Original Scientific Article

Abdominal Adhesions to Prosthetic Mesh Evaluated by Laparoscopy and Electron Microscopy

Michael L Baptista, MD, Margaret E Bonsack, MS, Isaac Felemovicius, MD, John P Delaney, MD, PhD, FACS

Background: Most adhesion experiments involve observations at a single time point. We developed a method to evaluate abdominal adhesions to surgical mesh by sequential laparoscopy.

Study Design: An abdominal wall defect was created in rats and repaired with polypropylene mesh. Sequential laparoscopic evaluation of adhesion formation was performed in each animal. The percentage of mesh area involved was scored (0% to 100%). At various time intervals animals were sacrificed and samples were obtained for light and scanning electron microscopy.

Results: Adhesions were already present on day 1, increased by day 7, and did not progress thereafter. Mesh surfaces free of adhesions were covered with a confluent mesothelial cell layer, first seen by scanning electron microscopy on day 5 and complete by day 7.

Conclusions: Intraabdominal adhesions are best studied by sequential laparoscopy. Adhesions develop within 1 day of prosthesis placement. Adhesion-free surfaces are carpeted with mesothelial cells by day 7 and remain free thereafter, for duration of study.


Abdominal wall hernias can often be repaired by suture approximation of the edges of the defect. But this approach is followed by a high incidence of recurrent herniation.1 The use of permanent synthetic prosthetic mesh materials provides a more secure repair, particularly for large defects.1,2 Frequently, there is no viable tissue available to separate the synthetic material from direct contact with the abdominal viscera, in which circumstance, adhesions of omentum and intestine always develop. One potential complication of such adhesions is intestinal obstruction. A more serious problem is that of intestinal fistulization through the junction of the prosthetic material with the abdominal wall.3-5

The most commonly used meshes are knitted, are macroporous, are synthesized from polypropylene or polyethylene, and share the potential for causing intestinal complications.3,5,6 An ideal prosthesis would not induce intraabdominal adhesions but at the same time would firmly incorporate into the abdominal wall. Smooth-surfaced impermeable materials, such as silicone, which effectively resist adhesion formation, do not develop the necessary fixation to the adjacent fascia and muscle.

Several experimental models have been used to investigate these issues.7-9 Time intervals for observation after prosthesis installation have varied from hours to months, but always involved a single observation per animal. We suggest here that adhesion formation is better studied by sequential observations than at a single arbitrary time.

The purpose of this article is to describe the dynamics of visceral adhesion formation to polypropylene mesh. The major innovation reported here is the use of repeated peritoneoscopy to allow serial observations and surgical manipulations of adhesions. The first set of experiments addressed the questions: 1) What role does omentum play in adhesion formation? and 2) What is the significance of the tissue backing the porous prosthesis, ie, peritoneum versus subcutaneous tissue? These observations were made at necropsy. The second group of studies involved repeated laparoscopy to determine adhesion dynamics, and timed sacrifice to obtain tissues for scanning electron microscopy of the prosthetic surface.

METHODS

Animals

Female Sprague-Dawley rats weighing between 275 and 325 grams were used. All rats were kept at least 1 week before operation to adjust to the laboratory environment. During this time they received standard lab chow and water, ad lib. They were housed in a temperature- and humidity-controlled environment with a 12-hour light-dark cycle. The animals were cared for by the University of Minnesota Research Animal Resources Department in accordance with the principles in the Guide For Care and Use of Laboratory Animals, NIH publication, revised 1993.

Surgical technique

Rats were anesthetized with an IP injection of sodium pentobarbital (30 to 40mg/k). The abdomen was shaved with an electric clipper and prepared with povidine-iodine solution. Procedures were done under aseptic conditions.

Abdominal wall resection and omentectomy: necropsy studies

Preliminary studies were done to assess the effects, with respect to adhesions, of the tissue backing the porous mesh—subcutaneous tissue versus peritoneum. It was our initial impression in this rat model that omentum had a greater propensity to adhere to polypropylene mesh than did intestine. This proposition was tested by removing the omentum in some animals.

In one group the polypropylene mesh was sewn around its periphery to the peritoneal surface on either side of a midline incision. Peritoneum, muscle, and skin were then reapproximated, so the prosthetic material had underlying peritoneum. In other animals an abdominal wall defect was created, preserving the skin and subcutaneous tissue but excising muscle and peritoneum. The outer surface of the mesh was exposed to the subcutaneous tissue rather than to peritoneum, mimicking the clinical situation. In another group of rats omentectomy was performed to observe the consequences on adhesion formation. So, four preparations were studied: with or without abdominal wall resection and with or without omentectomy. The groups were prepared sequentially with no attempt at randomization. Adhesions to mesh were evaluated by sacrificing the animals 30 days or more after operation. Data were analyzed and groups compared by two-way analysis of variance followed by inspection of differences between pairs of means by Duncan's multiple range test.

Adhesion dynamics: laparoscopy

In subsequent studies we used the model found to have maximum adhesion formation, namely, abdominal wall resection and preserved omentum. These animals were studied by repeated laparoscopy starting at day 1 and at chosen intervals, 3, 7, 14, and 28 days after mesh installation. Additional animals were subjected to this preparation and sacrificed at days 1, 3, 5, 7, 14, and 28 solely to obtain samples for scanning electron microscopy. The rats were arbitrarily designated as to sacrifice date at the time of mesh placement.

Technical considerations

Pilot studies demonstrated that interrupted sutures encouraged omentum or intestine to adhere to the cut edge of the prosthetic material, occasionally even to permit visceral herniation between sutures into the subcutaneous space. We subsequently used continuous monofilament polypropylene suture, everting the edge of the prosthesis and the cut edge of the abdominal wall away from the abdominal cavity. Even with this method there was some propensity for adhesions to form at the abdominal wall to prosthesis intersection.

A technical detail that proved important was that of skin closure. Some investigators have reported problems with skin dehiscence in the rat after laparotomy.8-10 In our hands, the association of an abdominal wall defect, polypropylene mesh, and simple skin approximation with interrupted or running nonabsorbable material frequently failed because the animal chewed on the sutures with resulting skin separation. The use of running intradermal absorbable suture eliminated this problem. An associated observation was that when the skin edges did separate and expose the mesh, extensive dense adhesions covered the intraabdominal surface under the exposed area. So any animal that developed skin dehiscence was discarded from further consideration. Of the 28 animals prepared for these studies 3 were eliminated because of skin breakdown (Table 1).

Table 1. Effect of Omentectomy and Abdominal Wall Resection, or Both, on the Area of Polypropylene Mesh Involved with Adhesions


    Mean  
   
 
Group No. of animals n % Range (%)

O + AWR + 7 8* 48 18–75
O – AWR + 7 3* 93 5–100
O + AWR – 5 10* 16 0–51
O – AWR – 6 13  67 25–100


* Values are significantly different from each other, p < 0.05. AWR, abdominal wall resection; O, omentectomy. Data are means with standard error of the mean in parentheses.

Laparoscopy

To test the tolerance of the rat to abdominal insufflation for laparoscopy a bulb pump was used to inject room air. A 25-gauge needle was inserted into the abdominal cavity and room air was slowly instilled while ventilatory rate and pattern were observed. Intraabdominal pressure up to 20 mmHg did not cause respiratory alterations. Seven mmHg was found to provide enough space for laparoscopic observations; subsequent exams were done without pressure measurements, simply instilling sufficient air to allow the needed visualization.

To accomplish the examination, an 8-mm skin incision was made in the flank 4 cm lateral to the umbilicus. A 5-mm Auto Suture Surgiport (Auto Suture Co, Norwalk, CT) beveled cannula was inserted, through which a 4-mm Comeg arthroscope (American Medical Endoscopy, Miami Beach, FL) was introduced. A Karl Storz Xenon Light Source 610 (Karl Storz Endoscopy-America, Culver City, CA) was attached. Observations were video recorded.

Magnification obtained with this set-up varied depending on the distance from the end of the scope to the tissue. With the tip close to the observed surface, magnification on the monitor was approximately 80 times. This allowed remarkably clear visualization of the microvasculature.

To quantitate adhesions, the prosthetic patch was visually divided into four equal quadrants (Fig. 1). Adhesions covering the mesh were estimated according to area of attachment, ranging from 0% to 100% (no adhesions to completely covered). The intraabdominal structure involved, omentum or intestine, location of adhesions, and surface appearance of uninvolved mesh were noted and recorded. After the examination was completed the scope and cannula were removed and the skin closed.

Figure 1

Figure 1. Laparoscopic images obtained on days 7, 14, and 28 after initial operation. The mesh is visually divided into four equal quadrants and adhesion area estimated. The edematous omentum on day 7 becomes translucent on days 14 and 28, exposing to the view the fibers of the underlying mesh. Individual fibers of the polypropylene mesh are easily seen, as is the vasculature, an advantage of laparoscopy.

Adhesiolysis

One group of six rats was studied for reformation of adhesions after laparoscopic adhesiolysis 1 week after abdominal wall resection and initial mesh placement and at intervals thereafter to assess possible reformation of adhesions. In this study, the firmness of the adhesions was scored on a scale of 1 to 3. A score of 1 meant they were loosely adhered and came free when the abdomen was inflated or by gentle probing with the tip of the scope. A score of 2 indicated moderate adherence such that the tissues required separation with a grasper and more vigorous blunt dissection. A score of 3 indicated firmly attached strong adhesions that had to be divided sharply. Hemostasis was obtained by compressing an instrument against the site of bleeding. Cautery was not used to avoid new adhesion formation secondary to thermal injury.

Histology

Animals were sacrificed with 100mg/kg IP injection of sodium pentobarbital. The abdomen was opened approximately 2cm from the prosthesis on the caudal and both lateral aspects of the prosthesis. The abdominal wall was carefully lifted in order to observe and score adhesions to the mesh. The entire prosthesis, adjacent abdominal wall, and adherent structures were then completely removed by incising 2cm from the cephalad edge of the polypropylene. The specimens were rinsed in saline, pinned on corkboards, and fixed in 10% neutral buffered formalin for 48 hours. They were cut into quarters to produce four samples, each of which included normal abdominal wall, prosthesis, and the transition area between. Tissues were routinely processed in an Autotechnicon (The Technion Co, Chauncey, NY) and embedded in paraffin. Samples were sectioned at 5 micrometers and stained with hematoxylin and eosin. To focus on collagen, a second set of slides was stained with sirius red plus hematoxylin according to the method of Junqueira and associates.11 Sirius red is a strong anionic dye with sulphonic acid groups that stains collagen by reacting with basic groups in the collagen molecule. Collagen birefringency was enhanced by polarization. Histologic specimens were evaluated by a microscopist who was always unaware of their origin.

Scanning electron microscopy

One rat was sacrificed on postplacement days 1, 3, 5, and 14, two on day 28, and three on day 7. Tissues were prepared for scanning electron microscopy as follows. Immediately after opening the abdomen the surgical mesh and surrounding area were flooded with 2.5% glutaraldehyde in 0.1M cacodylate buffer. A 1×1-cm sample of mesh, including an area with and another without adhesions, was removed and put in fresh glutaraldehyde buffer fixative overnight. The sample was then rinsed in 0.1M cacodylate buffer 3 times for 20 minutes each, and postfixed on ice with 1% osmium tetroxide in 0.1M buffer for 30 minutes. Samples were then rinsed in buffer, dehydrated in increasing alcohol series (50%, 70%, 80%, 95%, and 100%), and critical point dried in a Tousimis Model 780 A (Tousimis Research Corporation, Rockville, MD). Sputter coating with gold and palladium particles of 10nm was done. Observations and photographs were obtained using a Hitachi S-450 S and a Hitachi 4700 computerized scanning electron microscope (Hitachi Instrument Inc, Nissei Sangyo America, Ltd, Mountain View, CA).

RESULTS

Single observations at sacrifice: omentectomy and abdominal wall resection

In the absence of omentum, adhesions to the mesh were significantly fewer with or without abdominal wall resection than if omentum had been preserved. When the omentum was present, adhesions were far more prevalent if the abdominal wall had been resected. The most extensive adhesion formation to the surgical mesh developed with the combination of abdominal wall resection and intact omentum (range 75% to 100%) (Table 1).

Laparoscopic observations

Adhesions previously seen laparoscopically were compared with postmortem observations in the same animals. Necropsy observations tended to underestimate adhesion area. Details such as the presence of adipose cells, which identified adherent omentum, were seen with laparoscopic magnification but could not be appreciated at autopsy. The thin clear membranous omentum once adhered to the mesh was difficult to recognize as an adhesion by a single observation at necropsy but was readily identified by sequential laparoscopy.

Adhesions tended to attach first to the mesh and abdominal wall interface, then extended to cover larger areas of the mesh surface. It was very unusual to see adherence to the central surface without edge involvement.

At laparoscopy 24 hours after operation one could appreciate tissue swelling and initial growth of microvessels along the cut edge of the muscle. Some omental adhesions were invariably present by 24 hours. Adhesion-free areas of mesh had a shiny translucent surface. The interstices were sealed, as evidenced by the fact that no injected intraperitoneal air escaped through the mesh into the subcutaneous space, judged by inspection and palpation. In some instances a seroma was already present in the subcutaneous space contained there by the now relatively impermeable mesh.

Three days after placement of the prosthesis, microvessels could be seen growing onto the surface from the cut edge of the peritoneum. By day 7, the area involved with adhesions had increased compared with days 1 and 3. Blood vessels growing from the wound edges toward the center of the prosthetic patch were beginning to anastomose with omental vessels. Blood flow in small arteries was generally from the abdominal wall toward the adhesions, but in some animals bidirectional flow could be seen.

By day 14 edema and inflammation had subsided. There was no change in the extent of adhesions as compared with day 7. Microvascular anastomoses were more extensive.

On day 28 adhesions to the mesh were identical to those found on days 7 and 14. Strands of polypropylene were readily visible through the now translucent omentum (Fig. 1). At this time the adhesions had become firmly fixed to the mesh. The initial erythema and edema had disappeared. Wound contraction was evident from the fact that the center of the mesh folded inward toward the abdominal cavity and the original 2.5×2.5-cm abdominal wall defect was now diminished in size.

Table 2 summarizes the laparoscopic estimations of mesh area involved with adhesions. The most important observation is that those areas free of adhesions on day 7 remained so on subsequent examinations; that is, the adhesions did not progress.

Table 2. Percent of Polypropylene Mesh Area Covered by Adhesions Estimated by Laparoscopy after Abdominal Wall Resection with Preservation of Omentum


  Observation day
 
  1 3 7 14 28

n 7 4 25 23 23
Mean, % (range) 58
(5–100)
84
(67–100)
91
(75–100)
90
(75-100)
91
(75–100)

Light microscopy

Histologic preparations were difficult to obtain on day 1 because of weak attachment of the prosthetic fibers to the abdominal wall. During processing the mesh separated from the fragile adhesions and from the abdominal wall. Adequate histologic specimens were first obtainable on day 3, at which time the fibers of the mesh were seen to be coated by adhesions or by scattered cells, mostly neutrophils and fibroblasts. Macrophages were more prominent than on day 1. The samples did not yet demonstrate significant collagen deposition as judged by polarizing microscopy of sirius red stained samples.11

On day 7 inflammation was still present but the population of neutrophils had decreased. Macrophages were prominent around the polypropylene fibers (Fig. 2). Some fibroblasts were present but little collagen had yet infiltrated between mesh fibers.

Figure 2

Figure 2. Histology of the abdominal wall with polypropylene mesh. On days 1 and 3 inflammatory cells surround mesh fibers. On day 7 inflammation is still present but the predominant cells are macrophages. On day 28 most of the acute inflammation has subsided and histiocytes are now prominent. Hematoxylin and eosin stain, original magnification ×100.

Tissues harvested on day 28 had well-formed collagen interposed between the threads, along with macrophages and fibroblasts. The mesh was firmly incorporated into the abdominal wall by fibrous tissue. At the intersection of the sutured junction collagen was more abundant than at the center of the mesh (Fig. 3).

Figure 3

Figure 3. Distribution of collagen on day 28 shown by polarizing microscopy. The density of collagen is maximal at the muscle-mesh interface, seen as white to light gray. Arrows point to the muscle wall prosthesis intersection. The holes left behind by the individual mesh fibers after histologic preparation are marked with asterisks. Picrosirius red stain, original magnification ×40.

Adhesions always involved omentum and sometimes intestine. The bumpy adhesion-free surface seen at laparoscopy proved on histology to represent mesh fibers surrounded by histiocytes and fibrous tissue. The surface of the prosthesis facing the abdominal cavity demonstrated a layer consistent with mesothelial cells.

Scanning electron microscopy

On day 1 after operation, the polypropylene threads of the mesh were bare, as seen at low magnification scanning electron microscopy. Most of the polypropylene was directly exposed, with no tissue coverage. Omentum was attached to the mesh-abdominal wall interface with an abundant framework of fibrin. Fibroblasts were present in small numbers. Leukocytes were apparent in the spaces between the polypropylene threads. Few cells were attached to the mesh fiber surfaces at this time. Mesothelial cells were not yet identifiable.

On day 3 most of the surface of the polypropylene mesh was covered by a thin layer of tissue. Fibroblasts had increased since day 1, mostly in the crevices between mesh fibers. The fibrin framework was more dense, and it extended onto the areas free of adhesions. Still no mesothelial cells could be seen. By day 5 the entire surface of the mesh was covered and mesothelial cells had appeared (Figs. 4 and 5). Their characteristic microvilli were relatively sparse.

Figure 4

Figure 4. Scanning electron microscopy of an adhesion-free surface at low magnification on days 1, 3, and 5. On day 1 after operation, the mesh fibers are readily seen with few attached cells. The fibers are partially covered on day 3. On day 5 they are completely coated with a cellular layer (original magnification ×30).

Figure 5

Figure 5. Scanning electron microscopy of the prosthesis surface on days 7 and 28 after implantation. On day 7 the surface of the mesh shows elevations corresponding to the polypropylene fibers (original magnification ×25). Detail of this adhesion-free area demonstrates the surface to be completely carpeted with mesothelial cells (original magnification ×1,500). Depressions are seen on the surface corresponding to the interstices of the mesh (original magnification ×15). The surface on day 28 is covered with mesothelial cells as on day 7 (original magnification ×1,200).

By day 7 there were no bare polypropylene fibers. Leukocyte infiltration had subsided. The surface of the mesh was covered with a confluent carpet of mesothelial cells with abundant microvilli (Fig. 5). The surface on day 14 was similar to that seen on day 7.

On day 28 the abdominal surface of the mesh and the holes around the mesh fibers were covered by mesothelial cells (Fig. 5). Microvilli were more dense than on day 7. Macrophages were seen adjacent to omental adhesions.

Adhesiolysis

One week after mesh installation at least 75% of the surface was covered by adhesions. After mechanically separating the adhesions from the mesh subsequent exams demonstrated only a few small, newly formed adhesions. In 19 observations after day 21, no new adhesions developed (Table 3).

Table 3. Percent of Mesh Area Covered by Adhesions after Adhesiolysis


Day 7 14 21 28 100 280

1 73% (3) 7% (2) 0% (0) 6% (1) 0% (0) 0% (0)
2 100% (3) 25% (1) 0% (0) 0% (0) 0% (0) 0% (0)
3 94% (3) 0% (0) 0% (0)
4 94% (3) 0% (0) 0% (0) 0% (0) 0% (0)
5 92% (2) 0% (0) 14% (1) 0% (0) 0% (0) 0% (0)
6 98% (2) 0% (0) 4% (1) 0% (0) 6% (–) 6% (–)
Mean 92% 4% 3% 1% 1% 1%

Lysis was performed whenever adhesions were found. The percentages represent the area of adhesions before lysis. Of the 21 exams performed after the initial seventh day adhesiolysis, 17 showed no further adhesions. Adhesiolysis scores are in parentheses: 0, no adhesions; 1, freed with inflation or scope tip; 2, required grasper blunt dissection; and 3, required sharp dissection.

DISCUSSION

A provocative finding was that adhesion formation did not progress after day 7. Any area of mesh surface free of adhesions then remained so thereafter. The uninvolved surface was shiny and translucent. These observations indicate that an adhesion-resistant intraabdominal surface develops on polypropylene mesh within a week of installation. One might speculate that fairly short-lived protection by mechanical separation or biochemical inhibition could result in permanent freedom from adhesions between prosthetic mesh and abdominal viscera. Along the same lines, the adhesiolysis study suggests that if one were to mechanically break down adhesions to prosthetic mesh after 7 days, they would likely not reform. Such is not the case when visceral adhesions to injured peritoneum are divided. Both clinical and experimental observations indicate that subsequent to such lysis newly formed adhesions are often more extensive than the original.12,13

Laparoscopic findings of progression of adhesions up to day 7 and a stable adhesion-resistant surface thereafter correlates with the scanning electron microscopic findings of a mesothelial cell coating, which is not complete until then.

That mesothelial cells prevent adhesions is well documented.14-16 Human omental mesothelial cells in vitro produce hyaluronic acid.14 Jones and colleagues14 noted that ovarian cancer cell adherence in multiwell plates was prevented by a confluent mesothelial cell culture. The content of hyaluronic acid in the medium was found to be elevated. After hyaluronidase pretreatment the blocking of adhesions was abrogated.

Whitaker and associates15 reported that a pure culture of mesothelial cells was able to induce fibrinolysis. Another study16 suggested that the mesothelial fibrinolytic properties are associated with the secretion of tissue plasminogen activator. These results likely explain the observation that once the polypropylene mesh surface is populated with mesothelial cells it remains resistant to new adhesions.

In a relevant study by Raftery,13 a parietal peritoneal defect was surgically created. Sequential transmission electron microscopy was used to study healing. On postoperative day 3 a "primitive mesenchymal cell" appeared on the surface. On day 4 these cells were seen to have some microvilli. By day 5 mesothelial cells with mature microvilli were identifiable. By day 8 and later a complete layer of mesothelial cells covered the defect. The new mesothelium was believed to arise from subperitoneal connective tissue, whether from primitive mesenchymal cells or from fibroblasts was uncertain.13 These observations are in agreement with the time course of mesothelial cell coverage of prosthetic mesh observed in the present study.

Time of observation: sequential laparoscopy versus sacrifice

Adhesion formation is a dynamic process and sequential evaluation over an extended period of time provides important information. We found that peritoneoscopy could be undertaken at any chosen interval after placement of the prosthesis, allowing repeated in vivo observations of adhesion development. Information with respect to angiogenesis and blood flow in the microvasculature can be assessed nicely with the high magnification obtained at laparoscopy. The early time course, site, and progression of adhesion formation can be determined only with repeated in vivo visualization. Such ongoing changes are impossible to appreciate by single observations at sacrifice. Because variations occur among subjects, sacrifice with a single observation time and averaging the results is less meaningful than laparoscopic observations, where each animal provides multiple data points.

The extent of adhesions may be underestimated at necropsy exam. The thin transparent omental membrane once firmly incorporated onto the mesh may be recognized as an adhesion only if previously observed during early stages of attachment.

In conclusion, evaluation of intraabdominal adhesions to prosthetic mesh is best accomplished by means of sequential laparoscopy with each animal serving as its own control. Adhesions are already present 24 hours after operation. The area involved progresses during the first week. Segments of prosthetic mesh surface free of adhesions at 7 days remain uninvolved thereafter. The development of an adhesion-resistant surface coincides with formation of a confluent mesothelial cell coating. After mechanical separation (adhesiolysis), very few new adhesions form between abdominal viscera and prosthetic mesh. In this model, omentum has a greater propensity to adhere to mesh than does intestine and tends to attach first at the mesh abdominal wall interface.

References

1. Mudge M, Hughes LE. Incisional hernia: A 10-year prospective study of incidence and attitudes. Br J Surg 1985;72:70-1.

2. Bendavid R. The need for mesh. In: Bendavid R, ed. Prostheses and abdominal wall hernias. Austin, TX: RG Landes Company; 1994:116-122.

3. Karakousis C, Volpe C, Tanski J, et al. Use of a mesh for musculoaponeurotic defects of the abdominal wall in cancer surgery and the risk of bowel fistulas. J Am Coll Surg 1995;181:11-16.

4. Kaufman Z, Engelberg M, Zager M. Fecal fistula: a late complication of Marlex mesh repair. Dis Colon Rectum 1981;24:543-544.

5. Stone HH, Fabian TC, Turkleson ML, Jurkiewicz MJ. Management of acute full-thickness losses of the abdominal wall. Ann Surg 1981;193:612-618.

6. DeBord JR. Prostheses and hernia surgery: the evolution of the ideal material. In: Bendavid R, ed. Prostheses and abdominal wall hernias. Austin, TX: RG Landes Company; 1994:7-32.

7. Law NW, Ellis H. Adhesion formation and peritoneal healing on prosthetic materials. Clinical Materials 1988;3:95-101.

8. Simmermacher R, Lei B, Schakenraad J, Bleichrodt R. Improved tissue ingrowth and anchorage of expanded polytetrafluorethylene by perforation: an experimental study in the rat. Biomaterials 1991;12:22-24.

9. Meddings RN, Carachi R, Gorham S, French DA. A new bioprosthesis in large abdominal wall defects. J Pediatr Surg 1993;28:660-663.

10. Pans A, Pierard GE. A comparison of intraperitoneal prostheses for the repair of abdominal muscular wall defects in rats. Eur Surg Res 1992;24:54-60.

11. Junqueira ICU, Bignolas G, Brentani RR. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 1979;11:447-455.

12. Chmielewski G, Saxe J, Dulchavsky S, et al. Fibrin gel limits intra-abdominal adhesion formation. Am Surg 1993;58:590-593.

13. Raftery AT. Regeneration of parietal and visceral peritoneum: an electron microscopical study. J Anat 1973;115:375-392.

14. Jones LMH, Gardner MJ, Catterall JB, Turner GA. Hyaluronic acid secreted by mesothelial cells: a natural barrier to ovarian cancer cell adhesion. Clin Exp Metastasis 1995;13:373-380.

15. Whitaker D, Papadimitriou JM, Walters M. The mesothelium: its fibrinolytic properties. J Pathol 1982;136:291-299.

16. van Hinsberg VW, Kooistra T, Scheffer MA, et al. Characterization and fibrinolytic properties of human omental tissue mesothelial cells. Comparison with endothelial cells. Blood 1990;75:1490-1497.

Genzyme Corporation supplied some laboratory material; no author has any relationship with the company.

Received May 19, 1999; Revised September 20, 1999; Accepted October 1, 1999.

From the Department of Surgery, University of Minnesota Medical School, Minneapolis, MN, USA.

Correspondence address: John P Delaney, MD, PhD, FACS, University of Minnesota, FUHC, Box 89, 420 Delaware St SE, Minneapolis, MN 55455.

 

JACS

 


This page and all contents are Copyright © 1996-2000
by the American College of Surgeons, Chicago, IL 60611-3211