Incidence of Tissue Morcellation During Surgery for Uterine Sarcoma at a Canadian Academic Centre

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1 GYNAECOLOGY Incidence of Tissue Morcellation During Surgery for Uterine Sarcoma at a Canadian Academic Centre Innie Chen, MD, MPH, FRCSC, 1,2 Laura Hopkins, MSc, MD, FRCSC, 1,2 Bianca Firth, BSc, 2,3 Julia Boucher, 1,2 Sukhbir S. Singh, MD, FRCSC 1,2 1 Department of Obstetrics and Gynaecology, University of Ottawa, Ottawa ON 2 The Ottawa Hospital Research Institute, Ottawa ON 3 Faculty of Medicine, University of Ottawa, Ottawa ON Abstract Objectives: To determine the incidence of tissue morcellation during surgery for uterine sarcoma in a Canadian tertiary academic centre. Methods: In this retrospective cohort study, the clinical charts of all women who underwent hysterectomy for uterine sarcoma at the Ottawa Hospital between April 1, 2007, and March 31, 2014, were reviewed for their clinical characteristics and details of surgical treatment. Results: Sixty-six cases of uterine sarcoma were identified. The mean (± SD) age of patients was 62.1 ± 10 years, and 81.8% were postmenopausal. Of the tumours, 43.9% were carcinosarcomas, 28.8% were leiomyosarcomas, 13.6% were endometrial stromal sarcomas, 6.1% were adenosarcomas, 1.5% were uterine rhabdomyosarcomas, and 6.1% were undifferentiated sarcomas. None of the surgical specimens were morcellated by laparoscopic power morcellation, and 61/66 (92.4%) of patients had their surgery performed by a gynaecologic oncologist. In the remaining five women whose surgery was performed by a general gynaecologist (4 with leiomyosarcomas and 1 with undifferentiated uterine sarcoma), two surgical specimens were morcellated manually using a scalpel during the removal of presumed fibroids at hysterectomy performed by midline laparotomy. The first of these was a case performed as an emergency because of acute pelvic symptoms secondary to leiomyosarcoma, and the second case had a solitary leiomyosarcoma among multiple benign leiomyomata. Conclusion: Uterine sarcomas are uncommon, and morcellation is rarely performed but may nevertheless be performed in the surgical management of presumed fibroids. Further studies and the establishment of a national registry are needed to better quantify the risk of morcellation, to characterize clinical risk factors, and to provide surgical alternatives for women undergoing uterine surgery. J Obstet Gynaecol Can 2015;37(5): Key Words: Morcellation, uterine sarcoma, fibroid, hysterectomy Competing Interests: None declared. Received on October 19, 2014 Accepted on November 10, 2014 Résumé Objectifs : Déterminer l incidence du morcellement tissulaire dans le cadre des chirurgies visant des sarcomes utérins au sein d un centre universitaire tertiaire canadien. Méthodes : Dans le cadre de cette étude de cohorte rétrospective, les dossiers cliniques de toutes les femmes qui ont subi une hystérectomie en raison d un sarcome utérin à L Hôpital d Ottawa, entre le 1 er avril 2007 et le 31 mars 2014, ont été analysés en vue d en tirer les caractéristiques cliniques et d établir les détails du traitement chirurgical mis en œuvre. Résultats : Soixante-six cas de sarcome utérin ont été identifiés. L âge moyen (± σ) des patientes était de 62,1 ± 10 ans et 81,8 % d entre elles étaient postménopausées. Les tumeurs se répartissaient comme suit : 43,9 % d entre elles étaient de carcinosarcomes; 28,8 %, des léiomyosarcomes; 13,6 %, des sarcomes du chorion cytogène; 6,1 %, des adénosarcomes; 1,5 %, des rhabdomyosarcomes utérins; et 6,1 %, des sarcomes indifférenciés. Aucun des prélèvements chirurgicaux n a été soumis à un morcellement motorisé laparoscopique et, chez 61/66 (92,4 %) des patientes, la chirurgie a été menée par un gynéco-oncologue. Chez les cinq autres femmes (léiomyosarcomes dans quatre de ces cas et sarcome utérin indifférencié dans l autre), pour lesquelles la chirurgie a été menée par un gynécologue généraliste, deux prélèvements chirurgicaux ont été morcelés de façon manuelle au moyen d un scalpel pendant le retrait de fibromes présumés au moment d une hystérectomie menée par laparotomie médiane. Dans le premier de ces deux cas, l intervention a été menée d urgence en raison de la présence de symptômes pelviens aigus attribuables à un léiomyosarcome, tandis que dans l autre, la patiente en question présentait un léiomyosarcome solitaire situé parmi de multiples léiomyomes bénins. Conclusion : Les sarcomes utérins sont peu courants; de plus, bien qu un morcellement soit rarement mis en œuvre, une telle intervention peut néanmoins en venir à être menée dans le cadre de la prise en charge chirurgicale de fibromes présumés. La tenue d autres études et l établissement d un registre national s avèrent requis pour mieux quantifier le risque lié au morcellement, pour définir les facteurs de risque cliniques et pour fournir des solutions de rechange chirurgicales aux femmes qui doivent subir une chirurgie utérine. MAY JOGC MAI

2 Gynaecology INTRODUCTION It is well established that minimally invasive surgical techniques for hysterectomy are associated with reduced risk for intraoperative and postoperative morbidity, and a substantial portion of hysterectomies in Canada are therefore performed in this manner. 1 3 Uterine fibroids are the most common indication for hysterectomy; more than one third of hysterectomies are performed for this indication. The removal of large tissue specimens through a minimally invasive approach often requires the fragmentation of tissue through morcellation, either with a laparoscopic power morcellator or a scalpel. 4 While uterine fibroids are a common reason for uterine surgery, uterine sarcomas are by contrast relatively infrequent; the annual incidence of uterine leiomyosarcomas is approximately 0.64 per women. 4 6 It is generally not possible to distinguish between uterine fibroids and sarcomas preoperatively, and it has been estimated that approximately one in 350 to 500 women undergoing uterine surgery for presumed fibroids will have an unsuspected sarcoma However, the true incidence is largely unknown because the studies estimating the risk of occult malignancy at the time of hysterectomy are limited by their methodology and selection of study participants. Given the limitations of these studies and the questionable generalizability to Canadian populations and health care systems, there is a need to determine the risk of incidental diagnosis of uterine sarcomas in a Canadian setting. The purpose of this study was to determine the incidence of tissue morcellation during surgery for uterine sarcoma within a Canadian academic centre. The primary objective of this study was to determine if any cases of uterine sarcoma at the Ottawa Hospital were subject to any form of tissue morcellation. Our secondary objectives were to determine whether any cases were operated on by a non-gynaecologic oncologist and to determine the characteristics of care associated with such cases. METHODS In this retrospective chart review, the clinical records of all women with uterine sarcoma diagnosed at the Ottawa Hospital between April 1, 2007, and March 31, 2014, were reviewed for their clinical characteristics and details of surgical treatment. All women who had a hysterectomy for uterine sarcoma at the Ottawa Hospital were included in the study, and no exclusion criteria were applied. The medical record numbers for these cases were identified through the Ottawa Hospital Data Warehouse using the ICD 10-CA codes for malignant neoplasm of cervix uteri, corpus uteri, and uterus unspecified (C54*, C55*, C53*) and Diagnosis Type 4 (Morphology) codes for sarcoma or leiomyosarcoma (88903, 88913, 88963), Mullerian tumour/ carcinosarcoma (89503, 89803, 89813), endometrial stromal sarcoma (89303), sarcoma uterus not otherwise specified (88003), or adenosarcoma (89333). We then accessed the charts of these women and reviewed their clinical characteristics and details of surgical treatment. Information on patient demographics (age, gravidity, parity, menopausal status, past history of malignancy), clinical presentation (clinical symptoms, suspicion for rapid growth), ultrasound and MRI characteristics (number, size, and location of uterine mass), operative management (surgical specialty performing operation, type of uterine surgery, use of minimally invasive techniques, presence of tissue morcellation), and tumour characteristics (type and stage of uterine sarcoma) were systematically collected from clinical notes, radiologic reports, and pathology reports. In cases in which surgery was performed by a general gynaecologist rather than a gynaecologic oncologist, and in cases in which tissue morcellation took place, the charts were reviewed in further detail to identify preoperative, intraoperative, and postoperative events and outcomes. Descriptive statistics were used to characterize the study population. Continuous variables were summarized using means and standard deviations for normally-distributed data and medians and ranges for non-parametric data. Categorical variables were summarized using frequencies and proportions. Ethics approval was obtained from the Ottawa Health Science Network Research Ethics Board. RESULTS During the study period, 66 cases of uterine sarcoma were identified at the Ottawa Hospital. The clinical characteristics of this population are presented in Table 1. The mean (± SD) age was 62.1 ± 10 years, and 81.8% of the women were postmenopausal. In terms of clinical symptoms, 43.9% of the women experienced pain/ pressure symptoms, 13.6% reported heavy menstrual bleeding symptoms, and, 54.6% reported postmenopausal bleeding. More than half of the cohort (56.3%) presented with a single mass, 18.8% presented with two masses, and 25% presented with three or more masses. The mean diameter of the largest mass within each patient was 9.0 cm but ranged from 0.6 to 26 cm. The majority of these masses (69.4%) were subserosal, 11.1% were intramural, and 19.4% were submucosal. A suspicion of sarcoma based on rapid growth was documented in 16.7% of the 422 MAY JOGC MAI 2015

3 Incidence of Tissue Morcellation During Surgery for Uterine Sarcoma at a Canadian Academic Centre cases. Ten women had a history of previous malignancy, including six women with breast cancer and one with retinoblastoma. Histologic examination (Table 2) revealed that 43.9% of uterine sarcomas were carcinosarcomas, 28.8% were leiomyosarcomas, 13.6% were endometrial stromal sarcomas, 6.1% were adenosarcomas, 1.5% were uterine rhabdomyosarcomas, and 6.1% were undifferentiated sarcomas. After staging, it was determined that 43.6% of patients had stage 1 disease, 18.2% had stage 2 disease, 27.3% had stage 3 disease, and 10.9% had stage 4 disease. None of the surgical specimens were morcellated by laparoscopic power morcellation, and in 61/66 cases (92.4%), surgery was performed by a gynaecologic oncologist (Table 3). Of the five cases in which surgery was performed by a general gynaecologist, four were leiomyosarcomas and one was an undifferentiated uterine sarcoma. In three of these five cases, surgery was performed on an emergency basis. The first of these cases was a postmenopausal woman with new onset abdominal pain, heavy vaginal bleeding, and severe anemia requiring transfusion of four units of packed red blood cells. She was taken to the operating room for a total abdominal hysterectomy and bilateral salpingo-oophorectomy, and no morcellation was performed. The final pathology report showed a 13 cm leiomyosarcoma. The second case was a postmenopausal woman with a pelvic mass detected by ultrasound. She was assessed by the gynaecologic oncology service, and total abdominal hysterectomy and bilateral salpingo-oophorectomy was recommended, to be performed by a general gynaecologist. The surgery was performed as an emergency because of an acute exacerbation of symptoms. No morcellation was performed, and the final pathology report indicated a 20 cm leiomyosarcoma. The third case was a premenopausal woman with heavy menstrual bleeding in whom a pelvic ultrasound examination suggested that a fibroid was the underlying cause. Total abdominal hysterectomy and bilateral salpingooophorectomy was arranged, but she underwent surgery earlier than scheduled because of severe anemia requiring blood transfusion. No morcellation was performed, and the final pathology report indicated a 6.6 cm undifferentiated stage 1 uterine sarcoma. In two of the five cases performed by a generalist, manual morcellation was performed using a scalpel. The first of these cases was a premenopausal woman who was assessed by both the general gynaecology and gynaecology Table 1. Patient characteristics Mean age in years ± SD, n = ± 10.0 Menopausal status, n = 66, n (%) Pre-menopausal 12 (18.2) Post-menopausal 54 (81.8) Median gravidity (range), n = 59 2 (0 to 8) Median parity (range), n = 59 2 (0 to 7) History of previous malignancy, n = 66, n (%) Breast cancer 6 (9.1) Colon cancer 1 (1.5) Ovarian cancer 1 (1.5) Retinoblastoma 1 (1.5) Thyroid cancer 1 (1.5) Patient symptoms, n = 66, n (%) Pain or pressure 29 (43.9) Heavy menstrual bleeding 9 (13.6) Postmenopausal bleeding 36 (54.6) Ultrasound characteristics Number of masses, n = 48, n (%) 1 27 (56.3) 2 9 (18.8) 3 12 (25.0) Position of mass within uterus, n = 36, n (%) Submucosal 7 (19.4) Subserosal 25 (69.4) Intramural 4 (11.1) Mean diameter of largest mass in cm ± SD, n = 37 Documented concern about rapid growth, n = 66, n (%) Table 2. Pathologic characteristics Pathologic subtype, n = 66, n (%) 9.6 ± (16.7) Carcinosarcoma 29 (43.9) Leiomyosarcoma 19 (28.8) Endometrial stromal sarcoma 9 (13.6) Adenosarcoma 4 (6.1) Undifferentiated sarcoma 4 (6.1) Uterine rhabdomyosarcoma 1 (1.5) Stage, n = 55, n (%) I 24 (43.6) II 10 (18.2) III 15 (27.3) IV 6 (10.9) Mean diameter of largest uterine mass in cm ± SD, n = ± 5.9 MAY JOGC MAI

4 Gynaecology Table 3. Uterine sarcoma process of surgical care characteristics Surgeon subspecialty, n = 66, n (%) Gynaecologic oncology 61 (92.4) Gynaecology 5 (7.6) Surgical approach, n = 66, n (%) Abdominal 64 (97.0) Robotic 1 (1.5) Laparoscopic 1 (1.5) Presence of morcellation, n = 66, n (%) Power morcellation 0 (0) Manual morcellation 2 (3.0) oncology services because of a pelvic mass. MRI and PET scans suggested that the mass was a benign leiomyoma. A subtotal hysterectomy, begun with laparoscopic assistance and completed by midline laparotomy, was performed because of the patient s symptoms. Because of the size of the mass it was divided with a scalpel into two pieces for removal. The final pathology report indicated a 20 cm uterine leiomyosarcoma, and the patient subsequently underwent laparoscopic trachelectomy. The second case was a premenopausal woman with heavy menstrual bleeding and a previous hysteroscopic myomectomy for fibroids. She experienced ongoing bleeding and pressure symptoms, and underwent total abdominal hysterectomy and bilateral salpingectomy by midline laparotomy. The operative report suggested that there was a need to morcellate one of the masses in the uterus to remove it. The final pathology indicated a solitary 9 cm leiomyosarcoma among multiple benign leiomyomata. DISCUSSION The Ottawa Hospital is a tertiary academic centre to which patients are referred from surrounding community areas for both oncologic treatment and minimally invasive gynaecologic surgery. During the study period, an estimated 70% of hysterectomies performed for benign indications were carried out via minimally invasive routes at the Ottawa Hospital. 2 Our review of records indicated that there were two cases in which manual morcellation with a scalpel was performed, and no cases in which laparoscopic power morcellation was performed. In our study, five women with uterine sarcoma had surgery performed by a non-gynaecologist oncologist. In two of these cases a consultation with a gynaecologic oncologist had previously taken place. In the remaining three cases, two were performed as an emergency because of severe anaemia resulting from vaginal bleeding, and one had a leiomyosarcoma within a uterus affected by multiple fibroids. These cases, including the two in which manual morcellation was performed, reflect the difficulty in differentiating between fibroids and uterine sarcomas before surgery. This may be especially true in situations of acute pain or bleeding symptoms requiring emergency intervention or in situations in which there may be benign uterine leiomyomas coexisting with uterine sarcoma. Leiomyosarcomas are particularly difficult to differentiate from fibroids, and studies of preoperative imaging have not found reliable strategies to distinguish between the two Even if a diagnostic test has reasonable sensitivity and specificity, the positive predictive values would be considerably limited by the very low prevalence of uterine sarcoma in relation to the prevalence of fibroids. In our study we found that most women with uterine sarcoma were of advanced age and postmenopausal, both of which are known risk factors for the development of uterine sarcoma Suspicion of rapid growth was documented in only a fraction (16.7%) of the patients, and this is consistent with studies that have shown rapid growth to be a poor indicator of the presence of a sarcoma, as fibroids also have a tendency to change in size over time. 17 Among the 66 cases, four patients had a history of tamoxifen use, and two additional patients had possible tamoxifen exposure due to a history of breast cancer. Although the risk of sarcoma in women on tamoxifen therapy is also low, long-term tamoxifen use is a known risk factor for the development of uterine sarcoma In our cohort, there was also one patient with a history of hereditary retinoblastoma, which is also a known risk factor for uterine sarcoma. 22 While none of these clinical features alone can reliably differentiate between uterine sarcoma and fibroids, whether a combination of these features can assist in preoperative risk assessment warrants further study. A key strength of this study is that it included consecutive cases of uterine sarcoma dating from Because the data are current and were derived from a Canadian setting, we believe the results are generalizable to other tertiary academic centres. The main limitations are that the data were retrospectively collected and that the sample size was small because of the low incidence of uterine sarcoma. Given the importance of preoperative assessment, patient counselling, and informed consent in cases in which performing morcellation is considered, more studies are needed. Ideally these would take place through the establishment of national registries to obtain national estimates of the effect of morcellation on long-term outcomes. As the establishment of population-based 424 MAY JOGC MAI 2015

5 Incidence of Tissue Morcellation During Surgery for Uterine Sarcoma at a Canadian Academic Centre registries can take time, hospital-based chart reviews such as this study could be carried out in other Canadian hospital settings to corroborate our findings. Further studies of clinical risk factors are needed to facilitate preoperative risk assessment and the development of clinical decision aids to guide the use of morcellation techniques. Further research in other modes of surgical tissue retrieval is also warranted; these would include minilaparotomy, extracorporeal manual morcellation, morcellation in an intraperitoneal bag, or other processes that may facilitate decision-making such as intraoperative histologic sampling. 23 CONCLUSION Uterine sarcomas are uncommon, and morcellation of a sarcoma is rare but may be performed in the presence of presumed fibroids. The difficulty in preoperative differentiation between uterine fibroids and leiomyosarcoma highlights the importance of proper preoperative assessment and counselling in all cases in which tissue morcellation is considered. The establishment of a national registry would have the potential to allow better assessment of the true risk of tissue morcellation for Canadian women undergoing uterine surgery. Such a registry would also provide a framework for the further studies that are needed on clinical risk factors and alternatives to tissue morcellation during surgery. REFERENCES 1. Bernatchez-Laflamme SM, Bujold E, Roberge S, Laberge PY. Development of technicality indices of hysterectomies in Quebec. J Obstet Gynaecol Can 2013;35(2): Gale J, Chen I, Rattray D, Guo Y, Singh S. Strategic change in MIS hysterectomy rate at a tertiary care centre: a 7-year experience. J Obstet Gynaecol Can 2014;36(5): Chen I, Bajzak KI, Guo Y, Singh SS. A national survey of endoscopic practice among gynaecologists in Canada. J Obstet Gynaecol Can 2012;34(3): Canadian Institute for Health Information. Health indicators. Ottawa (ON): CIHI; Harlow BL, Weiss NS, Lofton S. The epidemiology of sarcomas of the uterus. J Natl Cancer Inst 1986;76(3): Chen I, Lisonkova S, Joseph KS, Williams C, Yong P, Allaire C. Laparoscopic versus abdominal myomectomy: practice patterns and health care use in British Columbia. J Obstet Gynaecol Can 2014;36(9): U.S. Food and Drug Administration. Quantitative assessment of the prevalence of unsuspected uterine sarcoma in women undergoing treatment of uterine fibroids: summary and key findings. Silver Spring (MD): FDA; Available at: MedicalDevices/Safety/AlertsandNotices/UCM pdf. Accessed September 23, Takamizawa S, Minakami H, Usui R, Noguchi S, Ohwada M, Suzuki M, et al. Risk of complications and uterine malignancies in women undergoing hysterectomy for presumed benign leiomyomas. Gynecol Obstet Invest 1999;48(3): Leibsohn S, d Ablaing G, Mishell DR Jr, Schlaerth JB. Leiomyosarcoma in a series of hysterectomies performed for presumed uterine leiomyomas. Am J Obstet Gynecol 1990;162(4):968 74; discussion Reiter RC, Wagner PL, Gambone JC. Routine hysterectomy for large asymptomatic uterine leiomyomata: a reappraisal. Obstet Gynecol 1992;79(4): Kamikabeya TS, Etchebehere RM, Nomelini RS, Murta EF. Gynecological malignant neoplasias diagnosed after hysterectomy performed for leiomyoma in a university hospital. Eur J Gynaecol Oncol 2010;31(6): Aviram R, Ochshorn Y, Markovitch O, Fishman A, Cohen I, Altaras MM, et al. Uterine sarcomas versus leiomyomas: Gray-scale and Doppler sonographic findings. J Clin Ultrasound 2005;33(1): Cornfeld D, Israel G, Martel M, Weinreb J, Schwartz P, McCarthy S. MRI appearance of mesenchymal tumors of the uterus. Eur J Radiol 2010;74(1): Harry VN, Narayansingh GV, Parkin DE. Uterine leiomyosarcomas: a review of the diagnostic and therapeutic pitfalls. The Obstetrician & Gynaecologist 2007;9(2): Moinfar F, Azodi M, Tavassoli FA. Uterine sarcomas. Pathology 2007;39(1): Brooks SE, Zhan M, Cote T, Baquet CR. Surveillance, epidemiology, and end results analysis of 2677 cases of uterine sarcoma Gynecol Oncol 2004;93(1): Parker WH, Fu YS, Berek JS. Uterine sarcoma in patients operated on for presumed leiomyoma and rapidly growing leiomyoma. Obstet Gynecol 1994;83(3): Wickerham DL, Fisher B, Wolmark N, Bryant J, Costantino J, Bernstein L, et al. Association of tamoxifen and uterine sarcoma. J Clin Oncol 2002;20(11): Wysowski DK, Honig SF, Beitz J. Uterine sarcoma associated with tamoxifen use. N Engl J Med 2002;346(23): Uehara T, Onda T, Togami S, Amano T, Tanikawa M, Sawada M, et al. Prognostic impact of the history of breast cancer and of hormone therapy in uterine carcinosarcoma. Int J Gynecol Cancer 2012;22(2): Lavie O, Barnett-Griness O, Narod SA, Rennert G. The risk of developing uterine sarcoma after tamoxifen use. Int J Gynecol Cancer 2008;18(2): Francis JH, Kleinerman RA, Seddon JM, Abramson DH. Increased risk of secondary uterine leiomyosarcoma in hereditary retinoblastoma. Gynecol Oncol 2012;124(2): Tulandi T, Ferenczy A. Biopsy of uterine leiomyomata and frozen sections before laparoscopic morcellation. J Minim Invasive Gynecol 2014;21(5): MAY JOGC MAI

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