Arch. Tierz., Dummerstorf 44 (2001) Special Issue, 203-212
Department of Sheep and Goal Breeding, University of Agriculture, 30-059 Krakow, Poland
DOROTA ANNA ZIEBA, MACIEJ MURAWSKI and EDWARD WIERZCHOS
Pattern of follicular development during the oestrous cycle of
prolific Olkuska sheep
Summary
Folliculogenesis was studied daily in 18 oestrous cycles in 6 prolific Olkuska ewes using transrectal ultrasonography
to record the number and size of all follicles > 2 mm in diameter. Blood samples were taken once a day and were
analysed for concentrations of FSH, LH and oestradiol. Follicular and hormonal data were analysed for associations
between different stages of the lifespan of the largest follicles of follicular waves, and detected fluctuations in serum
concentrations of FSH and oestradiol. Waves 1, 2, 3 and 4 emerged respectively on days: -1 to 3,4 to 8, 7 to 11 and
12 to 15. The mean number of follicles that reached > 4 mm diameter was 3.93 ± 1.1 follicles per wave, and 18.68 ±
1.9 follicles per oestrous cycle and a total number of 299 follicles observed. Mean length of the interwave interval
was 4.4 ± 1.6 days. The length of the interval between emergence of waves (4.4 ± 1.6 days) did not differ
significantiy from the interval between peak values for FSH fluctuations (4.8 + 1.3 days). We conclude that: 1) in
sheep the ovarian follicles emerge and grow throughout the oestrous cycle in the wave-like pattem; 2) thcre is a
close relationship between transient increases in FSH and oestradiol concentration and emergence of follicular
waves and 3) the preovulatory follicles are derived from the large follicles population present on the ovary at the
time of luteal regression.
Key Words: follicle, follicular wave, gonadotropins, prolific sheep
Zusammenfassung
Titel der Arbeit: Follikelentwicklung während des Brunstzyklus bei Olkuska Schafen
Bei sechs Olkuska-Mutterschafen wurde während 18 Brunstzyklen die Follikelentwicklung untersucht. Dazu wurde
mittels transrektaler Sonografie täglich die Anzahl und Größe aller Follikel > 2 mm erfaßt. Parallel erfolgte die
Analyse von FSH, LH und Östradiol. Insgesamt vier Follikelwellen traten an den Tagen -1 bis 3, 4 bis 8, 7 bis 11
und 12 bis 15 auf. Im Mittel konnten je Welle 3,93±1,1 Follikel mit einem Durchmesser von > 4 mm, je
Brunstzyklus 18,68±1,9 Follikel und insgesamt 299 Follikel beobachtet werden. Das mittlere Intervall zwischen
zwei Wellen betrug 4,4±1,6 Tage. Die Länge dieses Intervalls unterschied sich nicht signifikant vom Intervall
zwischen den FSH-Peaks (4,8±1,3 Tage). Daraus läßt sich ableiten, dass Ovarfollikel bei Schafen während des
Zyklus wellenartig auftreten und wachsen, es eine enge Beziehung zwischen dem kurzzeitigem Anstieg von FSH
und östradiol und dem Auftreten von Follikelwellen gibt und die präovulatorischen Follikel aus der Population
großer Follikel zum Zeitpunkt der Gelbkörperrückbildung stammen.
Schlüsselwörter: Follikel, Follikelwelle, Gonadotropine, besonders fruchtbare Schafe
Introduction
Initiation of follicular growth appears to be a continuous process, beginning immediately
after the first follicles are formed and continuing until the end of the reproduetive period
(PIERSON and GINTHER, 1984). In domestic ruminants, continuous renewing of
terminally growing follicles oecurs during the oestrous cycle aecording to a "wave"
pattern. The waves were defined from ultrasonographic studies in cows (GINTHER et al.,
1989) and consist of the contemporaneous appearance, about every 5-7 days, of a group
of follicles larger than 5 mm in diameter (PIERSON and GINTHER, 1984). The coneept
204
of a wave was generalized and aeeepted to various species, particularly polytocous
species, in which more than one follicle was observed (SMEATON and ROBERTSON,
1971).
Transrectal ovarian ultrasonography has only recently been adapted for the use in small
ruminants e.g. sheep (BARTLEWSKI and BAIRD, 1995; GINTHER et al., 1995;
RAVINDRA et al., 1993; SCHRICK et al., 1993; SOUZA et al., 1997) and goats
(GINTHER and KOT, 1994; SCHWARZ and WIERZCHOS, 2000) in which waves of
follicular growth oeeur during both the luteal and follicular phases of the cycle. One
study reported that two "phases" of growth of follicles > 2 mm in diameter were noticed
during the oestrous cycle (BRAND and De JONG, 1973). SMEATON and
ROBERTSON (1971) demonstrated that a large amount of oestradiol was released when
high FSH concentration was observed during the luteal phase of the ovine oestrous cycle.
They suggested that this was related to the dynamics of ovarian follicular growth in a
wave-like pattern and FSH is one of the major factors which stimulates follicular growth
and maturation (SMEATON and ROBERTSON, 1971). Day-to-day aecounts of ovarian
follicular changes have been reported for individual ewes throughout the oestrous cycle
so far (RAVINDRA et al., 1994) but the pattern of follicular development remains still to
be clarified.
The objeetives of the present study were to use transrectal ovarian ultrasonography as a
non-invasive technique in order to monitor day-to-day ovarian follicular events
throughout the oestrous cycle in high prolific Olkuska sheep and to evaluate the temporal
associations between the peripheral concentrations of gonadotropins and ovarian Steroids
and emergence of ovarian follicles.
Materials and Methods
2.1.
Animals and experimental procedure
Olkuska sheep are a native breed of Polish long-wool sheep which originated in the
Olkusz region in the South of Poland. This breed of sheep is characterized by high
fecundity, producing from 2 to 4 and sometimes 6 lambs per lambing (MURAWSKI et
al., 1994). There is evidence to suggest that Olkuska ewes, like the high fecundity
Booroola Merino (BINDON and PIPER, 1986) contain a major gene which influences
their Ovulation rate (MARTYNIUK and RADOMSKA, 1990).
The experiments were carried out in the middie of the reproduetive season (Octoberlanuary 1999/2000) using 6 mature high fecundity Olkuska sheep, aged 2-4 and weighing
45 to 50 kg. Sheep belonging to the University Research Farm in the Bielany area of
Krakow were maintained on pasture for the first month and from November on were kept
in barns.
The ovaries were examined by transrectal ultrasonographic imaging to monitor the
follicles and to establish the day of Ovulation which was detected by the collapse of large
follicles. The Scanner was a real-time, B-mode instrument with a 7.5 MHz linear-array
transducer (Aloka SSD 550 Micrus, Equine Therapy System, Inc., Greenwood Village,
CO, USA). Ultrasound scanning was carried out daily commenced for each ewe when it
was in oestrus; ultrasonography continued for 70 consecutive days between 08:00 and
11:00 h AM. All ovarian follicles > 2 mm in diameter were counted and their size and
Position sketched on ovarian charts. Similarly, the size and position of CL were also
mapped. Desired images were frozen on the screen, measurements were taken using the
205
built-in calliper-system, and a hard copy was made using a video processing unit
(Mitsubishi Electronics Co, Ltd., Tokyo, Japan).
2.2
Hormone analysis
Serum samples were analysed by radioimmunoassay for concentrations of FSH, LH and
oestradiol.
Complete RIA kits for the measurements of LH and FSH were obtained from Dr. A. F.
Parlow (National Hormone and Pituitary Program, Torrance, CA, USA). Radioiodination
procedure was performed according BRYANT and GREENWOOD (1968). Follicle
stimulating hormone was measured according the procedure given by WILLIAMS et al.
(1983). Standard curves ranged from 0.049 to 25 ng/ml. Sensitivity of the assay was 0.1
ng ml"1. Intra- and interassay coefficients of Variation (CV) were 6.7 and 13.4%
respectively. The relationship between real (x) and determined (y) amount of three
different concentrations of FSH added to the plasma samples is expressed by the linear
regression equation (y=1.12x+0.19).
Luteinizing hormone was estimated as described by ZIE.CIK et al. (1979) Standard
curves ranged from 0.078 to 10 ng/ml and sensitivity of the assay was 0.1 ng ml'1. Intraand interassay CV were 9.3 and 16.2% respectively. The precision of method for
measurement of 2,6 and 15 ng/ml (n=8) is illustrated by linear regression equation
(y=1.07x+0.28).
Oestradiol were determined radioimmunologically using Spectria kits (Orion,
Diagnostica, Finland) supplied by Polatom (Swierk, Poland). For oestradiol the limit of
assay sensitivity was 5 pg/ml. The coefficients of Variation within and between assays
were 10.28% and 2.9%, respectively. The mean recoveries were 85.6 - 108.9 %. The
cross-reaction with ethinylestradiol was 1.4 %. All other tested Steroids (oestrone,
oestriol, progesterone, testosterone, corticosterone) showed less then 1% cross-reaction.
2.3.
Follicular data and Statistical analysis
Day of emergence of a follicle was the day that the follicle was > 2 mm in diameter, with
an increase to > 3 mm the following day. The term wave was used to signify growth of a
group of follicles > 3 mm in diameter, and more than one consecutive day was allowed
for all follicles of a wave to emerge. When follicles reached > 4 mm on a consecutive
days, the day of a wave emergence was assigned to the day of emergence of the largest
follicle. The first wave at the beginning of the oestrous cycle was defined as a Wave 1,
and the following waves were numbered sequentially.
Follicular data (follicle > 2 mm in diameter) were combined for both ovaries of each ewe.
Consideration of data indicated that follicles that reached maximum diameter early in the
follicular wave sometimes emerged the day or even two days before Ovulation that the
wave began. Therefore, follicles were assigned to the wave in which they reached the
maximum diameter, and the analyses of follicle data began on Day -2 or -1 rather Day 0
(day of Ovulation).
Follicular and hormonal data were analysed for associations between various stages of
follicular wave development (follicle growing from 3 to > 4 mm) and peaks in serum
concentrations of FSH, LH and oestradiol. Analyses of variance were used to compare
means among the 4 waves. The association between emergence of follicular waves and
occurrence of identified FSH peaks was studied by t-test to compare the number of waves
206
with the number of peaks per the oestrous cycle and the length of intervals between
waves and between FSH peaks.
Analyses of variance for sequential data were used to evaluate the day effect averaged
over the 18 cycles. End point was the number of 2 mm follicles each day which later
reached > 3 or/and > 4 mm. A significant day effect for end point was followed by a
paired Student's t-test to detect nadirs and peaks. Those data were used to partitioning the
cycles into periods when the waves emerged. The same analyses were made for
circulating concentrations of FSH, LH and oestradiol. Spearman correlation was made
between the day effect of FSH concentration and the number of follicles emerging each
day. Analyses of variance were used to estimate the differences in mean maximum
diameter between the largest follicles from each wave.
Results
Before the study began we selected those ewes for experiments which showed a high rate
of ovulations, a mean of 3.75 corpora lutea. A total of 18 oestrous cycles and 72 follicular
waves was obtained from 6 ewes in the study. The mean length of the oestrous cycle was
16.75 ± 0.7 days. Follicles that reached maximum diameter > 3 mm (a total number of
304) emerged during the whole oestrous cycle. There were a different number of
follicular waves among observed cycles. The mean number of waves per cycle was 4. No
waves emerged on Day 16 and only one wave emerged on Day 10. Significantiy more
follicles emerged on days 2, 8 and 13 of the cycle (P<0.005). Mean length of the
interwave interval was 4.4 ± 1.6 days.
The characteristics of follicular waves are given in the Table. The mean number of
follicles that reached > 4 mm diameter was 3.93 ±1.1 follicles per wave, and 18.68 ± 1.9
follicles per cycle and a total number of 299 follicles observed.
Table
Characteristics of ovarian follicular waves (follicles growing from 3 to S 5 mm in diameter; mean ± SEM) identified
in four Olkuska ewes that underwent daily ultrasonography for 70 consecutive days of the breeding season
(Charakteristika von Ovarfollikelwellen fvon 3 bis S 5 mm Durchmesser wachsende Follikel])
Trait
Mean day of wave emergence
Range
No. of folliclesAvave
Maximum diameter (mm)
Interwave interval* (days)
Wave 1
Wave 2
Wave 3
Wave 4
0.4 ±0.1
-1-3
2.8+ 1.2
0.52 ±0.1
3.7 ±0.1
6.0 ±0.3
4-8
4.4+1.6
0.49 ±0.1
4.3 ±0.9
10.3 ±0.4
7-11
4.0 + 0.9
0.5 ±0.1
4.2 ±0.1
13.7 ± 1.1
12-15
4.7 ± 1.7
0.51 ±0.1
5.3 ±0.2
'Interwave inlerval refers to the number of days between emergence of the wave in that column and emergence of the next sequential wave
The analysis of daily serum FSH concentration showed basal levels around 0.44 ±0.1 ng
ml'1, (Fig. 1) Mean serum concentration on day 16 (1.81 ± 0.2 ng ml"1) was significantiy
higher than on the rest of the days. The associations between the follicular waves and
identified FSH peaks are shown for the 8 oestrous cycles. The length of the interval
between emergence of waves (4.4 ± 1.7 days) did not differ significantiy from the
interval between peaks values for FSH fluctuations (4.8 ± 1.3 days). The day effect of
FSH concentration and the number of follicles emerging each day was negatively
correlated (r= -0,46).
The analysis of daily serum LH concentration showed basal levels around 0.11 ± 0.05 ng
207
ml" , (Fig. 2) Mean serum concentration on day 17 (6.27 ± 0.4 ng ml'1) was significantiy
higher than on the rest of the days.
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6
7
8
9
10
11
12
13
14
15
16
17
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number of days from Ovulation
Fig. 1: Serum concentration of FSH (mean ± SEM) in jugular vein from daily blood samples throughout the oestrous
cycle of ewes (FSH-Konzentration im Blutserum wahrend des Brunstzyklus von Mutterschafen)
The stars indicate significant differences between days.
Mean serum estradiol concentrations showed a gradual increase from a low on day 14
(4.47 ± 1.3 pg ml"1) to reach a peak of 13.14 ± 3.8 pg ml"1 on the day before Ovulation
(Fig. 3). Serum concentration of oestradiol was quite variable during the remainder of the
oestrous cycle.
Discussion
Ultrasonography as commonly used in cattle, with some modifications, can be
successfully used in sheep for the study of the ovarian follicular dynamics. Studies using
endoscopy and ovarian ultrasound imaging have revealed that the growth of follicles to >
5 mm in diameter occurs in an orderly fashion, at approximately 5 day intervals,
throughout the oestrous cycle in ewes (GINTHER et al., 1995). However, studies
summarized by LOPEZ-SEBASTIAN et al. (1997), including that of SCHRICK et al.
(1993), did not find the waves of follicles growth.
Present studies strongly confirmed that the development of ovarian follicles in ewes
occurs in a wave pattern. Our data showed antral follicles emerging or growing from a
pool of follicles > 2 mm in diameter on most days of the cycle except day 16 and only
one follicular wave emerged on day 10. However, significantiy more follicles emerged
208
2
3
4
5
6
7
8
9
10
It
12
13
14
15
16
17
1
number of days from Ovulation
Fig. 2: Serum concentration of LH (mean ± SEM) in jugular vein from daily blood samples throughout the oestrus
cycle of ewes (LH-Konzentration im Blutserum während des Brunstzylkus von Mutterschafen)
on days 2, 8 and 13 of the cycle. In the study by GINTHER et al. (1995) on cyclic
Polypay ewes, sequential follicular waves emerged, on average, on days 0, 5, 9 and 14 of
the cycle and in the study by BARTLEWSKI et al. (1999), the mean day of wave
emergence were days 0, 5, 9 and 12 for Western white-faced and days 1, 6, 10 and 13 for
Finn sheep. There are breed differences, which is difficult to explain, but it is possible
that in prolific sheep follicles achieve smaller maximum sizes and all phases of follicular
development may occur with smaller follicles than they do in non-prolific breeds of
sheep. Previous studies concerning follicular dynamics in prolific and non-prolific breeds
of sheep indicated that follicles attained maturity at a smaller diameter in prolific animals
(DRIANCOURT et al., 1986; SCARAMUZZI and RADFORD, 1983, SOUZA et al.,
1997).
GINTHER et al. (1995) reported that the 8% of interovulatory intervals had three waves,
58% had four waves and 34% had five or six. In the study herein, there appeared to be
four major phases of growth of large antral follicles at about 4.4 ± 1.6 days intervals,
throughout the oestrous cycle, which is typical for ewes with the normal oestrous cycle.
However, on the basis of results of RAVINDRA (1993) and NOEL et al. (1993), three
waves may be the consistent pattern in some breeds, however; that mostly occurred
towards the end of the breeding season.
The total number of follicles > 3 mm in diameter reported in the study by BRAND and
DE JONG on Texel ewes (1973), and in the other studies (DRIANCOURT et al., 1988,
SCHRICK et al., 1993) seemed lower than observed in the present study. This may
reflect breed differences and the stage of the breeding season at which the studies were
undertaken.The ovulatory follicles emerged generally on day 13 and grew over a period
of 3 days at a rate of 1.0 mm per day. This was at the time when serum progesterone
concentrations started to decline. The growth rate of the ovulatory follicle in our study
was similar to that observed by DRIANCOURT et al. (1986) in the study on Booroola
Merino. GEBAROWSKA et al. (1996) showed that in Olkuska ewes like in Booroola
209
Merino the recruitment of ovulatory follicles lasts longer between 13 and 15 days of the
oestrous cycle and even additional follicles from the pool of selected follicles reach the
size of an ovulatory follicle by the time of LH surge and the Ovulation rate rises.
numtwr of diyi from ovulition
Fig. 3: Serum concentration of oestradiol (Mean ± SEM) in jugular vein from daily blood samples throughout the
oestrous cycle of ewes (Österadiol-Konzentration im Blutserum während des Brunstzyklus von Mutterschafen)
Several studies have examined the oestradiol concentrations and ovarian follicular
development (COX et al., 1971, RAVINDRA et al., 1994). A peak of oestradiol on the
day before Ovulation was noted in our study as has been noted by COX et al. (1971) and
RAVINDRA et al. (1994). Additional peaks of oestradiol on days 3 and 4 in the present
study and in the study by COX et al. (1971) and two more on days 9-10 and 12-13 of the
cycle have been shown, suggesting phases of follicular development at these times during
the oestrous cycle and supporting the data on follicles that showed emergence and growth
in a wave-like pattern of development. It is possible that large antral follicles are
maintained in prolific Olkuska ewes towards the end of the cycle and, added to the
ovulatory follicles emerging just before Ovulation, give as a result higher Ovulation rate
than in non-prolific genotype.
The importance of FSH in ovarian folliculogenesis in ewes has already been
demonstrated (BAIRD et al., 1990). The data from the present study confirm the
existence of a close temporal relationship between transient increases in circulating
concentrations of FSH and follicular growth. The increase in FSH concentration was
followed by the recruitment of follicles of the next wave as it was indicated by a negative
correlation between the day effect of FSH concentration and the number of follicles
emerging each day. The results confirm that rhythmically generated increases in serum
FSH concentrations may induce the growth of large follicles, but that follicular demise is
independent of the periodicity of FSH secretion. However, smaller follicles seem to
require more circulating FSH than larger ones, and thus may be fundamental to the
initiation of deviation. Moreover, the intrafollicular factors have may autocrine/paracrine
roles, including enhancing FSH action, inducing expression of LH receptors, and regulate
210
aromatase activity.
In summary, the growth of ovarian follicles during the oestrous cycle in high fecundity
Olkuska sheep exhibits a distinct wave-like pattern. Ovarian follicles emerged form the
pool of 2 mm follicles and the initial stages of the growth of the largest follicles appear to
be controUed primarily by increases in FSH secretion. The higher Ovulation rate in the
prolific Olkuska ewes appears to be the result of prolonged time of follicles recruitment
which was suggested for Booroola Merino (DRIANCOURT et al., 1991, KNOTHE and
WIERZCHOS, 1992; SCARAMUZZI et al., 1993) and confirmed by GEBAROWSKA
et al. (1996) in study on Olkuska sheep.
SOUZA et al. (1997) using ultrasonography showed that ovarian follicular dynamics did
not differ between sheep with or without the Booroola gene. That was confirmed by
BARTLEWSKI et al. (1999) in the study on two breeds of sheep with different Ovulation
rates, and obtained data strongly support the conclusion that the development of ovarian
follicles reaching an ovulatory size occurs in an orderly succession during the oestrous
cycle in ewes and that this phenomenon is apparently not influenced by differences in
prolificacy.
In the further work much more emphasis should be place on the intra-ovarian factors
associated with prolificacy, its role in deviation or in subsequent growth of the largest
follicles.
Conclusion
We conclude that: 1) in sheep the ovarian follicles emerge and grow throughout the
oestrous cycle in the wave-like pattern; 2) there is a close relationship between transient
increases in FSH and oestradiol concentrations during the cycle and emergence of
follicular waves and 3) the preovulatory follicles are derived from the large follicles
population present on the ovary at the time of luteal regression.
Acknowledgements
The authors would like to thank Prof. Jan Kotwica (Institute of Animal Reproduction and
Food Research, Polish Academy of Sciences, 10-718 Olsztyn-Kortowo, Poland) for
generous help with the FSH and LH RIA.
This study was supported by a grant 5 P06D 017 14 from the Polish State Committee for
Scientific Research.
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Authors' address
Dr. DOROTA A. ZIEBA, Dr. MACIEJ MURAWSKI, Prof. Dr. habil. EDWARD WIERZCHOS
University of Agriculture
Department of Sheep and Goat Breeding
30-059 KRAKOW, AL. MICKIEWICZA 24/28,
POLAND
Phone: (48) 12 66 24 086, Fax: (48) 12 33 33 07
E-mail: [email protected]