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Laparoscopy versus laparotomy for FIGO stage I ovarian cancer

  1. Theresa A Lawrie1,
  2. Lídia RF Medeiros2,
  3. Daniela D Rosa3,*,
  4. Maria Ines da Rosa4,
  5. Maria I Edelweiss5,
  6. Airton T Stein6,
  7. Alice Zelmanowicz7,
  8. Anaelena B Moraes8,
  9. Roselaine R Zanini8

Editorial Group: Cochrane Gynaecological Cancer Group

Published Online: 28 FEB 2013

Assessed as up-to-date: 23 NOV 2012

DOI: 10.1002/14651858.CD005344.pub3

How to Cite

Lawrie TA, Medeiros LRF, Rosa DD, da Rosa MI, Edelweiss MI, Stein AT, Zelmanowicz A, Moraes AB, Zanini RR. Laparoscopy versus laparotomy for FIGO stage I ovarian cancer. Cochrane Database of Systematic Reviews 2013, Issue 2. Art. No.: CD005344. DOI: 10.1002/14651858.CD005344.pub3.

Author Information

  1. 1

    Royal United Hospital, Cochrane Gynaecological Cancer Group, Bath, UK

  2. 2

    Post-graduation Program in Medical Sciences, Universidade Federal do Rio Grande do Sul, Social Medicine/Epidemiology, Porto Alegre, Rio Grande do Sul, Brazil

  3. 3

    Hospital Moinhos de Vento, Oncology Unit, Porto Alegre, Rio Grande do Sul, Brazil

  4. 4

    Universidade do Extremo Sul Catarinense, Medical School, Criciuma, Santa Catarina, Brazil

  5. 5

    Faculty of Medicine at Federal University of Rio Grande do Sul, Pathology, Rio Grande do Sul, Brazil

  6. 6

    Universidade Federal de Ciências da Saúde, Department of Public Health, Porto Alegre, Brazil

  7. 7

    Complexo Hospitalar Santa Casa, Cancer Prevention Centre, Rio Grande do Sul, Brazil

  8. 8

    Federal University of Rio Grande do Sul, Postgraduate Program in Epidemiology, Rio Grande do Sul, Brazil

*Daniela D Rosa, Oncology Unit, Hospital Moinhos de Vento, Rua Tiradentes 333, 2nd floor, Porto Alegre, Rio Grande do Sul, 90560-030, Brazil. dornellesrosa@hotmail.com.

Publication History

  1. Publication Status: Edited (no change to conclusions)
  2. Published Online: 28 FEB 2013

SEARCH

 

Background

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Description of the condition

This is an updated version of the original review that was first published in the Cochrane Database of Systematic Reviews 2008, Issue 4.

Ovarian cancer is the eighth most common cancer in women worldwide (Jemel 2011). A woman's risk of developing ovarian cancer before the age of 75 ranges from 0.5% in developing countries to 1% in developed countries (GLOBOCAN 2008; Jemel 2011). Just over a third of women with ovarian cancer are alive five years after diagnosis (EUROCARE 2003), largely because most women with ovarian cancer are diagnosed when the cancer is already at an advanced stage (Jemal 2008). International Federation of Gynaecology and Obstetrics (FIGO) stage I ovarian cancer (limited to the ovaries) is diagnosed in approximately 20% to 33% of women with ovarian cancer in developed countries (Maringe 2012) and diagnosis is usually made by accidental discovery at sonography, computerised tomography (CT scanning) or during laparoscopy. The incidence of accidental discovery of ovarian cancer at laparoscopy has been estimated to range from 0.65% (Wenzl 1996) to 0.9% (Muzii 2005) of premenopausal women and 3% of postmenopausal women who undergo the procedure for an adnexal mass (Muzii 2005), but may be higher depending on the selection criteria applied.

Most cancers of the ovary are epithelial (90%) with histological subtypes including serous (35%), endometrioid (10%), borderline (16%), mucinous (8%), clear cell (4%), undifferentiated and mixed epithelial (Kosary 2007). In general, the prognosis of ovarian tumours depends on the FIGO stage, tumour grade, histological subtype, age and the volume of residual disease after surgery (Benedet 2000), however for stage I tumours the most important prognostic indicators are considered to be the degree of differentiation (grade) and the occurrence of tumour rupture (Vergote 2001).

The standard management of women with ovarian cancer is comprehensive surgical staging by laparotomy, a midline abdominal incision that allows exposure of the entire abdomen. Comprehensive surgical staging includes a total hysterectomy, bilateral salpingo-oophorectomy, removal of all obvious sites of tumour, aspiration of cytological washings or ascites, omentectomy, retroperitoneal (pelvic and para-aortic) lymph node dissection or sampling and biopsy of all suspicious-looking areas including mesentery, liver and diaphragm (Benedet 2000; Schorge 2012). Systematic retroperitoneal lymph node dissection (RLND) may improve survival in stage I ovarian cancer by detecting microscopic disease (Chan 2007) and is considered a standard procedure in some centres (Schorge 2012), however the UK National Institute for Clinical Excellence (NICE) guidelines currently do not recommend RLND in stage I disease (NICE 2011).

A meta-analysis of four randomised controlled trials (RCTs) of adjuvant platinum-based chemotherapy, which included data from the International Collaborative Ovarian Neoplasm 1 (ICON1) trial (Trimbos 2003) and the Adjuvant Chemotherapy in Ovarian Neoplasm (ACTION) trial (Trimbos 2004), found that adjuvant chemotherapy significantly improved overall survival (OS) and progression-free survival (PFS) in women with early ovarian cancer (Winter-Roach 2012). However, it was considered not to be necessary in women with comprehensively staged, stage Ia or 1b grade 1 to 2 tumours, as subgroup analyses suggested that women who were optimally staged were unlikely to benefit from adjuvant chemotherapy. Hence, comprehensive surgical staging has an important impact on the subsequent management of women with early ovarian cancer, with adjuvant chemotherapy indicated when staging is considered to be inadequate (Elit 2004; Winter-Roach 2012).

 

Description of the intervention

The intention of surgical staging is to establish a diagnosis, to assess the extent of the disease and to remove as much gross tumour as possible (Schorge 2012). Surgical staging of ovarian cancer by laparoscopy is the same intra-abdominal procedure as that performed by laparotomy except that it involves two or more, much smaller, abdominal incisions, through which laparoscopic instruments are then inserted. Specimen retrieval bags are used to prevent spillage and possible seeding of cyst contents and to avoid contact with incision (port) sites. Cysts may be aspirated within the retrieval bag, or morcellated if solid, to facilitate extraction through the port sites (Ghezzi 2007). Larger specimens, like omentum, may be extracted through the vagina with the uterus after hysterectomy (Lee 2011; Park 2008a).

 

How the intervention might work

Several recent non-randomised studies (NRSs) in early ovarian cancer have reported that laparoscopic surgical staging is a safe and technically feasible procedure (Colomer 2008; Ghezzi 2009; Nezhat 2009; Park 2008b; Park 2010). The possible advantages of laparoscopy include smaller incisions, less blood loss, faster recovery, shorter hospital stay, fewer complications, less postoperative infection and a better visualisation of the tumour inside the abdomen as the laparoscopy image can be magnified (Gad 2011; Ghezzi 2007; Lee 2011). In addition, the shorter recovery period following laparoscopy means that chemotherapy can be commenced sooner compared with laparotomy (Ghezzi 2007; Nezhat 2009), potentially resulting in a favourable effect on survival.

However, laparoscopy has been associated with a higher rate of intraoperative cyst rupture for apparently benign (Muzii 2005) and borderline tumours (Fauvet 2005), which may result in upstaging of the unexpected ovarian cancer from stage Ia or 1b to Ic (Muzii 2005). It has been argued that some aspects of comprehensive surgical staging, particularly RLND, may be technically difficult to achieve via laparoscopy and, therefore, that laparoscopy should be restricted to women with pre-operative evidence of benign conditions only (Vergote 2004). Other disadvantages of laparoscopy may include longer operating times and the possibility of port-site metastases, although the risk of the latter in early disease is considered to be low (Schorge 2012). Furthermore, to facilitate laparoscopy, CO₂ is commonly used for pneumoperitoneum and has been shown to lower the peritoneal pH (Bergstrom 2008; Kuntz 2000) which may activate enzymes that increase tumour cell mitosis and growth factor production. In addition, mechanical damage to the mesothelium may occur with prolonged laparoscopic surgery, thereby increasing the risk of metastases in the abdominal cavity (Greene 1995; Volz 1999).

 

Why it is important to do this review

Laparoscopic surgical staging of stage I ovarian cancer remains controversial as it is unclear how the risks and benefits of this procedure compare with the conventional open approach by laparotomy. An earlier version of this systematic review, published in 2008, found insufficient evidence to evaluate laparoscopy for the management of early ovarian cancer as routine clinical practice. We continue to update this review with the aim of clarifying and consolidating the available evidence regarding this alternative surgical approach.

 

Objectives

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

To evaluate the benefits and harms of laparoscopy in the surgical treatment of FIGO stage I ovarian cancer (stages Ia, Ib and Ic) when compared with laparotomy.

 

Methods

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Criteria for considering studies for this review

 

Types of studies

RCTs and quasi-RCTs. We also considered prospective case-control studies where the results had been adjusted for the baseline case mix using multivariate analyses, and excluded those with historical (non-concurrent) controls.

 

Types of participants

Women with stage I ovarian cancer defined by FIGO as follows.

  • Stage Ia: unilateral tumours
  • Stage Ib: bilateral tumours
  • Stage Ic: identified tumour spillage, tumour capsular penetration, positive peritoneal cytology

 

Types of interventions

Surgical staging via laparoscopy (experimental group) versus laparotomy (control group) for stage I ovarian cancer.

 

Types of outcome measures

 

Primary outcomes

  1. Overall survival (OS)
  2. Progression free survival (PFS)

 

Secondary outcomes

  1. Operating time
  2. Intraoperative tumour rupture
  3. Pelvic and para-aortic lymph node yield
  4. Size of omental specimen
  5. Estimated blood loss and the need for blood transfusion
  6. Comprehensive staging achieved by the allocated procedure (conversion to laparotomy)
  7. Surgical complications (immediate and delayed) including: injuries to the bladder, ureter, blood vessels, nerves, small bowel and colon; febrile morbidity; intestinal obstruction; haematomas and infections
  8. Length of hospital stay
  9. Time to adjuvant chemotherapy
  10. Systemic complications
  11. Abdominal wall recurrence: laparoscopy (port sites) and laparotomy (midline incision).
  12. Quality of life

 

Search methods for identification of studies

 

Electronic searches

We conducted searches to identify all published and unpublished RCTs and NRSs that compared laparoscopy and laparotomy for stage I ovarian cancer. The search strategies identified studies in all languages and, when necessary, we translated non-English language papers so that they could be fully assessed for potential inclusion in the review.

We searched the Cochrane Gynaecological Cancer Review Group (CGCRG) Trials Register, Cochrane Central Register of Controlled Trials (CENTRAL 2007, Issue 2), MEDLINE (January 1990 to November 2007), EMBASE (1990 to November 2007), LILACS (1990 to November 2007), Biological Abstracts (1990 to November 2007) and CancerLit (1990 to November 2007). For this updated version of the review, we extended these searches to 6 December 2011. (See Appendix 1, Appendix 2, Appendix 3 and Appendix 4 for the search strategies).

 

Searching other resources

We handsearched the citation lists of relevant publications and included studies, and contacted experts in the field to identify further trials. For the original review we also handsearched the following conferences and publications: Gynecologic Oncology, International Journal of Gynaecological Cancer, British Journal of Cancer, British Cancer Research Meeting, Annual Meetings of the International Gynaecologic Cancer Society, Annual Meetings of the American Society of Gynecologic Oncologists, Annual Meetings of the European Society of Medical Oncology (ESMO), and Annual Meetings of the American Society of Clinical Oncology (ASCO).

 

Data collection and analysis

 

Selection of studies

Two review authors sifted the searches and identified potentially eligible studies. All authors assessed the methodology of these potentially eligible studies according to the specific inclusion criteria. Review authors were not blind to the authors, institutions or journals of potentially relevant studies.

 

Data extraction and management

No studies fulfilled the inclusion criteria for this review. For future versions of this review, two authors will independently extract data from included trials to a pre-designed data collection sheet that includes the following information:

  • Study methodology: description of randomisation, blinding, number of study centres, study duration, length of follow-up and number of study withdrawals.
  • Participants: number, mean age, mean risk score.
  • Intervention: type of intervention, dose and schedule.
  • Outcomes:

    • We will extract data to allow for intention-to-treat (ITT) analysis where possible.
    • For dichotomous outcomes (e.g. number of lymph nodes, complications or deaths), we will extract outcome rates to estimate a risk ratio (RR).
    • For continuous outcomes (e.g. quality of life (QoL) measures and duration of treatment) we will extract means and standard deviations (SD) to estimate a mean difference (MD).
    • For time-to-event outcomes (e.g. overall survival) we will extract the log of the hazard ratio (log(HR)) and its standard error from trial reports. If these are not reported, we will attempt to estimate the log (HR) and its standard error using Parmar's methods (Parmar 1998).

 

Assessment of risk of bias in included studies

For future versions of this review we will assess the risk of bias in included studies using The Cochrane Collaboration's tool (Higgins 2011) and the following criteria:

  1. selection bias: random sequence generation and allocation concealment;
  2. performance bias: blinding of participants and personnel (patients and treatment providers);
  3. detection bias: blinding of outcome assessment;
  4. attrition bias: incomplete outcome data;
  5. reporting bias: selective reporting of outcomes;
  6. other possible sources of bias.

 

Results

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Description of studies

 

Results of the search

The original search identified 706 citations, of which we retrieved 43 for detailed examination. We subsequently excluded 40 of these records and three NRSs (two case-control studies and one case series) were included in the original review (Ghezzi 2007; Hua 2005; Tozzi 2004; Figure 1). For this updated review, we excluded these NRSs but tabled their findings with other similar studies that were identified by the updated search (see Differences between protocol and review).

 FigureFigure 1. Study flow diagram of original search 17 May 2007

From the updated search we identified 1395 records (1140 after de-duplication), 28 of which we screened for possible relevance. Of these, 11 new studies were identified for classification (Chen 2010; Chi 2005; Colomer 2008; Ghezzi 2009; Lee 2011; Nezhat 2009; Park 2008a; Park 2008b; Park 2010; Park 2011; Wu 2010; Figure 2). Park 2008b, Park 2010 and Park 2011 are extensions of the same series.

 FigureFigure 2. Study flow diagram of updated search 30 November 2011

 

Included studies

There were no studies that met the inclusion criteria.

 

Excluded studies

Altogether we excluded 54 studies. None of these studies met the inclusion criteria in Types of studies. We have summarised the results of the relevant case series, case-control studies and retrospective cohort studies in three tables:  Table 1,  Table 2 and  Table 3, respectively. None of the comparative NRSs reported adjusting results for baseline characteristics and we considered all of them to be at a high risk of selection bias and other bias (e.g. outcome assessment bias).

 

Risk of bias in included studies

Not applicable.

 

Effects of interventions

There were no studies to include therefore no meta-analyses could be performed.  Table 2 and  Table 3 present the available data from the case-control and retrospective studies to date.

 

Discussion

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

Stage I ovarian cancer is a rare disease and the use of laparoscopy for surgical staging thereof is a relatively new field of clinical study, therefore data are scarce. Recent UK guidelines on the management of ovarian cancer do not consider laparoscopy as an approach to the surgical staging of early ovarian cancer (NICE 2011); however, the German Gynaecological Oncology Group (AGO) have cautiously included the option of this procedure in their recent guidelines, for selected patients and only when performed by expert laparoscopic oncology surgeons, pending further evidence (Mettler 2009).

 

Summary of main results

We found no randomised controlled trials (RCTs) to include in this review and from which to compare the risks and benefits of laparoscopy with the conventional open approach. Existing non-randomised evidence comparing these interventions is extremely limited and is particularly at risk of selection bias. We considered including case-control non-randomised studies (NRSs) in meta-analyses, however sample sizes were small, none of these studies reported performing statistical adjustments for baseline case mix using multivariate analyses (e.g. age, final FIGO stage, grade, tumour size, co-morbidity and adjuvant chemotherapy), the duration of follow-up varied widely, and the primary outcomes of this review (OS and PFS) were not consistently reported.

 

Overall completeness and applicability of evidence

 

Survival

According to Surveillance Epidemiology and End Results (SEER; Kosary 2007), five-year OS rates for stage Ia, Ib and Ic ovarian adenocarcinoma (excluding borderline tumours) are about 94%, 91% and 80% respectively. However, survival data relating to the surgical approach (laparoscopy versus laparotomy) in the existing literature are extremely limited: comparative studies of laparoscopy versus laparotomy for early ovarian cancer to date include three case-control studies ( Table 2; Chi 2005; Ghezzi 2007; Hua 2005) and five retrospective cohort studies ( Table 3; Lee 2011; Park 2008a; Park 2008b; Park 2010; Park 2011), three of which are expansions of the same case series (Park 2008b; Park 2010; Park 2011). Of these eight studies, six reported survival data but the length of follow-up varied widely or was not reported. Lee 2011 reported higher PFS rates in the laparoscopy group (100% for laparoscopy versus 91% for laparotomy) and did not report OS, however median follow-up was much shorter in the laparoscopy group compared with the laparotomy group (12 versus 25 months) and mean tumour size was significantly larger in the laparotomy group (P = 0.01). Park 2011 reported OS of 89% and 86% for laparoscopy and laparotomy respectively and PFS rates of 78% in each group, but did not report the duration of follow-up in each group. Ghezzi 2007 reported 100% OS in both groups, however the median duration of follow-up differed substantially between the groups (16 months in the laparoscopy group compared with 60 months in the laparotomy group).

Two studies conducted in women with early ovarian cancer (Park 2008a; Wu 2010) have reported unfavourable survival outcomes with laparoscopy. In Park 2008a (OS = 88% in the laparoscopy group versus 100% in the laparotomy group;  Table 3), one woman who was diagnosed with FIGO stage Ia grade 1 ovarian cancer was shown to have severely disseminated disease at seven months and died of the disease 15 months later; the other woman had stage Ia grade 2 ovarian cancer at laparoscopy and developed recurrence at the vaginal stump. The extent of laparoscopy surgical staging was considered sufficient in the latter case, the tumour was not ruptured and retrieval bags were used. Wu 2010 reported data from a cohort of women with stage 1 ovarian cancer treated between 1984 and 2006 and found that those in whom the initial surgical approach was laparoscopic had significantly worse PFS and OS than those who underwent laparotomy (OS hazard ratio (HR) = 3.52), however, comprehensive staging was not the purpose of the laparoscopy in most of these women, therefore these results are difficult to interpret. In general, we consider the available survival data to be of a very low quality, hence it is not possible draw any conclusions regarding the relative effect of laparoscopic surgical staging compared with laparotomy on ovarian cancer survival from the existing literature.

 

Feasibility

Measures of the technical feasibility of laparoscopy have included pelvic and para-aortic lymph node yields, the size of the omental specimen, operating times and intra-operative tumour spillage. All case-control and cohort studies identified have reported statistically similar yields of retroperitoneal lymph nodes between their laparoscopy and laparotomy groups. Only two comparative studies (Chi 2005; Park 2008b) have reported mean omental specimen volumes, which were not statistically significantly different. With regard to operating times, some studies report significantly longer times with laparoscopy (Chi 2005; Ghezzi 2007; Hua 2005; Lee 2011) whilst others have reported significantly shorter times with laparoscopy (Park 2008b; Park 2010; Park 2011). These differences probably reflect differences in surgeons' skills and laparoscopic techniques between investigator teams.

Rupture or spillage of ovarian tumours during surgery has been reported to occur more frequently with laparoscopy than laparotomy (Romagnolo 2006) and has been identified as a prognostic indicator of disease-free survival (Vergote 2001). To date, six out of eight NRSs have compared rates of tumour spillage between laparoscopy and laparotomy groups (Hua 2005;Lee 2011; Park 2008a; Park 2008b; Park 2010; Park 2011). Five of these studies reported no significant difference between the two groups, and one study (Lee 2011) reported a statistically significantly higher rate of spillage in the laparotomy group (0% versus 14.9%; P = 0.037) which also had a significantly larger mean tumour size compared with the laparoscopy group. The definitions of spillage vary and the distinction between tumour rupture and puncture is not detailed in most studies (Ghezzi 2009). To properly assess these outcomes, technique and definitions need to be clearly defined in future studies. However, these limited data suggest that laparoscopy staging of early ovarian cancer is technically feasible when performed by experienced laparoscopic gynaecology oncology surgeons.

An inherent shortcoming of laparoscopy for surgical staging is the inability to palpate lymph nodes and other peritoneal surfaces (Colomer 2008; Park 2008a), however Chi 2010 argues that intra-operative direct visualisation and evaluation of nodes by palpation is inherently subjective. In a recent prospective study, of 111 women with apparent early ovarian cancer who underwent comprehensive staging by laparotomy that included retroperitoneal lymph node dissection (RLND), retroperitoneal nodal metastases were present in 13.5% of the women (Ditto 2012), which suggests that without RLND many women would be under-staged. However, systematic RLND may be associated with significant morbidity and is not a routine part of staging for early ovarian cancer in the UK, where clinical guidelines currently recommend retroperitoneal lymph node assessment with sampling of suspicious nodes (NICE 2011). Therefore, where RLND is not routine, lymph node palpation may play a crucial role in the decision-making process with regard to sampling. Another technically difficult part of the surgical staging procedure is the examination of the diaphragmatic peritoneum behind the liver and spleen and the dome of the liver (Park 2008a); this may be more difficult with laparoscopy, although it has been argued that isolated metastases to these areas are rare (Ghezzi 2009).

 

Safety

Surgical staging for ovarian cancer is a radical procedure that may be associated with severe intra-operative vascular, nerve, lymphatic, bowel and urinary tract complications. Common postoperative complications include wound infection, ileus, febrile morbidity and lymphoceles (Ghezzi 2007; Lee 2011; Park 2008a; Park 2008b). Three comparative studies in early ovarian cancer have reported significantly fewer postoperative complications with laparoscopy compared with laparotomy (Hua 2005; Lee 2011; Park 2011). The following complications have been reported in the laparoscopy participants of studies in early ovarian cancer: umbilical hernias (Lee 2011), retroperitoneal haematoma (Ghezzi 2007), vascular injury (Colomer 2008; Ghezzi 2007; Park 2008b), lymphoceles (Lee 2011; Nezhat 2009), obturator nerve damage (Hua 2005), bowel injury or obstruction (Nezhat 2009; Park 2008a) and ureter injury (Park 2008b). Estimated blood loss (EBL) in all case-control ( Table 2) and comparative cohort studies ( Table 3) has been statistically significantly less than in the laparoscopy groups compared with laparotomy groups, with the exception of one study (Ghezzi 2007). In these studies, rates of blood transfusion in laparoscopy groups ranged from 0% to 15%, whereas transfusions were necessary in up to 30% (Park 2010) of women who underwent laparotomy.

There have been several reports of the occurrence of abdominal wall metastases following laparoscopy for ovarian cancer (Childers 1994; Gleeson 1993; Leminen 1999). However, in the studies of laparoscopy in stage I ovarian cancer that have reported this outcome, no port-site metastases had occurred by the time of reporting in Chi 2005 (20 women), Park 2008a (17 women), Park 2008b (19 women), Nezhat 2009 (36 women) and Lee 2011 (26 women). Port-site metastases may be technique-related and limited mostly to patients with advanced disease (Chi 2005; Nezhat 2009). In a study of laparoscopic cytoreductive surgery for advanced ovarian cancer and in which no port-site metastases occurred, the authors attributed their results to a surgical technique that employed endoscopic bags to retrieve intact specimens and a layered closure of the trocar site (Nezhat 2010). Lee 2011 and Chi 2005 have also reported employing this technique to prevent port-site metastases.

 

Other outcomes

Lee 2011 evaluated the relative cost of laparoscopy compared with open surgery in women with early ovarian cancer and found that laparoscopy resulted in higher costs due to the cost of disposable instrumentation and direct material/operating room costs, but the cost of hospital stay was higher in the laparotomy group because the stay was longer. Where bed costs are higher, this difference in cost might be eliminated, however the median lengths of hospital stay in the laparotomy groups in most of the studies reporting this outcome seem excessive with a range of up to 14.5 days ( Table 2;  Table 3). Literature on the quality of life for women undergoing laparoscopy compared with laparotomy is scant, however Lee 2011 reported significantly lower postoperative pain scores in the laparoscopy group.

 

Agreements and disagreements with other studies or reviews

A meta-analysis of eight RCTs comparing laparoscopic surgical staging with laparotomy for endometrial cancer has shown the laparoscopic approach to be safe, with statistically significantly fewer postoperative complications than laparotomy, and similar rates of intra-operative complications (Zullo 2012). It is possible that similar conclusions may, in time, be drawn about laparoscopy and laparotomy for stage I ovarian cancer, however the evidence for this is not currently in the literature.

 

Authors' conclusions

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

 

Implications for practice

Due to technological advancements in instrumentation and an increase in laparoscopic surgical expertise, the role of laparoscopy in gynaecological cancers is expanding, however there is still wide regional variation in the laparoscopic skills and competence of gynaecological-oncology surgeons. We did not find any good evidence to recommend laparoscopy for the routine management of women with stage I ovarian cancer.

 
Implications for research

Survival data for patients with gynaecological malignancies managed by laparoscopy are still lacking. A major barrier to conducting randomised controlled trials (RCTs) in early ovarian cancer is the anticipated difficulty in recruiting sufficient numbers of participants (Ghezzi 2009). Other difficulties include standardising the quality of the surgery and the skill of the surgeons. Subsequent results from such trials may only be applicable to expert laparoscopic oncology surgeons. However, we understand, from a personal communication, that the Korean Gynecologic Oncology Group (KGOG) is currently developing a protocol for a RCT comparing laparoscopy with laparotomy for early ovarian cancer. Two recently reported Korean cohort studies (Lee 2011; Park 2011) recruited 325 women between them within the same six-year period (2004 to 2010), suggesting that a multicentre RCT is feasible. Participating institutions should be subgrouped according to whether retroperitoneal lymph node dissection or lymph node assessment with sampling is performed routinely. Outcomes of RCTs should include overall and progression-free survival, complications (intra-operative and postoperative), the use of adjuvant chemotherapy, patient satisfaction, quality of life and costs. It would be helpful if costs are reported separately for the preoperative, intraoperative and postoperative periods.

 

Acknowledgements

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

We would like to thank Jo Morrison, Gail Quinn, Clare Jess and Tracey Bishop of the Cochrane Gynaecological Cancer Review Group team that is based at the Royal United Hospital, Bath, UK for their help, advice and support throughout the review process; Jane Hayes for performing the updated search; and the library staff at the Royal United Hospital, Bath, UK, who obtained many articles for us. We would also like to thank Lidia Medieros for acting as the Contact Author on the original review.

 

Data and analyses

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

This review has no analyses.

 

Appendices

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Appendix 1. CENTRAL search strategy

#1  MeSH descriptor Ovarian Neoplasms explode all trees
#2  ovar* near/5 (cancer* or tumor* or tumour* or neoplas* or carcinoma* or malignan* or adenocarcinoma*)
#3  (#1 OR #2)
#4  MeSH descriptor Laparoscopy explode all trees
#5  laparoscop* or celioscop* or peritoneoscop* or (endoscop* near/5 abdom*)
#6  MeSH descriptor Laparotomy, this term only
#7  laparotom* or (abdom* near/5 (surg* or incision))
#8  (#4 OR #5 OR #6 OR #7)
#9  (#3 AND #8)

 

Appendix 2. MEDLINE search strategy

1   exp Ovarian Neoplasms/
2   (ovar* adj5 (cancer* or tumor* or tumour* or neoplas* or carcinoma* or malignan* or adenocarcinoma*)).mp.
3   1 or 2
4   exp laparoscopy/
5   (laparoscop* or celioscop* or peritoneoscop* or (endoscop* adj5 abdom*)).mp.
6   Laparotomy/
7   (laparotom* or (abdom* adj5 (surg* or incision))).mp.
8   4 or 5 or 6 or 7
9   3 and 8
10 randomized controlled trial.pt.
11 controlled clinical trial.pt.
12 randomized.ab.
13 placebo.ab.
14 clinical trials as topic.sh.
15 randomly.ab.
16 trial.ti.
17 exp cohort studies/
18 exp case-control studies/
19 comparative study/
20 (cohort* or prospective* or retrospective* or control* or longitudinal or follow-up).mp.
21 10 or 11 or 12 or 13 or 14 or 15 or 16 or 17 or 18 or 19 or 20
22 9 and 21

key: [mp = protocol supplementary concept, rare disease supplementary concept, title, original title, abstract, name of substance word, subject heading word, unique identifier] 

 

Appendix 3. EMBASE search strategy

1   exp ovary tumor/
2   (ovar* adj3 (cancer* or tumor* or tumour* or neoplas* or carcinoma* or malignan* or adenocarcinoma*)).ti,ab.
3   1 or 2
4   laparoscopy/
5   (laparoscop* or celioscop* or peritoneoscop* or (endoscop* adj3 abdom*)).ti,ab.
6   laparotomy/
7   (laparotom* or (abdom* adj3 (surg* or incision))).ti,ab.
8   4 or 5 or 6 or 7
9   exp controlled clinical trial/
10 cohort analysis/
11 exp case control study/
12 exp comparative study/
13 (randomized or randomly or trial* or cohort* or prospective* or retrospective* or control* or longitudinal or follow-up).ti,ab.
14 9 or 10 or 11 or 12 or 13
15 3 and 8 and 14

key: [mp = title, abstract, subject headings, heading word, drug trade name, original title, device manufacturer, drug manufacturer, device trade name, keyword]

 

Appendix 4. LILACS search strategy

(MH:"ovarian neoplasms" or (ovar$ and (cancer$ or tumor$ or tumour$ or tumour$ or neoplas$ or carcinoma$ or malignan$ or adenocarcinom$))) and (MH:"laparoscopy" or laparoscop$ or MH:"laparotomy" or laparotom$)

 

What's new

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

Last assessed as up-to-date: 23 November 2012.


DateEventDescription

27 March 2014AmendedContact details updated.



 

History

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

Protocol first published: Issue 3, 2005
Review first published: Issue 4, 2008


DateEventDescription

20 December 2012AmendedAuthorship order amended

12 September 2012New citation required but conclusions have not changedEleven newly identified studies excluded, no studies included. Conclusions unchanged.

30 November 2011New search has been performedSearch updated.

9 November 2010AmendedAuthor contact details amended.

14 May 2008AmendedConverted to new review format.



 

Contributions of authors

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

Lidia Medieros (LM), Daniela Rosa (DR), Mary Bozetti (MB), Maria Ines Rosa (MR), Alice Zelmanowicz (AZ) and Airton Stein (AS) contributed to the writing of the protocol and the original review. LM, DR, MR, MB and Maria Edelweiss sifted the searches, selected studies and extracted data for the original review (which included NRSs). Anaelena Ethur (AE) and Roselaine Zanini (RZ) contributed to the protocol and methods section. Tess Lawrie (TL) sifted the updated search and wrote the first draft of the updated review. All authors approved the final version.

 

Declarations of interest

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

None.

 

Sources of support

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Internal sources

  • No sources of support supplied

 

External sources

  • National Institute for Health Research (NIHR), UK.
    This review received methodological, statistical and editorial support as part of the 10/4001/12 NIHR Cochrane Programme Grant Scheme: Optimising care, diagnosis and treatment pathways to ensure cost effectiveness and best practice in gynaecological cancer: improving evidence for the NHS.

 

Differences between protocol and review

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

For the original review (Medeiros 2008), we included NRSs and evaluated the quality of three studies (Ghezzi 2007; Hua 2005; Tozzi 2004) according to the STROBE and NOS tools. For the updated review, these studies were excluded, but we tabulated and discussed the data with other NRSs.

* Indicates the major publication for the study

References

References to studies excluded from this review

  1. Top of page
  2. Abstract
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Characteristics of studies
  19. References to studies excluded from this review
  20. Additional references
  21. References to other published versions of this review
Amara 1996 {published data only}
Berman 2003 {published data only}
Bristow 2000 {published data only}
Canis 1994 {published data only}
  • 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. Obstetrics and Gynecology 1994;83(5):707-12.
Canis 1997 {published data only}
Canis 2000 {published data only}
  • Canis M, Mage G, Wattiez A, Pouly JL, Sonteara SS, Bruhat MA. A simple management program for adnexal masses. Gynecologic Oncology 2000;7:113-8.
Chapron 1998 {published data only}
Chen 2010 {published data only}
  • Chen Y. Laparoscopic comprehensive staging for apparent early invasive epithelial ovarian cancers: surgical and outcome. Journal of Minimally Invasive Gynecology; 39th Global Congress of Minimally Invasive Gynecology, Las Vegas, NV United States. 2010; Vol. 17(6):S44.
Chi 2005 {published data only}
  • Chi D, Abu-Rustum NR, Sonoda Y, Ivy J, Rhee E, Moore K, et al. The safety and efficacy of laparoscopic surgical staging of apparent stage I ovarian and fallopian tube cancers. American Journal of Obstetrics and Gynecology 2005;192:1614-9.
Childers 1995 {published data only}
Childers 1996 {published data only}
Colomer 2008 {published data only}
  • Colomer AT, Jimenez AM, Bover Barcelo MI. Laparoscopic treatment and staging of early ovarian cancer. Journal of Minimally Invasive Gynecology 2008;15(4):414-9.
Darai1998 {published data only}
  • Darai E, Teboul J, Fauconnier A, Scoazec JY, Benifla JL, Madelenat P. Management and outcome of borderline ovarian tumors incidentally discovered at or after laparoscopy. Acta Obstetricia et Gynecologica Scandinavica 1998;77:451-7.
de Poncheville 2001 {published data only}
  • Poncheville L, Perrrotin F, Lefrancq T, Lansac J, Body G. Does paraaortic lymphadenectomy have a benefit in the treatment of ovarian cancer that is apparently confined to the ovaries?. European Journal of Cancer 2001;37:210-5.
Dottino 1999 {published data only}
Ghezzi 2007 {published data only}
  • Ghezzi F, Cromi A, Uccella S, Bergamini V, Tomera S, Franchi M, et al. Laparoscopy versus laparotomy for the surgical management of apparent early stage ovarian cancer. Gynecologic Oncology 2007;105(2):409-13.
Ghezzi 2009 {published data only}
  • Ghezzi F, Cromi A, Siesto G, Serati M, Zaffaroni E, Bolis P. Laparoscopy staging of early ovarian cancer. International Journal of Gynecological Cancer 2009;19:S7-13.
Goff 2006 {published data only}
Hua 2005 {published data only}
  • Hua KQ, Jin FM, Xu F, Zhu ZL, Lin JF, Feng YJ. Evaluations of laparoscopic surgery in the early stage malignant tumor of ovary with lower risk. Zhonghua Yi Xue Za Zhi 2005;85(3):169-72.
Kadar 1995 {published data only}
  • Kadar N. Laparoscopic surgery for gynaecological malignancies in women aged 65 years or more. Gynaecological Endoscopy 1995;4:173-6.
Klindermann 1995 {published data only}
  • Klindermann G, Maassen V, Kuhn W. Laparoscopic preliminary surgery of ovarian malignancies. Experiences from 127 German gynecologic clinics. Gerburtshilfe Frauenheikd 1995;55(12):687-94.
Leblanc 2004 {published data only}
  • Leblanc E, Querleu D, Narducci F, Occelli B, Papageorgiou T, Sonada Y. Laparoscopic restaging of early stage invasive adnexal tumors: a 10 year experience. Gynecologic Oncology 2004;94(3):624-9.
Leblanc 2006 {published data only}
Lécuru 2004 {published data only}
  • Lécuru F, Desfeux P, Camatte S, Bissery A, Robin F, Blanc B. Stage I ovarian cancer: comparison of laparoscopy and laparotomy on staging and survival. European Journal of Gynaecological Oncology 2004;25:571-6.
Lee 2011 {published data only}
  • Lee M, Kim SW, Lee SH, Yim GW, Kim JH, Kim JW, et al. Comparisons of surgical outcomes, complications, and costs between laparotomy and laparoscopy in early-stage ovarian cancer. International Journal of Gynecological Cancer 2011;21(2):251-6.
Maiman 1991 {published data only}
Malik 1998 {published data only}
Maneo 2004 {published data only}
Manolitsas 2001 {published data only}
Mehra 2004 {published data only}
  • Mehra G, Weekes ARL, Jacobs IJ, Visvanathan D, Menon U, Jeyarajah AR. Laparoscopy extraperitoneal paraaortic lymphadenectomy a study of its applications in gynecological malignancies. Gynecologic Oncology 2004;93:189-93.
Nezhat 1992 {published data only}
  • Nezhat F, Nezhat C, Welander CE, Benigno B. Four ovarian cancers diagnosed during laparoscopic management of 1011 women with adnexal masses. American Journal of Obstetrics and Gynecology 1992;167(3):790-6.
Nezhat 2009 {published data only}
  • Nezhat FR, Ezzati M, Chuang L, Shamshirsaz AA, RahamanJ, Gretz H. Laparoscopic management of early ovarian and fallopian tube cancers: surgical and survival outcome. American Journal of Obstetrics and Gynecology 2009;200(83):e1-6.
Nezhat 2010 {published data only}
  • Nezhat FR, DeNoble SM, Liu CS, Cho JE, Brown DN, Chuang L, et al. The safety and efficacy of laparoscopic surgical staging and debulking of apparent advanced stage ovarian, fallopian tube, and primary peritoneal cancers. Journal of the Society of Laparoscopic Surgeons 2010;14:155-68.
Park 2008a {published data only}
Park 2008b {published data only}
  • Park J-Y, Kim D-Y, Suh D-S, Kim J-H, Kim Y-M, Kim Y-T, et al. Comparison of laparoscopy and laparotomy in surgical staging of early-stage ovarian and fallopian tubal cancer. Annals of Surgical Oncology 2008;15(7):2012-9.
Park 2010 {published data only}
  • Park J-Y, Kim J-J, Kim D-Y, Kim J-H, Kim Y-M, Kim Y-T, et al. Laparoscopic management of early stage epithelial ovarian cancer. Journal of Minimally Invasive Gynecology: 39th Global Congress of Minimally Invasive Gynecology, AAGL 2010 Las Vegas, NV, United States. 2010; Vol. 17(6):S90.
Park 2011 {published data only}
  • Park J, Kim D, Kim J, Kim Y, Kim Y, Nam J. Laparoscopic versus laparotomic surgical staging for early-stage epithelial ovarian cancer. Gynecologic Oncology; 42nd Annual Meeting of the Society of Gynecologic Oncologists, Orlando, FL, United States. 2011; Vol. 120 (Suppl 1):S72.
Parker 1990 {published data only}
  • Parker WP, Berek JS. Management of selected cystic adnexal masses in postmenopausal women by operative laparoscopy. American Journal of Obstetrics and Gynecology 1990;63(5):1574-7.
Pomel 1995 {published data only}
Querleu 2003 {published data only}
  • Querleu D, Papageorggiou TH, Lambaudie E, Sonoda Y, Narducci F, LeBlanc E. Laparoscopic restaging of borderline ovarian tumours - results of 30 cases initially presumed as stage IA borderline ovarian tumours. British Journal of Obstetrics and Gynaecology 2003;110:201-4.
Querleu 2006a {published data only}
Querleu 2006b {published data only}
  • Querleu D, Leblanc E, Cartron G, Narducci F, Ferron G, Martel P. Audit of preoperative and early complications of laparoscopic lymph node dissection in 1000 gynecologic cancer patients. American Journal of Obstetrics and Gynecology 2006;195(5):1287-92.
Reich 1990 {published data only}
Romagnolo 2006 {published data only}
Rouzier 2005 {published data only}
  • Rouzier R, Pomel C. Update on the role of laparoscopy in treatment of gynecological malignancy. Current Opinion in Obstetrics and Gynecology 2005;17:77-82.
Spirtos 2005 {published data only}
  • Spirtos MN, Eisekop SM, Boike G, Schlaerth HB, Cappellari JO. Laparoscopic staging in patients with incompletely staged cancers of the uterus, ovarian, fallopian tube, and primary peritoneum: a Gynecologic Oncology Group (GOG) study. American Journal of Obstetrics and Gynecology 2005;193:1645-9.
Tozzi 2004 {published data only}
Tozzi 2005 {published data only}
Tropé 2006 {published data only}
Vaisbuch 2005 {published data only}
  • Vaisbuch E, Dgani R, Ben-Arie A, Hagay Z. The role of laparoscopy in ovarian tumors of low malignant potential and early-stage ovarian cancer. Obstetrical and Gynecological Survey 2005;60(5):326-30.
Vergote 2003 {published data only}
  • Vergote I, Trimbos BJ. Treatment of patients with early epithelial ovarian cancer. Current Opinion in Oncology 2003;15:452-5.
Vinatier 1996 {published data only}
  • Vinatier D, Cosson DM, Querleu D. Laparoscopy in gynaecological cancer. Surgical Oncology 1996;5:211-20.
Volz 1997 {published data only}
  • Voltz J, Köster S, Schaeff B. Laparoscopic management of gynaecological malignancies: time to hesitate!. Gynaecology Endoscopy 1997;6(3):145-6.
    Direct Link:
Wenzl 1996 {published data only}
Wu 2010 {published data only}
  • Wu Ti, Lee C-L, Liao P-J, Huang K-G, Chang T-C, Chou H-H, et al. Survival impact of initial surgical approach in stage I ovarian cancer. Chang Keng i Hsueh: Chang Gung Medical Journal 2010;33:558-67.

Additional references

  1. Top of page
  2. Abstract
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Characteristics of studies
  19. References to studies excluded from this review
  20. Additional references
  21. References to other published versions of this review
Benedet 2000
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Bergstrom 2008
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Chi 2010
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Gleeson 1993
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