Paper - Studies on the physiology of reproduction (1932) 4

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Andersen DH. and Kennedy HS. Studies on the physiology of reproduction. IV. Changes in the adrenal gland of the female rat associated with the oestrous cycle. (1932) J Physiol. 76, 247-260.

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This 1932 historic paper by Andersen and Kennedy describes the effect of thymectomy and of season on the age and weight of puberty in the female rat.



See also by this author: Andersen DH. Studies on the physiology of reproduction: I. The effect of thymectomy and of season on the age and weight of puberty in the female rat. (1932) J Physiol. 14;74(1):49-64. PMID 16994258

Andersen DH. Studies on the physiology of reproduction: II. The effect of thymectomy on the age of puberty in the male rat. (1932) J Physiol. 74(2):207-211. PMID 16994270

Andersen DH. Studies on the physiology of reproduction: III. The effect of thymectomy on fertility in the rat. (1932) J Physiol. 74(2):212-3. PMID 16994271

Andersen DH. and Kennedy HS. Studies on the physiology of reproduction. IV. Changes in the adrenal gland of the female rat associated with the oestrous cycle. (1932) J Physiol. 76, 247-260.

Andersen DH. and Kennedy HS. Studies on the physiology of reproduction: V. The adrenal cortex in pregnancy and lactation. (1933) J Physiol. 77(2): 159-73.

Modern Notes: {{rat} | thymus

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Studies on the Physiology of Reproduction

IV. Changes in the adrenal gland of the female rat associated with the Oestrous cycle

By Dorothy H. Andersen and Helen 8S. Kennedy.

(From the Department of Pathology, College of Physicians and Surgeons, Columbia University, New York City.)

Introduction

There are many isolated bits of evidence that point towards an intimate relationship between the adrenal cortex and the reproductive system. To review the entire literature relating to the subject is too large a task to be undertaken here. The two most suggestive types of evidence are the presence of abnormalities in secondary sex characters in cases of tumours of the adrenal cortex[Glynn, 1921, and others]; and the changes in the adrenal gland associated with various phases of reproduction. The present paper treats of the latter.

Hypertrophy of the cortex has been found associated with pregnancy in guinea-pigs [Castaldi, 1922; Kolde, 1913; Guieyesse, 1899; Kolmer, 1912] and its occurrence in rabbits [Kolde, 1913; Stilling, 1898] and in rats [Herring, 1920; Donaldson, 1924] has been denied. In mice there is diminution of the size of the adrenal, but hypertrophy of the zona glomerulosa [Masui and Tamura, 1926; Tamura, 1926]. The hypertrophy in guinea-pigs has been found associated with mitoses in the cortex and with enlargement of the cells in the zona fasciculata [Kolmer, 1912; Guieyesse, 1899; Castaldi, 1922]. It continues through lactation [Verdozzi, 1914]. A similar hypertrophy has been reported in spayed and castrated animals by Schenk [1910], Kolmer [1912], Kolde [1913], and others. Hatai [1913], working on rats, reported a decrease in the female and an increase in the male adrenal after removal of the gonads.

All observers agree on one point, and that is that the adrenal weight varies greatly in normal animals. According to Donaldson [1915] the only other organ weights in rats weighing 150 g. which vary to the same degree are the gonads. Boycott and Kellaway [1924] suggest that this variability indicates that form and function are less closely related here than in most organs. However, we are as yet unable to name the function of the cortex and are therefore at a loss to say whether hypertrophy means decreased function as in the thyroid or increased function as in most organs. Marassini [1906] noted a greater variability in the female, and many workers have observed a larger adrenal in the female than in the male.

Enlargement of the adrenal in connection with ovulation has been noted in frogs [Stilling, 1898], moles [Kolmer, 1918], and in pigeons [Riddle, 1923]. In all of these animals the reproductive season is limited to early spring. The first two undergo other marked physiological changes at that time, so that a direct correlation between the adrenal and ovulation as pointed out by Stilling is not clear. The only animal having a more frequent period of cestrus and one uncomplicated by other factors which has been studied is the mouse. Masui and Tamura [1926] reported enlargement of the adrenal cortex during cestrus in the mouse, but give very few data. Howard-Miller [1927] and Deanesley [1928] were unable to confirm it.

Many workers have investigated the effect of bilateral adrenalectomy on the cestrous cycle. The results have been variable, but the majority find a lengthening of the cycle in the adrenalectomized animals which do not have an abundance of accessories. The recent paper by Martin [1932] reviews the previous ones. That this effect is evidence of a specific cortico-gonadal relationship is unproven, as the cestrous cycle is known to be affected by any procedure which severely affects the well-being of the entire organism.

The present work is based on the probability that if adrenal changes can be found in pregnant and castrated animals they may also be associated with changes in the cestrous cycle.

The one property of the adrenal gland which can most readily be noted objectively and treated statistically is its weight, and it was felt that if a definite change in weight were found, one might expect to find also some change in the size or number of cells. Previous data obtained on adrenal weights in male rats convinced us that the relative weight was more constant, and therefore more significant than the actual weight at any given age, and it was therefore used. The rat was selected as the experimental animal because it has a regular cycle unrelated to season and because of the large numbers of animals required in obtaining reliable statistical data on so variable a thing as the adrenal weight.

TECHNIQUE.

In all, 190 female virgin rats of the same breed were used, and all but a few of Series I were bred in the laboratory.

The first series of rats used in this experiment and reported in Tables I and II included 127 animals. The rats were some of those used in an experiment on the effect of thymectomy on the age of puberty. In 20 of those reported in Table I the smears were not made over a long enough period to be suitable for the analysis in Table II. The adrenals, and in some cases the thyroid and pituitary, were weighed, and it was shown that thymectomy had no effect on the weights of these organs[Andersen, 1932]. The data on these thymectomized rats are therefore included. All rats having any evidence of ear or lung infections at autopsy were carefully excluded, as these are known to affect the adrenal weights [Donaldson]. The rats were given a standard synthetic diet, ad lb. {[Andersen, 1932], with due regard to good light, cage space, and water. Vaginal smears were made daily, beginning with the day on which the vagina opened.

Inspection of the figures obtained from these rats and grouped according to vaginal smears on the day of death showed that although there was a definite difference in the mean absolute and relative adrenal weights at different stages of the cestrous cycle, the individual variation was great, especially during the late post-cestrus and dicestrus phases. The rats with irregular cycles or cycles 6 days or more in length were then placed in a separate group and the remainder were regrouped with relation to the number of days after the first appearance of abundant cornified cells (4+) in the vaginal smear. The rats showing nucleated epithelial cells were included in the “pro-cestrus” group as before. The day after this nearly all the rats had a vaginal smear showing “4+” cornified cells, and this was termed the day of estrus. On the two days after cestrus the smear varied greatly: there were cornified cells, nonnucleated epithelial cells or leucocytes in varying amounts. The animals were grouped according to the number of days after cestrus instead of by the smear. The rats killed during late dicestrus, when the smear was still of the dicestrus type but the uterus showed early cestrus changes, were assigned to a separate group. The resulting figures gave a much sharper difference and this plan was subsequently followed. The grouping is therefore as follows:

(1) Pro-cestrus, smear showing epithelial cells, uterus much enlarged and filled with fluid. 250 D. H. ANDERSEN AND H. 8. KENNEDY.

(2) Cstrus, the first appearance of an abundance of cornified cells, uterus enlarged but containing less fluid.

(3) The day after (2), smear usually showing 4+ cornified cells but sometimes non-nucleated epithelial cells or leucocytes, or any combination of these; uterus rather smaller and contains no fluid.

(4) The day after (3) with a smear showing a few cornified cells or leucocytes; uterus quite small.

(5) Two days after (4). This stage was included only when the rat had regular cycles of 5 or 6 days in length. When the cycles were longer the rats were excluded from this series and when shorter the data were placed under (1). It was therefore necessary to know the usual length of the cycle for each rat, which was fairly constant.

(6) The day before expected cestrus, smear dicestrus; uterus shows early cestrus changes. 5

Since some of these stages are so short as to be missed in smearing only once daily, the 53 rats of our second series and the 20 rats of our third series were smeared every 8 hours for a period covering at least three complete cycles. The hours chosen were 9 a.m., 5 p.m., and 1 a.m. The rats were killed according to the classification of cestrus given above. The pro-cestrus group was killed immediately after the first appearance of large numbers of nucleated epithelial cells. The “estrus” group was killed after the first smear, in which many cornified cells were found, usually with many nucleated epithelial cells still present. The other group was killed at a given number of hours after “cestrus”: day after “oestrus,” after 24 hours; second day after “‘cestrus,” after 48 hours; dicestrus, 60-72 hours; day preceding expected cestrus, at any period after 72 hours, when the uterus showed early cestrus changes and the smear was still dicestrus.

These rats were of the same breed and received the same care as the first series, with the addition of 5 p.c. of dried yeast to the diet, which had no effect on the mean weight of either the body or the endocrine glands which were weighed. The results obtained from the greater frequency of smearing are only a little more clear-cut than in the first series, probably because the mean adrenal weight changes gradually during the cycle. In this second series the rats on the whole were a little older and heavier, but the majority in both series was between 80 and 140 days of age with the actual range 68-170 days. Four rats are added which had had no cycles for many weeks: they were all 8 months old and are not included in any of the other data. A third series included ten rats on a different but adequate diet, which contained 20 p.c. of fat.

adrenals were serially sectioned and used for data on the Cortex-medulla ratio. The weights of the adrenals in Series III are not Yncluded in the figures for adrenal weights at cestrus and dicestrus, but they correspond to them quite closely.

The animals were killed with chloroform, and autopsied at once. The desired organs were quickly dissected clean of connective tissue and fat and placed at once in a closed weighing bottle. The lungs and temporal bones were examined for evidences of infection. The organs were then weighed at once to 0-1 mg. It is believed that the error in dissection and weighing of the adrenals and pituitaries is not over 0-5 mg. The error is much greater in the thyroid weights because the outlines of the gland are not clear-cut. Moreover, the parathyroids are embedded in the thyroids and the weight of the thyroid includes them also. The organs were removed from the weighing bottle one by one and the bottle was weighed after the removal of each. In the first series the adrenal was weighed in each case and the thyroid and pituitary in some cases. In the second series the pituitary, thyroid, adrenal, and thymus were weighed. The ovaries and uterus were examined and preserved, but not weighed. After weighing, the organs were placed in Zenker’s fluid, except that in some cases one adrenal was placed in 10 p.c. formalin for fat stains.

In a group of 44 rats in the first series the ovaries, uterus, Fallopian tubes, pituitary, thyroid, and adrenal were sectioned. In a group of 16 rats of the second series these organs were serially sectioned. They were stained with hematoxylin and eosin. In the latter group frozen sections of one adrenal were made and stained for fat with Scharlach R and Nile blue sulphate. The data on the pituitary and thyroid changes will be presented in a subsequent paper.

In the ten rats of the third series both adrenals were serially sectioned at 5y and every tenth section was mounted. The sections were stained with hematoxylin and eosin and tracings of the outlines of the entire adrenal and the medulla were made with a projection apparatus at a magnification of x 40. These tracings were measured with a planimeter and the volume of the entire adrenal was calculated from the following formula: = planimeter readings x 50u (thickness of section)

0-2 (factor of planimeter) x 40 (magnification) = & planimeter readings x 0-625.

volume in cmm. =


The volume of the cortex was obtained by subtracting the medulla from the total volume.

In each case the probable error of the mean is calculated from the f la: oem pa. = 98/2.

THE VARIATIONS OF THE WEIGHT OF THE ADRENAL GLAND IN RELATION TO THE GSTROUS CYCLE.

The first series of 127 normal virgin rats, when grouped according to the presence in the vaginal smear of epithelial cells, cornified cells, leucocytes or no cells at all, gave the figures for the mean relative weight at these various stages which are shown in Table I. The difference beTaste I, The mean relative weight of the adrenals in various stages of the cestrous cycle

grouped according to the type of vaginal smear on the day of death.

Rats with cycles over

Entire series 6 days in length "FT

Adrenals Adrenals

Stage of cycle No. mg./kg. No. mg./kg. Pro-cestrus 8 250 1 193 Cstrus 32 263 4 235 Post-cestrus 29 240 7 236 Dicestrus 58 237 12 206 Entire series ... 127 246 24 219

tween the mean relative weight at cestrus and at dicestrus was not impressive, but in view of the number of animals represented it invited further investigation.

Inspection of the individual figures showed that many of the low figures were in rats having irregular cycles. After first eliminating the TaBLeE II. The mean relative weight of the adrenals grouped according to the number of

days after cestrus as well as by smear. Rats with long or irregular cycles are excluded,

age 68-150 days, weight 110-182 g.

Grouped by Grouped by No. of vaginal smear days after cestrus

—™\ "OF Adrenals Adrenals

Stage of cycle Vaginal smear No. mg./kg. No. mng./kg. I. Pro-cestrus Nucleated E.C. 7 260 7 260 +26 II. Gstrus First day 4+ C.C. 19 283 19 283 +28 III. Post-cestrus Second day of 4+ C.C. 4 239 Day after estrus W.B.C. or non- ll 251 15 248 424 nucleated E.C. IV. Dicestrus—2 days Varies: 4+ C.C., 10 234 after cestrus W.B.C. or no cells 29 233 +22 V. Dicestrus—3 days No cells 19 233 J after cestrus VI. Day before ex- Very few or no cells 13 269 13 269 +25 pected cestrus Uterus cestrous

Entire series oe woe ase ane

rats on which records were inadequate, the rats having irregular cycles were separated off and the adrenal weights averaged. The resulting figures left no doubt that this group had a lower mean relative adrenal weight than the group as a whole (Table II). Further inspection of the remaining data showed that in many cases the rats killed on the first and second days after cestrus had no cells in the smear while others had 4+ cornified cells or leucocytes. It seemed possible that the time after cestrus was a more important factor than the type of cells in the vaginal smear. The data were regrouped as described above with the results given in Table IT. The figure for cestrus is considerably increased, while that for dicestrus is lowered a little. We conclude on the basis of this finding that changes in adrenal weight with the phases of cestrus are more closely correlated with the number of days after cestrus than with the smear on the day of death.

THE WEIGHT OF THE ADRENAL IN RELATION TO BODY WEIGHT.

The figures in Table II show that there is a greater variation in the relative adrenal weight at cestrus than at any other period, and a less variation at dicestrus. This seems strange in view of the fact that the criteria for cestrus are more sharply defined than those of dicestrus. Moreover, it happened that one group of 25 animals in the second series on which we attempted to confirm the conclusions drawn from the first series were somewhat older and heavier than those in the first group. They ranged from 100 to 150 days in age and from 150 to 225 g. in weight. In this series the cestrus adrenal was surprisingly low and the dicestrus weight was a little lower than that in Series I. We were therefore led to collect all of our data on cestrous rats and arrange them by age and weight to see if there were a definite correlation. This correlation was found as shown in Tables III and IV and Fig. 1. The relative adrenal

TaBLE III. Rats killed at cestrus grouped by age.

Mean Adrenals Age weight —_—_——— (days) (g.) No. mg. mg./kg. Under 80 137 3 45-4 329 81- 90 147 3 40-7 295 91-100 163-1 8 44-6 279 101-110 162-6 7 42-7 269 111-120 159°5 4 42-0 224 121-130 198-3 3 48-0 245 131-140 195-0 3 42-2 218 141-150 188-6 5 48-7 264 151-160 _— 0 — — 161-170 219-8 4 51-9 236 Total 40 254

He

0°40 0°30 0:20

0:10


TaBiz IV. Rats killed at cestrus grouped by weight.



Mean Adrenals Weight age ——_ in g. No. (days) mg. mg./kg. 120-139 4 81-8 41:3 318418 140-159 10 101-4 43-0 287 +28 160-179 13 109-2 44-0 257414 180-199 4 131-2 49-5 258 +27 200-219 7 129-7 47-7 225 +20 220-249 2 166-0 55-0 235 +13 Total 40 omen XK ae M al e —t—« Female @ Oestrus ‘X= ea tee Xome o me ee me a eee mee eee mes meee» cee + mee oe sets ee Hawn new ang,



70 680 90 100 110 120 130 140 150 160 170 180 Age in days

Fig. 1. The relative weight of the adrenal gland at various ages in mature male and female rats.

weight decreases progressively as the weight of the rat increases. This relationship is not so sharply defined in regard to age, although since weight is to some extent a function of age there is some change there. Our experience corroborates Donaldson’s tables in regard to the wide variations in weight in normal young adult rats, bred and kept under PHYSIOLOGY OF REPRODUCTION, IV. 255

conditions which are apparently the same. This table brings out the point that the absolute weight increases gradually with body weight. These clearly defined results led to rearranging the data for all stages of the cycle according to weight. On the basis of the figures given in Table IV it was decided that all rats under 160 g. would form one group, those between 160-180 g. a second group and those over 180 g. a third group. The results of this rearrangement are shown in Table V. It is

TaBLE V. Weight of the adrenals at various phases of estrus grouped by weight.



Body weight Cc a \ Under 160 g. 160-180 g. Over 180 g. Stage of c A + c ~ + c ~ cycle No. mg. mg./kg. No. ing. mg./kg. No. mg. mg./kg. Pro-estrus 65 39-6440 286423 0 — _ 1 37-7 208

Cstrus 14 42-5434 296427 13 43-9403 265415 13 49-2443 237416

First day 7 33:042-4 240430 4 43-0405 253425 0 _ _ after cestrus

Second day 19 36-0+43-2 249423 8 41-440-4 244426 6 42:0+42-4 212+6 after oestrus

Third day 7 31:043-1 212418 5 40-2407 235408 1 41-9 215 after cestrus

Day before 11 37-8428 278420 2 50-0440 295421 0 _ — expected

cestrus

obvious that the greatest difference between the figures for both actual and relative adrenal weights for cestrus and dicestrus is found in the lighter rats. The adrenal weight at cestrus shows a much greater variation than that in dicestrus, although in both cases it is greater in the young animals.

CoRTEX-MEDULLA RATIO.

The relative volumes of the cortex and medulla of the ten rats in Series III are given in Table VI. The rats were killed at phases 2 and 5

TaBLE VI. Weight of adrenal cortex and medulla.

Adrenals Age Weight .——*~———, ‘° Cortex Medulla Rat No. (days) (g.) mg. mng./kg. mg./kg. mg./kg.

CEstrus 1081 op. 61 129 34-7 270°5 253-7 16-8 Dicestrus 1068 op. 64 149 36-6 245-5 227-3 18-2 Estrus 1061 c. 61 127 40-0 315-0 296-7 18-3 Dicestrus 1076 c. 62 142 35-8 252-1 235-1 17-0 Cstrus 1073 op. 62 170 44-4 261-5 244-5 17-0 Dicestrus 1079 op. 63 132 31-2 236-3 217-4 18-9 Estrus 1058 c. 63 150 41:5 276-8 260-7 16-1 Dicestrus 1050 c. 64 149 32-5 218-2 199-6 18-6 Estrus 974 73 168 45-0 268-0 251-7 16-3

Dicestrus 973 72 161 38-9 242-0 225-4 16-6

respectively. The mean percentage of medulla was found to be 6-08 + 0-17 for cestrus and 7:51 + 0°45 for diestrus. The mean relative weight of the cortex as calculated from this percentage is 261-5 + 12-2 mg./kg. for cestrus and 221-0 + 8-3 for dicestrus. The mean relative weight of the medulla is 16-9 + 0-5 mg./kg. for oestrus and 17-9 + 0-6 for dicestrus. It will be noted that the difference in cortex weight for cestrus and dicestrus is significant, while that for the medulla is not, in view of the probable error. This means that the change in weight is due entirely to cortex.

HISTOLOGICAL CHANGES.

A comparison of the sections taken from rats killed at cestrus and at 60 hours after cestrus, under the standard conditions given above, reveals no change in the medulla as seen in the hematoxylin and eosin or fat stains. There is a change in the cortex (Fig. 2). In dicestrus the adrenal has a wide and clearly defined glomerular zone, outlined by a line of condensed nuclei from the fascicularis. The cells in the outer portion of the fascicularis are somewhat larger than those in the inner portion, but they contain few vacuoles. The cytoplasm is decreased in the inner zone and it merges without any sharp demarcation into the zone of cells bordering the medulla. Near the medulla and often lying adjacent to it are small groups of cells with an eosinophilic cytoplasm which is more abundant than that in most of the cells of the inner third of the cortex.

In the adrenal at cestrus the glomerular zone is narrower and less clearly demarcated from the fascicularis. The cells of the outer half or two-thirds of the zona fascicularis are much enlarged, pale and vacuolated. The margin between this area and the more compact cells of the inner third of the cortex is irregular and not sharply defined. The eosinophilic cells near the medulla are enlarged, contain vacuoles and resemble the cells of the outer portion of fascicularis. Mitoses are extremely rare in the adrenal during both cestrus and dicestrus.

Scharlach R stains on frozen sections of the adrenal at dicestrus show an abundant deposit of large droplets of lipoid in the cortex which take the stain deeply. The margin of concentrated cells between the glomerular and fascicular zones and the more compact cells of the inner third of the latter do not take the stain. The nests of cells near the medulla do take it. At cestrus a few cells of the outer fourth of the medulla and some of the cells next the medulla contain large droplets which take the stain, but most of the cortex stains a diffuse pale red. Nile blue stains most of the cortical cells blue, although there is a little red-stained material in the inner portion of the zona fascicularis. The blue is somewhat more abundant at cestrus, although the difference is not as striking as in the Scharlach R stains,



1. Dicestrus. H. and E. 2. Gstrus. H. and E,


3. Dicestrus. Scharlach R. 4. Estrus. Scharlach R. Fig. 2.


THE ADRENALS IN ANIMALS HAVING IRREGULAR CYCLES OR NO CYCLES.

The data given in Table I show that the adrenal weight is quite low in animals having unusually long or irregular cycles. This led us to watch for animals which had had no cycles for some weeks preceding autopsy. Most of these animals were infected and therefore unsuitable for comparison, but four were found which were uninfected, and the adrenals in these animals were found to be quite small, and to have

TaBLE VII. Rats that had no cycles for several weeks preceding autopsy. Ovaries without corpora lutea or large follicles.

Adrenals Age Weight —— Rat (days) (g.) mg. mg./kg. 43-85 246 165 23 139 45-05 239 159 31 198 46-07 239 196 29 148 46-10 239 187 34 182

approximately the same relative weight as the adrenals of our spayed animals (data unpublished) (Table VII). Whether the lack of ovarian activity or the small adrenal is primary is, of course, still unknown.

Discussion

The evidence presented points to a definite change in the physiology of the adrenal cortex associated with cestrus. Whether this is an increase or decrease of activity is still a problem. It also remains to be proven that this change signifies a specific causal relationship.

Conclusions

1, The absolute and relative weights of the adrenal glands of the virgin female rat are greater at cestrus than at dicestrus, providing that the body weight is the same.

2. Rats having had irregular cycles or cycles of 6 days or over are found to have a lesser absolute and relative mean adrenal weight both at cestrus and dicestrus than those with regular cycles. PHYSIOLOGY OF REPRODUCTION, IV. 259

3. If the relative adrenal weights of the rats killed at cestrus are grouped according to the body weight of the rats, it is found that the absolute weight of both adrenal glands increases with body weight, while the relative weight decreases. The correlation is less close when the grouping is by age.

4. The relative adrenal weight of the rat in dicestrus is a fairly constant figure, regardless of the regularity of the cycle or the weight of the rat and is 0-20-0-23 g. per kg. body weight. The absolute weight is variable.

5. The difference between the mean relative weight of the adrenal gland at cestrus and dicestrus is therefore greater in lighter animals. In our series of 63 animals weighing less than 160 g. and having had regular cycles the mean relative weight at cestrus was 296 + 27 mg./kg., and at dicestrus 212 + 18. The difference in relative weight is about 25 p.c. of the figure for cestrus.

6. The difference between the mean absolute weight of the adrenal gland is also greater in lighter animals. The figures for the rats weighing less than 160g. are: cestrus, 42 + 3-4 mg.; dicestrus, 31 + 3-1. This represents a difference of about 25 p.c. of the weight at oestrus, and of 11 mg. between the two means. In the rats weighing 160-180 g. the difference is 4 mg. or about 9 p.c., and in those weighing over 180 g., 7 mg. or about 14 p.c. The mean difference in actual weight is therefore in the same order of magnitude in these series, although the number of rats in the last two groups is not great enough for the actual figures to be final.

7. The increase in weight is found to be due entirely to increase in the size of the cortex. The cells of the zona fascicularis and of the cell nests near the medulla are enlarged during cestrus and contain an increase in lipoid which appears pale pink when stained with Scharlach R.

8. Since the weight and histological appearance of the adrenal of the unmated female rat is so variable it is suggested that, in experiments in which the sex of the animal is a matter of indifference and the weight or appearance of the gland is a criterion, male animals should be used.

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Cite this page: Hill, M.A. (2024, March 19) Embryology Paper - Studies on the physiology of reproduction (1932) 4. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Studies_on_the_physiology_of_reproduction_(1932)_4

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