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vol.15 número1ANALISIS CUANTITATIVO DE LOS AXONES MIELINIZADOS EN LOS FASCICULOS GRACIL Y CUNEIFORME: ESTUDIO AL MICROSCOPIO OPTICOTRAYECTO DEL NERVIO GLUTEO INFERIOR ASOCIADO A LA DIVISION ALTA DEL NERVIO ISQUIATICO índice de autoresíndice de materiabúsqueda de artículos
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Revista chilena de anatomía

versión impresa ISSN 0716-9868

Rev. chil. anat. v.15 n.1 Temuco  1997

http://dx.doi.org/10.4067/S0716-98681997000100011 

ULTRASTRUCTURE OF THE VILLOUS FIBRINOID IN THE HUMAN FULL-TERM
PLACENTA

 

ULTRAESTRUCTURA DEL FIBRINOIDE VELLOSITARIO EN LA PLACENTA
HUMANA DE TERMINO

 

* Miguel A. Sala
** Maria Matheus
** Victório Valeri
* Ruberval A. Lopes

* Department of Stomatology (Pathology), School of Dentistry of Ribeirão Preto, SP, Brazil.
** School of Medicine of Ribeirão Preto, SP, Brazil.

 

SUMMARY: Fibrinoid material from human placental villi was studied by electron microscopy. Four constituents were identified in the fibrinoid substance: a homogeneous, amorphous matrix; microfibrils; cellular debris and calcified corpuscles. Microfibrils, showing no periodicity, were very abundant and irregularly arranged. Cellular debris derive, probably, from degenerated syncytiotrophoblast, whereas the calcified corpuscles are similar to the Michaelis-Gutmann bodies.

The present results suggest that fibrinoid material derives from both degeneration of the syncytiotrophoblast and synthesis by the residual Langhans cells and X-cells.

KEY WORDS: 1. Ultrastructure; 2. Full-term placenta; 3. Villous fibrinoid; 4. Human placenta.

 

INTRODUCTION

At the light microscope, fibrinoid material appears as a hyaline-like, homogeneous substance, stained pallid red by eosin, blue by Mallory’s phosphotungstic acid hematoxylin and strongly periodic acid-Schiff positive.

In the human placenta, the fibrinoid material is normally found in various regions of the intervillous chamber, such as the Langhans’ and Rohr’s strias, choriodecidual junction (Nitabuch’s stria), as well as in villi trunks and chorionic villi.

Villous fibrinoid substance is certainly one of the most characteristic histological features observed during placental organogenesis. Its identification can be considered an evidence of placental maturation (WISLOCKI & DEMPSEY, 1946; BOYD & HAMILTON, 1967; BURSTEIN et al., 1973).

In spite of the various differences demonstrated (ALTSHULER & ANGEVINE, 1949; KELLGREN et al., 1951; GLYNN & LOEWI, 1952; JOBST, 1954; WOLMAN & LAUFER, 1956), the distinction between fibrinoid material and fibrin from blood clotting is not unanimously admitted. Thus, BENIRSCHKE (1962) and WIGGLESWORTH (1969) use the term fibrin for both substances. On the other hand, the histological and histochemical features of placental fibrinoid material led GROSSER (1925), WISLOCKI & BENNETT (1943), HÖRMANN (1965), WILKIN (1965) and FOX (1968) to maintain the two terms.

Considerable controversy has also arisen over the origin of the villous fibrinoid material. Thus, WISLOCKI & BENNETT suggested that both mother and fetus contribute to the formation of fibrinoid material. Meanwhile, HÖRMANN and BOE (1967) favored the trophoblastic origin of the fibrinoid substance.

Although several histological and histochemical studies on the villous fibrinoid substance at the light microscopic level have been published, few comparable electron microscopic descriptions are available.

Thus, the purpose of the present paper was to describe the fine structural characteristics of the villous fibrinoid material in the human full-term placenta, with special emphasis on its origin.

MATERIAL AND METHOD

Six human placentas obtained by caesarean sections were used in the present study. All the cases were from uncomplicated full-term pregnancies that resulted in the birth of normal, live babies.

Tissue samples were taken from the subchorial region and marginal sinus, where the villous fibrinoid material is more frequent (SALA et al., 1982a). Small pieces of tissue were fixed immediately on recovery in 3 per cent glutaraldehyde in 0.1 mol/l phosphate buffer (pH 7.4), for 2 h, at 4ºC. After several rinses in 0.1 mol/l phosphate buffer, the specimens were postfixed in 1% osmium tetraoxide in 0.1 mol/l phosphate buffer (pH 7.4), for 2 h, at 4ºC and embedded in Araldite.

Sections, 1 µm thick, for survey by light microscopy, were cut and routinely stained with 1% toluidine blue solution at pH 10.5.

Ultrathin sections, 60 to 80 nm thick, were double-stained with uranyl acetate and lead citrate, and examined with a JEOL JEM-100C electron microscope.

RESULTS

Under the light microscope, villous fibrinoid material appears as a homogeneous substance stained

blue by toluidine blue. In early stages of villus degeneration, the fibrinoid material lies deep in the syncytiotrophoblast and external to the basement membrane. In more advanced stages, the fibrinoid mass gradually increases in size, whereas the syncytiotrophoblast overlying it undergoes atrophy and degeneration. Near the fibrinoid substance, the basement membrane shows increased thickness and the villous stroma frequently shows metachromasia.

A fully degenerated villus appears as a mass of fibrinoid substance with sparse peripheral syncytiotrophoblastic remnants and, sometimes, a scanty core of fibrosed stroma. Within the fibrinoid masses, it is often possible to find a group of round-shaped cells, with a central vesicular nucleus, showing a prominent nucleolus and basophilic cytoplasm, the so-called X-cells.

At the electron microscope, the placental fibrinoid material shows the following components:

1. A homogeneous, amorphous substance.

2. Very abundant microfibrils which display no periodicity, irregularly arranged (Fig. 1).

3. Cellular debris (Fig. 2), probably derived from degeneration of the syncytiotrophoblast.

4. Rounded or oval calcified corpuscles (Fig. 2).

The only cellular element present within the fibrinoid substance is the X-cell. These cells are typically roundish, with a few irregular microvilli, and a large vesicular and central nucleus, with prominent nucleolus. Their cytoplasm shows abundant microfibrils in the juxtanuclear region (Fig. 3), whereas a moderately developed rough endoplasmic reticulum and mitochondria are mainly located at the periphery. Desmosomes are frequently observed between adjacent X-cells.

Near the region undergoing fibrinoid degeneration, the trophoblastic basement membrane appears thickened and the villous stroma shows densely packed collagen fibrils.

The syncytiotrophoblast covering the fibrinoid masses frequently appears degenerated, with swollen mitochondria, myelin figures, and dense multivesicular bodies (Fig. 4).

Fig. 1. Placental fibrinoid material showing the microfibrillar compound (F). X 14,000.


Fig. 2. Placental fibrinoid showing cellular debris (D) and calcified corpuscles (C). X 14,000.

Fig. 3. X-cell with abundant microfibrillae (f). N: nucleus, m: mitochondria, r: endoplasmic
reticulum, d: desmosome. X 16,800 .

Fig. 4. Degenerating syncytiotrophoblast (S) covering the fibrinoid mass (F). X 8,400.

DISCUSSION

Fibrinoid substance appears as an amorphous mass within the trophoblast. More frequently, the fibrinoid material is located between the cytotrophoblast and syncytiotrophoblast (BOYD & HAMILTON) but it may be located also between the cytotrophoblast and the basement membrane (FOX). In the earliest stages of degeneration, the fibrinoid material is deposited deeply in the trophoblast, involving afterwards the basement membrane and encroaching upon the villous axis. In this manner, the fibrinoid is separated from the intervillous blood by a syncytial layer of trophoblast (BENIRSCHKE & KAUFMANN, 1995).

In later stages, the syncytiotrophoblast over the fibrinoid material undergoes degenerative changes and finally disappears. Degenerating syncytiotrophoblast shows pycnotic nuclei and cytoplasmic lysis, with swollen mitochondria, myelin figures and dense multivesicular bodies. Only after the disappearance of the syncytiotrophoblast, the fibrinoid does lie directly in contact with the maternal blood.

A frequent association between villous fibrinoid masses and thickening of the trophoblastic basement membrane was observed, as already described by ANDERSON & McKAY (1966) as well as SEN & LANGLEY (1974). This association, however, is not fully understood. According to McKORMICK et al. (1971) and SEN & LANGLEY, both fibrinoid deposition and thickening of the basement membrane may be manifestations of antigen-antibody reactions.

The calcified corpuscles observed within the fibrinoid material are morphologically similar to the Michaelis-Gutmann bodies (SALA et al., 1982b), that have been also related to immunological reactions. Similarly, BURSTEIN et al. claimed that the fibrinoid material is comparable with amyloid, which is recognised as one product of ageing and immune reactions.

The collagen fibrils of the villous stroma near the fibrinoid substance showed both ultrastructural and histochemical alterations similar to those observed in degenerating villi (WISLOCKI & DEMPSEY and ZACKS & BLAZAR, 1963).

WISLOCKI & BENNETT suggested three possible origins for the fibrinoid substance. According the present observations, the most probable among those possibilities is the trophoblastic origin by secretion and degeneration.

Both, the microfibrils and the amorphous components of the fibrinoid substance, appear to be synthesised by the residual cytotrophoblast and by the X-cells. Immunohistochemical evidences support the cytotrophoblastic origin and the secretory nature of fibrinoid (NANAEV et al., 1993). The cellular debris certainly derives from degeneration of the syncytiotrophoblast that covers the fibrinoid mass (FRANK et al., 1994).

The existence of desmosomes between adjacent X-cells supports the epithelial nature of these cells. Furthermore, by their ultrastructural characteristics, the most probable origin of the X-cells is from the residual cytotrophoblast of the chorionic villi.

It is possible to postulate that in the presence of a stimulus of a yet undefined nature, but probably related to circulatory disturbances, the residual cytotrophoblastic cell either synthesises or induces the synthesis of the amorphous and microfibrilar compound of the fibrinoid substance. With the increase of the fibrinoid masses, the residual cytotrophoblast cells progressively become isolated, receiving then the name of X-cells.

Thus, these cells show ultrastructural characteristics that resemble those of cytotrophoblast cells. Similarly, WYNN (1972) showed that the X-cells appear to be transitional in complexity from the undifferentiated cytotrophoblast cells to fully developed syncytiotrophoblast. Furthermore MAIDMAN et al. (1973) claimed that the X-cells display ultrastructural characteristics consistent with elements that are known to synthesise proteins for export or transport.

In conclusion, it is possible to assert that the villous fibrinoid substance is mainly secreted by the residual cytotrophoblastic cells and X-cells as consequence of metabolic changes probably induced by circulatory disturbances.

RESUMEN: El material fibrinoide de las vellosidades coriales humanas ha sido estudiado con el microscopio electrónico. Fueron identificados cuatro constituyentes en la substancia fibrinoide: una matriz homogénea, amorfa; microfilamentos; restos celulares y corpúsculos calcificados. Los microfilamentos no presentan periodicidad, son muy abundantes y se disponen irregularmente. Los restos celulares derivan, probablemente, del sinciciotrofoblasto degenerado, mientras que los corpúsculos calcificados son semejantes a los corpúsculos de Michaelis-Gutmann.

Los resultados obtenidos sugieren que el material fibrinoide deriva tanto de la degeneración del sinciciotrofoblasto como de la síntesis por las células de Langhans residuales y las células X.

PALABRAS CLAVE: 1. Ultraestructura; 2. Placenta de término; 3. Fibrinoide vellositario; 4. Placenta humana.

 

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Dirección para correspondencia:
Prof. Dr. Miguel A. Sala
Departamento de Estomatologia (Patologia)
Faculdade de Odontologia
Av. do Café s/n
14.090-904, Ribeirão Preto, SP
Brasil

Recibido : 26-12-1996
Aceptado:16-05-1997

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