Ovarian Cancer Surgical Staging,Laparoscopy Versus Laparotomy: A Comparative Study

Abstract

Background:

There are many concerns regarding using laparoscopically assisted staging surgery for ovarian cancer. In this study, we aimed to compare between conventional open laparotomy and laparoscopically assisted surgical staging of relatively early stage ovarian cancer regarding the surgical (operative and postoperative) and oncologic patients outcomes.

Patients and Methods:

We included 60 patients with ovarian cancer and divided them into two groups: the first group included 30 patients who underwent laparoscopic surgical staging and the other group included 30 patients who underwent open abdominal surgical staging.

Results:

We showed that patients who underwent laparoscopy have longer operative time, shorter time of hospital stay, and a shorter time interval between operation and starting chemotherapy than patients who underwent open surgery (p < 0.001). We found that patients who underwent laparoscopy have higher number of dissected pelvic and para-aortic lymph nodes than patients who underwent open surgery (p < 0.001).

Conclusions:

We showed the feasibility of laparoscopy in surgical staging of ovarian cancer performed by a qualified surgical team for selected ovarian cancer patients as it contributed to decreased intraoperative blood loss, earlier recovery, and shorter hospital stay than laparotomy. (J GYNECOL SURG 36:179)

Introduction

Epithelial ovarian cancers are a group of common cancers that are ranked as the fourth commonest gynecologic malignancies. The prognosis of such cancers is determined by their stage.¹ The standard guidelines for ovarian cancer staging surgery included total hysterectomy, bilateral salpingo-oophorectomy in addition to excision of the pelvic and/or para-aortic lymph nodes and omentum, in addition to taking several intra-abdominal biopsies through laparotomy. Histopathologic examination of the specimen gives clear data about the pathologic stage and the need for postoperative adjuvant therapy.²

Recently, due to advancement of minimally invasive surgeries, it becomes applied for surgery of malignant tumors not only for surgical management of benign lesions.^3,4 Querleu and LeBlanc have first reported in 1994 using laparoscopy for the accurate staging of ovarian tumors by performing dissection of infrarenal para-aortic lymph nodes.⁵ Since then, several studies highlighted benefits of laparoscopic surgery in management of ovarian cancers, which include reduction of pain, rapid recovery, shorter duration of postoperative hospitalization, and early initiation of chemotherapy.^6,7 But there are many concerns regarding using laparoscopically assisted ovarian cancer surgical staging approach, including postlaparoscopy malignant tissue implantation, inducing metastases at port site in addition to spillage of tumor. In addition, the accuracy of laparoscopically assisted complete ovarian cancer surgical staging in comparison with that of laparotomy is still unknown.² Laparoscopic surgical staging is a complex procedure in gynecology that needed a specific and long training period.

In this study, we aimed to compare between conventional open laparotomy and laparoscopically assisted surgical staging of relatively early stage ovarian cancer regarding the surgical (operative and postoperative) and oncologic patients outcomes.

Materials and Methods

The protocol of the current retrospective study was approved by the local Ethical Committee of Faculty of Medicine, Zagazig University. We included 60 female patients who underwent staging management for cancer of ovary in the period from August 2016 to August 2019 at General Surgery Department and Gynecology and Obstetrics Department, Faculty of Medicine, Zagazig University Hospital.

Inclusion criteria for patients in our study were (1) clinical and radiologic evidence of relatively early stage ovarian cancer, (2) no gross or radiologic evidence of the presence of distant metastasis, and (3) no evidence of severe cardiopulmonary disease.

The excluded criteria are (1) clinical and radiologic evidence of advanced ovarian cancer of International Federation of Gynecology and Obstetrics (FIGO) stage IV, (2) clinical and radiologic evidence of malignancy of another organ, and (3) patients who have a history of fertility-sparing surgery.

Preoperative routine

The preoperative routine included pelvic examination, imaging, and blood sampling.

Before laparoscopy, all included patients were informed about the therapeutic options, the risk of the procedures, and possibility of conversion to laparotomy. We acquired patients' written consent for using their personal data for our research.

Surgical procedures

The patients' specimens were staged using the recommendations of FIGO.⁸ We estimated amount of lost blood from suction devices contents evaluation. Period of hospital stay was assessed starting from the first day after operation. We considered transfusion of blood, organ damage, and changing the procedure of laparoscopy to laparotomy (in women who underwent laparoscopic surgery) as intraoperative complications.

We calculated operative time as the time from skin to skin. We defined postoperative complications as any adverse events related to the procedure and occurred within 30 days of surgery.

Technique of laparoscopic surgery

The patients were placed in the lithotomy position and a general endotracheal tube anesthesia was placed. We used a self-made uterine manipulator. We performed laparoscopy using carbon dioxide with intra-abdominal pressure of ∼12 mm Hg. We inserted a Veress needle for creating pneumoperitoneum through the umbilicus, and we inserted a 10-mm trocar through the umbilical incision. We placed the patients in Trendelenburg position, then we inserted three ancillary trocars under direct vision. At first, we explored the pelvic, abdominal organs, and the peritoneal surface. The staging procedure included performing total hysterectomy, bilateral salpingo-oophorectomy, and dissection of pelvic and para-aortic lymph nodes on both sides in addition to omentectomy and appendectomy.⁹

Laparotomy technique

The surgical procedures of laparotomy were similar to laparoscopy, except that we made a vertical midline abdominal incision.

We gave all patients an antibiotic prophylaxis half an hour preoperatively (intravenous cefoxitin sodium 2 g).

Postoperative management

Patients were given six cycles of platinum-based adjuvant chemotherapy, every 3 weeks, based on risk according to cancer grade and stage.

We evaluated the studied patients with full pelvic examination and detailed ultrasound assessment every 3 months for the first 2 years, then for every 6 months for the first 5 years, and every year thereafter. We recorded time and areas of recurrence. We calculated disease-free survival rate from the operation time to time of recurrence or to time of the last follow-up in patients who were not presented with recurrence.

We calculated overall survival rate from surgery to date of death or to date of last follow-up.

Statistical analysis

We collected, processed, and analyzed data using SPSS 22.0 for Windows (SPSS, Inc., Chicago, IL). Tests used were chi-square test and Fisher's exact test for different variables, whereas the Kaplan–Meier method and the log-rank test for assessment of survival rates.

Results

Demographic data and patient characteristics

This study included 60 patients with relatively early stage ovarian cancer and we divided them into two groups: the first group included 30 patients who underwent laparoscopic surgical staging, and the other group included 30 patients who underwent open abdominal surgical staging.

We found no statistically significant differences in both groups regarding age, histologic type, grade, or stage of the tumors.

Detailed patient characteristics are found in Table 1.

Table 1.

Demographic Data and Characteristics of Studied Patients

Variables	Total	Management techniques		p
	Total	Laparoscopy	Open surgery
	N = 60 (%)	n = 30 (%)	n = 30 (%)
Age (years)
Mean ± SD	47.93 ± 10.57	46.43 ± 11.2	50.33 ± 9.29	0.147
Range	25–65	25–60	25–65
Comorbidity
Absent	44 (73.3)	25 (56.8)	19 (43.2)	0.08
Present	16 (26.7)	5 (31.2)	11 (68.8)
Histopathologic type
Endometroid	10 (16.7)	4 (40)	6 (60)
Mucinous	20 (33.3)	10 (50)	10 (50)	0.766
Serous	30 (50)	16 (53.3)	14 (46.7)
Operation
Optimal debulking	22 (36.7)	6 (27.3)	16 (72.7)
Radical surgery	38 (63.3)	24 (63.2)	14 (36.8)	0.007^*
Grade
High	12 (20)	5 (41.7)	7 (58.3)	0.519
Low	48 (80)	25 (52.1)	23 (47.9)
FIGO stage
IA	11 (18.3)	5 (45.5)	6 (54.5)	0.739
IB	8 (13.3)	6 (75)	2 (25)	0.254
IC	11 (18.3)	8 (72.7)	3 (27.3)	0.181
IIB	8 (13.3)	5 (62.5)	3 (37.5)	0.797
IIC	8 (13.3)	0 (0)	8 (100)	0.005^*
IIIA	4 (6.7)	2 (50)	2 (50)	1
IIIB	10 (16.7)	4 (40)	6 (60)	0.731
Lymph node
Negative	46 (76.7)	24 (52.2)	22 (47.8)
Positive	14 (23.3)	6 (42.9)	8 (57.1)	0.542
Distant metastasis
Negative	60 (100)	30 (50)	30 (50)	1

p < 0.05 is statistically significant.

FIGO, International Federation of Gynecology and Obstetrics; SD, standard deviation.

Operative and perioperative results

Detailed operative findings are found in Table 2.

Table 2.

Correlations Between Operative and Peroperative Findings of Studied Patients

Variables	Total	Management techniques		p
	Total	Laparoscopy	Open surgery
	N = 60 (%)	n = 30 (%)	n = 30 (%)
Pelvic node count
Mean ± SD	17.05 ± 3.12	19.77 ± 1.85	14.33 ± 1.03	<0.001^**
Range	13–23	17–23	13–16
Para-aortic lymph node count
Mean ± SD	7.12 ± 1.49	8.17 ± 1.09	6.07 ± 1.02	<0.001^**
Range	5–10	7–10	5–8
Operative time (minutes)
Mean ± SD	259.75 ± 50.97	307.83 ± 17.75	211.67 ± 13.67	<0.001^**
Range	190–340	280–340	190–230
Blood loss (mL)
Mean ± SD	600	570	600	0.186
Range	500–1200	250–1200	300–1200
Hospital stay (days)
Mean ± SD	4.8 ± 1.33	3.83 ± 0.75	5.77 ± 1.04	<0.001^**
Range	3–8	3–5	4–8
Time to adjuvant therapy
Mean ± SD	24.53 ± 5.28	19.87 ± 2.99	29.2 ± 1.63	<0.001^**
Range	13–32	13–25	27–32
Intraoperative complications
Absent	53 (88.3)	28 (52.8)	25 (47.2)	0.424
Present	7 (11.7)	2 (28.6)	5 (71.4)

p ≤ 0.001 is statistically highly significant.

We showed that patients who underwent laparoscopy have longer operative time, shorter time of hospital stay, and a shorter time interval between operation and starting chemotherapy than patients who underwent open surgery (p < 0.001). That was a clinically important difference, as the sooner the starting of chemotherapy, the better the prognosis will be.

We found that patients who underwent laparoscopy have higher number of dissected pelvic and para-aortic lymph nodes than patients who underwent open surgery (p < 0.001), we found no statistically significant difference in the incidence of intraoperative complications between both studied groups. We showed that patients who underwent open surgery have a higher rate of postoperative complications than patients who underwent laparoscopy. We recorded no postoperative deaths.

Follow-up results and patients outcome

We followed our patients for 36 months and assessed progression, recurrence, and survival outcomes after surgery (Table 3). Mean recurrence free survival (RFS) in the laparoscopy group was 25.36 months, whereas median RFS in the open surgery group was 21.79 months. Mean overall survival (OS) in the laparoscopy group was 31.83 months, whereas mean OS in the open surgery group was 28.5 months.

Table 3.

Comparison Between Patients Who Underwent Different Surgical Techniques Regarding Response to Treatment and Patient Outcome (Relapse and Death)

Variables	Total	Management techniques		p
	Total	Laparoscopy	Open surgery
	N = 60 (%)	n = 30 (%)	n = 30 (%)
Chemotherapy (n = 22)
Resistant	15 (68.2)	6 (40)	9 (60)	1
Sensitive	7 (31.8)	2 (28.6)	5 (71.4)
Response after four cycles
CR	42 (70)	26 (61.9)	16 (38.1)
PD	2 (3.3)	1 (50)	1 (50)
PR	14 (23.3)	2 (14.3)	12 (85.7)	0.023^*
SD	2 (3.3)	1 (50)	1 (50)
Response after eight cycles
CR	56 (93.3)	28 (50)	28 (50)
PD	2 (3.3)	1 (50)	1 (50)	1
SD	2 (3.3)	1 (50)	1 (50)
Postoperative complications
Absent	44 (73.3)	25 (56.8)	18 (43.2)
present	16 (26.7)	5 (31.2)	11 (68.8)	0.08
Relapse (n = 56)
Absent	34 (60.7)	20 (58.8)	14 (41.2)
Present	22 (39.3)	8 (36.4)	14 (63.6)	0.101
Death
No	46 (76.7)	25 (54.3)	21 (45.7)
Yes	14 (23.3)	5 (35.7)	9 (64.3)	0.222
Disease-free survival
Mean ± SD	2.27 ± 0.75	2.43 ± 0.84	2.11 ± 0.88	0.166
Range	1–3	1–3	1–3
Overall survival
Median	33	33	22	0.179
Range	11–36	11–36	11–36

p < 0.05 is statistically significant.

CR, complete response; PD, progressive disease; PR, partial response; SD, stable disease.

We found no cases of port-site metastases or recurrence. There were statistically nonsignificant differences between both groups regarding response to treatment after eight cycles, postoperative complications, recurrence, death, recurrence-free survival, or overall survival rates.

Discussion

Laparotomy was the traditional approach of surgical staging of ovarian cancer patients. In 1973, Bagley et al. published the first study about using laparoscopy for ovarian cancer patients.¹⁰

Chen et al. reported a comparative study between using laparotomy and laparoscopy for surgical staging of ovarian cancer patients in the early stage.¹¹ They showed that laparoscopy has a longer time of operation, a lower intraoperative blood loss, and a shorter duration of hospital stay than laparotomy, which pointed to feasibility of using laparoscopically assisted surgical staging for patients with ovarian cancer.

Similar results were found by previous researchers that laparoscopically assisted staging surgery for ovarian malignancies patients in the early stages is effective.^12–14

Since a decade, there are much technical and conceptual advancement in laparoscopic treatment and staging of ovarian cancer patients, but there are some noted pitfalls for patients managed with laparoscopy.^15–18

In this study, we compare between using laparoscopy and laparotomy for surgical staging of ovarian cancer and we showed that both management techniques are safe and feasible, but the laparoscopic technique has more advantages than traditional laparotomy: lower intraoperative blood loss, larger number of harvested lymph nodes, shorter duration of hospitalization and shorter duration of starting postoperative adjuvant therapy. In addition, we showed that the magnification power of laparoscopy provided a better peritoneal surface view than its direct visualization during laparotomy. Similarly, previously published studies showed near results.^2,9,14,18

We found that laparoscopy has more operative time than laparotomy; Minig et al. obtained slightly different results by finding a similar surgical time between their groups of patients.¹⁸ Also, similar surgical time in both laparoscopy and laparotomy was shown by other authors.^15,19 During the follow-up period, disease-free survival and overall survival rates were similar among both groups, which were in line with previously published studies.^14,15,18,19

This showed that laparoscopy is an excellent technique with many advantages, but there are still many concerns about risks detected during use of laparoscopic surgery in ovarian cancer that included cancer upstaging due to intraoperative rupture of the cancer in addition to occurrence of metastasis at port site, but these disadvantages could be avoided by improvement of the instruments and hand skills of the laparoscopy team and the need for specialized devices to remove the tumor without rupture or tumor spillage.² Laparoscopy was found to be a feasible and safe technique with a lower complication rate that has ranged in previous studies from 0% to 17%.^9,16–19 Laparoscopic surgery safety required not only a perfect surgical team and techniques but also needed a careful ovarian cancer patient selection.

Size of the ovarian cancer has been found to have a role in the success of laparoscopy in removing the tumor without spillage. The maximum accepted size of the ovarian cancer that allows performing surgical staging by laparoscopy successfully without rupture is a matter of controversy, some authors showed that a size of 10 cm is the maximum allowed size to make the procedure using laparoscopy, whereas others have stated that the size of the tumor must be small enough to completely enter in the laparoscopic bag independent from its size.¹⁸ Occurrence of port-site metastases was not detected in our study, in accordance with Ramirez et al.²⁰ It was previously found that the incidence of occurrence of port-site metastasis ranged from 2% to 26% in advanced ovarian cancer patients who underwent laparoscopic evaluation.²¹

Summary and conclusion

In this study when comparing laparoscopy and laparotomy in surgical staging of relatively early stage ovarian cancer patients, we showed that laparoscopy provided a better operative field visualization in addition to enhanced magnification, which allowed better tumor removal, between surgical staging. Moreover, laparoscopy contributed to decrease in intraoperative blood loss, earlier recovery, and shorter hospital stay that lead to decrease in postoperative morbidity in comparison with laparotomy. Because of the several advantages of laparoscopy when performed by a qualified surgical team for selected ovarian cancer patients, it was found to be more feasible and effective than laparotomy.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funds were received for this article.

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