Laparoscopic, robotic and open method of radical hysterectomy for cervical cancer: A systematic review

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1 Review Article, robotic and open method of radical hysterectomy for cervical cancer: A systematic review Puliyath Geetha, M Krishnan Nair 1 Department of Obstetrics and Gynaecology, SUT Academy of Medical Sciences, Post Vencode, Vattappara, Trivandrum, 1 Department of Oncology, SUT Royal Hospital, Pattom Palace, Pattom, Trivandrum, Kerala, India Address for correspondence: Dr. Puliyath Geetha, Department of Obstetrics and Gynaecology, SUT Academy of Medical Sciences, Post Vencode, Vattappara, Trivandrum , Kerala, India. pgeetha98@yahoo.co.in Abstract BACKGROUND: Over the last two decades, numerous studies have indicated the feasibility of minimally invasive surgery for early cervical cancer without compromising the oncological outcome. OBJECTIVE: Systematic literature review and meta analysis aimed at evaluating the outcome of laparoscopic and robotic radical hysterectomy (L and R) and comparing the results with abdominal radical hysterectomy (A). SEARCH STRATEGY: Medline, PubMed, Embase, Cochrane library and Reference lists were searched for articles published until January 31 st 2011, using the terms radical hysterectomy, laparoscopic radical hysterectomy, robotic radical hysterectomy, surgical treatment of cervical cancer and complications of radical hysterectomy. SELECTION CRITERIA: Studies that reported outcome measures of radical hysterectomy by open method, laparoscopic and robotic methods were selected. Data collection and analysis: Two independent reviewers selected studies, abstracted and tabulated the data and pooled estimates were obtained on the surgical and oncological outcomes. RESULTS: Mean sample size, age and body mass index across the three types of studies were similar. Mean operation time across the three types of studies was comparable. Mean blood loss and transfusion rate are significantly higher in A compared to both L and R. Duration of stay in hospital for R was significantly less than the other two methods. The mean number of lymph nodes obtained, nodal metastasis and positive margins across the three types of studies were Quick Response Code: Access this article online Website: DOI: / similar. Post operative infectious morbidity was significantly higher among patients who underwent A compared to the other two methods and a higher rate of cystotomy in L. CONCLUSIONS: Minimally invasive surgery especially robotic radical hysterectomy may be a better and safe option for surgical treatment of cervical cancer. The laparoscopic method is not free from complications. However, experience of surgeon may reduce the complications rate. Key words: Cervical cancer, hysterectomy, minimally invasive radical hysterectomy INTRODUCTION Open radical hysterectomy and pelvic lymph node dissection has been considered as the standard surgical treatment for early stage cervical cancer for more than 100 years. [1] After the first total laparoscopic radical hysterectomy with pelvic and paraaortic lymphadenectomy which was performed by Nezhat in June of 1989, [2] in the last two decades minimally invasive endoscopic surgery has become an acceptable alternative for open method. In recent years, robotic surgery became popular and the first robotic radical hysterectomy with lymphadenectomy performed in 2006 by Sert and Abeler. [3] The benefits of minimal invasive surgery are less wound related problems, increased patients comfort, better visualization, less blood loss, short recovery time, decreased analgesic requirements, shorter hospital stay and early recovery. [4] The use of robotic surgery has been said to be associated with faster performance times, increased accuracy, enhanced dexterity, faster suturing, and reduced number of errors when compared to conventional laparoscopic surgery. [5,6] However, debate exists on two points. These are the oncological outcome and the safety of the procedures. So far, there are no prospective randomised controlled studies available in these aspects. Recently one prospective randomised controlled on laparoscopic vs abdominal radical hysterectomy in patients with early cervical cancer was conducted by U.S. National Institutes Journal of Minimal Access Surgery July-September 2012 Volume 8 Issue 3 67

2 of Health, (clinical trials. govstudy NCT ) and has been completed. However, its results are not available. We performed a systematic review and meta-analysis on outcomes of laparoscopic, robotic and open abdominal methods of radical hysterectomy and compared the data to aggregate the current best evidence on the subject. MATERIALS AND METHODS Sources A systematic literature search was performed independently by the two authors in January 2011 using online databases for medical literature from 1980 onwards [MEDLINE, EMBASE, BioMed Central, Cochrane Database of Systematic Reviews (CDSR)]. In order to maximize the probability of identifying potentially relevant articles, broad search terms were used (cervical cancers, gynaecological malignancies, minimally invasive surgeries). Additional searches were made by screening reference lists from articles of interest, as well as citations of articles of interest. Furthermore, attempts were made to identify relevant unpublished studies by searching the Cochrane Register of Controlled Trials (CENTRAL), ClinicalTrials.gov, International Standard Randomised Controlled Trial Number Register (ISRCTN) and the International Clinical Trials Registry Platform (ICTRP). Study selection and statistical analysis Articles in any language were eligible for inclusion in the meta-analysis if they reported one or more oncological and surgical outcome measures for treatment of early cervical cancer and English translation was available. There were 1560 articles identified by search. About 320 articles were potentially relevant. Others were deemed irrelevant based on title and or abstract. There were 21 studies available for laparoscopic radical hysterectomy, 12 for robotic radical hysterectomy and 14 for open radical hysterectomy. Others were excluded due to various reasons. Some full articles, reviews and meta-analyses were non-english. Studies which included advanced stage of cervical cancers, those treated with chemotherapy prior to surgery, original data was not presented, and articles in which outcome of interest was not reported. All studies were observational cohort studies. No RCTs were available.the article was prepared following the guidelines proposed by the Meta analysis of Observational Studies in Epidemiology (MOOSE) Statement. [7] We used published data from literature and thus the present was exempted from Local Research and Ethics Committee approval. Details such as sample size, mean age in years, body mass index, mean operating time, mean blood loss, oncological data like mean lymph node yield, nodal metastasis, recurrence, and intra operative and postoperative complications were collected from studies published on radical hysterectomy. Distributions of these variables in studies using abdominal, laparoscopic and robotic radical hysterectomy are presented in Tables. Mean of these variables across the three types of radical hysterectomy was compared using analysis of variance (ANOVA). Post hoc comparison of means was carried out using Bonferroni correction for multiple comparisons. RESULTS There were 21 studies (1339 patients) of laparoscopic radical hysterectomy, 14 open radical hysterectomy (1552 patients) and 12 robotic radical hysterectomy (327 patients) [Tables 1-3]. Table 1: radical hysterectomy studies Author Place of Nature of Study period Furmovits M USA Retrospective Jan 2004 to Dec 2006 Li G.Yan X China Prospective Aug 1998 to Dec 2005 Zakashansky USA Prospective 2000 to 2006 F R Nezhat USA Prospective Aug 2000 to Jun 2006 AbuRustum NR USA Retrospective Dec 2000 to Dec 2002 Ramirez PT USA Retrospective May 2004 to Aug 2005 Chen Y, Xu H China Prospective Feb 2001 to Jun 2007 C Pomel France Retrospective 1993 to 2001 F Nezhat USA Retrospective Jan 2004 to Feb 2005 J F Magrina USA Prospective Apr 2003 to M B Serta Norway Prospective Apr 2004 to Aug 2005 N M Spirtos USA Prospective Jul 1994 to Dec 1996 Putambekar SP India Retrospective Sept 2002 to Dec 2006 Protopapas USA Prospective Aug 2000 to June 2006 Lee EJ Korea Retrospective Jan 1994 to Dec 2001 Yan X.Li G China Retrospective Aug 1998 to Mar 2010 No. of patients Naik R UK Prospective 20 months 7 Colombo PE France Prospective 2000 to 2008 Estape R USA Prospective July 2004 to July 2006 Javier F USA Prospective Apr 2003 to Ling B China Retrospective Feb 2003 to July Journal of Minimal Access Surgery July-September 2012 Volume 8 Issue 3

3 Table 2: Open radical hysterectomy studies Author Furmovits NI Li G, Yan X Zakashansky Abu-Rustum N R Place of Nature of Study period USA Retrospective Jan 2004 to Dec 2006 China Prospective Aug 1998 to Dec 2005 No. of patients Among these, 29 (60%) were prospective studies, and 40% were retrospective studies. Mean sample size across the three types of studies were similar. ANOVA F (2, 44) = 1.02; P = Mean age of patients and mean body mass index across the three types of studies were similar. (ANOVA F (2, 39) = 1.21; P = 0.9 and ANOVA F (2, 20) = 1.20; P = respectively). Mean operation time across the three types of studies was similar. ANOVA F (2, 44) = 1.1; P = 0.3. Though laparoscopic and robotic appear to take more time compared to open, the difference was not big enough to be statistically significant. Mean blood loss (ml) for the three types of studies was different. ANOVA F (2, 44) = 21.6; P < 01. Mean blood loss was significantly higher in open operation compared to both laparoscopic and robotic. The difference in blood loss between laparoscopic and robotic was not statistically significant. Both laparoscopic and robotic had significantly lower proportion of patients with blood transfusion compared to open method. (ANOVA F (2, 24) = 20.5; P<01). Although the robotic appears to require less blood transfusion, the difference between transfusion percentages between laparoscopic and robotic is not big enough to be statistically significant. Duration of stay 54 USA Prospective 2000 to USA Retrospective 1990 and E N1 Ko USA Retrospective Aug 2004 to Aug 2007 Naik R UK Prospective 20 months 1 Colombo PE France Prospective 2000 to Estape R USA Prospective May 2002 to 14 July 2006 J F Magrina USA Prospective Apr 2003 to M B Serta Protopapas Norway Prospective Mar 2000 to Mar 2004 USA Prospective Aug 2000 to Jun 2006 Lee EJ Korea Retrospective Jan 1994 to Dec 2001 H W RSchreuder E Hewy Netherlands Retrospective July 2004 to Jul 2006 Florida Prospective Jul 1965 to Jun Table 3: Robotic radical hysterectomy studies Author Farr R. Nezhat Place of Nature of Study period year USA Prospective Apr 2006 to Jan 2008 Kim YT KOREA Retrospective Jun 2006 to May 2007 Ko EM USA Retrospective Aug 2006 to Jun 2007 J F. Magrina USA Prospective Apr 2003 to M. BSerta Norway Prospective Nov 2005 to Nov 2009 Lowe MP USA Retrospective Apr 2003 to Aug 2008 H W RSchreuder Vasilescu C Netherlands Retrospective July 2004 to July 2008 No. of patients in hospital for robotic was significantly less than that of open (ANOVA F (2, 42) = 6.44; P = 04). All the other pair-wise differences were not big enough to be statistically significant. The linear trend also is statistically significant, F (1, 42) = 12.86; P<.001 [Table 4]. Regarding oncological outcome, mean nodal metastasis across the three types of studies was similar. ANOVA F (2, 32) = 2.85; P = 73. Mean positive margin across the three types of studies was similar. ANOVA F (2, 34) = 1.10; P =.345. Positive margin was zero in all except one pertaining to robotic. Mean number of lymph nodes obtained across the three types of studies was similar. ANOVA F (2, 40) = 1.98; P = [Table 5]. Mean percentage of patients with infectious morbidity for the three types of studies was also different. ANOVA F (2, 36) = 6.24; P = 05. Post-operative infectious morbidity was significantly higher among patients who underwent open compared to the other two methods. The difference in infectious morbidity between laparoscopy and robotic was well within chance fluctuations. Mean percentage of patients with non-infectious morbidity for the three types of studies was similar. ANOVA F (2, 37) = 1.80; 13 1() Romania Prospective Es tape R USA Prospective Aug 2006 to Apr 2008 Persson J Sweden Prospective Dec 2005 to Sept 2008 Oleszczuk A Magrina JF Germany Prospective Nov 2007 to May 2008 USA Prospective Apr 2003 to Journal of Minimal Access Surgery July-September 2012 Volume 8 Issue 3 69

4 Table 4: Descriptive statistics for mean operating time Type of Median Maximum Mean Std. Open Robotic Total Descriptive statistics for mean duration of hospital stay Type of Median Maximum Mean Std. Open Robotic Total Descriptive statistics of mean blood loss Type of Median Maximum Mean Std. Open Robotic Total Descriptive statistics of percentage of patients who required blood transfusion Type of Median Maximum Mean Std. Open Robotic Total : Radical hysterectomy P = Not even a single case of bowel injury was reported among patients who underwent robotic. Bowel injury was reported in 3/13 open and 5/19 laparoscopic studies. Mean number of patients with ureteric injury for the three types of studies was similar. ANOVA F (2, 39) = 1.21; P = 0.9. Ureteric injury was reported in 7/13 (53.8%), 6/19 (31.6%) and 2/10 (20%) of A, L and R studies, respectively. Mean number of cystotomy for the three types of studies was different. ANOVA F (2, 39) = 3.62; P = 36. The difference between mean cystotomy between A and L was statistically significant [Table 6]. Cystotomy was reported in 16/19(84.21%) studies in L, while it is 6/13(46.15%) in A and 4/10(40%) in R. Vessel injury was reported in 6/19(31.57%), 5/13(38.46%) and 0/10 (0%) studies in L, A and R respectively. Conversion to laparotomy was reported in 9/20 studies of laparoscopic, while the same was reported in one out of 10 reports of robotic. Table 5: Descriptive statistics for nodal metastasis Type of Recurrence percentage for the three types of studies was similar. ANOVA F (2, 34) = 0.58; P = Follow-up period for the three types of studies was similar. ANOVA F (2, 38) = 2.13;.133 [Table 7]. Though the follow-up period for open was relatively high, the ANOVA resulted in non-significant result, probably due to small sample size and relatively higher standard for the open group. DISCUSSION Median Maximum Mean Std. Deviation Open Robotic Total Descriptive statistics for positive margin Type of Median Maximum Mean Std. Deviation Open Robotic The current evidence shows that minimally invasive surgery is associated with less morbidity compared with open surgery and can be considered as an alternate option for surgical management of cervical cancer without compromising the oncologic outcome. There are several studies in literature, which compared laparoscopic or robotic surgeries with open method. In majority of the studies, the operating time for laparoscopy was higher compared with open method. [8-17] One pilot by Ko EM, Muto MG, comparing robotic and open radical hysterectomy showed significantly higher mean operative time for robotic radical hysterectomy than open radical hysterectomy (4:50 vs 3:39 h, P=002). [18] Study by Lee, Kang,, showed that there is no difference in operating time for both abdominal and laparoscopic method. [19] Two other studies also reported no difference in operating time for open, robotic and laparoscopic Total Descriptive statistics for mean number of lymph nodes obtained Type of Median Maximum Mean Std. Deviation Open Robotic Total : Radical hysterectomy 70 Journal of Minimal Access Surgery July-September 2012 Volume 8 Issue 3

5 Table 6: Descriptive statistics for post-operative infectious morbidity Type of Median Maximum Mean Std.Deviation Open Robotic Total Descriptive statistics for post-operative non-infectious morbidity Type of Median Maximum Mean Std. Open Robotic Total Descriptive statistics for Cystotomy Type of Median Maximum Mean Std. Open Robotic Total : Radical hysterectomy methods. [20,21] Pooled data in this meta analysis suggest that there is no statistically significant difference in mean operating time between open, robotic and laparoscopic methods. In all comparative studies, laparoscopic and robotic methods were associated with shorter hospital stay when compared to open method. Mean blood loss and transfusion rates were more for open method. In a comparative between laparoscopic and robotic radical hysterectomy, Farr R. Nezhat, MD, M. Shoma Datta showed that there is no difference between operating time, hospital stay, mean pelvic lymph node yield or intraoperative or postoperative complications between robotic and laparoscopic method. [21] Our meta analysis also showed similar results. Infectious morbidity and blood loss are more for open method compared to other two. The number of cystotomies and vessel injuries are slightly higher for laparoscopic method compared to open and robotic methods. Another which compared robotic with laparoscopic and open methods by M. Bilal Serta, and Vera Abeler showed the mean operating times (skin-to-skin) for patients undergoing robot-assisted laparoscopic radical hysterectomy (RAL), total laparoscopic radical hysterectomy (TL) or abdominal radical hysterectomy (A) were 263 ± 70, 364 ± 57 and 163 ± 26 min respectively. Patients receiving laparotomy had shortest operative time, followed by those undergoing RAL Table 7: Descriptive statistics for recurrence percentage MLIIID and then laparoscopy (P<001 for both). [15] Estimated blood loss was significantly reduced in robot-assisted surgeries compared to surgeries involving laparoscopy and laparotomy (82 ± 74 ml vs. 164 ± 131 ml (P<001) and 595 ± 284 ml (P = 23), respectively. [15] Schreuder suggested a relatively short learning curve for robotic procedures (a learning curve of 14 cases reduced the team s total theatre time by 48%). [22] Other studies also showed advantages of robotic surgery in terms of acceptable blood loss, operating time, parametrial margins, a nodal yield. [20,23,24] However, the cost of the DaVinci robotic surgical system is a limiting factor for the development of robotic surgery. The intraoperative costs of these operations may be higher, but indirect costs in terms of reduced hospital stay and reduced complications should be taken into account. [25] LIMITATIONS OF THE STUDY Median Maximum Mean Std. Deviation Open Robotic Total Descriptive statistics for follow-up in months Type of Median Maximum Mean Std. Open Robotic Total : Radical hysterectomy The broad search strategy used for this meta analysis and the multitude of databases searched has reduced bias during literature search. However, certain unpublished studies could have been missed. Even though the numbers in individual cohort were of considerable size, the numbers of studies included were low. The broad search strategy used for this systematic review and the multitude of databases searched has reduced bias during literature search. Double counting and piece together data from multiple reports of the same were avoided by juxtaposing author names, sample sizes, and outcome data. This reduced bias during inclusion. Ideally in a design like this, it would be better to exclude observational studies with less than 20 cases. However, the precise number is a matter and case reports or very small series are also included and the impact for publication Journal of Minimal Access Surgery July-September 2012 Volume 8 Issue 3 71

6 bias may be there. The data presented is a mixture of prospective and retrospective studies and comparative and non-comparative ones. The heterogeneity risk is there. The risk of selection bias by the included studies is also noticed. For example, lymph node metastases were rare when the DaVinci surgical system was used (mean 2%). This contrasts to the traditional surgery where lymph node metastasis rate was 12%. Similarly, tumour was found occasionally at the margin of a robotic or laparoscopic case (mean of 1.7%) but apparently occurred more than three times more commonly in open surgery (mean was 5.5%). One explanation chance is if the difficult cases were done using familiar open methods and easy early-cancer cases were selected for the novel new toy. Of particular note are the large numbers of patients in retrospective series, where the quality of data would be of more concern. In the open open radical hysterectomy group, the largest series contains approximately 2/3 of all the cases; however, this was completed over 20 years ago. In addition, many of the laparoscopic studies significantly pre-date the robotic studies. Image quality, instrumentation and energy sources have all improved dramatically over recent years and therefore it is not possible to compare like with like. CONCLUSION Minimally invasive surgery is an alternate option for radical surgery in early-stage cervical cancer. However, laparoscopic method is not free from complications. Experience of surgeon may reduce complications. Robotic surgery is associated with less morbidity compared to open and laparoscopic method in this meta analysis. This may be due to better magnification, dexterity, flexibility and considerable reduction in surgeon s fatigue during surgery compared to other methods. Given the drawbacks of observational studies with their multiple inherent biases, it is difficult to see that the conclusions reached as a result of this systematic review are likely to change practice. The potential advantages of minimal access surgery techniques eg shorter hospital stay, less infectious morbidity are apparent from individual observational studies. However, because of the inherent biases relating to case selection for different surgical techniques treating the same disease, the only way to reliably look at differences between the individual techniques would be to perform randomised studies comparing the different techniques. Only studies of this type will lead to potentially valid conclusions about key oncological outcomes, quality of life and risks of major morbidity. REFERENCES 1. Averette HE, Nguyen HN, Donato DM, Penalver MA, Sevin BU, Estape R,. Radical hysterectomy for invasive cervical cancer: A 25-year prospective experience with the Miami technique. 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7 22. Schreuder HW, Zweemer RP, van Baal WM, van de Lande J, Dijkstra JC, Verheijen. From open radical hysterectomy to robot-assisted laparoscopic radical hysterectomy for early stage cervical cancer: Aspects of a single institution learning curve. Gynecol Surg 2010;7: Geisler JP, Orr CJ, Khurshid N, Phibbs G, Manahan KJ. Robotically assisted laparoscopic radical hysterectomy compared with open radical hysterectomy. Int J Gynecol Cancer 2010;20: Nam EJ, Kim SW, Kim S, Kim JH, Jung YW, Paek JH,. A case-control of robotic radical hysterectomy and pelvic lymphadenectomy using 3 robotic arms compared with abdominal radical hysterectomy in cervical cancer. Int J Gynecol Cancer 2010;20: Vasilescu C, Sgarbura O, Tudor S, Popa M, Turcanu A, Florescu A,. Robotic radical hysterectomy with pelvic lymphadenectomy: Our early experience. Chirurgia 2009;104: Cite this article as: Geetha P, Nair MK., robotic and open method of radical hysterectomy for cervical cancer: A systematic review. J Min Access Surg 2012;8: Date of submission: 04/08/2011, Date of acceptance: 19/10/2011 Source of Support: Nil, Conflict of Interest: None declared. Journal of Minimal Access Surgery July-September 2012 Volume 8 Issue 3 73