Histomorphic changes in the ovary during the estrous cycle of a wild rat, Bandicota bengalensis

ABH~RAM S A H U ' Histophysiology Laboraton, Department qf Zoolog!. I/nlver.slh qf' Ctrlcutta, 35 B .C. Road, Calcutttr 7000 19, India

Received August 3. 1983

SAHU, A. 1984. Histomorphic changes in the ovary during the estrous cycle of a wild rat, Bandicota bengalensis. Can. J . Zool. 62: 1052- 1058.

Histomorphic changes in the ovary of Bandicota bengalensis were studied during various stages of the estrous cycle. The ovarian follicles were classified into nine size groups and their frequency distribution was determined for the different phases. In all the ovaries 70% of the follicles were nonantral and below 201 pm in diameter. During proestrus and estrus the ovary possessed the highest number of nonatretic follicles. The follicles ranging above 600 pm were absent at metestrus and diestrus. Preovulatory follicles (>700 pm) were present only during estrus. indicating ovulation during the night of the day of estrus. Excepting the 30- to 50-pm follicles. all other follicles were susceptible to atresia in the cycling rats. Maximum atresia was noticed in the 201- to 500-pm follicles. The number of atretic follicles was hishest at diestrus and lowest at estrus. In the continuous diestrous rats, about 50% of the atretic follicles were in the range of 30- 100 pm. Three recognizable types of corpora lutea were found in the ovary. The volume of the first and second type corpora lutea was highest at proestrus and estrus, respectively. Mean number of first and second type corpora lutea was 3.87 and 4.56. respectively. and thus about four ova ovulated per ovary during each estrous cycle in this wild rat.

SAHU, A. 1984. Histomorphic changes in the ovary during the estrous cycle of a wild rat. Bandicota bengalensis. Can. J . Zool. 62: 1052- 1058.

Les changements histomorphiques de I'ovaire ont kt6 etudies chez Bandicot~r heng~r1en.si.s a divers moments de son cycle. Les follicules ovariens peuvent se classifier en neuf groupes selon leur taille: la distribution de frequences de ces groupes a Ctk determinee au cours des diffirentes phases du cycle. Dans tous les ovaires, 70% des follicules n'ont pas d'antrum et mesurent moins de 201 pm de diamktre. Durant les phases preoestrus et oestrus, I'ovaire contient un nombre plus grand de follicules non atrksiques. Les follicules de plus de 600 pm sont absents durant le mktoestrus et le dioestrus. II y a des follicules prC-ovulaires (>700 pm) seulement durant I'oestrus, ce qui indique que I'ovulation se produit durant la nuit du jour de I'oestrus. Tous les follicules. sauf les follicules de 30-50 pm, sont susceptibles d'atresie chez les rats durant le cycle. C'est dans les follicules de 201 -500 pm que I'atresie est le plus evidente. Le nombre de follicules atresiques atteint son maximum au cours du dioestrus et son minimum durant I'oestrus. Chez les rats qui sont continuellement en phase de dioestrus, cinquante pourcent des follicules atrksiques sont dans le groupe 30- 100 pm. Trois types de corps jaunes se reconnaissent dans I'ovaire. Le volume des corps jaunes du premier type est maximum au cours du prCoestrus et celui des corps jaunes du second type est maximum au cours de I'oestrus. Les nombres moyens respectifs de corps jaunes du premier et du second type sont 3,87 et 4.56; ces rats produisent donc quatre ovules par ovaire durant chaque cycle de I'oestrus.

[Traduit par le journal]

Introduction The changes occurring in the number of ovarian follicles

during the estrous cycle have been well studied in laboratory rodents (see Harrison and Weir 1977; Hirshfield and Midgley 1978; Hirshfield 1983) and it has been reported that the total number of small and medium-sized follicles does not vary throughout the estrous cycle, but the number and size of largest follicles fluctuate greatly. Most of the follicles do not mature completely but become atretic (Ingram 1962; Guraya 1973; Byskov 1974; Harrison and Weir 1977; Weir and Rowlands 1977), depending on the size of the follicles and stages of the estrous cycle (Mandl and Zuckerman 19526; Hirshfield and Midgley 1978; Hirshfield 1983; Faddy et al. 1983). The atresia of the follicles is closely related with the formation of inter- stitial gland cells (Guraya 1973). The rate of ovulation is spe- cies specific but it may vary in different strains of the same species (Bradford 1969; Land and Falconer 1969; Land et al. 1974). Ovulation is followed by the formation of corpora lutea, the growth and development of which have been studied well in the rat (Boling 1942; Deane 1952) and in many other mam- mals (see Harrison and Weir 1977).

Although there are several reports on the follicular kinetics, growth rate and atresia, and corpus luteum formation in the

'Address for correspondence: Dr. Abhiram Sahu, c/o Dr. E. R. Smith, Department of Obstetrics and Gynecology. The University of Texas Medical Branch, Galveston, TX, U.S. A. 77550.

laboratory rodent, there is little information about the ovary of wild rodents (Mossman and Duke 1973; Jones 1978; Eriksson 1983). Thus the present study was undertaken to evaluate quantitatively the follicular kinetics, atresia, and other histo- morphic changes in the ovary during estrous cycle of a wild rat, Bandicota bengalensis, a common rodent pest in India. This study may be useful for comparative studies of the mammalian ovary, especially between the wild and laboratory rodents.

Materials and methods

Adult female bandicoot rats, Bandicota hengalensis (Gray), were trapped from grain storage warehouses in Calcutta through March and April. They were caged individually to prevent them from fighting, which often results in death (Ghosh and Maiti 1974). Animals were provided with food (rice, wheat, chick-peas, rat pellets) and water ad libitum. After 7 days of acclimatization in the laboratory (25"C, lights on from 0600 to 1800). rats were studied for several cycles by the vaginal smear technique (Zarrow et al. 1964; Sahu and Maiti 1978). Individuals showing fairly regular 5-day cycles were selected for study. Four groups of rats ( 10 rats per group) were used for different stages (proestrus, estrus. metestrus, diestrus) of the estrous cycle. Another group of five rats exhibiting diestrous vaginal smears for more than I month was also included as continuous diestrous (CD) group.

Rats were killed at 1200 by cervical dislocation. The ovaries, oviduct-uterus and cervix-vagina were removed quickly, trimmed of extraneous tissues, and weighed on torsion balance to the nearest 0 . I mg. The left ovary of each rat was prepared for light microscopy

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SAHU 1053

TABLE 1 . Weight changes of the gonad and accessory tissues during the estrous cycle of the bandicoot rat

Ovary Oviduct -uterus Cervix - vagina

Relative Relative Relative Absolute (mg/100 g Absolute (mg/ I00 g Absolute (mg/100 g

Stage (mg) body weight) (mg) body weight) (mg) body weight)

Proestrus ( 10) Estrus ( 10) Metestrus ( 1 0 ) Diestrus ( 10)

p value vs. estrus

Continuous diestrus (5)

p value vs. estrus

p value vs. diestrus

NOTE: Values are given as the means 5 SE: those in parentheses indicate the number

by standard procedures. The ovaries were sectioned serially at 5 pm and stained with Masson's trichrome. Diameter of all the nonatretic follicles was measured with a calibrated ocular micrometer from the serial sections of the ovary at a magnification of 100x. The mean diameter was the mean of two perpendicular diameters measured in the section containing the largest cross section of the oocyte. Follicles were classified according to their diameters into nine arbitrary types (Lane and Davis 1939): 30-50, 51 - 100, 101 -200, 201 -300 pm, and so on up to 700 pm and greater. Diameters of the atretic follicles were measured using the mean of maximum diameter and a diameter at right angles to i t . Atretic follicles were characterized by loss of nucleus or pycnosis, change of shape or swelling of the oocyte accom- panied by pycnosis . karyorhexis. shrinkage, luteinizat ion. or local thinning of the membrana granulosa. Only atretic follicles with oocytes still surrounded by cumulus cells or their remnants were included in the measurements.

Corpora lutea (CL) were divided into three types: (i) those formed during the current cycle, (ii) those that were one cycle older, (iii) those that were two or more cycles older. CL were counted and the volumes were determined according to the method of Rowlands (1956). In the CD rats only the third type of CL were present and they were very small and greatly degenerated; thus their numbers and volume were not determined.

Statistical analyses were done using Student's t-test (Fisher 1963). Level of significance was compared for a particular type of follicle in relation to the lowest and highest mean values obtained during differ- ent stages unless otherwise indicated. Mean values of CD rats were compared with those of estrous and diestrous rats.

Results Gmvimetr~l

Ovarian weight increased to the highest level at estrus and decreased significantly at diestrus, being lowest in the CD rats. Weight of the genital tract (oviduct-uterus, cervix-vagina) was significantly decreased at diestrus compared with estrus and it was further lowered in the CD rats (Table 1 ).

Nonatretic .follicles Histology The follicles smaller than 30 p.m were surrounded by a layer

of undifferentiated spindle-shaped cells. The follicles ranging from 30 to 50 p.m contained a single layer of granulosa cells around the oocyte and the number of granulosa layers was increased along with the follicular development (Fig. I ). An antrum was first observed mainly in follicles of 401 -500 p.m

of rats used. NS. not sisnificant

in diameter (Fig. 2) but rarely in 301- to 400-p.m follicles. As the follicles enlarged further, the granulosa layers became thin with distinct cumulus oophoros accompanied by a large antrum. In the preovulatory follicles few invaginations were noticeable in the periphery of the granulosa (Figs. 3 and 4).

Follicul~lr kinetics The follicles with a diameter <30 p.m were not counted.

In the bandicoot ovary the largest number of follicles (about 70%) were in the range of 51 -200 p.m in diameter and the number was sharply diminished as the follicles increased beyond 200 p.m (Table 2). The total number of nonatretic follicles was highest at proestrus and lowest at metestrus. Large Graafian follicles (>600 p.m) were absent during metestrus and diestrus while the follicles >700 p.m were only present at estrus. In the CD rats follicles >500 p.m in diameter were absent and the number of 5 1- to 200-p.m follicles was signifi- cantly lower than that of proestrus.

Thecal tissue was differentiated into theca interna and externa in the antral follicles (Fig. 2). In every follicle ob- served, the theca interna occupied the greater part of the thecal tissue.

Atretic .follic.les Histology In the atretic follicles, granulosa cells degenerated, be-

coming pycnotic and smaller in size (Fig. 5). In the aged atretic follicles, oocytes were divided and fragmented (Fig. 6) and the granulosa layer became thinner. Luteinization of the granulosa layers of atretic follicles with the ovum still inside (Figs. 7 and 8) was rare in the bandicoot ovary.

Follicular kinetics The great preponderence of atretic follicles fell into the 201-

to 500-p.m category. The follicles ranging from 30 to 50 p.m showed no atresia during the estrous cycle, but they shared 40% of the atretic follicles in CD rats and were mainly charac- terized by the pycnotic oocyte. In the cycling rats the follicles ranging from 5 1 to 200 p.m became highly atretic at diestrus, while the 301- to 500-p.m follicles showed maximum atresia at proestrus, but the total number of atretic follicles was highest at diestrus and lowest at estrus. Atresia of large follicles (601 -700 p.m) was mainly noticed at metestrus and absent at proestrus or estrus. In the CD rats total number of atretic follicles was greatly increased (Table 3).

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C A N . J . ZOOL. VOL. 62. I984

Frc Mass theca powe Note view and : Gran gram

;. I. A small follicle ( 100 pm) with three layers of granulosa cells surrounded by thin layer of thcca. x 250. All sections are SI

on's trichrome stain. FIG. 2. High power view of a medium-sized antral folliclc (420 pm) with distinct liquor folliculi. Note well intema and externa. x 250. FIG. 3. A preovulatory follicle showing few invaginations (arrows) in thc granulosa layer. x 100. F I ~

:r view of the section in Fig. 3 to show the granulosa layer invagination (arrow). x 250. FIG. 5. Section through the ovary during two follicles in the initial stages of atresia and one normal healthy follicle with a sign of antrum formation. x 100. FIG. 6. k of an atretic follicle containing fragmented ovum. Theca is transformed into glandular tissue. Granulosa cclls are elongated, f~ ;how fibrous degeneration. X 250. FIG. 7. A large atretic Graafian folliclc showing dispersed granulosa ccl Is surrounding ulosa layers show luteinization. x 100. FIG. 8. Higher magnification of the section in Fig. I 1 to show the ovum and well ilosa lutein cells. x250.

tained with -developed 3. 4. High metestrus.

Iigh power -agmented, the ovum. -developed

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TABLE 2. Number of nonatretic follicles in each ovary during the estrous cycle of the bandicoot rat

Follicle p value of p value of diameter Proestrus Estrus Metestrus Diestrus CDvs . CDvs .

(range), C L ~ (10) (10) (10) ( 10) CD (5) estrus diestrus

30-50 51-100

101 -200 201 -300 301 -400 401 -500 50 1 - 600 601 -700

>700 Total no. of

follicles

NOTE: Values are given as the means 2 SE; those in parentheses indicate the number of' rats used. CD. continuous diestrus. Levels of significance: u , p < 0.001: h. p < 0 . 0 0 5 ; c. p < 0.025: N S . not significant.

TABLE 3. Number of atretic follicles in each ovary during the estrous cycle o f the bandicoot rat

Follicle p value of p value of diameter Proestrus Estrus Metestrus Diestrus CD vs. CD vs.

(range). krn (10) ( 10) (10) ( 10) CD (5) estrus diestrus

30-50 51-100

I0 I - 200 201 -300 30 1 -400 40 1 - 500 50 1 - 600 60 I - 700

>700 Total no. of

follicles

Nurt-.: Values are given as means + SE: those in parentheses indicate the number of rats used. CD. continuous diestrus. Levels ol significance: o . p < 0 . 0 0 5 : h. p i 0.010: c . p < 0.025: N S . not significant.

Corpor~r lute0 The CL which were formed just after ovulation contained a

fluid-filled cavity (Figs. 9 and 10) without fibrocytes and lutein cells with no clear cell boundaries. In the CL of the second cycle, lutein cells became polyhedral (Fig. 1 1 ) and fibrocytes invaded, but these CL had no central cavity. The third type of CL (Fig. 12) possessed mostly the degenerated, pycnoyic, and vacuolated lutein cells accompanied by large numbers of fibro- cytes and leucocytes. Volumes of the first type of CL increased from metestrus to proestrus but declined at estrus (Table 4). The second type of CL were the biggest among all other types, and volumes were maximum at estrus. The third type of CL were maximum during metestrus and diestrus, but their vol- umes were higher at estrus. From the mean number of first and second type CL (Table 4), it was evident that about four ova ovulated during one estrous cycle in this wild rat. Interstitial gland

based either on the size (diameter) of the follicles (Lane and Davis 1939; Mandl and Zuckerman 1952b; Peppler and Greenwald 1970; Hirshfield and Midgley 1978) or on the num- ber of granulosa cells per follicle (Pedersen and Peters 1968; Greenwald 1974). For convenience in this study, we classified the follicles according to their diameters into nine arbitrary types (see Materials and methods) which may be compared with types 3, 4, 5u, 5b. 6, between 6 and 7, 7, 8, and 9, respectively, of Pedersen and Peters (1968). The present study has revealed that in the bandicoot rat, the antrum appeared in follicles ranging over 350 pm in diameter (mostly in the 40 1 -pm follicles). This observation thus differed from that in the laboratory rat where the antrum was reported to appear in the follicles between 100 and 200 pm in diameter (Mandl and Zuckerman 1 9 5 2 ~ ) and even in the 75-pm follicles, and it might not occur in 400-pm follicles (Hirshfield and Midgley 1978).

Large numbers (ca. 15-20 in the largest 5-pm ovarian sec- It was evident that the number of follicles varied in relation tion) of interstitial glands were noticed in the ovary of the to their sire and to the stages of the estrous cycle. About 70% bandicoot rat. Some of the interstitial glands still possessed an of the total number of follicles were below 200 pm i n diameter.

Ovum surrounded by degenerated granulosa Thus, the most numerous follicles were healthy nonantral ones, (Fig. 13). Interstitial glands were composed of polyhedral cells as in the laboratory rat ( L ~ ~ ~ and ~~~i~ 1939; and with -. - round . "'lei and were arranged in definite cords Zuckerman 1952b). mouse (Faddy et al. 1976). and in the wild (Fig. 14).

Discussion mouse (Eriksson 1983). ~owev;r. in the laboratory rat, fol- licles with a diameter less than 350 pm do not vary throughout

Classification of the ovarian follicles in rodents has been the estrous cycle (Mandl and Zuckerman 19526; Hirshfield and

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FIG. 9. A recently formed corpus luteum (first type) during metestrus. x 100. All sections are stained with Masson's trichrome. FIG. 10. High power view of the section in Fig. 9 showing the peripheral differentiated lutein cells and central undiffcrcntiated cells. X250. Fig. 11. A portion of the second type of corpus luteum showing the cords of well-differentiated lutein cells. x250. FIG. 12. Part of thc third type of corpus luteum exhibiting degenerated lutein cells and infiltration of a large number of fibrocytes. X 250. FIG. 13. Section of ovary showing one interstitial gland containing degenerated ovum and granulosa layers. x250. FIG. 14. Section through the ovary showing cords of interstitial gland. x250.

Midgley 1978). In a recent study Hirshfield ( 1983) observed that in the rat the number of healthy follicles <300 pm in diameter dropped significantly from proestrus to estrus, while in the bandicoot rat the number of these follicles declined significantly from proestrus to metestrus. The present study also revealed that the follicles 1600 pm in diameter were present throughout the estrous cycle, whereas in the laboratory rat follicles of 390-500 pm were absent at diestrus and pro- estrus (Hirshfield and Midgley 1978). The large Graafian fol- licles (over 600 pm) were absent at metestrus and diestrus,

while they appeared at proestrus; the follicles above 700 pm (presumably preovulatory) were present only at estrus. Inden- tation of the granulosa by theca was noticed in the preovulatory follicle (Figs. 3 and 4), which has also been reported in labora- tory rats (Deane 1952). Furthermore, very recently formed corpora lutea (Fig. 5) were only noticed at metestrus. Thus it appears that ovulation occurs during late estrus, while in labo- ratory rats ovulation occurs during the early hours of the day of estrus (Schwartz 1969). From the present study it also appears that commitment to ovulation or degeneration is made long

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TABLE 4. Changes in number and volume of corpora lutea during the estrous cycle of the bandicoot rat

First cycle Second cycle Older than two cycles

Volume Volume Volume Stage No. ( x 10' pm3) No. ( X 10' pm3) No. ( x 10' pm3)

Proestrus (6) 2.5050.34 223.01 5 16.08 3.6650.33 163.635 19.92 5.665 1.48 91.235 19.65 Estrus (6) 4.0050.57 204.33k20.56 5.0050.65 277.68k57.28 6.005 1.76 1 19.3353 1.69 Metestrus (6) 5.60+0.40 180.3059.78 5.40t0.24 207.16k24.42 12.20k2.60 64.30k5.44 Diestrus (6) 3.4050.5 1 197.50524.63 4.2050.20 195.48561.01 10.605 1.33 99.235 14.76

Mean 3.87 201.28 4.56 2 10.98 8.62 93.52

NOTE: Values are given as means ? SE: those in parentheses indicate the number of rats.

before formation of the Graafian follicles, probably when the follicles reach 201 km in size.

As in other mammals (Ingram 1962; Guraya 1973; Byskov 1974; Harrison and Weir 1977), atresia was very common in the bandicoot ovary. It was evident that the follicles in the range of 201 -500 km were most susceptible to atresia and this was comparable with that of the rat (Hirshfield and Midgley 1978). The follicles 30-50 km in diameter became atretic only in the CD rats, where 40% of the atretic follicles were in this size range. Follicles ranging from 5 1 to 200 km became maximally atretic during diestrus. Atresia in the pre- antral follicles were also found in the mouse (Oakberg 1979; Ericksson 1983) and rat (Hirshfield 1983). Degenerative changes such as oocyte fragmentation and phagocytosis of the granulosa cells in the aged atretic follicles of this wild rat were the same as in other mammals (Byskov 1974, 1979; Farookhi 198 1 ). Presence of a degenerated oocyte (Fig. 13) or crumpled zona pellucida within the interstitial glands might indicate that the interstitial glands were possibly formed from the atretic follicles as reported in various mammals (see Harrison and Weir 1977). However, luteinization in the granulosa of atretic follicles having ova inside was rarely seen in the bandicoot ovary, the inlportance of which is not clear.

In the bandicoot rat, the highest mean volume of the corpus luteum was much lower than that reported in laboratory rat (277 X 10' krn3 vs. 545 x 10' km3, Boling 1942; 277 x 10' km3 vs. 790 x 10' krn" Deane 1952). Vacuolization reported in the one-cycle-old CL (Boling 1942) did not occur in the first and second type CL of this wild rat; the discrep- ancies were possibly due to difference in species. The number of CL during estrous cycle suggest that about four ova ovulate per ovary during one estrous cycle in bandicoot rats.

From the present study it was evident that the weight of the ovary and the genital tract was significantly higher at estrus than at diestrus and that the weight was lowest in CD rats. Our results corroborate with those found in the collared lemming (Hasler and Banks 1975) and the gray squirrel (Cowles et al. 1977). It seems that the ovary of the bandicoot rat is highly active at estrus.

This investigation suggests that in Bandicota bengalensis, the number of follicles greatly varies in relation to the size of the follicles and stages of the estrous cycle. The basic micro- scopic anatomy of the ovary in this wild rat was almost similar to that of the laboratory rat, and differences were noticed in the appearance of the antrum in the follicles, the time of ovula- tion, and the growth and regression of the corpus luteum.

supervision throughout the investigation. This study was sup- ported by Junior and Senior Research Fellowship grants from the University Grants Commission, Government of India.

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The author is grateful to professor Asok Ghosh, Sir Nilratan 597 - 605. Sircar Professor of Zoology, University of Calcutta, for his INGRAM. D. C. 1962. Atresia. In The ovary. Vol. I. 1st ed. Edited by

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