Placenta
Volume 31, Issue 10 , Pages 848-852, October 2010

Hans Strahl’s pioneering studies in comparative placentation

  • A.M. Carter

      Affiliations

    • Cardiovascular and Renal Research, Institute of Molecular Medicine, University of Southern Denmark, 5000 Odense, Denmark
    • Corresponding Author InformationCorresponding author. Tel.: +45 6550 3716; fax: +45 6613 3479.
    • ,
  • A. Mess

      Affiliations

    • Department of Research, Museum of Natural History, Leibniz-Community, Berlin, Germany

Accepted 9 July 2010. published online 16 August 2010.

Article Outline

Abstract 

Hans Strahl, a contemporary of Duval and Hubrecht, made many important contributions to comparative placentation. Despite this he is not well known and some of his original observations tend to be attributed to later authors. Strahl published a classification of placental types based on their shape and relationship to maternal tissues. This greatly influenced the work of Otto Grosser, who became better known in part because his work was more accessible to other scientists and clinicians. Strahl described the development of the fetal membranes across a broad range of mammalian orders extending his observations beyond parturition to the post partum involution of the uterus. He paid close attention to structures designed for histotrophic nutrition including the areolae of moles, haemophagous organs of carnivores and tenrecs and chorionic vesicles of lemurs and lorises. We here provide a summary of some of the most important findings made by Strahl including work on placentation in carnivores and higher primates that remains unsurpassed.

Keywords: Carnivores, Chorioallantoic placenta, Choriovitelline placenta, Great apes, History of science, Insectivores, Ruminants, Tenrecs, Terminology

 

Back to Article Outline

1. Introduction 

The introduction of paraffin embedding by Edwin Klebs in 1869 [1] allowed thin tissue sections to be cut and stained. Other innovations included differential staining, the rotary microtome for creating serial sections, and improvements to the microscope such as the introduction of achromatic lenses. Together these technical improvements laid the groundwork for the rapid advances made by embryologists in the late nineteenth and early twentieth century. A.A.W. Hubrecht from Utrecht, Otto Grosser in Vienna, and Mathias Duval in Paris are names familiar to many scientists. In addition, J.P. Hill of London is among those acknowledged by students of marsupial placentation. Equally important, yet largely forgotten, are the contributions of Hans Strahl of Marburg and Giessen (Fig. 1). Strahl made several important discoveries in the realm of comparative placentation that often are credited to later workers. In an attempt to redress the balance, we highlight some of Strahl’s findings and assess his standing among contemporaries as well as his legacy. We have kept biographical details to a minimum as a full account is available elsewhere [1], [2].

Back to Article Outline

2. Early life 

Hans Strahl was born in Berlin in 1857. He lost his father at an early age and was raised by his mother and two close friends of the family; Rudolph Wagener and Nathanael Lieberkühn had the official status of adoptive father and legal guardian. In 1867, all four moved to Marburg where Lieberkühn and Wagener held academic appointments at the Institute of Anatomy. With this background it is perhaps not surprising that Strahl studied medicine and pursued an academic career. He achieved his habilitation at the remarkable age of 24 with a thesis on the early development of reptiles [3]. When Lieberkühn died, Strahl undertook to finish an uncompleted paper on the green border of the dog placenta [4]. Thus began a lengthy period of research on the comparative anatomy of the uterus and placenta. Strahl continued his work at Marburg until 1895, when he was called to the Chair of Anatomy at Justus Liebig University in Giessen.

Back to Article Outline

3. Placentation in carnivores 

Strahl completed and illustrated Lieberkühn’s paper on the green border of the dog placenta [4] which showed extravasation of maternal blood and uptake of the erythrocytes by tall, columnar trophoblast cells. Although he followed with papers of his own on dog [5], [6] and cat [7], and later described the placenta of an African civet (Civettictis civetta) [8], Strahl is best remembered for his work on the domestic ferret (Mustela putorius furo) [9], [10], [11]. He showed that the large blood-filled sacs of mustelid placentae are haemophagous organs equivalent in function to the green border of the dog placenta [10]. Although such organs had been described for the European otter (Lutra lutra) and other species by Bischoff [12], the latter erroneously thought they contained fetal blood.

A controversial view espoused by Strahl [7] was that uterine epithelium made an important contribution to the structure of the carnivore placenta. In light of the contrary opinion held by contemporary authors, including Duval [13] and Grosser [14] (see also [15]), he chose to revisit the issue in his later paper on the ferret [11]. The conclusion he reached was a compromise in which he envisaged both the uterine epithelium and the trophoblast contributing to the network of cells surrounding the maternal capillaries. More recent authors accept that the uterine epithelium of the ferret undergoes initial syncytialization, forming a multinucleate layer referred to as “symplasma” (e.g. [16]). However, contrary to Strahl [11], they regard syncytialization as a prelude to degeneration of this cell layer. There are multinucleated masses or giant cells close to the barrier that Wislocki and Dempsey [17] argue are maternal, but these are not thought to be epithelial in origin.

Back to Article Outline

4. Placentation in the mole and tenrec 

Early embryologists were interested in insectivores because they were regarded as mammals with many primitive traits. Hubrecht [18] chose to work with the European hedgehog (Erinaceus europaeus) in which development of the fetal membranes is quite difficult to follow as it is complicated by secondary interstitial placentation of the blastocyst. Strahl [19], [20] was more fortunate in choosing the European mole (Talpa europaea), where establishment of a yolk sac (choriovitelline) placenta followed by a chorioallantoic placenta is far easier to follow [21]. Among the special features described by Strahl [19] were the areolae (Plazentardrüse), which are thought to play an important role in histiotrophic nutrition of the embryo [22]. They are formed of columnar trophoblast above the openings of uterine glands (Strahl’s figure is reproduced in ref. [21]).

In addition, Strahl [8] described the placenta of the tail-less tenrec (Tenrec ecaudatus) collected on Madagascar by Alfred Voeltzkow. This paper appeared well before the better known description by Goetz [23], although the latter author certainly received better material from Hans Bluntschli. Strahl [8] was the first to describe the prominent haemophagous organ found at the centre of the placental disk and to characterize the presence there of crystals of haematoidin, a breakdown product of haemoglobin. He noted that in addition to the placental disk there was a more diffuse placenta and later used it to illustrate his terminology (see below).

Back to Article Outline

5. The villous placenta of the nine-banded armadillo 

Since human placenta is villous, with an intervillous space, it is familiar to students of medicine. Therefore it is often not recognized that this is an unusual placental form. Apart from higher primates, it occurs only in armadillos and anteaters. There the intervillous space is established in unique fashion by villi branching into pre-existing blood spaces in the uterine wall. This was first described by Strahl [24], [25], [26], [27] for the nine-banded armadillo (Dasypus novemcinctus) and Fernandez [28] for the Southern long-nosed armadillo (D. hybridus).

The armadillo membranes are familiar to many scientists through the recent work of Enders [29], [30], but there was much interest in the embryology of armadillos a century ago. Then as now the focus was on obligate twinning and discussion was fuelled by the work of Fernandez in Argentina (e.g. [31]) and Newman and Patterson in Texas [32]. An entertaining account of how this research depended on a regular supply of gravid armadillos is given by Garcia [33].

Back to Article Outline

6. The mesoplacenta 

In addition to armadillos, Strahl obtained and described some South American rodents. In Azara’s agouti (Dasyprocta azarae), he showed that the term placenta maintained only a tenuous connection to the uterine wall through a structure he called the mesoplacenta (Mesoplacentarium) [34]. This would later be described in greater detail by his pupil Hellmut Becher [35]. One of Strahl’s particular interests was involution of the uterus post partum [6], which was the starting point for his classification of placentation [36]. Many hystricognath rodents engage in post partum mating and Strahl [34] noticed that detachment of the mesoplacenta would result in little tissue damage and facilitate the early establishment of a new placenta. Analogous conditions were later found in relatives of the agouti such as the guinea pig (Cavia porcellus) [37]. The necrosis in the mesoplacenta observed by Strahl [34] would later be re-interpreted as an apoptotic process [38].

Back to Article Outline

7. Placentation in primates 

When Hill [39] reviewed placentation in primates little was known about the placentae of great apes and, indeed, this still is the case [40]. Hill [39] was, however, familiar with the work of Emil Selenka [41], [42], who had collected gravid uteri of gibbons and orangutans during an expedition to the Dutch East Indies. When Selenka died in 1902, his legacy was passed to a trio of authors that included the embryologists Hubrecht and Strahl. This resulted in an important publication by Strahl on the placenta of the gibbon (Hylobates sp.) and orangutan (Pongo sp.) [43]. Because later work has been mainly on delivered placentae, the papers of Selenka [41], [42] and Strahl [43] remain our best documentation that interstitial implantation with the formation of a decidua capsularis occurs in all the great apes. The accompanying histology is disappointing and focuses on the structure of the villous trees and fibrin deposition. No attempt was made to characterize the placental bed. Knowledge of trophoblast invasion in the great apes has emerged only recently and data on the orangutan is still needed [40].

In contrast to other primates, lemurs and lorises have epitheliochorial placentation. Once again some of the earliest descriptions of placentae from lower primates were those of Strahl. His paper on a member of Galagidae, the Northern greater galago (Otolemur garnettii) [44] was well in advance of the better known study of Galago demidoff by Gérard [45]. He showed that it had a diffuse, epitheliochorial placenta with chorionic vesicles fed by uterine glands. This was in accordance with contemporary observations on a member of Lorisidae, the slow loris (Nycticebus coucang) by Hubrecht [46]. Later Strahl [8] would extend these observations to two lemurs, Van der Decken’s sifaka (Propithecus deckenii coronatus) and the mongoose lemur (Eulemur mongoz).

Back to Article Outline

8. Placentation in ruminants 

In addition to lower primates, epitheliochorial placentation is found in many domesticated species and Strahl assembled an extensive collection of such placentae [47]. The most comprehensive study of placentation in ruminants [48] was based on this collection. Most ruminants have cotyledonary placentae, referred to as Semiplacenta multiplex in Strahl’s [36] classification, although the number of cotyledons varies greatly. Strahl [47] noted that there were important differences, too, in the number and structure of the villi between deer species on the one hand (red deer, Cervus elaphus; roe deer, C. capreolus) and domestic cattle (Bos taurus) and sheep (Ovis aries) on the other. There was similarly variation among the antelopes [47], as later addressed by Hradecky and co-workers [49]. Interestingly, chevrotains, which are considered to be primitive ruminants, have diffuse placentae. Strahl [50] was among the first to note this in his study of the Java mouse-deer (Tragulus javanicus). He used data on the mouse-deer and non-ruminants such as the domestic pig (Sus scrofa) to define his Semiplacenta diffusa [36]. A recent evolutionary survey reflects these findings: it regards the cotyledonary placenta as an apomorphic differentiation within Cetartiodactyla with two independent steps, i.e. a transformation to polycotyledonary forms in higher ruminants (Pecora) and to oligocotyledonary ones in cervids and moschids [51].

Together with Emil Gasser, who was a pupil of Lieberkühn and his successor at Marburg, Strahl built up an extensive collection of human embryological slides. These are preserved as the Gasser-Strahl Collection at the Anatomical Museum of Philipps University in Marburg [52]. The museum has additional slides dating from Strahl’s early studies on the development of non-mammalian vertebrates. Unfortunately for posterity, Strahl’s collection of placentae at Giessen was destroyed during an air raid in 1944.

Back to Article Outline

9. Terminology and legacy – Strahl’s influence on Grosser 

Our knowledge and classification of placentae is greatly influenced by the work of Otto Grosser [14]. Even recent approaches to placental evolution follow his classification [53], [54], [55], [56], [57], [58]. In contrast, recent researchers have overlooked the comprehensive review published three years earlier by Hans Strahl [36]. To better understand this discrepancy, we need briefly to contrast the aims, contents and methodical approaches of the two studies.

Strahl’s review [36] was a book chapter, “Die Embryonalhüllen der Säuger und die Plazenta” published in Hertwig’s “Handbuch der vergleichenden und experimentellen Entwicklungslehre der Wirbeltiere.” It was an extraordinarily broad, detailed and careful comparative survey both of the fetal membranes and their development and of the placenta in various mammals – including conditions in the human. Strahl recognized the overwhelming structural and developmental variability of these systems; discussed the methodical problems of getting proper material and gave extensive credit to the results and illustrations of previous authors – he provided figures only when particular taxa or stages had not been investigated before. Thus, readers of Strahl’s chapter had to cope with different styles and arguments within a largely descriptive study. As a key outcome of his survey, Strahl offered a new system of placental forms (Table 1), distinguishing between Semiplacenta (Halbplacenta) and Placenta vera (Vollplacenta). Only in the latter are maternal tissues including blood removed at or shortly after birth (Table 1). Though not explicitly mentioned, this distinction reflects different grades of invasiveness. Both Semiplacenta and P. vera include several subtypes according to the architecture of the feto-maternal unit in the definitive or term placenta (Table 1). In consequence, Strahl applied characteristics of different ontogenetic periods to his system, but without integrating the development of the fetal membranes. His order of placental forms was complex and rather complicated for practical usage.

Table 1. The placental classification of Hans Strahl, published in 1906 [36], based on characteristics of the term placenta and the condition at birth. Semiplacentas are usually non-invasive (epitheliochorial type of Grosser [14]), whereas placentae verae include medium (endotheliochorial) and highly invasive (haemochorial) forms.
TermCharacteristicsExamples
SemiplacentaMaternal blood vessels are not affected by birth
Semiplacenta avillosa (allantoid)Without villiPerameles
Semiplacenta avillosa (omphaloid)Without villiDasyurus
Semiplacenta diffusaVilli present all over the chorionic surfaceCetacea, Suidae, Equidae, Camelidae, Manis, Tapirus, Hippopotamus, Lemuridae
Semiplacenta multiplexVilli mainly concentrated into cotyledonsRuminantia
Semiplacenta zonariaRing-shaped location of villiDugonga
Placenta veraMaternal tissues including blood delivered or degenerate in situ at or after birth
Placenta zonaria simplexRing-shaped placentaCarnivora,b Pinnipedia,bHyraxc
Placenta zonaria compositaeRing-formed placenta, free villiLoxodontab
Placenta zono-discoidalisRing-formed placenta differentiates into a double diskMustelidae (Putorius)b
Placenta discoidalisDisk-like placenta (includes forms with one or two disks)Talpa,bErinaceus,cSorex,b Rodentia,cOryctolagus,cTupaia,bCynocephalus,c most Primates including Tarsius,c Chiropterab, c
Placenta perforataDisk-like placenta with a central blood spaceCentetesc

aAccording to Turner [63]; it is probably endotheliochorial.

bEndotheliochorial.

cHaemochorial.

The broader appeal of Grosser’s system [14] was due to a number of factors. First he provided a simple but convincing classification in relation to the function of the mature placenta, i.e. the interhaemal barrier or the layers of fetal and maternal tissue that nutrients need to pass through. Second, he addressed a core audience, physicians and medical students, and advertised his work as the first comprehensive study on the development of the fetal membranes and placentation with special reference to the human. Third, he included available data on comparative anatomy and ontogeny in mammals to formulate hypotheses on the unknown processes of early placentation in the human. This is a recognizably modern approach. Finally, Grosser provided excellent figures, all in the same style, even when results had been published previously. This procedure made his book a more useful work of reference than Strahl’s chapter.

To do him justice, Grosser did credit established ideas and explicitly mentioned Hertwig’s “Handbuch” and its authors R. and O. Hertwig, Schauinsland and Strahl as a principal source for comparative data. Grosser followed Strahl’s system in using Semiplacenta (Placenta apposita) and Placenta vera (Placenta conjugata) as major categories when presenting the diversity of placental forms in mammals ([14] pp. 95ff). However, he questioned the systematic value of Strahl’s concept:

“Wenn auch für die Systematik ebenso wenig brauchbar, hat diese Einteilung den Vorzug, dass sie nicht mit ihrem Einteilungsprinzip in Widerspruch gerät, in Fällen, wie z.B. bei den Nagern”. (“Even if not useful for systematics, this classification has the advantage that it is not in conflict with its own principles, e.g. in cases such as the rodents.”).

Grosser introduced and explained the placental subtypes provided by Strahl, but incorporated these ideas into his own concept, focusing on the histology of the functioning placenta and the basic implantation processes that lead to different conditions. As a result, only a simplified version remained ([14] pp. 104–188), comprising the Semiplacenta diffusa (pig) and Semiplacenta multiplex (ruminants) as well as the Placenta zonaria (most carnivores) and Placenta discoidalis (rodents, insectivores, bats, primates) as subtypes of the Placenta vera. In his conclusions, Grosser provided a phylogenetic ranking of the placental forms with special reference to the invasiveness of fetal tissues and the resulting number and structure of maternal layers in the feto-maternal unit: Placenta epitheliochoriales (S. diffusa), Placenta syndesmochoriales (S. multiplex), Placenta endotheliochoriales or angiotheliochoriales (P. zonaria) and Placenta haemochoriales (P. discoidalis). Consequently, the former Semiplacenta came to represent a non-invasive type1 while the two subtypes of P. vera represented the medium and highly invasive types. In addition, Grosser provided several links to original papers and special aspects of Strahl’s terminology.

Later influential reviews of placentation include those of Amoroso [59] and Mossman [60]. Amoroso had spent several years in Freiburg and Berlin and had mastered the German language. Thus, according to his biographer [61], Amoroso was one of few people in the English-speaking world who was acquainted with the details of work by Bischoff, Grosser, Reichert, Schauder and Strahl. It is thus significant that Amoroso [59] came down firmly on the side of Grosser and was rather dismissive of Strahl’s attempts at classification. Like Grosser, however, he referred extensively to Strahl’s original work and he cited a dozen of his publications. Mossman [60] likewise built on the Grosser classification; he acknowledged it was preceded by placental classification by shape but did not mention Strahl in this respect. Although Mossman referenced many of Strahl’s papers, he did not cite and very likely had not read the chapter in Hertwig’s Handbuch. Finally, Starck [62], in an influential German review, briefly referred to Strahl’s classification in Semiplacentae and Placenta verae but gave much greater prominence to the Grosser classification. It should perhaps be remembered that Strahl died in 1920 after spending his final years as an administrator; he was President of his University in the difficult years after World War I [1]. Grosser, on the other hand, lived until 1951 and was a dominant presence at embryological meetings in the years preceding the Second World War.

Back to Article Outline

Acknowledgements 

We are grateful to Strahl’s biographer, Dr. Hans-Rainer Duncker for sharing his insights into the life and work of this scientist. Dr. G Aumüller kindly showed one of us (AMC) the Gasser-Strahl Collection at Philipps-Universität, Marburg. We thank Dr. Rudolf Leiser for his help and encouragement. The portrait photograph was kindly provided by University Archives, Justus Liebig Universität, Giessen.

Back to Article Outline

Conflict of Interest 

The authors do not have any potential or actual personal, political, or financial interest in the information described in this paper.

Back to Article Outline

References 

  1. Duncker HR, Hans Strahl. (1857–1920) Anatom. In:  Gundel HG,  Moraw P,  Press V editor. Giessens gelehrte zweite teil. Marburg: Elwert; 1982;p. 939–954
  2. Henneberg B, Hans Strahl. Anat Anz. 1922;55:211–220
  3. Strahl H. Zur geschichte der Reptilienentwickelung. Ergeb Anat Entwicklungsgesch. 1894;4:505–541
  4. Lieberkühn N. Der grüne Saum der Hundeplacenta. Arch Anat Physiol. 1889;21:196–212
  5. Strahl H. Untersuchungen über den Bau der Plazenta. III. Der Bau der Hundeplazenta. Arch Anat Physiol Anat Abt. 1890;185–201
  6. Strahl H. Der puerperale Uterus der Hündin. Anat Hefte. 1895;5:336–399
  7. Strahl H. Untersuchungen über den Bau der Plazenta. IV. Die histologische Veränderungen der Uterusepithelien in der Raubthierplazenta. Arch Anat Physiol Anat Abt. 1890;118–134
  8. Strahl H. Beiträge zur vergleichenden Anatomie der Placenta. Abh Senckenb Naturf Ges. 1905;27:263–319
  9. Strahl H. Über die Plazenta von Putorius furo. Anat Anz. 1889;4:375–377
  10. Strahl H. Zur Kenntnis der Frettchenplazenta. Anat Anz. 1896;12:539–543
  11. Strahl H, Ballmann E. Embryonalhüllen und Plazenta von Putorius furo. Berlin: Verl der Königl Akad der Wiss; 1915;
  12. Bischoff TLW. Über das Vorkommen eines eigenthümlichen Blut und Haematoidin enthaltenden Beutels an der Plazenta der Fischotter (Lutra vulgaris). Sitzungsb Königl Bayerisches Akad Wissensch München. 1865;1:214–225
  13. Duval M. Le Placenta des Carnassiers. Paris: Félix Alcan; 1895;
  14. Grosser O. Vergleichende Anatomie und Entwicklungsgeschichte der Eihäute und der Placenta. Vienna: Wilhelm Braumüller; 1909;
  15. Lüsebrink FW. Die erste Entwickelung der Zotten in der Hundeplacenta. Anat Hefte. 1892;1:163–185
  16. Leiser R, Koob B. Development and characteristics of placentation in a carnivore, the domestic cat. J Exp Zool. 1993;266:642–656
  17. Wislocki GB, Dempsey EW. Histochemical reactions in the placenta of the cat. Am J Anat. 1946;78:1–46
  18. Hubrecht AAW. The Placentation of Erinaceus europaeus with remarks on the phylogeny of the placenta. Q J Microsc Sci. 1889;30:283–404
  19. Strahl H. Über den Bau der Plazenta von Talpa europaea und über Plazentardrüsen. Anat Anz. 1890;5:362–366
  20. Strahl H. Untersuchungen über den Bau der Plazenta. V. Die Placenta von Talpa europaea. Anat Hefte. 1892;1:113–161
  21. Carter AM, Enders AC. Placentation in mammals once grouped as insectivores. Int J Dev Biol. 2010;54:483–493
  22. Enders AC, Carter AM. Comparative placentation: some interesting modifications for histotrophic nutrition – a review. Placenta. 2006;27(Suppl. A):11–16
  23. Goetz RH. Studien zur Placentation der Centetiden. I. Eine Neu-untersuchung der Centetesplacenta. Z Anat Entwickl. 1937;106:315–342
  24. Strahl H. Über den Bau der Placenta von Dasypus novemcinctus. Anat Anz. 1913;44:440–447
  25. Strahl H. Über den Bau der Placenta von Dasypus novemcinctus II. Anat Anz. 1914;47:472–476
  26. Strahl H. Beiträge zur Entwicklungsgeschichte von Tatusia novemcincta L. Z Angew Anat Konstitutionsl. 1917;2:1–40
  27. Strahl H. Ein corpus cavernosum uteri. Anat Anz. 1917;50:65–70
  28. Fernandez M. Die Entwicklung der Mulita. Revista del Museum de la Plata. 1915;21:1–519
  29. Enders AC. Development and structure of the villous haemochorial placenta of the nine-banded armadillo (Dasypus novemcinctus). J Anat. 1960;94:34–45
  30. Enders AC. Implantation in the nine-banded armadillo: how does a single blastocyst form four embryos?. Placenta. 2002;23:71–85
  31. Fernandez M. Über einige Entwickelungsstadien des Peludo (Dasypus villosus) und ihre Beziehung zum Problem der spezifischen Polyembryonie des Genus Tatusia. Anat Anz. 1915;48:305–327
  32. Newman H, Patterson J. The development of the nine-banded armadillo from the primitive streak to birth, with special reference to the specific polyembryony. J Morphol. 1910;21:359–440
  33. Garcia SV. Local species, the market, and transportation in embryological research: the study of polyembryony in armadillos in the early twentieth century. Hist Cienc Saude-Manguinhos. 2008;15:697–717[online]
  34. Strahl H. Eine Placenta mit einem Mesoplacentarium. Anat Anz. 1905;26:524–528
  35. Becher H. Die Entwicklung des Mesoplacentariums und die Placenta bei Aguti (Dasyprocta azarae Schl.). Z Anat Entw Gesch. 1921;61:337–364
  36. Strahl H. Die Embryonalhüllen der Säuger und die Placenta. In:  Hertwig O editors. Hertwig’s Handbuch der vergleichenden und experimentellen Entwicklungslehre der Wirbeltiere. Jena: G. Fischer; 1906;p. 235–368
  37. Uhlendorf B, Kaufmann P. Die Entwicklung des Plazentastieles beim Meerschweinchen. Anat Histol Embryol. 1979;8:233–237
  38. Miglino MA, Carter AM, Dos Santos Ferraz RH, Fernandes Machado MR. Placentation in the capybara (Hydrochaerus hydrochaeris), agouti (Dasyprocta aguti) and paca (Agouti paca). Placenta. 2002;23:416–428
  39. Hill JP. The developmental history of the primates. Phil Trans R Soc Lond B. 1932;221:45–178
  40. Carter AM, Martin RD. Comparative anatomy and placenta evolution. In:  Pijnenborg R,  Brosens I,  Romero R editor. Placental bed disorders: basic science and its translation to obstetrics. Cambridge University Press; 2010;p. 109–126
  41. Selenka E. Entwickelung des Gibbon (Hylobates und Siamanga). In:  Selenka E editors. Menschenaffen (Anthropomorphae) Studien über Entwickelung und Schädelbau. Wiesbaden: CW Kreidel’s Verlag; 1899;p. 95–172
  42. Selenka E. Entwickelung des Gibbon (Hylobates und Siamanga) Fortsetzung. In:  Selenka E editors. Menschenaffen (Anthropomorphae) Studien über Entwickelung und Schädelbau. Wiesbaden: CW Kreidel’s Verlag; 1900;p. 173–208
  43. Strahl H. Primaten-Placenta. In:  Hubrecht AAW,  Strahl H,  Keibel F editor. Menschenaffen (Anthropomorphae) Studien über Entwickelung und Schädelbau. Wiesbaden: CW Kreidel’s Verlag; 1903;p. 415–491
  44. Strahl H. Der Uterus gravidus von Galago agisymbanus. Abh Senckenb Naturf Ges. 1899;26:155–199
  45. Gérard P. Études sur l’ovogenèse et l’ontogenèse chez les Lémuriens du genre Galago. Arch Biol. 1932;43:93–151
  46. Hubrecht AAW. Spolia nemoris. Q J Micr Sci. 1894;36:77–125
  47. Strahl H. Zur Kenntnis der Wiederkäuerplacentome. Anat Anz. 1912;40:257–264
  48. Andresen A. Die Plazentome der Wiederkäuer. Morphol Jahrb. 1927;57:410–485
  49. Hradecky P, Mossman HW, Stott GG. Comparative histology of antelope placentomes. Theriogenology. 1988;29:693–714
  50. Strahl H. Zur Kenntnis der Placenta von Tragulus javanicus. Anat Anz. 1905;26:425–428
  51. Klisch K, Mess A. Evolutionary differentiation of cetartiodactyl placentae in the light of the viviparity-driven conflict hypothesis. Placenta. 2007;28:353–360
  52. Grundmann K, Aumüller G. Geschichte der anatomie an der Philipps-Universität Marburg. 1992;http://www.uni-marburg.de/fb20/anatomie/pdf/geschichteanato
  53. Carter AM, Enders AC. Comparative aspects of trophoblast development and placentation. Reprod Biol Endocrinol. 2004;2:46
  54. Vogel P. The current molecular phylogeny of Eutherian mammals challenges previous interpretations of placental evolution. Placenta. 2005;26:591–596
  55. Mess A, Carter AM. Evolutionary transformations of fetal membrane characters in Eutheria with special reference to afrotheria. J Exp Zool (Mol Dev Evol). 2006;306B:140–163
  56. Mess A, Carter A. Review: evolution of the placenta during early radiation of placental mammals. Comp Biochem Physiol A Mol Integrat Physiol. 2007;148:769–779
  57. Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc Natl Acad Sci U S A. 2006;103:3203–3208
  58. Elliot MG, Crespi BJ. Phylogenetic evidence for early hemochorial placentation in Eutheria. Placenta. 2009;30:923–1004
  59. Amoroso EC. Placentation. In:  Parkes AS editors. Marshall’s Physiology of Reproduction. Volume 2:London: Longmans; 1952;p. 127–311
  60. Mossman HW. Vertebrate fetal membranes: comparative ontogeny and morphology; evolution; phylogenetic significance; basic functions; research opportunities. Houndmills, Basingstoke, Hampshire and London: Macmillan; 1987;
  61. Short RV. Emmanuel Ciprian Amoroso. Biogr Mem Fellows R Soc. 1985;31:3–3016 September 1901–30 October 1982
  62. Starck D. Ontogenie und Entwicklungsphysiologie der Säugetiere. part 22, 9(7) In:  Kükenthal W editors. Handbuch der Zoologie. volume 8:Berlin: Walter Gruyter; 1959;p. 1–276
  63. Turner W. On the placentation of Halicore dugong. Trans Roy Soc Edinb. 1889;35:641–662
  • 1 The Placenta syndesmochoriales in ruminants is characterised by areas with intimate association of fetal and maternal tissues (cotyledons), but without complete removal of the maternal parts. Nowadays, because of an intact maternal uterine epithelium in most areas of the placenta, this condition is usually included in the Placenta epitheliochorialis, a more precise description being Placenta synepitheliochoriales.

PII: S0143-4004(10)00264-X

doi:10.1016/j.placenta.2010.07.004

Placenta
Volume 31, Issue 10 , Pages 848-852, October 2010

Article Tools

* Image Usage & Resolution