CASE SERIES

Unanticipated Uterine Pathologic Finding After Morcellation During Robotic-Assisted Supracervical Hysterectomy and Cervicosacropexy for Uterine Prolapse Audra Jolyn Hill, MD,* Ashley W. Carroll, MD,* and Catherine A. Matthews, MDÞ

Background: Identification of occult malignancy after intra-abdominal morcellation at the time of robotic-assisted supracervical hysterectomy and cervicosacropexy for uterine prolapse may lead to challenging postoperative management and leads one to question the need for preoperative evaluation. Cases: We present 2 cases of occult endometrial carcinoma after robotic-assisted supracervical hysterectomy and cervicosacropexy with intra-abdominal uterine morcellation from January 2008 to December 2010. A total of 63 patients underwent the stated surgical procedure with 2 patients (3.17%) found to have abnormal uterine pathologic finding with International Federation of Gynecology and Obstetrics grade 1 endometrial adenocarcinoma. Both cases occurred in asymptomatic postmenopausal patients without risk factors for endometrial cancer, including no history of postmenopausal bleeding or hormone replacement therapy. Owing to intraoperative uterine morcellation and cervical retention, appropriate postoperative management was controversial and problematic. Each patient was referred to gynecologic oncology. To date, both patients are without evidence of residual disease. Conclusion: Owing to the risk of occult uterine pathologic finding and complicated postoperative management, preoperative endometrial assessment should be considered on all postmenopausal patients undergoing intra-abdominal uterine morcellation, regardless of risk factors. Key Words: pelvic organ prolapse, morcellation, unanticipated malignancy (Female Pelvic Med Reconstr Surg 2014;20: 113Y115)

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ith the progression of minimally invasive surgery and the introduction of robotic technology, surgeons now have an increased ability to offer a variety of minimally invasive techniques to correct pelvic organ prolapse. Transabdominal sacrocolpopexy is known as a durable and effective treatment for the repair of level one support defects with satisfactory results ranging from 93% to 97%,1 with a reoperation rate of 2.3 to 4.4%.2,3 With the introduction of laparoscopic sacrocolpopexy by Nezhat et al4 in 1994 and later the adoption of robotic technology in 2005, more women are undergoing a minimally invasive sacrocolpopexy procedure with decreased blood loss, quicker recovery time, and overall reduced morbidity.1,5,6 In comparison with the traditional abdominal approach, robotic sacrocolpopexy has been shown to have equivalent anatomical outcomes and From the *Department of Obstetrics and Gynecology, Virginia Commonwealth University Health System, and †Division of Urogynecology and Reconstructive Pelvic Surgery, University of North Carolina, Chapel Hill, NC. Reprints: Catherine A. Matthews, MD, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599. E-mail: Catherine_matthews@ med.unc.edu. The authors have declared they have no conflicts of interest. Presented as an oral poster presentation at the 32nd American Urogynecologic Society Annual Meeting, Providence, RI. Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/SPV.0b013e31829ff5b8

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durability of repair based on short-term results,1,5Y7 with longterm outcomes currently being evaluated. Mesh exposure is consistently identified as the most common complication after sacrocolpopexy, with rates ranging from 2% to 10%.8 Modifiable risk factors include smoking, type of mesh material, and concomitant hysterectomy.8 If a supracervical hysterectomy is performed rather than a total hysterectomy, thereby avoiding a colpotomy, the potential for reduced rates of mesh exposure exists.8,9 Additional benefits of supracervical hysterectomy include decreased blood loss and operative time compared to total laparoscopic hysterectomy.10 In contrast, if a total hysterectomy is performed, the lifetime risk of abnormal uterine and/or cervical pathologic finding is eliminated. In addition, with the removal of the cervix, one is able to prevent postoperative cyclical bleeding, which has been reported to range from 17% to 19% and may potentially lead to further intervention.11 Based on this evidence and the concern for increased rates of cuff dehiscence with concurrent total robotic hysterectomy,12 we made a clinical practice decision to preferentially perform concurrent robotic supracervical hysterectomy with sacrocolpopexy in women with uterovaginal prolapse who had no history of abnormal vaginal bleeding or abnormal cervical cytologic finding. Minimally invasive supracervical hysterectomy requires intra-abdominal morcellation for removal of the surgical specimen. The literature regarding management of a uterine malignancy that is identified on a morcellated specimen is limited, and this clinical scenario presents a significant postoperative dilemma. Not only does morcellation increase the risk of dissemination of intra-abdominal disease13,14 but retention of the cervix, suspended by synthetic mesh, raises a potential surgical challenge for subsequent trachelectomy. Currently, preoperative screening for occult endometrial cancer in women with uterovaginal prolapse is not routinely performed or recommended. With the reported incidence of occult endometrial carcinoma ranging from 0.3% to 15%15Y18 in asymptomatic women, we present a case series that evaluated the incidence and management of abnormal uterine pathologic finding in women undergoing robotic surgical procedures for pelvic organ prolapse that required intraabdominal morcellation, and we assessed the need for preoperative evaluation to detect occult malignancy in this population.

MATERIALS AND METHODS After institutional review board approval was obtained, a retrospective review of Virginia Commonwealth University’s urogynecology database was performed from January 2008 to December 2010. Subjects who underwent robotic-assisted supracervical hysterectomy and concomitant sacrocolpopexy were identified and individually reviewed via electronic medical records. Demographic characteristics, including age, race, and body mass index (BMI) and a complete medical history including menopausal status and use of hormone replacement therapy

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were obtained. Risk factors for endometrial cancer such as abnormal vaginal bleeding, genetic predisposition, history of postmenopausal bleeding, and parity were documented. Abnormal vaginal bleeding was identified via chart review using standard definitions of menorrhagia or metrorrhagia. Postmenopausal status was defined as last menstrual period more than 1 year before clinic visit. All hysterectomy specimens were sent for histopathological examination regardless of preceding history or symptoms. Review of surgical pathology was conducted on all subjects. After identification of abnormal pathologic finding, individual chart review was performed with documentation of intraoperative findings and further management decisions. Cases with premalignant or known malignant uterine or cervical pathologic findings were excluded.

CASE SERIES Of the 63 subjects identified, two (3.17%; 95% confidence interval, 0.38%Y11.1%) were found to have occult International Federation of Gynecology and Obstetrics grade 1 endometrial adenocarcinoma. Our first case was a 66-year-old white woman, gravida 5, para 3, who presented with complaints of symptomatic pelvic organ prolapse. The patient denied history of abnormal Papanicolaou test results or postmenopausal bleeding. On physical examination, her BMI was noted to be 21 kg/m2; her pelvic organ prolapse quantification examination result revealed stage IIIA pelvic organ prolapse. Initially, the prolapse symptoms were conservatively managed; however, the patient ultimately desired surgical management. She underwent a robotic supracervical hysterectomy, cervical sacropexy, and concomitant sling placement without incident and was discharged home on postoperative day 2. Unfortunately, the final pathology report returned reporting a microscopic focus of endometrial adenocarcinoma with less than 50% myometrial invasion; she was then referred to gynecologic oncology to assist with further management. After extensive counseling with gynecologic oncology, she underwent a robotic-assisted bilateral salpingo-oophorectomy (BSO), endocervical curettage (ECC) and peritoneal biopsies, all of which were negative for malignancy. Postoperative follow-up included ECC and cervical cytologic examination every 6 months, all of which remain negative to date. The second case of occult endometrial adenocarcinoma was identified in a 61-year-old white woman, gravida 3, para 1, who presented with symptomatic pelvic organ prolapse along with mixed urinary symptoms. The patient denied history of abnormal Papanicolaou test results or postmenopausal bleeding. Physical examination revealed a BMI of 30 kg/m2 with stage III pelvic organ prolapse. She also elected for surgical management and underwent a robotic supracervical hysterectomy, cervical sacropexy with BSO, with BSO performed secondary to patient’s age. The surgical procedures were performed without complications, and she was discharged home on postoperative day 1. Similarly, the final pathology report returned with more than 50% myometrial invasion with bilateral fallopian tubes and ovaries without evidence of malignant dysplasia. She was referred to gynecologic oncology and ultimately opted for no further surgical staging, radiation, or chemotherapy. She is similarly being followed with cervical cytologic examination and ECC biannually with no evidence of disease to date. In summary, both cases were found in asymptomatic postmenopausal subjects with no documented history of postmenopausal bleeding or hormone replacement therapy. Both subjects had BMIs less than 30 kg/m2 and age older than 60. Neither subject reported a history of abnormal uterine bleeding and therefore did not undergo a preoperative gynecological ultrasound or endometrial biopsy. Neither patient had a history of

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abnormal cervical cytologic finding. After identification of carcinoma on the morcellated uterine specimens, both subjects were referred to gynecologic oncology for further management; neither patient opted for trachelectomy or mesh removal.

DISCUSSION Endometrial cancer has a lifetime risk of 2.69%19 in the general population with the primary presentation of postmenopausal vaginal bleeding in 90% of cases. Risk factors include obesity, nulliparity, prolonged exposure to unopposed estrogen, and a family history of breast, ovarian, and colon cancer. However, up to 20% of patients with a diagnosis of endometrial malignancy have no symptoms at the time of diagnosis.20 In a retrospective review of women undergoing hysterectomy with reconstructive pelvic surgery, Frick et al15 demonstrated a 2.6% rate of endometrial hyperplasia or carcinoma in asymptomatic postmenopausal women. The specific threat presented by an occult endometrial cancer in women undergoing supracervical hysterectomy and uterine morcellation is the potential for an iatrogenic increase in recurrence risk due to dissemination of malignant cells within the abdomen. This, accompanied with the increased surgical risk incurred by a patient with a cervicosacropexy who needs subsequent trachelectomy and surgical staging, raises the clinical question of whether preoperative endometrial assessment should routinely be performed in all postmenopausal women considering supracervical hysterectomy and cervicosacropexy. There is a paucity of data to direct management of patients who have undergone supracervical hysterectomy and are found to have an occult malignancy on pathologic examination. In one case series of 17 subjects, 2 of 13 subjects who elected for a second surgical exploration were upstaged. Both of the cases, however, were for a diagnosis of leiomyosarcoma on the morcellated specimen, a tumor that is typically more aggressive than the adenocarcinomas seen in our subjects. The authors of this study did suggest that complete surgical restaging is valuable to tailor postoperative treatment and prevent unnecessary overtreatment with adjuvant chemotherapy or radiation of those with clinical stage I disease.21 Surgical restaging after a cervicosacropexy, however, is much more complicated owing to the presence of mesh along the cervix and vagina. The dilemma, therefore, remains as to how best to serve women presenting with uterovaginal prolapse who are considering sacrocolpopexy for surgical management. No reliable costeffective tool exists for the detection of endometrial cancer in these asymptomatic women. Endometrial biopsy, transvaginal ultrasound, saline infusion sonohysterography, and dilation and curettage are all means of evaluating the uterine lining, but each of these methods has limitations as a screening tool in the asymptomatic patient. Endometrial biopsy has limited use in the detection of focal lesions where false-negative biopsy results may occur in 2.5% to 32.5% of cases.19,20 Transvaginal ultrasound to evaluate the endometrial stripe has good data to support its use in patients with postmenopausal bleeding, but the normal value for endometrial thickness in asymptomatic patients has not been well established. Statistical models project that a stripe thickness of 11 mm portends a 6.7% risk of cancer and 0.002% if the endometrium was 11 mm or less.22 In a recent retrospective study by Ramm et al, 168 of 708 women underwent preoperative screening either by endometrial biopsy or transvaginal ultrasound before surgical interventions for pelvic organ prolapse. The incidence of endometrial adenocarcinoma was found to be 0.6% (5/708) with 4 of the 5 patients having normal preoperative screening results and no reported history of postmenopausal bleeding. This highlights the difficulty of evaluating the endometrium preoperatively in the * 2014 Lippincott Williams & Wilkins

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asymptomatic patient.23 Saline infusion sonohysterography is another noninvasive procedure that allows for a detailed evaluation of the endometrial cavity and has been shown to be equivalent to hysteroscopy in diagnosing polypoid lesions, atrophy, and endometrial hyperplasia in the symptomatic postmenopausal woman.24 Unfortunately, there are limited studies evaluating the use of saline infusion sonohysterography in the asymptomatic postmenopausal patient regarding benign or malignant pathologic finding. Usually, hysteroscopy with dilation and curettage is reserved for patients who have already undergone ultrasound and plus or minus biopsy with suspicious or inconclusive reports suggesting further workup. It does not present a costeffective or clinically feasible option for our patient population. The benefits of cervical preservation, with reduced rates of mesh exposure, blood loss, and lower rates of bladder and ureteral injury, have to be weighed against the risk of an occult endometrial cancer. Patients need to be extensively counseled about the additional risks of uterine morcellation and the potential compromise to their survival if an occult malignancy exists. Patients should be given the option of total hysterectomy with concomitant sacrocolpopexy as removal of the surgical specimen intact through the vagina would at least not do any harm. We acknowledge that the postoperative management of mesh exposure is less complicated than the subsequent management of an occult malignancy in a specimen that has undergone morcellation in the abdomen. This study is limited by a small sample size. Our rate of occult malignancy of 3% is consistent with previously reported rates of occult endometrial cancer found in asymptomatic women. Our data and the results presented by Frick et al15 suggest that postmenopausal women are at higher risk. Larger studies are needed to determine the true rate of occult malignancy in this patient population and to assess for the need of preoperative screening. One study suggests that all patients who are undergoing morcellation should have preoperative evaluation with both endometrial biopsy and ultrasound.25 At our institution, we now perform transvaginal ultrasound in our postmenopausal population before surgical management. With continued progression of minimally invasive surgical procedures and the potential of identifying abnormal pathologic finding after intra-abdominal morcellation, further studies and guidelines for postoperative management need to be investigated. Postmenopausal women who elect to undergo supracervical hysterectomy need to be apprised of this notable rate of occult endometrial cancer and consider the postoperative impact of their surgical decision. REFERENCES 1. Elliott DS, Frank I, Dimarco DS, et al. Gynecologic use of robotically assisted laparoscopy: Sacrocolpopexy for the treatment of high-grade vaginal vault prolapse. Am J Surg 2004;188(suppl 4A):52SY56S. 2. Diwadkar GB, Barber MD, Feiner B, et al. Complication and reoperation rates after apical vaginal prolapse surgical repair: a systematic review. Obstet Gynecol 2009;113(2 Pt 1):367Y373. 3. Nygaard IE, McCreery R, Brubaker L, et al. Abdominal sacrocolpopexy: a comprehensive review. Obstet Gynecol 2004;104(4): 805Y823.

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6. Daneshgari F, Kefer JC, Moore C, et al. Robotic abdominal sacrocolpopexy/sacrouteropexy repair of advanced female pelvic organ prolaspe (POP): utilizing POP-quantification-based staging and outcomes. BJU Int 2007;100(4):875Y879. 7. Elliott DS, Krambeck AE, Chow GK. Long-term results of robotic assisted laparoscopic sacrocolpopexy for the treatment of high grade vaginal vault prolapse. J Urol 2006;176(2):655Y659. 8. Tan-Kim J, Menefee SA, Luber KM, et al. Prevalence and risk factors for mesh erosion after laparoscopic-assisted sacrocolpopexy. Int Urogynecol J 2011;22(2):205Y212. 9. Bensinger G, Lind L, Lesser M, et al. Abdominal sacral suspensions: analysis of complications using permanent mesh. Am J Obstet Gynecol 2005;193(6):2094Y2098. 10. Mueller A, Renner SP, Haeberle L, et al. Comparison of total laparoscopic hysterectomy (TLH) and laparoscopy-assisted supracervical hysterectomy (LASH) in women with uterine leiomyoma. Eur J Obstet Gynecol Reprod Biol 2009;144(1):76Y79. 11. Ghomi A, Hantes J, Lotze EC. Incidence of cyclical bleeding after laparoscopic supracervical hysterectomy. J Minim Invasive Gynecol 2005;12(3):201Y205. 12. Kho RM, Akl MN, Cornella JL, et al. Incidence and characteristics of patients with vaginal cuff dehiscence after robotic procedures. Obstet Gynecol 2009;114(2 Pt 1):231Y235. 13. Kill LM, Kapetanakis V, McCullough AE, et al. Progression of pelvic implants to complex atypical endometrial hyperplasia after uterine morcellation. Obstet Gynecol 2011;117(2 Pt 2):447Y449. 14. Anupama R, Ahmad SZ, Kuriakose S, et al. Disseminated peritoneal leiomyosarcomas after laparoscopic ‘‘myomectomy’’ and morcellation. J Minim Invasive Gynecol 2011;18(3):386Y389. 15. Frick AC, Walters MD, Larkin KS, et al. Risk of unanticipated abnormal gynecologic pathology at the time of hysterectomy for uterovaginal prolapse. Am J Obstet Gynecol 2010;202(5):507 e501Ye504. 16. Renganathan A, Edwards R, Duckett JR. Uterus conserving prolapse surgeryVwhat is the chance of missing a malignancy? Int Urogynecol J 2010;21(7):819Y821. 17. Koss LG. Detection of occult endometrial carcinoma. J Cell Biochem Suppl 1995;23:165Y173. 18. Hofmeister FJ. Endometrial biopsy: another look. Am J Obstet Gynecol 1974;118(6):773Y777. 19. Howlader N, Noone AM, Krapcho M, et al, eds. SEER Cancer Statistics Review, 1975Y2010, National Cancer Institute. Bethesda, MD. 20. Malkasian G Jr, Annegers J, Fountain K. Carcinoma of the endometrium: stage I. Am J Obstet Gynecol 1980;136(7):872Y888. 21. Einstein MH, Barakat RR, Chi DS, et al. Management of uterine malignancy found incidentally after supracervical hysterectomy or uterine morcellation for presumed benign disease. Int J Gynecol Cancer 2008;18(5):1065Y1070. 22. Smith-Bindman R, Weiss E, Feldstein V. How thick is too thick? When endometrial thickness should prompt biopsy in postmenopausal women without vaginal bleeding. Ultrasound Obstet Gynecol 2004;24(5): 558Y565. 23. Ramm O, Gleason JL, Segal S, et al. Utility of preoperative endometrial assessment in asymptomatic women undergoing hysterectomy for pelvic floor dysfunction. Int Urogynecol J 2012;23(7):913Y917.

4. Nezhat CH, Nezhat F, Nezhat C. Laparoscopic sacral colpopexy for vaginal vault prolapse. Obstet Gynecol 1994;84(5):885Y888.

24. Bingol B, Gunenc Z, Gedikbasi A, et al. Comparison of diagnostic accuracy of saline infusion sonohysterography, transvaginal sonography and hysteroscopy. J Obstet Gynaecol 2011;31(1):54Y58.

5. Geller EJ, Siddiqui NY, Wu JM, et al. Short-term outcomes of robotic sacrocolpopexy compared with abdominal sacrocolpopexy. Obstet Gynecol 2008;112(6):1201Y1206.

25. Hagemann IS, Hagemann AR, LiVolsi VA, et al. Risk of occult malignancy in morcellated hysterectomy: a case series. Int J Gynecol Pathol 2011;30(5):476Y483.

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Unanticipated uterine pathologic finding after morcellation during robotic-assisted supracervical hysterectomy and cervicosacropexy for uterine prolapse.

Identification of occult malignancy after intra-abdominal morcellation at the time of robotic-assisted supracervical hysterectomy and cervicosacropexy...
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