Should We Manage Large Ovarian Cysts Laparoscopically?

Abstract

Objective: The aim of this research was to evaluate the feasibility and surgical outcomes of laparoscopic surgery for large ovarian cysts in women <40 years of age. Materials and Methods: This was a retrospective evaluation (Canadian Task Force classification 11-2 design) of 55 women (ages <40) with large ovarian cysts (≥10 cm) with features suggestive of benign disease managed laparoscopically at Paul's Hospital, in Cochin, Kerala, from July 2006 to April 2013. All patients were followed-up for a minimum of 1 year. Patients who were diagnosed as having borderline ovarian tumors were evaluated for their present clinical status at the end of study. Results: Laparoscopic surgery was performed successfully for all patients. The mean operative time, estimated blood loss, and hospital stay were, respectively, 109.6 minutes (range: 40–255), 304.6 mL (range: 100–650), and 1.1 days (range: 1–3). Conversion to laparotomy was performed in none of the patients. Five cases of borderline malignancy were detected. Of these 5 cases; 3 underwent laparoscopic adnexectomy; 1 underwent bilateral cystectomy with staging biopsies, conceived 3 months postsurgery, and subsequently underwent laparoscopic adnexectomy at another center; and 1 underwent a unilateral laparoscopic cystectomy, and had a laparotomy and adnexectomy in another institution after 1 month. Conclusions: The current study supports laparoscopic management of large ovarian cysts as a technically feasible and effective method if proper case selection is applied. (J GYNECOL SURG 32:251)

Introduction

Laparoscopic management of benign ovarian cysts is considered the “gold standard” because of its known benefits.¹ However, most patients with large ovarian cysts are managed with conventional laparotomy. The technical issues include trocar insertion, poor visualization, and difficulty with enucleation and specimen retrieval. The potential risk of malignancy in a large ovarian cyst, and the risk of spillage and upstaging or incomplete staging are other important concerns.² These large ovarian cysts often occur in younger women for whom conservation of reproductive function is a priority. This must be weighed against the low risk of unsuspected malignancy.³

The aim of the current study was to evaluate the feasibility and surgical outcome of laparoscopic surgery for large ovarian cysts in women below 40 years of age.

Materials and Methods

This was a retrospective study of (Canadian Task Force classification 11-2 design) of 55 patients with large ovarian cysts managed laparoscopically from July 2006 to April 2013 in the department of endoscopy, at the Centre for Advanced Endoscopy and Infertility Treatment, Paul's Hospital, Cochin, Kerala, India. The institutional ethics committee of Paul's Hospital approved the study.

Inclusion criteria were ovarian cysts of ≥10 cm and age <40 years.

Exclusion criteria were patients with sonographic features suspicious for malignancy, such as the presence of ascites, solid areas, complex masses, thick irregular septa, and internal or external excrescences, as well as ovarian masses with complex consistencies other than dermoid cysts. In addition, patients with omental cake or pelvic or para-aortic lymphadenopathy noted on computed tomography scans were excluded from the study.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki declaration of 1975, as revised in 2000. Informed consent was obtained from all of the patients who underwent cystectomy or adnexectomy with or without staging biopsies.

Procedures

Data were evaluated for patient characteristics (age, body mass index (BMI), parity, and previous surgeries) and operative details, such as duration of surgery, amount of fluid aspirated, estimated blood loss (EBL), type of surgery, intraoperative complications, postoperative events, conversion to laparotomy, duration of hospital stay, and pathologic findings.

A detailed history was taken for each patient regarding severity of abdominal pain, dysmenorrhea, dyspareunia, bowel symptoms, infertility, previous abdominopelvic infections, and surgeries. Clinical examination, abdominal and transvaginal ultrasonography was performed by the operating surgeon prior to surgery. In celibate patients transabdominal ultrasonography was performed. Preoperative abdominopelvic magnetic resonance imaging (MRI) was performed in cases when suspicious sonographic features were detected. Color Doppler scanning was performed to look for low-resistance flow patterns in patients with suspicion of malignancy. CA-125 testing was performed for all patients and, in selected patients, testing was performed for alpha-fetoprotein, beta–human chorionic gonadotropin, and lactate dehydrogenase.

Patients were admitted to the hospital on the day of surgery and kept nil per oral for 6 hours prior to surgery. Bowel preparation was performed for each patient, using a sodium phosphate solution enema. Antibiotic prophylaxis was administered at the time of induction of anesthesia. Procedures were performed under general anesthesia. All surgical procedures were performed by the first author.

In each patient, a pneumoperitoneum was created using a Veress needle at the Palmer's point, which is 3 cm below the left costal margin in the midclavicular line.⁴ Peritoneal entry was accomplished with a visual technique, using a TERNAMIAN EndoTIP^tm (Karl Storz, Tuttlingen, Germany) 3 cm above the upper border of the mass. The secondary-port positions were modified according to the size and accessibility of the mass. A three accessory-port technique was used, with two ports in the lower quadrants lateral to the inferior epigastric artery and the third port in the suprapubic area. Abdominopelvic inspection was performed to check for omental and bowel adhesions and to confirm the preoperative diagnosis. Peritoneal washings were taken for cytology testing. The ovarian cyst was punctured with a secondary trocar, cyst fluid was aspirated, and the patient was kept in a reverse Trendelenburg position to avoid spillage into upper abdomen. Then the cyst wall was inspected for solid areas and other signs of malignancy.

A decision was made whether to perform cystectomy or adnexectomy with or without staging biopsy. Cystectomy was performed in cases of patients with benign cystic teratomas, endometriotic cysts, cysts without any suspicious solid areas, and in patients who were desirous of fertility preservation. Adnexectomy was chosen when the benign nature of the cysts was doubtful and the contralateral ovaries were normal. Frozen section was not accomplished because of unavailability.

For performing cystectomy, a controlled tear of 1 cm was made on the edge of each cyst by traction with two graspers, rather than using sharp-cutting scissors. This step separated the cyst wall from the ovarian tissue. After identification of the cleavage plane, the cyst wall was held with a toothed grasper and the ovarian tissue was held with an atraumatic grasper; traction and countertraction were applied to separate the cyst from the ovarian tissue. Complete removal of the cyst wall was performed. Enucleation was accomplished gently near the ovarian ligament and hilum to avoid bleeding and injury. In any case when the cyst wall was firmly adherent to the ovary, it was excised with sharp dissection using scissors. A large endobag was used to collect the cyst specimen. Adnexectomy was performed by coagulating and dividing the infundibulopelvic ligament, ovarian ligament, and the medial end of the tube.

In cases of dermoid cysts, special precautions were taken to avoid spillage to prevent chemical peritonitis. A large endobag was placed around each cyst and enucleation of the cysts was carried out in the endobag, avoiding the spillage of the sebaceous material and hair into the peritoneal cavity. The cyst wall and contents were placed in the endobag and removed through a 10-mm trocar site after enlarging the incision to 2–3 cm or by a colpotomy incision. The colpotomy incision was sutured with 1-0 Vicryl®. The peritoneal cavity was lavaged with several L of normal saline, and the floating sebaceous contents were aspirated first from the surface.

In cases when intraoperative findings were suspicious of malignancy, peritoneal washings were collected and multiple peritoneal biopsies were taken from the pelvis and mesentery in the right and the left paracolic area and subdiaphragmatic region, and an infracolic omentectomy was performed.

Postsurgical follow-up

The patients were discharged 1 day after surgery. All patients were followed-up at 1, 6, and 12 months, and were evaluated for any symptoms and recurrences. Postal questionnaires were sent to patients and telephonic inquiries were made to learn about the patients' clinical status.

Statistical analyses

All statistical analyses were performed with the IBM SPSS for Windows, version 20.0. An analysis of variance test was used to compare the quantitative characteristics of the patients and the outcomes. A chi-square test or Fisher's exact test was used to calculate the associations among qualitative characteristics, with significance set at p < 0.05.

Results

Patients' characteristics are shown in Table 1. The mean age of patients was 26.96 years (range: 15–8). The mean BMI was 25.05 (range: 18–42 kg/m²). Forty percent were celibate and 27.27% were nulligravida. The mean diameter of the ovarian cysts was 13.9 cm (range: 10.0–24.0). Chief complaints were abdominal pain in 65.45%, and dysmenorrhea in 14.54%, and 12.72% of the patients presented with infertility, while 7.27% had irregular cycles. Twelve patients had histories of previous surgeries. Fifty-two percent of the patients had CA-125 values >35 international units(IU)/mL, with a mean value of 95 IU/mL, which was not statistically significant. Risk of Malignancy Index (RMI) scores of all the patients were <200. The mean (range) ADNEX [Assessment of Different NEoplasias in the adneXa] model score of all the patients was 97.39% (95%–98.2%) benign.⁵

Table 1.

Patient Characteristics

Variables	N = 55
Age (years)
Mean (range)	26.96 (15–38)
BMI (kg/m²)
Mean (range)	25.05 (18–42)
Parity
Celibate	22 (40.00%)
Nulligravida	15 (27.27%)
Parous	18 (32.73%)
Diameter of cysts (cm)
Mean (range)	13.9 (10–24)
10 ≤ 15	33 (60.0%)
15 ≤ 20	16 (29.1%)
20–25	6 (10.9%)
Symptoms
Abdominal pain	36 (65.45%)
Infertility	7 (12.72%)
Dysmenorrhea	8 (14.54%)
Irregular cycles	4 (7.27%)
# of patients with previous surgery	12
Previous one surgery	9
Previous two or more surgeries	3

BMI, body mass index.

The mean duration of surgery and EBL were 109.6 minutes (range: 40–255) and 304.6 mL (range 100–650), respectively (Table 2). The mean duration of hospital stay was 1.1 day (range: 1–3). Two patients had postoperative fever, and 1 patient had a primary-trocar site infection. There were no conversions to laparotomy and no major intraoperative complications. Laparoscopic surgical procedures performed were as follows: unilateral cystectomy in 23 patients; bilateral cystectomy in 14 patients; staging biopsy in 12 patients, unilateral adnexectomy in 5 patients; and right adnexectomy with left cystectomy in 1 patient. Histopathologic examinations of the cysts showed that 40.0% of the patients had endometriosis, 14.54% had serous cyst adenomas, 18.18% had dermoid cysts, 14.54% had mucinous cyst adenomas, and 9.09% had borderline tumors.

Table 2.

Operative Details

Variables	N = 55
Duration of surgery (min)
Mean (range)	109.6 (40–255)
Fluid aspirated (mL)
Mean (range)	1700.91 (500–6000)
EBL (mL)
Mean (range)	304.64 (100–650)
Type of laparoscopic surgery
Unilateral cystectomy	23 (41.81%)
Bilateral cystectomy	14 (25.45%)
Unilateral cystectomy + staging biopsy	7 (12.73%)
Bilateral cystectomy + staging biopsy	2 (3.63%)
Unilateral adnexectomy	5 (9.09%)
Unilateral adnexectomy + staging biopsy	3 (5.45%)
Right adnexectomy + left cystectomy	1 (1.82%)
Hospital stay (days)
Mean (range)	1.1 (1–3)
Histopathology
Endometriosis	22 (40.00%)
Serous cyst adenoma	8 (14.54%)
Mucinous cyst adenoma	8 (14.54%)
Mixed epithelial	2 (3.63%)
Dermoid cyst	10 (18.18%)
Borderline tumor	5 (9.09%)

min, minutes; EBL, estimated blood loss.

Clinicopathologic factors are shown in Table 3. The proportion of patients with borderline malignancy was significantly higher among those with cysts ≥20 cm but this was not statistically significant.

Table 3.

Clinicopathologic Factors According to Cyst Size

	Cyst size (cm)
Variables	(10 < 15) n = 33	(15 < 20) n = 16	(20–25) n = 6	p-Value
Age (years, mean ± SD)	29.82 ± 5.71	23.56 ± 6.26	20.33 ± 4.89	<0.001
BMI (kg/m²) (mean ± SD)	25.55 ± 4.91	24.94 ± 4.71	22.67 ± 2.58	0.386
Multilocularity on ultrasonography	3 (9.1%)	3 (18.8%)	3 (50%)	0.054
EBL (mL, mean ± SD)	288.79 ± 77.81	312.50 ± 69.52	370.83 ± 143.54	0.092
Duration of surgery (min, mean ± SD)	115.30 ± 49.86	94.63 ± 38.99	118.17 ± 39.37	0.308
Hospital stay (days, mean ± SD)	1.09 ± 0.38	1.00 ± 0.00	1.50 ± 1.22	0.103
Borderline malignancy	2 (6.1%)	1 (6.3%)	2(33.3%)	0.045

SD, standard deviation; BMI, body mass index; EBL, estimated blood loss; min, minutes.

There were 5 cases of borderline malignancy (Table 4). In 1 case, preoperatively, a 24-year-old female had normal tumor markers and no signs that were suggestive of malignancy on ultrasonography and MRI, but she underwent a bilateral cystectomy with staging biopsies, which, on histopathology testing, revealed a borderline mucinous tumor. This patient conceived spontaneously 3 months after surgery, delivered normally, and subsequently had an open hysterectomy with a bilateral salpingo-ophorectomy in another center for recurrence of the cyst.

Table 4.

Characteristics of Patients' Borderline Ovarian Tumors

Patients	Age (yrs)	Parity	CA-125 (IU/mL)	Cyst diameter (cm)	Ultrasonography findings	RMI Score/ ADNEX Model	Type of laparoscopic surgery	Histopathology	Follow-up (May 2014)
1	1	Celibate	25	23	Multiloculated cyst with thick septations without solid areas	25/96.8	Right adnexectomy with staging biopsy (13/06/2012)	Borderline mucinous tumor	No evidence of recurrence (after 2 yrs)
2	24	Nulligravida	30	10	Bilateral multiloculated cyst without solid areas	90/98.1	Bilateral cystectomy with staging biopsies (23/2/2010)	Borderline mucinous tumor	Conceived after 3 mos, FTND, followed by total abdominal hysterectomy with bilateral salpingo-ophorectomy for recurrence of cyst 1 mo after delivery; no recurrence (after 3 yrs)
3	25	Celibate	115	20	Multiloculated cyst without solid areas	115/95	Unilateral cystectomy (7/11/2006)	Borderline mucinous tumor	Laparotomy with adnexectomy 1 mo later (no recurrence after 8 yrs)
4	28	P1L1	39	19	Multiloculated cyst without solid areas	39/96.4	Right adnexectomy (28/2/2006)	Borderline mucinous tumor	No recurrence (after 8 yrs)
5	38	P2L2, sterilized	100	11	Multiloculated cyst without solid areas	100/96.3	Right adnexectomy (5/8/2011)	Borderline mucinous tumor with foci of microinvasion	No recurrence (after 3 yrs)

yrs, years, IU, international units; RMI, Risk of Malignancy Index; ADNEX, Assessment of Different NEoplasias in the adneXa; FTND, full-term normal delivery; mo, month; P, para; L, live.

Three other patients with borderline malignancy had normal tumor markers and no signs suggestive of malignancy noted on ultrasonography and MRI. These patients underwent laparoscopic adnexectomies, which, on histopathologic examination, revealed borderline mucinous tumors with foci of microinvasion. These patients did not undergo any other surgeries or receive any chemotherapy after this surgery. There were no recurrences noted on follow-ups at 1, 6 and 12 months.

There was another 25-year-old patient who had unilateral laparoscopic cystectomy for a 20-cm multiloculated cyst and, postoperatively, she had a prolonged low-grade fever for 3 days with encysted fluid collection noted on postoperative ultrasonography, which was managed by antibiotics. Her histopathology testing revealed a borderline mucinous tumor. This patient underwent laparotomy and adnexectomy in another institution 1 month after the first surgery.

Clinicopathologic factors of patients with borderline malignancy are compared in Table 5. Borderline malignancy was significantly associated with multilocularity on ultrasonography.

Table 5.

Clinicopathologic Factors of Patients with Borderline Malignancy

	Borderline malignancy
Variables	No (n = 50)	Yes (n = 5)	p-Value
Age (years, mean ± SD)	27.06 ± 6.68	26.00 ± 8.28	0.742
BMI (kg/m²) (mean ± SD)	24.92 ± 4.56	26.4 ± 6.10	0.505
Cyst size (cm, mean ± SD)	13.69 ± 3.73	16.60 ± 5.77	0.12
Multilocularity on ultrasonography	7 (14%)	5 (100%)	<0.001
EBL (mL, mean ± SD)	290.60 ± 65.23	445.00 ± 148.32	<0.001
Fluid aspirated (mL, mean ± SD)	1615.00 ± 1165.72	2560.00 ± 904.43	0.085
Operating time (min, mean ± SD)	109.58 ± 45.12	109.80 ± 62.15	0.992
Hospital stay (days, mean ± SD)	1.06 ± 0.314	1.60 ± 1.34	0.022

SD, standard deviation; BMI, body mass index; EBL, estimated blood loss; min, minutes.

All of the patients were followed up for a period of 1 year at 1, 6 and 12 months with clinical examinations, CA-125, transabdominal sonography, and transvaginal sonography. Only 1 patient with endometriosis had a recurrence of her endometrioma and had repeat surgery.

Discussion

Laparoscopic surgery is considered the treatment of choice in the management of small-to-moderate sized ovarian cysts, but experience related to laparoscopic surgery as a treatment modality for large ovarian masses remains limited.¹

In the present study, 10 was used cm as a definition for a large ovarian cyst as was done in a similar study.⁶ A randomized prospective study by Yuen et al. in patients with benign ovarian masses showed that laparoscopic surgery can reduce operative morbidity, postoperative pain, analgesics' use, hospital stay, and recovery period.⁷ Several studies have reported on laparoscopic surgery for patients with large ovarian cysts, but the numbers of patients included in these reports were small.^8–10

A patient's age is an important consideration when managing a large ovarian cyst. Cystectomy for management of a large ovarian cyst is usually performed in young women who desire to preserve their ovarian functions.¹¹ In the current study, the mean age of the patients was 26.96 years (range: 15–38), compared to a study by Alobaid et al. in which the mean age was 30.6 years.¹ The chief complaint was abdominal pain in 65.45% of patients in the current study, which was similar to a study by Eltabbakh et al. in which 69.7% presented with abdominal pain.² Lim et al. had 29.6% patients presenting with abdominal pain and discomfort as the chief complaints.¹² In the current study, the mean cyst size was 13.9 cm (range: 10–24), compared to a range of 13–14.6 cm in other studies.^2,12

Peritoneal entry was accomplished using the TERNAMIAN EndoTIP to avoid inadvertent rupture of the cysts, whereas Eltabbakh et al. applied an open technique using a Hasson's cannula.² In patients who were desirous of fertility preservation, cystectomy was performed after cyst aspiration. Stamatellos et al. described cyst aspiration in large cysts to aid their removal laparoscopically after malignancy had been excluded.¹³ There are serious concerns, such as intraperitoneal spillage, which may cause pseudomyxoma peritonei or peritoneal seeding of cancer. Therefore, treatment of a cyst must include careful and copious peritoneal lavage performed immediately after the procedure, using several L of irrigation saline.¹⁴ It has been shown that, with copious saline irrigation, postoperative chemical peritonitis is <1%.^15,16

The reverse Trendelenburg position is important at the end of the procedure to optimize the results of lavaging. In cases of dermoid cysts, the cystectomies were performed in endobags to reduce spillage, whereas, in a study by Chong et al., a puncture site on a cyst was held using a Kelly clamp to prevent spillage.¹¹ Irrigating the abdominal cavity with several L of saline involves long operating time, which is a limitation of the current authors' technique. Conversion to laparotomy occurred in none of the patients, whereas conversion to laparotomy occurred in 4.9%–6.1% of patients in other studies.^2,12

In the current study, histopathologic examination revealed benign tumors in 90.91% of the cases, and 5 cases (9.09%) had borderline malignancy, which was high compared to the 3.7% reported by Lim et al.¹² However, in the Lim et al. study, the incidence of invasive epithelial ovarian carcinoma was 2.5%, and, in the current study, there were no cases of malignancy.¹² All of the 5 cases of borderline malignancy had no features (exclusion criteria) suggestive of malignancy noted on preoperative workups, and their RMI scores were <200.¹⁷ All borderline malignancy cases were multiloculated, compared to 14% in the benign group, which was statistically significant. Two of the borderline malignancies were >20 cm, but this was not statistically significant, compared to the sizes of the benign cysts.

According to Fauvet et al., borderline malignancy can be managed by laparoscopic cystectomy or adnexectomy and patient survival is not affected, although the chance of recurrence was high in that study's cystectomy group.¹⁸ However, tumor recurrence and metastatic disease are rare in borderline mucinous ovarian tumors.¹⁹ In the current study, there were 5 cases of borderline malignancy and 1 of these patients underwent unilateral laparoscopic cystectomy and another 1 underwent bilateral cystectomy with staging biopsies. The former patient underwent laparotomy and adnexectomy at another center 1 month later, while the latter patient conceived 3 months postsurgery, and post delivery she had an open hysterectomy with a bilateral salpingo-ophorectomy for recurrence of her cyst. The other 3 patients underwent unilateral adnexectomies with staging biopsies performed in one of these procedures. These 3 patients were normal at follow-up.

There was a recurrence of an endometriotic cyst in only 1 patient, who presented with primary infertility; she had to undergo a repeat laparoscopic cystectomy 3 years after her primary surgery.

Port-site metastasis after laparoscopic removal of malignant tissue is another reported complication.^20,21 In the current cases, the ovarian cysts were extracted using an endobag to prevent port-site contamination. None of these patients developed metastatic lesions on trocar sites during the study's follow-up period.

Because of the potential risk of malignancy, selection of patients for laparoscopic management of large ovarian cysts is very important. It is generally agreed that ovarian cancer should not be managed laparoscopically, especially when operators are not able to perform the surgical procedure without rupture.²² It is uncertain whether or not an intraoperative rupture has the same prognostic significance as ovarian-surface involvement and/or positive peritoneal washings in stage I ovarian cancers.^23–26 However, most patients with ruptured cysts need postoperative chemotherapy. The new ADNEX Model scoring system can help to some extent in early detection of borderline malignancy. When an adenexectomy is planned, use of an endobag helps prevent spillage of contents. In cases of small cysts, enucleation in toto helps prevent spillage. For large cysts, aspiration in the reverse Trendelenburg position minimizes spillage risk.

Lecuru et al., in a retrospective multicenter study, suggested that there was no difference in outcome after laparoscopic management of ovarian cancer, but surgical staging was suboptimal in a significant number of laparoscopically managed cases.²⁷ In the current study, laparoscopic staging biopsies of ovarian cysts was performed in 12 cases (22.2%) that had intraoperative findings that were suspicious of malignancy. Exploration of the retroperitoneum for lymph nodes was not performed, as MRI/CT scans did not reveal any enlarged lymph nodes. However, in cases of malignancy, this staging is suboptimal and was a limitation of the current study. Nonavailability of frozen section was also a limitation of the current study.

In the current study, a higher incidence of borderline malignancy was observed than had been seen in other studies. The current authors agree that there could have been a selection bias in the cohort, as the Paul Hospital center is known for laparoscopic management in infertility and gynecology rather than gynecology/oncology. Thus, patient selection was not optimal. When selecting patients for management of ovarian cysts laparoscopically, the potential risk of malignancy is a major concern. Large cysts with multilocularity noted on ultrasonography scans should alert clinicians to doubt the benign nature of such cysts. The role of sonography has been emphasized in the recent ADNEX Model scoring system. However, laparoscopic management of large ovarian cysts is technically feasible if proper patient selection is made.

Conclusions

The limiting factor for laparoscopic management of large ovarian cysts is not cyst size but rather the potential risk of malignancy, given that a higher incidence of borderline malignancy was observed. Large multiloculated ovarian cysts should be considered as potentially malignant and an oncologist should be consulted for an opinion. Adnexectomy may be a better option for such cases, provided that the contralateral ovaries are normal. The current study supports laparoscopic management of large ovarian cysts as a technically feasible and effective method if proper case selection is made.

Footnotes

Author Disclosure Statement

The authors declare that they have no conflicts of interest.

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