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Predictors of Clinical Outcomes in the Laparoscopic Management of Adnexal Masses

From the Departments of Obstetrics and Gynecology, and Biostatistics and Bioinformatics, Duke University Medical Center, Durham, North Carolina.

Address reprint requests to: Andrew Berchuck, MD, Box 3079 Duke University Medical Center, Durham, NC 27710; E-mail: berch001{at}mc.duke.edu.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
OBJECTIVE: Laparoscopy has become an accepted approach in the management of adnexal masses. We evaluated clinical outcomes of laparoscopic management of adnexal masses thought to be benign preoperatively.

METHODS: We performed a retrospective study of patients undergoing laparoscopic evaluation of adnexal masses over a 7-year period. Regression models evaluated predictors of blood loss, length of stay, complications, mass rupture, conversion to laparotomy, and operating time. Preoperative predictors of malignant and borderline disease were evaluated using a separate model.

RESULTS: Complications occurred in 8% of 396 patients undergoing laparoscopic evaluation of adnexal masses and were associated with concurrent hysterectomy (P = .01) and smaller mass (P = .01). Conversion to laparotomy occurred in 25% and was associated with larger mass (P = .001), prior hysterectomy (P = .002), and younger age (P = .002). Mass rupture occurred in 25% and was associated with prior (P < .001) or concurrent (P = .003) hysterectomy and younger age (P = .001). Blood loss greater than 500 mL was associated with concurrent hysterectomy (P < .001). Length of stay was associated with concurrent (P < .001) and prior (P < .001) hysterectomy, larger mass (P = .01), prior abdominal surgery (P = .009), and medical comorbidities (P = .007). Malignancy occurred in 2%, and laparoscopic management was not associated with adverse outcomes.

CONCLUSION: Adnexal masses thought to be benign preoperatively were successfully managed laparoscopically in three fourths of cases and clinical outcomes were acceptable. To a great extent, adverse events were attributable to concurrent hysterectomy rather than removal of the adnexal mass.

Significant advances in laparoscopic surgical techniques over the past 20 years have been fueled by the development of more sophisticated instruments. The promises of less postoperative pain, faster recovery times, and lower costs have driven patient demand, and more gynecologic procedures are now performed laparoscopically than in the past. However, the introduction of laparoscopic approaches to surgery has not always fulfilled all of its proponents’ expectations. Expensive laparoscopic equipment can detract from or completely negate the cost benefit of shorter hospitalizations.^1–3 Additionally, the skills used in laparoscopic and open procedures differ, and a significant number of laparoscopic cases are required to ascend the associated learning curve. Finally, the pattern of complications associated with laparoscopic procedures often is distinct from that of the corresponding open procedure.

Laparoscopic removal of adnexal masses was pioneered by gynecologists who were among the most experienced laparoscopic surgeons. Their initial reports in the literature documented good clinical outcomes, and these have encouraged widespread use of this technique. Although prospective trials designed to define the value and pitfalls of laparoscopy in the management of adnexal masses have not been performed, this has become an accepted approach for gynecologists regardless of their level of laparoscopic training and skill.

Laparoscopic removal of adnexal masses is most often performed in the United States by obstetrician–gynecologists rather than gynecologic oncologists. Thus, several authors have emphasized preoperative identification of risk factors for malignancy to reserve the laparoscopic approach for masses that are likely benign.^4,5 The rationale for avoidance of laparoscopic removal of ovarian cancers is that inadvertent spillage could worsen the prognosis and/or mandate administration of chemotherapy to patients with stage I disease who would otherwise not receive it.⁶ Conversely, some gynecologic oncologists advocate laparoscopic exploration for adnexal masses regardless of risk factors, with complete staging of all malignancies either through an open approach or laparoscopically.^7–9

Since the introduction of operative laparoscopy in our department, which includes both obstetrican–gynecologists and gynecologic oncologists, the laparoscopic approach has been limited to masses thought to be benign preoperatively. We have reviewed the initial 7 years of experience with laparoscopic management of adnexal masses to determine the frequency of adverse outcomes in a setting in which these procedures are being performed by a diverse group of staff members and trainees. We also have sought to identify the clinical factors predictive of adverse outcomes with laparoscopic removal of adnexal masses.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
We retrospectively reviewed the Duke University Medical Center Operating Room Database to identify all cases in which a gynecologic surgeon undertook a laparoscopic procedure with the intention of removing a pelvic mass from July 1, 1994, to June 30, 2001. Chart reviews were performed of cases meeting the following inclusion criterion: all patients with a preoperative diagnosis of adnexal mass whose surgery was initiated laparoscopically. Exclusion criteria included laparoscopic procedures performed for the following indications: a positive pregnancy test with the suspicion of ectopic pregnancy, pelvic pain, pelvic inflammatory disease, or infertility. Demographic and clinical information was obtained from patient records. All procedures were performed by an attending gynecologic surgeon. Assistants consisted of a first, third, or fourth year resident for general gynecology cases and a second, third, or forth year resident or a fellow for subspecialty (oncology, urogynecology, or reproductive endocrinology) cases.

We examined seven candidate predictor variables for their association with six clinical outcome variables:

1. Estimated blood loss greater than or less than 500 mL.
   
2. Length of hospital stay, a five-level ordinal variable created by collapsing all length of stay values greater than 4 days into a single category.
   
3. Presence or absence of perioperative complications. Both major and minor complications were included, as listed in Table 1; they include intraoperative (urinary tract injury, bowel injury, uterine perforation, vascular injury, nerve injury, subcutaneous emphysema, hemorrhage) and postoperative (incisional disruption, urinary retention, partial small bowel obstruction, postoperative transfusion, any readmission, any reexploration) events.
   
4. Presence or absence of intraoperative mass rupture, defined as any rupture, intentional or unintentional, that resulted in spill of cyst contents into the peritoneal cavity. If a mass was drained intentionally within a collection bag to facilitate removal without a resulting peritoneal spill, the mass was not considered ruptured.
   
5. Presence or absence of conversion to laparotomy.
   
6. Length of time in operating room (minutes). The length of the operative procedure was not available. The log of operating room time was used to create an approximately normally distributed variable.
   

1. Mass size, determined radiographically (centimeters).
   
2. Hysterectomy status, a three-level variable indicating whether the patient underwent hysterectomy with the current surgery, had a prior hysterectomy, or never had a hysterectomy. Concurrent and prior hysterectomy were each compared with no hysterectomy.
   
3. Number of prior abdominal surgeries.
   
4. Presence or absence of any serious medical comorbidity, including hypertension, diabetes mellitus, chronic obstructive pulmonary disease, coronary artery disease, or asthma.
   
5. Age at surgery (years).
   
6. A two-level variable indicating whether the operating surgeon was a gynecologic oncologist or other gynecologist (generalist or other subspecialist).
   
7. Operating room date, recorded as values 1–14 corresponding to the fourteen 6-month periods between 1994 and 2001. This variable was created to detect changes in outcomes over time.
   

Because only 18 patients had estimated blood loss greater than 500 mL, the Fisher exact test and the Wilcoxon test were used to determine the association of estimated blood loss with the predictor variables. The proportional odds logistic regression model was used for modeling length of stay, the general linear model was used for modeling operating room time, and the logistic regression model was used for the remaining three outcome variables.

The seven predictor variables were entered into the regression models in a hierarchical order in keeping with their relative clinical importance.

1. Mass size and hysterectomy status were first entered together into each model and their significance tested, controlling for each other.
   
2. Number of abdominal surgeries and medical comorbidities were tested next, controlling for the first two variables.
   
3. Age was entered next, controlling for the prior four.
   
4. Surgeon and operating room date were tested separately, controlling for all previous variables.
   

The sample size varies across these four models because of the presence of missing values, which is especially large for the two variables entered at step b. A two-sided type I error rate () of .01 was used for all tests.

Results from the logistic regression models are given in terms of odds ratios (ORs) and their 95% confidence intervals (CIs). Results from the general linear model of log of operating room time are given in terms of estimated regression coefficients (ßs) and their CIs. Additionally, unadjusted probabilities and unadjusted means within subgroups are used to describe some effects.

In a separate analysis, we looked for clinical variables that could distinguish patients with and without malignancy. Malignancy was defined in two ways: invasive cancer only and invasive cancer plus borderline tumors. Because very few patients had malignancy, the Fisher exact test was used to compare patients with and without malignancy. The Wilcoxon test was used to compare these patients’ ages.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
We identified 396 patients who underwent laparoscopic surgical evaluation of an adnexal mass by 46 different gynecologic surgeons between June 1994 and June 2001. Patient characteristics are listed in Table 2. Median age was 43; 37% of patients were postmenopausal. The median number of prior abdominal procedures was one, with a range of zero to five. Twenty-two percent of patients had previously undergone hysterectomy, whereas 18% of patients underwent hysterectomy with the current surgery. The median preoperative mass size was 5.2 cm (range 0.5–17). Twenty-six percent of masses were less than 4 cm, 57.4% were between 4 and 8 cm, and 16.6% were greater than 8 cm. Forty-seven percent of patients underwent unilateral or bilateral salpingo-oophorectomy without hysterectomy. Eighteen percent underwent hysterectomy with unilateral or bilateral salpingo-oophorectomy. Other procedures included ovarian cystectomy (18%), cyst drainage (3.5%), salpingectomy (3%), myomectomy (1.5%), appendectomy (0.5%), and lysis of adhesions or no further intervention (8%). Conversion to laparotomy occurred in 25% of cases.

The distribution of outcome variables is listed in Table 4. Associations of outcomes with the candidate predictor variables are given below, ordered by outcome variable.

Mass size (P = .01), concurrent (P < .001) and prior (P < .001) hysterectomy, number of prior abdominal surgeries (P = .009), and medical comorbidities (P = .007) significantly predicted length of stay (Table 5). Seventy-eight percent of patients undergoing hysterectomy had a length of stay of more than 1 day, compared with 45% of patients with prior hysterectomy and 19% of patients with no hysterectomy. Sixty-two percent of patients with at least one major comorbidity had a lenth of stay of more than 1 day, compared with 39% of patients with no major comorbidities. Forty-six percent of patients with masses of at least 8 cm had a length of stay of more than 1 day, compared with 32% of patients with masses smaller than 5 cm.

Intraoperative rupture of cystic masses occurred in 25% of cases and was associated with prior hysterectomy (P < .001), concurrent hysterectomy (P = .003), and younger age (P = .001) (Table 5). Mass rupture occurred in 13% of patients undergoing concurrent hysterectomy, 11% of patients with prior hysterectomy, and 33% of patients without a hysterectomy.

Conversion to laparotomy occurred in 25% of cases. Prior hysterectomy (P = .002), larger mass (P = .001), and younger age (P = .002) were predictive of conversion to laparotomy (Table 5). Thirty-two percent of the 58 masses 8 cm or greater required conversion, compared with 19% of 144 masses less than 5 cm. Eighteen percent, 37%, and 34% of patients with no hysterectomy, prior hysterectomy, and concurrent hysterectomy, respectively, required conversion. There was no difference in the proportion of cases converted to laparotomy between generalists and oncologists.

Hysterectomy status (P < .001), larger mass (P = .006), and surgeon (P < .001) were predictive of longer operating room time. Patients undergoing a hysterectomy during the current surgery had a mean operating room time that was 84 minutes longer than that of patients with no hysterectomy (ß = .48; CI 0.39, 0.58). Patients with a prior hysterectomy required 54 extra minutes (ß = .18; CI 0.10, 0.26). Patients with masses greater than 5 cm had a mean operating room time that was 21 minutes longer than that of patients with smaller masses (ß = .019; CI 0.006, 0.033). Gynecologic oncologists had a significantly shorter mean operating room time than that of other gynecologists, regardless of whether the procedure included a hysterectomy (ß = - .16; CI -.24, -.08).

Invasive cancer was found in eight of 396 patients (2%). Borderline pathology was found in four of 396 patients (1%). The ultrasonographic characterization of the mass was weakly predictive of invasive cancer, but the association was not significant (P = .04). Ten percent of solid masses were malignant, compared with 1.5% of complex and 2.7% of simple cystic masses. Nodularity weakly predicted neoplasms that were either borderline or invasive (P = .03) but did not predict invasive neoplasms alone (P = .46). Neither a family history of ovarian or breast cancer nor CA 125 values were predictive of malignancy. Among five patients with invasive ovarian cancers, two had a preoperative CA 125 value (U/mL) greater than 65, one had a CA 125 value between 35 and 65, and two had a CA 125 value less than 35. The patient with fallopian tube carcinoma had a CA 125 of 90. Both patients with metastatic cancer had normal CA 125 values.

Among the patients with invasive ovarian cancer, two had stage IIIC disease at diagnosis (Table 6). One was lost to follow-up after a negative second-look laparotomy at 6 months. The other died of her disease at 35 months. There were two stage IC ovarian cancers. One was a serous adenocarcinoma that was stage IC on the basis of capsular involvement. This patient received postoperative intraperitoneal ³²P and has been without evidence of recurrence for 88 months. The second patient had a microinvasive (less than 0.5 mm) adenocarcinoma arising in a serous borderline neoplasm that ruptured intra-operatively. No further treatment was recommended, and this patient is without recurrence at 38 months. The final patient had a stage IA adult granulosa cell tumor and is without evidence of recurrence at 29 months. The only fallopian tube carcinoma was stage IC based on positive peritoneal cytology, but an intraperitoneal spill also occurred during removal of the mass. This patient received four postoperative cycles of carboplatin and paclitaxel chemotherapy and remains without recurrence at 16 months. There were no laparoscopic port site or abdominal wall metastases.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

Eltabbakh et al¹⁷ analyzed 204 consecutive operative laparoscopies and found that a history of at least one prior laparotomy predicted major complications at laparoscopy or conversion to laparotomy. Likewise, we found that prior abdominal surgery predicted longer hospital stay. Prior hysterectomy was also predictive of longer hospital stay and mass rupture. Prior hysterectomy was more strongly associated with adverse outcomes than prior abdominal surgery, probably because adhesions affecting subsequent pelvic surgical procedures are more likely to result from hysterectomy than from most other abdominal procedures. Given our low overall complication rate, we do not feel that risk factors such as prior hysterectomy, prior abdominal surgeries, or large mass should be contraindications to the laparoscopic approach. Rather, they should be recognized as factors that may add to the difficulty of the proposed procedure.

The year in which the surgery was performed was not associated with complication rates during the 7-year period evaluated. A decrease in complications over time might be expected for an individual surgeon because of the learning curve. Voitk et al^18,19 reported significant decreases in operating time and in the number of complications for individual surgeons after at least 50 laparoscopic inguinal hernia repairs and after 200 laparoscopic cholecystectomies. Another study²⁰ failed to find a relationship between the experience of the surgeon and the incidence of bile duct injuries during laparoscopic cholecystectomy. In our study only six of the 46 surgeons performed more than 20 laparoscopic evaluations of adnexal masses over the 7-year period, and four of these were gynecologic oncologists. This lack of experience likely reflects the significant flux in the size and composition of the general gynecology faculty at our institution during the period encompassed by our study. The tail of the learning curve, during which complications and operating time are expected to decrease, is likely not evident in our study because of the small number of procedures per individual surgeon.

Our rate of conversion to laparotomy was 25%, which is higher than the 8–12% rate previously reported.^{13,14,17,21,22} Unlike some other published studies, ours is a comprehensive review of operative laparoscopies performed over a 7-year period at our institution and involved 46 different staff surgeons, both general obstetrician–gynecologists and various subspecialists. Our findings therefore may be more representative of general clinical practice than studies involving only two or three highly experienced laparoscopic surgeons.^10,23 We found that conversion to laparotomy was more common in patients with larger masses, younger patients, and in those undergoing concurrent or prior hysterectomy. By comparison, conversion rates for laparoscopic cholecystectomy vary from under 5% for elective procedures to 18% in cases of acute cholecystitis.^24,25 Appropriate decisions to convert to laparotomy in our study may have contributed to the reasonable 8% complication rate observed. Removal of adnexal masses is not the only laparoscopic procedure performed by gynecologists, however, and total laparoscopic experience may be a better gauge of mastery of the learning curve.

Mass rupture occurred in 25% of cases and was associated with concurrent hysterectomy, mass size, and younger age. Although most prior studies do not report the percentage of mass rupture during laparoscopic removal, Sadik et al¹⁶ reported mass rupture in 146 of 220 cases (67%) but removed all of these through an endoscopic bag. There is no standard procedure for removal of adnexal masses among the numerous surgeons involved in this study. The approach on our oncology service is removal of masses inside an endoscopic bag with controlled drainage within the bag through the port site before removal, thus avoiding a peritoneal spill. In retrospectively comparing laparoscopy and laparotomy for adnexal surgery, Gal et al²⁶ found an overall rate of rupture of 25% during laparoscopic management of adnexal masses, compared with 9.4% during laparotomy. The authors found that rupture of cystic ovarian masses is more common during laparoscopy when ovarian cystectomy is attempted but equally likely using either approach if adnexectomy is performed. In the present study, patients undergoing concurrent hysterectomy were less likely to have mass rupture than others; this might be explained by easier removal of the ovaries through the upper vagina as opposed to a small abdominal wall port.

Among five cases of invasive ovarian cancer, one was upstaged to stage IC on the basis of rupture. Whether the benefits of the laparascopic approach outweigh the risk of malignant mass rupture remains to be determined. Some clinicopathologic studies have identified mass rupture as a poor prognostic factor in early-stage ovarian cancer^27,28; other studies have found that although preoperative rupture of a stage I cancer may be a poor prognostic factor, intraoperative rupture is not associated with a worse outcome.^29–31 Whether patients whose malignant masses rupture intraoperatively have higher recurrence rates or not, the standard of care dictates that these patients should receive postoperative chemotherapy, which significantly affects quality of life. In the current study, intraoperative rupture of malignancies did not affect subsequent management because the only patient who was upstaged had a microinvasive adenocarcinoma arising in a borderline neoplasm and was not treated with chemotherapy. Another concern is the potential development of abdominal wall metastases at laparoscopic port sites, which has been reported in as many as 16–25% of patients with ovarian cancer.^32,33 We have not seen any laparoscopic port site metastases among the eight patients with primary or metastatic malignancies. Until further studies prove the safety of laparoscopic management of ovarian malignancy, however, we favor the laparoscopic approach only for masses thought to be benign preoperatively.

Functional cysts, simple cysts, and normal pathology comprised 118 cases (29.8%) in the current study. This percentage of patients without significant pathology is consistent with prior studies of adnexal masses managed laparoscopically, with the rate of functional cysts ranging from 18% to 55%.^15,16,22 Recently, it has been determined that unilocular cystic adnexal masses under 10 cm in postmenopausal women may be followed with minimal risk of ovarian cancer.³⁴ However, the decision to follow a known mass conservatively must be made on an individual basis, taking into account CA 125, family history, and the patient’s level of anxiety. Certainly, younger patients with symptomatic adnexal masses that do not respond to conservative management should be considered surgical candidates, and a certain number of these will ultimately be diagnosed with functional cysts.

Although several of the patients in this study with cancers had elevated serum CA 125 levels, the positive predictive value of CA 125 for malignancy was poor. CA 125 was likely not predictive of malignancy in this series because of the very small numbers of malignancies detected. This was a result of a concerted effort to avoid the laparoscopic approach when there was a suspicion of malignancy. Thus, it is not surprising that most of the few cases of cancer had relatively low CA 125 levels.

In conclusion, adnexal masses thought to be benign preoperatively were managed successfully via the laparoscopic approach in about three fourths of cases, and clinical outcomes were acceptable. Most complications and adverse outcomes such as estimated blood loss greater than 500 mL, prolonged operating time, and increased length of hospital stay were at least partially attributable to hysterectomy rather than removal of the adnexal mass. A majority of these procedures were performed by gynecologists who had treated relatively few such cases. Further studies will clarify whether the use of laparoscopy for routine staging of ovarian malignancies is advisable.

	Footnotes

 
doi:10.1016/S0029-7844(03)00480-0

Received November 5, 2002. Received in revised form February 19, 2003. Accepted March 13, 2003.

	REFERENCES

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2. Sultana CJ, Sogor L. Laparoscopy vs. laparotomy for gynecologic procedures. Impact on resident training. J Reprod Med 1996;41:225–30.[Medline]

3. Dorsey JH, Holtz PM, Griffiths RI, McGrath MM, Steinberg EP. Costs and charges associated with three alternative techniques of hysterectomy. N Engl J Med 1996;335: 476–82.[Abstract/Free Full Text]

4. Drouin PD-LJ, Ehlen T, Ghatage P, Heywood M, Lotocki RJ, Murphy KJ, et al. Guidelines for the laparoscopic management of the adnexal mass. J Soc Obstet Gynaecol Can 1998;20:983–9.

5. Shalev E, Eliyahu S, Peleg D, Tsabari A. Laparoscopic management of adnexal cystic masses in postmenopausal women. Obstet Gynecol 1994;83:594–6.[Medline]

6. Rubin SC, Wong GY, Curtin JP, Barakat RR, Hakes TB, Hoskins WJ. Platinum-based chemotherapy of high-risk stage I epithelial ovarian cancer following comprehensive surgical staging. Obstet Gynecol 1993;82:143–7.[Abstract/Free Full Text]

7. Childers JM, Lang J, Surwit EA, Hatch KD. Laparoscopic surgical staging of ovarian cancer. Gynecol Oncol 1995; 59:25–33.[Medline]

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12. Quasarano RT, Kashef M, Sherman SJ, Hagglund KH. Complications of gynecologic laparoscopy. J Am Assoc Gynecol Laparosc 1999;6:317–21.[Medline]

13. Childers JM, Nasseri A, Surwit EA. Laparoscopic management of suspicious adnexal masses. Am J Obstet Gynecol 1996;175:1451–7.[Medline]

14. Parker WH, Berek JS. Management of selected cystic adnexal masses in postmenopausal women by operative laparoscopy: A pilot study. Am J Obstet Gynecol 1990; 163:1574–7.[Medline]

15. Canis M, Mage G, Pouly JL, Wattiez A, Manhes H, Bruhat MA. Laparoscopic diagnosis of adnexal cystic masses: A 12-year experience with long-term follow-up. Obstet Gynecol 1994;83:707–12.[Medline]

16. Sadik S, Onoglu AS, Gokdeniz R, Turan E, Taskin O, Wheeler JM. Laparoscopic management of selected adnexal masses. J Am Assoc Gynecol Laparosc 1999;6: 313–6.[Medline]

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