ash comprised 7.5 % and ether
extract (EE) comprised 3.5 %; the ME was 2615 Kcal kg-1. The alfalfa
composition and ME was as follows: DM comprised 91.5 %,
CP comprised 13.0 %, CF comprised 34.0 %, crude ash comprised 8.29 %, EE
comprised 1.00 %, ADF comprised 8.0 %, NDF comprised 49.0 %;
the ME was 2000.22 kcal kg-1. Fresh water was always available to the goat kids.
Management of experimental goat kids did not interfere with the general
operation of the station, and the study was conducted within standard
ethical norms. Some properties of experimental goat kids are shown in
Table 1.
Some properties of the experimental goat kids.
BreedGendernAverage birthAverage age at the beginningAverage live weights at theweight (kg)of experiment (days)beginning of experiment (kg)White goat (n=13)Male73.06146.53Female63.10156.51Angora goat (n=12)Male72.91155.51Female52.50144.39Blood collection and IGF-1 analysis
During the experimental period, the first samples (Period 1) were taken 14–15 d
after birth, and samples (periods 2–10) were the taken at
15 d intervals for 5 months. On sampling days, blood samples were regularly taken
from the vena jugularis of each goat kid using vacuum containers
without anticoagulant (VACUETTE® TUBE 8 mL
Z Serum Sep Clot Activator). The blood samples were centrifuged at
4000×g for 5 min, and the serum was stored at -20∘C until
the analysis was carried out. IGF-1 concentrations were determined in the blood serum
using a commercial ELISA kit (Fine Test Goat IGF-1 Cat. no. EG0002). The intra- and
inter-assay coefficients of variation were <8 % and <10 %,
respectively. The least detectable concentration was 14 ng mL-1.
Measurement of body traits
With respect to body trait measurements, the body weight (BW), withers height (WH), rump height (RH),
body length (BL), chest depth (CD), chest width (CW), chest girth (CG) and
cannon bone circumference (CBC) of each kid were regularly measured on the
same sampling days. BW was measured using a commercial hanging scale (±10 g). A measuring tape was used to measure the height, length, depth and
width of the goat kids, whereas other body measurements were taken using a
flexible tape measure. All measurements were taken by the same operator and
followed the methodology of Herrera et al. (1996).
Climatic values, the temperature–humidity index (THI) and the
photoperiod
Climatic values and the photoperiod were obtained from the Turkish State
Meteorological Service (Anonymous, 2016) in order to estimate the severity of
heat stress during the experimental period. The temperature–humidity index (THI)
was calculated using the following equation, reported by Marai et al. (2001) for
sheep and goats:
where db ∘C is the dry bulb temperature (∘C) and RH is the
relative humidity (RH %)/100. The values obtained indicate the
following: < 22.2 signifies the absence of heat stress; 22.2 to < 23.3 represents moderate heat stress: 23.3 to <25.6 represents severe heat stress
and 25.6 and above represents extreme severe heat stress
(Marai et al., 2007).
In addition, the average climatic values, the THI index values and
the photoperiod lengths are shown in Table 2.
Average climatic values, the temperature–humidity index (THI) and
the length of the photoperiod during the experimental period.
* The first samples (Period 1) were taken 14–15 d after
birth, and the other samples (periods 2–10) were the taken at 15 d
intervals.
Statistical analysis
Data were analyzed by a mixed model in SAS (2017) using repeated measurement
analysis with breed, gender and period as fixed effects and the live weight of
the animal at the beginning of the experiment as the covariate. IGF-1 concentration
differences within and between groups and their interactions were evaluated.
Multiple comparisons were made using a Tukey test if significance was
indicated by the analysis of variance. Correlation coefficients (Pearson)
between IGF-1 concentrations and some body trait measurements were calculated according
to the CORR procedure in SAS (2017). Results are shown as the mean
± standard error (X‾±Sx‾), and the significance
level was set at α=0.05.
ResultsClimatic values during the experimental period
Patterns of climatic values during the experiment period are shown in
Fig. 1. As seen from Fig. 1, the photoperiod values increased until
Period 6, the THI and temperature values increased until Period 8 and then
they all gradually decreased thereafter. It has been determined that the
experimental kids were heat stressed during the last periods (from Period 6 to
Period 10) of the experiment (Table 2).
Changes in the average temperature, the temperature–humidity index (THI) and
the photoperiod during the experimental periods. * The first samples (Period 1) were taken
14–15 d after birth, and the other samples (periods 2–10) were
then carried out at 15 d intervals.
IGF-1 concentrations in prepubertal goat kids
IGF-1 concentrations in experimental kids progressively increased until
Period 8 and then progressively decreased until end of the experiment
(Fig. 2); the differences in the IGF-1 concentrations between the periods
were found to be statistically significant (P<0.05; Table 3). Significant
differences were found (P<0.05) with respect to IGF-1
concentrations between female and male kids in White goat kids, whereas no significant differences
between female and male kids were observed in Angora goat kids (regarding IGF-1
concentrations). Differences between the same genders from different breeds were also
found to be statistically important (P<0.05).
Changes in IGF-1 concentrations of kids during the experimental periods.
* The first samples (Period 1) were taken 14–15 d after birth, and the
other samples (periods 2–10) were then carried out at 15 d intervals.
Least squares means and standard errors (X‾±Sx‾) of IGF-1 concentrations in White goat and Angora goat kids.
Notes: a, b, c, d, e, f, g: Means in the same column with
different superscripts differ significantly at p<0.05. X, Y: Means in the same row with different superscripts differ significantly at
p<0.05 (in the comparison of the genders within breeds). A, B: Means in the same row with different superscripts differ significantly at
p<0.05 (in the comparison of the same gender between breeds). * The first
samples (Period 1) were taken 14–15 d after birth, and the other samples
(periods 2–10) were then carried out at 15 d intervals.
Some body trait measures in prepubertal goat kids
Periodic mean values of some body trait measures for White and Angora goat kids are
shown in Tables 4 and 5, respectively. An almost linear increase was observed
in all of the body trait measures in all of goat kids examined during the experimental
period. When the body weights of kids at the end of the experiment were
compared with their birth weights, it was found that White goat kids grew more than Angora goat
kids, and male kids grew more than female kids.
Periodic mean values (X‾±Sx‾) of some body
trait measures in White goat kids.
F: female; M: male; BW: body weight; WH: withers height; RH: rump
height; BL: body length; CD: chest depth; CW: chest width; CG: chest girth;
CBC: cannon bone circumference. * The first samples (Period 1) were taken 14–15 d
after birth, and the other samples (periods 2–10) were then carried out at
15 d intervals.
Periodic mean values (X‾±Sx‾) of some body
trait measures in Angora goat kids.
F: female; M: male; BW: body weight; WH: withers height; RH: rump
height; BL: body length; CD: chest depth; CW: chest width; CG: chest girth;
CBC: cannon bone circumference. * The first samples (Period 1) were taken 14–15 d
after birth, and the other samples (periods 2–10) were then carried out at
15 d intervals.
Correlations between IGF-1 concentrations and some body trait measures in
prepubertal goat kids
Phenotypic correlations between IGF-1 and some body trait measures in White goat
and Angora goat kids are shown in Table 6. Correlations between IGF-1 and
some body trait measures were not found to be statistically significant (P>0.05) in female White goat kids, whereas these correlations (except
CBC) were found to be statistically significant (P<0.01) in male White goat kids.
In Angora goat kids, IGF-1 concentrations were correlated with BW
(P<0.01), WH (P<0.01), RH (P<0.01), BL (P<0.01), CD (P<0.01), CW
(P<0.01), CG (P<0.01) and CBC (for females: P<0.01; for males P<0.05).
Correlation coefficients between IGF-1 and some body trait measures in
prepubertal goat kids.
This study was carried out from mid-April to mid-August, which
comprised a range of seasonal variations regarding factors such as the THI, the temperature and
the photoperiod that could affect the IGF-1 concentrations of the experimental goat kids.
Thus, the effects of climatic factors such as temperature, heat stress and
photoperiod on IGF-1 concentrations of experimental kids may have been
confounded with one another. Because the experiment was not carried out under
controlled photoperiod/temperature conditions, it was not clear which
climatic factors more heavily impacted the IGF-1 concentrations of the
prepubertal kids. However, in this study, the pattern of IGF-1 concentrations
in the kids was similar to the change in the photoperiod during the experimental period (Fig. 2).
It has also been previously reported that IGF-1 concentrations in farm animals are
significantly affected by environmental factors (Sarko et al., 1994). In many
previous studies, especially those conducted on ruminants, it is suggested that seasonal
changes in IGF-1 concentrations are mainly driven by photoperiod (Dahl et
al., 2000). In addition, it has been reported that the photoperiod has a significant effect
on IGF-1 concentrations in goats (Flores et al., 2015, 2018; Hernández et
al., 2016). Similarly, in a study carried out on male red deer, it was
reported that melatonin implantation, which had “short-day effects”, suppressed
IGF-1 release (Suttie et al., 1992). Another study on cattle reported that
the IGF-1 levels of cattle in a 16 h light per day group for 4 months
were considerably higher than those in an 8 h light per day group
(Spicer et al., 1994). Furthermore, in studies investigating the effect of
environmental temperature on IGF-1 concentrations in farm animals, Richards
et al. (1995) found a negative correlation between environmental temperature
and IGF-1 concentrations, and Aggarwal and Upadhyay (2013) reported that
IGF-1 concentrations in their study decreased during the summer months. Similarly, in this
study, it can be seen that IGF-1 concentrations of kids started to decrease
during periods of high temperature and heat stress (Figs. 1 and 2).
As seen from Tables 4 and 5, all body trait measures increased linearly
as the kids grew. However, there were differences both between breeds and
between genders in terms of the growth rate. It is known that IGF-1 concentrations show a
positive correlation with skeletal development, protein accumulation and
growth rate in farm animals (Bishop et al., 1989). Thus, positive
correlations between IGF-1 concentrations and live weight and weight gain
have been reported in farm animal species such as cattle, pigs, sheep and
poultry (Bishop et al., 1989; Davis and Simmen, 1997). In this study,
statistically significant positive correlations were also found between IGF-1
concentrations and some body trait measures in kids, except in female White goat kids
(Table 6). The presence of positive and significant correlations between
IGF-1 and growth traits is an expected outcome due to the growth and
development of prepubertal goat kids; however, these correlations may be
negative in adult goats. As a matter of fact, it has been reported that there is a
negative correlation between IGF-1 concentrations and body mass in 36
mammalian species, and that high IGF-1 levels allow for cancer growth and thus
shorten the animal's life span (Stuart and Page, 2010). However, this result contrasts
with the reported negative correlations (r=-0.56) between IGF-1
concentrations and live weight in Angora goat kids (Acuti et al., 2009). In
summary, the findings obtained from this study are generally compatible with
studies on other mammalian species.
Conclusion
Results of this study indicate that there is a significant relationship
between IGF-1 concentrations and growth characteristics of goat kids.
IGF-1 releases in prepubertal goat kids increased due to increases in the
photoperiod and environmental temperature, and statistically
significant positive correlations between IGF-1 concentrations
and some body trait measures were also found in prepubertal kids.
Data availability
The data sets can be taken from the figures/tables or are available upon request from the corresponding author.
Competing interests
The author declares that there is no conflict of
interest.
Acknowledgements
The author would like to thank Gursel Dellal for valuable suggestions on the
writing of this paper, Huseyin Polat for carrying out the hormone analysis and Seyrani Koncagul
for helping with the statistical analysis.
The author is also grateful for their general support in the realization of this study.
This research did not receive any specific grants from funding agencies in the
public, commercial or not-for-profit sectors.
Review statement
This paper was edited by Manfred Mielenz and reviewed by
Huseyin Polat and one anonymous referee.
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