the peritoneal elastic lamina*

6
J. Anat. (1991), 177, pp. 41-46 41 With 4 figures Printed in Great Britain The peritoneal elastic lamina* P. J. T. KNUDSEN Institute of Pathology, Aalborg Sygehus, DK 9000 Aalborg, Institute of Pathological Anatomy, Hjorring Sygehus, DK 9800 Hjorring, and Institute of Forensic Medicine, University of Aarhus, DK 8000, Aarhus C, Denmark (Accepted 7 January 1991) INTRODUCTION The peritoneal elastic lamina (lamina elastica peritonei, LEP) is a little-known component of the peritoneum, being composed of a network of elastic fibres situated immediately beneath the basement membrane of the peritoneal mesothelium, separated from this by a scanty layer of connective tissue, poor in collagen fibres. The LEP as a separate entity has been referred to only rarely (Morson & Dawson, 1979; Dobbie, Zaki & Wilson, 1981). A similar structure has been described in animals (Rhodin, 1974; Parsons, Marko & Wansor, 1983), but no precise description of the extent of this structure in man is available. Since it might prove useful, both for normal anatomical and for pathoanatomical studies, it was decided to undertake a systematic study by light microscopy. MATERIAL AND METHODS In order to demonstrate the extent of the LEP, samples were removed from 10 consecutive patients who had died without antemortem evidence of intra-abdominal disease, and whose abdominal cavity was normal at autopsy. An attempt was made to remove the samples as soon as possible after death, but observance of Danish law meant, for all practical purposes, an interval of at least 6 hours. Samples were taken from the peritoneal covering of all intraperitoneal and retroperitoneal organs- stomach, small and large intestine, appendix, liver, spleen, gall bladder, pancreas, uterus and fallopian tubes as well as from the parietal peritoneum on both sides above and below the navel, the diaphragm and the testis. Sections were taken perpendicular to the peritoneal surface from the samples from the parietal peritoneum and the intestines. Selected sections were also cut at a right angle to these, parallel to the plane of the fibres of the LEP so that they were vizualised 'en face'. Following paraffin embedding, the sections were submitted to a variety of elastic stains, Weigert's or Verhoefls stains with or without Van Gieson Hansen counterstain being used routinely, supplemented by Orcein or Victoria Blue as required. Because of the state of preservation of the autopsy samples, a supplementary series of slides from grossly normal areas of organs covered with peritoneum removed at operation stomach, small and large intestine, appendix, spleen, gall bladder, testis, uterus and the fallopian tubes-was investigated. The organs examined in this series were removed either because of disease in the vicinity, for technical reasons or * Reprint requests to Dr Peter J. T. Knudsen, Institute of Forensic Medicine, University of Aarhus, Finsensgade 15, DK 8000, Aarhus C, Denmark.

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Page 1: The peritoneal elastic lamina*

J. Anat. (1991), 177, pp. 41-46 41With 4 figures

Printed in Great Britain

The peritoneal elastic lamina*

P. J. T. KNUDSENInstitute of Pathology, Aalborg Sygehus, DK 9000 Aalborg, Institute of PathologicalAnatomy, Hjorring Sygehus, DK 9800 Hjorring, and Institute of Forensic Medicine,

University of Aarhus, DK 8000, Aarhus C, Denmark

(Accepted 7 January 1991)

INTRODUCTION

The peritoneal elastic lamina (lamina elastica peritonei, LEP) is a little-knowncomponent of the peritoneum, being composed of a network of elastic fibres situatedimmediately beneath the basement membrane of the peritoneal mesothelium,separated from this by a scanty layer of connective tissue, poor in collagen fibres. TheLEP as a separate entity has been referred to only rarely (Morson & Dawson, 1979;Dobbie, Zaki & Wilson, 1981). A similar structure has been described in animals(Rhodin, 1974; Parsons, Marko & Wansor, 1983), but no precise description of theextent of this structure in man is available. Since it might prove useful, both for normalanatomical and for pathoanatomical studies, it was decided to undertake a systematicstudy by light microscopy.

MATERIAL AND METHODS

In order to demonstrate the extent of the LEP, samples were removed from 10consecutive patients who had died without antemortem evidence of intra-abdominaldisease, and whose abdominal cavity was normal at autopsy. An attempt was madeto remove the samples as soon as possible after death, but observance of Danish lawmeant, for all practical purposes, an interval of at least 6 hours. Samples were takenfrom the peritoneal covering of all intraperitoneal and retroperitoneal organs-stomach, small and large intestine, appendix, liver, spleen, gall bladder, pancreas,uterus and fallopian tubes as well as from the parietal peritoneum on both sidesabove and below the navel, the diaphragm and the testis. Sections were takenperpendicular to the peritoneal surface from the samples from the parietal peritoneumand the intestines. Selected sections were also cut at a right angle to these, parallel tothe plane of the fibres of the LEP so that they were vizualised 'en face'. Followingparaffin embedding, the sections were submitted to a variety of elastic stains, Weigert'sor Verhoefls stains with or without Van Gieson Hansen counterstain being usedroutinely, supplemented by Orcein or Victoria Blue as required.

Because of the state of preservation of the autopsy samples, a supplementary seriesof slides from grossly normal areas of organs covered with peritoneum removed atoperation stomach, small and large intestine, appendix, spleen, gall bladder, testis,uterus and the fallopian tubes-was investigated. The organs examined in this serieswere removed either because of disease in the vicinity, for technical reasons or

* Reprint requests to Dr Peter J. T. Knudsen, Institute of Forensic Medicine, University of Aarhus,Finsensgade 15, DK 8000, Aarhus C, Denmark.

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P. J. T. KNUDSEN

following trauma. The operation samples were stained in the same way as those fromthe autopsy cases.

RESULTS

In sections cut parallel to the plane of the fibres of the LEP, it was found that thelayer consisted of elastic fibres running at various angles to each other (Fig. 1).Frequently a dominant direction could be demonstrated, but this was not veryconsistent, and no reliable indication of a dominant direction for any one organ wasfound.

In the serosa of the stomach, the wall of which contains large amounts of elastictissue, an elastic layer consistent with the LEP was found, most distinct in areas wherefatty tissue or connective tissue separated the serosa from the external muscular layer(Fig. 2). This was discernible only with difficulty where the serosa lay immediatelyadjacent to the musculature. At sites where a transition between the two was found,such as where ligaments are attached to the stomach wall, the LEP could easily befollowed from them into the serosa of the stomach.The LEP was easily demonstrated in every section in the small as well as in the large

intestine (Figs 3 and 4), as was to be expected from previous observations (Morson &Dawson, 1979). By extending the sections from the intestinal wall along the mesenteryit was seen that the LEP did not encircle the intestine, but could be followed all theway to the posterior abdominal wall, where it continued as part of the parietalperitoneum. The LEP of the small intestine in particular was a very well-definedstructure, consisting of quite thick elastic fibres running in parallel with thinner fibresconnecting them. The main direction was subject to considerable variation.

In the appendix a very delicate LEP was found, behaving exactly like that of thelarge intestine, i.e. in continuity with that of the mesenteriolum appendicis and notmaking a complete circle. In the liver and spleen, both of which have a thick coveringof connective tissue containing elastic tissue as one of its main components, the LEPwas indistinguishable, but at the attachments of both organs, where the connectivetissue ligaments blend into the capsule, the LEP could easily be followed as itseparated itself from the many layers of elastic and connective tissue and continued asa single layer of elastic tissue, similar to that seen in the intestine.

In the wall of the gall bladder, however, which is composed of a much looserconnective tissue, the LEP was found under the mesothelium as in the intestines, andcould be followed as the peritoneum was reflected to the surface of the liver.The pancreas, situated retroperitoneally, behaved quite like the intraperitoneal

organs. The LEP was remarkably easy to find, even in the autopsy cases whereconsiderable autolysis was seen. The nonpregnant uterus and the fallopian tubes werevery similar to the liver and spleen, the LEP being hard to distinguish on the organ

Fig. 1. Left. The elastic fibres of the mesentery in plan view, showing a general longitudinalorientation of the thicker fibres. Verhoeff's elastic stain x 180.Fig. 2. Right. The elastic fibres of the serosa of the stomach at the attachment of one of theligamentous folds of the peritoneum. Note that the fibres follow the surface, not the muscle layersof the stomach. Orcein x 90.Fig. 3. Left. The very well developed elastic layer of the small intestine forming a near continuousband in the serosa. Orcein x 180.Fig. 4. Right. The attachment of the mesocolon to the colon. The elastic layer is seen to continuefrom the intestinal serosa into the mesentery, leaving the area between the attachments without acircular elastic layer. Weigert's elastic stain x 90.

42

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Peritoneal elastic lamina

2

x P t.h

A; :;tIbt t

'is.:. (4

Figs. 14. For legend see opposite.

43

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proper, but easily found in the attachments. Finally, the bladder displayed aprominent LEP in the peritoneal covering.The parietal peritoneum was sampled widely, since nothing was known previously

as to the LEP in the parietal peritoneum. All the samples displayed a well-demarcatedLEP, with no predilection for particular sites as to the shape, direction or size of thefibres.The testes are intraperitoneal in origin but in descending take with them a part of

the investing peritoneum, the tunica vaginalis. Accordingly samples were taken toinvestigate whether the elastic layer of the peritoneum was part of the tunica vaginalis.In the sections a similar elastic tissue was found, scant but consistent. For comparisonrandom samples were removed from the pleura and the pericardium. A similar elasticlayer is known to exist there and was very easy to demonstrate, especially in the pleura.

DISCUSSION

While elastic tissue has been studied intensively in some parts of the body both innormal subjects and in some disease states, such as in vessel walls, the lungs, and inthe breast in patients with carcinoma, the elastic tissue of the peritoneum has not beenthe subject of very great interest. The presence of elastic tissue in the peritoneum wasnoted in studies of the gastrointestinal tract at the end of the nineteenth and in thebeginning of twentieth century (Dobbertin, 1896; Legge, 1897; Livini, 1899; Patzelt,1936), but the existence of a distinct membranous or reticular structure in theperitoneum of man, analogous to that of the pleura (Spencer, 1977; Thomas, 1987) orof the pericardium (Ferrans, Ishihara & Roberts, 1982; Thomas, 1987), has only beennoted by few, and no systematic study of the topographical distribution of thestructure has previously been undertaken. In animals, however, the presence of elastictissue beneath the mesothelium of the peritoneum has been described (Rhodin, 1974)and its presence has been used for experimental purposes (Parsons et al. 1983). Whilethe elastic tissue in the peritoneum of man has been mentioned mainly in the intestinalserosa (Morson & Dawson, 1979), its alleged presence in the human parietalperitoneum (Seifert, 1927) has only once been convincingly demonstrated (Dobbieet al. 1981; Thomas, 1987).The investigations described in this paper are concerned mainly with the topography

of the LEP, because the acceptance of the presence of the structure as a normalanatomical entity is the prerequisite for its use in experimental and clinical work. TheLEP is found ubiquitously in the visceral and parietal peritoneum, but developed toa variable extent, according to the properties of the organ it covers. As may beexpected, the LEP is most prominent in organs in which a considerable and rapidchange of volume takes place, as in the intestines and the gall bladder, while it is lessprominent or discernible only with difficulty in static or nearly static organs such asthe uterus, appendix, liver, spleen, etc. It is worth noting, however, that at theattachments of peritoneum, the LEP is easily demonstrated. It can, for example, befollowed from the parietal peritoneum of the posterior abdominal wall, along theligaments of the porta hepatis or the spleen until it merges with the copious elastictissue of their capsules.The stomach is in an intermediate category, being an organ with large variations in

size and shape; but as the serosa covering the stomach is scanty, and the elastic tissueof the stomach wall plentiful, the LEP may be hard to demonstrate. As is the case withthe liver and the spleen, the peritoneal attachments at the lesser and greater curvatures

44 P. J. T. KNUDSEN

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Peritoneal elastic lamina 45consistently display an LEP and by following it from there, it may be seen to continueinto the serosa of the stomach.

In the parietal peritoneum the LEP may be followed from the intestinal serosa alongthe mesentery to the abdominal wall, as has been illustrated in animals (Rhodin, 1974).It can be found all over the parietal peritoneum, which may have significance for thosemaking peritoneal biopsies.For normal anatomical purposes the LEP is useful, since we can now safely assume

that the peritoneum includes LEP. The LEP should also be useful for clinical work.It may provide a baseline for measuring the thickness of the peritoneum in variousirritative conditions, for example, in patients undergoing continuous ambulatoryperitoneal dialysis (CAPD), or it might give an indication of the extent of metastaseswithin the abdominal cavity. Knowledge of the LEP might be useful for studies oftransport of particulate matter across the peritoneum (Parsons, Marko, Braun &Wansor, 1982; Parsons, Marko, Rademacher & Frank, 1985).

In relation to nomenclature, it seems preferable for the present to retain thenonspecific term lamina or layer, permitting a more precise term to be devised later.

SUMMARY

The structure and extent of the submesothelial elastic tissue of the peritoneum,tentatively termed the peritoneal elastic lamina (lamina elastica peritonei, LEP), wasstudied in autopsy and biopsy material by light microscopy. The investigationconfirms the presence of a well-defined network of elastic fibres just beneath thebasement membrane of the visceral and parietal peritoneum in man. The LEP isclaimed to be analogous to similar elastic tissue in other serosal cavities, the pleura andthe pericardium, as previously described. The LEP may be useful for normalanatomical as well as pathoanatomical investigations.

The inspiration and support of my senior colleagues at the Institutes, particularlyDr Peter Stubbe Teglbjaerg, Aalborg Hospital, the technical assistance of Mrs K.Ugilt, Hj0rring Hospital, and the photographic assistance of Mrs A. Dalmose and MrS. Shapiro, Aarhus Municipal Hospital, are gratefully acknowledged. This study waspreviously presented in part at the PAX-Conference on Peritoneal Access, Lund,Sweden, in June 1987.

REFERENCES

DOBBERTIN, R. (1896). Ober die Verbreitung und Anordnung des elastischen Gewebes in den Schichten desgesamten Darmkanals. Rostock: Universitats-Buchdruckerei von Adler's Erben.

DOBBIE, J. W., ZAKI, M. & WILSON, L. (1981). Ultrastructural studies on the peritoneum with special referenceto chronic ambulatory peritoneal dialysis. Scottish Medical Journal 26, 213-223.

FERRANS, V. J., IsHIHARA, T. & ROBERTS, W. C. (1982). Anatomy of the pericardium. In Pericardial Disease(ed. P. S. Reddy, D. F. Leon & J. A. Shaver), pp. 15-29. New York: Raven Press.

LEGGE, F. (1897). Sulla distribuzione topografica dellefibre elastiche nelrapparecchio digerente. Cagliari: Tip.Muscas di P. Valdes.

LIVINI, F. (1899). Sulla distribuzione del tessuto elastico in varii organi del corpore umano. Monitore ZoologicoItaliano 10, 12-23.

MORSON, B. C. & DAWSON, I. M. P. (1979). In Gastrointestinal Pathology, pp. 228 and 492. Oxford: Blackwell.PARSONS, D. F., MARKO, M., BRAUN, S. J. & WANSOR, K. V. (1982). Ascites tumor invasion of mouse

peritoneum studied by high-voltage electron microscope stereoscopy. Cancer Research 42, 4574-4583.PARSONS, D. F., MARKO, M., RADERMAcHER, M. & FRANK, J. (1985). Shape changes and polarization of cells

migrating through tissue. A high-voltage electron microscope and computer graphics study of serial thicksections. Tissue and Cell 17, 491-510.

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PARSONS, D. F., MARKO, M. & WANSOR, K. (1983). Elastic reticulum and collagen of normal mouseperitoneum. Micron 14, 1-10.

PATZELT, V. (1936). Der Darm. In Verdauungsapparat, Handbuch der mikroskopischen Anatomie des Menschen(ed. W. von Mollendorf), Part 3, pp. 292-296. Berlin: Springer.

RHODIN, J. A. G. (1974). In Histology; A Text and Atlas, p. 576. London: Oxford University Press.SEIFERT, E. (1927). Peritoneum einschliesslich Netz. In Verdauungsapparat, Handbuch der mikroskopischenAnatomie des Menschen (ed. W. von Mollendorf), Part 1, pp. 337-360. Berlin: Springer.

SPENCER, H. (1977). In Pathology of the Lung, p. 77. Oxford: Pergamon Press.THOMAS, N. W. (1987). Embryology and structure of the mesothelium. In Pathology of the Mesothelium (ed.

J. S. P. Jones). Berlin, Heidelberg: Springer.