Awareness of the Causes Leading to Surgical Ablation of Ovarian Function in Premenopausal Breast Cancer—A Single-Center Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design
2.2. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Dowsett, M.; Folkerd, E.; Doody, D.; Haynes, B. The biology of steroid hormones and endocrine treatment of breast cancer. Breast 2005, 14, 452–457. [Google Scholar] [CrossRef]
- Suh, K.J.; Kim, S.H.; Lee, K.H.; Kim, T.Y.; Han, S.W.; Kang, E.; Kim, E.-K.; Kim, K.; No, J.H.; Han, W.; et al. Bilateral salpingo-oophorectomy compared to gonatropin-releasing hormone agonist in premenopausal hormone receptor-positive metastatic breast cancer treated with aromatase inhibitors. Cancer Res. Treat. 2017, 46, 1153–1163. [Google Scholar] [CrossRef] [Green Version]
- Nourmoussavi, M.; Pansegrau, G.; Popesku, J.; Hammond, G.L.; Kwon, J.S.; Carey, M.S. Ovarian ablation for premenopausal breast cancer: A review of treatment considerations and the impact of premature menopause. Cancer Treat. Rev. 2017, 55, 26–35. [Google Scholar] [CrossRef]
- Li, J.-W.; Liu, G.-Y.; Ji, Y.-J.; Yan, X.; Pang, D.; Jiang, Z.-F.; Chen, D.-D.; Zhang, B.; Xu, B.-H.; Shao, Z.-M. Switching to anastrozole plus goserelin vs continued tamoxifen for adjuvant therapy of premenopausal early-stage breast cancer: Preliminary results from a randomized trial. Cancer Manag. Res. 2019, 11, 299–307. [Google Scholar] [CrossRef] [Green Version]
- National Comprehensive Cancer Network. Clinical Practice Guidelines in Oncology-v.3.2013. Available online: https://www.nccn.org/professionals/physician_gls/ (accessed on 13 March 2020).
- Bui, K.T.; Willson, M.L.; Goel, S.; Beith, J.; Goodwin, A. Ovarian suppression for adjuvant treatment of hormone receptor-positive early breast cancer. Cochrane Database Syst. Rev. 2020, 2020. [Google Scholar] [CrossRef] [PubMed]
- Ferrandina, G.; Amadio, G.; Marcellusi, A.; Azzolini, E.; Puggina, A.; Pastorino, R.; Ricciardi, W.; Scambia, G. Bilateral Salpingo-Oophorectomy Versus GnRH Analogue in the Adjuvant Treatment of Premenopausal Breast Cancer Patients: Cost-Effectiveness Evaluation of Breast Cancer Outcome, Ovarian Cancer Prevention and Treatment. Clin. Drug Investig. 2017, 37, 1093–1102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rossi, E.; Morabito, A.; De Maio, E.; Di Rella, F.; Esposito, G.; Gravina, A.; Labonia, V.; Landi, G.; Nuzzo, F.; Pacilio, C.; et al. Endocrine effects of adjuvant letrozole + triptorelin compared with tamoxifen + triptorelin in premenopausal patients with early breast cancer. J. Clin. Oncol. 2008, 26, 264–270. [Google Scholar] [CrossRef]
- Jannuzzo, M.G.; Di Salle, E.; Spinelli, R.; Pirotta, N.; Buchan, P.; Bello, A. Estrogen suppression in premenopausal women following 8 weeks of treatment with exemestane and triptorelin versus triptorelin alone. Breast Cancer Res. Treat. 2009, 113, 491–499. [Google Scholar] [CrossRef]
- Pistelli, M.; Della Mora, A.; Ballatore, Z.; Berardi, R. Aromatase inhibitors in premenopausal women with breast cancer: The state of the art and future prospects. Curr. Oncol. 2018, 25, 168–175. [Google Scholar] [CrossRef] [Green Version]
- Kwon, J.S.; Pansegrau, G.; Nourmoussavi, M.; Hammond, G.; Carey, M.S. Long-term consequences of ovarian ablation for premenopausal breast cancer. Breast Cancer Res Treat. 2016, 157, 565–573. [Google Scholar] [CrossRef]
- Haldar, K.; Giamougiannis, P.; Wilson, C.; Crawford, R. Laparoscopic salpingo-oophorectomy for ovarian ablation in women with hormone-sensitive breast cancer. Int. J. Gynecol. Obstet. 2011, 113, 222–224. [Google Scholar] [CrossRef] [PubMed]
- Sayakhot, P.; Vincent, A.; Deeks, A.; Teede, H. Potential adverse impact of ovariectomy on physical and psychological function of younger women with breast cancer. Menopause 2011, 18, 786–793. [Google Scholar] [CrossRef] [PubMed]
- Rosenberg, S.M.; Tamimi, R.M.; Gelber, S.; Ruddy, K.J.; Bober, S.L.; Ba, S.K.; Borges, V.F.; Come, S.E.; Schapira, L.; Partridge, A.H. Treatment-related amenorrhea and sexual functioning in young breast cancer survivors. Cancer 2014, 120, 2264–2271. [Google Scholar] [CrossRef] [PubMed]
- Zhang, P.; Li, C.-Z.; Jiao, G.-M.; Zhang, J.-J.; Zhao, H.-P.; Yan, F.; Jia, S.-F.; Hu, B.-S.; Wu, C.-T. Effects of ovarian ablation or suppression in premenopausal breast cancer: A meta-analysis of randomized controlled trials. Eur. J. Surg. Oncol. 2017, 43, 1161–1172. [Google Scholar] [CrossRef] [PubMed]
- Singh, G. Oophorectomy in Breast Cancer—Controversies and Current Status. Indian J. Surg. 2012, 74, 210–212. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fleming, G.; Francis, P. Use of luteinising-hormone-releasing hormone agonists as adjuvant treatment in premenopausal patients with hormone-receptor-positive breast cancer: A meta-analysis of individual patient data from randomised adjuvant trials. Breast Dis. 2008, 19, 85. [Google Scholar] [CrossRef]
- Vogl, S.E. Adjuvant ovarian suppression for resected breast cancer: 2017 critical assessment. Breast Cancer Res. Treat. 2017, 166, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Burstein, H.J.; Lacchetti, C.; Anderson, H.; Buchholz, T.A.; Davidson, N.E.; Gelmon, K.E.; Giordano, S.H.; Hudis, C.A.; Solky, A.J.; Stearns, V.; et al. Adjuvant endocrine therapy for women with hormone receptor–positive breast cancer: American society of clinical oncology clinical practice guideline update on ovarian suppression. J. Clin. Oncol. 2016, 34, 1689–1701. [Google Scholar] [CrossRef]
- Bernhard, J.; Luo, W.; Ribi, K.; Colleoni, M.; Burstein, H.J.; Tondini, C.; Pinotti, G.; Spazzapan, S.; Ruhstaller, T.; Puglisi, F.; et al. Patient-reported outcomes with adjuvant exemestane versus tamoxifen in premenopausal women with early breast cancer undergoing ovarian suppression (TEXT and SOFT): A combined analysis of two phase 3 randomised trials. Lancet Oncol. 2015, 16, 848–858. [Google Scholar] [CrossRef] [Green Version]
- Bellet, M.; Gray, K.P.; Francis, P.A.; Láng, I.; Ciruelos, E.; Lluch, A.; Climent, M.A.; Catalán, G.; Avella, A.; Bohn, U.; et al. Twelve-Month estrogen levels in premenopausal women with hormone receptor–positive breast cancer receiving adjuvant triptorelin plus exemestane or tamoxifen in the suppression of ovarian function trial (SOFT): The SOFT-EST Substudy. J. Clin. Oncol. 2016, 34, 1584–1593. [Google Scholar] [CrossRef] [Green Version]
- Hagemann, A.R.; Zighelboim, I.; Odibo, A.O.; Rader, J.S.; Mutch, D.G.; Powell, M.A. Cost-Benefit of laparoscopic versus medical ovarian suppression in premenopausal breast cancer. Breast J. 2011, 17, 103–105. [Google Scholar] [CrossRef]
- Dungan, J. Ovarian Conservation at the Time of Hysterectomy and Long-Term Health Outcomes in the Nurses’ Health Study. In Year Book of Obstetrics, Gynecology and Women’s Health; Mosby: Maryland Heights, MO, USA, 2010; Volume 2010, pp. 318–319. [Google Scholar]
- Lipschutz, D.I. Long-Term mortality associated with oophorectomy compared with ovarian conservation in the nurses’ health study. Obstet. Gynecol. 2013, 122, 395–396. [Google Scholar] [CrossRef] [PubMed]
- Løkkegaard, E.; Jovanovic, Z.; Heitmann, B.; Keiding, N.; Ottesen, B.; Pedersen, A. The association between early menopause and risk of ischaemic heart disease: Influence of Hormone Therapy. Maturitas 2006, 53, 226–233. [Google Scholar] [CrossRef] [PubMed]
- A Rocca, W.; Grossardt, B.R.; de Andrade, M.; Malkasian, G.D.; Melton, L.J. Survival patterns after oophorectomy in premenopausal women: A population-based cohort study. Lancet Oncol. 2006, 7, 821–828. [Google Scholar] [CrossRef]
Age (Median, IQR) Years | 43.5 IQR 7 (8–52) |
<45 years | 51.9% (n = 41) |
≥45 years | 48.1% (n = 38) |
BMI (Median, IQR) kg/m2 | 24.5 IQR 6 (18–42) |
Relevant Clinical Background | |
Obesity (BMI > 30.0 kg/m2) | 14.3% (n = 11) |
Past thromboembolic events | 1.3% (n = 1) |
Gynecological Data | |
Age of menarche (mean ± SD years) | 12.2 ± 1.5 (9–16) |
Combined hormonal contraception (any length) | 48.1% (n = 38) |
Combined hormonal contraception length of use >10 years | 26.6% (n = 21) |
Obstetric Data | |
≥1 Term pregnancy | 72.2% (n = 57) |
Breastfeeding | 59.5% (n = 47) |
Duration in months (median, IQR) | 6 IQR 8 (1–24) |
Reasons for OSA | |
Remaining menstrual cycles (Group 1) | 34.2% (n = 27) |
Patient choice (Group 2) | 31.6% (n = 25) |
Disease progression (Group 3) | 16.5% (n = 13) |
Gynecological organic disease (Group 4) | 13.9% (n = 11) |
Tamoxifen intolerance or contraindication (Group 5) | 3.8% (n = 3) |
Tumor Characteristics | |
Differentiation Grade | |
Well differentiated (Grade 1) | 25.3% (n = 20) |
Moderately differentiated (Grade 2) | 63.3% (n = 50) |
Poorly differentiated (Grade 3) | 11.4% (n = 9) |
Histopathological Analysis | |
DCIS | 8.9% (n = 7) |
IDC | 73.4% (n = 58) |
IDC + DCIS | 17.7% (n = 14) |
Immunohistochemistry | |
Positive estrogen receptors | 100.0% (n = 79) |
Positive progesterone receptors | 88.6% (n = 70) |
Positive HER2 | 20.3% (n = 16) |
Axillary invasion | 41.2% (n = 33) |
Reasons for Ovarian Surgical Ablation | <45 Years | ≥45 Years | p |
---|---|---|---|
Maintenance of menstruation | 41.5% (n = 17) | 26.3% (n = 10) | 0.156 |
Patient’s informed choice | 17.1% (n = 7) | 47.4% (n = 18) | 0.004 |
Disease progression/salvation attempt | 26.8% (n = 11) | 5.3% (n = 2) | 0.01 |
Organic gynecological disease | 9.8% (n = 4) | 18.4% (n = 7) | 0.266 |
Contraindications/severe intolerance to hormone therapy with tamoxifen | 4.9% (n = 2) | 2.6% (n = 1) | 1 |
Maintenance of Menstruation—Group 1 (n = 27) | |
Age (Median, IQR) | 43.0 (IQR 6) years |
<40 years | 22.2% (n = 6) |
40–45 years | 48.1% (n = 13) |
>45 years | 29.6% (n = 8) |
Neoadjuvant chemotherapy | 11.1% (n = 3) |
Previous hormone therapy | 100.0% (n = 27) |
Previous OMA | 55.6% (n = 15) |
Time Between Diagnosis and OSA | |
0 to 3 months | 0.0% (n = 0) |
>3 months to 11 months | 11.1% (n = 3) |
1 year to 5 years | 77.8% (n = 21) |
>5 years | 11.1% (n = 3) |
Hormone Therapy after OSA | |
Tamoxifen | 48.1% (n = 13) |
Aromatase inhibitors | 37.0% (n = 10) |
Switch to aromatase inhibitors after tamoxifen | 3.7% (n = 1) |
Adjuvant radiotherapy | 66.7% (n = 18) |
Adjuvant chemotherapy | 40.7% (n = 11) |
Locoregional recurrence (until 2020) | 7.4% (n = 2) |
Distant metastasis (until 2020) | 3.7% (n = 1) |
5-year disease-free survival | 96.3% (n = 26) |
5-year overall survival | 100.0% (n = 27) |
Death from any cause (until 2020) | 11.1% (n = 3) |
Patient’s Informed Choice—Group 2 (n = 25) | |
Age (Median, IQR) | 46.0 (IQR 5) years |
<40 years | 12.0% (n = 3) |
40–45 years | 28.0% (n = 7) |
>45 years | 60.0% (n = 15) |
Previous hormone therapy | 4.0% (n = 1) |
Previous OMA | 4.0% (n = 1) |
Time Between Diagnosis and OSA | |
0 to 3 months | 56.0% (n = 14) |
>3 months to 11 months | 32.0% (n = 8) |
1 year to 5 years | 12.0% (n = 3) |
>5 years | 0.0% (n = 0) |
Locoregional recurrence | 4.0% (n = 1) |
5-year disease-free survival | 72.0% (n = 18) |
5-year overall survival | 88.0% (n = 22) |
Death from any cause (until 2020) | 12.0% (n = 3) |
Disease Progression/Salvation Attempt—Group 3 (n = 13) | |
Age (Median, IQR) | 40.9 (IQR 6) years |
<40 years | 23.1% (n = 3) |
40–45 years | 69,2% (n = 9) |
>45 years | 7.7% (n = 1) |
Positive HER2 Adjuvant trastuzumab | 15.4% (n = 2) 100.0% (n = 2) |
Tumor Grade | |
Grade 1 | 15.4% (n = 2) |
Grade 2 | 84.6% (n = 11) |
Grade 3 | 0.0% (n = 0) |
TNM Classification at Diagnosis (T) | |
2 | 53.8% (n = 7) |
3 | 23.1% (n = 3) |
4 | 23.1% (n = 3) |
TNM Classification at Diagnosis (N) | |
0 | 7.7% (n = 1) |
1 | 53.8% (n = 7) |
2 | 38.5% (n = 5) |
TNM Classification at Diagnosis (M) | |
0 | 15.4% (n = 2) |
1 | 84.6% (n = 11) |
Local of Distant Metastasis | |
Bone | 54.5% (n = 6) |
Visceral | 18.2% (n = 2) |
Visceral and bone | 27.3% (n = 3) |
Stage at Diagnosis | |
I or II | 15.4% (n = 2) |
III or IV | 84.6% (n = 11) |
Neoadjuvant chemotherapy | 76.9% (n = 10) |
Axillary Lymph Node Dissection | 76.9% (n = 10) |
During the first surgery | 90.0% (n = 9) |
After the first surgery (disease progression) | 10.0% (n = 1) |
Pathological Characteristics | |
IDC | 76.9% (n = 10) |
DCIS | 15.4% (n = 2) |
IDC + DCIS | 7.7% (n = 1) |
Previous hormone therapy | 30.8% (n = 4) |
Previous OMA | 30.8% (n = 4) |
Time Between Diagnosis and OSA | |
0 to 3 months | 53.8% (n = 7) |
>3 months to 11 months | 23.1% (n = 3) |
1 year to 5 years | 23.1% (n = 3) |
>5 years | 0.0% (n = 0) |
Hormonal Therapy after OSA | |
Tamoxifen | 15.4% (n = 2) |
Aromatase inhibitors | 76.9% (n = 10) |
Switch to aromatase inhibitors after tamoxifen | 7.7% (n = 1) |
Adjuvant radiotherapy | 28.0% (n = 7) |
Adjuvant chemotherapy | 61.5% (n = 8) |
5-year disease-free survival | 23.1% (n = 3) |
5-year overall survival | 61.5% (n = 8) |
Death from any cause (until 2020) | 69.2% (n = 9) |
Organic Gynecological Disease—Group 4 (n = 11) | |
Age (Median IQR) | 47.4 ± 4.8 (IQR 13) years |
<40 years | 0.0% (n = 0) |
40–45 years | 45.5% (n = 5) |
>45 years | 54.5% (n = 6) |
Organic Gynecological Disease | |
Myomatous uterus | (n = 6) |
Hysterocele | (n = 2) |
Premalignant endometrial disease | (n = 1) |
Bilateral ovarian complex cysts | (n = 2) |
Previous hormone therapy | 18.2% (n = 2) |
Previous OMA | 18.2% (n = 2) |
Time Between Diagnosis and OSA | |
0 to 3 months | 63.6% (n = 7) |
>3 months to 11 months | 9.1% (n = 1) |
1 year to 5 years | 27.3% (n = 3) |
>5 years | 0.0% (n = 0) |
Locoregional recurrence | 0.0% (n = 0) |
5-year disease-free survival | 100.0% (n = 11) |
5-year overall survival | 100.0% (n = 11) |
Death from any cause (until 2020) | 0.0% (n = 0) |
Contraindications/Severe Intolerance to Tamoxifen—Group 5 (n = 3) | |
Age | |
<40 years | 33.3% (n = 1) |
40–45 years | 33.3% (n = 1) |
>45 years | 33.3% (n = 1) |
Contraindications or Intolerance to Tamoxifen | |
Significant cardiovascular risk | (n = 2) |
Severe neurologic symptoms and polyarthralgia | (n = 1) |
Previous hormone therapy | 100.0% (n = 3) |
Previous OMA | 100.0% (n = 3) |
Locoregional recurrence | 33.3% (n = 1) |
5-year disease-free survival | 33.3% (n = 1) |
5-year overall survival | 100.0% (n = 3) |
Death from any cause (until 2020) | 0.0% (n = 0) |
Age (Mean ± SD) | 40.8 ± 5.3 (28–52) years |
<45 years | 80.0% (n = 20) |
≥45 years | 20.0% (n = 5) |
Reasons for OSA | |
Maintenance of menstruation | 60.0% (n = 15) |
Patient informed choice | 4.0% (n = 1) |
Disease progression/salvation attempt | 16.0% (n = 4) |
Organic gynecological disease | 8.0% (n = 2) |
Contraindications/severe intolerance to tamoxifen | 12.0% (n = 3) |
Hormone therapy with tamoxifen | 88.0% (n = 22) |
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Oliveira, J.C.; Sousa, F.C.; Gante, I.; Dias, M.F. Awareness of the Causes Leading to Surgical Ablation of Ovarian Function in Premenopausal Breast Cancer—A Single-Center Analysis. Medicina 2021, 57, 385. https://doi.org/10.3390/medicina57040385
Oliveira JC, Sousa FC, Gante I, Dias MF. Awareness of the Causes Leading to Surgical Ablation of Ovarian Function in Premenopausal Breast Cancer—A Single-Center Analysis. Medicina. 2021; 57(4):385. https://doi.org/10.3390/medicina57040385
Chicago/Turabian StyleOliveira, Joana Correia, Filipa Costa Sousa, Inês Gante, and Margarida Figueiredo Dias. 2021. "Awareness of the Causes Leading to Surgical Ablation of Ovarian Function in Premenopausal Breast Cancer—A Single-Center Analysis" Medicina 57, no. 4: 385. https://doi.org/10.3390/medicina57040385
APA StyleOliveira, J. C., Sousa, F. C., Gante, I., & Dias, M. F. (2021). Awareness of the Causes Leading to Surgical Ablation of Ovarian Function in Premenopausal Breast Cancer—A Single-Center Analysis. Medicina, 57(4), 385. https://doi.org/10.3390/medicina57040385