Book - Contributions to Embryology Carnegie Institution No.1-2

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I have decided to take early retirement in September 2020. During the many years online I have received wonderful feedback from many readers, researchers and students interested in human embryology. I especially thank my research collaborators and contributors to the site. The good news is Embryology will remain online and I will continue my association with UNSW Australia. I look forward to updating and including the many exciting new discoveries in Embryology!

Mall FP. On the fate of the human embryo in tubal pregnancy. (1915) Contrib. Embryol., Carnegie Inst. Wash. Publ. 221, 1: 1-104.

   Fate of the Human Embryo in Tubal Pregnancy: Introduction | Acknowledgments | Tubal pregnancy with normal embryos | Tubal pregnancy with pathological embryos | Tubal pregnancy with pathological ova | Fertility and sterility | Implantation in tubal pregnancy | Normal implantation in uterus | Normal embryos in the tube | The trophoblast | Normal embryos from 6 to 9 mm in length | Normal embryos over 9 mm long | Conclusions regarding normal implantation | Pathological embryos in tubal pregnancy | Pathological ova in tubal pregnancy | Degeneration of villi and chorion | Summary | Cause | Normal implantation | Tubal pregnancy containing pathological embryos | Pathological ova | Addendum | Description of the individual specimens | Bibliography of papers cited | Explanation Plates 1, 2, and 3
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Fertility and Sterility

It has been repeatedly observed that the larger number of tubal pregnancies are found in women who are mothers, but who have not been pregnant for a number of .years, or in women who have been married for a relatively long time but who have never been pregnant. It is also well known that tubal pregnancy frequently occurs in women who have been treated for salpingitis. In fact, Engstrom operated four times for tubal pregnancy on women who had been treated for salpingitis on the same side on which the pregnancy was found. These data point very decidedly toward a causal relation between an acquired inflammatory process and tubal pregnancy.


According to Ahlfeld (Lehrbuch der Geburtshulfe, Leipzig, 1903) tubal pregnancy is due to obstructions in the tube lumen which arrest the ovum in its passage to the uterus. These abnormalities in the tube frequently follow inflammation of the perimetrium, which explains the greater frequency of tubal pregnancy in women who have already borne children. The adhesions around the uterus produce a kinking of the tube and a catarrhal inflammation of its lining membrane.


Ahlfeld states further that tubal pregnancy is relatively more frequent in large cities. This may be due partly to the fact that the patients have freer access to good surgeons, but also to the higher percentage of gonorrhea is these communities. Thus, during a period of 16 years, Ahlfeld observed only two cases of tubal pregnancy in his clinics in Giessen and Marburg, and that this was not due to faulty diagnosis is proved by the fact that gynecological patients often remained in his clinics for long periods of time and he frequently opened the abdominal cavity for other reasons; furthermore, no case of tubal pregnancy came to autopsy. Most of his patients came from country districts, and Ahlfeld states that gonorrhea is of much rarer occurrence among the country people of Hesse than in large cities. Nevertheless, during the 5 years following those 16, with an increase of gynecological patients in Marburg, there was a marked increase of cases of tubal pregnancy. To what extent venereal diseases play a causal role in tubal pregnancy remains an open question, but this much seems to be certain: gonorrhea is at least one of the causes of the inflammatory changes which obstruct the tube-lumen and thereby favor the arrest of the ovum in its passage through the tube.


In all his wide experience Tait states that he never saw a case of unruptured tubal pregnancy (Lectures on Ectopic Pregnancy, Birmingham, 1888), and in fact he doubted very much whether a diagnosis could be made before rupture, although as early as 1710 Petit had maintained to the contrary. At the time Tait wrote tubal pregnancy was believed to be a rare disease and the peasant women around Marburg may not have gone to Ahlfeld's clinic for a minor complaint. Hence the condition may not have been recognized. Now that unruptured tubes are frequently removed and found to contain only a few villi, we must conclude that without operative interference many of the patients would get well. Again, sometimes tubal abortion occurs, and the ovum may degenerate, together with its encircling clot. Even with rupture, therefore, the disease may not prove fatal. All these possibilities must be taken into account in the further discussion and investigation of the causal relation of gonorrhea and tubal pregnancy.


In discussing the frequency of diverticula in the tube a difficulty arises from the fact that we possess no suitable standard to follow. Whenever the diverticulum is very pronounced as, for instance, when it can be found with a probe, where there is a double ostium, or when the uterine end of the tube is obliterated we could readily account for the arrest of the ovum in its passage to the uterus. However, in most cases of tubal pregnancy anomalies of this kind are not found, but instead we have inflammatory changes which have produced adhesions between the folds in the tube. As a result, there are produced numerous small pockets, any of which might be able to catch up the ovum. Unfortunately, so far we have never examined a specimen from a very early case of tubal pregnancy, and in the somewhat advanced cases the ovum is found not in the folds of the tube, but well implanted within the muscular wall. Hence it would seem that if the ovum is caught up in the small pocket it immediately proceeds to burrow into the tube wall, and later there is a secondary rupture into the tube lumen. This is the condition seen in our youngest specimen, No. 808.


The form of the tube lumen has been carefully studied by Kroemer in a single case. He cut serial sections of a tube which appeared to be normal. The specimen came from a multipara, 48 years old. To the naked eye the tube, which was 9 cm. long, seemed perfectly normal. It was hardened immediately in formalin and cut into serial sections 15/z thick. Reconstructions were made from three portions of the tube, from the interstitial portion, from the middle of the isthmus, and from the middle of the ampulla. Kroemer found that throughout its length the tube showed definite folds, beginning within the uterus and becoming more and more pronounced as the fimbriated end was approached; he also found a number of diverticula, some of which were quite pronounced. In fact, he is of the opinion that a third of all tubes will probably show such anomalies, and in view of their great frequency he believes that they are of little importance as the cause of tubal pregnancy. Under normal conditions the ciliated cells of the tube will carry the ovum over such a pocket or out of it in case it becomes lodged in one of them, provided only that there has been no previous inflammatory process to interfere with the action of the cilia. If the latter, however, do not act, normally, the ovum may be retarded in its progress and may have grown too large to pass through the uterine end of the tube when it reaches it, as most of the diverticula are in the ampulla. This explanation would account for the large percentage of pregnancies found in the outer portion of the tube.


Simple transverse folds of mucous membrane are to be viewed as normal structures and not as evidences of disease. They are to be found as the remnants of pseudo-follicular salpingitis. This condition can be recognized with the naked eye, for the individual folds are much less marked, having become matted together as a result of the inflammatory processes, the folds having become confluent. Nor does Kroemer believe that this condition is due to gonorrhea, because as a consequence of this disease there is a distention of the tube, with obliteration of the tube folds, and the entire wall of the tube becomes smooth, there being no formation of pockets. He states that chronic forms of gonorrheal inflammation show no anomalies of the folds of the tube wall, but that the ovum is retarded on account of the destruction of the ciliated covering. His ideas are based upon the theory that there is a normal stream of fluid passing through the tube to the uterus, that this stream is caused by the action of the cilia, and that, inflammatory conditions checking the stream, the ovum is not carried through the tube. Tubal pregnancies following gonorrheal salpingitis indicate that the process is healing. The ovum is carried partly through the tube because the healing process is not complete. In fact, there is a tendency to view follicular salpingitis as healing process.


Kroemer's description of a single case is very suggestive, but his conclusion rests upon evidence which this case can not give, for we have yet to know the extent and activity of the ciliated lining of the tube in question. He finds these pockets in a tube from a woman 48 years old, and because they appear to be normal he rules them out as a cause of tubal pregnancy. His paper, however, is valuable, as it gives us a better idea of the form of the entire tube than we possessed before. It remains to extend this work, as he himself suggests, to include the study of a great number of other tubes which are believed to be normal. Such a study should also consider the extent of the ciliated lining within the tube.


In my own collection no effort was made at first in the earlier cases to secure histories, but those with clinical histories which bear upon the subject are numerous and may be collected into three groups: those containing normal embryos, those containing pathological embryos, and those containing pathological ova.


In the first group, containing normal embryos, I find records regarding the number of children and their ages in 14 cases. The statement that a long period of sterility occurs before tubal pregnancy is fully borne out.


  1. No. 256. The woman was the mother of one child 8 years old.
  2. No. 426. The woman had had two children, 13 and 8 years old respectively.
  3. No. 456. One child 15 years old.
  4. No. 496. Last pregnancy 7 years previously.
  5. No. 503. Two children, the younger 3^ years old.
  6. No. 612. One child 8 months old.
  7. No. 657. Had been married twice and had had one child, 17 years old; otherwise had never been pregnant until this tubal pregnancy occurred.
  8. No. 667. This was the first pregnancy.
  9. No. 706. This is the fourth pregnancy after a mechanical abortion 5 years previously and another abortion 2 years previously.
  10. No. 728. This was the second pregnancy.
  11. No. 790. Had been married 7 years, but had had no previous pregnancy. Uterine and tubal trouble.
  12. No. 808. One child 2J years old.
  13. No. 898. Married 8 years; no previous pregnancy.
  14. No. 891. One child 3-J years old.


In the pathological embryos, the cases in which data are at hand regarding children are:


  1. No. 477. Was the mother of a child 1 year old.
  2. No. 478. Three children, the youngest 3 years old.
  3. No. 479. Two children and an abortion; pelvic trouble during the last 4 years.
  4. No. 685. Had been married 7 years, this being her first pregnancy.
  5. No. 697. Two children (ages not given) and four abortions. No history of uterine trouble.
  6. No. 729. Married 6 years, had had one child and two abortions, with a history of syphilis and probably of gonorrhea. There were marked morphological changes in the tube wall.
  7. No. 766. Had been married 7 years, this being her first pregnancy.
  8. No. 784. 41 years old, had been married 14 weeks, this being her first pregnancy. No history of venereal diseases, but a chronic inflammation of both tubes with pelvic peritonitis was found.
  9. No. 804. One pregnancy 3 years before.
  10. No. 846. Four pregnancies, the last 10 years before.
  11. No. 882. Previous abortions.


In the third group, in which there are no embryos, but degenerated ova, we have the following:


  1. No. 367. The woman had been married 14 years and had had 2 children, 11 and 12 years old.
  2. No. 488. Abortion 7 years before.
  3. No. 540. The woman had had one child, 10 years old. There was a history of chronic inflammatory pelvic disease since its birth.
  4. No. 553. Had had one child, 13 months old.
  5. No. 570. Had been married 15 months and had had one miscarriage 4 months later.
  6. No. 686. Had had one child, 11 years old. A history of pelvic inflammation. Tube wall was found inflamed.
  7. No. 720. Had had 7 children (the youngest 4 years old) and 6 abortions, 2 since birth of last child.
  8. No. 726. Had had one child, 5 months old, and an abortion 3 months after its birth.
  9. No. 754. Had had one child, 5 years old.
  10. No. 762. Had been married 6 years and aborted during the first year; otherwise never pregnant.
  11. No. 777. Had been married twice in 5 years, this being her first pregnancy. Her first husband had gonorrhea. A histological examination of the tube folds showed them to be matted together and inflamed.
  12. No. 787. Had been married 7 years, this being her first pregnancy. Histological examination showed marked follicular salpingitis.
  13. No. 794. 29 years of age, had had two children, 5 and 6 years respectively.
  14. No. 815. One child, 9 years old.
  15. No. 835. Two children, youngest 6 years old.
  16. No. 891. Youngest child 10 years old.
  17. No. 892. Youngest child 7 years old.


All of these cases in which histories are given point clearly towards a long period of sterility as well as toward infection before the tubal pregnancy occurred. At this place it may be well to cite in greater detail a very good instance bearing upon this point. No. 488 is a specimen from a case of double ectopic pregnancy, in which the tube from the second operation was sent to me. It contained a pathological ovum, 5 mm. in diameter. The woman was married in 1903 at the age of 21 years. The next year she had an abortion performed, after which she was troubled continuously with pelvic attacks, being treated for them and having in consultation a number of prominent physicians. Five years after the mechanical abortion she was operated upon for appendicitis, at which time it was found that the tube and ovaries were adherent. These were separated by the surgeon, who hoped thereby to bring about a condition to favor pregnancy, as the woman was anxious to have a child. A year later she was operated upon for tubal pregnancy. The other tube was found well matted together and would have been removed, had it not been for the woman's desire to have a child. The following year pregnancy took place in this tube, which contained the pathological ovum mentioned above. Examination of the specimen showed that the folds of the tube had become adherent, forming a follicular salpingitis. This seems to be a clear case in which the trouble may have arisen from the abortion which was performed 7 years before the second tubal pregnancy.

Implantation in Tubal Pregnancy

We have examined with care all the tube walls and as yet have never found any tissue that could be considered as the decidua, nor have we found any specimens of early implantation. Whenever we have encountered an ovum which was very small, it was invariably found separated from the tube wall by a definite layer of blood. It would appear that in these cases some time had elapsed since the implantation, which could hardly be accomplished without attachment of the ovum to the tube wall. For the present we must admit that the trophoblast often fastens itself to one of the folds of the tube and gets its nourishment from the adjacent venous sinuses, for which it seems to have a great affinity. In older specimens the trophoblast has eaten its way into the muscle wall and tapped blood-vessels, from which marked hemorrhages have taken place. In the uterus the formation of the decidua seems to aid in checking the hemorrhage by forming, as it were, a dam between the tips of the villi and eroded uterus upon which the trophoblast feeds, only a little of the blood passing this dam to enter the spaces between the villi. Nor do the trophoblast and syncytium at once become active as a result of the increased amount of nourishment. In general the trophoblast between the villi becomes necrotic and contracts into small yellow spherical masses about 1 mm. in diameter, which in turn are often eaten up by other syncytial cells. It appears therefore that in a normal condition of the chorion and uterus the trophoblast keeps the blood from entering the spaces between the villi. In the tube, however, there being no decidua, implantation must be effected by the trophoblast alone. The tube wall does not respond as actively as does the uterine wall. In the latter case implantation is aided by the production of the decidua. In the tube we must necessarily have more hemorrhage, and in studying the chorion one finds numerous hemorrhages between the villi, forming old blood coagula. The fibrinous substance is formed and the trophoblast makes every effort to implant itself in these clots. So we have a double process. The trophoblast has eaten into the tube wall, and at the same time is attaching itself to the clots of blood which have escaped into the lumen. We have every indication in specimens under 2 cm. in diameter of repeated hemorrhages into the lumen. They first form a series of clots around the chorion, fresher clots occur between the older ones, and finally there are delicate streams of uncoagulated blood upon which the ovum is nourished. The trophoblast spreads into long strands between the muscle cells of the tube wall and taps fresh blood sinuses. It spreads in old blood clots along fibrin strands, forming streaks of cells, which often extend several millimeters beyond the tips of the villi. Even the best of specimens frequently show such extensive hemorrhage around the chorion and such marked degeneration of the villi that it is a wonder that the ovum continues to grow normally. In fact, in the majority of cases the hemorrhage has rapidly detached it and it begins to degenerate. It collapses and grows in an irregular fashion, and if the specimen is not aborted into the peritoneal cavity it undergoes further and complete degeneration. Were not these specimens removed by surgeons, I think that in many cases spontaneous healing would occur. In some specimens we find a smaller organized clot with a very few fibrous villi scattered through it. Such a condition must be considered as a tubal pregnancy which has healed spontaneously.


Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)
   Fate of the Human Embryo in Tubal Pregnancy: Introduction | Acknowledgments | Tubal pregnancy with normal embryos | Tubal pregnancy with pathological embryos | Tubal pregnancy with pathological ova | Fertility and sterility | Implantation in tubal pregnancy | Normal implantation in uterus | Normal embryos in the tube | The trophoblast | Normal embryos from 6 to 9 mm in length | Normal embryos over 9 mm long | Conclusions regarding normal implantation | Pathological embryos in tubal pregnancy | Pathological ova in tubal pregnancy | Degeneration of villi and chorion | Summary | Cause | Normal implantation | Tubal pregnancy containing pathological embryos | Pathological ova | Addendum | Description of the individual specimens | Bibliography of papers cited | Explanation Plates 1, 2, and 3



Cite this page: Hill, M.A. (2020, August 15) Embryology Book - Contributions to Embryology Carnegie Institution No.1-2. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Book_-_Contributions_to_Embryology_Carnegie_Institution_No.1-2

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