Paper - The Trophoblast - A Rejoinder (1904)

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Hubrecht AA. The Trophoblast: A Rejoinder. (1904) Science. 1904 Sep 16;20(507): 367-70. PMID 17734040

A.A.W. Hubrecht and the naming of the trophoblast. (2013)
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Trophoblast cells do not contribute cells directly to the embryo, but have important roles in implantation and placentation. For current information about these cells see the Trophoblast page.

Here is also the abstract from a recent paper by Pijnenborg and Vercruysse that discusses the historic introduction of the term "trophoblast" by A.W.W. Hubrecht in 1889.

Pijnenborg R & Vercruysse L. (2013). A.A.W. Hubrecht and the naming of the trophoblast. Placenta , 34, 314-9. PMID: 23395301 DOI.


"The term 'trophoblast' was introduced in 1889 by the Dutch embryologist A.W.W. Hubrecht during his study of early postimplantation stages in the hedgehog. He had selected this species because of its supposed relatedness to ancestral early mammals, which might provide clues to the evolution of viviparity. Although the new term referred in the first place to the nutritive activity of these cells, Hubrecht was well aware of other possible functions, including a protective role by their positioning at the interface between mother and conceptus. He also paid attention to the invasive activity of the trophoblast into the decidua, but was confused about the nature of the trophospongial layer of the placenta. Because of the structural analogy between early postimplantation stages in hedgehogs and humans, he speculated that, in contrast to other primate groups, anthropoids might have been derived from an evolutionary line separate from ancestral insectivore-like mammals. Although the latter idea has obviously become out of date, Hubrecht's writings provide a fascinating insight in the evolutionary thinking at that time, and therefore still merit a close study." Copyright © 2013 Elsevier Ltd. All rights reserved.
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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)

The Trophoblast: A Rejoinder


Hubrecht AA.

September 16, 1904.

The name Trophoblast was used for the first time by me in the meeting of the Anatomical Congress at Wiirzburg in 1888, and its earliest definition is found in the report of that meeting in Nos. 17 and 18 of the Anatomischer Anzeiger, Bd. III. "We there read, concerning a very early stage of the hedgehog (p. 510) :

”Die aussere Wand der Keimblase ist verdickt (drei bis vierschichtig) und besitzt wabige Lacunen. Fur diese aussere (epiblastische) Schicht sei der. Name Trophoblast gewahlt."

In a footnote we find in addition (p. 511):

”Es ist meiner Ansicht nach zweckmassig, sich bei der Saugethier-embryologie diesen Namen zu wahlen, um damit den nicht zum Aufbau des Embryos verwendet werdenden Epiblast anzudeuten * * *."

It is evident from the citations here given that the names outer epiblastic wall of the mammalian blastocyst and trophoblast are synonyms. Later researches have been directed towards the question how in other mammals than the hedgehog the separation between the epiblast of the embryonic shield, i. e., the formative epiblast and the trophoblast, comes about.

In the same Bd. III. of the Anatomischer Anzeiger, on p. 907, mention is again made of the hedgehog's ' geschlossene Tropho, blastblase (wie ich den primaren Epiblast, von dem sich durch Abspaltung der Epiblast des Fruchthofes nach innen abhebt, zu benennen vorschlug).'

Again, in the article on the placentation of Erinaceus in Vol. 30, Pt. 3 (1889), of the Quart. Joum. of Microsc. Science, where the definition was reproduced, it is insisted upon (p. 298) that "the use of the name trophoblast will render unnecessary such circumlocutory expressions as 'outer epiblastic layer of the blastocyst,' 'primitive exochorion,' etc." Further argumentation on p. 299, in which the allantoidean and the omphaloidean trophoblast is defined, leaves not the faintest doubt as to what the name trophoblast has originally . stood for.

Five years later (1894), in an article, 'Spolia nemoris,' which appeared in Vol. 36 of the, Quart. Joum. of Micr. Science, I again insisted (p. Ill) that 'new and valid reasons are thus accumulated for designating the outer layer of precociously segregated epiblast cells that form the wall of this vesicle" [the early mammalian blastocyst] by a separate name, [for which] I have proposed the name of trophoblast.' Somewhat further is added (p. 112) : 'in Tupaja and Tarsius portions of the trophoblast undergo very active proliferating processes preparatory to the placentary fixation of the blastocyst, whereas in my former papers I have described the same activity for Erinaceus and Sorex.'

Finally, in 1895 (Verhandl. der Eon. Akad. v. Wetenschappen te Amsterdam, Vol. IV, No. 5, p. 18), I reafirm that:

”die von mir. Trophoblast genannte Keimschicht ist * * * die aussere schicht der Saugethierkeimblase welche vor der definitiven Ausbildung des formativen Epiblastes dieses sowie die Hypoblastanlage umhiillt und an der Bildung des Embryos iiberhaupt keinen Antheil nimmt.”

In this last paper I have for the first time asserted that in my opinion the Sauropsidan arrangement, as well as that of the Ornithodelphia, can not possibly be looked upon as ancestral to what we find in the monodelphic (and didelphic) mammalia and that, on the contrary, the trophoblast (I. c, p. 57, No. 7) is a precociously segregated .larval envelope which encloses an inner cell mass, out of which the embryo is going to be built up. I have at the same time drawn a comparison between the mammalian trophoblast and the 'Deckschicht' in amphibian development and have also drawn attention to those cases where remnants of a trophoblastic layer could be detected in the Sauropsida.

Only in 1902, however, have I gone yet further back, and leaving the recent amphibia out of the ancestral line, I have attempted to draw a comparison between the trophoblast (and the other foetal membranes coexistent with it) of the Amnio ta and larval envelopes of invertebrate predecessors (Verhandl. der Kon. Akad. v. Wetenschappen te Amsterdam, Vol. VIII., No. 6, 1902, p. 53). Alinea! It has now been shown that since the first introduction of the name trophoblast sixteen years ago my own definition and interpretation of it has not undergone any alteration, although advances have been made in the appreciation of its theoretical significance.

And it is for this reason difficult for me to understand that the name has been misunderstood both by embryologists and by gynaecologists, even to such an extent that the writing of the present article seems necessary to prevent further confusion.

So, for example, Charles S. Minot's definition of the trophoblast on p. 100 of his 'Laboratory Text-book of Embryology' (1903) as 'a special layer of cells developed on the outer surface of the ectoderm of the mammalian blastodermic vesicle' is both wrong and misleading. Several statements in the same paragraph on p. 107, e. g., that the trophoblast is sometimes developed only later; that it disappears when the placenta is being formed, etc., are likewise in complete disaccordance with the original definition, such as it was substantiated by the different quotations given above.

In attempting to explain for myself how Minot can have fallen into this error — from which consultation of the papers above quoted would have withheld him — I can not but suppose that Bonnet's 'Grundriss der Entwickelung der Haussaugethiere ' must have led him astray. . In this we find on p. 31 a woodcut (Pig. 17), in which the trophoblast (Bonnet's primarer Ectoblast) is represented as a separate layer outside of the ectoderm of the monodermic blastocyst of the hedgehog and which woodcut is marked 'nach Hubrecht,' although I never published anything of the kind, nor in my writings have ever, as we have seen above, given the slightest justification to an interpretation so entirely inconsistent with my own views which have repeatedly been expressed without any ambiguity. Already on p. 19 of my paper of 1895[1] have I called attention to the fact that Bonnet's woodcut was a misrepresentation of my own views and have on Plate IV., Pig. 81, reproduced a hardly known figure of Kolliker's of the rabbit's blastocyst, which, on the contrary, is in complete accordance with those views. Misrepresentations, however, are hard to kill.

In Hertwig's 'Handbuch der vergl. Entwickelungslehre der Wirbelthiere' (Bd. I., S. 917) and in Weber's ' Saugethiere ' (S. 284) similar transpositions of my intentions in insisting on the recognition of a distinct trophoblast have not crept in. I cite from Hertwig:

”Die verschiedene Entwickelung der Trophoblastes hat Hubrecht in folgenden Satzen knrz zusammengef asst. " " Die von mir Trophoblast genannte Kiemschicht ist fur. die Anheftung des Saugethierkeimes an die miitterlichen Gewebe in erster Linie bestimmt : dabei entwickeln sich zu gleicher Zeit in der mannigfaltigsten Weise lokalisierte oder iiber die ganze Oberflache sich orstreckende Wucherungen, welche zur Ernahrung des Embryos dienen." "Der definitive formative Epiblast welcher als sogenannte Keimscheibe oder Embryonalschild auf der oberen Flache der Keimblase hervortritt, ist zur Zeit seines ersten Auftretens nie an der Oberflache gelegen, sondern immer von Trophoblastzellen iiberlagert.

“”Die Art und Weise wie diese Ueberlagerung des formativen Epiblastes durch Trophoblastzellen ein Ende nimmt, ist sehr verschieden; entweder entsteht zwischen Epiblast und Trophoblast ein persistierender Raum, welcher etwas spater zur Amnionhohle wird (Erinaceus, Arvicola), oder es tritt eine engere Verwachsung von den Epiblastrandern mit dem Trophoblast ein, worauf ein Durchbruch der deckenden Trophoblastzellen erfolgt, welche letztere spater zu Grunde gehen (Tupaja, Maulwurf, vielleicht auch Pledermaus und Schwein) oder endlich, es wird die trophoblastische Deckschicht oberhalb der Keimscheibe sehr erheblich abgefiecht, wodurch der formative Epiblast und der Trophoblast dem Anschein nach in engstem genetischem Verbande stehen, wahrend in Wirklichkeit der Verband zwischen dem peripheren Bezirk des Trophoblastes und sejnem als Deckzellenschicht zu bezeichnenden Abschnitt auch hier die primare, die anfanglich kontinuierliche Verbindungsweise gewesen ist (Lepus, Sorex.)" ' ' Der Entwickelungsgang kann eine Abkurzung erfahren, indem die Amnionhohle innerhalb eines vom Trophoblast verfriiht abgetrennten Epiblastzellenkorpers spontan erscheint (Cavia, Pteropus)." . I hope that these quotations may dispel eventual doubts about the significance of the term trophoblast.

I have now to consider the application of that term in gynaecology, more especially its application to the placentation of man and of other mammals. I find that its use has become more general with English and American than with German authors, and at the same time it would seem as if also in this case a tendency to misunderstand the real significance of the term has sprung up.

This tendency is very naturally explained when we consider how important a factor for the process of placentation the proliferation of trophoblast cells has been shown to be. This proliferation is especially very luxurious in man (Siegenbeek van Heukelom, Peters) in the hedgehog (Hubrecht), whereas in many other insectivora and rodents its multiform complications are exceedingly varied. In consequence many investigators have been led to believe that the name trophoblast was originally restricted to those proliferating 'regions, whereas we have demonstrated' above that this has never been so. Add to this that the proliferation of cells contributing to the formation of the placenta yet in another way is apt to lead to confusion because such proliferation is in no way limited to embryonic cells, but is also noticed— sometimes to a more considerable extent-^in maternal cells belonging to the epithelial lining of the uterus or to the subepithelial maternal tissues. In this way debates have arisen between Strahl and Liisebrink on one side and Duval, van Beneden and myself on the other, of which debates the object was to make out in how far the material of the proliferating placenta should be looked upon as maternal and in how far as embryonic, trophoblastic tissue.

These debates will no doubt, in the course of time, as the number of carefully observed cases increases, lead to a unanimous interpretation. As it was, I have myself, for sheer diffidence of attributing too prominent a part to trophoblastic proliferation (of which I was, nevertheless, together with Duval, the first advocate), in one case stopped short of the real solution, and have for the hedgehog restricted the extent of the trophoblast more than was necessary. Since then I have corrected this in a doctor dissertation of one of my pupils (Resink, 1903), but there is no doubt that I am myself thus responsible for a certain amount of vagueness and misrepresentation which has prevailed in the application of the term trophoblast to different placentas, more particularly of man and the monkeys, where the question arose in how far certain syncytial tissues should be looked upon as maternal or as embryonic. Even for pathological anatomy this proved to be a momentous question in so far as the deciduoma malignum, if traced to remains of trophoblast cells, would be very different from other deciduomse, that found their origin in maternal tissue.

Now that the placentation of Tarsius, Tupaja, Sorex, Vespertilio, Cercocebus, Talpa, Qaleopithecus, Sciurus, Lepus, a. o., has been more carefully examined (trophoblastic proliferation having been figured by Selenka as early as 1887, for one of the Didelphia [Opossum] ), divergence of opinion will in a few years hence have been replaced by unanimity also on this head.

And then the application of the name trophoblast to those placental elements that arise from the embryonic layer originally designated by that name will be in no way confusing, but will, on the contrary, contribute to keep before our eyes the intimate relation between the facts as they take place under our eyes and their phylogenetic origin.

With perfect justification Strahl has protested (Hertwig's 'Handbuch der Entwickelungslehre der "Wirbelthiere, ' I., 2, p. 311) against a misapplication of the terminology, which I have attempted once more to explain in this article, when authors who have insufficiently studied the subject even go so far as to speak of a maternal trophoblast beside the embryonic !

I hope that this paper may henceforth render misinterpretations such as are discussed in it impossible.

A. A. W. Hubrbcht.

University of Utrecht.

  1. Verhandel. Kon. Akad. Amsterdam, Vol. IV., No. 5.

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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)

Cite this page: Hill, M.A. (2024, June 24) Embryology Paper - The Trophoblast - A Rejoinder (1904). Retrieved from

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