Christian-Albrechts-University Kiel, Kiel, Germany, and Polyclinic of Bordeaux, Bordeaux, France
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1 REPRODUCTIVE SURGERY FERTILITY AND STERILITY VOL. 82, NO. 2, AUGUST 2004 Copyright 2004 American Society for Reproductive Medicine Published by Elsevier Inc. Printed on acid-free paper in U.S.A. A randomized, prospective, controlled, multicenter clinical trial of a sprayable, site-specific adhesion barrier system in patients undergoing myomectomy Liselotte Mettler, M.D., a Alaine Audebert, M.D., b Enrique Lehmann-Willenbrock, M.D., a,c Kourosh Schive-Peterhansl, M.D., a and Volker R. Jacobs, M.D. a,d Christian-Albrechts-University Kiel, Kiel, Germany, and Polyclinic of Bordeaux, Bordeaux, France Received December 18, 2002; revised and accepted December 9, Funded by Confluent Surgical (Waltham, Massachusetts), including direct study, clinical, and product costs. Reprint requests: L. Mettler, M.D., Department of Obstetrics and Gynecology, Universitätsklinikum Schleswig-Holstein, Campus Kiel, Michaelisstrasse 16, Kiel 24105, Germany (FAX: ; endo-office@ .unikiel.de). a Department of Obstetrics and Gynecology, Christian- Albrechts-University Kiel. b Polyclinic of Bordeaux. c Present address: Frauenklinik (OB/GYN), Reinhard-Nieter- Krankenhaus, Wilhelmshaven, Germany. d Present address: Frauenklinik (OB/GYN), Technical University Munich, Munich, Germany /04/$30.00 doi: /j.fertnstert Objective: To assess the safety and effectiveness of a sprayable, site-specific adhesion barrier system (SprayGel; Confluent Surgical, Waltham, MA) for reduction of adhesion formation. Design: Prospective, randomized, controlled phase III trial. Setting: University clinic (Kiel, Germany) and private clinic (Bordeaux, France). Patient(s): Sixty-six women aged 34.9 years (range, years) undergoing laparoscopic or open uterine myomectomy, enrolled over a 15-month period. Intervention(s): Patients were randomized to receive either optimal surgical treatment plus adhesion barrier or optimal surgical treatment alone, followed by second-look laparoscopy. Main Outcome Measure(s): Initial and second-look laparoscopy procedures were assessed for incidence, extent, and severity of adhesions; all patients were followed for safety analysis. Result(s): When compared with initial surgery, the mean adhesion tenacity score of adhesions seen at second-look laparoscopy was significantly reduced in treatment patients compared with control patients (0.6 vs. 1.7, a 64.7% reduction). Mean adhesion extent score at second-look laparoscopy compared with initial surgery was 4.5 cm 2 vs. 7.2 cm 2, mean adhesion incidence score was 0.64 vs Of 64 patients, 40 (62.5%) returned for second-look laparoscopy. Conclusion(s): This adhesion barrier was safe, well tolerated, and demonstrated efficacy in a population of patients known to be at risk for adhesion formation. There were no adverse effects attributable to the product and no patients in whom it could not be applied. (Fertil Steril 2004;82: by American Society for Reproductive Medicine.) Key Words: Adhesion barrier, adhesion prevention, myomectomy, hydrogel, laparoscopy, polyethylene glycol, postsurgical adhesions, infertility, abdominal pain, SprayGel The considerable incidence of postoperative adhesion formation has been well described elsewhere, as have the tremendous clinical and financial costs associated with them (1 6). The risk of serious complications resulting from adhesions, including chronic pelvic pain, infertility, and intestinal obstruction (7 10), is high. In addition, adhesions are associated with an increased risk of complications and prolonged operative times at subsequent surgeries (11 13). Postoperative adhesion formation is particularly common after pelvic surgery, including the very procedures undertaken to treat adhesion formation (3, 14). Despite meticulous microsurgical techniques and the adoption of laparoscopic approaches to minimize insult to sensitive tissues, the problem of adhesions persists (1, 3, 14, 15). Therefore, additional prophylactic measures have been sought. Although a number of products have been evaluated to reduce or prevent adhesions, many are difficult to deliver to the target tissue by laparoscopic approaches, which are so commonly used for gynecologic procedures. In addition, some of these products are either not absorbable or resorb too quickly, resulting in minimal efficacy; or have actually demonstrated increased risks of complications from adverse effects. The SprayGel adhesion barrier (Confluent Surgical, Waltham, MA) is a synthetic hydrogel, which forms when two polyethylene glycol 398
2 (PEG)-based liquids are sprayed onto target tissue, where the precursor liquids cross-link within seconds to form an absorbable, flexible, adherent gel barrier in situ (16, 17). The delivery system is a 5-mm-diameter, air-assisted sprayer that can be used in either laparoscopic or open procedures. The gel barrier remains intact at the site of application for approximately 5 to 7 days, protecting the target tissue during the normal wound-healing period, and then gradually breaks down through hydrolysis into PEG constituent molecules that are resorbed and rapidly cleared by the kidneys (16 19). The material has been shown to be highly biocompatible (16, 17). This new adhesion prevention system was evaluated in a prospective, randomized, controlled clinical phase III, multicenter trial to evaluate its efficacy to prevent adhesions and patient safety. MATERIALS AND METHODS This clinical study was conducted at two investigational sites, in accordance with the Declaration of Helsinki, the European Directives on Medical Devices 95/46/EEC, EN 540, ISO 14155, and ICH Harmonized Tripartite Guideline for Good Clinical Practice, as well as reviewing ethics committees. Approval of the Christian-Albrechts-University Kiel institutional review board was obtained. This study included patients aged 18 years who were candidates for conservative laparoscopic or laparotomic myomectomy and thought to benefit from second-look laparoscopy within 16 weeks; thus, each enrolled patient underwent two surgeries. Patients scheduled to undergo open or laparoscopic surgery for leiomyoma or leiomyomatous uteri who had given written informed consent to participate in the study before undergoing their scheduled procedure and who met preoperative and intraoperative eligibility criteria were randomly assigned to treatment with the hydrogel barrier and good surgical technique (treatment group) or to good surgical technique alone (control group). The surgeon was blinded to the randomization until the completion of the surgical resection procedure, at which time a preprinted, sealed envelope was opened, revealing to which group the patient would be assigned. All potentially eligible women were examined within 30 days before surgery; examination included medical and surgical history, medication history, physical examination, and standard clinical laboratory tests: hematology (white blood cell count, red blood cell count, hematocrit, platelet count), serum chemistry (liver and renal function), serum electrolytes, urinalysis, and pregnancy tests. All patients were examined at discharge and immediately before the second-look laparoscopy procedure, which was performed 3 16 weeks after myomectomy. Patients were contacted by telephone 1 week after initial surgery to evaluate their general health and occurrence of any adverse events. Laboratory tests performed at baseline were repeated at the discharge visit after laparoscopy, at the second-look laparoscopy preprocedure visit, and at the termination visit (only for patients who withdrew from the study before completing the second-look laparoscopy preprocedure visit). At the time of scheduled myomectomy, the investigator conducted the procedure according to usual practice. The decision of type of access to the pelvis was mainly based on the weight of the patient, anticipated intra-abdominal visibility, myoma size, and operation mode preference of the surgeon. A conversion from laparoscopy to an open procedure was counted as open procedure. At the beginning of any procedure the incidence, severity, area, and location (anterior, posterior, or fundus) of pre-existing uterine adhesions were recorded. Incidence was defined as the mean number of sites adherent to the uterus. For each single adhesion site, the localization (anterior/posterior/fundus) was noted, as well as the organ to which it was attached (e.g., ovary, tubes, bladder, bowel, or other [to be specified]). Severity was defined as the mean adhesion tenacity score, which ranged from 0 to 3: 0 no adhesions, 1 filmy or avascular adhesions, 2 vascular and/or dense adhesions, 3 cohesive adhesions. This score was given for each single adhesion. The third parameter was the extent of adhesions, defined as the mean area of the uterus covered by adhesions, expressed as centimeters squared (length width of each single adhesion). The location, size, and number of myoma removed, and number and length of each uterine incision was also recorded. Uterine incisions were closed with synthetic absorbable suture material, maximum size 3-0, and the suture tails were trimmed. Upon completion of the myomectomy but before final closing, each patient was intraoperatively reassessed to confirm continued eligibility for enrollment into the study (e.g., no other adhesion prevention products used, no use of nonabsorbable sutures, no accidental enterotomy, no exposure to fluids other than Ringer s lactate or saline). Patients who failed the intraoperative enrollment criteria were withdrawn from the study without additional followup. After surgical myomectomy and assessment of eligibility, patients were randomly assigned in a 1:1 ratio to the treatment or control group at each clinical site, according to preprinted slips in sealed envelopes that had been prepared before the start of the study with a computer-generated randomization schema. For patients randomized to the treatment group, the surgeon coated all suture lines and potentially adhesiogenic surfaces on the uterus and adjacent structures with the adhesion barrier (SprayGel), according to instructions provided by the manufacturer, using the 5-mm air-assisted sprayer. A transient, dilute solution of methylene blue dye (final concentration mg/ml) incorporated into one of the two precursor solutions allowed easy visualization of where the hydrogel barrier had been applied. After adhesion barrier FERTILITY & STERILITY 399
3 FIGURE 1 Flow chart. Distribution of patients in the SprayGel trial. application, the applied hydrogel coating was irrigated with lactated Ringer s or saline solution to ensure a moist surface over all the treated tissues. The first eligible patient at each investigational site was not randomized but was treated with the adhesion barrier to familiarize the investigators with its use. These pilot patients were followed for safety analysis but not for efficacy. Patients randomized to the control group at the conclusion of their procedure were irrigated and closed in the usual fashion. Patients who were successfully randomized to either of the two study groups underwent a second-look laparoscopy 3 16 weeks after the initial procedure. The incidence, severity, and total area of uterine adhesions were recorded during the second-look laparoscopy before any adhesiolysis. Adhesiolysis and any other interventional or diagnostic procedures were performed as necessary and completed as per standard practice. The study termination visit was conducted after the second-look laparoscopy. A total of 69 patients were enrolled into the study (Fig. 1). Five patients were not randomized: 2 (1 in each center) served as training (initial) treatment patients and were followed for safety assessment only but not for efficacy, and 3 were excluded before randomization because they changed their minds (withdrawal from the study). Of the remaining 64 patients, 34 were randomized to the treatment group and 30 were randomized to the untreated control group. Twentytwo of 34 treated patients (64.7%) and 18 of 30 control patients (60.0%) returned for second-look laparoscopy. Although the randomization was with a 1:1 ratio, both centers had unequal numbers of treatment and control patients when the study was closed, on the basis of the computer-generated randomization scheme used. It is coincidental that both study centers had more patients in the treatment group when the study was closed (see Table 1, Fig. 1). No patients were lost to follow-up, but the overall return rate for second-look laparoscopy was only 62.5%. In the end, approximately one in three patients refused to return for second-look laparoscopy despite repeated telephone calls. Because the relatively high drop-out rate was similar in both groups (40.0% in the control group vs. 35.3% for the treatment group), one-sided bias seems unlikely. The primary objectives of this clinical evaluation were to estimate the effectiveness and safety of the adhesion barrier. Primary measurements were the incidence of all adhesions to the uterus; the extent of de novo or recurrent adhesions (as area in centimeters squared); and the severity (or tenacity) of adhesions (score 0 3, as defined previously). 400 Mettler et al. Randomized trial of new adhesion barrier Vol. 82, No. 2, August 2004
4 TABLE 1 Patient demographics for treatment and control groups. Treated group SD Control group SD No. randomized Age (y) 34.9 (28 52) (23 45) 5.9 Height (cm) ( ) ( ) 6.8 Weight (kg) 64.8 (49 90) ( ) 11.8 No. prior myomectomy 5 (14.7) 1 (3.3) No. prior adhesiolysis 3 (8.8) 0 (0.0) Primary cause of surgery (no.) Infertility 11 (32.4) 9 (30.0) Pain 16 (47.1) 16 (53.3) Other 7 (20.6) 5 (16.7) Leiomyoma removed No. 2.6 (0 18) (0 14) 3.2 Weight (g) (0 452) (0 520) 104 Uterine incisions No. 1.9 (1 8) (1 6) 1.2 Length (cm) 7.4 (3 28) (3 26) 4.6 No. completed second-look laparoscopy 22 (64.7) 18 (60.0) Note: Data are expressed as mean (range) or number (percent). A Wilcoxon signed rank test was used to assess statistically significant differences for continuous variables, whereas the Mantel-Haenszel test was used for categoric variables. Statistical significance was defined as P.05, a trend was defined as P 0.1 and.05. A P value of.01 was defined as not significant (NS). Laboratory findings and adverse and intercurrent events were monitored regularly and tabulated for all patients throughout the study period. RESULTS Patient demographics for the treatment and control groups were similar (Table 1). Most patients in this study had their procedure performed laparoscopically (n 28, 82.4% of treated patients and n 23, 76.7% of control patients). Of 64 patients, 13 had an open or converted to open procedure with similar distribution in both groups (6 treated vs. 7 control patients). The type of myoma removed was mainly intramural (n 29, 84.4% of treated patients vs. n 27, 89.7% of control patients). No statistically significant differences were observed between the two groups with regard to leiomyoma removed or uterine incisions. At the time of the initial procedure, patients randomized to the treatment group had similar pre-existing adhesion incidence, with a mean of 0.4 for the treatment group vs. 0.2 for the control group (P NS), a mean severity score of 0.3 for both groups on a scale of 0 3 (P NS), and a mean area of 1.9 cm 2 for both groups (P NS). Spray application of the adhesion barrier was easy in both open and laparoscopic procedures. The product adhered well to target tissue, thus allowing immediate aggressive irrigation without dislodging the barrier. Mean time to apply the sprayable barrier was 3.7 minutes, and an average of 1.9 kits was applied per treatment patient. Drains were used in a majority of patients at one center (Kiel), which would have precluded the use of regional instillates. For most of the patients in this trial, a straight sprayer was used for adhesion barrier application. It was discovered that the straight sprayer was unable to obtain adequate posterior uterine coverage in laparoscopic cases. Therefore, near the end of the study a sprayer with a fixed bend was introduced into the study, allowing for improved posterior coverage. Although not all randomized patients returned for secondlook laparoscopy, no statistically significant differences were found between the patients who did return and those who did not with respect to surgery type, primary reason for surgery, length of surgery, discharge examination, or 1-week clinic visit. Primary efficacy outcomes were incidence (total adhesions), severity (mean tenacity scores), and extent (total area in centimeters squared) of uterine adhesions seen during the second-look laparoscopy. Despite the fact that both groups had similar pre-existing adhesion incidence, severity, and area, treatment patients were more often adhesion-free at second-look laparoscopy: 7 of 22 treatment patients were adhesion-free (31.8%) vs. 2 of 18 (11.1%) in the control group. Unfortunately, the number of patients was too small to prove statistical significance (P NS). The mean adhesion tenacity scores were significantly lower for the treatment group (1.0 vs. 1.9 for the control group, P.002). Only the median area of the uterus covered with adhesions was similar (7.4 cm 2 for the treatment group vs. 7.8 cm 2 for the control group, P NS). FERTILITY & STERILITY 401
5 FIGURE 2 Change in adhesion incidence from initial procedure to second-look laparoscopy (P.035). When we compared second-look laparoscopy values with those of initial myomectomy surgery, control patients were more apt to form adhesions, as shown by the increased incidence of adhesions in the control group compared with the treatment group (0.64 for treatment vs for control, P.035, Fig. 2), along with a greater increase in severity (0.6 for treatment vs. 1.7 for control, P.001, Fig. 3). Although adhesion area increased less in the treatment group than in the control group from initial to second-look laparoscopy, the difference was statistically not significant (4.5 cm 2 for treatment vs. 7.2 cm 2 for control, P NS). No adverse events were related to the use of the adhesion barrier. DISCUSSION Despite adoption of microsurgical and laparoscopic techniques to minimize the trauma of surgery, the surgical technique alone has not effectively eliminated postsurgical adhesion formation or the consequences of its associated complications (3, 14, 15). A significant percentage of infertility, chronic pelvic pain, and intestinal obstruction are the result of postoperative adhesion formation (3, 14, 15, 17, 20, 21). An ideal adhesion barrier should demonstrate efficacy in the presence of blood, be resorbable, and be easy to use in endoscopic procedures, but must not promote infection or inflammatory reaction or affect the normal wound-healing process (15, 16, 22). Other adhesion-prevention products have required absolute hemostasis to be effective, have been challenging either to handle or apply laparoscopically, or their use has run the risk of potentiating infection. In addition, a site-specific barrier that adheres well to target tissue would have the advantage of protecting the tissue most at risk of adhesion formation. Because the synthetic precursor solutions in the adhesion barrier system studied (SprayGel) consist of PEG molecules with complementary reactive end functional groups, they do not polymerize until they react at the tissue surface, where they form a very flexible and conformal hydrogel barrier. The hydrogel is nontoxic, strongly adherent, and does not migrate the way most other barriers or instillate products can (16, 17). It was very easy and quick to apply in open and laparoscopic cases. Our clinical experience supports the theoretical safety profile of the product, because there is no risk of viral transmission with the synthetic components, and the PEG-based hydrogel does not potentiate infection (16, 17). Methylene blue has been added to one of the solutions to allow visualization of the treated areas. The dye diffuses from the hydrogel and is resorbed within hours of application. The hydrogel is strongly adherent, which allowed us to irrigate liberally immediately after deposition, to leave fluid when desired, and to place drains when necessary. 402 Mettler et al. Randomized trial of new adhesion barrier Vol. 82, No. 2, August 2004
6 FIGURE 3 Change in adhesion severity from initial procedure to second-look laparoscopy (P.001). Limitations of this study are mainly due to the nature of adhesions, which makes them difficult to measure and quantify. Although definitions for adhesion incidence, severity, and extent in area were made and used in this study, they imply a subjective factor that cannot be eliminated. Another limitation of this study is that at second-look laparoscopy the physician was most of the time but not always unaware of the group (treatment or control) the patient was randomized to at initial myomectomy. This aspect cannot eliminate potentially unintended bias, although obvious bias was not possible. Even though, when compared with the initial surgery, there was a statistically significant decrease in incidence and severity scores, a larger study would be required to assess the efficacy of this adhesion barrier in different surgical procedures and populations. These results demonstrate the ability of the SprayGel hydrogel barrier to possibly reduce postoperative adhesion formation after laparoscopic or open myomectomy. Certainly, a slight change in tenacity of adhesions appeared. This unique material circumvented many of the problems associated with earlier attempts to prevent adhesions (23, 24) and in our experience did not otherwise adversely affect patient health or outcomes (1 7, 20 22). We believe the product is particularly well-suited to use in gynecologic surgery, where site-specific treatment might be a significant advantage. Although adhesion barrier-treated patients had fewer adhesions at second-look laparoscopy, the number of patients assessed here was limited, and larger, more definitive studies are underway. This product might be well suited for infertility surgery, endometriosis, pelvic floor repair, and any surgeries carried out for adhesiolysis. It might well have practical application in cancer surgery, given the need for repeat procedures, but this needs to be further investigated. References 1. Ray NF, Denton WG, Thamer M, Henderson SC, Perry S. Abdominal adhesiolysis: inpatient care and expenditures in the United States in J Am Coll Surg 1998;186: Ellis H, Moran BJ, Thompson JN, Parker MC, Wilson MS, Menzies D, et al. Adhesion-related hospital readmissions after abdominal and pelvic surgery: a retrospective cohort study. Lancet 1999;353: Lower AM, Hawthorn RJ, Ellis H, O Brien F, Buchan S, Crowe AM. The impact of adhesions on hospital readmissions over ten years after 8849 open gynaecological operations: an assessment from the Surgical and Clinical Adhesions Research Study. Br J Obstet Gynaecol 2000; 107: Monk BJ, Berman ML, Montz FJ. Adhesions after extensive gynecologic surgery: clinical significance, etiology, and prevention. Am J Obstet Gynecol 1994;170: Menzies D, Ellis H. Intestinal obstruction from adhesions how big is the problem? Ann R Coll Surg Engl 1990;72: DiZerega GS, DeCherney AH, Diamond MP, Ellis H, Gomel V, Haney AF, et al. Peritoneal surgery. New York: Springer, Steege JF, Stout AL. Resolution of chronic pelvic pain after laparoscopic lysis of adhesions. Am J Obstet Gynecol 1991;165: Oelsner G, Sivan E, Goldenberg M, Carp H, Admon D, Mashiach S. Should lysis of adhesions be performed when in-vitro fertilization and embryo transfer are available? Hum Reprod 1994;9: Stout AL, Steege JF, Dodson WC, Hughes CL. Relationship of laparoscopic findings to self-report of pelvic pain. Am J Obstet Gynecol 1991;164:73 9. FERTILITY & STERILITY 403
7 10. Ellis H. The magnitude of adhesion related problems. Ann Chir Gynaecol 1998;87: Szigetvari I, Feinman M, Barad D, Bartfai G, Kaali SG. Association of previous abdominal surgery and significant adhesions in laparoscopic sterilization patients. J Reprod Med 1989;34: Van Der Krabben AA, Dijkstra FR, Nieuwenhuijzen M, Reijnen MM, Schaapveld M, Van Goor H. Morbidity and mortality of inadvertent enterotomy during adhesiotomy. Br J Surg 2000;87: Coleman MG, McLain AD, Moran BJ. Impact of previous surgery on time taken for incision and division of adhesions during laparotomy. Dis Colon Rectum 2000;43: Diamond MP, DeCherney AH. Pathogenesis of adhesion formation/ reformation: application to reproductive pelvic surgery. Microsurgery 1987;8: Gomel V, Urman B, Gurgan T. Pathophysiology of adhesion formation and strategies for prevention. J Reprod Med 1996;41: Dunn R, Lyman MD, Edelman PG, Campbell PK. Evaluation of the SprayGel adhesion barrier in the rat cecum abrasion and rabbit uterine horn adhesion models. Fertil Steril 2001;75: Ferland R, Mulani D, Campbell PK. Evaluation of a sprayable polyethylene glycol adhesion barrier in a porcine efficacy model. Hum Reprod 2001;16: Yamaoka T, Tabata Y, Ikada Y. Distribution and tissue uptake of poly(ethylene glycol) with different molecular weights after intravenous administration to mice. J Pharm Sci 1994;83: Johns DA, Ferland R. Initial feasibility study of a sprayable hydrogel adhesion barrier system in patients undergoing laparoscopic ovarian surgery. Fertil Steril 2002;77(Suppl 1):S Porpora MG, Koninckx PR, Piazze J, Natili M, Colagrande S, Cosmi EV. Correlation between endometriosis and pelvic pain. J Am Assoc Gynecol Laparosc 1999;6: Caspi E, Halperin Y, Bukovsky I. The importance of periadnexal adhesions in tubal reconstructive surgery for infertility. Fertil Steril 1979;31: Wiseman DM, Gottlick-Iarkowski L, Kamp L. Effect of different barriers of oxidized regenerated cellulose (ORC) on cecal and sidewall adhesions in the presence and absence of bleeding. J Invest Surg 1999;12: Farquhar C, Vandekerckhove P, Watson A, Vail A, Wiseman D. Barrier agents for preventing adhesions after surgery for subfertility. Cochrane Database Syst Rev 2000;(2):CD Watson A, Vandekerckhove P, Lilford R. Liquid and fluid agents for preventing adhesions after surgery for subfertility. Cochrane Database Syst Rev 2000;(3):CD Mettler et al. Randomized trial of new adhesion barrier Vol. 82, No. 2, August 2004
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