THE SCHILLER-DUVAL BODY
This eponym was first used in a paper by Huntington et al. in 1963 titled “Germinal tumors exhibiting the endodermal sinus pattern of Teilum in young children” 9 (Fig. 6). When I last considered this matter 7 I was not certain that Huntington and colleagues introduced the eponym as they did in a somewhat understated manner in their paper, but it is now clear they did for the following reason. When preparing this work I read over many letters between Dr Teilum and Dr Aleksander Talerman who had a close friendship and interest in the yolk sac tumor 7 and in a letter to Dr Talerman dated 11th of September 1974 Dr Teilum writes as follows “As you know I dislike Huntington’s term ‘Schiller-Duval bodies’ since they are not bodies but histologic structures which occur in cross or longitudinal sections and it may cause a lot of trouble to introduce two eponyms, which in those connections will be incomprehensible for most pathologists.” His phrasing in the letter surely makes it clear that he attributed introduction of the eponym to Huntington and colleagues.
Dr Teilum disliked the eponym for other reasons. When I co-authored an essay on him a few years ago 3 I corresponded with Dr Reidar Albrechtsen, who worked with Teilum for several years and co-authored several papers on the yolk sac tumor with him 10–12. He informed me that Teilum did not like the eponym and pursuant to becoming aware of that I noted that in his writings he never used it. His dislike was because Dr Schiller’s interpretation of the neoplasm did not stand the test of time and of course Duval worked many decades before the yolk sac tumor became established and surely never saw one, working as he did in a completely different field. That notwithstanding, the die is cast as far as the eponym is concerned and although one can sympathize with Teilum’s reservations the embryological observations of Duval played a crucial role in Teilum giving the neoplasm the name applied to it for many years and although Schiller’s paper, based on what we now know is imperfect, the same could be said of numerous papers. The reservations just noted should not detract from the observations of individuals made based on knowledge at the time and which, albeit flawed, prompted the development of our knowledge in an area. Furthermore, despite a current trend to avoid eponyms I am in favor of them as they remind us of workers from prior times almost always in a pleasing way and in many circumstances label a tumor, formation, or entity of whatever kind, in a crisp manner that descriptive terminology would not readily accomplish. The author of one of two excellent books on eponyms in gynecology and obstetrics, Dr T.F. Baskett, begins his preface with a sentence with which I could not agree more “Despite misguided attempts to discourage them, eponyms continue to enrich the language and literature of medicine 13.”
Regarding the possible eponym “Teilum Tumor,” Huntington et al. 9 pointed out, quite appropriately, that it might be in their words “ambiguous” in view of the “range of this distinguished student’s interests” (referring to the breadth of Teilum’s contributions and knowledge). Despite the fame of the eponym that has come to be associated with Teilum’s tumor it is not considered in the two meritorious books on eponyms referred to above 13,14 although they focus primarily on clinical aspects and journal readers are surely as familiar with it as they are with another eponymous formation of neoplasia, the Call-Exner body or another one commemorating Schiller, the Schiller stain; the last two eponyms are included in the books just noted.
The first depiction of what we now know as Schiller-Duval bodies I have been able to find is in figure 4 of Schiller’s 1939 paper “Mesonephroma Ovarii” (Fig. 7 top) 5. In the legend he describes “small cystic spaces corresponding to glomeruli, each containing a capillary loop.” His figure 7 also shows a single Schiller-Duval body. It was his likening these formations to glomeruli that led him to feel that the neoplasms in his series were of Wolffian derivation. I have a slide of “mesonephroma” from Dr Schiller’s collection, conceivably a case from his paper (Fig. 7 bottom). It shows small cellular papillae with minimal stroma lacking a central blood vessel and therefore not according to Schiller-Duval bodies. That slide shows features of clear cell carcinoma. Schiller appears to have considered papillae as seen in that neoplasm and those seen in the yolk sac tumor in the one overall category of structures that were “glomerulus-like” and hence his conclusions that all the tumors in his report were mesonephric. In the next paper in the literature that appears to contain cases of yolk sac tumor, published the next year 15 all three reported tumors appear to have had Schiller-Duval bodies. In that study the formations were taken to indicate that the neoplasms were of vascular nature. Once his interest in the yolk sac tumor had taken hold Teilum very quickly clearly appreciated what we now know as Schiller-Duval bodies, commenting on and illustrating papillary formations with their features in his first paper on the tumor, in German, in 1943 16 and again in his first English language paper on it the next year 17. In the latter report Figure 1 shows in his words “characteristic perivascular cell mantles.” By that time he clearly felt that Schiller’s 1939 interpretation of the neoplasms as mesonephric was wrong. This theme was of course continued by Teilum over the years in his many papers on this topic and his book (Fig. 5) 18–23. In his paper in Cancer in 1959 (Fig. 5) 20 and his book he has a stunning plate which has illustrations of two Schiller-Duval bodies, one from an ovarian tumor and one from a testicular tumor, and for comparison two pictures of the endodermal sinuses of the rat placenta (Fig. 8). The similarities between the formations in the tumors and those of nature are striking. The frequency of findings Schiller-Duval bodies in the yolk sac tumor has varied in the literature. It was as high as 75% in the series of Kurman and Norris 24, predominating in 20% of the tumors. In a recent paper on testicular yolk sac tumors they were, however, seen in any number in only about 20% of the cases 25. My anecdotal experience with ovarian examples leads me to believe that they are not conspicuous in any more than about 20% of those neoplasms also. Irrespective of their exact frequency they are photogenic when seen and it is no surprise that they have been depicted frequently in the literature, including on one occasion gracing the cover of a book on germ cell tumors (Fig. 9 right) 26.
When commenting on the structure of the Schiller-Duval body (Figs. 1, 8, 10) it is surely appropriate to initially note the definition Dr Teilum himself provided in the first edition of his textbook 23, when referring to figures 95 and 96, low and high power views of Schiller-Duval bodies. He describes “groups of characteristic perivascular formations consisting of a mesodermal core with a capillary in its center and covered with a visceral layer of cylindric cells of epithelial appearance. The surrounding capsular sinusoid space is lined by a single-parietal layer of flat cells with prominent nuclei. The general patterns often resemble a complicated labyrinth of communicating cavities or channels with papillary processes and festoon-shaped configurations.” The term just used refers back to figure 23 of that work in which a drape-like appearance characteristic of festoon morphology is indeed depicted when many Schiller-Duval bodies are present but to a degree at least the plane of section imparts the festoon appearance. In my own opinion the resemblance to festoons is limited when the bodies are seen in classic form. Dr Robert Scully’s definition in his second fascicle 27 reads as follows: “They consist of single papillae that are rounded or elongated depending on the plane of section, with fibrovascular cores containing single vessels. Primitive columnar cells cover the papillae, which occupy spaces lined by cuboidal, flat, or hobnail cells.” Dr Scully had obtained, in late 1969, a rat placenta from which he had slides made enabling him in his first fascicle to illustrate its endodermal sinuses (see fig. 227 of that work).
While preparing this essay I reviewed six yolk sac tumors from Dr Scully’s collection in which Schiller-Duval bodies were particularly prominent and a routine hospital case of the same nature and make the following remarks based on my review of those cases (Fig. 10). There is of course little to add to the remarks of the two authorities whose descriptions were just provided. The low power appearance when many of these remarkable structures are present is striking (Fig. 10A). The cells covering the papillae are generally cuboidal (Figs. 10B, C). The flattened nature of the cells at the periphery of the space into which the papillae projects is much emphasized in the literature but is by no means always present. In addition, whether artifact-related or real, projection into a space is by no means invariable. The degree of dilatation of the central blood vessel is variable, usually being modest but occasionally striking; it may contain red blood cells or be empty. As others have noted, the appearance of the Schiller-Duval bodies varies from rounded (most common) to elongated (Fig. 10D) according to the plane of section. Most of the formations are of modest size. When they are small (Fig. 10F) it may be difficult to differentiate them from nonspecific cellular micropapillae seen in some yolk sac tumors but these do not have a blood vessel in the core of the papilla.
Issues in distinction of Schiller-Duval bodies from other formations are limited because of their distinctive features. The picturesque necklace pattern of the diffuse embryoma form of mixed germ cell tumor may occasionally produce a pseudopapillary pattern (see fig 1 in the paper of Cardoso de Almeida and Scully) 28, but those structures do not have a central core of mesenchyme within the papillae but rather a cavity. The embryoid bodies of the polyembryoma may appear at first glance in some situations to have a papillary nature (see fig. 3C of Stall and Young) 29. The resemblance is again only superficial but those not familiar with these unusual manifestations of germ cell tumors occasionally encounter some confusion in this regard and of course both the necklace pattern of diffuse embryoma and embryoid bodies may be seen in association with Schiller-Duval bodies as part of mixed germ cell tumors.
It would be inappropriate not to comment on Dr Robert W. Huntington Jr, the senior author of the paper in which the eponym Schiller-Duval bodies was proposed 9. With the invaluable help of several others (see Acknowledgments), I was able to get some information about him. He was born in 1907 in Hartford, Connecticut and graduated from Yale University School of Medicine (1933) where he interned. In the mid-1930s he moved to St. Louis and spent a year as Theron Catlin Fellow in Pediatrics at St. Louis Children's Hospital during which time he had a significant interest in infectious diseases. He moved to Los Angeles circa 1938 initially working at the LA County Hospital. He appears to have served in the United States Navy from 1941-1945. After the war he worked at Kern County General Hospital in Bakersfield, California and also had an academic affiliation with the University of Southern California School of Medicine beginning in 1946 and continuing until 1976. He attained the rank of Clinical Professor of Pathology. He was active in the California Tumor Tissue Registry and presented the fall seminar of that organization on “Tumors of General Pathology” in December 1970. Not surprisingly several of the 25 cases he presented were yolk sac tumors. He wrote a number of other fine papers on the yolk sac tumor 30–33 in addition to that giving birth to the eponym. Given his contributions on the yolk sac tumor Dr Huntington clearly was recognized as something of an authority on it. For example in one of the Clinicopathologic Conferences of the Massachusetts General Hospital (Case 34, 1969), in which Schiller-Duval bodies are depicted, Dr Robert Scully who presented the pathology references a personal communication with Dr Huntington concerning what was known about the prognosis of the yolk sac tumor at that time. Dr Huntingon died in 1989.
Given the thorough nature of the essay on Schiller authored by the late Dr John G. Gruhn and Dr Lawrence M. Roth 4 I will only briefly summarize his life and career based predominantly on it. He was born in Vienna in 1887 and as an undergraduate worked as a demonstrator in physiology for Exner, himself well known for being part of an equally famous eponym in gynecologic tumor pathology, the Call-Exner body. Schiller received his medical degree in 1912 and after military service in the First World War worked as a pathologist in a military hospital in Vienna and it was during those years that his studies of cervical cancer and development of what became known as the Schiller stain were undertaken. He had an active professional life doubtless meeting many leaders of European medicine of that era (Fig. 11). However in 1937 the political climate in Europe at that time prompted him to emigrate with his family to the United States where he first worked at Jewish Memorial Hospital in New York before moving in 1938 to Cook County Hospital in Chicago. It was during those early Chicago years that his report on “mesonephromas” appeared (Fig. 7 top) 5. In 1944 Hans Popper took over from Schiller as director of pathology at Cook County Hospital and Schiller then became director of laboratories for the Women’s and Children’s Hospital. Dr Schiller remained active throughout the early to mid 1950s until ill health gradually took its toll and he died in 1960. He was survived by his wife and 2 daughters, Esther and Susanne, whose daughter Lili provided material for this essay.
These remarks are almost entirely based on an outstanding essay by Drs R. Pijnenborg and L.Vercruysse published in 2006 6. They review in detail Duval’s work, including that of interest to us here 34,35 but I restrict my remarks here to brief notes on his life. Duval was born in 1844 in Grasse and studied medicine at the University of Strassbourg. His early work as an anatomist was undertaken there but interrupted by the Franco-Prussian War in which he served as an Army doctor. Thereafter he moved to Paris where he obtained a degree in physiology which the authors of the essay cited note was “the real beginning of an outstanding academic career.” He ultimately served in Paris as professor of anatomy and histology and wrote several textbooks on those topics. Pijnenborg and Vercruysse praised Duval for the quality of his descriptions and beautiful drawings and also note that he played a role in improving histologic techniques. As well as publishing the works already noted and his 600 page long work on the mouse and rat placenta 28, he published a book on Darwinism. It was the similarity of what Pijnenborg and Vercruysse describe as “intraplacental yolk sac extensions”—“the sinuses of Duval” and the papillary formations in the yolk sac tumor that of course link Duval with Schiller in the eponym. A reader interested in an elegant consideration of the endodermal sinuses of Duval may wish to read the comments on them by Gonzalez-Crussi 36.
The life and career of Teilum (Fig. 4) have recently been considered in detail this journal 3. He graduated in medicine from the University of Copenhagen in 1929 and trained in clinical medicine including forensic medicine before becoming a pathologist in the late 1930s. He worked at the Institute of Pathological Anatomy at the University of Copenhagen from the late 1930s through the rest of his career which continued in an active manner until close to his death in 1980. Although best known to readers of this journal for his work on the yolk sac tumor he was a very rounded pathologist with among other things a great interest in amyloidosis. His interests in the ovary extended well beyond the germ cell tumors and particular note should be made of his interest in sex cord—stromal tumors and their similarities with those of the testis. His stature as an authority on ovarian tumors resulted in him being one of the illustrious group who participated in the first World Health Organization Classification of ovarian tumors; he also served on the companion testis tumor group.
During the preparation of this essay Dr Schiller’s granddaughter provided some correspondence between him and Dr Teilum. Most of it concerns the issue of their different understandings of the tumor they had a shared interest in. It was of a very professional cordial nature. Dr Teilum visited with Dr and Mrs Schiller in the early summer of 1948 at which time their differing opinions would have been well known to one another. A letter Dr Teilum sent to them when he had returned to Denmark reads in part “I beg you and Mrs. Schiller to receive my most hearty thanks for the pleasant time I had with you in Evanston and Chicago. I cannot tell you how much I appreciate the visit in your beautiful home and I am indeed very indebted to you for all your time and courtesy.” In another letter a year later Dr Teilum again thanks Dr Schiller and his wife and in that reference is made to Dr Teilum’s sending of a painting as a gift.
THE YOLK SAC TUMOR
As the Schiller-Duval body is such a well-known feature of the yolk sac tumor, it is appropriate to conclude which selected remarks on this remarkable neoplasm 37 and how it came to light. The first case that seems to be unquestionably in this group is a testicular example reported in 1910 38 and although other examples likely exist in the literature it was not until Schillers’s paper provoked Teilum’s interest that the neoplasm came to attention. Because of Teilum’s insightful observations Schiller’s “mesonephromas” are now considered to include cases of yolk sac tumor and in other instances clear cell carcinoma and Dr Robert Scully’s note card providing his interpretation of the 10 cases in Schiller’s paper bears this out (Fig. 12). As can be seen he thought two of the tumors were pure yolk sac tumors, one yolk sac tumor with a dermoid cyst and one yolk sac tumor as part of a malignant mixed germ cell tumor. He favored the diagnosis of yolk sac tumor in a fifth case. Notably, despite the title of the paper, one of the tumors was a vaginal primary occurring in the typical very young age group of that entity 39. Two of the remaining tumors were thought to be definite clear cell carcinoma and two probably in that category. Although the card illustrated implies he was not certain about the final case his notes on the paper itself indicate he felt it was likely clear cell carcinoma and my review of the illustration of it (fig. 20 of Schiller’s paper) would indicate an almost certain clear cell carcinoma diagnosis. In essence there was 50/50 split between clear cell carcinoma and yolk sac tumor in Schiller’s series. As is not surprising given what we now know, the five cases of yolk sac tumor occurred in young people (oldest 26 yr) whereas the clear cell carcinomas occurred in an older age group (youngest 38 yr). One other comment of mild historical interest is that figure 1 of his paper shows typical hobnail cells of clear cell carcinoma, but he refers to them as “button-like.” It was only a little later in his writings on this topic that he introduced the now famous hobnail cell terminology.
Teilum first noted that some of Schiller’s cases resembled a pattern of neoplasia he had observed in testicular tumors which we would now classify as mixed germ cell tumors with a yolk sac tumor component. My knowledge of Dr Teilum’s proposing the name “endodermal sinus tumor” for the yolk sac tumor is based on information passed onto me by Dr Scully who informed me, as I note elsewhere 7, “in the mid 1950s Dr Teilum visited an embryologist in Paris who was working on the rat placenta and he shared with Teilum slides of that organ that contained structures referred to as endodermal sinuses first described by Duval in 1891. Teilum was struck by the resemblance between their appearance and the papillae in the tumor he was interested in and that resulted in him settling on the designation ‘endodermal sinus tumor’”. He had first 16,17 referred to the tumor based on the papillary formations as “adenopapilliferous epithelioma,” then for a brief period “gonocytoma 18,” before for a decade or so until the mid 1950s calling them “extraembryonic mesoblastoma” 19 the latter used in the first large study of ovarian examples reported by other workers, Santesson and Marrubini 40. Even other terms were used for testicular examples as summarized by Nogales et al. 36. It was only circa 1965 that the designation endodermal sinus tumor, used in arguably Teilum’s single best paper 20, was replaced by the broader designation “yolk sac carcinoma” or “yolk sac tumor” and although he accepted the new terminology he did so somewhat reluctantly. Nogales has reviewed the development of the now well-known designation 37,41 so I do not repeat it here other than to note the following. The name yolk sac tumor came to be seen to be preferable for several reasons, one being that the pattern that resembles the endodermal sinuses of the rat placenta is only one of many the tumor may exhibit and is much less common than the more typical reticular-microcystic pattern. Also, and importantly, the resemblance of its epithelium to that of the normal yolk sac gradually became clear and the demonstration, first using immunofluorescence and quickly thereafter immunohistochemistry by, among others, Teilum and associates in 1974 10 settled that matter. Immunohistochemistry was soon applied on a relatively large series of cases of yolk sac tumor by Kurman and Norris 24, confirming the initial observations on smaller numbers of tumors. The book of Nogales is an invaluable source of information on the yolk sac tumor (Fig. 9, left) and among many other things reviews the experimental work of G.B. Pierce and colleagues on this topic.
Teilum’s writings and other excellent contributions such as that of Kurman and Norris made the yolk sac tumor much better known by the late 1970s than in earlier times. Attesting to that is the fact that Dr Scully’s files from earlier years contain many more cases of yolk sac tumor than seen in later years, presumptively because as time went by pathologists became more familiar with the neoplasm and less often needed a second opinion. While this essay was in preparation Dr Kurman told this writer that seeing many cases with Dr Scully when a fellow with him in the early 1970s spurred the former’s interest in the tumor and led to him pursuing a study of them 24 when he, shortly thereafter, spent time at the Armed Forces Institute of Pathology.
The entire story of the yolk sac tumor and its grouping together with some cases of clear cell carcinoma in the category of “mesonephroma ovarii” became close to complete when, in 1967, Scully and Barlow presented convincing evidence that the clear cell carcinoma was a tumor of mullerian nature 42. The clear cell carcinoma itself has a somewhat checkered history and before the paper just noted others, particularly Dr Lars Santesson, had felt it likely a mullerian tumor but the contribution of Scully and Barlow “sealed the deal.”
During the years the yolk sac tumor and clear cell carcinoma were becoming established as the distinct entities we know today, there were periodic contributions on cases of “true” Wolffian tumors (mesonephromas). The validity of some of them was not always certain but the matter became more clarified in the early 1980s in part because the earlier recognition of broad ligament tumors almost certainly of Wolffian derivation by Kariminejad and Scully 43 (the differential diagnosis of broad ligament tumors being much narrower) made it easier to conclude that ovarian tumors with the same picture where themselves of Wolffian derivation 44,45.
Gynecologic pathology contains within it many fascinating eponyms, some more warranted than others. Many have their own often fascinating stories but few are surely more intriguing than that of the Schiller-Duval body linking as it does two eminent pathologists with a distinguished anatomist who worked decades earlier, and a neoplasm, which is one of the most remarkable of all human tumors. It is a neoplasm about which we are still learning and readers will be well aware of the extent to which the spectrum seemingly encompassed under the rubric of “yolk sac tumor” has expanded in recent years. It seems appropriate to link the observation just made with one made by Dr Huntington when he revisited the matter (in 1972) 33 in an essay titled “Endodermal Sinus and Other Yolk Sac Tumors, A Reappraisal,” co-authored with Dr Weldon K. Bullock, long-time stalwart of the California Tumor Tissue Registry. That essay was in a special issue of Acta Pathologica et Microbiologica Scandinavica, honoring the 70th birthday of Dr Teilum. The authors wrote as follows “Just how broadly the concept of yolk sac tumor can appropriately be applied remains to be determined.” Their comment to a degree anticipated recent exploration concerning variants deemed to be under the yolk sac tumor umbrella but quite different for the most part from patterns elaborated by Teilum. Somewhat in accord with that is the recent proposal by an authority on these tumors, Dr F.F. Nogales who, with his colleagues, suggested that the designation yolk sac tumor itself might be revisited and replaced by the broader designation, primitive endodermal tumor 41. Time will tell on how the entire story of the yolk sac tumor plays out in the decades ahead but one thing surely certain is that the particular papillary formations containing vessels within them will forever be referred to as “Schiller-Duval bodies.”
Writing on the Schiller-Duval body obviously prompted reflections on the pathologist memorialized by the first portion of the eponym, Dr Walter Schiller and fortuitously, soon after I decided to write this essay I became acquainted with Dr Schiller's granddaughter Ms. Lili Fiore. She kindly provided many interesting pictures two of which are included, and some information about him not previously known to me. Ms. Diane McElroy, Assistant Director of the California Tumor Tissue Registry was most helpful to the author in attempting to obtain information on Dr Robert Huntington and providing information on the California Tumor Tissue Registry, including drawing attention to Dr Huntington's presenting the Fall 1970 seminar. Dr Clive Taylor of Los Angeles generously worked on getting information on Dr Huntingon as did Ms. Jo Gallo of Kern School of Medicine, USC, Dr Lawrence Roth of Indiana University School of Medicine and Dr James Wright of Calgary; they collectively provided the information I have on him here. Dr Robert J. Kurman shared with me comments of interest with regard to his 1976 paper and overall interest in the yolk sac tumor. I thank Dr Reidar Albrechtsen of Copenhagen for information based on his work with Dr Teilum. Finally, material of the late Dr Aleksander Talerman generously donated to me by his widow Margaretha, was helpful in preparing the essay and led the writer to find one particularly interesting letter mentioned in the essay; it also contained a slide of “mesonephroma” from Dr Schiller’s collection.
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Keywords:©2019International Society of Gynecological Pathologists
Schiller-Duval body; Mathias Duval; Walter Schiller; Gunnar Teilum; Robert W. Huntington Jr; Yolk sac tumor