Paper - On The Age Of Human Embryos

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Mall FP. On the age of human embryos. (1918) Amer. J Anat. 23: 397-422.

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Franklin Mall (1911)
Franklin Mall (1911)

On The Age Of Human Embryos

Franklin P. Mall

Johns Hopkins Medical School, Baltimore, Md.

Two figures And Eight Tables

In the Manual of Human Embryology, published seven years ago, I presented the evidence by which We may determine the age of an embryo or fetus, in my chapter dealing with this subject.[1]See also Note on the collection of human embryos in the Anatomical Laboratory of the Johns Hopkins University.[2]

In the second paper I gave a formula by which the age of embryos up to 100 mm. long could be determined. That is, to multiply the CR length in millimeters by 100 and extract the square root; the product is the age in days. I wish to state that this formula gives the age according to the His convention, which I now believe to be incorrect, as demonstrated in my chapter in the Manual. This conclusion was also reached independently by Bryce and Teacher. A fairly complete bibliography is to be found. in the papers by Mall (1), Bryce and Teacher (3), Triepel (2) and Grosser (6).</ref> It was there pointed out that the best check in arranging embryos in time sequence is obtained from our knowledge of comparative embryology ; also, that the only factor which can be depended upon in every case is what I then termed the ‘menstrual age;’ that is, the age of the embryo as computed by the time elapsing between the beginning of the last menstrual period and the date of the abortion.

In order to procure a satisfactory curve of growth for the Whole period of gestation, I succeeded in collecting about 1000 specimens from the different months of pregnancy with the data given concerning them ,' namely, the measurements of the embryos and the dates of menstruation and of abortion. It was also necessary to establish standard measurements for the embryos, chief of which are sitting-height and standing—height; these are known respectively as crown—rump (CR) and crown heel (CH). Tables were prepared by which the average measurements of the one for a given stage could be converted into the average measurements of the other; for it is well known that embryologists are given to using the crown—rump measurement for smaller specimens, while anthropologists and obstetricians generally use the crown-heel measurement for larger specimens.

Menstruation Age

My tabulation of the menstrual age was made as follows: All the measurements of the embryos and fetuses were converted into crown—rump or sitting-height measurements. These were then used as ordinates, while the menstrual ages were used as abscissae; in other words, each specimen was entered upon a chart in which the menstrual age and the sitting-height together made a co-ordinate. In this way the 1000 specimens were spread over a millimeter chart, 500 m.m. high and 350 mm. wide. It was found that the individual records arranged themselves along a path about 20 mm. wide at the base line, and about 4.0 mm. Wide toward the upper margin of the chart. In addition to this central zone containing most of the records there were numerous scattered entries far out of line. These were especially numerous at the bottom of the chart, which would indicate that in early abortions there is an undue number of poor records; or, at least, records showing greater irregularity in the menstrual periods. In order to determine a mean menstrual age the chart was marked square by square in such a way that exactly one half of the records were circumscribed by two lines enclosing the usual or normal cases, leaving one quarter of the scattered records to the right of one line, the other quarter to the left of the other line. The first group includes those specimens which grew very slowly and may have been pathological; the second, those cases in which menstruation continued after pregnancy. The two lines which include the middle group are practically parallel, beginning about 20 mm. apart, around the records of the early specimens, and ending about 40 or 50 mm. apart around the specimens from the latter part of pregnancy. The distance between these two lines was then divided exactly, and it is this line which marks the mean menstrual age of embryos throughout pregnancy. In a general way it is reproduced as the line OH in figure 145 in the Manual of Human Embryology (p. 200).

I have spoken of the age thus determined at different times as the menstrual age, or more properly speaking the mean menstrual age, because there is a Very large probable variation. For instance, a number selected at random from the table on page 199 of the Manual, with a mean menstrual age of 51 days, would also show a probable deviation of from 40 to 62 days. Such embryos have a height of 11 mm.; therefore, when we obtain embryos of this length, we may expect that one-half of them have a menstrual age of from 40 to 62 days; in other words, in small specimens there is a probable variation of three weeks. Viewed from another angle, one-half of the embryos with a menstrual age of 51 days would range from 4 to 25 mm., while the average would be 11 mm.; hence, we are probably dealing with a pretty large error which cannot be definitely located. At present it would appear that pregnancy may begin at any time during the intermenstrual period, but it is difficult to determine the most probable time. What I published in the Manual has received careful criticism from Triepel[3] but he nevertheless also accepts the term menstrual age, and recommends that we use it in the future.

Copulation Age

After constructing the curve and table referred to above, showing the mean menstrual age, I entered as the probable or true age a line in the curve and a column in the table which fall in a position exactly ten days earlier than the mean menstrual age. This was done for the following reasons: According to the more recent statistics of Issmer, that writer found the average duration of pregnancy in 1220 cases to be 280 days, when estimated from the first day of the last menstrual period; and in 628 cases, 269 days when estimated from fruitful copulation. In general these figures correspond with those of Ahlfeld, Hecker and Hasler, who collected about 500 cases in which the date of fruitful copulation was given. Therefore, in a group of 1200 cases the duration of pregnancy, when reckoned from the last menstrual period, was fully ten days longer than when computed from the time of copulation; and it seems to me that in order to determine the true age it is necessary to deduct these ten days from the menstrual ago. Even then I believe we should be careful not to use the word true, since the time of copulation does not necessarily record the time of fertilization. For this reason it might be well if we introduced the term, copulation. age, to distinguish it from menstrual age, and from two other ages I am about to give. These could be termed ovulation age and fertilization age, the latter being the only true age, since we must always figure the beginning of development from the time of fertilization.

The curve in the chart, which I gave in my publication, as representing the true age, but which I now will speak of as the copulation age, was constructed from cases of newborn children, and isprobably the more valuable because it eliminates all of the irregularities of early pregnancy which accompany natural abortion. After the curve was completed, however, we received into our collection a few embryos, measuring less than 25 mm., the accompanying records of which gave the time of copulation as well as of menstruation. The copulation ages of these specimens were then entered upon the chart shown in the hianual with stars (fig. 147), and curiously enough nearly all of them fall exactly upon the line of the curve, showing that what was assumed to be a difference at the end of pregnancy is also indicated again in specimens from the beginning of pregnancy. In both cases the difference between the menstrual age and the copulation age is about 10 days. When this chart was made it contained seven stars, but after it had been sent to the printer I found another case in the literature. Also, about the same time I received a copy of a book published by Bryce and Teacher,[4] which gave a second case, and these were added to the curve. To my great surprise and pleasure I found that these authors had reached a conclusion similar to mine; namely, that the age of young embryos is no longer to be computed according to the convention of His. They not only give a‘ detailed and excellent account of their own specimen, but also reconsilder all other cases of young specimens in relation to their age, which have been published by well—known writers. They assume that the copulation age is probably very nearly the true age of embryos, and that henceforth we will have to consider the question from this standpoint.

According to Bryce and Teacher, it is now generally admitted that the menstrual cycle in man and monkeys is homologous with the oestrus cycle of the lower mammals. The oestrus cycle is divided by Heape into pro-oestrum, oestrus and dioestrum, and this division has been confirmed for many mammals by his own researches and those of F. H. A. Marshall. During prooestrum the generative organs of the female show signsof special activity, such as swelling of the vulva, coloration or flushing of the surroundings, and a discharge of blood or mucus from the vagina. This is immediately followed by the ‘oestrus,’ or ‘period of desire,’ ‘during which alone the female is capable of impregnation and will receive the male. If pregnancy does not occur, oestrus, after a brief space in which desire subsides (metoestrum), is succeeded by a period of quiescence or dioestrum, which lasts till pro—oestrum again sets in. In polyoestrous mammals several cycles of this kind may follow one another. Menstruation in the human female is homologous with pro-oestrum, as first pointed out by Heape. Though ‘there is no fixed ‘period of desire’ there is an indication that a vestige of this persists, in the fact that a phase of more pronounced oestrus commonly succeeds the cessation of menstruation. This View is confirmed by our records, for We frequently hear from a patient that a fruitful copulation occurred shortly after the menstrual period; and it may be that this opinion records also the rupture of the Graafian follicle. According to J. G. Clark[5] this is accompanied by vascular hyperemia of the ovary, and the possibility of a spasm of the ovary is not to be excluded, for there is an abundance of muscle in this organ which no doubt has a function to perform.

The following histories include all cases from our collection in which the copulation history is given. I have also added the Watt[6] case because it is the only one I have been able to find in the literature since the publication of the Manual. 1 have included all cases because I think it is best not to select those which suit my convenience in making a curve, but to give the poor material together with the good. A few of the records are sufficiently complete to be unimpeachable; the remainder are given for what they are worth.


No. 1399

No. 1399 (Dr. H. N. Mateer, Wooster, Ohio.) Embryo, GL 1 mm. Chorion 10 X 9 mm. From a hysterectomy. Copulation September 19 and September 27. Operation, October 19. (I have been unable to find out date of last period, but it is probably recorded.) Copulation age 22 or 30 days. If the former is taken, it matches the curve exactly.

No. 779

No. 779 (Dr.——— , Baltimore.) Embryo, GL 2.75 mm. The specimen though otherwise normal was later found to have spina bifida. It came from the physician’s wife. She is 37 years old, and is the mother of one child and this is her first abortion. She is very anxious to have children. Last period, August 29 to September 2. Abortion, October 12. Fruitful copulation, in the Woman’s opinion, September 25 and later. She does not state specifically that copulation occurred between September 2 and September 25. Menstrual age, 44 days. Copulation age, 17 days or less. Doubtful case.

Watt’s case

(Dr. Watt, Toronto.) Twin embryos, GL 2.75 and 3.55 mm.

Mother, 3. German Jewess, 30 years old, robust and healthy, four children and this one abortion. Last period, December 3 to 6, 1907; first copulation December 20. Slight flow January 3, with similar flow on January 11, 12 and 13, abortion following on January 14. Menstruation age, 42 days. Copulation age, 25 days or less.

No. 1182 b

(Dr. C. E. Caswell, Wichita, Kansas.) VVoman aged 27, four living children and one abortion. Husband has syphilis and so has one child. Mother seems to have escaped. Last period, March 25 to April 4. Abortion, May 10. Mother is sure that conception took place April 14. Menstrual age 46 days. Copulation age, 26 days. Doubtful case.

No. 470

No. 470 (Dr. H. C. Ellis, Elkton, Md.) Embryo, CR 4 mm. Chorion, 20 x 13 mm.

Mother, 24 years old, two healthy children. Abortion during an attack of mumps with very high fever. Last period October 5, 1910, and copulation about October 15. Abortion November 9. Menstrual age, 35 days; copulation age not over 25 days.

No. 588

No. 588 (Dr. G. L. Wilkins, Baltimore.) Embryo, CR 4 mm.

Last period January 26 to February 3. Had no intercourse with husband for several weeks prior to this and only three or four days after period but not later. Abortion March 16, 1912. She has had two healthy children, 14 and 20 years old respectively, and not less than eleven abortions. Dr. Wilkins believes that all the abortions were induced. Menstrual age, 50 days. Copulation age, 38 or 39 days.

No 1507

No. 1507 (Dr. C. B. Ingraham, Denver, Colorado.) Macerated embryo, GL 4 mm.

A Jewess who last menstruated May 7 to 11; abortion June 22. Woman had opportunity to become pregnant shortly after this period or again just before the next. Menstrual age, 46 days; copulation age, 40 days or 17 days. Record not satisfactory, especially since specimen ‘s also pathological.

No. 208

No. 1208 (Dr. J. Y. Dale, Lamont, Pa.) _ Normal embryo, CR 7 mm., GL 8 mm. The specimen was enclosed in an almond-shaped ovum, measuring 22 x 11 x 11 mm., and there was considerable magma Within the exocoelom. The specimen came from a married woman whose last period began on December 28, 1901, and who had coitus only twice, January 5 and January 7, between this period and the time of abortion, February 15, 1902. Dr. Dale informs me that the data are entirely reliable, as both the Woman and her husband are thoroughly trustworthy. The specimen was secured for me by Prof. John G. Clark of the University of Pennsylvania, Who thought that its unique history gave it greater Value. Menstrual age, 49 days ; copulation age, 39 to 41 days.

No. 1461

No. 1461 (Dr. H. A. Wright, Seattle, Washington.) Embryo, CR 9.8 mm.

Menstrual age, 28 days; copulation, 27 days. Data inaccurate and incomplete. Not a reliable case.

No. 443

No. 443 (Dr. William Grant, Baltimore.) Embryo about 10.5 mm. long. The specimen was sent at the suggestion of Prof. T. S. Cullen on account of its interesting history. Menstrual age, 27 days and copulation age, 28 days. On account of the manner in which the history was given, and because of the degree of development of the embryo, the data can hardly be admitted as correct. The husband had been away from home for four months prior to the time of coitus, which was on the last day of menstruation. The woman is the mother of four healthy children and menstruates regularly every 28 days. The patient was reluctant to show the specimen to the physician, and both she and her family defended her character, a fact which would seem still further to convict her. For this reason the record is not to be considered reliable so far as the age of the embryo is concerned.

No. 167

No. 167 (Dr. A. H. Ritter, Brooklyn, N. Y.) Embryo, CR 14.5 mm., NL 13.5 mm.

The normal embryo was sent in a beautiful normal ovum measuring 30 x 30 x 20 mm. The specimen came from a multipara whose last period was from November 26 to December 2, 1899. first copulation after the period on December 15. Due to a surgical operation on January 24 there was continuous hemorrhage until January 3 when the ovum was passed. In the event that conception took place after the last period, this specimen could not be more than 46 days old. Menstrual age, 65 days; copulation age, 46 days.

No. 1390

No. 1390 Dr. G. N. J. Sommer, Trenton, N. J.) Embryo CR 18 mm.

Last period, December 18 to 22. Operation for tubal pregnancy, February 10. Conception took place on December 25, as the Woman was in the habit of using preventive means and same were not used on Christmas eve. Menstrual age, 54 days; copulation age, 47 days. Reliable case.

No. 1584

No. 1584 (Dr. F. H. Church, Bonnville, N. Y.) Embryo, CR 18 mm. Chorion 35 x 31 X 25 mm.

Unmarried woman, age 21, first pregnancy. Last period August 15; menstruation regular, every 28 days. Criminal abortion, October 10. Coitus, September 13 and 14. Menstrual age, 56 days; copulation age, 26 and 27 days. Not reliable.

No. 26

No. 26 (Dr. C. E. Simon, Baltimore.) Fetus, CR 25 mm., CH 30 mm. This specimen, which was somewhat injured and therefore ditficult to measure with precision, was brought to me by Dr. Simon, February 25 C?) 1894 with the following history. The mother, an unmarried Woman 27 years old, was a servant in Dr. Simon’s family, and had but recently come from Germany. She remained at home continually until New Year’s eve, when she went to a ball and remained out all night. Her last period took place on December 12 and lasted six days. During the night of December 31 she was with her lover and the abortion followed on February 25. On January 16, after missing her January period, she took a cupful of mustard powder with the hope that it would produce abortion, but instead it nearly killed her. On January 21, she recovered, and resumed her household duties. (See record of the case by Simon, N. Y. Med. Jour., March 17, 1894.) Later she fell into the hands of an abortionist and the embryo came away during the night of February 24. Dr. Simon assured me at the time of the abortion that it was absolutely impossible for the pregnancy to have taken place at any time excepting the night of December 31.

Menstrual age, 75 days; copulation age, 56 days. Reliable case.

No. 616

No. 616 (Dr. S, P. Warren, Portland, Me.) Embryo, CR 26 mm. Unmarried woman, 18 years old; last period began August 9 and continued 7 days. Coitus three times within 9 days after the last period. Curetted after 24 hours of pain, October 13, 1912.

Menstrual age, 65 days; copulation age, 56 days (?). Not reliable.

No. 1535

No. 1535 (Dr. Philip F. Williams, Philadelphia).

Embryo, CR 28 mm. Chorion, 50 x 4.5 x 15 mm.

Unmarried woman, 20 years old; first pregnancy. Last period, May 3 to 7. Abortion, July 6. Last coitus, May 10 (?). Menstrual age, 62 days; copulation age, 55 days. Doubtful age, but it falls close to the time of the probable age.

No. 373

No. 373 (Specimen loaned by Prof. Simon H. Gage, Ithaca, N. Y., Cornell Collection, Homo No. 11.) Embryo, CR 31 mm.

Last period, May 9. Conception, May 21. Natural miscarriage July 17, after 2 to 3 days bleeding. No other data. According to these records the menstrual age is 69 days and the copulation age 57 days.

No. 849

No. 849 (Dr. Shipley, Baltimore.) Embryo, CR 52.5 mm.

Mother, white, unmarried, age 20. Last period, December 11 to 15, 1913. Abortion, March 3. Coitus from Which mother dates pregnancy occurred just after the cessation of the last menstrual period in December, but she admits that she had frequent intercourse previous to this period.

Menstrual age, 82 days; copulation age, 77 days ('3) Doubtful case.

No. 591

No. 591 (Dr. G. C. McCormick, Sparrows Point, Md.) Embryo, CR 62 mm. End of last period, January 1, 1912. Coitus, January 7; abortion, March 29.

Menstrual age, 93 days; copulation age, not over 82 days.

No. 1635

No. 1635 (Dr. Henry Leaman, Philadelphia.) Embryo, CR 70.5 mm. Mother, 40 years old, 9 children. Last period, August 26 to 30; abortion, November 29. Copulation but once about September 3 to 15. Self induced abortion.

Menstrual age, 95 days; copulation age, 75 to 87 days. Records contradictory.

No. 322

No. 322 (Dr. West, Bellaire, Ohio.) Embryo, CR 8590 mm.

The specimen is probably from an induced abortion. The mother says that fruitful coitus took place on June 17 and the abortion on September 20, copulation age 95 days.

No. 1295 c

(Dr. L. J. Commiskey, Brooklyn, N. Y.) Embryo, CR 87.

Woman, 43 years old, mother of one child and this is her second abortion. Last period, April 24 to 28; abortion, July 27. Woman states with great certainty that the productive coitus took place either May 4 or 6.

Menstrual age, 94 days; copulation age, 84 or 82 days. Doubtful case.

No. 1310

No. 1310 (Dr. B. G. Pool, Washington, D. C.) Embryo, CR 95 mm.

first pregnancy of unmarried Woman, 18 years old. Last period, July 25 to 30, 1915; abortion, November 6. Said to be from a single coitus on August 9. Menstrual age, 104 days; copulation age, 89 days. Doubtful case. *

No. 894

No. Template:CE894 (Dr. E. L. Mortimer, Baltimore, Md.) Embryo, CR 121 mm.

White mother, age 29, three children and two abortions. Last period, July 24 to 28; criminal abortion, November 21. Husband works on a boat and returned home August 1. Menstrual age, 120 days; copulation age, not over 112 days.

No. 142

No. 142 (Dr. G. H. Hocking, Govans, Md.) Embryo, CR 142 mm.

Mother, age 43, has five children. Mcnstruatcd May 29 to June 9; abortion, October 5 after several weeks’ flow. Woman says pregnancy could not have taken place before June 18.

Menstrual age. 129 days; copulation age, 109 days. Doubtful case.

The summary of these cases together with all others of the same kind which I have been able to gather from the literature, is given in table 1. This is an elaboration of the table given in the Manual. The data are sufiiciently complete so that those who choose may look up the original records. Most of them, however, will be found in abstract form in the articles by Triepel and by Grosser.[7] The specimens in the Carnegie Collection are recorded above.

All of the specimens just given are entered upon figure 1. The mean menstrual age and the mean copulation age are taken from the data given in the table and in the curve published in the Manual. For the specimens here considered the menstrual ages are indicated by means of dots, the copulation ages by large solid circles. The time is calculated by days, and the measurements of the embryos are croWn—rump. The numbers of several specimens for which the copulation age is given are marked in figure I;. for instance, No. 443 and No. 1310. One of the Rabl cases is also indicated. I am of the opinion that all these marked records should really be excluded from the figure as they do not appear to be very reliable. However, I have included them for the sake of completion. Six of the copulation cases are crossed in the figure with an X, and are given again in table 2.

It will be noticed that these six records fall almost exactly upon the curve given. They are, I believe, the only ones Which are entirely reliable; that is, they record embryos which are the product of single copulations, and for this reason their maximum ages are established. A word regarding specimen No. 26, which is recorded in the literature as representing an embryo 30 mm. long. As we are at present dealing with CR measurements, this should be 25 mm. It appears on the chart in the Manual as 30 mm., for the reason that the curve was constructed on the basis of the standing height, or CH length of the embryos. The tables given by Triepel and by Grosser should, therefore, have this measurement corrected accordingly.

I have also entered upon my figure the ages of the embryos according to their degree of development as given by Triepel in order to show that he has practically adopted the curve of deVelopment given by Bryce and Teacher a11d also by myself. He has really taken what I have designated as the copulation age, minus about two days for each stage, assuming, as do also Bryce and Teacher, that there is this interval of two days between copulation and fertilization. For the sake of completion the curve giving the His convention is also included in the figure.

Table 1

Table 1
Length of Embryo (mm) Menstruation (days) Possible Time Author Embryo No.,
Embryo 0.15 38 Exactly 16 days Bryce-Teacher, 1908
Ovum 5.5 X 3.3 42 20 days before and earlier Reichert, 1873
Embryo 1.0 22 and 30 days before No. 1399
1.2 C?) 38 19 days (Delaporte) See Grosser Anat. Anz. xlvii, 1914
1.3 34 Exactly 21 days Etcrnod, Anat. Anz. Xv, 1899
1.5(?) 35 14 days Fetzer, Anat. Anz. Erg. Hft. Xxxvii, 1910
2.75 44 17 days and later No. 779
2.75 42 25 days and later Watt, Carnegie Contributions to Em3,33 42 (Twin) Ebryology, ii, 1915
3 46 26 days (?) No. 1182b.
3.2 48 40 days and later His, AME, vol. 2, 1882
4.0 35 25 days (?} No. 470
4.0 50 38 days No. 588
4.0 46 40 days and 17 days C?) No. 1507
6.0 50 40 days and later Kollmann’s Atlas, 1907
7 49 39 and 41 days No, 1208
7.75 57 45 days and later His
8.8 42 Exactly 38 days Tandler, Anat. Anz., Xxl, 1907
9.8 28 27 days (3) N0. 1461
10 60 49 days and earlier His
10.5 27 22 days C?) No. 443
11 55 31 days (?) Rahl, Entwickl d. Gesicht
13.6 63 53 days and later His
14 65 Exactly 47 days Rahl
14.5 65 46 days and later No. 167
18 54 Exactly 47 days No. 1390
18 56 26 or 27 days ('3) No. 1584
25 75 Exactly 56 days No. 26
26 65 56 days No. 616
28 62 55 days C’) No. 1535
31 69 57 days No. 373
52.5 82 77 days (‘?) No. 849
62 93 Not over 82 days No. 591
70.5 95 75 or 87 days C’) No. 1635
85 (N 95 days No. 322
87 94 82 or 84 days (‘I’) No. Template:CE12950
95 104 89 days (?) No. 1310
121 120 N ot over 112 days No. 984
142 129 Not over 109 days No. 1284


Fig. 1 Menstruation age and copulation age taken from the curve constructed by me and published in the Manual of Human Embryology. All embryos are entered with CR. length. I have also added for the sake of comparison the curve giving the convention of His. NL and CR give the neck-rump and crown-rump lengths respectively, according to His. The fertilization age is according to Bryce and Teacher for smaller embryos, and according to Tricpel for larger ones. The dots record the menstrual age of the embryos under consideration, and the squares the copulation age. The crossed squares mark the best records, as mentioned in the text. It may be noted again that the curves are not constructed from these records, but the records are entered to test the curve.

Table 2

Table 2
Author CR Length of Embryo (mm) Copulation Age (days)
Bryce and Teacher 0.15 16
Eternod 1.3 21
Tandler 8.8 38
Rabl, V 14.0 44
No. 1390 18.0 47
No. 26 25.0 56

I wish again to emphasize the fact that the curves given in the figure are not constructed from the records of the specimens in question, and it is quite clear, I think, that the new cases give no reason for materially altering the mean copulation curve as given by me in the Manual seven years ago. The relation of these curves to the ovulation age and to the fertilization age remains to be established, and as far as the evidence will permit this will be done in the following paragraphs.

Ovulation Age

The question of the time of ovulation in relation to menstr11ation or to copulation is by no means answered, although the literature upon the subject is extensive. If the time of ovulation could be definitely determined We would then be able to ascertain the ages of embryos with very fair precision. Wherever possible We have collected ovaries with our specimens, but so far have obtained only one accompanying a young ovum. This specimen, No. 970 in our collection, is from a filipino girl, 16 years old, Who died four days after taking hydrochloric acid with suicidal intent on account of her condition. The ovum, which measures 5 x 3 mm., is not quite normal in appearance but is Well implanted. The corpus luteum is well formed, and solid, with no remnant of blood within it. The Herzog[8] specimen, which is also from a filipino woman who Was killed in an accident, likewise had a small ovum measuring 2.3 X 1.2 mm., well implanted in the uterus. In this case the corpus luteum was ‘fresh but closed.’ The Well known Reichert specimen which measured 5.5 x mm., with a copulation age of 16 days or more, has in one ovary a Well-formed corpus luteum, 20 X 17.5 mm. which has Within it a small cavity containing some blood. finally, Johnstone[9] describes and pictures the corpus luteum of an ovum almost the size of Peters’ specimen, which measures 13 X 10 mm. Its center is occupied by a large mass of pale, finely granular material which stained pink with eosin. The periphery is composed of a layer of lutein cells bordered on the inside by a layer of red blood corpuscles. The lutein layer, which is 8 X 10 cells deep, is crinkled, owing to papillary ingrowths of connective tissue. There is a great deal‘ of vacuolation of the lutein cells and the whole layer is quite vascular. The specimen came from a woman, aged 29, who died suddenly, not having missed a period, nor was it suspected that she was pregnant.

A step in advance on the study of the structure of the corpus luteum was made by R. Meyer[10] in his excellent paper on the subject. He classifies its development into four stages as follows:

  1. Proliferation or early hyperemic stage of the Graafian follicle with transformation of the granular cells into lutein cells.
  2. Early hyperemic stage of the corpus luteum with beginning transformation into the second stage of granular metamorphosis. The blood-vessels now permeate the layer of lutein cells.
  3. Mature or blossoming stage of the corpus luteum.
  4. Stage of involution.

Sometimes when the follicle ruptures it simply collapses, and hemorrhage does not always take place within it. The specimens studied by Meyer were increased in number and reported in relation to the menstrual cycle by Ruge II[11] who gives the following data:

Table 3

Table 3
Stage Number of Specimens Time of Occurrence in relation to Menstruation
Proliferation 10 1 to 14th day
Vascular 10 10 to 16th day
Mature 44 16 to 28th day
Involution 18 1 to 13th day

Table 4

Table 4
Stage Number of Specimens Time of Occurrence in relation to Menstruation
Proliferation 10 1 to 14th day
Vascular 10 10 to 16th day
Mature 44 16 to 28th day
Involution 18 1 to 13th day

Ovulation occurred in the stage of proliferation, and always during the first 14 days of the period. However, this stage does not form a regular sequence of development during the first two weeks, but the specimens were of unequal development and could not be arranged in the order of time. It is impossible to determine the time elapsing between ovulation and the formation of the third stage of mature corpus luteum, but Meyer and Ruge believe that always a number of days must intervene. finally, the stage of involution overlaps that of proliferation. At any rate the work of lVIeyer and Ruge demonstrates that the fresh corpus luteum as described by Fraenkel[12] appeared a number of days before he thought it did, thus completely overthrowing Triepel’s assumption that the probable time of ovulation is on the 19th day. According to Ruge, it occurs sometime during the first 14 days of the menstrual month which supports the theory I am advocating.

These are all the reliable data I have been able to collect regarding the time of development of the corpora lutea in human beings. I had thought that it would be possible to extend the subject somewhat further if the corpus luteum in the pig could be standardized in relation to the size of the embryo found in the uterus. This Work was carried through by Corner, but unfortunately does not include the earlier stages of the corpus luteum, and it is just these data that We need if We are to determine accurately the age of freshly ruptured Graafian vesicles. Corner[13] made a careful study of the histological changes in the corpus luteum of the sow for all but the earliest stages of pregnancy. He finds that the corpus luteum is already solid at 20 days, this stage being reached earlier, he believes, than in human beings Where this central cavity remains longer. By the aid of refined cytological methods he recognizes seven distinct stages during pregnancy as follows:

Table 5

Table 3
Stage Length of Embryo Approximate Age
1. Preparatory period Less than 20 mm. (?) 25
2. Exoplasrnic development (I) 20-30 25-30
3. Exoplasmic development (II) 39- 55 30—40
4. Transitory period 55-140 40-75
5. Endoplasmic development (I) 140-170 75—105
6. Endoplasmic development (11) 170—220 105-110
7. Retrogression 220-290 110 to term

Although this study cannot be transferred to the human directly, it at any rate suggests that the latter may be standardized. It is hoped to establish at least a relation between the early stages of the corpus luteum and the size of the ovum and embryo; and that in the course of time the age of this body may be estimated With precision.

It may be noted that Corner showed definitely that the size of the embryo found in the uterus could be estimated with considerable accuracy by the cytological condition of the lutein cells; however, all his specimens were from corpora lutea presumably a little older than the human ones mentioned above. In a measure we may fill in the gap in the earlier stages from the report by Sobotta[14] on the development of the corpus luteum in the mouse. He found in this study that during the first 24 hours after ovulation the cavity of the follicle fills with serous fluid or blood, at the time the lutein cells become cut up into compartments by the formation of connective tissue septi. This process continues during the following day or two, and finally the central cavity is nearly obliterated, containing, however, a central mucoid nucleus at the middle of the third day after ovulation.

The irregular summary from the several species is about as follows:

  1. In the mouse the central cavity of the corpus luteum is obliterated about the middle of the third day after ovulation;
  2. it is obliterated in human specimens accompanying ova about the size of those studied by Bryce and Teacher, and by Peters;
  3. it is obliterated in the pig considerably before the 25th day.

It may also be noted that Corner states that the corpus luteum of menstruation is of irregular shape in its development, while that of pregnancy is uniform and even. He speaks of the former as if the cells were arranged like a mob, and the latter as if organized like an army.

Finally, a few words regarding Fraenkel’s studies, out of which Triepel has made so much capital. According to Fraenkel, Villemin in 39 operations found no freshly ruptured follicles in the first two weeks after the menstrual period, but observed many from 12 to 14 days before it. Fraenkel himself describes hemorrhagic follicles as follows: Very fresh, fresh, quite fresh and not very fresh, showing that his average of 19 days after the last menstrual period is not the average time of ovulation, but the average of older corpora lutea in several stages of development. From a study of Fraenkel’s papers it may be seen quite clearly that what he reports as fresh corpora lutea are by no means necessarily fresh, but may possibly vary in age fully a week. In fact he intimates that they are not all fresh, and Triepel makes a slight allowance for this reason. These papers have been carefully analyzed by Grosser, who finally reached the conclusion that ovulation does not take place on the 19th, but at the latest on the 16th day after the beginning of menstruation. This figure is not so very far from the average given in my curve; in fact it is a little more than the average age accepted by Triepel as the normal according to the degree of development of the embryo. Triepel has attempted to force a curve which runs exactly 12 days after the average menstrual age of specimens, into one which should be exactly 19 days after this curve, in order to fit Fraenkel’s opinion regarding the proper time of ovulation. This of course is an impossible feat.

The conclusion to be drawn, therefore, is that we cannot possibly establish a satisfactory ovulation age of embryos from the data now at our disposal; but I believe that we have material within our reach whereby we may eventually be able to determine with greater certainty the probable time of ovulation. Before this can be done with the human, however, it will be necessary to study anew the degree of development of the corpus luteum for various days after menstruation, with new material selected from cases which are otherwise normal. This can be done in any large gynecological clinic.

Fertilization Age

According to Bryce and Teacher, the comparative infrequency of pregnancy during continuous cohabitation points to some special circumstance connected with successful impregnation. This "circumstance would appear to be simultaneous ovulation and limited power of fertilization on the part of the spermatozoa. As regards the former the work of J. G. Clark is of interest. According to this writer ovulation is accompanied with hypere— mia of the ovary, and, he believes, is hastened by it. He injected the blood vessels of an ovary in which there were fresh corpora lutea, as well as swollen Graafian follicles, and found that the injected fluid immediately ran out of the ruptured follicle. In a few instances the fluid entered mature follicles, causing them to become dense and finally to rupture when the vascular pressure was continued for a sufficiently long period. This suggests at least that a factor in fertilization is the rupture of a Graafian vesicle, due to orgastic reaction in the uterus,- tubes and ovaries when copulation takes place immediately after menstruation. At this time ovulation is most likely to occur in lower animals, and all the facts indicate that the same is true in human beings. It_ is known that in the rabbit, dog and pig there must be repeated copulation in order to insure impregnation. A single mating rarely suffices. Thus, for instance, according to Weysse,[15] only three out of the nine sows became pregnant after being covered but a single time. This would indicate that the fertilization power of the sperm was of short duration, as Bryce and Teacher seem to think is the case in human beings.

According to Waldeyer[16] live spermatozoa were found in the bitch eight days after copulation, and dead cells, that is motionless cells at the end of 17 days. Living moving spermatozoa were found in a woman three days after death. Living sperm cells were found -in the Fallopian tube of a patient 9 days after admission to the hospital and 3% weeks after copulation. On the other hand, spermatozoa have been found upon the surface of the ovary of the rabbit and sow two hours after copulation. In Waldeyer’s opinion the power to fertilize remains as long as the sperm cells retain normal motility, and there are no facts to deny that human sperm has the power to fertilize over a week after copulation.

Spermatic cells of animals that emit them into water die in a very short time if they are greatly diluted, and have a much longer life if only a little water is added. Thus in fertilizing trout eggs ‘dry’ sperm is used, while if the sperm is added to water containing the eggs but few eggs are fertilized. This question has been tested recently in Arbaeia by F. R. Lillie,[17] who makes the following interesting statements: The spermatozoa are absolutely immobile while they are in the body of the male, but become intensely active when suspended in sea-water. They then become relatively inactive, but can be restored again by the addition of fresh sea-water. VVhen greatly diluted they lose their fertilizing power completely in about an hour, and when diluted by 250,000 times their volume in water this power lasts but a few minutes. The loss of fertilizing power cannot be due to a loss of motility, for long after the former occurs no loss of vitality or motion is observed. In man the secretion of the prostate gland maintains the motility of spermatozoa much more effectively than does normal saline solution, and it is said that the secretions of the mucous membrane of the uterus and tubes have a similar influence. Thus it would seem that when motility is accelerated it does not indicate that the power to fertilize is prolonged, as asserted by Waldeyer. Lillie’s experiments certainly do not favor such a view, and Bryce and Teacher infer the same when they state that were the spermatozoa to retain for a long time their power of fertilization, no ovum could escape fertilization.

For the sake of argument Bryce and Teacher deduct 24 hours from the copulation age of their specimen (16% days) and estimate that it would have been 15% days old had it lived up to the time of abortion. This seems to me to be reasonable, as are the other statements in their admirable paper.

In View of the difference between the fertilization power of spermatozoa and their motility, as expressed in Lillie’s report, we may admit with considerable safety that the fertilization power of sperm is of shorter duration than is the power on the part of the egg to be fertilized. Furthermore, the theory that a fruitful copulation should be accompanied by ovulation at about the same time is a necessary one, in order to account for all of the combinations which are encountered in human beings. Nor is the assumption of Bryce and Teacher of an oestrus following menstruation untenable, and the possibility of a relation between orgastic reaction and ovulation is not to be overlooked.


Fig. 2 Cohabitation curve according to Siegel. The main division of the menstrual month and the probable time of ovulation are given. One hundred cases of pregnancy, occurring in the wives of soldiers after their husbands‘ furlough of one week. Each day of the furlough is entered as a possible day of conception. In all probability the 1st to the 4th day and the 18th to the 21st day belong to the sterile portion of the month.

An interesting study in this connection has been made by Siegel,[18] using the Wives of German soldiers as his subjects. These Women, who became pregnant during their husband’s furlough, game to the maternity hospital to be confined, and it was easy to obtain records of the menstrual, history as Well as the times of furlough, which in each case was of about a week’s duration. Figure 2, taken from Siege1’s paper, gives the result of the tabulation of 100 of such cases. Each day of the furlough is entered in the curve. Thus, if the furlough lasted from the 8th to 16th day of the menstrual cycle it was entered for each of these days.

it is noteworthy that there was no entry for the last seven days of the menstrual month, indicating that pregnancy did not take place either a Week before this nor within the week following; that is, there is a sterile period of about 18 days and a fertile period from the end of menstruation to the 15th day, which includes the probable time of ovulation. Of course only those cases which came to the maternity hospital could be recorded, and it is interesting to note that none of the 100 pregnancies dated from a furlough during the last week of the menstrual month. Such did not end in conception. Siegel was able to gather 10 cases in which the husband was on furlough a few days before the menstrual period, and in none did pregnancy follow. He cites further cases gathered by Wohler from the records of the same maternity hospital for the past ten years. These included 160 pregnancies among newly married women, in whom conception had occurred during the first five Weeks after marriage. Among this group there were 65 cases in which marriage took place within the eight days preceding the menstrual period, and in each of them one more menstruation followed, which fact alone would indicate a sterile condition during the Week preceding it. The records of Siegel, although not entirely satisfactory, demonstrate quite conclusively that the most probable time for conception is during the week or ten days after the period of menstruation.

From what has been written above we may, for the sake of argument, accept one day as the average time between copulation and fertilization. The time at which this is most likely to occur is between the 4th and 13th day after the first day of menstruation, as shown by the following table. This table is compiled from the records of our own cases, given above, each datum being obtained by subtracting the copulation age from the menstruation age. A similar result is obtained by dividing the total number of days by the number of cases, which equals exactly 13. That is, the average copulation date is the 13th day after the beginning of the last menstrual period. The figures upon which this result are based are not altogether satisfactory, but if the six cases given in the table are recorded, the average date is one day later; that is, the 14th. The figures of these cases are as follows:

Table 6

Table 6
Days between menstruation and copulation
1 2 3 4 5 6 7 8 9 10 11 12 1314 15 16 17 18 19 20 21 22 23? 25 26 27 28 30

No. of Cases....l10012j213\14 2 3 1 0 1 0 l IV3 2 1‘ 2‘0‘ 11C|~0{1 1 1 1 1 ‘

Table 7

Table 7
Author Length of embryo (mm) Time Between First Day
Menstruation and Copulation
Bryce and Teacher 0.15 22
Eternod 1 .3 13
Tandler 8.8 4
Rabl 14.0 18
No.1390 18.0 7
No. 26 25.0 19

In this group just half of the cases date from the first two weeks of the menstrual cycle, and the other half from the second two weeks. It is recalled that in over 1000 cases of full term births the mean as computed from the time of menstration and of copulation duration of pregnancy differed exactly 11 days, and that in my curve a difference of 10 days was taken. The theory of Bryce and Teacher and of Triepel is that fertilization takes place two days after copulation, and, therefore, they figure two days less than I did as the mean ovulation or fertilization age. Between these two theories I presume that we are within two or three days of the real age.

It appears to me probable that fertilization takes place nearly always within the uterine tubes - very rarely upon the surface of the ovary, as ovarian pregnancy is extremely rare; and probably also because the spermatozoa have lost their fertilizing power by the time they have passed the tube. No doubt this power is greatest in the tubes, as in these narrow channels the sperm would not be unduly diluted, but instead there would be a tendency to bring it together again. The ovum would probably be fertilizable for fully 24 hours after ovulation, this time being sulficient to bring it into the outer end of the tube. The following table gives the copulation age of the rat’s ovum, according to Huber, and of the dog’s, according to Bischoff. I have taken the measurements from their illustrations which are to scale. The third column gives the greatest diameter of the human ovum, with the length of the embryo in the 4th column. The second portion of the table gives the fertilization age for the third week, according to Bryce and Teacher and to Triepel. It will be seen that the former allows 48 hours for fertilization after copulation, a period of time Which, in my opinion, is abundantly long. finally Triepel’s column is practically identical with that of Bryce and Teacher.

Table 8

Table 8
Copulation Age Dog days Menstruation Age days

Age Eat , v - Human Embryo (}:§i'l:\?(il3rZl°1d . Age (1-luhei) (Bischofi) Ovum - Teacher) (rriepel) days mm. mm. mm. mm. mm. mm.

1 0.07 0.15
2 0.07 0.14
3 0.09 0.14
4 0.10 0.16
5 0.11 0.16
6 0.25 0.18
7 0.40 0.20
8 0.65 0.21
9 1.30 0.28
10 0.30
11 1.00
12 2.00
13 3.00
14 4.00 0.15 0.15
15 5.00 0.19 0.19
16 5.00 2.0 0.15
17 6.00 3.5 0.2 0.37
18 5.0 0.3 0.37
19 6.5 0.6 1.3 1.3
20 8.0 0.9 1.54 1.54
21 10.0 1.3 2.15

Literature Cited

  1. Keibel F. and Mall FP. Manual of Human Embryology I. (1910) J. B. Lippincott Company, Philadelphia.
  2. Mall FP. Report upon the collection of human embryos at the Johns Hopkins University. (1911) Anat. Rec., 5(7): 343–357.
  3. Triepel, A. 1915 Alterbestirnmung bei menschlichen Embryonen. Anat. Anz., Bd. 46, 1914. Also Bd. 48.
  4. Bryce TH. and Teacher JH. Contributions To The Study Of The Early Development And Imbedding Of The Human Ovum 1. An Early Ovum Imbedded In The Decidua. (1908) James Maclehose and Sons. Glasgow.Bryce TH. Teacher JH and Kerr JMM. Contributions To The Study Of The Early Development And Imbedding Of The Human Ovum 2. An Early Ovarian Pregnancy. (1908) James Maclehose and Sons. Glasgow.
  5. Clark JG. The origin, growth and fate of the corpus luteum as observed in the ovary of the pig and man. (1899) Johns Hopkins Hospital Reports, 7:
  6. Watt JC. Description of two young twin embryos with 17-19 paired somites. (1915) Contrib. Embryol., Carnegie Inst. Wash. 2: 15-54.
  7. Grosser, O. 1914 Alterbcstimmung junger menschlichen Embryonen; Ovulations und Menstruationstermin. Anat. Anz., Bd. 47.
  8. Herzog MA. A contribution to our knowledge of the earliest known stages of placentation and embryonic development in man. (1909) Amer. J Anat., 9(3): 361-400.
  9. Johnstone, R. W. 1911 Contribution to the study of the early human ovum. Journal of Obstetrics and Gynaecology of the British Empire.
  10. Meyer, R. 1911 Ueber corpus luteum—Bi1dung beim Meuschen. Archiv fur Gynaekologie, Bd. 93, 1911.
  11. Ruge II, Carl 1913 Ueber ovulation, corpus luteum and menstruation. Archiv fur Grynaekologie, Bd. 100.
  12. Fraenkel: Archiv fiir Gynaekologie, Bd. 91.
  13. Corner, George W. 1915 The corpus luteum of pregnancy; as it is in swine. Contributions to Embryology, vol. 2, Publication No. 223, Carnegie Institution of Washington.
  14. Sobotta. 1896 Ueber die Bildung des corpus luteum bei der Maus. Archiv fur Mik. Anat., Bd. 47.
  15. Weysse, Arthur Wisswald 1894 The blastudermic vesicle sus scrofa domesticus. Proc. Amer. Acad. Arts and Sciences, vol. 30.
  16. Waldeyer, W. 1906 Hertwig’s Handbuch der Vergleieh. und Exper. Entwickelungslehre der Wirbeltiere. Bd. 1, T1. 1, Erste Halfte.
  17. Lillie, F. R. 1915 Analysis of variation in the fertilizing power of sperm suspensions of Arbacia. Biol. Bull., vol. 28.
  18. Siegel, P. W. 1915 Warum ist der Beisehlaf befruehtend? Dent. Med. Woch.. 41.

Mall FP. On the age of human embryos. (1918) Amer. J Anat. 23: 397-422.

Cite this page: Hill, M.A. (2019, January 20) Embryology Paper - On The Age Of Human Embryos. Retrieved from

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