Beneficial effects of Beta-carotene injections
prior to treatment with PGF2α on the fertility
of postpartum dairy cows
S.S. AY1*, D. KAYA2, I. KUCUKASLAN3, A.R. AGAOGLU4, B. EMRE5, J. HANDLER6, M. FINDIK1, S. ASLAN7
Ondokuz Mayis University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynaecology, 55139, Kurupelit, Samsun, TURKEY.
Kafkas University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynaecology, 36300, Pasacayiri, Kars, TURKEY.
3Dicle University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynaecology, 21280, Diyarbakir, TURKEY.
4Mehmet Akif Ersoy University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynecology, 15030, Burdur, TURKEY.
5Harran University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynecology, 63200, Urfa, TURKEY.
6Clinic for Horses, Department of Veterinary Medicine, Freie Universität Berlin, GERMANY.
7Ankara University, Faculty of Veterinary Medicine,Department of Obstetrics and Gynaecology, 06110, Diskapi, Ankara, TURKEY.
1
2
*Corresponding author: [email protected] or [email protected]
SUMMARY
This study examined the effects of Beta-carotene (βC) injections before estrus
synchronization with PGF2α on fertility parameters in cows. A total of 124
postpartum (pp) cows were used. In GI (n=25), βC (Carofertin®, 0.4
mg/kgBW, i.m.) was injected on d 15 and 45 pp. In GII (n=25), βC was administered on d 15 pp. In GIII (n=25), βC was administered on d 45 pp. In
GIV (n=25), βC was injected on d 35 and 45 pp. GV (n=24) was set aside as
a control group. All animals received PGF2α (Iliren®, 0.0015 mg/kgBW,
i.m.) on d 50 and 61 pp. Blood samples were collected on d 15, 48 and three
days after each βC injection. The overall pregnancy rate was determined to
be higher in GI (100%) and GIV (88.0%) than GV (70.8%) (P<0.01). The
number of services per conception was the lowest in GI (1.4) and GII (1.4),
while days of first service were lower in GIII (90.3 d) and GIV (90.8 d)
(P<0.05). The insemination index was found to be lowest in GI (1.4). These
results suggest that two administrations of βC in the early and late pp period
before administering PGF2α can improve fertility. It was concluded that when
serum βC concentrations remain high for a long time (30d) as a results of βC
injections, fertility can be improved.
Keywords: Beta-carotene, fertility parameters, postpartum
cows.
RÉSUMÉ
Effets d’ administrations de bêta-carotène avant le traitement avec des
PGF2α sur la fertilité des vaches laitières au cours du post-partum
Cette étude a examiné les effets d’administrations de bêta-carotène (βC) réalisées avant un traitement de synchronisation de l'œstrus avec des PGF2α sur
les paramètres de la fertilité chez la vache en post-partum (pp). L’étude a
concerné au total 124 vaches en post-partum Les vaches du groupe I (n = 25)
ont reçu une administration de βC (Carofertin®, 0,4 mg/kgBW, im) 15 et 45 jours
après la parturition. Les vaches du groupe II (n = 25) et du groupe III (n = 25)
ont reçu une seule administration de βC à la même dose au stade 15 jour pp.
Les vaches du groupe IV ont reçu une administration de βC 35 et 45 jours pp.
Les vaches du groupe V (n=24) ont constitué le groupe contrôle. Tous les animaux ont reçu une administration de PGF2α (Iliren®, 0,0015 mg/kgBW, im)
50 et 61 jours après la parturition. Les prélèvements de sang ont été réalisés
au cours des 15ème et 48ème jours pp et trois jours après chaque administration
de βC. Les taux de gestation des vaches du groupe I (100 %) et du groupe IV
(88,0 %) ont été supérieurs à celui du groupe contrôle (GV, 70,8 %, P < 0,01).
Le nombre d'inséminations par conception a été le plus faible pour les vaches
des groupes I et II (1,4), tandis que le nombre de jours avant le premier service
a été le plus faible pour les vaches des groupes III (90,3 d) et IV (90,8 d, P < 0,05).
Nos résultats suggèrent que deux administrations de βC, réalisées au début
et à la fin de la période pp avant un traitement aux PGF2α, pourrait améliorer
la fertilité. Il a é été conclu que le maintien de concentrations sériques élevées
pendant les 30 jours suivant la parturition pourrait améliorer de la fertilité associée au traitement.
Mots clés : Bêta-carotène, paramètres de fertilité, vaches,
post-partum.
Introduction
Beta-carotene (βC) is the primary precursor for vitamin A
but it also acts independently from vitamin A. It is mainly intake from forages. After being metabolized in the intestine, it
is absorbed as retinol [35] and transported with high density
lipoproteins and stored in liver and adipose tissue. The corpus
luteum (CL) contains high βC levels [3]. Beta-carotene serum
concentrations vary depending on breed, lactation [34], peripartal stage [23] and nutrition [35]. Beta-carotene concentrations
in plasma, CL and follicular fluid also vary according to the
stage of the estrous cycle or pregnancy [18].
Revue Méd. Vét., 2012, 163, 8-9, 387-392
A positive relationship between supplemental βC and reproductive function has been demonstrated [20]. Low βC
concentrations in blood serum have been associated with prolonged estrus, silent estrus [19] and signs of estrus that are
less pronounced [24]. It has been reported that the addition of
βC to daily rations during pre-and post-partum periods significantly increases conception rates while reducing the pregnancy index (PI; number of services per pregnancy) [22].
Many authors reported an increase in infertility as a result of
deficient of βC in cows [5, 31].
It has been reported that delayed formation of the CL and
low progesterone (P4) production after estrus are observed in
388
cows with low serum concentrations of βC [5]. A positive correlation has been reported between βC concentrations in the
CL, CL diameter and plasma P4 concentrations during different stages of estrus and the second trimester of pregnancy [6,
18]. KAWASHIMA et al. [27] demonstrated that changes in
plasma βC concentrations during the peripartum period differ
between ovulatory and anovulatory cows during the first follicular wave postpartum. This indicates that low βC concentrations in plasma during the prepartum period may be one of
the factors related to the complex mechanism of first postpartum anovulation in dairy cows.
Beta-carotene is also a potent antioxidant [10] and giving it
has an important role in immunity. During the first 24 hours
after parturition, plasma βC concentrations decrease in cows,
but increase in newborns fed colostrum, and a positive correlation between the plasma concentration in cows and colostrum has been reported [26].
Calving, the involution period and the start of lactation result
in metabolic stress associated with an increase in the production
of free radicals and reactive oxygen species [16]. Administration of antioxidants and an adequate supply of nutrients are
the most appropriate strategies for eliminating or minimizing
metabolic stress and its detrimental effect [12]. It is well
known that during this period, especially during the first week
of the pp period, the βC concentrations in plasma dramatically
decrease in cows [33]. Therefore this study was designed to
determine the effects of postpartum βC injections on blood
serum βC concentrations, fertility parameters and reproductive disorders in cows before synchronization with PGF2α.
AY (S.S.) AND COLLABORATORS
BS= Blood Samples; AI: Artificial Insemination.
FIGURE 1: Schematic view of the study design.
POSTPARTUM EXAMINATIONS, ARTIFICIAL INSEMINATIONS
AND PREGNANCY CONTROL
Postpartum examinations were performed with transrectal
palpation, ultrasonography and vaginoscopy on d 30, 45 pp and
before the AI in all groups. All animals were inseminated after
d 61 pp when estrus was first observed by an experienced veterinarian. Diagnosis of pregnancy was performed with ultrasonography (Agroscan L, 5 MHz, ECM, Angouléme, France)
on d 30 and 45 after insemination. Endometritis was determined
according to criteria specified by KAYA [28]. According to
these criteria, in transrectal palpation, the location of the uterus,
the diameters of the horns and the presence of asymmetry were
investigated. In the ultrasonographic examination, fluid accumulation in the uterine lumen was evaluated. Finally, during the
vaginoscopic examination the presence and character of cervical
discharge were investigated.
BLOOD SAMPLES AND BETA-CAROTENE ASSAYS
Material and Methods
ANIMALS AND TREATMENTS
The study consisted of 124 postpartum (pp) Holstein-Friesian
cows between 4 to 5 years of age without any pp problems,
such as retained fetal membranes and acute metritis. The study
was performed on a commercial dairy farm and cows were
fed with a total mix ration twice daily that included corn and
grass silage, hay, canola and a balanced grain ration. Animals
were divided randomly into five groups.
First, βC was administered to all groups through an injection.
The βC dose was determined in accordance with previous data
[13] and the manufacture’s recommendation. The total dose
was divided into two doses and injected in different areas of
the rump. In group I (GI; n=25), βC (Carofertin®, 0.4 mg/kgBW
i.m., Alvetra&Werfft AG) was injected two times on d 15 and
45 pp. In group II (GII; n=25), βC was administered only once
on d 15 pp. In group III (GIII; n=25), βC was also injected
only once on d 45 pp. In Group IV (GIV; n=25), βC was administered two times on d 35 and 45 pp. In Group V (GV;
n=24), no βC injection was given and it was kept as a control
group. All of the animals in the study received PGF2α (Tiaprost trometamol, Iliren® 0.0015 mg/kgBW; i.m., Intervet)
on d 50 and 61 pp after the βC injection (Figure 1).
Blood samples were collected just before βC injections and
on d 15 pp, i.e. at the start of the study, and three d after each
βC injection in all groups, i.e., on d 18 pp in GI; on d 48 pp
in GIII and on d 38 pp in GIV. Blood samples were also collected on d 48 pp in all groups. In GV, it was only collected
on d 15 and 48 pp (Figure 1).
Ten milliliters of blood samples for determination of serum
concentration of βC was obtained from jugular vein by use of
vacutainer vials. Blood samples were centrifuged immediately
after collection for 15 min at 2000 x g at room temperature;
serum was decanted and stored at -20°C until assayed.
Beta-carotene concentrations were determined by spectrophotometric analysis and measured as described previously
[39] after extraction using a carotene photometer (Schimadzu
UV-mini 1240). Extraction efficiency was > 95%. The interassay coefficients of variation averaged 9.7%.
FERTILITY PARAMETERS
The following parameters were evaluated in this study: The
reproductive disorder rate (endometritis and cystic ovaries;
%), first service pregnancy rates (FSPR; pregnancy rates after
first insemination; %), overall pregnancy rates (OPR: pregnancy rates after a maximum of three consequent inseminaRevue Méd. Vét., 2012, 163, 8-9, 387-392
THE EFFECT OF BETA-CAROTENE ON FERTILITY IN COWS
tions; %), pregnancy index (PI: number of services per pregnancy), insemination index (INI: number of services per animal), days to first service (D-FS: time from calving to first
service; day), days open (D-OP: time from calving to pregnancy; day). Fertility parameters of the cows with reproductive
disorders were not evaluated.
389
the values obtained on d 15 and 38 pp in GIV (P < 0.001).
On the other hand, there was no difference between on d 38
and 48 pp (P > 0.05). However, no statistically significant difference was found between GIII and GIV (P > 0.05) on d 48
pp (Table I and Figure 2).
STATISTICAL ANALYSIS
The data were analyzed statistically using SPSS® 16.0
(SPSS Inc, Chicago, Illinois, USA). Descriptive statistics was
used for determination of mean and standard error of means.
Non-parametric tests were used for inter- and intra-group analysis and the One-Way ANOVA test for comparison of values
in the groups. The data structure take into considering error
of variances, homogeneity control was done by homogeneity
of variance test in post hoc analysis. Tukey Multiple Range
Test procedure in post hoc analysis was applied to the data
with assuming equal variances, however, for unequal variances assuming, Tamhane’s T2 test was also used in the data
set. The Fisher’s exact test was used to compare rates (Endometritis, OPR and FSPR). Differences were considered significant when P < 0.05.
Results
Beta-carotene concentrations were found to increase substantially (P < 0.001) on d 15 and 48 in all groups injected with
βC (GI, GII, GIII and GIV). βC serum concentrations were
increased in GII (P < 0.01) on d 48, but remained lower than
the values obtained in the other groups. The greatest increase
in βC concentrations was found on d 48 pp compared to d 15
pp in GIV, to which βC injections were administered on d 35
and 45 pp (P < 0.001). No increase was found in the control
group (P > 0.05) (Table I).
There were no differences in βC concentrations in any of
the groups on d 15 pp (P > 0.05) when the βC concentrations
were compared. However, a significant increase was found in
the groups on d 48 pp, when βC concentrations were found
to be significantly higher in groups injected with βC (GI, GII,
GIII and GIV) than in GV (P < 0.001). The βC concentrations
were found to be higher on d 18 than on d 15 pp in GI and
GII (P < 0.001). There was a significant difference between
Days
15
18
38
48
P Value
GI1 (n=25)
94.7 ± 11.2a
238.5 ± 26.2b
355.5 ± 36.7b,c
a:b < 0.001
b:c < 0.05
GII2 (n=25)
103.3 ± 13.7a
298.8 ± 31.6b
192.4 ± 24.2c
a:b < 0.001
a:c < 0.01
Black bars with differnt superscripts (a, b, c, d) are significantly different
(P < 0.001), white bars with same superscripts (a) are not significantly
different (P > 0.05).
FIGURE 2: Blood serum concentration of βC (μg/dl) in groups on d 15
and 48.
After the injections, OPR was determined to be significantly
higher in GI (100%; P < 0.01) and GIV (88.0; P < 0.05) than
it was in other groups (GII, GIII and GV; 80%, 84% and
70.8%, respectively). On the other hand, the INI of GI was
determined to be significantly lower than GIII and GV (P <
0.05). The D-FS were found significantly lower in GI, GIII
and GIV than in GV (P < 0.05) (Table II). The D-OP values
of GI and GII tended to be lower than those of GIII and GV
(P < 0.07).
The number of cases of endometritis in the study was found
to be significantly (P < 0.05) lower in GIV (0.0%) than in the
control group (16.66%) while it was lower in other study
groups (8.0%; GI, GII and GIII) compared to GIV (Table III).
All cases of endometritis were detected after d 61.
Discussion
It has been demonstrated that βC is normally transported to
the ovary and CL with high density lipoproteins in the cow
GIII3 (n=25)
108.9 ± 13.7a
410.9 ± 24.1b
GIV4 (n=25)
85.8 ± 18.7a
366.6 ± 30.6b
441.9 ± 29.8b
GV (n=24)
73.5 ± 10.2a
105.3 ± 10.8a
a:b < 0.001
a:b < 0.001
NS
(-):Blood samples were not collected.
1,2,3,4Values with different superscripts in the same column (a,b,c) are significantly different (P < 0.001;P < 0.01; P < 0.05).
Values with the same superscripts in the same column are not significantly (NS) different (P > 0.05).
TABLE I: Blood serum βC concentrations (μg/dl).
Revue Méd. Vét., 2012, 163, 8-9, 387-392
390
AY (S.S.) AND COLLABORATORS
Parameters
FSPR (%)
GI (n=25)
60.0a
GII (n=25)
56.0a
GIII (n=25)
44.0a
GIV (n=25)
40.0a
GV (n=24)
45.8a
OPR (%)
100a,c
80.0b
84.0b
88.0a
70.8b,d
PI (No)
INI(No)
D-FS
X±SD; d)
D-OP
(X±SD; d)
1.4a
1.4a
1.4a
1.8a,b
1.6a
2.0b
1.6a
1.9a,b
1.5a
2.0b
P value
NS
a,b: < 0.05
c,d: < 0.01
NS
a,b: < 0.05
95.9±6.2a,b
98.2±7.4a
90.3±7.2a,b
90.8±5.5a,b
112.9±10.8c
b,c: < 0.05
100.2±7.6a
101.6±6.3a
114.9±13.6a
111.2±7.7a
114.4±10.4a
NS
GV (n=24)
16.66a,c
8.3a
P value
b:c < 0.05
NS
Values with different superscripts (a,b,c) in the same row are significantly different (P < 0.05; P < 0.01 ).
NS:Non-Significant
TABLE II: Fertility parameters evaluated in the present study.
Parameters (%) GI (n=25)
Endometritis
8.0a
Cystic ovaries
0.0a
GII (n=25)
8.0a
0.0a
GIII (n=25)
8.0a
0.0a
GIV (n=25)
0.0a,b
4.0a
Values with different superscripts (b, c) in the same row are significantly different (P < 0.05).
NS: Non-Significant
TABLE III: Rate of reproductive disorders in groups.
[37], and has a positive effect on LH secretion [17]. Therefore,
the aim of this study was to show how fertility parameters
improved by performing βC injections before the PGF2α applications applied shortly after uterine involution completed
both clinically and histologically [40] and also in the early
postpartum period when the pituitary gland becomes responsive
to GnRH [41].
In the present study, subsequent to the βC injections, significant increases in serum βC concentrations were observed in
all of the treated groups while during the same period in the
control group, only a tendency was found. There are studies
showing an increase in blood serum βC concentrations after
βC injections and supplementation. These studies reported
that βC concentrations remained high between 16 and 19 d
after βC injections [1, 38]. In GII, with a single injection of
βC on d 15 pp, a significant decrease in serum βC concentrations
was found within 30 d after the injection.
It seems that an increase in serum βC concentrations in GI
with two injections of βC at d 15 and 45 pp preceding PGF2α
administration has a positive effect on fertility parameters
(OPR=100%; PI=1.4). On the other hand, although improvement of fertility parameters was found in GIV as a result of
βC injections on d 35 and 45 pp, PI (1.6) was found to be higher
than in the other groups. There was significantly lower OPR
(70.8%) and longer D-FS (112.9 d) in GV, which was injected
only with PGF2α compared to GI (100% and 95.2 d, respectively). Supplemental βC may increase pregnancy rates for
heat-stressed cattle in the summer [1]. Daily supplementation
of βC reduces PI and increases OPR in the pre- and post-partum
stage [29]. Some researchers have reported that an increase in
embryonic death in cows with lower serum βC concentrations
[6] and higher serum βC concentrations has a positive effect
on embryo quality in cattle [38]. In this study, the effect of
high serum βC concentration on the embryo and other factors
obtained from βC injections is considered to increase fertility.
The uptake of βC by the CL and the endometrium in various
species has been demonstrated by previous studies [14, 36].
Therefore, as an antioxidant, βC in the endometrium provides
a more optimal uterine environment for implantation and embryo development [43]. This finding might explain the high
OPR results after βC injections. The data obtained from this
study suggest that βC injections prior to PGF2α injections increase OPR. Moreover, the report from ARECHIGA et al. [1]
might explain why the double injection of βC is more effective
in terms of improving OPR than the single injection in our
study. According to this report, there is a need for long term
supplementation in heat stressed cows in order to provide adequate βC concentration in uterine tissue.
DRILLICH et al. [14] reported that days open in cows with
spontaneous estrus and induced estrus (PGF2α) yielded 110.9
± 34.5 and 113.5 ± 35.5 d (P > 0.05), respectively. While DFS was found to be similar to GV (112.9 ± 10.8 d) in this
study, it was found to be lower in all injected groups. It was
also determined to be significantly lower in GI, GIII and GIV
than in the GV. Although, D-OP was found between 100.2 and
114.9 d in all groups, which is similar to our present research,
no significant difference was found among the groups.
KAWASHIMA et al. [27] reported that both the energy status
and plasma βC concentrations during the peripartum period
may affect ovulation in the first follicular pp wave in dairy
cows. Plasma concentrations of βC decrease throughout the
dry period and reach their nadir in about the first week pp.
The lower plasma βC concentrations during the prepartum period directly affect the occurrence of anovulation [27, 42]
Revue Méd. Vét., 2012, 163, 8-9, 387-392
THE EFFECT OF BETA-CAROTENE ON FERTILITY IN COWS
since it takes about six weeks for antral follicles to reach the
preovulatory stage [42] while the dominant follicle of the first
or second follicular wave reaches preovulatory size at two to
three weeks pp. These physiological explanations demonstrate
why the PGF2α application after the βC injections on d 15
and 45 pp, which were administered to positively influence
of ovarian activity, increased fertility parameters. In our opinion, βC injections applied during this period enhance the positive effect of some other hormones and various factors that
are important to the genital tract by increasing serum βC
concentrations. Thus βC injections make the sexual cycle’s
synchronization with PGF2α more successful.
The supplementation of βC reduced the incidence of retentio
secundinarum and endometritis in cows [30]. ASLAN et al.
[5] also demonstrated that βC injections combined with
GnRH injections during the postpartum period reduced puerperal disorders and improved fertility in cows. The data showed
that the endometritis rate after the βC injection was found to
be higher in the GV (16.66%) than in injected groups. It might
be supposed that the incidence of endometritis in GV was higher considering that the number of animals in each group is
equal though the incidence of endometritis in the GV was only
significantly higher compared to GIV. The relationship between immunity and βC is well known. Beta-carotene involves
the leukocyte membrane [8] and stimulates lymphocyte proliferation and phagocytosis. As a result, the activated natural
defense mechanism leads to a decreased incidence of mastitis
[9, 33] and retentio secundinarum [33]. KAEWLAMUN et
al. [25] have shown that the percentage of neutrophils in endometrial swab from the cervix and uterus at d 28 pp is lower
in the group that received βC than it is in the control group.
These data may explain the lower incidence of endometritis
in the groups that received βC in our study.
Beta-carotene is found in the bovine CL in extremely high
concentrations and is responsible for the characteristic bright
yellow color of the CL [36]. Using the Raman spectroscopy
method, ARIKAN et al. [3] has shown that βC is spread over
the entire volume of the luteal cells with higher concentrations
occurring at distinct sites, including the surface. It has been
reported that high LH and βC concentrations in luteal cells
may be involved in luteolysis [2]. It is also known that the βC
deficiency plays an important role in the formation of ovarian
cysts [7]. INABA et al. [21] reported that cows with ovarian
cysts had significantly lower plasma βC concentrations than
cows without ovarian cysts. It has also been reported that cows
which receive βC supplements cows have a much lower incidence of ovarian cysts than cows without supplements [32].
As a result of the early pp βC injections, ovarian cysts were
not found due to an increase in the concentrations of serum
βC. However, ovarian cysts were found in only one case in
GIV (4.0%), and two cases in the GV (8.3%). Ovarian cyst
results in this study correspond to the findings of earlier research, which are consistent with follicular wave and anovulation. Several studies have failed to find beneficial effects on
fertility from βC supplementation [4, 15], but both studies are
related to follicular wave [27, 42] and our findings suggest
that the injection time of βC is important.
It has also been reported that more than 50% of the cysts
regressed spontaneously in the early pp period [27, 42], and
Revue Méd. Vét., 2012, 163, 8-9, 387-392
391
the majority of ovarian cysts (70%) developed within 45 d
after calving [44]. The rate of 4.0% suggests that ovarian cysts
in GIV might be a consequence of injections of βC during the
late pp period. In this study, the fact that groups which were
injected with βC in the early pp period did not develop ovarian
cysts supports the authors referred to above.
In summary, the data obtained from this study clearly show
the positive effect of βC injections on fertility parameters.
Even a single injection of βC during the pp period before
PGF2α treatment is sufficient to increase blood βC concentrations and improve fertility. On the other hand, a double injection of βC in both early (d15) and late (d45) pp period is
much more effective at improving fertility, especially OPR,
in cows. These positive effects can be related to various factors
in the endometrium [12]. Therefore, further studies are necessary to investigate the relationship between endometrial factors and βC supplementation; its dose, supplementation route,
and the time of administration.
In conclusion, this study demonstrated that βC injections
have a significant positive effect on fertility parameters at d
15 and 45 pp before the PGF2α injections. It was concluded
that with this method of administration in GI results in a better
OPR, PI and INI as well as significantly lower D-OP than in
the other groups in this study.
Acknowledgement
The authors thanks Alvetra&Werfft AG (Wien, Austria) for
their financial supports; and Akbel Milk and Milk Product
Company (Eregli, Turkey) for making this study possible in
their dairy farm.
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