Choosing the Right Patient: Planning for Laparotomy or Laparoscopy in the Patient With Endometrial Cancer

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1 Choosing the Right Patient: Planning for Laparotomy or Laparoscopy in the Patient With Endometrial Cancer Allison Ball, MD, MSc, 1 James R. Bentley, MBChB, FRCSC, 1 Colleen O Connell, PhD, 2 Katharina E. Kieser, MD, FRCSC, MSc 1 1 Department of Obstetrics and Gynaecology, Dalhousie University, Halifax NS 2 Perinatal Epidemiology Research Unit, IWK Health Centre, Halifax NS Abstract Objective: Endometrial cancer remains the most commonly diagnosed gynaecologic cancer in North America. The staging and initial treatment of endometrial cancer involves surgery. Laparoscopic surgery is increasingly used as an alternative to laparotomy. Patient selection for laparoscopy can be optimized by examining factors involved in both the choice of surgical approach and the ultimate procedure performed. We wished to identify factors that might be barriers to laparoscopic surgery in women with endometrial cancer who had surgery performed by the gynaecologic oncology group at the Capital District Health Authority (CDHA) in Halifax, Nova Scotia. Methods: We conducted a retrospective review of the records of women with endometrial cancer, histologically confirmed preoperatively between 2005 and 2007, who underwent surgery at the CDHA. Results: Between 2005 and 2007 in Nova Scotia, 428 cases of endometrial cancer were diagnosed, and 289 women with a preoperative diagnosis of endometrial cancer underwent surgery at the CDHA. Of these, 66.1% (191/289) underwent a planned laparotomy, and 33.9% (98/289) had a planned laparoscopy. The proportion of attempted laparoscopies increased from 21.9% to 57.1% (P = 0.002) over time, while there was no change in the conversion rate (P = 0.23). Patients with abnormal findings on pelvic examination were more likely to have a laparotomy (RR = 1.5; 95% CI 1.34 to 1.68). Independent predictors of laparoscopic conversion to laparotomy were age 75 years or over (P = 0.03) and non-endometrioid histology (P = 0.002). Conclusion: Our data identify age and non-endometrioid histology as independent factors for conversion of surgery for endometrial cancer from laparoscopy to laparotomy. With this information we can optimize patient selection for laparoscopic surgery. Patients undergoing a conversion to laparotomy do not have a significant increase in surgery time or perioperative morbidity. Key Words: Endometrial cancer, laparoscopy, surgery, perioperative morbidity Competing Interests: None declared. Received on November 7, 2010 Résumé Objectif : Le cancer de l endomètre demeure l un des cancers gynécologiques diagnostiqués le plus souvent en Amérique du Nord. La stadification et le traitement initial de ce type de cancer nécessitent une chirurgie. La chirurgie laparoscopique est utilisée de plus en plus en tant que solution de rechange à la laparotomie. Le choix des patientes pour la pratique d une laparoscopie peut être optimisé en étudiant les facteurs qui influencent tant le choix de la méthode chirurgicale à adopter que l intervention ultimement pratiquée. Notre objectif était d identifier les facteurs qui pourraient faire obstacle à la chirurgie laparoscopique chez les femmes présentant un cancer de l endomètre et qui avaient été opérées par le groupe d oncologie gynécologique de la Capital District Health Authority (CDHA), à Halifax, en Nouvelle-Écosse. Méthodes : Nous avons effectué un examen rétrospectif des dossiers de femmes présentant un cancer de l endomètre, confirmé par histologie avant l intervention chirurgicale entre 2005 et 2007, qui ont été opérées à la CDHA. Résultats : Entre 2005 et 2007 en Nouvelle-Écosse, 428 cas de cancer de l endomètre ont été diagnostiqués et 289 femmes chez lesquelles on a diagnostiqué un cancer de l endomètre avant l intervention chirurgicale ont été opérées à la CDHA. De celles-ci, 66,1 % (191/289) ont subi une laparotomie planifiée et 33,9 % (98/289) ont subi une laparoscopie planifiée. La proportion de tentatives de laparoscopie est passée de 21,9 % à 57,1 % (P = 0,002) au fil du temps, alors que le taux de conversion n a pas changé (P = 0,23). Les patientes dont l examen pelvien a donné des résultats anormaux étaient davantage susceptibles de subir une laparotomie (RR = 1,5; IC à 95 %, 1,34 1,68). Les prédicteurs indépendants de conversion de la laparoscopie en laparotomie étaient un âge supérieur à 75 ans (P = 0,03) et une histologie non endométrioïde (P = 0,002). Conclusion : Nos données ont déterminé que l âge et une histologie non endométrioïde sont des facteurs indépendants de conversion de laparoscopie en laparotomie en ce qui concerne le cancer de l endomètre. Grâce à ces renseignements, nous pouvons optimiser le choix des patientes en vue d une laparoscopie. Les patientes qui passent de la laparoscopie à la laparotomie ne présentent pas une augmentation significative du risque sur le plan de la durée de la chirurgie ou de la morbidité périopératoire. Accepted on January 10, 2011 J Obstet Gynaecol Can 2011;33(5) MAY JOGC MAI 2011

2 Choosing the Right Patient: Planning for Laparotomy or Laparoscopy in the Patient With Endometrial Cancer INTRODUCTION Endometrial cancer is the fourth most common cancer diagnosis in North American women. 1 In 2009 in Canada, there were an estimated 4400 new cases diagnosed and 800 deaths. 2 The current standard for primary treatment of endometrial cancer involves surgical staging, hysterectomy, and bilateral salpingooophorectomy, followed by adjuvant radiation and/ or adjuvant chemotherapy if indicated. During the last decade, laparoscopic surgery has become an alternative to traditional laparotomy for many patients. Trial results indicate that survival outcomes after laparoscopic surgery are the same as after laparotomy. 3 6 Further, data from randomized controlled trials have shown laparoscopic management to be superior to laparotomy in terms of postoperative morbidity, length of hospital stay, and quality of life Because the majority of women with this diagnosis will not die of the disease, but often have significant comorbidities, the additional morbidity arising from surgery is a consideration in choosing management. Despite this evidence supporting the use of laparoscopy in the treatment of endometrial cancer, it remains uncertain for several reasons which patients should be offered this approach. Although there is a historical belief that both obese and elderly patients are poor candidates for laparoscopic surgery, studies comparing surgical approaches in endometrial cancer patients of each of these populations of endometrial cancer patients challenge this bias These populations can benefit from the decreased perioperative morbidity associated with laparoscopic surgery. Surgeons discomfort with performing laparoscopic surgery, particularly lymph node sampling, may also discourage them from offering this approach to their patients. However, we do not know whether preoperative factors may help predict conversion of surgery in these patients from laparoscopy to laparotomy. In our centre, the use of laparoscopic surgery for the treatment of endometrial cancer has increased over the last decade. During the study period, patients were selected for a laparoscopic approach if their BMI was < 40, if the surgeon determined they had cervical descent and/or appropriate vaginal calibre for the surgery to be performed, and if they had no history of previous intra-abdominal sepsis or known dense intra-abdominal adhesions. The objective of the study was to identify factors that predicted conversion from laparoscopic surgery to laparotomy in women with endometrial cancer who were undergoing surgery in the Division of Gynaecologic Oncology in the CDHA. By examining the factors involved in the choice of surgical approach and the final performed procedure we hoped to improve and expand the selection of patients for laparoscopic surgery. METHODS We conducted a retrospective study of women with preoperatively confirmed endometrial cancer diagnosed between 2005 and 2007 who had surgery performed by members of the Division of Gynaecologic Oncology in the Capital District Health Authority in Halifax, Nova Scotia. The division accepts referrals from within the province of Nova Scotia for all gynaecologic cancers, and for select indications from the other Maritime Provinces. Thus, women whose preoperative diagnosis of cancer was changed to hyperplasia on postoperative pathology review are included in the data, as the initial decision for surgical approach was made on the assumption that cancer was present. We collected information on mode of surgery, patient, tumour factors (BMI, age, ASA status, preoperative imaging, preoperative pelvic examination findings, preoperative histology), and surgical factors (number of lymph nodes dissected, rate of conversion from laparoscopy, total operating time, estimated intraoperative blood loss, duration of hospital stay, and postoperative complication rates). Surgical staging was determined according to FIGO 1988 guidelines. 21 Medical charts were reviewed and data extracted into FileMaker Pro v.8.5 (FileMaker Inc., Santa Clara CA). Data analysis was then performed using SPSS version 14 (IBM Corp., Somers NY).Continuous variables were analyzed using the Student t test. Categorical variables were analyzed using chi-squared or Fisher exact tests. Logistic regression was performed to analyze factors predictive of conversion to laparotomy. Statistical significance was defined as P Approval was obtained from the Capital Health Research Ethics Board. RESULTS Between January 2005 and December 2007, 428 women in Nova Scotia had a diagnosis of endometrial cancer (Figure). Their surgical procedures took place between January 2005 and December 2008, although they had all received the diagnosis between 2005 and Patients were excluded from analysis if they had initial primary surgery outside the CDHA (n = 71), had cancer diagnosed postoperatively rather than preoperatively (n = 60), had no surgical management of their cancer (n = 30), had MAY JOGC MAI

3 Women in Nova Scotia with a preoperative histologic diagnosis of endometrial cancer between January 2005 and December 2007 Diagnosis of endometrial cancer between 2005 and 2007 (n = 428) No surgery (n = 30) Stromal malignancy (n = 2) Incomplete data (n = 7) Post-operative diagnosis (n = 60) Surgery in periphery (n = 71) Received Sx at CDHA (n = 289) Planned laparotomy (n = 191 ) (n = 98) Completed laparoscopy (n = 81 ) Converted to laparotomy (n = 17 ) incomplete data (n = 7), or had a stromal malignancy (n = 2). Some patients were excluded for more than one reason. Six patients with atypical hyperplasia who had been referred for management by the oncology team were included in the analysis, as the approach to their surgery was the same as for those with endometrioid histology. Of 289 women included in the analysis, 66.1% (191/289) underwent a planned laparotomy, and laparoscopy was planned for 33.9% (98/289). The rate of attempted laparoscopies increased from 21.9% to 57.1% over the time of the study (P = 0.002), but there was no change in the conversion rate from laparoscopy to laparotomy (P = 0.23). The overall conversion rate was 17.3% (17/98). Preoperative characteristics and demographics are outlined in Table 1. There were no differences in mean age, parity, or number of previous abdominal surgical procedures among the three groups. The mean BMI of women undergoing a planned laparotomy was 33.9, significantly higher than for the other two groups (P < 0.001). Patients with higher ASA classifications were more likely to undergo a laparotomy. Histologic findings recorded preoperatively included endometrioid and atypical endometrial hyperplasia, clear cell carcinoma, papillary serous adenocarcinoma, malignant mixed müllerian tumour, and other (examples of which include poorly differentiated and mucinous carcinoma). Preoperative pelvic examination was classified as normal or abnormal. Examples of findings in an abnormal pelvic examination included a bulky uterus, a fixed uterus, or a pelvic mass. Women with an abnormal pelvic examination were more likely to undergo a laparotomy than women with a normal examination (RR = 1.5; 95% CI 1.34 to 1.68). However, when a laparoscopy was performed, logistic regression did not find that an abnormal pelvic examination predicted conversion to a laparotomy (P = 0.099). Perioperative characteristics are shown in Table 2. Mean total operating time was significantly shorter in the laparotomy group (P < 0.001), although the duration of surgery did not differ between the laparoscopy group and the conversion group. Mean estimated blood loss was significantly greater in the laparotomy group than in the other two groups (P = 0.001). Mean duration of postoperative stay was shortest in the completed laparoscopy group: 1.5 days (P < 0.001) compared with 5.4 and 4.3 days, respectively, in the laparotomy and conversion groups. There was no significant difference between the last two groups. Pelvic and para-aortic lymph node dissections were performed in 67.0% and 4.5% of all patients respectively. Pelvic lymph node dissections were performed in 57.8% of patients undergoing laparotomy, significantly less than in both the completed laparoscopy and conversion groups (84.0% and 88.9%, respectively; P < 0.01). There were no significant differences among the groups with respect to the frequency of para-aortic lymph node dissection. Surgical staging was assigned in all 289 cases. The overall rate of conversion from a laparoscopic approach to a laparotomy was 17.3%. Reasons for conversion are summarized in Table 3. The most common reason was operative difficulty (e.g., intra-abdominal adhesions, enlarged uterus, morbid obesity). Other reasons included unanticipated intra-abdominal findings (e.g., small bowel mesenteric mass) and laparoscopic access injury. 470 MAY JOGC MAI 2011

4 Choosing the Right Patient: Planning for Laparotomy or Laparoscopy in the Patient With Endometrial Cancer Table 1. Preoperative patient characteristics (n = 191) Completed laparoscopy (n = 81) Planned laparotomy Conversion (n = 17) P Mean age in years (SD) 63.5 (11.1) 61.8 (9.1) 65.0 (12.0) Median BMI (range) 33.9* ( ) 27.1 ( ) 28.8 ( ) < 0.001*; 0.01 Median parity (range) 2 (0 to >5) 2 (0 to >5) 2 (0 to >5) Nulliparous 20.9% 16.1% 23.5% Median no. of previous abdominal surgical 1 (0 4) 1 (0 4) 1 (0 4) procedures (range) Preoperative histology Endometrioid 137 (71.7%)* 76 (93.8%) 10 (58.8%) < 0.001*; < Clear cell 6 (3.1%) 1 (1.2%) 2 (11.8%) Papillary serous 17 (8.9%)* 1 (1.2%) 4 (23.5%) < 0.05*; < 0.01 Malignant mixed müllerian tumour 14 (7.3%) 1 (1.2%) 0 < 0.05* Other (i.e., poorly differentiated, 17 (8.9%)* 0 1 (5.9%) < 0.05* mucinous) Preoperative pelvic examination Normal 117/184 (63.6%)* 73/76 (96.1%) 13/16 (81.2%) < 0.001* Abnormal (bulky uterus, pelvic mass) 67 (34.6%) 3 (3.9%) 3 (18.8%) Preoperative imaging Valid n = 113 Valid n = 80 Valid n =16 Yes 101 (89.4%)* 51 (63.8%) 11 (68.8%) < 0.001* No 12 (10.5%) 29 (36.2%) 5 (31.2%) ASA classifications Valid n = (10.2%)* 23 (28.4%) 4 (23.5%) < 0.001* (67.2%) 52 (64.2%) 11 (64.7%) 3 41 (22.0%)* 6 (7.4%) 2 (11.8%) < 0.001* 4 1 (0.5%) 0 0 * Laparotomy versus completed laparoscopy Laparotomy versus conversion Completed laparoscopy versus conversion Both perioperative and postoperative complications were identified (Table 4). Perioperative complications included vascular, bowel, ureter, or nerve injury, and blood transfusion within 30 days of surgery. Postoperative complications included thrombotic events, new onset renal failure, wound complications, and ileus and intraperitoneal abscesses. Overall perioperative complication rates were not significantly different among the three surgical groups, except that more women undergoing a planned laparotomy required blood transfusions within 30 days of surgery (15.1% vs. none in the other two groups; P < 0.001). Overall postoperative complication rates were significantly greater in the laparotomy group than in both the completed laparoscopy group and the conversion group (P < 0.001). Specifically, the laparotomy group had more other complications, such as arrhythmias, pneumonia, hernia, and vault cellulitis (P < 0.01). There were no significant differences in rates of wound complications, fascial dehiscence, and thrombotic events. Multivariate logistic regression was performed to identify independent factors that may be predictive of conversion from laparoscopy to laparotomy. Included in the multivariate analysis were age, BMI, ASA classification, number of previous abdominal surgical procedures, preoperative histology, and estimated blood loss. This analysis found that age 75 years (P = 0.03) and non-endometrioid histology (P = 0.002) were independent predictors of conversion from laparoscopy to laparotomy (Table 5). DISCUSSION During the study period, the rate of conversion from laparoscopy to laparotomy in women undergoing surgery for endometrial cancer remained stable at 17.3%. Current MAY JOGC MAI

5 Table 2. Perioperative characteristics Laparotomy Completed laparoscopy Conversion (n = 191) (n = 81) (n = 17) P Mean operating time in minutes (SD) (33.5)* (47.5) (32.4) < 0.001*; <0.001 Pelvic lymph node dissection 109 (57.1%)* 68 (84.0%) 15 (88.2%) < 0.001*; 0.02 Mean number of pelvic lymph nodes (SD) 11.6 (6.3) 11.5 (5.3) 12.9 (7.5) Para-aortic lymph node sampling 9 (4.7%) 1 (1.2%) 3 (17.6%) < 0.05 Mean number of para-aortic lymph nodes (SD) 3.4 (2.2) (0.6) Mean estimated blood loss in ml (SD) (470.1)* (109.8) (92.7) 0.001* Mean duration of postoperative stay in days (SD) 5.4 (3.1)* 1.5 (0.7) 4.3 (3.2) < 0.001*; < Stage I 116 (60.7%)* 68 (84.0%) 11 (64.7%) < 0.001* II 31 (16.2%) 7 (8.6%) 4 (23.5%) III 26 (13.6%) 6 (7.4%) 2 (11.8%) IV 18 (9.4%)* 0 0 < 0.01* * Laparotomy versus completed laparoscopy Laparotomy versus conversion Completed laparoscopy versus conversion published conversion rates for endometrial cancer surgical staging vary greatly, ranging from 3% 22 to 26% in the recently published LAP2 study. 12 Such variation is due to differing experience among the surgeons and the learning curve of the surgical team. Our data show that, while the conversion rate remains stable, the proportion of surgical procedures performed laparoscopically is increasing at our centre. This suggests that members of the gynaecologic oncology group are choosing a wider variety of patients for laparoscopy as they become more comfortable with the approach. This benefits patients with cancer, as laparoscopy is less invasive and results in a shorter postoperative recovery As expected, our data are consistent with previous studies showing that laparoscopic surgery is associated with increased operating time but decreased intra-operative blood loss and shorter hospital stay. The preoperative decision regarding approach to surgery was multifactorial, but the patient s BMI was a major consideration. Very high BMI can pose a challenge for both the surgeon and the anaesthetist. Here, the differences in BMI did not affect the rate of conversion from laparoscopy but did affect the rate of lymphadenectomy in each group. The benefits associated with a technically challenging lymphadenectomy do not always outweigh its risks. There was also a significantly different rate of postoperative complications between the groups in our study. As expected, patients having a laparotomy had more postoperative complications. This may be due to the fact that patients with a higher BMI are in this group, as are patients with more aggressive histology, and these factors may combine with the laparotomy incision to contribute to the higher complication rate. The primary aim of this study was to identify factors associated with conversion from laparoscopy to laparotomy, in order to improve patient selection for the appropriate surgical approach. Multivariate analysis indicates that independent factors associated with conversion are age 75 years and non-endometrioid histology. BMI, ASA classification, estimated blood loss, previous abdominal surgery, and abnormal pelvic examination are not independent factors in predicting conversion. The information gained in this study will facilitate a more rational surgical approach. Women with an increased BMI who were undergoing a laparoscopy were not found to require conversion more frequently. Our study highlights the fact that increased BMI is not always a contraindication to laparoscopy, and if the laparoscopic approach is attempted in these women, it is often completed. Women with an increased BMI are the very patients who benefit most from having minimally invasive surgery. Data to support this have emerged over the past decade in studies regarding the feasibility of Table 3. Reasons for conversion from laparoscopy to laparotomy Reasons for conversion Frequency Access injury 1 (5.9%) Unanticipated intra-abdominal findings 3 (17.6%) (small bowel mesenteric mass, abnormal liver lesion, enlarged suspicious ovary) Operative difficulty 12 (70.6%) (adhesions, uterine size, morbid obesity) Other 1 (5.9%) (inability to identify ureter) 472 MAY JOGC MAI 2011

6 Choosing the Right Patient: Planning for Laparotomy or Laparoscopy in the Patient With Endometrial Cancer Table 4. Complications (n = 191) Planned laparotomy Completed laparoscopy (n = 81) Conversion (n = 17) P Perioperative complications Blood transfusion within 30 days 24 (12.5%) 0 0 < Vascular 5 (2.6%) 0 1 (5.9%) NS Bowel 1 (0.5%) 0 0 NS Bladder/ureter injury 2 (1.0%) 1 (1.2%) 0 NS Nerve 1 (0.5%) 0 0 NS Other (subcutaneous emphysema, 2 (1.0%) 1 (1.2%) 0 NS cardiac arrhythmia) Any perioperative complications 30 (15.7%) 2 (2.5%) 1 (5.9%) Postoperative complications Deep vein thrombosis/pulmonary embolism 1 (0.5%) 1 (1.2%) 0 NS Cardiac complication 3 (1.6%) 1 (1.2%) 0 NS Renal failure 3 (1.6%) 0 0 NS Fascial dehiscence 1 (0.5%) 0 0 NS Wound complication (hematoma, infection, 32 (16.7%) 6 (7.4%) 1 (5.6%) NS skin breakdown) Ileus 11 (5.8%) 1 (1.2%) 1 (5.9%) NS Abscess 3 (1.6%) 3 (3.7%) 0 NS Other (pneumonia, hernia, cardiac arrhythmia, vault cellulitis) 20 (10.5%) 0 0 < 0.01 Any postoperative complications 54 (28.3%) 9 (11.1%) 2 (11.8%) < 0.01 N.B. Some patients had more than one complication performing laparoscopic surgery for endometrial cancer in the obese population. 3,14 Perioperative morbidity in the obese patient is decreased when laparoscopic surgery is used. 23,24 Laparoscopy in the older age group has been a controversial issue and is only now emerging as a mainstream choice for patients. It has been thought that the lower physiologic reserve and higher incidence of cardiopulmonary disease in elderly patients would contraindicate laparoscopic surgery. 25 In fact, patients in this population have shown the capacity to tolerate laparoscopy, and they stand to benefit greatly from its use. 26 In our study we found an increased risk of conversion to laparoscopy in patients 75 years. Patients in this age group may have a longer history of symptoms and may therefore have cancer at a more advanced stage. Furthermore, age is a risk factor for non-endometrioid histology. Further study is required to explore this finding. The strengths of this study include the large number of complete data sets available over a provincial population. The close follow-up of these patients also allowed us to track their complication rates accurately. Our study was designed to aid in preoperative clinical decision-making before the final pathology and staging is known. For that reason, we included six patients with atypical endometrial hyperplasia on final pathology who had been referred to a gynaecologic oncologist for their surgery. Limitations of the study include the fact that the laparoscopy rate in our centre was not stable for the duration of the study. We identified an increase in the proportion of laparoscopies performed, which is encouraging, but some of our findings may have been affected by variations in the availability of appropriate laparoscopic equipment and the experience of the operating room team. The ability to choose the appropriate surgical route for a woman with endometrial cancer is important to minimize the associated surgical morbidity when the survival outcomes are the same for both laparoscopy and laparotomy. It was reassuring to find that operating time and perioperative morbidity were not significantly increased in women who required a conversion from laparoscopy to laparotomy. We plan to increase the overall proportion of women who are offered a laparoscopic approach for endometrial cancer but use caution in women 75 years of age and in women with non-endometrioid histology on preoperative biopsy. MAY JOGC MAI

7 Table 5. Odds of converting from laparoscopy to laparotomy: multivariate logistic regression OR 95% CI P Body mass index (BMI) to ASA classification to Previous abdominal surgery to Normal abdominal examination to Histology (endometrioid versus non-endometrioid) to Estimated blood loss to Age 75 years to CONCLUSION Our data identify age and non-endometrioid histology as independent factors for conversion of surgery for endometrial cancer from laparoscopy to laparotomy. In identifying both positive and negative risk factors for conversion from a laparoscopic approach to laparotomy, our hope is to enhance appropriate patient selection for laparoscopic surgery and to ensure that care for women who do require conversion to laparotomy is not compromised. REFERENCES 1. Purdie DM, Green AC. Epidemiology of endometrial cancer. 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