Radical Trachelectomy for Early-Stage Cervical Cancer: A Survey of the Society of Gynecologic Oncology and Gynecologic Oncology Fellows-in-Training.

ORIGINAL STUDY

Radical Trachelectomy for Early-Stage Cervical Cancer A Survey of the Society of Gynecologic Oncology and Gynecologic Oncology Fellows-in-Training Sara J. Churchill, MD,* Shannon Armbruster, MD,Þ Kathleen M. Schmeler, MD,þ Michael Frumovitz, MD,þ Marilyn Greer, PhD,§ Jaime Garcia, MA,§ Glenda Redworth, MS,§ and Pedro T. Ramirez, MDþ Objective: The aim of this study was to survey gynecologic oncologists and fellows-intraining regarding the role of radical trachelectomy (RT) and conservative surgery in patients with early-stage cervical cancer. Materials and Methods: From June 2012 to September 2012, the Society of Gynecologic Oncology member practitioners (n = 1353) and gynecologic oncology fellows (n = 156) were sent group-specific surveys investigating current practice, training, and the future of RT for early-stage cervical cancer management. Results: Twenty-two percent of practitioners (n = 303) and 24.4% of fellows (n = 38) completed the surveys. Of the practitioners, 50% (n = 148) report performing RT, 98% (n = 269) support RT as treatment for squamous carcinoma, and 71% (n = 195) confirm the use of RT for adenocarcinoma. Most practitioners offer RT treatment for stages IA2 to IB1 smaller than 2 cm (n = 209, 76.8%) regardless of grade (77.7%) or lymph vascular space invasion (n = 211, 79.3%). Only 8% (n = 23) of practitioners feel that RT is appropriate for stage IBI larger than 2 cm. Respectively, both practitioners and fellows most frequently perform robotic-assisted (47.0%, n = 101 and 59.1%, n = 13) and abdominal (40.5%, n = 87 and 68.2%, n = 15) RT approaches. After training, fellows project the use of robotic-assisted (71%, n = 22) or abdominal methods (58.1%, n = 18). Overall, 75% (n = 227) of practitioners and 60% (n = 23) of fellows speculate that over the next 5 years, less radical procedures will be used to manage early-stage cervical cancer. Conclusions: Our findings suggest that practitioners and fellows believe RT remains an option for early-stage cervical cancer patients. However, a significant proportion of all respondents believe that less radical surgery may be a future consideration for patients with low-risk early-stage cervical cancer. Key Words: Radical trachelectomy, Conservative surgery, Cervical cancer Received June 25, 2014, and in revised form December 21, 2014. Accepted for publication December 21, 2014. (Int J Gynecol Cancer 2015;25: 681Y687)

*Department of Obstetrics and Gynecology, Cedars-Sinai Medical Center, Los Angeles, CA; †Department of Obstetrics and Gynecology, Summa Health System, Akron, OH; ‡Division of Surgery, Department of Gynecologic Oncology and Reproductive Medicine, and §Department of Institutional Research, The University of Texas MD Anderson Cancer Center, Houston, TX. Copyright * 2015 by IGCS and ESGO ISSN: 1048-891X DOI: 10.1097/IGC.0000000000000397 International Journal of Gynecological Cancer

Address correspondence and reprint requests to Pedro T. Ramirez, MD, Department of Gynecologic Oncology, Unit 1362, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030. E-mail: [email protected]. Supported in part by the National Institutes of Health through MD Anderson’s Cancer Center Support grant CA016672. The authors declare no conflicts of interest.

& Volume 25, Number 4, May 2015

Copyright © 2015 by IGCS and ESGO. Unauthorized reproduction of this article is prohibited.

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International Journal of Gynecological Cancer

cervical cancer is the fourth most common Worldwide, cause of female cancer and the most common cause of

death from gynecological cancer.1 Due to prevention and early detection, cervical cancer mortality rates in the United States steadily declined from 1975 to 2003; however, mortality rates have remained stable since 2003. The American Cancer Society projects that in 2014, there will be 12,360 new cases of cervical cancer and 4020 cervical cancer-related deaths.2 According to the National Cancer Institute, 40.1% of cervical cancers are diagnosed in women between the ages of 20 and 44 years, specifically 14.3% of cancers are identified in women aged 20 to 34 years, whereas 25.8% are diagnosed between the ages of 35 and 44 years.3 Traditionally, earlystage cervical cancer (stage IA2-IB1) was treated by radical hysterectomy and bilateral pelvic lymphadenectomy, resulting in infertility. Over the last few decades, the average maternal age at first birth has steadily increased across developed nations. In 1970, only 1 of 100 first births was to women aged 35 years and older, whereas in 2006, this number increased to 1 of 12.4 Therefore, an increasing number of nulliparous women who desire future fertility are at risk of cervical cancer, possibility leading to hysterectomy before giving birth.5,6 In 1994, Dargent et al7 introduced radical trachelectomy (RT) as a fertility-sparing option for women with early-stage cervical cancer.8 Since the inception of RT into clinical practice, studies have described similar rates of recurrence (5%) as well as morbidity and mortality when compared with radical hysterectomy, leading to the conclusion that RT is a viable fertilitysparing management option for early-stage cervical cancer.9,10 Although multiple studies report the gynecological and obstetrical outcomes of fertility preservation for appropriately selected early-stage cervical cancer patients,10Y14 little is known about the current practice patterns and opinions of RT among practicing and training gynecologic oncologists. Current literature speculates on a trend toward even more conservative management than RT, specifically pelvic lymphadenectomy with simple hysterectomy or cervical conization, as well as neoadjuvant chemotherapy followed by conservative surgery.14Y17 The purpose of this study was to describe current Society of Gynecologic Oncology (SGO) member practice trends, fellowship training patterns, and opinions concerning the current and future utility of RT.

MATERIALS AND METHODS Approval from the institutional review board was obtained along with the permission of the SGO to obtain a membership list of practicing gynecologic oncologists (practitioners) and gynecologic oncology fellows-in-training (fellows). Two surveys, one to practitioner SGO members in the United States and one to the fellows at board-certified training programs, were sent via the US mail at 3 time points (June, August, and September of 2012). Each survey contained a study identification number to control for duplicate survey responses. The surveys were anonymous and did not contain any identifying information of the practitioner or fellow. The practitioner survey was estimated to take 10 minutes to complete. The fellow survey was estimated to take 7 minutes to complete. Both

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surveys assessed baseline demographics, RT training, and opinions surrounding the future of RT as a cancer management plan for early-stage cervical. In addition, the practitioner survey assessed practice patterns, indications for RT, preferred method of procedure, as well as preoperative, intraoperative, and postoperative management. The 2 survey instruments were analyzed separately, and all unknown or missing responses were removed from the analyses. The survey was designed to accommodate multiple responses to the same question or omission of responses. The survey results were entered into a database at the Department of Institutional Research at The University of Texas MD Anderson Cancer Center. Data were analyzed using SPSS 19.0 for Windows.

RESULTS Demographics There was a 22.4% response rate to the 1353 surveys mailed to SGO practitioners (n = 303) and a 24.4% response rate to the 156 surveys mailed to fellows (n = 38). Practitioner responders were typically male (63.1%), aged 40 to 50 years (32%), from an academic center (42.6%) spread across US regions, and in practice with 1 to 5 faculties (71.6%) (Table 1). Fellows were typically female (71.1%), aged 30 to 40 years (97.4%), from a solely academic center (78.4%), from the northeast United States (43.4%), and in a hospital system with 6 to 10 faculties (44.4%) (Table 2).

Practice Background Half of practitioner respondents (n = 148) report performing an RT with 70.7% (n = 179) reporting 1 or less RTs in the past year. Most practitioners (63.1%) do not anticipate a change in their RT practice over the next 5 years, whereas a small percentage (18.8%) of practitioners plan to increase their RT use, and a few practitioners (14.6%) who do not perform RT expect to begin performing the procedure in the future. Various reasons were documented from practitioners who do not perform an RT (49.8%) such as lack of training (53.4%), patients without medical indication (49.6%), and/or a patient not desiring the procedure (39.1%). Most fellows (83.4%) plan to perform RT at least 2 to 6 times per year after fellowship. Both practitioners (56.1%) and fellows (50%) feel competence and expertise in performing an RT is attained after completion of 2 to 5 procedures annually.

Training Most practitioners (88.0%) and fellows (89.5%) believe that senior fellows should be trained to perform RT. When asked about the necessity of postfellowship training for RT, most practitioners (75.7%) feel additional training should be used, whereas only 26.3% of fellows believe additional training is necessary. Most fellows (76.3%) report that RT is performed at their institution, whereas only 57.9% report that fellows receive specific training in the procedure. Sixty-eight percent of fellows receive specific training for abdominal, 59.1% for robotic, 18.2% for laparoscopic, and 18.2% for vaginal RTs (Table 3). At the majority of institutions (60.7%), RT is performed by only a small number (G25.0%) of the * 2015 IGCS and ESGO




TABLE 1. Demographics of practitioner respondents

1. Practice categorization Academic center Academic and community based Community Other 2. No. attending gynecologic oncologists in your practice None 1Y5 6Y10 11Y20 920 3. Current practice location Midwest Northeast Southeast Southwest West Other 4. Sex Female Male 5. Age, y 30Y40 41Y50 51Y60 61Y70 970

n

%

284 121 81 75 7 282

42.6 28.5 26.4 2.5

32 202 35 12 1 287 60 74 72 35 40 6 282 104 178 285 66 86 83 32 18

11.3 71.6 12.4 4.3 0.4

Role of Radical Trachelectomy in the SGO

(76.8%) feels that RT is indicated for International Federation of Gynecology and Obstetrics stages IA2 to IBI (G2 cm). The grade of cancer is not a determining factor for most practitioners (77.7%). The vast majority indicates that RT is appropriate for squamous carcinoma (98.2%) and adenocarcinoma (71.2%), but only 57.3% feel this procedure is indicated for adenosquamous carcinoma and a minority for clear cell (12.4%), papillary serous (7.7%), neuroendocrine (4.0%), or other histologic subtypes (1.5%). The majority indicates that neoadjuvant chemotherapy is inappropriate management (79.1%) and that lymph vascular space invasion (LVSI) is not a contraindication to RT (79.3%).

Patient Management

20.9 25.8 25.1 12.2 13.9 2.1

Seventy-five percent of responding practitioners offer RT as a treatment option the majority of the time when appropriate. Nearly all fellows (96.7%) plan to discuss RT with patients as a fertility-sparing option for early-stage cervical cancer after completing fellowship. For responding practitioners, positron emission tomography and computed tomography (PET/CT) scan is the preferred preoperative imaging method, used by 71.0% of practitioners over magnetic resonance imaging (MRI) (55.5%). Most practitioners send the cervical specimen for frozen section (78.0%), place an intraoperative cervical cerclage (88.8%), and never perform lymphatic mapping (68.3%).

36.9 63.1

TABLE 2. Demographics of fellow respondents

23.3 30.2 29.1 11.2 6.3

faculty. During the majority of fellow-attended RT cases, 56% of fellows perform greater than half of RT surgery.

Surgical Method Most practitioners perform robotic (47.0%) or abdominal (40.5%) RT, with vaginal (15.8%) and laparoscopic (6.0%) RT being less common. When asked if a practitioner’s self-reported skill level for a specified RT procedure is very good or good, most practitioners endorse this statement for abdominal (67.6%) and robotic (35.1%) RT, whereas the minority does so for vaginal (16.6%) and laparoscopic (12.7%) approaches (Table 3). Some respondents reported multiple surgical approaches for RT.

Patient Indications Nearly all practitioners (92.8%) endorse RT as treatment for early-stage cervical cancer. Most practitioners believe that RT is indicated for women younger than age 30 years (84.4%), and a large proportion (49.8%) feel this is appropriate for ages 36 to 40 years (Table 4). The majority

1. Practice categorization Academic center Academic and community based Community 2. No. attending gynecologic oncologists on faculty 1Y5 6Y10 11Y15 915 3. Current fellowship location Midwest Northeast Southeast Southwest West Other 4. Sex Female Male 5. Age, y 30Y40 41Y50

* 2015 IGCS and ESGO


n

%

37 29 7 1 36

78.4 18.9 2.7

12 16 2 6 37 6 16 5 4 5 1 38 27 11 38 37 1

33.3 44.4 5.6 16.7 16.2 43.3 13.5 10.8 13.5 2.7 71.1 28.9 97.4 2.6

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TABLE 3. Selected survey responses for practitioners and fellows

1. RT approach for practitioners Robotic Abdominal Vaginal Laparoscopic 2. Practitioner skill assessment (very good/good) of performing specified RT procedures Abdominal Robotic Vaginal Laparosopic 3. Fellow RT training by specific procedure Abdominal Robotic Laparoscopic Vaginal 4. Fellows preferred methods of performing RT Robotic Abdominal Vaginal Laparoscopic

n

%*

215 101 87 34 13 225Y234†

47.0 40.5 15.8 6.0

135 79 38 29 22

83.9 64.7 41.3 38.2

15 13 4 4 31

68.2 59.1 18.2 18.2

22 18 5 5

71.0 58.5 16.1 16.1

*Percentages are based on the number of participants responding to each questions; some participants marked multiple answers. †Varying numbers of total responses were received for each type of RT.

Approximately half of practitioners routinely (975% of time) preserve the uterine arteries. Postoperatively, the most commonly reported complications are neocervical stenosis (37.3%), lymphocysts (14.5%), amenorrhea (11.0%), and infection (5.1%).

Future Directions The majority of both practitioners (77.3%) and fellows (89.5%) feel RT will have a lasting role in gynecologic oncology. Fellows plan to practice robotic RT (71.0%) and abdominal RT (58.1%) after completing their fellowship training (Table 3). Most practitioners (72.1%) and fellows (60.4%) also believe that in the next 5 years, there will be a role for less ‘‘radical’’ procedures than RT in the management of early-stage cervical cancer.

DISCUSSION Early-stage cervical cancer can be successfully managed with RT; however, our data indicate that only half of responding gynecologic oncologists perform the procedure.

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Most practitioners endorse RT as a treatment for patients younger than the age of 30 years, stages IA2 to IBI with lesions smaller than 2 cm, squamous carcinoma and adenocarcinoma, and that grade is not a limiting factor. Furthermore, most agreed

TABLE 4. Practitioner responses about patient indications for RT n 1. RT ideally indicated in this age group, y G30 30Y35 36Y40 41Y45 46Y50 Age is not a factor Other 2. Role of RT in FIGO cancer stages IAI with LVSI IA2 only IA2-IBI (G2 cm) IA2-IBI (G4 cm) IIA Other 3. Role of RT in cervical cancer grades Grade 1 Grade 2 Grade 3 Grade is not a factor Other 4. Role of RT in histologic subtypes Adenocarcinoma Adenosquamous Clear cell Neuroendocrine Papillary serous Squamous Other 5. LVSI is a contraindication to RT Yes No 6. Role of neoadjuvant chemotherapy in early-stage cervical cancer Never IBI 92 cm IB2 IIA

269 227 200 134 23 4 35 24 272 76 101 209 23 3 10 273 55 40 8 212 273 274 195 157 34 11 21 269 4 266 55 211 258 204 37 23 10

%* 84.4 74.3 49.8 8.6 1.5 13.0 8.9 27.9 37.1 76.8 8.5 1.1 3.7 20.1 14.7 2.9 77.7 3.7 71.2 57.3 12.4 4.0 7.7 98.2 1.5 20.7 79.3

79.1 14.3 8.9 3.9

*Percentages are based on the number of participants responding to each questions; some participants marked multiple answers. FIGO, International Federation of Gynecology and Obstetrics.





that neoadjuvant chemotherapy is inappropriate management and that LVSI is not a contraindication to treatment. The most common surgical approach reportedly performed by practitioners and fellows was the robotic approach. Current practitioners who do not perform RT most frequently cite the reasons of training and patients without proper indication for the procedure. Furthermore, for those practitioners who do perform RT, the majority performs no more than 1 case annually. Interestingly, practitioners and fellows endorse that 2 to 5 annual cases are necessary to maintain expertise. Despite this discrepancy, practitioners do not foresee increasing their case numbers, and the training of fellows remains limited. Our survey data note a lack of consensus regarding indications for RT, which could lead practitioners to overlook appropriate candidates. Eligibility criteria for RT were published in 1998 that included desire to maintain fertility, age younger than 40 years, no evidence of impaired infertility, stage IA2 to IBI, lesion size smaller than 2 cm, squamous or adenocarcinoma histology, and absence of high-risk histology.18 Support of and adjustments to the original criteria arose as new data was uncovered. Our results indicate that most practicing physicians still abide by the original guidelines. Current literature supports reinforcing the initial age criteria. Only half of practitioners endorse RT in women aged 36 to 40 years. Age has not been associated with increased risk of recurrence or worsened oncological outcomes after RT.19,20 In addition, post-RT conception rates of women aged 20 to 40 years ranges from 40% to 70%.11,21,22 Therefore, we recommend that women should not be excluded from RT consideration solely based on age older than 35 years. Adjustment of previous RT guidelines involves the use of neoadjuvant chemotherapy and treatment of IB1 lesions measuring 2 to 4 cm. Lanowska et al23 in 2014 reported only 1 recurrence in a 23-month follow-up time after 2 to 3 cycles of paclitaxel, ifosfamide, and cisplatin followed by radical vaginal trachelectomy in 18 patients with tumor sizes of 2.1 to 5 cm and negative lymph nodes. A recent study suggests that patients with lesions larger than 2 cm may be candidates for RT if their lesion is very exophytic and has minimal stromal invasion.24 In another retrospective review of 29 patients with tumors measuring 2 to 4 cm, 9 patients underwent fertilitysparing procedure with only 1 recurrence over 44 months.25 Vercellino et al26 followed patients with stage I cervical cancer larger than 2 cm in diameter with negative pelvic and para-aortic lymph nodes who received neoadjuvant chemotherapy followed by vaginal RT. A total of 18 patients were eligible for the study. Twelve women (67%) were diagnosed with metastasis in 1 or more lymph nodes, and thus received primary chemoradiation. Six women (33%) underwent neoadjuvant chemotherapy and radical vaginal trachelectomy. Three patients had a complete response, and 3 patients showed more than 50% tumor size reduction. All 6 women were free of recurrent disease after 30.6 months.26 Currently, this data is experimental and has yet to be adopted into routine practice, but requires further investigation. Several categories of the survey results mirror current findings within the literature, including use of frozen section, cerclage placement, and postoperative complications.11,22,27


Other responses deviate from the current literature and include preoperative image assessment, uterine artery preservation, and lymphatic mapping. More practitioners use PET/ CT imaging instead of MRI. The literature has inconsistent results regarding the sensitivity of 1 modality over another, with some studies favoring MRI, whereas others favor PET/ CT.28,29 Other studies have showed that PET/CT has no correlation with recurrence and is associated with significant additional cost, whereas an MRI can effectively identify highrisk patients who will likely need a radical hysterectomy30Y32 with less associated cost. A recent review by Noel et al33 demonstrated how MRI accurately depicts the criteria necessary for determining whether a patient is an ideal candidate for RT. In our institution, the imaging modality of choice for the preoperative evaluation of patients scheduled to undergo RT is pelvic MRI. Uterine artery preservation is thought to benefit future fertility by retaining a greater portion of the uterine blood supply, but has yet to be widely integrated in clinical treatment.34,35 Most practitioners currently do not perform lymphatic mapping, despite the fact that it may avoid a complete pelvic lymph node dissection that results in lymphocysts and lymphedema following 6% to 20% of cases.36,37 This finding may be attributed to the fact that only 42.6% of respondents were from academic centers where lymphatic mapping and sentinel node identification may be more commonly performed. Continued research is needed to determine the clinical significance of uterine artery preservation, and lymphatic mapping should be considered in all patients. Despite the projected lasting use of RT, most practitioners and fellows believe that more conservative approaches to early-stage cervical cancer will emerge within the next 5 years. This aligns with current prospective trials evaluating the role of conization, simple trachelectomy, or simple hysterectomy for management of low-risk early-stage cervical cancer.38 One such study is the ConCerv, which is a multiinstitutional prospective trial investigating conservative treatment for women with IA2 or IB1 disease, squamous carcinoma (all grades), adenocarcinoma (grade 1 and 2), and tumor size less than or equal to 2 cm.39 Data from the ConCerv trial and other ongoing prospective trials, including SHAPE and GOG 278, have the potential to influence the current opinions and management plan for low-risk early-stage cervical cancer.40,41 However, currently, RT remains an important option for management option. In situations where practitioners are not comfortable or able to perform RT, due to lack of training or insufficient annual cases, referral to a high volume RT center should be considered. Limitations of our study include the following: sample selection bias as the group was only identified via SGO membership status and fellows at board-certified training programs during the specified time frame; there was a low survey response rate from both groups; the survey relied on participant recall, which may present a bias to actual occurrences; the survey was voluntary, so there is potential that those that completed the survey may respond differently than those that did not; and some SGO members indicated in the comments that they were not practicing gynecological oncologists. Based on these limitations, it is difficult to fully generalize these findings to all gynecologic oncologists.



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The future role of RT in the treatment of early-stage cervical cancer is unknown. The results of this survey suggest that the gynecologic oncology community recognizes the importance of RT in current and future practice. Future studies and collaborations are encouraged to consider conservative surgery in low-risk patients with early-stage cervical cancer. We strongly suggest that patients considered for RT be referred to high-volume centers to optimize oncologic and obstetrical outcomes.

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38. Ramirez PT, Pareja R, Rendo´n GJ, et al. Management of low-risk early-stage cervical cancer: should conization, simple trachelectomy, or simple hysterectomy replace radical surgery as the new standard of care? Gynecol Oncol. 2014;132:254Y259. 39. Schmeler KM, Frumovitz M, Ramirez PT. Conservative management of early stage cervical cancer: is there a role for less radical surgery? Gynecol Oncol. 2011;120:321Y325. 40. Plante M, The SHAPE Trial. Available at: http:// www.gcig.igcs.org/Spring2012/2012_june_shape_trial.pdf. 41. Covens A, GOG Protocol 278. Available at: http://www.gcic.igcs.org/Spring2012/2012_june_cervix_ cacner_committee.pdf.



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