expanded polytetrafluoroethylene is an effective barrier in preventing pelvic adhesions after...

Expanded polytetrafluoroethylene is an effectivebarrier in preventing pelvic adhesions after radicalsurgery for ovarian cancerB. J. MONK,* J. M. FOWLER,† R. A. BURGER,‡ K. F. McGONIGLE,§ G. L. EDDY# & F. J. MONTZ¶*Division of Gynecologic Oncology, Department of Obstetrics and Gynecology Southwest Cancer Center, Texas TechUniversity Health Sciences Center, Lubbock, Texas, 79430; †Division of Gynecologic Oncology, Department ofObstetrics and Gynecology University of Minnesota, Minneapolis, Minnesota, 55455; ‡Division of GynecologicOncology, Department of Obstetrics and Gynecology University of California Irvine Medical Center, Orange,California, 92668; §Department of Gynecology, Division of Surgery City of Hope National Medical Center, Duarte,California, 91010; #Division of Gynecologic Oncology, Department of Obstetrics and Gynecology SUNY at Syracuse,Syracuse, New York, 13210; and ¶Gynecologic Oncology Service, Department of Obstetrics and Gynecology Universityof California Los Angeles, Los Angeles, California, 90095

Abstract. Monk BJ, Fowler JM, Burger RA, McGonigle KF, Eddy GL,Montz FJ. Expanded polytetrafluoroethylene is an effective barrier in pre-venting pelvic adhesions after radical surgery for ovarian cancer. Int JGynecol Cancer 1998; 8: 403–408.

Objective: To determine the efficacy of expanded polytetrafluoroethyl-ene(ePTFE) in preventing pelvic adhesions following primary surgicaldebulking of epithelial ovarian cancer.

Methods: Twenty-one patients with advanced ovarian cancer under-going optimal debulking including excision of the pelvic peritoneumwere randomized intraoperatively to either a control group or to a subsetundergoing coverage of the pelvic peritoneal defect with ePTFE. Follow-ing chemotherapy, a second look procedure was performed and adhe-sions scored. The pelvis was divided into quadrants, and each quadrantwas assessed for the extent and type of adhesion involvement (avascular,vascular, thick) and given a composite score (range 0–20). In addition,any visceral structures involved with adhesions were noted. The numberof quadrants involved with adhesions and the mean adhesion scoresbetween the control and experimental group were compared using atwo-tailed Fisher’s exact and t-test, respectively.

Results: Thirteen patients (six ePTFE recipients and seven-controls)were evaluable and underwent surgical reassessment while six eitherrefused second look (N = 2) and/or chemotherapy (N = 2) or progressed(N = 2). One patient in both the ePTFE and control groups died of diseaseprior to reassessment. Forty-two percent (10 of 24) of the pelvic quad-rants covered with ePTFE contained adhesions compared to 86% (24 of28) in the control group (P = 0.001). The mean total quadrant adhesionscore was also lower when ePTFE was used, 1.6 ± 3.2 (range 0–8) vs 8.7 ±5.7 (range 2–17) (P = 0.01). The incidence of bowel loop adhesions, organ/structure involvement and postoperative complications was similar inboth groups.

Address for correspondence: Dr. F. J. Montz, Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, 600 N. Wolfe St.,Houck 248, Baltimore, MD 21287-1248, USA.

Int J Gynecol Cancer 1998, 8, 403–408

© 1998 IGCS

Conclusions: An ePTFE membrane is effective in preventing pelvicadhesions after radical debulking for ovarian cancer. The clinical impli-cations associated with its use, however, require further study.

KEYWORDS: adhesion prevention, expanded polytetrafluoroethylene.

Current therapy for advanced epithelial ovarian can-cer includes cytoreductive surgery followed by mul-tiagent cytotoxic chemotherapy(1). Even after aggres-sive combination therapy, approximately 14,800American females will die from this disease in 1996,making ovarian carcinoma the most deadly gyneco-logic malignancy in the United States(2). Among themany clinical and pathologic factors prognostic of sur-vival, the amount of residual disease remaining afterdebulking surgery seems to be most predictive of out-come(3). For this reason, radical surgical procedureshave been advocated by many experts as a means toaccomplish maximal cytoreduction and, therefore, im-prove survival(4–6). Unfortunately such proceduresfrequently require extensive pelvic operations whichare not only techniquely difficult, but are also associ-ated with a moderate complication rate(3–7).

Perhaps the most important complication of radicalpelvic surgery and ovarian cancer debulking is theformation of adhesions and their sequelae which ispredominantly intestinal obstruction(8). In one largeseries of patients with intestinal obstructions, 48% hada history of prior pelvic surgery as a contributingcause, with pelvic adhesions being the most commonetiologic factor(9).

Since the extent of a gynecologic operation and acancer diagnosis as the indication for surgery correlatewith the risk of adhesion formation and subsequentpostoperative intestinal obstruction(8), we initiated aseries of studies investigating various adjuvants in theprevention of pelvic adhesions following radical gy-necologic cancer operations in animal models. Ini-tially, medicinals such as intraperitoneal recombinanttissue plasminogen activator and the systemic admin-istration of a non-steroidal anti-inflammatory drugwere used with moderate success(10,11). These agentsare thought to prevent adhesion formation throughretardation of fibrin deposition, fibroblast prolifera-tion, capillary ingrowth, and ultimately collagen de-position, which are believed to be central to adhesionformation. Since similar mechanisms are also impor-tant in hemostasis, the risk of bleeding, as well asother systemic toxicities, have unfortunately limitedthe clinical usefulness of these agents in humans.Therefore, other adjuvants such as inert barriers whichcould be directly applied to the surgical site have been

proposed as agents meritorious of further clinicalstudy.

In 1992, we reported that ePTFE (The PRECLUDEt

Peritoneal Membrane, W. L. Gore and Associates,Flagstaff, AZ) decreased postoperative adhesion for-mation by 89% in a porcine model of radical pelvicsurgery. ePTFE was also effective in preventing smallbowel loops from adhering to the pelvic operativesite(12,13). In order to investigate the efficacy of ePTFEas an adjuvant to prevent pelvic adhesions after radi-cal surgery in humans, we undertook a prospectivemulticenter, randomized, controlled trial among pa-tients with epithelial ovarian cancer.

Materials and methods

Patients with histologically confirmed FIGO stage IIIand IV adenocarcinoma of the ovary were prospec-tively entered into a randomized, controlled, multi-center study investigating the efficacy of ePTFE in theprophylaxis of peritoneal adhesions following radicalpelvic surgery. Patients were eligible for study if aradical pelvic resection was required to remove theextraovarian spread of metastatic carcinoma. This in-cluded resection of pelvic structures so that the entirepelvis was denuded of peritoneum. In order to pre-vent bacterial contamination of the membrane, thosesubjects with septicemia or severe infection and/orgros spill of fecal contents were excluded from thestudy. In addition, other confounding factors such asgross residual pelvic disease, a history of pelvic radia-tion, a previous history of an intraperitoneal malig-nancy or another therapy for adhesion prevention,were criteria for exclusion. Postoperatively, studyparticipants were eligible for four to eight cycles ofcisplatin based systemic chemotherapy. Finally, adhe-sions were scored when patients underwent reassess-ment surgery as part of the management for theirovarian cancer. All study sites received certificationthrough their Internal Review Board (Human SubjectProtection Committee) and all patients signed an in-formed consent.

The study consisted of two groups of patients: anexperimental group which received an ePTFE mem-brane to cover the pelvic peritoneal defect and a con-trol group which had the peritoneal defect left uncov-

404 B. J. Monk et al.

© 1998 IGCS, International Journal of Gynecological Cancer 8, 403–408

ered. Randomization was accomplished through asealed envelope which was appended to the patient’sfile and consent form. The contents of the envelopewere opened if all inclusion criteria were met and afterabdominal ceiliotomy and surgical debulking. Thecontents of the envelope randomly assigned a patientto receive the ePTFE (experimental group) or to havethe defect left uncovered (control group).

After resection of the pelvic tumor as well as extir-pation of reproductive organs (including hysterec-tomy and bilateral salpingo-oophorectomy) the ePTFEmembrane was implanted in the study group patients.This was accomplished by tailoring the surgical mem-brane to cover completely the peritoneal defect and atleast 1 cm of bordering normal peritoneum. Greateramounts of overlap were encouraged to minimize thepossibility of adhesion formation around the mem-brane. Thus, the membrane and normal peritoneumoverlapped by at least 1 cm. The membrane was im-planted in as flat a manner as possible with a runningsuture technique employing a nonabsorbable mono-filament suture (eg 3-0 nylon/prolene or Gore-Tex su-ture) on a taper, piercing point or a reverse cuttingneedle. A 2–3 mm bite into the surgical membrane wastaken to avoid suture pull out. In order to avoid isch-emia, suture was tied securely but not tightly.

Patients randomly selected for the control group didnot undergo coverage of the peritoneal defect. Thepatients received the customary standard/best careprocedure in accordance with radical pelvic surgery atthe discretion of the surgeon. Photo or video docu-mentation of the pelvis was performed at the comple-tion of surgery and following membrane implantationwhen applicable for quality control.

Following debulking surgery with or without mem-brane implantation in the experimental and controlgroup, respectively, the patients underwent systemiccytotoxic chemotherapy consisting of four or eightcourses of cisplatin-based chemotherapy accordingthe investigator’s discretion.

Normal hospital postoperative treatment was ad-ministered. Patients were evaluated by history and

physical examination for incision and wound healing,bowel and bladder function, as well as any unantici-pated event or complication potentially related to ad-hesion formation or membrane implantation (ie pain,infection or seroma formation) at monthly intervals.

After the completion of chemotherapy, a secondlook surgery was performed according to standardsurgical procedures for center/surgeon when indi-cated(1). Adhesion assessment was done for both con-trol and experimental groups. The surgical membranewas partially retrieved or, when necessary to docu-ment response to chemotherapy, completely removedfrom the experimental group providing visualizationof the underlying surfaces. However, the investiga-tor/surgeon was permitted to leave a portion of themembrane in situ if it was thought to be beneficial infuture adhesion prevention or if disease was docu-mented in the upper abdomen making disease assess-ment under the membrane less important. The pelviswas also assessed for abscess formation, lymphade-nopathy, and foreign body reaction at the time of sur-gical exploration. A portion of the removed surgicalmembrane was then fixed in formalin and sent toW. L. Gore and Associates, Inc. for historical evalua-tion. Any remaining ePTFE was submitted by the sur-geon for histopathologic review at the individual in-stitution. Finally, the surfaces and tissue underlyingthe membrane were documented with photography orvideo tape to avoid observer variation and bias.

Adhesion assessment and scoring was performed aspreviously described(12). Briefly, the pelvis was di-vided into quadrants with the vaginal apex dividingthe pelvis into right and left anterior and right and leftposterior. Each quadrant was assessed separately forthe percentage of adhesion involvement in the quad-rant as well as the type of adhesions involved (avas-cular, vascular, or thick) (Table 1). Any surroundingorgans or structures involved with adhesions and thelocation of the attachment were documented. Thenumber of adherent loops of small bowel (if any) andtheir attachment location were noted.

The surgeon/investigator was responsible for all

Table 1. Adhesion scores

Adhesion grade Point score

Grade 0 0 Points No adhesionsGrade 1 1 Point Avascular: easily lysed and failing to bleedGrade 2 3 Points Vascular: easily lysed, but bleeding at time of lysisGrade 3 5 Points Thick: requiring extensive sharp surgical dissection

The adhesion score per quadrant was calculated by estimating the percentage of eachquadrant involved in adhesions and multiplying by the grade (i.e. 20% involved bygrade 1 adhesions equals 0.2 plus 40% involved by grade 3 adhesions for a totaladhesion score of 2.2) Modified from Montz et al.(12)

Expanded polytetrafluoroethylene membrane 405


data collection. This was accomplished on standard-ized forms. Documentation at the time of initialceiliotomy, monthly postoperative follow up, secondlook surgery, and unanticipated events were recorded.Unanticipated events not associated with the knowncomplications of ePTFE were to be reported immedi-ately to the study coordinator.

The number of quadrants involved with adhesionsand the mean adhesion scores among the experimen-tal and control groups were compared using a two-tailed Fisher’s exact test and the student t-test, respec-tively, using computer based software. A P value(alpha) less than 0.05 was considered significant.

Results

Between May 1993 and December 1994, 21 patientswith advanced ovarian cancer undergoing optimal de-bulking including excision of the pelvic peritoneumwere randomized intraoperatively to either a controlgroup or coverage of the pelvic peritoneal defect withePTFE. Six centers participated in the study with eachenrolling at least one patient (1, 2, 3, 4, 4, and 7 pa-tients each). Eleven patients received the ePTFE mem-brane as coverage of their peritoneal defect while 10patients acted as controls. The average patient age was60 years (range 40–75) and did not differ between thecontrol and membrane groups.

After an average of 192 days (range 148–238), sur-gical reassessment was performed in 13 patients (sixePTFE recipients and seven controls) with each centerperforming at least one second look operation. Twopatients refused second look surgery, two refused che-motherapy, and two other patients progressed duringstandard chemotherapeutic regimens. Another patientin both the study and control groups died of diseaseprior to reassessment. Forty-two percent (10 of 24) ofthe pelvic quadrants covered with ePTFE containedadhesions compared to 86% (24 of 28) in the controlgroup (P = 0.001). The total quadrant adhesion scoreper patient was lower when ePTFE was used to coverthe peritoneal defect compared to controls [1.6 ± 3.2(range 0–8) vs 8.7 ± 5.7 (range 2–17) (P = 0.01)]. Sincethe implanted membrane was obviously visible, it wasnot possible to blind adhesion assessment.

No statistical difference was detected betweenbowel loop adherence, organ structure adhesion in-volvement or postoperative complications when thestudy and control groups were compared (Table 2).Similarly, no difference in persistent disease present atsecond look was detected. Histopathologic review ofthe retrieved membranes did not show any tissue in-

growth or foreign body reaction. In addition, inflam-matory response was absent.

The most frequent sites of adhesion formation inpatients who had the membranes sutured in situ oc-curred at the periphery of the membranes where thesutures were placed. Four of the six ePTFE membranerecipients who underwent surgical reassessment dem-onstrated some adhesion formation in these areas. An-other individual demonstrated adhesion formation atthe periphery of the membrane which did not appearto be related to suturing. In the final membrane recipi-ent, the membrane was noted to be partially detachedat the time of surgical reassessment. No abnormalitiesdirectly related to the implantation of the surgicalmembrane were detected in any patients except forone individual in whom a fibrous capsule beneath themembrane made pelvic lymphadenectomy difficult.No patient experienced abscess formation or signifi-cant bowel or bladder compromise.

Discussion

Ovarian carcinoma and other gynecologic malignan-cies as well as their surgical management are majorcauses of intestinal obstruction. For example, among368 gynecologic patients treated at the Medical Col-lege of Virginia by Krebs and Goplerud for mechani-cal small bowel obstruction, 305 (83%) were due to aprimary or recurrent gynecologic malignancy, almostexclusively arising from the ovary. The second mostcommon cause of obstruction, however, was postop-erative adhesions (41 patients, 14.5%) most of whichfollowed an operation performed for a gynecologiccancer(14).

Although the most common cause of intestinal ob-

Table 2. A comparison of clinical characteristics among pa-tients undergoing optimal debulking of epithelial ovarian can-cer randomized to coverage of the pelvic peritoneal defect withePTFE or nothing (control)

ePTFE Control

Patient quadrant adhesion scores* 1.6 8.7Bowel loop adherence

Yes 3 5No 3 2

Organ/structure adhesion involvementYes 4 6No 2 1

Postoperative complicationsYes 1 1No 5 6

Persistent disease present at second lookYes 3 4No 3 3

*P = 0.01



struction among patients with ovarian cancer is tumorcompression, select patients treated with cytoreduc-tive surgery will experience intestinal obstruction sec-ondary to adhesions(15). In a report of 37 ovarian can-cer patients who required an operation for intestinalobstruction at some point during their disease, eight(22%) were secondary to adhesions and not recurrenttumor(16). The stage of disease and temporal relation-ship between previous surgery and intestinal obstruc-tion are useful in distinguishing patients whose ob-struction is caused by recurrent tumor from those withintraperitoneal adhesions. Intestinal obstructions oc-curring in the immediate postoperative period andthose following treatment for early stage ovarian can-cer usually are related to adhesions whereas delayedobstruction, especially those which occur in the pres-ence of advanced disease, are usually tumor re-lated(8,17).

At the present time, there is no known surgical ad-juvant proven to prevent adhesions or their sequelaefollowing radical pelvic surgery for ovarian carcinomaor any other gynecologic malignancy. The mainstay toadhesion prevention remains gentle tissue handling,meticulous hemostasis, copious irrigation, prophy-laxis against infection, limiting foreign body reactionand preventing thermal injury. Although these surgi-cal principles apply to all types of operations sincethey can influence the risk of most complications as-sociated with surgical procedures, extensive pelvic pa-thology associated with pelvic cancers and the fre-quent need for radical resections often limit the degreeto which tissue damage and ischemia can be mini-mized. In order to overcome these inherent obstaclesin adhesion prevention after radical gynecologic op-erations, we report the results of the first prospectiveclinical study of adhesion prevention in the pelvic sur-gery literature. When used to cover the pelvis afteroptimal debulking of advanced ovarian cancer withextensive excision and destruction of the pelvic peri-toneum, ePTFE is effective in limiting adhesion for-mation.

The PRECLUDEt Peritoneal Membrane (PPM) is a0.1 mm thin sheet of ePTFE. Initially used in pericar-dial reconstruction, this inert, biocompatible polymerhas been in clinical use for over 15 years(18). No provencase of rejection of this premanently implanted mate-rial has been reported. The PPM differs from otherePTFE products in its thickness and its small pore size(<1 mm). The very small poor size ensures no cellularingrowth or tissue attachment when the membrane isinterposed between injured peritoneal or pelvic struc-tures. In addition, its inert nature incites little or noinflammatory response(21,22). Together, these proper-

ties of the PPM make it an ideal candidate as an ad-hesion preventive barrier to be used following radicalpelvic surgery.

Initial investigations into the efficacy of the PPM asan effective agent in peritoneal adhesion preventionfocused on infertility surgery. In 1988, Boyers and col-leagues reported that the PPM was effective in de-creasing adhesion formation in a rabbit pelvic side-wall/uterine horn injury model(19). Further study inhumans by the Surgical Membrane Study Group, amulticenter infertility group similar to the oncologygroup in the current study, reported a significant de-crease in pelvic sidewall adhesions when the opera-tive site was covered by the PPM(20). Procedures suchas lysis of adhesions and myomectomy were includedin this study and efficacy was documented at secondlook surgery when the membrane was removed. Simi-lar to the present report, morbidity such as infectionfrom the PPM was absent and histologic analysis ofthe retrieved membranes did not show tissue adher-ence or foreign body reaction.

In order to expand upon these findings in the re-productive surgery literature, we initially began to in-vestigate the efficacy of the PPM in reducing adhesionformation in animals after radical pelvic surgery. Ourearliest experimentation with the PPM in a radical pel-vic surgery canine model failed to demonstrate a sig-nificant anti-adhesion formation effect(21). However,this study did identify the importance of meticuloussuturing of the membrane in place with permanentsuture. This prevents membrane collapse and wrin-kling of the PPM. Even with this technique, the cur-rent study showed that some adhesions still occur atthe periphery of the ePTFE membrane. Nevertheless,further studies using a similar radical pelvic surgeryanimal model to cover large peritoneal defects withthe PPM properly sutured into place identified a con-sistent effectiveness in adhesion prevention(12,13). Thislaboratory experience led to the current prospective,randomized, multicenter study among patients under-going surgical debulking for epithelial ovarian cancer.This clinical setting provided the unique opportunityto study adhesion prevention after a common radicalgynecologic operation while allowing determinationof efficacy of the PPM at the time of a planned surgicalreassessment. Unfortunately, it was not possible toblind adhesion assessment since the ePTFE membranewas clearly visible among study participants after im-plantation. However, there appeared to be a clear de-crease in postoperative adhesion formation when themembrane was used to cover the denuded pelvis.Since bulky residual pelvic tumor would probably in-terfere with membrane application, the effectiveness

Expanded polytetrafluoroethylene membrane 407


of the PPM is most likely limited to those who un-dergo complete or optimal debulking of their pelvicdisease.

Although the current study showed neither a sig-nificant decrease in clinical bowel obstruction nor adecrease in adherent loops of small bowel to the pelvicoperative site, animal studies showing a decrease inadherent small bowel loops suggest that a clinical ben-efit may be present(12,13). Because the anti-adhesioneffect of the PPM was so dramatic, it was deemedunethical to continue to accrue patients on the currentstudy, thus preventing some patients the opportunityto receive the PPM through randomization to the con-trol group. Stopping the study early limited our abilityto show a significant reduction in adhesion relatedcomplications such as bowel obstruction. Therefore,until more data are available demonstrating a clini-cally significant effect of surgical adjuvants such as thePPM on preventing adhesion related sequelae, thefoundation of preventing complications caused by ad-hesions after extensive pelvic surgery will remain thelimitation of tissue ischemia and injury through alter-ations in surgical technique. Unfortunately, such at-tempts are freuqently not possible during extirpativecancer operations or when extensive pelvic pathologyis present.

Acknowledgments

Financial support was provided by W. L. Gore andAssociates, Inc., in Flagstaff, Arizona.

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Accepted for publication August 25, 1998



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