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Gladstone RJ. and Wakeley C. The Pineal Organ. (1940) Bailliere, Tindall & Cox, London. PDF

   The Pineal Organ (1940): 1 Introduction | 2 Historical Sketch | 3 Types of Vertebrate and Invertebrate Eyes | Eyes of Invertebrates: 4 Coelenterates | 5 Flat worms | 6 Round worms | 7 Rotifers | 8 Molluscoida | 9 Echinoderms | 10 Annulata | 11 Arthropods | 12 Molluscs | 13 Eyes of Types which are intermediate between Vertebrates and Invertebrates | 14 Hemichorda | 15 Urochorda | 16 Cephalochorda | The Pineal System of Vertebrates: 17 Cyclostomes | 18 Fishes | 19 Amphibians | 20 Reptiles | 21 Birds | 22 Mammals | 23 Geological Evidence of Median Eyes in Vertebrates and Invertebrates | 24 Relation of the Median to the Lateral Eyes | The Human Pineal Organ : 25 Development and Histogenesis | 26 Structure of the Adult Organ | 27 Position and Anatomical Relations of the Adult Pineal Organ | 28 Function of the Pineal Body | 29 Pathology of Pineal Tumours | 30 Symptomatology and Diagnosis of Pineal Tumours | 31 Treatment, including the Surgical Approach to the Pineal Organ, and its Removal: Operative Technique | 32 Clinical Cases | 33 General Conclusions | Glossary | Bibliography
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The Pineal Organ - The Human Pineal Organ

Chapter 25 Development and Histogenesis

The stages in development of the derivatives of the primary ependymal elements of the brain and spinal cord, which we have described in Chapter 22, are of great importance in connection with the study of the structure of the fully developed pineal body. In the early phases of development it was shown by Cajal that the ependymal cells extend through the whole thickness of the wall of the neural tube, as is seen in Golgi preparations of the chick embryo at the third day of incubation. At a later stage, when the width of the neural tube has increased, there is a tendency for the central part or body of the cell, which contains the nucleus, to separate from its attachment to either the internal or the external limiting membrane, or it may lose its connection with both of these membranes. In the latter case the cell is said to be liberated, and it may form a branched neuroglial cell of the astrocyte or oligodendric type. In those cases in which the attachment of the inner end of the cell element to the internal limiting membrane is retained, the cell may develop into a definitive ependymal cell, lining either the central canal of the spinal cord or a ventricle of the brain (Fig. 261, a), whereas if the internal connection is lost (Fig. 261, c) and the cell body remains anchored to the external limiting membrane or to the glial membrane covering the pial sheath of vessels penetrating the substance of the brain or spinal cord, the cell may differentiate into a subpial astrocyte, e.g. the cells or fibres of Bergmann, in the molecular layer of the cerebellum, or into a fixed " vascular " astrocyte, as contrasted with the free unattached type, which appears to be connected by its processes with those of neighbouring astrocytes. Besides these three principal types, intermediate forms are frequent : thus, one large process of an astrocyte provided with an expanded foot-plate may preserve its attachment to the sheath of a vessel, while the other small branched processes appear in Golgi preparations to end in free extremities.


There is, however, a considerable amount of doubt as to whether the apparent continuity of the neuroglial cell-elements is a true uninterrupted connection of one glial cell with another, since many of the modern neurologists hold the view that both the glial cells and the nerve cells are independent units. The discussion of this interesting and fundamentally important problem presents many difficulties, and we do not propose to enter into the question here, since, apart from its general bearing on the structure of nervous tissue, it does not specially affect the study of the pineal organ ; for, whether the processes of the glial cells are merely in contact or are continuous with each other, there seems to be a functional continuity in the framework as far as support is concerned. At this point it will be necessary to refer to the view which was originally taken by His with respect to the origin of neuroglia cells and neuroblasts. He believed that the medullary plate is primarily formed of undifferentiated cells which give rise to " germinal cells " and " spongioblasts." The former in his opinion gave rise to neuroblasts and ultimately to nerve cells, whereas the spongioblasts developed into the supporting neuroglial tissue and ependyma. The germinal cells or the cells next the internal limiting membrane which are undergoing mitosis give rise to two daughter cells, both of which, he thought, migrated outward through the spongioblasts into the mantle zone, where they could be distinguished by their large size and pale vesicular nucleus, and were spoken of as " neuroblasts." Schaper, in 1897, contended that the germinal cells gave origin to both neuroblasts and spongioblasts, and that the indifferent cells which resulted from their division were capable of producing either neuroglia cells or nerve cells even after the outward migration of the indifferent cells from the internal limiting membrane had already occurred. Whether an actual migration of whole cells takes place or simply an outward movement of the nucleus along a protoplasmic strand which has grown out as a process from the body of the cell is a much debated question, but we are inclined to believe that the latter alternative is the correct interpretation of the changed position of the nuclei. The migration by amoeboid movements of microglial cells has, however, been definitely proved and recorded on cinematograph films.




Fig. 261. — Transverse Section through the Spinal Cord of a Ten-day Chick Embryo, showing the Supporting Cells. (After Lenhossek, 1895) a. : ependymal cell. c. : astroblast, or displaced epithelial b. : supportive spongioblast. cells.



It has been demonstrated by Cajal that at an early period of embryonic life the spongioblasts send out a process which on reaching the external limiting membrane expands into a conical swelling or foot-plate, while the inner end, retaining its attachment to the internal limiting membrane, develops one or more processes resembling cilia which project into the central canal or a ventricle of the brain (Fig. 223, Chap. 22, p. 322, and Fig. 261). The foot-plate at the outer end is in relation with the vessels of the pia mater outside the external limiting membrane, and it is believed that it serves to absorb material from the blood for the nourishment of the nerve tissue, for in the earlier stages of development the latter does not possess the rich blood supply which it has in late embryonic stages and in foetal life. In these later stages, when the central area of the nerve tissue has become vascularized, foot-plates are developed on those processes of the neuroglia cells which come into relation with the sheaths of ingrowing vessels (Fig. 220, p. 318), and it is said that with further evolution there is a tendency for the sub-pial expansions to disappear and eventually for the attachment of the inner end of the cell to the internal limiting membrane to be lost. Branched lateral processes from the body of the cell have in the meantime been developed, and eventually one or more thick processes of the cell which have become attached by a foot-plate to the sheath of a vessel constitute what are known as its vascular processes, while the others, namely, the dendritic processes, either end freely or communicate with similar processes of adjoining neuroglia cells. The foot-plates on the vascular processes of the neuroglia cells are somewhat like the club-shaped expansions of the parenchyma cells of the pineal body (Fig. 218, Chap. 22, p. 317), and it is possible that serving as points of attachment, the latter have the same function as the foot-plates, namely, that of absorbing nourishment from the blood circulating in the vessel to which the expansion is attached.

In both neuroglial and pineal parenchyma cells the terminal expansions are frequently conical or trumpet-shaped, but the expansions of the neuroglial processes more often have the form of flat oval plates applied to the surface of the vascular sheath (Fig. 262), whereas the ends of the processes of the pineal cells are more typically club-shaped and the cells usually give off several processes each of which terminates in an expansion.




Fig. 262. — Footplate of Neuroglial Cell attached to Sheath of Blood Vessel : Rabbit. (After Penfield.)

The drawing shows two rows of cells of the oligodendroglia type ; these are situated between myelinated fibres of the cerebral white matter. One large fibrous astrocyte is seen above two oligodendroglial cells. Gliosomes stained by the method of Del Rio-Hortega are seen in relation with the cell-bodies and processes of both types of cell.


At a later period of foetal development, and especially at about thetime of birth, small cells with few and slender processes are developed between the medullated fibres of the white matter in the brain and spinal cord. These are termed oligodendrocytes, and their small round nuclei, lying in rows between parallel nerve-fibres, have long been recognized in specimens stained with the ordinary nuclear dyes such as iron haematoxylin. The appearance of these small cells in rows between the nervefibres is strongly suggestive of multiplication by amitotic division, more especially as mitotic figures are not often seen at this stage of development and the nuclei frequently lie in pairs. It also seems possible that they represent a modified or immature form of astrocyte rather than a distinct type, the modification from the usual astrocyte form into the interfascicular type of cell found in the white matter being due to the presence of the medullated white fibres, which limit the expansion and formation of processes in certain directions. The existence of transitional forms between the oligodendrocytes and the astrocytes among the cells in the aforementioned rows is an additional point in favour of this interpretation. Oligodendrocytes are also found in relation with large nerve-cells, such as those in the anterior cornua of the spinal cord and the pyramidal cells of the cortex cerebri (Fig. 263). These are often spoken of as satellite cells or perineuronal cells, whereas the oligodendrocytes found between the medullated nerve-fibres of the white matter in the brain and spinal cord are known as interfascicular cells. The small round granules lying in or on the processes of both types of oligodendrocyte which are termed gliosomes are believed to be concerned in the formation of the myelin sheath of nerve-fibres, and the relation of the perineuronal and interfascicular oligodendrocytes to the nerve cells and nerve-fibres suggests an homology of the oligodendrocytes of the central nervous system with the ganglionic capsular cells and the cells of the sheath of Schwann in the peripheral nervous system. The small branched cells with acidophil granules which are found in relation with the parenchyma cells of the pineal body possibly represent oligodendrocytes in this organ.


The mode of development of neuroglial fibres and the question of the existence of an intercellular substance we shall discuss later in the description of the structure of the normal pineal organ and the changes which it undergoes in disease or as a result of involution, but, as we have thought it advantageous to allude to some of the characteristic features of neuroglial tissue in the central nervous system before entering on the description of the pineal organ itself, so also we think that it will be profitable to discuss now the structure and some of the principal modifications of the normal ependyma of the brain and spinal cord, and the changes which it undergoes in disease or as a result of degeneration.


In the fully developed pineal organ the definitive ependyma is limited to the cells lining the pineal recess, but under certain conditions remnants of the original ependymal lining of the primary cavity of the pineal diverticulum or of its secondary outgrowths may persist as the lining membrane of one type of pineal cyst, and it seems possible that even after the full development of the organ has been attained and all traces of the original cavity have disappeared, certain cells which resemble the embryonic spongioblasts or primary ependymal cells retain the power of differentiating into either ependyma or neuroglia. This supposition may also apply to the development of ependymal cells lining the cavities in certain cases of syringomyelia, but when epithelium is found lining cysts in the pineal body or the cavities in the grey matter of the spinal cord it is usually of an irregular type — pseudo-ependymal — and the typical ependyma of the tall columnar form is seldom seen. The variations which occur in the normal ependyma and choroidal epithelium of the ventricles and central canal of the spinal cord are very considerable. These changes in the structure and form of the epithelium are related to varying mechanical and other conditions which are present in different parts of the brain and spinal cord. Thus the lining epithelium may be modified in one situation to form a sensory epithelium, e.g. the retina of the lateral eyes, and in another to form a secretory organ, as in the choroidal epithelium of the ventricles ; and since ependyma enters largely into the composition of the pineal organ as a whole, we propose to give a short summary of the morphology and functions of the ependyma in general, with the view of gaining a better insight into the structure and possible functions of this tissue as it occurs in the epiphysis of mammals. The morphology of the ependyma has been specially studied by Agduhr and Studnicka, and the following brief note is largely based on Agduhr's account of the ependyma in Penfield's Cytology of the Nervous System.


Fig. 263. A — Oligodendrocytes in relation with pyramidal cell of cerebral cortex human. (After Penfield and Cone, redrawn from Cowdry's Special Cytology.) B — Microglial cell, in relation with nerve-cell of grey matter. C — Fibrous astrocyte, showing perivascular feet and gliosomes. D — Protoplasmic astrocyte, also showing perivascular expansions and gliosomes. F. As. : fibrous astrocyte. OL., OL.D. : oligodendrocytes. Gl. : gliosome. P. As. : protoplasmic astrocyte. M. Gl. : microglial cell (mesoglia). P.V. Exp. : perivascular expansion. N.C. : nerve cell. Sp. : spines.



The ependyma is seen in its simplest form in the central nervous system of Amphioxus and of cyclostomes, in which the supporting tissue of the central nervous system is said to be wholly epithelial throughout life. The term " ependyma," as usually understood, is applied to the epithelial lining of the ventricular cavities of the brain and central canal of the spinal cord, but in the embryonic condition in all vertebrates, before the development of nerve cells and nerve-fibres, it extends through the whole thickness of the wall of the neural tube and takes part in the formation of the internal and external limiting membranes. Later, when the differentiation of this wall into zones has taken place, the term " ependyma " is often applied to the inner zone, which consists of several layers of spongioblasts, or " primary ependymal cells." This inner zone at a later stage is seen to be further differentiated into the definitive ependyma, glioblasts or astroblasts, and neuroblasts. Still later, the supporting function of the neuroglial tissue is supplemented by the ingrowth of vessels with their connective tissue sheaths.


From the morphological standpoint it must be remembered also that the lining membrane of outgrowths from the cerebral vesicles is homologous with the ependyma, and thus the epithelial lining of the following parts is ependymal in origin : the olfactory lobes ; the optic vesicles, including the pigment and sensory layers of the retina ; the infundibulum of the hypophysis ; the choroidal epithelium ; the paraphysis ; the epiphysis and the subcommissural organ ; also the lamina terminalis and the roof and floor-plates of the brain and spinal cord. The shape, the structure, and the function of the ependymal cells in these different situations varies. Thus the cells may be flattened, cubical, or columnar in form. They may be club-shaped, flask-shaped, or bottleshaped. They may be specialized in form, as in the hexagonal pigment cells, or rod and cone cells of the retina ; they may be glandular in type, as in the choroidal epithelium or in the paraphysis. They are, in some situations, devoid of cilia, in others they possess well-defined cilia, having minute rod-like particles or blepharoplasts at their bases, and their free ends converging to a point from the wide basal or ventricular end of the cell. The cells may be close together or separated by an interval. The basal ends of the cells may be joined by intercellular bridges so as to form an internal limiting membrane or separated so that the spaces between the cells open into the ventricular cavities or central canal of the spinal cord.


Large intra- and inter-ependymal nerve cells have been demonstrated by Agduhr (1922) in the ependyma lining the central canal of the spinal cord in the human subject and in various mammalian animals. These cells frequently end in a club-shaped process which projects into the central canal and resembles the club-shaped projections of the sensory cells described by Dendy and Studnicka in the parietal organ of cyclostomes and fishes. These cells have been beautifully demonstrated by the Nissl method of staining, and Agduhr has shown connections (synapses) between peripheral processes of intra-ependymal cells and the processes of cells lying in the nerve substance external to the ependyma.

The Functions of the Ependyma

These may be enumerated in the following order : Generative. Supporting. Secretory. Pigment formation. Special sense.


Lining membrane for protection and limitation of the nerve-tissues. Causation of currents in the cerebrospinal fluid by means of its cilia. A membrane concerned in dialysis and filtration, or serving as a limiting barrier.


Receptive cells concerned in reflex mechanisms. The generative capacity has already been referred to in connection with the differentiation from it of spongioblasts, neuroblasts, and the definitive ependyma, as has also the supportive character of the early ependymal elements. The limiting function of the definitive ependymal layer is, moreover, obvious, and the supposed action of the cilia in producing movement of the cerebrospinal fluid is well known. The special problems concerning dialysis, filtration, and the formation of a barrier to the passage of certain fluids or substances, whether normal or extraneous, into the cerebrospinal fluid are familiar to neurologists.

The secretory function of the modified ependymal epithelium which covers the choroidal plexuses is well established, and is definitely proved by inferences made in cases of obstruction to the outflow of cerebrospinal fluid from the ventricles and by direct observation of secretion of the fluid on the surface of the choroid plexus — in the human subject by Mott and Cushing, and in animals by Dandy and Blackfan. It is generally thought that the ependyma in other situations has a limited power of secretion of cerebrospinal fluid, but normally only to a very small extent. The question of the power of the ependymal cells to absorb cerebrospinal fluid has been studied by Nahagas and others. According to Nanagas a very small amount of cerebrospinal fluid may be absorbed through the ependyma lining the ventricles of the brain in normal animals (kittens), and evidence obtained from post-mortem examinations shows that obliteration of the lumen of the central canal of the spinal cord, which sometimes occurs in old age, is not followed by distension of the cana below the obstruction.

We have already considered the formation of pigment in the outer layer of the retina, in nerve tissues, and in the epidermis, and it will thus be only necessary to recall its frequent presence in the parenchyma cells and fibro-glial tissue of the pineal body : a condition which may be partly due to degenerative changes setting in at an early age, before degeneration has commenced in the nerve tissues as a whole, either as a result of disease or old age ; or it may in part be due to an hereditary trait, which has been preserved from the remote period when it may be inferred pigment was normally present in large quantity in the parietal sense-organ of our reptilian ancestors.

The possible function of the ependyma as a sensory layer containing receptive nerve-cells which are concerned in reflex action is strikingly suggested by Agduhr's demonstration of nerve cells in the ependyma lining the central canal of the spinal cord and brain stem in animals and the human subject. The existence of nerve cells in the ependyma which are connected by their peripheral processes with nerve cells in the adjacent grey matter suggests that impulses originating in the ependyma may be transmitted to ganglion cells in the grey matter of the spinal cord or brain stem. Whether the impulses are transferred to the cortex of the brain and give rise to a conscious sensation or not, it seems quite possible and even probable that they may originate reflex actions.


The function of the subcommissural organ, which is developed as a thickening of the ependyma below the posterior commissure and inferior peduncle of the pineal body (Fig. 185, B, p. 261), is not known, nor is that of Reissner's fibre, which is developed in relation with the subcommissural organ (Fig. 134, p. 188).

Microglia

Any investigation into the structure and pathology of an organ such as the pineal body, which is derived as an outgrowth from the central nervous system would be incomplete without a reference to the nature and origin of microglia as it occurs in the cerebrospinal system generally. The microglia or mesoglia is sometimes alluded to as the " third element " in the composition of nervous tissue. This name was originally given by Cajal (1913) to a group of small non-nervous elements which were afterwards differentiated by the special staining methods of Del RioHortega into oligodendrocytes and microglia, the former neuroglial in nature, the latter mesodermal. Hortega accordingly proposed to restrict the application of the term " third element " to the microglia, and allocate the oligodendrocytes to the neuroglial constituents or " second element." Thus, of the three constituents of nerve tissue excluding the connective tissue and vessels, the " first element " comprises the nerve cells ; the " second element " the neuroglia, including both astrocytes and oligodendrocytes ; and the " third element " is represented by the microglia. The microglia cells are small branched elements with minute nuclei of irregular form which stain deeply by Nissl's method ; the ordinary nuclear dyes such as hematoxylin ; and the silver carbonate method of Del Rio-Hortega which also brings out clearly the cell-body and processes. The latter are irregular in form and size and are characterized by small thorn-like spines. The cells have phagocytic properties and are under certain conditions capable of amceboid movements. Thus, according to the descriptions of Hortega, during the migratory phase in the development of the microglia, throughout the nervous tissue, it consists of roundish cells with pseudopodia, the various shapes of which indicate the motility of the cells. " After this initial phase the cells become branched, and when they take up their positions in the tissue they have small dark nuclei, surrounded by scanty cytoplasm prolonged into two or more thin, wavy, branched processes beset with spines which end freely, that is, they are not anastomosed among themselves nor are they connected with the neuroglia elements." He also holds the view that in a broad sense the microglia of the central nervous system represents from the functional standpoint the reticulo-endothelium of mesodermal tissues. It has been known to fix certain colloids to phagocytose erythrocytes and cellular debris, and it is believed to be concerned in the elimination of substances resulting from metabolism and degeneration of nerve cells. Thus, it is found to participate actively in inflammatory and destructive processes involving the central nervous system, and as a result of the motility of the cells and their increase in size under pathological conditions they assume various forms, becoming rod-like, lamellar, or rounded in shape, and frequently contain fat granules.

Development of Microglia

The microglia, according to the description of Del Rio-Hortega, does not appear until the last period of embryonic life. In foetuses at term and in new-born animals it is abundant both beneath the pia mater and spreading inward along the course of the vessels of the brain and cerebellum. It is developed later than the neuroglia, at the time when the vessels of the pia mater have reached their full development. The cells which give rise to the microglia are believed to be mesodermal in origin and are first visible immediately beneath the pia mater on the surface of the brain and spinal cord ; they are found also in relation with the tela choroidea of the third ventricle below the corpus callosum and fornix, and also beneath the pia mater covering the white matter of the cerebral peduncles. It is also abundantly formed in connection with the vascular folds of the tela choroidea inferior and on the surface of the cerebellum.

Originating as a layer of rounded or flattened cells beneath the pia on the surface of the brain, the microglial cells afterwards develop pseudopodia and migrate deeply into the substance of the white and grey matter, and eventually they reach the ependyma lining the ventricles or central canal of the spinal cord.

The cells beneath the pia are at first rounded, cuboidal, or flattened ; they increase in size and develop irregular bulbous processes; later, when they reach their ultimate destination, they become fixed and dendrites are formed, on which later the characteristic spines are developed. The cells are said by Hortega to lie in the neuroglia, and their processes do not communicate with each other.


The nuclei in the early stages of development are easily visible in specimens stained with the ordinary nuclear dyes. They form two or three layers beneath the pia and resemble the nuclei of lymphocytes and proliferating endothelium, and in cases of injury or disease may be readily mistaken for these.


The microglia cells having attained their full development become " fixed " and are described as being in the resting condition. They are found throughout the nervous system in the grey and white matter, being, however, more abundant in the grey matter than in the white. It is probable that the normal number of cells is maintained during adult life by amitotic division of the nuclei, although mitotic figures have occasionally been seen (Del Rio-Hortega). Having reached their full development and entered the resting phase, in a fixed position, they may retrace their stages of development in reverse order ; the processes gradually thickening and becoming shorter, until they assume the form of pseudopodia, and the body becomes rounded. This process of devolution is seen in cases of injury to the brain, when the cells having assumed amoeboid characters, migrate towards the focus of inflammation, hsemorrhage, or degeneration and there act as phagocytes, engulfing leucocytes, erythrocytes, and broken-down nerve tissue. Their function is, therefore, similar to that of leucocytes and the cell-elements of the reticuloendothelium, and before the ordinary methods of staining were supplanted by the special methods of staining with silver carbonate, the appearances were interpreted as those of inflammation as it occurs elsewhere in the body generally and attended by the accumulation of leucocytes and proliferation of endothelium.


Relations of Microglia to Nerve-cells and Vessels

Microglial cells, like oligodendrocytes, are found as satellite cells of large neurones, such as the Purkinje cells of the cerebellar cortex. They may be associated either with the body of the cells or with its processes. They may be distinguished from oligodendrocytes by their small, deeply stained, and irregularly shaped nuclei and by the spines on their processes. Microglia cells are also found in relation with the adventitia of the vessels lying in the white or grey matter.


As might be expected, microglial cells are present in the retina and in the optic nerve, and they have been found in the fibrous plaques of the human pineal organ.


   The Pineal Organ (1940): 1 Introduction | 2 Historical Sketch | 3 Types of Vertebrate and Invertebrate Eyes | Eyes of Invertebrates: 4 Coelenterates | 5 Flat worms | 6 Round worms | 7 Rotifers | 8 Molluscoida | 9 Echinoderms | 10 Annulata | 11 Arthropods | 12 Molluscs | 13 Eyes of Types which are intermediate between Vertebrates and Invertebrates | 14 Hemichorda | 15 Urochorda | 16 Cephalochorda | The Pineal System of Vertebrates: 17 Cyclostomes | 18 Fishes | 19 Amphibians | 20 Reptiles | 21 Birds | 22 Mammals | 23 Geological Evidence of Median Eyes in Vertebrates and Invertebrates | 24 Relation of the Median to the Lateral Eyes | The Human Pineal Organ : 25 Development and Histogenesis | 26 Structure of the Adult Organ | 27 Position and Anatomical Relations of the Adult Pineal Organ | 28 Function of the Pineal Body | 29 Pathology of Pineal Tumours | 30 Symptomatology and Diagnosis of Pineal Tumours | 31 Treatment, including the Surgical Approach to the Pineal Organ, and its Removal: Operative Technique | 32 Clinical Cases | 33 General Conclusions | Glossary | Bibliography
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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)

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