Prediction of Myometrial Invasion in Stage I Endometrial Cancer by MRI: The Influence of Surgical Diagnostic Procedure
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Patients and Study Design
2.2. MRI Protocol
2.3. Histopathologic Analysis
2.4. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Zhang, S.; Gong, T.T.; Liu, F.H.; Jiang, Y.T.; Sun, H.; Ma, X.X.; Zhao, Y.H.; Wu, Q.J. Global, Regional, and National Burden of Endometrial Cancer, 1990–2017: Results from the Global Burden of Disease Study, 2017. Front. Oncol. 2019, 9, 1440. [Google Scholar] [CrossRef]
- Siegel, R.; Naishadham, D.; Jemal, A. Cancer statistics, 2012. CA Cancer J. Clin. 2012, 62, 10–29. [Google Scholar] [CrossRef] [Green Version]
- Lai, C.-H.; Wang, C.-J.; Chao, A. The Clinical Management of Endometrial Cancer in Young Women. Curr. Obstet. Gynecol. Rep. 2013, 2, 26–31. [Google Scholar] [CrossRef]
- American College of Obstetricians and Gynecologists. ACOG practice bulletin, clinical management guidelines for obstetrician-gynecologists, number 65, August 2005: Management of endometrial cancer. Obs. Gynecol. 2005, 106, 413–425. [Google Scholar] [CrossRef]
- Kinkel, K.; Kaji, Y.; Yu, K.K.; Segal, M.R.; Lu, Y.; Powell, C.B.; Hricak, H. Radiologic staging in patients with endometrial cancer: A meta-analysis. Radiology 1999, 212, 711–718. [Google Scholar] [CrossRef]
- Lin, G.; Ng, K.K.; Chang, C.J.; Wang, J.J.; Ho, K.C.; Yen, T.C.; Wu, T.I.; Wang, C.C.; Chen, Y.R.; Huang, Y.T.; et al. Myometrial invasion in endometrial cancer: Diagnostic accuracy of diffusion-weighted 3.0-T MR imaging-initial experience. Radiology 2009, 250, 784–792. [Google Scholar] [CrossRef] [PubMed]
- Chao, A.S.; Chao, A.; Wang, C.J.; Lai, C.H.; Wang, H.S. Obstetric outcomes of pregnancy after conservative treatment of endometrial cancer: Case series and literature review. Taiwan J. Obstet. Gynecol. 2011, 50, 62–66. [Google Scholar] [CrossRef] [Green Version]
- Wang, C.J.; Chao, A.; Yang, L.Y.; Hsueh, S.; Huang, Y.T.; Chou, H.H.; Chang, T.C.; Lai, C.H. Fertility-preserving treatment in young women with endometrial adenocarcinoma: A long-term cohort study. Int. J. Gynecol. Cancer 2014, 24, 718–728. [Google Scholar] [CrossRef] [PubMed]
- Shan, W.; Wang, C.; Zhang, Z.; Gu, C.; Ning, C.; Luo, X.; Zhou, Q.; Chen, X. Conservative therapy with metformin plus megestrol acetate for endometrial atypical hyperplasia. J. Gynecol. Oncol. 2014, 25, 214–220. [Google Scholar] [CrossRef] [Green Version]
- Brown, A.J.; Westin, S.N.; Broaddus, R.R.; Schmeler, K. Progestin intrauterine device in an adolescent with grade 2 endometrial cancer. Obs. Gynecol. 2012, 119, 423–426. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, M.L.; Seong, S.J. Clinical applications of levonorgestrel-releasing intrauterine system to gynecologic diseases. Obs. Gynecol. Sci. 2013, 56, 67–75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boussios, S.; Mikropoulos, C.; Samartzis, E.; Karihtala, P.; Moschetta, M.; Sheriff, M.; Karathanasi, A.; Sadauskaite, A.; Rassy, E.; Pavlidis, N. Wise Management of Ovarian Cancer: On the Cutting Edge. J. Pers. Med. 2020, 10, 41. [Google Scholar] [CrossRef]
- Kim, J.S.; Turbov, J.; Rosales, R.; Thaete, L.G.; Rodriguez, G.C. Combination simvastatin and metformin synergistically inhibits endometrial cancer cell growth. Gynecol. Oncol. 2019, 154, 432–440. [Google Scholar] [CrossRef]
- Lee, T.Y.; Martinez-Outschoorn, U.E.; Schilder, R.J.; Kim, C.H.; Richard, S.D.; Rosenblum, N.G.; Johnson, J.M. Metformin as a Therapeutic Target in Endometrial Cancers. Front. Oncol. 2018, 8, 341. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Guo, Y.R.; Lin, J.F.; Feng, Y.; Billig, H.; Shao, R. Combination of Diane-35 and Metformin to Treat Early Endometrial Carcinoma in PCOS Women with Insulin Resistance. J. Cancer 2014, 5, 173–181. [Google Scholar] [CrossRef] [Green Version]
- Boronow, R.C.; Morrow, C.P.; Creasman, W.T.; Disaia, P.J.; Silverberg, S.G.; Miller, A.; Blessing, J.A. Surgical staging in endometrial cancer: Clinical-pathologic findings of a prospective study. Obs. Gynecol. 1984, 63, 825–832. [Google Scholar]
- Zivanovic, O.; Carter, J.; Kauff, N.D.; Barakat, R.R. A review of the challenges faced in the conservative treatment of young women with endometrial carcinoma and risk of ovarian cancer. Gynecol. Oncol. 2009, 115, 504–509. [Google Scholar] [CrossRef]
- Wang, Y.; Yang, J.X. Fertility-preserving treatment in women with early endometrial cancer: The Chinese experience. Cancer Manag. Res. 2018, 10, 6803–6813. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mitsuhashi, A.; Habu, Y.; Kobayashi, T.; Kawarai, Y.; Ishikawa, H.; Usui, H.; Shozu, M. Long-term outcomes of progestin plus metformin as a fertility-sparing treatment for atypical endometrial hyperplasia and endometrial cancer patients. J. Gynecol. Oncol. 2019, 30, e90. [Google Scholar] [CrossRef] [PubMed]
- Fujii, S.; Kido, A.; Baba, T.; Fujimoto, K.; Daido, S.; Matsumura, N.; Konishi, I.; Togashi, K. Subendometrial enhancement and peritumoral enhancement for assessing endometrial cancer on dynamic contrast enhanced MR imaging. Eur. J. Radiol. 2015, 84, 581–589. [Google Scholar] [CrossRef]
- Ito, K.; Matsumoto, T.; Nakada, T.; Nakanishi, T.; Fujita, N.; Yamashita, H. Assessing myometrial invasion by endometrial carcinoma with dynamic MRI. J. Comput. Assist. Tomogr. 1994, 18, 77–86. [Google Scholar] [CrossRef] [PubMed]
- Sironi, S.; Colombo, E.; Villa, G.; Taccagni, G.; Belloni, C.; Garancini, P.; DelMaschio, A. Myometrial invasion by endometrial carcinoma: Assessment with plain and gadolinium-enhanced MR imaging. Radiology 1992, 185, 207–212. [Google Scholar] [CrossRef]
- Cunha, T.M.; Félix, A.; Cabral, I. Preoperative assessment of deep myometrial and cervical invasion in endometrial carcinoma: Comparison of magnetic resonance imaging and gross visual inspection. Int. J. Gynecol. Cancer 2001, 11, 130–136. [Google Scholar] [CrossRef] [PubMed]
- Beddy, P.; Moyle, P.; Kataoka, M.; Yamamoto, A.K.; Joubert, I.; Lomas, D.; Crawford, R.; Sala, E. Evaluation of depth of myometrial invasion and overall staging in endometrial cancer: Comparison of diffusion-weighted and dynamic contrast-enhanced MR imaging. Radiology 2012, 262, 530–537. [Google Scholar] [CrossRef]
- Andreano, A.; Rechichi, G.; Rebora, P.; Sironi, S.; Valsecchi, M.G.; Galimberti, S. MR diffusion imaging for preoperative staging of myometrial invasion in patients with endometrial cancer: A systematic review and meta-analysis. Eur. Radiol. 2014, 24, 1327–1338. [Google Scholar] [CrossRef] [PubMed]
- Nougaret, S.; Horta, M.; Sala, E.; Lakhman, Y.; Thomassin-Naggara, I.; Kido, A.; Masselli, G.; Bharwani, N.; Sadowski, E.; Ertmer, A.; et al. Endometrial Cancer MRI staging: Updated Guidelines of the European Society of Urogenital Radiology. Eur. Radiol. 2019, 29, 792–805. [Google Scholar] [CrossRef]
- Kitajima, K.; Murakami, K.; Yamasaki, E.; Kaji, Y.; Sugimura, K. Accuracy of integrated FDG-PET/contrast-enhanced CT in detecting pelvic and paraaortic lymph node metastasis in patients with uterine cancer. Eur. Radiol. 2009, 19, 1529–1536. [Google Scholar] [CrossRef]
- Franchi, M.; Garzon, S.; Zorzato, P.C.; Laganà, A.S.; Casarin, J.; Locantore, L.; Raffaelli, R.; Ghezzi, F. PET-CT scan in the preoperative workup of early stage intermediate- and high-risk endometrial cancer. Minim. Invasive Ther. Allied Technol. 2020, 29, 232–239. [Google Scholar] [CrossRef]
- Tsuyoshi, H.; Tsujikawa, T.; Yamada, S.; Okazawa, H.; Yoshida, Y. Diagnostic value of 18F-FDG PET/MRI for staging in patients with endometrial cancer. Cancer Imaging 2020, 20, 75. [Google Scholar] [CrossRef]
- Otero-García, M.M.; Mesa-Álvarez, A.; Nikolic, O.; Blanco-Lobato, P.; Basta-Nikolic, M.; de Llano-Ortega, R.M.; Paredes-Velázquez, L.; Nikolic, N.; Szewczyk-Bieda, M. Role of MRI in staging and follow-up of endometrial and cervical cancer: Pitfalls and mimickers. Insights Imaging 2019, 10, 19. [Google Scholar] [CrossRef]
- Scioscia, M.; Noventa, M.; Laganà, A.S. Abnormal uterine bleeding and the risk of endometrial cancer: Can subendometrial vascular ultrasound be of help to discriminate cancer from adenomyosis? Am. J. Obs. Gynecol. 2020, 223, 605–606. [Google Scholar] [CrossRef]
- Cunningham, R.K.; Horrow, M.M.; Smith, R.J.; Springer, J. Adenomyosis: A Sonographic Diagnosis. Radiographics 2018, 38, 1576–1589. [Google Scholar] [CrossRef] [PubMed]
- Sundar, S.; Balega, J.; Crosbie, E.; Drake, A.; Edmondson, R.; Fotopoulou, C.; Gallos, I.; Ganesan, R.; Gupta, J.; Johnson, N.; et al. BGCS uterine cancer guidelines: Recommendations for practice. Eur. J. Obstet. Gynecol. Reprod. Biol. 2017, 213, 71–97. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colombo, N.; Creutzberg, C.; Amant, F.; Bosse, T.; González-Martín, A.; Ledermann, J.; Marth, C.; Nout, R.; Querleu, D.; Mirza, M.R.; et al. ESMO-ESGO-ESTRO Consensus Conference on Endometrial Cancer: Diagnosis, Treatment and Follow-up. Int. J. Gynecol. Cancer 2016, 26, 2–30. [Google Scholar] [CrossRef] [Green Version]
- Santaballa, A.; Matías-Guiu, X.; Redondo, A.; Carballo, N.; Gil, M.; Gómez, C.; Gorostidi, M.; Gutierrez, M.; Gónzalez-Martín, A. SEOM clinical guidelines for endometrial cancer (2017). Clin. Transl. Oncol. 2018, 20, 29–37. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamagami, W.; Mikami, M.; Nagase, S.; Tabata, T.; Kobayashi, Y.; Kaneuchi, M.; Kobayashi, H.; Yamada, H.; Hasegawa, K.; Fujiwara, H.; et al. Japan Society of Gynecologic Oncology 2018 guidelines for treatment of uterine body neoplasms. J. Gynecol. Oncol. 2020, 31, e18. [Google Scholar] [CrossRef]
- Network, N.C.C. Uterine Neoplasm (Version 3.2021). Available online: https://www.nccn.org/professionals/physician_gls/pdf/uterine_blocks.pdf (accessed on 3 June 2021).
- Hamilton, C.A.; Pothuri, B.; Arend, R.C.; Backes, F.J.; Gehrig, P.A.; Soliman, P.T.; Thompson, J.S.; Urban, R.R.; Burke, W.M. Endometrial cancer: A society of gynecologic oncology evidence-based review and recommendations, part II. Gynecol. Oncol. 2021, 160, 827–834. [Google Scholar] [CrossRef]
- Lin, G.; Huang, Y.T.; Chao, A.; Ng, K.K.; Yang, L.Y.; Ng, S.H.; Lai, C.H. Influence of menopausal status on diagnostic accuracy of myometrial invasion in endometrial cancer: Diffusion-weighted and dynamic contrast-enhanced MRI at 3 T. Clin. Radiol. 2015, 70, 1260–1268. [Google Scholar] [CrossRef]
Number of Cases | 263 |
---|---|
Age, years (mean, +/− SD) | 53.5 +/− 10.3 |
Histological type, N (%) | |
Endometrioid | 249 (94.7) |
Clear cell | 5 (1.9) |
Serous | 5 (1.9) |
Undifferentiated | 2 (0.8) |
Adenosquamous | 1 (0.4) |
Well-differentiated | 1 (0.4) |
Tumor grade, N (%) | |
1 | 165 (62.7) |
2 | 70 (26.6) |
3 | 28 (10.6) |
Myometrial Invasion | By Histology, N (%) | By MRI, N (%) |
---|---|---|
Negative | 92 (35.0) | 89 (33.8) |
Positive, <50% thickness | 145 (55.1) | 174 (66.2) |
Positive, ≥50% thickness | 26 (9.9) | 0 |
Total Cohorts | Pathology | |||
---|---|---|---|---|
Positive | Negative | Total | ||
MRI | Positive | 125 (47.5%) | 49 (18.6%) | 174 (66.2%) |
Negative | 46 (17.4%) | 43 (16.3%) | 89 (33.8%) | |
Total | 171 (65.0%) | 92 (35.0%) | 263 (100%) | |
Group 1 | Pathology | |||
Positive | Negative | Total | ||
MRI | Positive | 15 (45.5%) | 6 (18.2%) | 21 (63.6%) |
Negative | 8 (24.2%) | 4 (12.1%) | 12 (36.3%) | |
Total | 23 (69.7%) | 10 (30.3%) | 33 (100%) | |
Group 2 | Pathology | |||
Positive | Negative | Total | ||
MRI | Positive | 15 (41.7%) | 9 (25.0%) | 24 (66.7%) |
Negative | 9 (25.0%) | 3 (8.3%) | 12 (33.3%) | |
Total | 24 (66.7%) | 12 (33.3%) | 36 (100%) | |
Group 3 | Pathology | |||
Positive | Negative | Total | ||
MRI | Positive | 19 (41.3%) | 12 (26.1%) | 31 (67.4%) |
Negative | 4 (8.7%) | 11 (23.9%) | 15 (32.6%) | |
Total | 23 (50.0%) | 23 (50.0%) | 46 (100%) | |
Group 4 | Pathology | |||
Positive | Negative | Total | ||
MRI | Positive | 69 (51.5%) | 19 (14.2%) | 88 (65.7%) |
Negative | 22 (16.4%) | 24 (17.9%) | 46 (34.3%) | |
Total | 91 (67.9%) | 43 (32.1%) | 134 (100%) |
Variables | N | OR (95% CI) | p-Value |
---|---|---|---|
Age | 263 | 0.978 (0.953–1.002) | 0.074 |
ER | |||
Negative | 17 | Reference | |
Positive | 103 | 0.826 (0.281–2.430) | 0.729 |
PR | |||
Negative | 18 | Reference | |
Positive | 102 | 1.243 (0.409–3.780) | 0.701 |
CA125 (U/mL) | |||
<35 | 196 | Reference | |
≥35 | 57 | 0.686 (0.363–1.296) | 0.245 |
Menopause age (year) | |||
<55 | 120 | Reference | |
≥55 | 42 | 1.853 (0.901–3.809) | 0.093 |
Family History of EC | |||
No | 258 | Reference | |
Yes | 5 | 1.183 (0.194–7.207) | 0.856 |
Diabetes history | |||
No | 215 | Reference | |
Yes | 48 | 0.861 (0.444–1.667) | 0.657 |
BMI | |||
<30 | 205 | Reference | |
≥30 | 58 | 1.461 (0.806–2.648) | 0.211 |
Radiation history | |||
No | 261 | Reference | |
Yes | 2 | 1.777 (0.110–28.732) | 0.686 |
Pre-debulking surgery | |||
1 | 33 | 0.737 (0.285–1.906) | 0.529 |
2 | 36 | Reference | |
3 | 46 | 0.533 (0.219–1.301) | 0.167 |
Pre-debulking surgery | |||
1, 2 | 69 | 1.902 (1.078–3.571) | 0.027 |
3 | 46 | 1.21 (0.595–2.459) | 0.599 |
4 | 134 | Reference | |
Pre-debulking surgery | |||
1, 2, 3 | 115 | 1.625 (0.964–2.739) | 0.068 |
4 | 134 | Reference | |
Pre-debulking surgery | |||
1 | 33 | 1.671 (0.765–3.653) | |
2 | 36 | 2.268 (1.072–4.80) | 0.198 |
3 | 46 | 1.21 (0.595–2.459) | 0.032 |
4 | 134 | Reference | 0.599 |
The Guidelines | Quote the Content Related with MI Assessment |
---|---|
British Gynecologic Cancer Society (BCGS) [33] |
|
European Society for Medical Oncology (ESMO), European Society for Radiotherapy and Oncology (ESTRO), and European Society of Gynaecological Oncology (ESGO) consensus conference [34] |
|
European Society of Urogenital Radiology (ESUR) [26] |
|
GEICO (Spanish Group for Investigation in Ovarian Cancer) and SEOM (Spanish Society of Medical Oncology) [35] |
|
Japan Society of Gynecologic Oncology (JSGO) [36] |
|
National Comprehensive Cancer Network (NCCN) guideline [37] |
|
Society of Gynecologic Oncology (SGO) [38] |
|
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Chen, W.-C.; Hsu, L.-T.; Huang, Y.-T.; Pan, Y.-B.; Ueng, S.-H.; Chou, H.-H.; Chang, T.-C. Prediction of Myometrial Invasion in Stage I Endometrial Cancer by MRI: The Influence of Surgical Diagnostic Procedure. Cancers 2021, 13, 3275. https://doi.org/10.3390/cancers13133275
Chen W-C, Hsu L-T, Huang Y-T, Pan Y-B, Ueng S-H, Chou H-H, Chang T-C. Prediction of Myometrial Invasion in Stage I Endometrial Cancer by MRI: The Influence of Surgical Diagnostic Procedure. Cancers. 2021; 13(13):3275. https://doi.org/10.3390/cancers13133275
Chicago/Turabian StyleChen, Wei-Chun, Le-Tien Hsu, Yu-Ting Huang, Yu-Bin Pan, Shir-Hwa Ueng, Hung-Hsueh Chou, and Ting-Chang Chang. 2021. "Prediction of Myometrial Invasion in Stage I Endometrial Cancer by MRI: The Influence of Surgical Diagnostic Procedure" Cancers 13, no. 13: 3275. https://doi.org/10.3390/cancers13133275