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Original research
Surveillance patterns of cervical cancer patients treated with conization alone
  1. Silvana Pedra Nobre1,
  2. Varvara Mazina2,
  3. Alexia Iasonos3,
  4. Qin C Zhou3,
  5. Yukio Sonoda1,
  6. Ginger Gardner1,
  7. Kara Long-Roche1,
  8. Mario M Leitao1,
  9. Nadeem R Abu-Rustum1 and
  10. Jennifer J Mueller1
  1. 1 Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York, USA
  2. 2 Obstetrics and Gynecology, University of Washington, Seattle, Washington, USA
  3. 3 Epidemiology-Biostatistics, Memorial Sloan Kettering Cancer Center, New York, New York, USA
  1. Correspondence to Dr Jennifer J Mueller, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA; muellerj{at}mskcc.org

Abstract

Objectives To determine surveillance patterns of stage I cervical cancer after cervical conization.

Methods A 25-question electronic survey was sent to members of the Society of Gynecologic Oncology. Provider demographics, surveillance during year 1, years 1–3, and >3 years after cervical conization, use of pelvic examination, cytology, Human papillomavirus testing, colposcopy, and endocervical curettage were queried. Data were analyzed.

Results 239/1175 (20.1%) responses were collected over a 5-week study period. All providers identified as gynecologic oncologists. During year 1, 66.7% of providers perform pelvic examination and 37.1% perform cytology every 3 months. During years 1–3, 61.6% perform pelvic examination and 46% perform cytology every 6 months. At >3 years, 54.4% perform pelvic examination every 6 months and 43% perform annual pelvic examination. 66.7% of respondents perform cytology annually, and 51.9% perform annual Human papilloma virus testing. 85% of providers do not offer routine colposcopy and 60% do not offer endocervical curettage at any point during 5-year follow-up. 76.3% of respondents screen patients for Human papilloma virus vaccination.

Conclusions To date, there are no specific surveillance guidelines for patients with stage I cervical cancer treated with cervical conization. The most common surveillance practice reported is pelvic examination with or without cytology every 3 months in year 1 and every 6 months thereafter. However, wide variation exists in visit frequency, cytology, and Human papillomavirus testing, and there is a clear trend away from using colposcopy and endocervical curettage. These disparate surveillance practices indicate a need for well-defined, uniform surveillance guidelines.

  • cervical cancer
  • surgical oncology
  • surgical procedures, operative

https://doi.org/10.1136/ijgc-2020-001338

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    HIGHLIGHTS

    • First national survey on surveillance patterns in stage I cervical cancer after conization

    • Highlights trends in surveillance patterns among gynecologic oncologists across the United States

    • Frequency of Human papilloma virus screening varies: 25% of providers do not offer it

    Introduction

    Fertility-sparing treatment is recognized as a feasible conservative approach in patients with early-stage cervical cancer, and an alternative for women wishing future pregnancy.1–3 Uniform guidelines on surveillance following fertility-sparing treatment of early-stage disease focus on patients who have undergone trachelectomy.4 However, specific practice recommendations for surveillance of those treated by cervical conization are lacking.

    The current National Comprehensive Cancer Network (NCCN) Guidelines provide recommendations for surveillance of early-stage cervical cancer, distinguishing patients undergoing fertility-sparing surgery from those undergoing definitive surgery.4 These guidelines include history and physical examination every 3–6 months for 2 years, every 6–12 months for 3–5 years, and then annually, based on the patient’s risk of recurrence. Cervical or vaginal cytology is recommended annually. There is no recommendation for Human papillomavirus (HPV) screening. Imaging is recommended as indicated, based on symptoms or examination findings suspicious for recurrence. However, current surveillance guidelines do not distinguish women undergoing cervical conization from those undergoing trachelectomy.

    In 2017, the Society of Gynecologic Oncology released a Society Position Statement updating recommendations on post-treatment surveillance and diagnosis of recurrence in gynecologic malignancies.5 It states that surveillance should focus on recurrent disease amenable to treatment, resulting in cure or long-term survival. In cervical cancer, surveillance focuses predominantly on locoregional recurrence. History and physical examination are the only consistent methods reported for detecting recurrence.5 If recurrence is suspected, imaging is recommended. Biopsy should be obtained before definitive radiation or exenteration. While HPV persistence is likely a risk factor for recurrence, routine HPV testing has not been studied sufficiently to recommend it in surveillance.5

    We surveyed gynecologic oncologists in the United States regarding their practice patterns in surveillance of patients with stage I cervical cancer treated with cervical conization. Our goal was to better characterize current practice patterns and identify variations. We also reviewed published trials evaluating surveillance patterns following conservative surgery for early-stage disease. We hypothesize that there is a need for more specific practice guidelines for surveillance in this setting.

    Methods

    After approval from our Institutional Review Board, we created a 25-question electronic survey using the REDCap platform (online supplementary appendix A). This includes questions regarding provider demographics, surveillance methods, and general clinical management during the first year (year 1), years 1–3, and >3 years following cervical conization (either cold knife cone or loop electrosurgical excision procedure). Surveillance methods include pelvic examination, cervical cytology, HPV screening, colposcopy, and endocervical curettage regardless of Papanicolaou (Pap) smear result. With permission from the Society of Gynecologic Oncology, we acquired a list of United States-based, full-time members. An email describing our project and containing a hyperlink to the REDCap survey was sent to all members. Two follow-up emails were sent over a 5-week period. The survey was open from March 11, 2019 to April 22, 2019. Data were then analyzed.

    Supplemental material

    We searched the National Center for Biotechnology Information database for relevant citations regarding cervical cancer surveillance after fertility-sparing treatment. We performed keyword searches combining disease-specific terms (eg, cervical cancer) with treatment-specific terms (eg, trachelectomy, conization, fertility-sparing). We limited our search to English language studies and did not limit results by date. We searched the United States National Institutes of Health clinical trial registry at ClinicalTrials.gov to identify ongoing trials.6 This was supplemented by hand-searching reference lists of key papers for relevant citations.

    Statistical analysis

    Descriptive summary statistics were applied to describe the cohort of respondents. We applied Fisher’s exact test to compare surveillance methods, patterns between different practice types, and different number of years post-fellowship training. Fisher’s exact test was used to identify differences in frequencies of a surveillance practice among groups. The tests were performed separately within each time period (year 1, years 1–3,>3 years). Descriptive plots were generated for review of the data, based on frequency of surveillance methods.

    Results

    We surveyed a total of 1381 Society of Gynecologic Oncology members: 1175 (85%) identified as gynecologic oncologists. 239 members responded: 238 identified as gynecologic oncologists (overall response rate, 20.1%). Two providers were excluded: one identified as a gynecologic oncologist but did not perform cervical conization for stage I cervical cancer, the other identified as a gynecologic pathologist.

    Demographics

    237 providers were included in the final analysis: 232 (98%) identified as gynecologic oncologists, 5 (2%) did not provide a response. Table 1 describes participant demographics. 138 gynecologic oncologists (58%) identified their practice setting as academic, 77 (32%) as private, and 22 (9%) as “other” (Table 1). 26% of respondents had graduated from fellowship training within the past 5 years; 21% were 6–10 years' post-graduation; 14%, 10–15 years' post-graduation; and 39%, >15 years' post-graduation. 32% of respondents practice in the South, 21% the Mid-Atlantic, 19% the West, 19% Midwest, and 9% New England.

    View this table:
    Table 1

    Provider demographics

    Overall surveillance methods and patterns

    Patterns of surveillance methods are shown in Table 2 and Figure 1. In year 1 after cervical conization, 66.7% of respondents perform pelvic examination and 37.1% perform cytology every 3 months, 32.9% perform pelvic examination and 33.3% cytology every 6 months, 28.7% perform cytology annually; 27.4% do not perform HPV testing during year 1, 26.2% perform HPV testing annually, 24.9% every 6 months; 85.7% do not perform colposcopy during year 1; and 49.4% do not perform endocervical curettage.

    View this table:
    Table 2

    Overall surveillance methods

    Figure 1
    Figure 1

    Surveillance patterns in stage I cervical cancer after cervical conization: year 1, years 1–3, and >3 years.

    In years 1–3, 61.6% perform pelvic examination and 46% perform cytology every 6 months; 6.3% perform annual pelvic examination, 40.5% annual cervical cytology; 35.4% perform HPV testing annually, 26.2% every 6 months, 27% do not perform HPV testing during years 1–3; 85.2% do not perform colposcopy; and 57.8% do not perform endocervical curettage at any time during years 1–3.

    At >3 years, 54.4% perform pelvic examination every 6 months; 43% perform annual pelvic examination; 66.7% perform annual cervical cytology; and 51.9% perform annual HPV testing. 86.9% do not perform colposcopy, 72.6% do not perform endocervical curettage.

    General clinical management

    79.3% of respondents reported no age limit for fertility-sparing surgery at their institutions. Of those who did report an age limit, 6.7% identified 40, 4.6% identified 45, and 2.1% identified 43 years as the upper limit, respectively. 43.8% report <10% of their patients of reproductive age undergo fertility-sparing surgery for stage I cervical cancer, 23.6% report 10%–25% undergo fertility-sparing surgery, 16% report 25%–50% undergo fertility-sparing surgery, 8.8% report 50%–75% undergo fertility-sparing surgery, and 7.1% report >75% undergo fertility-sparing surgery for stage I cervical cancer.

    We asked respondents to specify when they offer or recommend completion hysterectomy for patients initially treated with cervical conization alone. 62.2% offer hysterectomy after completion of childbearing; 73.3% on detection of invasive carcinoma; 44% to patients with persistent HPV infection or high-grade squamous intraepithelial lesion cytology; 69% when positive margins are found on repeat cone biopsy; 34.7% when a new lesion is detected on imaging; and 60% on patient request alone. More than 90% offer no routine imaging after cervical conization, 5.4% offer positron emission tomography/CT scans yearly.

    We evaluated practice patterns with respect to HPV vaccination, contraceptive counseling, and referral to generalist obstetrician-gynecologists for routine gynecologic care. 76.3% of respondents report screening patients for routine HPV vaccination, 65.9% offer to complete the vaccination series. 72.5% follow patients for 5 years after cervical conization before discharging them to generalist obstetrician-gynecologists. 80% counsel patients on contraception. 40% recommend pregnancy no earlier than 6 months, 29% no earlier than 1 year after cervical conization.

    Comparison between academic and private practice gynecologic oncologists

    We compared surveillance patterns between academic and private practice gynecologic oncologists. We found no statistically significant differences between these groups with respect to frequency of surveillance methods throughout all three time periods. We noticed trends among both groups similar to trends in the overall group analysis (Figure 2). The majority of academic (66.4%) and private practice (74%) respondents perform physical examination every 3 months during year 1, every 6 months during years 1–3 (64.9% and 63.4%, academic and private practice physicians, respectively), and every 6–12 months at >3 years. Use of cytology followed a similar pattern: in year 1, the majority of academic (37.2%) and private practice (45.5%) physicians perform cytology every 3 months; during years 1–3, 47.8% academic and 53.3% private practice physicians perform cytology every 6 months; and 40.4% academic and 33.3% private practice physicians perform annual cytology. At >3 years, 66.9% of academic and 61.8% of private practice physicians perform annual cytology, 31.6% academic and 36.8% private practice physicians perform cytology every 6 months. HPV screening patterns vary: however, no statistically significant difference was found between the two cohorts (Figure 2). At >3 years, 56% of academic and 53.3% of private practice physicians perform annual HPV screening. During all time intervals, neither routine colposcopy nor endocervical curettage are performed by most respondents in either cohort.

    Figure 2
    Figure 2

    Comparison of surveillance methods between academic and private practice gynecologic oncologists.

    Comparison between number of years from fellowship training

    We analyzed whether number of years from completion of fellowship training influenced frequency of surveillance (Figure 3). There was a statistically significant difference between recently graduated gynecologic oncologists and those >10 years' post-fellowship training. During year 1, fewer recently trained respondents perform pelvic examinations every 3 months (57.3%), compared with 75.2% of those >10 years' post-fellowship (P=0.004). Frequency of cervical cytology differed between the two groups throughout all surveillance time periods: 43.6%, 61.8%, and 80.6% of recently graduated practitioners perform annual Pap smears during year 1, years 1–3, and >3 years, respectively, compared with those >10 years' post-fellowship: 16.1%, 23.1%, and 57.3% during year 1, years 1–3, and >3 years, respectively (P<0.001).

    Figure 3
    Figure 3

    Comparison of surveillance methods between gynecologic oncologists<10 years from fellowship and gynecologic oncologists>10 years from fellowship.

    Frequency of HPV screening varied across all time intervals, showing a statistically significant difference between respondents<10 years vs those >10 years' post-fellowship: 38.1% of recently graduated practitioners perform HPV screening annually during year 1, 51% perform annual screening during years 1–3, 63.7% perform annual screening at >3 years; 27.6% of those >10 years' post-fellowship perform HPV screening every 6 months during year 1; 33.6% perform HPV screening every 6 months during years 1–3; and 50% perform annual HPV screening at >3 years (P=0.006). There was no significant difference in colposcopy and endocervical curettage practice patterns between the two groups (P=0.6 and P=0.2, respectively).

    Discussion

    We describe surveillance methods used by gynecologic oncologists in patients undergoing cervical conization for stage I cervical cancer in the United States. After data analysis, patterns emerged in the frequency of use of surveillance tools and timing of surveillance. In year 1, there was a trend toward pelvic examination and cervical cytology every 3 months. As more time elapsed, frequency of pelvic examination and cytology decreased: most respondents reported using these every 6 months during years 1–3, then annually at >3 years. Neither routine colposcopy nor endocervical curettage were performed during any time period by most of the respondents.

    In terms of frequency and time interval, HPV screening varied most. Trends are based solely on provider preference: NCCN Guidelines do not offer recommendations for HPV screening. This wide variation merits a closer look, indicating a need for guidelines regarding frequency of HPV testing in surveillance of these patients.

    The respondents perform surveillance at time intervals mostly coinciding with NCCN Guidelines. In our survey, however, respondents perform pelvic examination and cytology more frequently than the NCCN Guidelines recommend: 66% perform pelvic examination every 3 months during year 1, 66% every 6 months during years 1–3. Annual cytology, as recommended by the NCCN, is performed by most only at >3 years: most perform cytology every 3 or 6 months in years 1–3 (online supplementary figure 1). Interestingly, physicians>10 years' post-fellowship performed surveillance more frequently than recent graduates: this may reflect either a training pattern or anecdotal bias. These findings highlight a need to tailor surveillance guidelines and also suggest an opportunity for continued education of modern screening practices in the setting of early-stage cervical cancer initially treated with cervical conization alone.

    Supplemental material

    The published findings of prospective trials evaluating the feasibility of conservative treatment of low-risk, early-stage cervical cancer, are summarized chronologically in online supplementary table S1. Thirteen prospective trials published during and after 2000 were identified.2 7–18 Most patients had stage IB1 disease, although many trials also included patients with stage IA1 with or without lymphovascular invasion, and stage IA2 disease. Eight trials (61%) offered cone biopsy, others included either simple trachelectomy or trachelectomy with parametrectomy. In all but one trial,7 pelvic lymph node dissection was part of the surgical procedure.

    Supplemental material

    Four of the 13 trials did not reference a surveillance methodology. In those that did, the most common included pelvic examination and cervical cytology at 3- to 4-month intervals for the first 1–2 years, and every 6–12 months thereafter. Colposcopy and biopsies were performed based on abnormal results. Four of the 13 trials utilized routine colposcopy. Three of the 13 trials used routine endocervical curettage at the time of cytologic assessment, without colposcopy. Only one trial routinely screened patients for HPV DNA and recommended HPV vaccination to all participants. One trial described routine MRI at 6, 12, and 24 months.12 Overall, the variety of surveillance modalities and follow-up intervals highlights lack of a consistent surveillance strategy among specialists caring for this patient population.

    There are currently three prospective trials examining the role of conservative surgery in early-stage cervical cancer: GOG 278, SHAPE, and ConCerv. ConCerv is a single-arm, international trial evaluating the safety and feasibility of conservative management (either conization for patients desiring fertility, or simple hysterectomy for those who do not) in stage IA2–IB1 cervical cancer.19 All patients are followed with pelvic examination and cervical cytology every 3 months for 2 years, and to date show a low recurrence rate of 4.3%.19 Although follow-up is not yet complete, this may potentially propagate the use of conservative surgery in the treatment of early-stage cervical cancer. However, this further emphasizes the need for specific, uniform surveillance guidelines after cervical conization.

    Our study is the first nationwide survey on surveillance patterns for patients with stage I cervical cancer treated with cervical conization. Society of Gynecologic Oncology practice surveys published in the past 5 years have reported response rates ranging from 10% to 43%. Our overall response rate of 20% is, therefore, comparable. Our study does have some limitations. Although the response rate is comparable to that of prior published surveys, this may limit its ability to generalize the conclusions to all gynecologic oncologists. It may also be subject to selection bias, as only Society of Gynecologic Oncology members were recruited. Patient population type (ie, urban, suburban, or mixed) could potentially influence responses and practice patterns. To address this, a sub-analysis was done and demonstrated that patient population type was not associated with differences in practice patterns. It is also possible that some questions in the survey may not have elicited accurate responses.

    The United States has among the lowest number of cases of advanced-stage cervical cancer in the world, due to widespread use of the revolutionizing Pap test and access to preventive medical care. In countries with a high use of HPV vaccines (Gardasil, Cervarix, etc.) there has been a significant decrease in rates of cervical dysplasia, genital warts, and cervical cancer:20 the overall incidence in all women has decreased almost 60% over the past 35 years.21 However, most cases of newly diagnosed cervical cancers are in women of childbearing age.21 Although its overall incidence continues to decrease in the United States, it remains the second most common cause of cancer-related deaths in women worldwide.22

    Care is enhanced when gynecologic oncologists use clear and uniform surveillance guidelines for patients with early-stage disease wishing to preserve their fertility. The goal of surveillance is to identify new or recurrent disease earlier, so it can be treated appropriately and, if possible, with fertility-sparing surgery. This should be balanced with the goal of minimizing invasive examinations, procedures, and tests. Some patients may become confused and anxious if they are not undergoing a certain test routinely but see that others are. Updating treatment guidelines will facilitate more uniform retrospective studies of oncologic outcomes and provide data demonstrating which surveillance methods and timing of examinations yields the most efficient detection of new or recurrent disease.

    This study provides a current snapshot of surveillance methods used by gynecologic oncologists in the United States, and the frequency of use. This unique insight and its comparison with standing guidelines, highlights the need for clarification regarding the use of certain surveillance methods, including HPV screening. It may serve as a partial basis for the creation of a blueprint for uniform surveillance in this unique patient population.

    References

    1. ↵
      2. Wright JD ,
      3. NathavithArana R ,
      4. Nathavithrana R , et al
      . Fertility-conserving surgery for young women with stage IA1 cervical cancer: safety and access. Obstet Gynecol 2010;115:585–90.doi:10.1097/AOG.0b013e3181d06b68 pmid:http://www.ncbi.nlm.nih.gov/pubmed/20177290
      OpenUrlPubMed
    2. ↵
      2. Yahata T ,
      3. Nishino K ,
      4. Kashima K , et al
      . Conservative treatment of stage IA1 adenocarcinoma of the uterine cervix with a long-term follow-up. Int J Gynecol Cancer 2010;20:1063–6.doi:10.1111/IGC.0b013e3181e768b6 pmid:http://www.ncbi.nlm.nih.gov/pubmed/20683418
      OpenUrlAbstract/FREE Full Text
    3. ↵
      2. Cui RR ,
      3. Chen L ,
      4. Tergas AI , et al
      . Trends in use and survival associated with fertility-sparing trachelectomy for young women with early-stage cervical cancer. Obstet Gynecol 2018;131:1085–94.doi:10.1097/AOG.0000000000002613 pmid:29742670
      OpenUrlPubMed
    4. ↵
      2. Koh W-J ,
      3. Greer BE ,
      4. Abu-Rustum NR , et al
      . Cervical cancer, version 2.2015. J Natl Compr Canc Netw 2015;13:395–404.doi:10.6004/jnccn.2015.0055 pmid:http://www.ncbi.nlm.nih.gov/pubmed/25870376
      OpenUrlAbstract/FREE Full Text
    5. ↵
      2. Salani R ,
      3. Khanna N ,
      4. Frimer M , et al
      . An update on post-treatment surveillance and diagnosis of recurrence in women with gynecologic malignancies: Society of Gynecologic Oncology (SGO) recommendations. Gynecol Oncol 2017;146:3–10.doi:10.1016/j.ygyno.2017.03.022 pmid:28372871
      OpenUrlPubMed
    6. ↵
      1. NIH
      . U.S. National library of medicine. Available: https://clinicaltrials.gov/ct2/results?cond=Cervical+Cancer&term=conservative+surgery&cntry=&state=&city=&dist= [Accessed 11 Jan 2019].
    7. ↵
      2. Schorge JO ,
      3. Lee KR ,
      4. Sheets EE
      . Prospective management of stage IA(1) cervical adenocarcinoma by conization alone to preserve fertility: a preliminary report. Gynecol Oncol 2000;78:217–20.doi:10.1006/gyno.2000.5857 pmid:http://www.ncbi.nlm.nih.gov/pubmed/10926806
      OpenUrlCrossRefPubMed
    8. ↵
      2. Landoni F ,
      3. Parma G ,
      4. Peiretti M , et al
      . Chemo-conization in early cervical cancer. Gynecol Oncol 2007;107:S125–6.doi:10.1016/j.ygyno.2007.07.011 pmid:http://www.ncbi.nlm.nih.gov/pubmed/17727935
      OpenUrlCrossRefPubMedWeb of Science
    9. ↵
      2. Rob L ,
      3. Pluta M ,
      4. Strnad P , et al
      . A less radical treatment option to the fertility-sparing radical trachelectomy in patients with stage I cervical cancer. Gynecol Oncol 2008;111:S116–20.doi:10.1016/j.ygyno.2008.07.021 pmid:http://www.ncbi.nlm.nih.gov/pubmed/18725167
      OpenUrlCrossRefPubMedWeb of Science
    10. ↵
      2. Maneo A ,
      3. Sideri M ,
      4. Scambia G , et al
      . Simple conization and lymphadenectomy for the conservative treatment of stage IB1 cervical cancer. an Italian experience. Gynecol Oncol 2011;123:557–60.doi:10.1016/j.ygyno.2011.08.009 pmid:http://www.ncbi.nlm.nih.gov/pubmed/21907396
      OpenUrlCrossRefPubMed
    11. ↵
      2. Fagotti A ,
      3. Gagliardi ML ,
      4. Moruzzi C , et al
      . Excisional cone as fertility-sparing treatment in early-stage cervical cancer. Fertil Steril 2011;95:1109–12.doi:10.1016/j.fertnstert.2010.11.010 pmid:http://www.ncbi.nlm.nih.gov/pubmed/21122837
      OpenUrlPubMed
    12. ↵
      2. Palaia I ,
      3. Musella A ,
      4. Bellati F , et al
      . Simple extrafascial trachelectomy and pelvic bilateral lymphadenectomy in early stage cervical cancer. Gynecol Oncol 2012;126:78–81.doi:10.1016/j.ygyno.2012.04.004 pmid:http://www.ncbi.nlm.nih.gov/pubmed/22487540
      OpenUrlCrossRefPubMed
    13. ↵
      2. Raju SK ,
      3. Papadopoulos AJ ,
      4. Montalto SA , et al
      . Fertility-sparing surgery for early cervical cancer – approach to less radical surgery. Int J Gynecol Cancer 2012;22:311–7.doi:10.1097/IGC.0b013e3182370f51 pmid:22237381
      OpenUrlAbstract/FREE Full Text
    14. ↵
      2. Biliatis I ,
      3. Kucukmetin A ,
      4. Patel A , et al
      . Small volume stage 1B1 cervical cancer: is radical surgery still necessary? Gynecol Oncol 2012;126:73–7.doi:10.1016/j.ygyno.2012.03.041 pmid:http://www.ncbi.nlm.nih.gov/pubmed/22465521
      OpenUrlPubMed
    15. ↵
      2. Plante M ,
      3. Gregoire J ,
      4. Renaud M-C , et al
      . Simple vaginal trachelectomy in early-stage low-risk cervical cancer: a pilot study of 16 cases and review of the literature. Int J Gynecol Cancer 2013;23:916–22.doi:10.1097/IGC.0b013e3182954ddf pmid:http://www.ncbi.nlm.nih.gov/pubmed/23669441
      OpenUrlAbstract/FREE Full Text
    16. ↵
      2. Sopracordevole F ,
      3. Chiossi G ,
      4. Barbero M , et al
      . Surgical approach and long-term clinical outcome in women with microinvasive cervical cancer. Anticancer Res 2014;34:4345–9.pmid:http://www.ncbi.nlm.nih.gov/pubmed/25075069
      OpenUrlAbstract/FREE Full Text
    17. ↵
      2. Andikyan V ,
      3. Khoury-Collado F ,
      4. Denesopolis J , et al
      . Cervical conization and sentinel lymph node mapping in the treatment of stage I cervical cancer: is less enough? Int J Gynecol Cancer 2014;24:113–7.doi:10.1097/IGC.0000000000000034 pmid:http://www.ncbi.nlm.nih.gov/pubmed/24335661
      OpenUrlAbstract/FREE Full Text
    18. ↵
      2. Rizzuto I ,
      3. MacNab W ,
      4. Nicholson R , et al
      . Less radical surgery for women with early stage cervical cancer: our experience on radical vaginal trachelectomy and laparoscopic pelvic lymphadenectomy. Gynecol Oncol Rep 2019;28:65–7.doi:10.1016/j.gore.2019.03.005 pmid:http://www.ncbi.nlm.nih.gov/pubmed/30911594
      OpenUrlPubMed
    19. ↵
      2. Schemeler K ,
      3. Paraeja R ,
      4. Lopez A , et al
      . ConCerv: a prospective trial of conservative surgery for low-risk early stage cervical cancer. IGCS19-0750. Int J Gynecol Cancer 2019;29:A14–15.
      OpenUrlAbstract/FREE Full Text
    20. ↵
      2. Bogani G ,
      3. Leone Roberti Maggiore U ,
      4. Signorelli M , et al
      . The role of human papillomavirus vaccines in cervical cancer: prevention and treatment. Crit Rev Oncol Hematol 2018;122:92–7.doi:10.1016/j.critrevonc.2017.12.017 pmid:http://www.ncbi.nlm.nih.gov/pubmed/29458794
      OpenUrlPubMed
    21. ↵
      1. NIH
      . National Cancer Institute Surveillance, Epidemiology, and End Results Program. cancer STAT facts: cervical cancer. Available: https://seer.cancer.gov/statfacts/html/cervix.html [Accessed 11 Jan 2019].
    22. ↵
      1. NIH
      . Research portfolio online reporting tools (report). cervical cancer. Available: https://archives.nih.gov/asites/report/09-09-2019/report.nih.gov/nihfactsheets/ViewFactSheet28c7.html?csid=76&key=C#C [Accessed 11 Jan 2019].

    Footnotes

    • Twitter @leitaomd

    • Contributors Silvana Pedra Nobre: conception and design; analysis and interpretation of data; drafting of article; revising article critically for important intellectual content; final approval of version to be published; agrees to be accountable for all aspects of the work. Varvara Mazina: conception and design; analysis and interpretation of data; drafting of article; final approval of version to be published; agrees to be accountable for all aspects of the work. Alexia Iasonos: analysis and interpretation of data; drafting of article; final approval of version to be published; agrees to be accountable for all aspects of the work. Qin C. Zhou: analysis and interpretation of data; final approval of version to be published; agrees to be accountable for all aspects of the work.Yukio Sonoda: Interpretation of data; revising article critically; final approval of version to be published; agrees to be accountable for all aspects of the work. Ginger J. Gardner: interpretation of data; revising article critically; final approval of version to be published; agrees to be accountable for all aspects of the work. Kara Long Roche: interpretation of data; revising article critically; final approval of version to be published; agrees to be accountable for all aspects of the work. Mario M. Leitao, Jr.: interpretation of data; revising article critically; final approval of version to be published; agrees to be accountable for all aspects of the work. Nadeem R. Abu-Rustum: interpretation of data; revising article critically; final approval of version to be published; agrees to be accountable for all aspects of the work. Jennifer J. Mueller: conception and design; analysis and interpretation of data; drafting of article; revising article critically for important intellectual content; final approval of version to be published; agrees to be accountable for all aspects of the work.

    • Funding This study was funded in part through the NIH/NCI Support Grant P30 CA008748.

    • Competing interests Dr. Abu-Rustum reports grants from Stryker/Novadaq, grants from Olympus, grants from GRAIL, outside the submitted work. Dr. Iasonos reports consultant and personal fees from Mylan, outside the submitted work. Dr. Leitao is a consultant for Intuitive Surgical Inc., outside the submitted work. Dr. Long Roche reports other (travel expenses to a Survivorship Conference, where she spoke) from Intuitive Surgical Inc., outside the submitted work.

    • Patient consent for publication Not required.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data availability statement All data relevant to the study are included in the article or uploaded as supplementary information. All data relevant to the study are included in the article or uploaded as supplementary information.