Early laparoscopy after pelvic operations to prevent adhesions: safety and efficacy*

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1 FERTILITY AND STERILITY Copyright The American Fertility Society Printed in U.S.A. Early laparoscopy after pelvic operations to prevent adhesions: safety and efficacy* Robert P. S. Jansen, F.R.A.C.O.G.t Department of Obstetrics and Gynaecology, Royal Prince Alfred Hospital, Camperdown, Sydney, Australia Laparoscopy 12 days after 256 consecutive operations for infertility allowed early diagnosis and treatment of postoperative adhesions that might otherwise have jeopardized the result. Despite scrupulous microsurgical techniques, complete absence of adnexal adherences was present in only 31 of 73 (42.5%) patients without initial adhesions and in 15 of 183 (8.2%) patients who had adhesions lysed. New or reformed adhesions usually were easily separable, often without bleeding, and often with much apparent improvement in fimbrio-ovarian anatomy. There were no significant complications and the safety of early postoperative (second-look) laparoscopy seems established. A modification of the 1979 American Fertility Society endometriosis scoring system was used to quantitate adhesions in 38 patients who subsequently underwent an additional (third-look) pelvic procedure. Adhesions were worse as a result of the laparoscopy in no patients, unchanged in 5 patients, and improved in 33 patients; overall, there was a significant reduction in median adhesion scores from 8 at laparoscopy (95% confidence limits of median, 6 to 10) to 2 at final observation (95% limits, 0 to 4; P < 0.001, rank sum test). Laparoscopy between the time of serosal healing (8 days) and established adhesion fibrosis (21 days) is a safe and effective way of reducing peritoneal adhesions after pelvic operations in young women. Fertil Steril 49:26, 1988 In 1975, Swolin 1 reported unprecedentedly good results after salpingostomy operations for chronic salpingitis. Swolin advocated and carried out a postoperative laparoscopy 6 weeks after such infertility operations to allow diagnosis and treatment of adhesions that were forming. In part, he attributed his relatively good results to the efficacy of the laparoscopy in optimizing tubo-ovarian anatomy. Several reports have since indicated that early postoperative laparoscopy is safe when carried out at intervals from 8 days2,3 to 8 weeks or longer 4-8 after pelvic operations in young women. Received March 23, 1986; revised and accepted August 19, * Presented in part at the forty-first annual meeting of The American Fertility Society, September 28 to October 2, 1985, Chicago, Illinois. t Reprint requests: Dr. Robert P. S. Jansen, The Fertility Laboratory, Royal Prince Alfred Hospital, Camperdown, Sydney 2050, Australia. Only one report has specially addressed the efficacy of early laparoscopy in preventing pelvic adhesions.3 I have previously reported experience with 256 consecutive infertility operations 9,1o in which postoperative laparoscopy was carried out 12 days after laparotomy for infertility. Thirty-eight patients have since had a third procedure, either laparoscopy or laparotomy, at which the outcome in relation to adhesion formation was evaluated. MATERIALS AND METHODS Patients and Operations Two hundred fifty-six young women (median age, 29 years; range, 21 to 42 years) had pelvic operations for infertility between February 1982 and October The operations comprised salpingolyses and salpingostomies for chronic salpingitis and peritubal adhesions (n = 99), excision of endometriosis (n = 60), and midtubal resections and anastomoses for sterilization reversal or isth- 26 Jansen Early postoperative laparoscopy Fertility and Sterility

2 mic salpingitis (n = 97). All operations were for infertility and were carried out using microsurgical principles described elsewhere.9.lo Peritoneal tissues were irrigated during operation with warm, isotonic Ringer lactate solution applied to exposed tissues. Some patients received intraperitoneal 32% dextran and/or 5% hydrocortisone sodium succinate,9 and some patients received intraperitoneal sodium heparin 5000 U/1lO (the subsequent laparoscopy allowed the efficacy of these substances in preventing adhesions to be evaluated9.lo). Prospective patients were told of the possible benefit of early postoperative laparoscopy when their infertility operation was first discussed; 14 patients of a total 270 operated on during the time of the study did not proceed with early postoperative laparoscopy and the laparoscopy rarely was carried out as early as 8 days or as late as 21 days. Care was taken in closing the anterior parietal peritoneum at the end of each operation in anticipation of the postoperative laparoscopy and the hazard of bowel injury that anterior adhesions might cause. Laparoscopic Methods Laparoscopies were carried out under general anesthesia and a set procedure was followed. After peritoneal insufflation and insertion of an 8-mm laparoscope just below the umbilicus, a second puncture was made in the right iliac fossa under direct intraperitoneal vision for insertion of a blunt probe. Omental adhesions to the anterior parietal peritoneum (uncommon) or bowel adhesions to pelvic structures (rare) were detached with the probe. The uterus was raised out of the pelvis by an assistant manipulating an intrauterine elevator fastened to the cervix. With careful identification of serosal cleavage planes, adnexal adherences to the uterus were separated, the tube was detached from the ovary with laterally-directed sweeping movements, and the ovary then was detached from underlying peritoneum of the ovarian fossa or uterosacral ligament. Free peritoneal fluid usually was left in place and used to moisten the detached peritoneal tissues. Adhesion Scores Adhesions were scored using a modification of the 1979 American Fertility Society classification of endometriosis/ 1 without the points which that scheme confers upon endometriomas. Each ovary and tube were scored individually from 0, for no adhesions, through 6, for complete encapsulation. For each ovary, mild adhesions earned 2 points, partial encapsulation earned 4 points; for each tube, adhesions that did not distort the tube earned 2 points, those that did, but did not enclose the tube, earned 4 points; general peritoneal adhesions remote from the tubes' fimbrial ends and from the ovaries (i.e., adhesions that can be expected to have little impact on fertility) received a maximum of 3 points. No points were conferred upon adnexa either not operated on or removed through salpingoovariectomy. Scores were calculated retrospectively by examination of the diagrams and notes made (1) at the pelvic operation; (2) at postoperative laparoscopy; and (3) at any further procedure, such as laparoscopy for diagnosis, laparoscopy for oocyte collection, operation for ectopic pregnancy, or cesarean section. Statistical Methods Confidence limits (95%) of median scores were calculated according to the formula (n + 1)/2 ± n, where n is the number of values in each array. Arrays of adhesion scores at the first, second, and third procedures were compared for statistically significant differences using the nonparametric Mann-Whitney rank sum test. RESULTS Adhesion Occurrence at 12 Days Despite scrupulous microsurgical techniques, there was complete absence of adnexal serosal adherences in only 31 of 73 (42.5%) patients who had not had adhesions at initial operation. Adherences that occurred were almost always between tube and ovary, or between ovary and underlying peritoneal serosa of the ovarian fossa or uterosacral ligament. Adherences often were broad, with much reduction in fimbrial mobility, yet separation was generally achieved easily, often with minimal or no bleeding, and resulted in an immediate and major improvement in adnexal mobility (Fig. 1). Adnexal adherences were absent in only 15 of 183 (8.2%) patients who had had adhesions lysed at initial operation. Separating reformed adherences was often as readily achieved as separating new adherences, but occasionally quite dense and difficult dissections were needed, particularly if sigmoid epiploic tags were involved. Pregnancies occurred in all diagnostic categories, despite the treatment Jansen Early postoperative laparoscopy 27

3 Figure 1 (A) Left ampulla (a) broadly but lightly adherent to left ovary 12 days after tubal anastomosis, with the fimbriae (f ) diverted laterally, away from the underlying ovary. (B) Blunt dissection between ampulla and ovary with the probe; the site of attachment is unrelated to the anastomosis site (arrow). (C) The fimbriae (f) have been mobilized from the ovarian surface without causing bleeding at the site of previous adherence of the ampulla to the ovary (0). of substantial adhesions at postoperative laparoscopy (Table 1). Ultimate Adhesion Occurrence Thirty-eight patients subsequently came to laparoscopy, laparotomy, or cesarean section (Table 1), allowing objective assessment of the practice of dividing adhesions at 12 days. Although the selection of these 38 patients from among 256 subjected to early laparoscopy is not random, a majority (n = 30) had been unsuccessful in achieving pregnancy by the time of the third procedure, so any A 25 B Figure 2 Effect of postoperative laparoscopy on adhesion scores in patients with no initial adhesions (A), and with initial adhesions (B). Procedures: initial infertility operation (#1), postoperative laparoscopy (#2), and subsequent evaluation (#3). selection bias has probably been in favor of the null hypothesis (i.e., that early laparoscopy is not advantageous to restoration of normal pelvic peritoneal anatomy and hence to fertility). The median adhesion score at the time of third-look laparoscopy was 2 (95% confidence limits of median, 0 to 4), substantially and significantly less than the median adhesion score of 8 (95% limits, 6 to 10) found at the time of postoperative laparoscopy (P < 0.001, rank sum test). Figure 2 shows the progress of adnexal peritoneal adhesion scores through the three procedures in patients without initial adhesions (n = 14; Fig. 2A) and in patients in whom adhesiolysis was part of the operation for infertility (n = 24; Fig. 2B). Similar improvements are seen as a result of the postoperative laparoscopy in the two subgroups. In patients with no initial adhesions (n = 14), the median adhesion score at postoperative laparoscopy was 9 (95% limits, 4 to 10) and, at the third procedure, the median adhesion score was 2 (95% limits, o to 5; P < 0.002, rank sum test). In patients with initial adhesions (n = 24, median initial adhesion score 12,95% limits of median 6 to 15), the median adhesion score at postoperative laparoscopy was 9 (95% limits, 6 to 11) and, at the third procedure, the median adhesion score was 2 (95% limits, 0 to 5; P < 0.001, rank sum test). 28 Jansen Early postoperative laparoscopy Fertility and Sterility

4 Table 1 Adhesion Scores at Initial Operation (1), Postoperative Laparosocopy (2), and Subsequent Procedure (3) Used to Evaluate the Efficacy of Division of Adhesions at Postoperative Laparoscopy Patient Diagnosis l a 1 Endometriosis (ll)b 0 2 Endometriosis (3) 0 3 Endometriosis (3) 0 4 Hydrosalpinges 0 5 Sterilization reversal 0 6 Endometriosis (8) 0 7 Endometriosis (6) 0 8 Endometriosis (3) 0 9 Endometriosis (5) 0 10 Sterilization reversal 0 11 Endometriosis (7) 0 12 Endometriosis (8) 0 13 Endometriosis (9) 0 14 Endometriosis (12) 0 15 Sterilization reversal 2 16 Endometriosis (12) 3 17 PID' 4 18 Previous surgery 4 19 Endometriosis (4) 4 20 Sterilization reversal 6 21 h PID 6 22 PID, TR i for SIN j 6 23 PID 6 24 Endometriosis (12) 8 25 PID PID, TR for SIN PID Previous surgery Previous surgery k PID PID PID PID PID PID PID PID PID 25 a Adhesion scores in this column indicate the extent of sal pingolysis procedures. b Endometriosis point scores" are given in parentheses: scores> 6 generally indicate endometriotic cysts., GIFT, gamete intrafallopian transfer. d Spontaneously pregnant after or before the described third procedure. Self-adherent tube bunched over anatomosis site at second procedure; postanastomosis length restored at third procedure. 2 3 Third procedure 2 0 GIFT'laparoscopy 2 0 Diagnostic laparoscopy 3 0 Diagnostic laparoscopy [P] d 4 4 Diagnostic laparoscopy 4 4 Diagnostic laparoscopy 4 0 Diagnostic laparoscopy [P] 6 4 GIFT laparoscopy 8 2 Diagnostic laparoscopy 8 0 GIFT laparoscopy [P] 8 0 Diagnostic laparoscopy 10 5 GIFT laparoscopy 10 0 GIFT laparoscopy 12 8 GIFT laparoscopy 12 4 Diagnostic laparoscopy 6 0 Diagnostic laparoscopy' 4 2 GIFT laparoscopy [P] 4 0 Diagnostic laparoscopy 6 2 IVFg laparoscopy GIFT laparoscopy 4 2 [P] C-section 8 0 Diagnostic laparoscopy 10 0 Ectopic pregnancy 11 5 Diagnostic laparoscopy 2 0 Diagnostic laparoscopy 8 2 Diagnostic laparoscopyd 8 0 Diagnostic laparoscopy IVF laparoscopy GIFT laparoscopy 12 6 IVF laparoscopyd 13 4 IVF laparoscopy 14 4 Ectopic pregnancy 10 2 Ectopic pregnancy 18 8 Diagnostic laparoscopy 10 4 Ectopic pregnancyd 23 6 Ectopic pregnancy 4 0 [P] C-section 8 8 Diagnostic laparoscopy 4 0 [P] C-section 'PID, pelvic inflammatory disease. D IVF, in vitro fertilization. h Bowel adherent to ovary at postoperative laparoscopy. i TR, tubal resection and anastomosis. j SIN, salpingitis isthmica nodosa. k Ovary completely denuded of capsule at first procedure; light adherences covered it at second procedure; ovary completely free at third procedure. Complications There were no instances of visceral injury at postoperative laparoscopy. One patient developed unusual pelvic pain and tenderness unaccompanied by fever; antibiotics were prescribed and symptoms resolved. DISCUSSION Published reports show that adnexal adhesions are common after pelvic operations in women,2-8 even after meticulous surgery. For example, Pittaway et al.8 found that only 2 of 33 normal ovaries operated on for wedge resection or ovarian cystectomy were free of adhesions at subsequent laparoscopy. Diamond et al.? employing laser adhesiolysis, reduced existing ovarian adhesions only from 72.9% to 61.2% of patients, as determined at subsequent laparoscopy; pelvic sidewall and omental adhesions were slightly worse at postoperative laparoscopy. These observations have been confirmed by the present study. Despite scrupulous Jansen Early postoperative laparoscopy 29

5 microsurgical techniques, adnexal adherences were absent at postoperative laparoscopy in only 31 of 73 (42.5%) patients who had had no adhesions initially and in only 15 of 183 (8.2%) patients who had had adhesions lysed. Fibrosis of unlysed fibrin begins 3 days after serosal trauma and is mostly complete by 21 daysp-14 If postoperative laparoscopy is carried out with the aim of reducing adhesions, timing the laparoscopy 6 weeks after operation may be later than ideal to change the course of peritoneal adhesion formation. Mesothelial repair of defective peritoneum occurs mainly by transformation of attached peritoneal macrophages12,15 or differentiation of underlying mesenchyme,13,16 so the size of a peritoneal defect is irrelevant to the time it takes to reperitonealize deficient serosa13,16; increased mitosis of adjacent undisturbed serosal cells occurs,12,13,15 but this is an important means of peritoneal repair only over short distances. Because peritoneal repair is complete by 8 days after serosal injury,12-16 newly forming serosal adherences should presumably be lysed as soon as practicable after this time, before fibrosis is established. Several European studies have emphasized the ease with which all adhesions can be separated at 8 days,2,3 although the stated purpose of early timing in these series was to carry out the laparoscopy during the same hospital admission as the infertility operation. The only other report of such early timint claimed that pelvic conditions were unfavorable for laparoscopic adhesiolysis in the first 1 to 2 weeks after operation because of bleeding and abdominal wall edema. These disadvantages were not encountered at 12 days in the present series. Reports consistently indicate that, although some adhesions can be lysed after long intervals, many adhesions can be untreatable after 4 weeks.5,8 In my experience, an interval of 2 weeks can be too long for adhesions involving the omentum or sigmoid colon. Patients through the course of the present series occasionally were readmitted as early as 8 days or as late as 21 days because of their individual circumstances; there were advantages apparent in early admission and disadvantages in later admission. My more recent general experience with 10 days has been favorablep Trimbos-Kemper et al.3 repeated laparoscopies on 64 of 188 patients and found that 51.6% of adnexa freed of adhesions at laparoscopy remained free of adhesions subsequently. The present results show that adhesions would often have been little improved without the postoperative laparoscopy: 30 Jansen Early postoperative laparoscopy the laparoscopy was crucially important in reducing the adhesions, regardless of whether initial adhesions were present (Fig. 2). If the results in the 38 patients who had subsequent evaluative procedures can be generalized to all 264 patients who had adhesions treated at postoperative laparoscopy, then the overall incidence of completely adhesion-free outcomes after microsurgery and early postoperative laparoscopy is approximately 70% when there are no initial adhesions, and 40% when adhesions are part ofthe reason for operating. The extent to which early laparoscopy affects pregnancy rates with different kinds of pelvic surgery is still to be determined. There are no randomized studies in which the effectiveness of postoperative laparoscopy has been evaluated in comparison to an adequate control group, nor does the present study address this question in a controlled way. There are indications, however, that pregnancies happen earlier than they otherwise might if laparoscopy is carried out after tubal anastomosis,!8 operation for endometriosis,!7 and operation for pelvic adhesions.3 Among sterilization-reversal patients, analysis of postoperative treatment of new versus reformed adhesions shows that lysis of new adhesions is the more efficacious, with pregnancy rates decreased in this group (compared with patients without adhesions) only among those patients with adhesion scores greater than 10 at postoperative laparoscopy.18 No serious complications have been reported from early postoperative laparoscopy, although precautions should be taken to avoid placing the second puncture site too close to healing skin incisions.3,5 Diamond et al.7 described a patient with a partial large bowel obstruction, presumed to be due to a sigmoid hematoma, which resolved without intervention. The possibility of pelvic abscess formation exists if postoperative bleeding has taken place and a pelvic hematoma is infected during the laparoscopy procedure; aspiration of old blood and possibly replacement with physiologic solutions under systemic antibiotic cover may be advisable in such circumstances. It is reasonable to conclude from this study that early postoperative laparoscopy is safe and effective in reducing the ultimate development of adnexal adhesions after pelvic operations in women. Advantages also accrue in the training of pelvic surgeons when the results of pelvic operations are regularly seen soon afterwards. It remains to be determined which kinds of pelvic operation benefit Fertility and Sterility

6 most from postoperative laparoscopy, but the present study indicates that significant advantage is obtained regardless of whether adhesions are initially present. REFERENCES 1. Swolin K: Electromicrosurgery and salpingostomy: long term results. Am J Obstet Gynecol 121:418, Suchet-Henry J, Loffredo V: Traitement chirurgical des sterilites tubaires. Interet de la greffe de peritoine libre et de la coelioscopie precoce dans la prevention des adherences. Nouv Presse Med 9:311, Trimbos-Kemper TCM, Trimbos JB, van Hall EV: Adhesion formation after tubal surgery: results ofthe eighth-day laparoscopy in 188 patients. Fertil Steril 43:395, Surrey MW, Friedman S: Second-look laparoscopy after reconstructive pelvic surgery for infertility. J Reprod Med 27:658, Raj SG, Hulka JF: Second-look laparoscopy in infertility surgery: therapeutic and prognostic value. Fertil Steril 38:325, DeCherney AH, Mezer HC: The nature of posttuboplasty pelvic adhesions as determined by early and late laparoscopy. Fertil Steril 41:643, Diamond MP, Daniell JF, Martin DC, Feste J, Vaughn WK, McLaughlin DS: Tubal patency and pelvic adhesions at early second-look laparoscopy following intraabdominal use of the carbon dioxide laser: initial report ofthe intraabdominallaser study group. Fertil Steril 42:717, Pittaway DE, Daniell JF, Maxson WS: Ovarian surgery in an infertility patient as an indication for a short-interval second-look laparoscopy: a preliminary study. Fertil Steril 44:611, Jansen RPS: Failure of intraperitoneal adjuncts to improve the outcome of pelvic surgery in young women. Am J Obstet Gynecol 153:363, Jansen RPS: Failure of intraperitoneal heparin to influence peritoneal adhesion-formation. Surg Gynecol Obstet. In press 11. The American Fertility Society: Classification of endometriosis. Fertil Steril 32:633, Johnson FR, Whitting HW: Repair of parietal peritoneum. Br J Surg 49:653, Ellis H, Harrison W, Hugh TB: The healing of peritoneum under normal and pathological conditions. Br J Surg 52:471, Milligan DW, Raftery AT: Observations on the pathogenesis of peritoneal adhesions: a light and electron microscopical study. Br J Surg 61:274, Eskeland G: Regeneration of parietal peritoneum in rats. 1., A light microscopical study. Acta Pathol Microbiol Immunol Scand 68:355, Raftery AT: Regeneration of parietal and visceral peritoneum: a light microscopical study. Br J Surg 60:293, Jansen RPS: Unpublished data 18. Jansen RPS: Tubal resection and anastomosis. I. Sterilization-reversal. Aust NZ J Obstet Gynaecol 26:294, 1986 Jansen Early postoperative laparoscopy 31

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