Blood vessels of the Peyer's patch in the mouse: I. Topographic studies

THE ANATOMICAL RECORD 206:391-401(1983)

Blood Vessels I . Topographic

of the Peyer’s Patch in the Mouse: Studies

K. YAMAGUCHI AND G.I. SCHOEFL Department of Experimental Pathology, John Curtin School of Medical Research, Australian National University, Canberra, ACT 2601, Australia

ABSTRACT The topographic distribution of blood vessels in Peyer’s patches of mice was studied by light and scanning electron microscopy with whole mounts of flattened gut segments and vascular corrosion casts. Peyer’s patches are imbed- ded in the intestinal wall and share its blood supply. Two to four mural trunks may contribute to the area of the patch. In and around the lymphoid nodules the microcirculation is highly specialized. The nodule is permeated by a meshwork of fine capillaries that is supplied by arterioles entering on the serosal and lateral surfaces. Blood flow to the lymphoid nodule appears to be monitored by arterial sphincters; the dense lymphatic tissue can also be bypassed by arteriovenous communications. An extensive venous network encircles the nodule. Most of these venules are lined by high endothelium which is penetrated by lymphocytes. The geometry of these vessels suggests a slow and turbulent flow in these vascular segments that may aid margination of lymphocytes. A planar capillary plexus lies subjacent to the mucosal epithelium in the dome area.

Peyer’s patches are clusters of lymphoid nodules in the wall of the intestine. They play an important role in immune reactions of the gut (Miiller-Schoop and Good, 1975; Bienenstock et al., 1980). Both B and T lymphocytes have been shown to recirculate through them (Go- wans and Knight, 1964; Evans et al., 1967), and the IgA-secreting cells of the intestinal mucosa have their origin in this tissue (Hus- band et al., 1977). Anatomically, they may be compared to the cortical area of lymph nodes spread out so that the lymphoid nodules come to lie in one plane. Thymus-dependent and thymus-independent regions comparable to those in the lymph node have been identified (Fried- berg and Weissman, 1974; Abe and Ito, 1978). Peyer’s patches lack afferent lymphatics; gut antigens may reach the lymphoid tissue via the specialized follicle-associated epithelium (Bockman and Stevens, 1977; Owen, 1977).

Peyer’s patches do not have a separate blood supply. The lymphoid nodules are embedded in the wall of the intestine and their microcirculation is a part of the general circulation of the gut. In the immediate area of the patch, the vascular pattern is modified and blood vessels in and around the lymphoid tissue are highly specialized. Of particular interest have been the high-endothelium venules, vascular

segments in which large numbers of recircu- lating lymphocytes migrate across the vascular wall (Gowans and Knight, 1964). There is general agreement that these blood vessels are localized largely around the lymphoid follicles (Abe and Ito, 1977; Bhalla et al., 1981; An- derson et al., 1976; Schoefl, 1970). Their three- dimensional distribution in relation to other vascular segments of the gut has, to our knowl- edge, not been described.

In the present study, we have examined the microcirculation of this lymphoid tissue in flattened segments of gut in which the blood vessels had been filled with a colored injection mass and in preparations in which the vascular network had been replicated with resin.

MATERIALS AND METHODS

Thirteen outbred male mice with body weights varying between 25 and 30 gm were used. Seven were prepared for examination with the light microscope and six for scanning electron microscopy.

Received December 15. 1982; accepted April 18, 1983

K. Yamaguchi’s present address. Institute of Laboratory Animals, Yamaguchi Unlversity, School of Medicine, Ube 755, Japan.

(c) 1983 ALAN R. LISS, INC

392 K. YAMAGUCHI AND G.I. SCHOEFL

Injection Preparations Under ether anesthesia, the thoracic aorta

was canulated with polyethylene tubing (SP 31, Dural Plastics, Dural, NSW, Australia). To improve flow through the intestine, both renal vessels were clamped off as well as the lower abdominal aorta and the inferior vena cava just proximal to the iliac bifurcations. The right atrium was cut, and the intestinal circulation was perfused with 5 ml of 10% formol-saline and subsequently filled with a warm 5% gelatin solution prepared by mixing equal amounts of 10% gelatin and a colloidal carbon suspen- sion (C11/1431a, Pelikanwerke, Hannover, Germany). The outflow was then clamped and the perfused tissue was covered with crushed ice for 15 min to allow gelling of the injection mass. Pieces of intestine containing a Peyer’s patch were cut out, pinned onto plastic sheets, and fixed for an additional period of 1-2 days. Two patches of each animal were cut with a razor blade into transverse slices of approxi- mately 0.5mm; the others were left intact. Both types of preparations were dehydrated with alcohol, cleared in xylol, and finally mounted on glass slides in Gurr’s neutral mounting me- dium.

In mice, the entire thickness of the intestinal wall is only about 0.5mm, and flattened segments can be mounted in toto for topographic studies of the vascular distribution. Whole mounts and slices were examined on a Zeiss dissecting microscope and on a Zeiss photomi- croscope using transillumination.

A few additional animals were similarly perfused with Microfil (Canton Bio-Medical Prod- ucts, Boulder, CO) and wholemounts were prepared and examined as above.

Resin Corrosion Casts Six mice were canulated as above. Three were

perfused with a 2% glutaraldehyde/2% for- maldehyde mixture in 0.1 M sodium cacodylate buffer, and three were perfused with saline before the intestinal circulation was filled with Mercox (Dai-Nippon Ink Co., Ltd., Osaka, Ja - pan). When the resin had hardened, segments of the intestine containing a Peyer’s patch were cut out and corroded in several changes of 10% KOH over a period of 3-4 days. The resulting vascular casts were washed in alcohol and freeze-dried. They were coated with gold (20 nm) and examined in a Cambridge Stereoscan 180. Stereopairs were recorded for most areas examined.

RESULTS

Between 7 and 11 Peyer’s patches, composed of up to 16 nodules, could be identified in the

small intestine. They have no definite locations along the length of the gut and there was no correlation with major vascular trunks of the intestinal wall. They are always located, however, on the antimesenteric border.

Observations on Injection Preparations A low-power view of a wholemount prepa-

ration is illustrated in Figure 1. The Peyer’s patch stands out as an aggregate of pale nodules intercalated into the vascular supply of the gut. The general distribution of blood vessels of the Peyer’s patch is seen best from the serosal surface (Figs. 1, 2); much of the vascular bed is obscured by villi when the preparation is viewed from the mucosal surface (Fig. 3). Two to four major arterial trunks may contribute to the area of the Peyer’s patch. These trunks originate from the mesenteric arcades, ascend on either side of the gut wall, and anastomose freely across the antimesenteric border (Fig. 1). Anastomoses of the arterial and of the venous network are commonly seen in most areas of the gut wall (Figs. 1, 2).

Major arterial trunks are accompanied by veins, but near the Peyer’s patch they divide into two to three smaller vessels that take an independent course (Fig. 2). Some enter the superficial aspect of the Peyer’s patch or run along its edge; others distribute into the adjacent intestinal tissue. Within the patch, their ramifications are not constant. They may course between the nodules; sometimes they cross over them. These arterial branches give off lateral arterioles, often a t right angles, towards the lymphoid nodule and they anastomose with similar vessels entering the Peyer’s patch from the opposite side (Fig. 2).

Individual nodules are supplied by two to four arterioles. These enter directly or subdi- vide before they break up into a capillary meshwork that permeates the dense lymphatic tissue. Points of entry are towards the serosal pole of the nodule or near its lateral surface (Fig. 4; see also Diagram 1). Although the capillary net within the nodule is visible to some depth, the three-dimensional arrangement is difficult to judge in these preparations. Viewed from the mucosal surface, the nodule is en- sheathed by a superficial network of capillaries in the dome area (Fig. 3). There appear to be few communications with the internal meshwork of the nodule.

Venous vessels are more numerous than arterial vessels and they tend to follow the con- tours of the nodule more closely. Much of the lymphoid tissue is drained by venules that arise near the serosal pole of the nodule and descend to larger vessels in the internodular space (Fig.

BLOOD VESSELS OF THE PEYER’S PATCH 393

Fig. 1. From a segment of gut cut open near the mesenteric attachment illustrating the location of a Peyer’s patch in the antimesenteric border (AMB). In the lower half of the picture, mural trunks (MT) of one side of the gut wall are

4). Radicals of these venules communicate with arterioles via short thoroughfares (Fig. 4). These do not appear to be arteriovenous anastomoses in the strict sense, since they may give rise to one or several capillaries that penetrate the nodule. Venules are usually recognized by an abrupt increase in vessel caliber (Fig. 4). In this tissue, they are lined by high endothelium that is permeated by large numbers of mi- grating lymphocytes. These venules form a basket-like girdle on the serosal but not mucosal aspect of the nodule before they drain into larger vessels of the same kind deeper in the tissue. There they follow the spaces between the nodules, and eventually they join larger venous trunks of the gut wall that are lined by flat endothelium.

A slice across the Peyer’s patch is shown in Figure 5. The lymphoid nodules stand out as pale areas, though the vascular density of the capillary mesh is, in fact, greater than that of vessels in the internodular area. Villi associated with the Peyer’s patch are large and share a common blood supply with the lymphoid tissue.

Observations on Resin Casts The casts of blood vessels other than high-

endothelium venules had a smooth surface with

shown to branch off the mesenteric arcades (MA). Mural trunks of the opposite side (top) are not included in the picture. The blood vessels were injected with Microfil. x 8.

imprints of endothelial nuclei. These were es- pecially prominent in arterioles (Fig. 11). In the high-endothelium venules, the replicated endothelial surface was irregular and had numerous pits and depressions (Figs. 10 , l l ) . The diameter of vessels was generally larger in animals which had not been prefixed by perfu- sion, and high-endothelium venules appeared smoother in these preparations.

Resin casts allowed a more detailed examination of the vascular distribution and they were particularly helpful in examining internal networks that are largely obscuredin wholemounts. Low-power views of the serosal surface and of a transverse fracture of such casts are illustrated in Figures 6 and 7. The common vascular supply to lymphoid tissue and to intestinal tissue is shown clearly in these preparations. Along a short distance, a parent vessel may give off alternate branches into the Peyer’s patch and, away from it, into the various layers of the gut wall (Fig. 7).

In the area of the Peyer’s patch, the vascular bed is highly specialized. As was noted in the carbodgelatin-injected wholemounts, individual lymphoid nodules are supplied by a few arterioles and drained by many high-endothelium venules (Fig. 8). Most of these vessels are restricted to the superficial zone of the nodule,


whereas the deeper lymphoid parenchyma is permeated by a mesh of capillaries. Arterioles enter the nodule near its serosal pole and on its sides (Fig. 10). Constrictions were seen frequently a t their points of origin (Fig. 11); they suggested the presence of arterial sphincters. Thoroughfare channels from arterial to venous vessels were particularly evident in these casts, and what had not been appreciated in the injected wholemounts was the numerous anastomotic connections of the high-endothelium venules either via short segments of fine vessels or links of larger caliber (Fig. 11).

Another peculiarity noted was the three-dimensional orientation of small branches of these venules as they join to form larger collecting vessels. Often several vessels, converging from various directions, joined at one point or within a short distance from each other (Fig. 11). In a few preparations, all of which were from animals in which the vascular bed had not been fixed prior to filling with the resin, sphincter- like constrictions were seen at the junctions of high-endothelium venules with larger vessels. They were not evident in casts of animals perfused with fixative before the resin.

Vessels of the substance of the lymphoid nodule could be examined in fractured specimens (Fig. 12). The network of fine vessels appeared denser towards the serosal pole and was penetrated by a few arterioles and smooth-walled venules (Fig. 13). Vascular meshes in the lower half of the nodule were larger and there was an apparent elongation of the meshes from the center towards the dome area. A superficial planar network with relatively few connections to the interior of the nodule covered the

Fig. 2. Serosal surface of the Peyer’s patch. Most of the larger vessels of the gut wall and of the patch are visible. Anastomoses (arrows) are frequent on the arterial (A) and on the venous (V) side. Carbon-gelatin injection. x 16.

Fig. 3. Mucosal surface. Only the flat capillary mesh of the dome area (see Diagram 1) is clearly visible. Most other vessels are obscured by prominent intestinal villi that surround each lymphoid nodule. Carbon-gelatin injection. x 28.

Fig. 4. Higher magnification of the serosal surface. Ar- terioles (A) and high-endothelium venules (HV) follow the surface of the lymphoid nodule and are linked by many arteriovenous communications (arrows). Carbon-gelatin injection. x 100.

Fig. 5 . Cross section of a Peyer’s patch. A fine meshwork of capillaries permeates the lymphoid nodules (N). Villi (V) adjacent to the nodules are prominent. x 35.

S P

Diagram 1. Diagrammatic representation of blood vessels associated with lymphoid nodules of the Peyer’s patch as seen from the serosal surface (top) and in cross section (bottom). Arteries (A) are shown in outline, venules and small veins (V) with attenuated endothelium in solid black. Stippling indicates high-endothelium venules. LS denotes lateral surface, SP serosal pole, and MP mucosal pole or dome area.

dome area (Fig. 9). This vascular layer tended to stay largely intact even when most of the nodular meshwork had been shelled out during fracturing (Fig. 6); branches supplying it derived mainly from vessels in the internodular space.

Villi adjacent to the nodules have a common blood supply, as do the small capillaries of the muscular externa. This network of fine vessels is not obvious in wholemounts and is usually fragmented during handling of the resin casts (Fig. 7).

DISCUSSION

Peyer’s patches are of common occurrence in the intestinal wall of mammals. In rats and mice, they are conspicuous structures; individual lymphoid nodules bulge out the muscle wall and can be seen clearly. As already noted by Hummel(1935) and also by Abe and Ito (19771, Peyer’s patches do not have definite locations along the length of the intestine, and there is no constant orientation in relation to major vascular trunks supplying the gut wall. Blood


Fig. 6. Resin corrosion cast fractured across a Peyer’s patch. The fracture goes across the internal meshwork of one nodule (“1. In another nodule ( N ) , this meshwork has been shelled out, but the planar capillary plexus (P) on the mucosal surface appears largely intact. x 40.

Fig. 7. A similar preparation viewed from the serosal surface. Note alternate branches (arrows) of an artery (A) into the patch and away from it into the intestinal wall. Fragments of muscle capillaries (MC) can be seen in the lower half. x 40.

BLOOD VESSELS O F THE PEYER’S PATCH 397

Fig. 8. High-endothelium venules (HV) and arterioles Fig. 9. Mucosal surface illustrating the flat capillary (A) on the serosal surface of the lymphoid nodule. x 85. plexus that covers the dome area. x 80.


Fig. 10. Close-up of a lymphoid nodule. A small artery (A) is entering from the right, and branches enter the dense lymphatic tissue on the serosal and lateral surfaces. x 120.

Higher-power view of the same area. This view

illustrates a constriction thought to be the site of a n arterial sphincter (S), arteriovenous communications (arrows) and a large-caliber venous anastomosis (double arrow). Note small tributaries of high-endothelium venules (HV) coming to- gether a t a nodal point. x 300. Fig. ll.


Fig. 12. Higher-power view of the fractured Peyer’s patch shown in Figure 6, illustrating the dense internal capillary network of the lymphoid nodule. The meshwork appears densest in the area of the germinal center. x 90.

Fig. 13. Higher magnification close to the serosal surface. Small arterioles (A) and smooth-walled venules (V) penetrate the meshwork of the nodule. The upper right in- cludes a few branches of high-endothelium venules. x 300.


vessels of a particular Peyer’s patch area may be derived mainly from one mural trunk or from as many as four. The lymphoid nodules, however, are always located on the antimesenteric border, which places them into a vascular bed that is not directly entered by large vessels and is rich in anastomotic connections on both the arterial and on the venous side (Noer, 1945; Baez, 1977). The lymphoid nodules are intercalated in this vascular bed and are an integral part of it. The supply of even small vessels may be shared by the lymphoid tissue with adjacent tissues. The overall pattern of an anastomotic net is continuous across the area of the Peyer’s patch, though each lymphoid nodule has its own characteristic microcirculation.

Arterial vessels enter the nodule near the serosal pole and on its lateral aspects, breaking up into a capillary mesh that permeates the germinal center. Although reference has been made frequently to a poor vascular supply of the center (Herman, 1980; Blau, 1977; Ander- son et al., 1976), the relative density of blood vessels is higher in the nodules than in the areas surrounding them, though in the latter the vessels are larger and hence more conspicuous.

Small blood vessels in the germinal center of Peyer’s patches have recently been men- tioned by Abe and Ito (1977) and also by Bhalla et al. (1981). Muratori (1937, 19381, who re- viewed the older literature on the distribution of blood vessels in lymphoid follicles of Peyer’s patches, feels that seemingly avascular follicles are usually the result of incomplete filling of the vascular bed. In his own investigations on Peyer’s patches of rat, rabbit, cat, and guinea pig, he describes a delicate meshwork of capillaries permeating the follicle, which agrees with our findings in the mouse. We feel that the apparent difficulty of filling vessels in the lymphatic nodules may, in fact, reflect a characteristic property of this microcirculation.

We observed constrictions at points where arterioles branched off to enter the lymphoid nodule. This suggests the presence of sphincters and that blood flow to the lymphoid nodule can be readily controlled. Although such sphincters have not been described by other authors (Anderson et al., 1976; Bhalla et al., 1981) we have seen them in in vivo preparations (Yamaguchi and Schoefl, 1983) and we feel that they may be of more common occurrence. Apparently, they control whether blood flows through the dense lymphatic tissue of the nodule or whether it is shunted away from it.

Muratori (1937, 1938) refers to capillaries of the lymphoid follicle as being particularly delicate. These sphincters may function to protect capillaries of the lymphoid nodules from large pressure fluctuations, which in Peyer’s patches may be the result of peristalsis or distension of the gut wall by luminal content.

Blood bypassing the dense lymphatic tissue can readily distribute within an anastomotic meshwork, which in the gut is characteristic for both arteries and veins (Noer, 1945). Da- below (1938/1939) proposed that the large villi that surround lymphoid nodules may also con- stitute an overflow area. And finally, blood may be shunted to the venous side via arteriovenous communications on the serosal surface of the lymphoid nodule. They occur in the Peyer’s patches of several species (Muratori, 1937,1938) and they have been noted by Anderson and Anderson (1975) in the rat lymph node. The arteriovenous communications link the arterial side with an exceptionally voluminous venous bed that forms an anastomotic mesh on the lateral and serosal surface of the nodule. I t does not extend to the surface facing the intestinal mucosa. Most of the vessels of this venous system are lined by high endothelium that is permeated by lymphocytes (Hummel, 1935; Schoefl, 1970; Abe and Ito, 1977).

Blood flowing from a few arterial vessels into a wide venous meshwork would be expected to be slowed down, and the three-dimensional arrangement, i.e., the meeting of several branches a t nodal points, suggests in addition a fair amount of turbulence in this venous circulation. Both of these factors, slowing of the blood stream and turbulence, would tend to favor contact of lymphocytes with the endothelium and may thus aid in the margination of lymphocytes prior to migration across the vascular wall.

An additional regional mechanism of regu- lating venous pressure and flow by sphincters in the segmental veins of rat lymph nodes was proposed by Anderson and Anderson (1975). Such sphincters, however, were not observed by them in rat Peyer’s patches and they were not evident in our preparations. In a few in- stances, vascular casts appeared to replicate sphincter-like configurations at points where high-endothelium venules terminated in larger collecting vessels. However, since they were only seen in a few preparations in which the vascular bed had not been fixed prior to casting it with resin and since they have not so far been observed in vivo, their significance is un- certain.

BLOOD VESSELS O F THE PEYER’S PATCH 401

On the mucosal surface, the dome area, the lymphoid nodule is covered by a planar capillary network. Bhalla et al. (1981) describe a similar pattern in the rat. This network has relatively few communications with that of the nodule itself. Supply and drainage are largely via vessels that originate in the internodular area and enter obliquely without penetrating the dense lymphatic tissue.

The epithelium covering this area is perme- able to macromolecules and marker particles and has been proposed as a possible route for immunoglobulin transfer to the gut lumen and for access of antigen to the lymphoid tissue (Bockman and Stevens, 1977; Owen, 1977; Joel et al., 1978). A specific involvement ofthe sube- pithelial capillary plexus has, so far, not been demonstrated. Large numbers of macrophages were noted in the dome area by Sobhon (1971) and Abe and Ito (1977), and carbon particles, when fed over long periods, readily accumu- lated in those macrophages and in other areas of the Peyer’s patch but there was little evidence of their uptake by nearby blood vessels and into the systemic circulation (Joel et al., 1978). Carbon, however, has a large particle size, and uptake of smaller molecules may occur. These vessels may represent segments of the circulation of the villus displaced by sec- ondary accretion of lymphatic tissue (Hummel, 1935).

Diagram 1 recapitulates the distribution of blood vessels in the Peyer’s patch. Individual nodules are supplied by a few arterioles and drained by many high-endothelium venules. These venules are oriented around the sides and towards the serosal surface of the nodule. The action of arterial sphincters can shunt the blood away from the lymphoid tissue to adjacent areas of the gut wall; within the nodule, the dense lymphatic tissue of the center of the nodule can be bypassed via arteriovenous communications. A planar capillary plexus faces the mucosal surface and drains towards the interfollicular spaces.

ACKNOWLEDGMENTS

We thank Mrs. Kathy McIntyre and Ms. Marie Colvill for excellent technical and pho- tographic assistance.

LITERATURE CITED Abe, K., and T. Ito (1977) A qualitative and quantitative

morphologic study of Peyer’s patches of the mouse. Arch. Histol. Jpn., 40:407-420.

Abe, K., and T. Ito (1978) Qualitative and quantitative morphologic study of Peyer’s patches of the mouse after neo- natal thymectomy and hydrocortisone injection. Am. J. Anat., 151:227-238.

Anderson, A.O., and N.D. Anderson (1975) Studies on the structure and permeability of the microvaculature in normal rat lymph nodes. Am. J. Pathol., 80t387-418.

Anderson, N.D., A.O. Anderson, and R.G. Wyllie (1976) Spe- cialized structure and metabolic activities of high endothelial venules in rat lymphatic tissues. Immunology, 31r455-473.

Baez, S. (1977) Skeletal muscle and gastrointestinal micro- vascular morphology. In: Microcirculation. G. Kaley and B.M. Altura, eds. University Park Press, Baltimore, Vol. 1, pp. 69-94.

Bhalla, D.K., T. Murakami, and R.L. Owen (1981) Micro- circulation of intestinal lymphoid follicles in rat Peyer’s patches. Gastroenterology, 81:481-491.

Bienenstock, J., A.D. Befus, and M. McDermott (1980) Mu- cosal Immunity. Monogr. Allergy, 16:l-8.

Blau, J.N. (1977) A comparative study of the microcirculation in the guinea pig thymus, lymph nodes and Peyer’s patches. Clin. Exp. Immunol., 27:340-347.

Bockman, D.E., and W. Stevens (1977) Gut-associated lym- phoepithelial tissue: Bidirectional transport of tracer by specialized epithelial cells associated with lymphoid follicles. J. Reticuloendothel. SOC., 21 t245-254.

Dabelow, A. (193811939) Die Blutgefassversorgung der lym- phatischen Organe. Anat. Anz., 87r179-224.

Evans, E.P., D.A. Ogden. C.E. Ford, and H.S. Micklem (1967) Repopulation of Peyer’s patches in mice. Nature, 216t36-38.

Friedberg, S.H., and I.L. Weissman (1974) Lymphoid tissue architecture. 11. Ontogeny of peripheral T and B cells in mice: Evidence against Peyer’s patches as the site of gen- eration of B cells. J. Immunol., Z13t1477-1492.

Gowans, J.L., and E.J. Knight (1964) The route of re-circulation of lymphocytes in the rat. Proc. R. SOC. B, 159:257-282.

Herman, P.G. (1980) Microcirculation of organized lymphoid tissues. Monogr. Allergy, 16:126-142.

Hummel, K.P. (1935) The structure and development of the lymphatic tissue in the intestine of the albino rat. Am. J. Anat., 57t351-383.

Husband, D.A.J., H.J. Monie, and J.L. Gowans (1977) The natural history of the cells producing IgA in the gut. In: Immunology of the gut. Ciba Found. Symp., 46r29-54.

Joel, D.D., J.A. Laissue, and M.E. LeFevre (1978) Distri- bution and fate of ingested carbon particles in mice. J. Reticuloendothel. SOC., 24:477-487.

Muller-Schoop, J.W., and R.A. Good (1975) Functional studies in Peyer’s patches: Evidence for their participation in intestinal immune responses. J. Immunol., 114r1757-1760.

Muratori, G. (1937) Vascolarizzazione e circolazione sanguigna nelle placche di Peyer di vari mammiferi. Monitore 2001. Ital., 48:217-223.

Muratori, G. (1938) Osservazioni sulla vascolarizzazione sanguigna delle placche di Peyer. Arch. Ital. Anat. Em- briol., 1 I :491-512.

Noer, R.J. (1945) The blood vessels ofthe jejunum and ileum: A comparative study of man and certain laboratory animals. Am. J. Anat., 73:293-334.

Owen, R.L. (1977) Sequential uptake of HRP by lymphoid follicle epithelium of Peyer’s patches in the normal unob- structed mouse intestine: An ultrastructural study. Gas- troenterol., 72r440-451.

Schoefl, G.I. (1970) Structure and permeability of venules in lymphoid tissue. Proc. 7th Int. Congr. Electron Mi- crosc., Grenoble, 3:589-590.

Sobhon, P. (1971) The light and electron microscopic studies of Peyer’s patches in non germ-free adult mice. J. Mor- phol., 135t457-481.

Yamaguchi, K., and G.I. Schoefl(1983) Blood vessels of the Peyer’s patch in the mouse: 11. In vivo observations. Anat. Rec., 206: 403-417.

Blood vessels of the Peyer's patch in the mouse: I. Topographic studies

Documents

Transcript of Blood vessels of the Peyer's patch in the mouse: I. Topographic studies