Effect of progesterone administration

during growing phase of first dominant

follicle on follicular wave pattern in buffalo
heifers

M. H. Jan, H. Kumar, S. Kumar,

R. K. Sharma, A. Gupta & K. L. Mehrara

Tropical Animal Health and

Production

ISSN 0049-4747

Trop Anim Health Prod

DOI 10.1007/s11250-019-02143-2

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Tropical Animal Health and Production
https://doi.org/10.1007/s11250-019-02143-2

REGULAR ARTICLES

Effect of progesterone administration during growing phase of first

dominant follicle on follicular wave pattern in buffalo heifers
M. H. Jan 1 & H. Kumar 2 & S. Kumar 1 & R. K. Sharma 3 & A. Gupta 1 & K. L. Mehrara 1

Received: 26 June 2019 / Accepted: 31 October 2019

# Springer Nature B.V. 2019

Abstract
In buffaloes, like other domestic mammals, antral follicles develop in a wave-like pattern. Factors predictive of a particular
follicular wave pattern are yet to be identified. In this study, we examined the preponderance of 2- versus 3-wave patterns in 46
interovulatory intervals (IOIs) from 36 buffalo heifers, in which a subset of 10 heifers was scanned for 2 consecutive IOIs to
record the repeatability of follicular wave pattern. Two-wave pattern was detected in 63.0% and 3-wave follicular pattern in
27.0% IOIs. The dominant follicles (DF) of both wave 1 as well as the ovulatory wave attained a smaller (P < 0.05) maximum
diameter in 3-wave cycle as compared to 2-wave cycle. The mean duration of IOI was significantly shorter in 2-wave
compared to three-wave cycles (20.5 ± 0.3 vs. 22.3 ± 0.2 days; P < 0.05). Out of 10 buffalo heifers, 7 displayed non-
alternating patterns and 3 had alternating follicular wave patterns. We also tested the hypothesis that progesterone adminis-
tration during early IOI results in increased preponderance of 3-wave pattern and heifers inseminated after ovulation of the
third wave DF will have greater fertility. Sixteen heifers subjected to progesterone treatment from D0 (day of ovulation) in a
decreasing dose until D5 were compared with control heifers (n = 10). Progesterone treatment significantly reduced the
maximum diameter of DF of wave 1 (P < 0.001), whereas the mean duration of IOI remained unchanged (P > 0.05) between
the two groups. Progesterone administration during early IOI significantly increased the proportion of 3-wave cycles as
compared to control (P < 0.05). The hypothesis that progesterone administration during IOI results in increased preponderance
of 3-wave pattern was supported. However, no change in fertility was recorded in progesterone-treated heifers (7 pregnant out
of 16; 43.8%) as compared to untreated control heifers (4 out of 10 heifers; 40.0%). In summary, progesterone administration
in buffalo heifers during the growing phase of wave 1 resulted in greater preponderance of 3-wave follicular patterns, with no
significant effect on fertility.

Keywords Buffalo heifers . Follicular wave . Fertility . Interovulatory interval . Progesterone

Introduction in number of waves is due to difference in CL life span

Studies in the buffalo have unequivocally reported a greater
preponderance of 2-wave over 3-wave follicular dynamics
(Baruselli et al. 1997; Manik et al. 1998; Warriach and
Ahmad 2007). Previously, it was believed that the difference
* M. H. Jan
mhjan.ivri@gmail.com
1
ICAR-Central Institute for Research on Buffaloes, Sub-Campus,
Nabha, Punjab 147201, India
2
ICAR-Indian Veterinary Research Institute, Izatnagar, UP, India
3
ICAR-Central Institute for Research on Buffaloes, Hisar, Haryana,
India
(Ginther et al. 1989b). Recent studies suggest the role of
intraovarian location of corpus luteum and dominant follicle
in regulation of 2- vs. 3-wave pattern in cattle (Ginther et al.
2013a, b, c, d, 2014b, 2015; Ginther and Bashir 2013).
Furthermore, a reciprocal relationship between dominant fol-
licle and FSH surge has been implicated in regulating the
follicle emergence and dominance in wave 1 and wave 2
(Ginther et al. 2013c, 2014b). A complex hormonal dynamic
is observed in 2- vs. 3-wave follicle patterns which are repeat-
able in heifers (Ginther et al. 2013c, d).
More recent evidence has emerged to show that changes in
the mechanisms regulating follicular growth rate influence the
wave pattern and that the cycle length is the effect rather than
cause of follicular wave pattern (Jaiswal et al. 2009; Boer et al.
2011). It was postulated that the 2-wave pattern is a default
 Author's personal copy
pattern and an alteration in the dominance of the dominant
follicle (DF) of wave 1 induces the occurrence of a 3-wave
pattern (Jaiswal et al. 2009). In the cattle (Fortune 1993) and
buffalo (Baruselli et al. 1997), the early emergence of second
wave (9 vs. 11 d) and late onset of luteolysis in 3-wave estrous
cycles as compared to 2-wave cycles has been recorded that
may be the consequence of the weaker dominance of the DF
of wave 1. Perhaps extended dominance of wave 1 in 2-wave
patterns (Fortune et al. 1988; Sirois and Fortune 1988; Savio
et al. 1988; Baruselli et al. 1997; Jaiswal et al. 2009) is asso-
ciated with extended estrogen production (Singh et al. 1998),
resulting in early luteal regression in 2-wave patterns as com-
pared to 3-wave cycles (14.1 ± 0.3 vs. 16.6 ± 0.4 d in cow). In
cattle, it was reported that the duration of the DF of wave 1 is
inversely related to the day of onset of luteal regression, the
number of waves per interovulatory interval (IOI) and the
duration of the IOI (Jaiswal et al. 2009), indicating that a
shorter dominance period may be associated with late onset
of luteal regression, 3-wave pattern and longer IOI. Therefore,
any attempt to reduce dominance period of DF of wave 1 may
be associated with late onset of luteal regression and 3-wave
pattern. Adams and co-workers (Adams et al. 1992) adminis-
tered decreasing doses of progesterone from day 0 to 5
through subcutaneous route to cycling heifers. They reported
that progesterone administration during early luteal phase ab-
breviated the period of dominance, induced suppression of DF
of wave 1, hastened the second FSH surge and resulted in
early emergence of wave 2.
Our hypothesis is that the shortening the dominance
phase of wave 1 in 2-wave pattern will result in early
emergence of 2nd wave and the need for 3rd wave to
emerge before luteal regression occurs, thereby
transforming the 2-wave pattern into 3-wave pattern.
The shorter dominance of DF of wave 1 will be induced
by early exposure of wave 1 to high progesterone envi-
ronment that limits LH secretion necessary for the growth
of follicle. Furthermore, it is believed that 2-waves yield
follicles that are older (~ 3 days) and larger at ovulation
than 3-waves (Baruselli et al. 1997; Sichtar et al. 2010).
Extended duration of dominance of the ovulatory follicle
has a detrimental effect on pregnancy rate in cattle (Mihm
et al. 1994; Ahmad et al. 1996; Austin et al. 1999; Bleach
et al. 2004). It was found that pregnancy rate was high in
3-wave pattern as compared to 2-wave pattern (Townson
et al. 2002). Therefore, the second hypothesis that proges-
terone exposure during early growth phase of wave 1 will
increase pregnancy rate of the cycle due to transformation
of 2-wave patterns normally present into 3-wave patterns.
The objectives of the present study were to determine the
preponderance of follicular wave patterns and their repeat-
ability in Nili-Ravi buffalo heifers and the response to
progesterone administration during early growth phase
of wave 1, and fertility after AI.
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Materials and methods
Experimental animals
The present study was conducted at the Central Institute for
Research on Buffaloes, Nabha, in the Punjab State of India.
The experimental station is located at 30°22′ N latitude and
76°12′ E longitude, having tropical climate characteristics
where the weather is hot and sub-humid for most of the year,
yearly temperature ranges from a minimum of 2 °C to a max-
imum of 48 °C and yearly relative humidity ranges from a
minimum of 50% to a maximum of 85%. Nulliparous buffalo
heifers, 2–2.5 years of age and weighing 300–400 kg, were
selected for this study. All heifers were fed the same diet as a
TMR twice daily to meet or exceed the dietary requirements
for buffalo heifers (Paul and Patil 2007).
Ultrasonography
Experiment 1
Thirty-six (36) Nili-Ravi buffalo heifers were enrolled in the
study. Teaser bull was paraded daily in heifer sheds to identify
heifers in heat. After identification, the animal was brought to
crate for ultrasonographic examination. During each ultraso-
nographic examination, ovaries were scanned by transrectal
ultrasonography using linear-array transducer with dynamic
frequency range of 5–7.5 MHz (Easy-scan, BCF Technology
Ltd.). All the heifers were scanned daily until occurrence of
ovulation. Interovulatory interval (IOI) was defined as time
period between two successive ovulations. Individual follicu-
lar and luteal structures were recorded and identified using
previous day records. A total of 46 cycles were monitored in
which a subset of 10 heifers was scanned for two consecutive
inter-estrus intervals and follicular wave pattern in each IOI
was recorded.
Experiment 2
Sixteen (16) heifers in estrus were selected and progesterone
(Sigma-Aldrich Chemicals Pvt. Ltd., India) treatment was
started from D0 (day of ovulation) in a decreasing dose up
to D5 of 2nd IOI. Heifers received progesterone in sesame oil
(Sigma-Aldrich Chemicals Pvt. Ltd., India) vehicle (2 mL) by
subcutaneous injection from D0 (day 0 = day of ovulation) to
day 5 (Fig. 1). The daily dose of 150, 150, 100, 75, 50, and 25
mg, respectively, was given. Ovarian ultrasonography was
carried out to record the follicular wave pattern (number of
follicular waves). Control heifers (n = 10) received 2 mL of
sesame oil vehicle through subcutaneous injection using the
same schedule. All the heifers were inseminated with good
quality frozen semen at the end of IOI (2nd estrus) and were
 Author's personal copy
Trop Anim Health Prod

Fig. 1 Diagram of the treatment

protocol and activities in the
study. D0 = day of ovulation; PD
= pregnancy diagnosis, IOI =
interovulatory interval, AI =
artificial insemination

confirmed for pregnancy by ultrasonography at day 45 post-
insemination.
Statistical analysis
All statistical analyses were carried out using IBM SPSS
Statistics 16.0 (SPSS, Chicago, IL). Student’s t test was used
to make comparisons between 2-wave versus 3-wave patterns
and treatment versus control when data were normally distrib-
uted, non-parametric tests were done when data were not nor-
mally distributed. The proportions of animals pregnant were
examined using Chi-square analysis. Data were presented as
mean ± SEM, and differences were considered to be signifi-
cant when P < 0.05.
Results
Follicular wave pattern
Table 1 describes the characteristics of follicular wave patterns
in buffalo heifers during spontaneous estrus. Overall, during
this study, a total of 46 IOIs were monitored, and 2-wave
pattern was recorded in 29 (63.0%) and 3-wave follicular pat-
tern was recorded in 17 (27.0%) IOIs. The dominant follicles
of both wave 1 as well as ovulatory wave attained a smaller (P
< 0.05) maximum diameter in 3-wave as compared to 2-wave
cycle (Fig. 2). However, there was no significant (P > 0.05)
difference in the mean diameters of the CL between different
follicular wave patterns. The mean IOI duration was
significantly shorter in 2-wave compared to 3-wave cycles
(20.5 ± 0.3 vs. 22.3 ± 0.2 days; P < 0.05).
Out of 46 IOIs, 24 were of duration of ≤ 21 days and the
remaining 22 were of duration of ≥ 22 days. Majority of IOIs
of ≤ 21-day duration were of the 2-wave pattern (20 out of 24,
78.9%), whereas only 4 were 3-wave pattern. Out of 22 IOIs
of ≥ 22-day duration, 13 were 3-wave pattern and 9 were 2-
wave pattern (Fig. 3).
Repeatability of wave pattern
The length of IOI was repeatable in buffalo heifers on two
consecutive cycles. Buffalo heifers having either ≤ 21- or ≥
22-day IOI in first cycle tended to have similar length of IOI in
second cycle (8 out of 10, 80% repeatability). The repeatabil-
ity of follicular wave patterns was also analysed. The follicular
wave pattern was considered to be non-alternating if the fol-
licular wave pattern in two consecutive cycles remains the
same. Like the length of IOI, the underlying follicular wave
patterns also tended to be non-alternating. Out of 10 buffalo
heifers, 7 (70%) had non-alternating patterns and 3 (30%) had
alternating (characterized by wave “switching”) follicular
wave patterns (Fig. 4).
Effect of progesterone treatment on follicular wave
pattern and fertility
Sixteen heifers were subjected to progesterone treatment from
D0 (day of ovulation) in a decreasing dose till D5 and 10
heifers were kept as control. Post-treatment, 2-wave pattern
was recorded in only 4 heifers and 12 heifers showed 3-wave

Table 1 Comparison of the characteristics of follicular wave patterns in spontaneous estrus (46) cycles of 36 buffalo heifers

End point 2-Wave cycle 3-Wave cycle P value

Number of heifers 29 17 –
Percentage of cycles 63.0% 37% –
Interovulatory interval (day) 20.5 ± 0.3 22.3 ± 0.2 < 0.05
Maximum diameter of wave 1 dominant follicle (mm) 12.3 ± 0.3 10.2 ± 0.2 < 0.05
Diameter of ovulatory follicle (mm) 13.2 ± 0.3 11.2 ± 0.3 < 0.01
Maximum diameter of CL 14.7 ± 0.5 15.3 ± 0.4 NS

NS not significant
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Trop Anim Health Prod

Fig. 2 Mean ± SEM for

diameters of the dominant follicle
in 2-wave cycles (n = 29) and 3-
wave cycles (n = 17). *Significant
(P < 0.05) difference between 2-
and 3-wave cycles at the
particular day of interovulatory
interval

pattern. Progesterone treatment significantly increased the
proportion of 3-wave cycles as compared to control (P <
0.05) (Table 2).
The mean duration of IOI among progesterone-treated
heifers did not differ (P > 0.05) with control (Table 2). In
the treated heifers, the mean maximum diameter of the DF of
wave 1 was smaller (P < 0.001) compared to untreated con-
trol. There was no significant (P > 0.05) difference in the
mean diameters of the ovulatory follicle as well as CL be-
tween heifers of the two groups. Pregnancy rates of treated
and untreated heifers did not differ (P > 0.05). The pregnan-
cy rate of treated heifers was 43.8% (7 pregnant out of 16),
whereas that of control heifers was 40.0% (4 out of 10
heifers) (Table 2).
Discussion
The temporal characteristics of 2- and 3-wave IOIs have been
examined in both cattle and buffalo, but factors predictive of a
specific pattern have not been identified. The repeatability of
wave pattern in the present study was in agreement with
Jaiswal and co-workers (Jaiswal et al. 2009), who reported
repeatability value (70%) in crossed Hereford (B. taurus) cat-
tle. However, both higher (88%) (Imron et al. 2016) and lower
(~ 55% and 66%) (Price and Carriere 2004; Sichtar et al. 2010;
Ginther and Bashir 2013) values of repeatability have been
reported. It is evident from our results that exposure to exog-
enous progesterone early in the cycle resulted in higher pre-
ponderance of 3-wave cycles (75%) as compared to normal
cycles (~ 30%). Our results as well as previous studies indicate
that the change in the growth of the dominant follicle of wave
1 can alter the follicular wave pattern. Progesterone treatment
during start of IOI is believed to reduce the dominance of
dominant follicle of first wave and hence induce the occur-
rence of a 3-wave pattern. The notion is supported from the
findings that an extended life-span of the dominant follicle
delayed the peak in the circulating concentrations of FSH
and subsequent emergence of wave 2 (Kastelic et al. 1990;
Ko et al. 1991; Adams et al. 1992), whereas a shorter period of
functional dominance hastened the emergence of the next fol-
licular wave (Adams et al. 1992, 1993).

Fig. 3 Frequency distribution of 8

interovulatory intervals in 2-wave 2-wave cycle
7
Number of interovulatory

cycles (n = 29) and 3-wave cycles

(n = 17)
3-wave cycle
6
5
intervals

4
3
2
1
0
18 19 20 21 22 23 24
Duration of interovulation interval (days)
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Fig. 4 Repeatability pattern of 2-

and 3-wave interovulatory first IOI second IOI
intervals (IOIs) in heifers (n = 10) 7
examined during consecutive
IOIs. *Wave switching/

Follicular wave pattern

6
alternating patterns 3 * * 3 *
5
3 2 3
4
2 2 2 2 2
3
3 3 3
2
2 2 2 2 2 2 2
1
0
492 541 568 573 542 537 549 547 557 562

Heifer Identification No.

The suppressive effect of exogenous progesterone on
growth of dominant follicle of wave 1 has been recorded in
heifers (Adams et al. 1992), ewes (Rubianes et al. 1996;
Viñoles et al. 1999), and goats (Menchaca and Rubianes
2002). An early increase in progesterone concentration or ex-
ogenous progesterone administration soon after ovulation has-
tened the follicular turnover, advanced the emergence of wave
2, thereby increasing the number of follicular waves during
IOI in goats (Menchaca and Rubianes 2002). Factors that
reduce dominance of dominant follicle of wave 1 (such as
under-nutrition and heat stress) were also associated with in-
creased proportion of 3-wave cycles (Murphy et al. 1991;
Badinga et al. 1993; Wilson et al. 1998; Mackey et al.
2000). Our results are in contradiction with an earlier study
that showed administration of progesterone during the
metestrous phase of the cycle shortened the cycle and reduced
the occurrence of 3-wave pattern (Burke et al. 1994). This
may be due to greater hypothalamo-pituitary suppression by
CIDR device containing larger amount of progesterone and
the removal of device resulted in accelerated synthesis of
prostaglandin F2α causing premature luteolysis. However,
shortening of the cycle length (or increased occurrence 1 wave
cycle) was not observed by administrating doses used in the
present study (Adams et al. 1992). The decreasing doses of
progesterone used in the present may have starved the grow-
ing follicle of wave 1 from LH but not reduced the LH con-
centration to the level of initiating the luteolytic cascade.
Interestingly, Ginther (1970) prevented the premature
luteolysis by simultaneous injections of human chorionic go-
nadotrophin (hCG) during early metestrous in progesterone-
treated cows.
The model explaining the regulation of 2- and 3-wave pat-
terns has been proposed (Jaiswal 2007). It is believed that the
dominance and hence estrogenic activity of dominant follicle
of wave 1 govern the number of waves during IOI as well as
the onset of luteolysis, which is in turn dependent on the
progesterone concentration during early luteal phase.
According to this model, low progesterone during early IOI
would result in high pulse frequency of LH (Ireland and
Roche 1982), greater dominance and estrogenic activity of

Table 2 Effects of a progesterone treatment started just after ovulation (day 0) on follicular wave characteristics and fertility of subsequent ovulation in
buffalo heifers

End point Heifers P value

Progesterone treated (n = 16) Control (n = 10)

Interovulatory interval (day) 19.6 ± 0.2 20.3 ± 0.4 > 0.05

Maximum diameter of wave-1 dominant follicle (mm) 8.3 ± 0.1 12.5 ± 0.2 < 0.001
Diameter of ovulatory follicle (mm) 12.3 ± 0.2 14.2 ± 0.3 > 0.05
Maximum diameter of CL 14.6 ± 0.2 15.8 ± 0.4 NS
Pregnancy rate (%)a 43.8% 40.0% > 0.05
Number of cycles with 3-wave pattern (%)a 12 (75%) 3 (30%) < 0.05
a
Chi-square test
 Author's personal copy
the dominant follicle of wave 1 (Adams et al. 1992), and early
induction of cascade for luteolysis (Villa-Godoy et al. 1985).
Another hypothesis that intraovarian location of corpus
luteum and dominant follicle affects the length of cycles and
follicular wave pattern has been extensively studied in cattle
(Ginther et al. 2013a, b, c, d, 2014a, 2015; Ginther and Bashir
2013). Local effect of estradiol from the dominant follicle and
the systemic effect of FSH might affect follicle wave pattern
but has not been experimentally tested (Ginther et al. 2013a, b,
c, 2014b). Since estradiol has an anti-luteotrophic effect dur-
ing the initial days of an IOI (Lemon 1975) and luteolytic
effects during diestrus (Araujo et al. 2009), the dominant fol-
licle may be selectively benefited with the higher pulse fre-
quency of LH and acquires a luteolytic role. Contrarily, higher
progesterone especially the early rise in circulating concentra-
tion of progesterone in 3-wave cycles is believed to lower
pulse frequency of LH. As a result, the dominant follicle of
the first wave does not acquire longer dominance, secrete less
estrogen, luteolytic mechanism is delayed and 3-wave pattern
is induced. Therefore, the model hypothesises a proverbial
“tug of war” like situation at the beginning of the cycle
governing the number of follicular waves. The role of proges-
terone in regulation of wave-pattern is evident from presence
of higher mean circulatory progesterone during the luteal
phase in 3-wave (1.99 ± 0.53 ng/ml) as compared to 2-wave
(2.77 ± 1.01 ng/ml) cycles (Baruselli et al. 1997). Contrary to
the hypothesis, we found no difference in maximum diameters
of CL as well as mean duration of IOI between treated and
control heifers, suggesting that although progesterone pre-
vents dominance of DF of wave 1, the luteolytic signal occurs
at the normal time. This demonstrates that the factors ultimate-
ly responsible for controlling cycle duration act independently
of progesterone control. Thus, our hypothesis and model pro-
posed were partially supported.
Pregnancy rates in cattle with 2-wave versus 3-wave pat-
terns were compared (Ahmad et al. 1997; Townson et al.
2002; Bleach et al. 2004; Celik et al. 2005) based on the
notion that the competence of the oocyte to become fertilized
and develop into an embryo is associated with the develop-
mental status of the follicle that contains it (Vassena et al.
2003). In 2- versus 3-wave IOI, the ovulatory follicle grows
for a longer period (9 vs. 6 days; Jaiswal et al. 2009) and
attains a greater diameter (16 vs. 14 mm in cattle; Ginther
et al. 1989a and 15.5 vs. 13.4 cm in buffalo; Baruselli et al.
1997). The oocyte that is released at ovulation is 3 days older
relative to the day of wave emergence in 2-wave versus 3-
wave IOI. Hence, 2-wave IOI ovulate aged oocytes that are
less fertile than their 3-wave counterparts (Townson et al.
2002). In a study involving 106 cows (68% 2-wave and
30% 3-wave), pregnancy rate of 2-wave cows was less than
that of 3-wave cows (63% vs. 81%, respectively; P = 0.058)
(Townson et al. 2002). In the present study, progesterone ex-
posure during the early IOI transformed erstwhile majority of
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2-wave into 3-wave patterns; however, the conception rate
was comparable to untreated heifers. Our findings were in
agreement with Ahmad and collaborators (Ahmad et al.
1997), who observed no difference in fertility after insemina-
tion following 2-waves (36 of 44, 82%) or 3-waves (6 of 6,
100%) of follicular development. This may be due to consid-
erably smaller sample size in our studies. Previously, an in-
creased duration of ovulatory follicle development from the
time of emergence (or dominance) to estrus (as observed in 2-
wave pattern) was associated with reduced pregnancy rates
following AI in dairy cows undergoing spontaneous estrous
cycles (Bleach et al. 2004). Interestingly, a higher predomi-
nance of cycles with 2-waves (72.2%) in repeat breeding
cattlewas observed as compared to 3-wave (16.6%) cycles
(Perez-Marin et al. 2003).
In conclusion, the findings support the hypothesis that pro-
gesterone exposure at the beginning of first follicular wave is
associated with increased preponderance of 3-wave cycles in
buffalo heifers. In addition, the effect of progesterone expo-
sure early in the cycle on fertility of subsequent ovulation
needs to be tested on a larger population.
Acknowledgements Our thanks to Director, ICAR-Central Institute for
Research on Buffaloes for providing necessary facilities.
Authors’ contributions M. H. Jan conducted the experiment and prepared
the manuscript, S. Kumar and A. Gupta assisted in animal experimenta-
tion, K. L. Mehrara provided assistance in animal handling and ultraso-
nography, R. K. Sharma and H. Kumar conceived and supervised the
work.
Funding information This study was funded by ICAR-Central Institute
for Research on Buffaloes, Hisar (Haryana), India.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
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