Window of Opportunity: Rate of Referral to Infertility Providers among Reproductive-Age Women with Newly Diagnosed Gynecologic Cancers
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Demographics
3.2. Cancer Types
3.3. Gynecologic Oncology Providers
3.4. Treatment Types
3.5. Documentation
3.6. Attendance and Pregnancy
3.7. Mixed Model
4. Discussion
Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Woodruff, T.K. The Emergence of a New Interdiscipline: Oncofertility. Cancer Treat. Res. 2007, 138, 3–11. [Google Scholar] [CrossRef] [PubMed]
- Ethics Committee of the American Society for Reproductive Medicine. Fertility preservation and reproduction in patients facing gonadotoxic therapies: An Ethics Committee opinion. Fertil. Steril. 2018, 110, 380–386. [Google Scholar] [CrossRef] [PubMed]
- Holman, D.A. Fertility Preservation in Gynecologic Cancer. Semin. Oncol. Nurs. 2019, 35, 202–210. [Google Scholar] [CrossRef] [PubMed]
- Kohn, J.R.; Kashi, P.K.; Acosta-Torres, S.; Beavis, A.L.; Christianson, M.S. Fertility-Sparing Surgery for Patients with Cervical, Endometrial, and Ovarian Cancers. J. Minim. Invasive Gynecol. 2021, 28, 392–402. [Google Scholar] [CrossRef] [PubMed]
- Nezhat, C.; Roman, R.A.; Rambhatla, A.; Nezhat, F. Reproductive and Oncologic Outcomes after Fertility-Sparing Surgery for Early Stage Cervical Cancer: A Systematic Review. Fertil. Steril. 2020, 113, 685–703. [Google Scholar] [CrossRef] [PubMed]
- Bastings, L.; Baysal, O.; Beerendonk, C.C.M.; Braat, D.D.M.; Nelen, W.L.D.M. Referral for Fertility Preservation Counselling in Female Cancer Patients. Hum. Reprod. 2014, 29, 2228–2237. [Google Scholar] [CrossRef] [PubMed]
- Goodman, L.R.; Balthazar, U.; Kim, J.; Mersereau, J.E. Trends of Socioeconomic Disparities in Referral Patterns for Fertility Preservation Consultation. Hum. Reprod. 2012, 27, 2076–2081. [Google Scholar] [CrossRef] [PubMed]
- Banerjee, R.; Tsiapali, E. Occurrence and Recall Rates of Fertility Discussions with Young Breast Cancer Patients. Support. Care Cancer 2016, 24, 163–171. [Google Scholar] [CrossRef]
- Hartup, L.A.; Go, V.-A.; Robinson, R.D. Standardized Reproductive Endocrinology and Infertility Consultation for Pediatric and Adolescent Oncology Patients. J. Adolesc. Young Adult Oncol. 2024, 13. [Google Scholar] [CrossRef]
- Stewart, K.; Campbell, S.; Frumovitz, M.; Ramirez, P.T.; McKenzie, L.J. Fertility Considerations Prior to Conservative Management of Gynecologic Cancers. Int. J. Gynecol. Cancer 2021, 31, 339–344. [Google Scholar] [CrossRef]
- Nitecki, R.; Woodard, T.; Rauh-Hain, J.A. Fertility-Sparing Treatment for Early-Stage Cervical, Ovarian, and Endometrial Malignancies. Obs. Gynecol. 2020, 136, 1157–1169. [Google Scholar] [CrossRef] [PubMed]
- Kipling, L.M.; Shandley, L.M.; Mertens, A.C.; Spencer, J.B.; Howards, P.P. The Use of Fertility Treatments among Reproductive-Aged Women after Cancer. Fertil. Steril. 2024, 121, 578–588. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Chen, L.; Ruan, J.Y.; Cheung, W.Y. Discussions about Reproductive and Sexual Health among Young Adult Survivors of Cancer. Cancer Med. 2016, 5, 1037–1046. [Google Scholar] [CrossRef] [PubMed]
- Hohmann, C.; Borgmann-Staudt, A.; Rendtorff, R.; Reinmuth, S.; Holzhausen, S.; Willich, S.N.; Henze, G.; Goldbeck, L.; Keil, T. Patient Counselling on the Risk of Infertility and Its Impact on Childhood Cancer Survivors: Results from a National Survey. J. Psychosoc. Oncol. 2011, 29, 274–285. [Google Scholar] [CrossRef] [PubMed]
- Winship, A.L.; Alesi, L.R.; Sant, S.; Stringer, J.M.; Cantavenera, A.; Hegarty, T.; Requesens, C.L.; Liew, S.H.; Sarma, U.; Griffiths, M.J.; et al. Checkpoint Inhibitor Immunotherapy Diminishes Oocyte Number and Quality in Mice. Nat. Cancer 2022, 3, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Macklon, K.T.; De Vos, M. Cryopreservation of ovarian tissue for fertility preservation in breast cancer patients: Time to stop? Reprod. Biomed. Online 2024, 49, 103939. [Google Scholar] [CrossRef]
- Floyd, J.L.; Campbell, S.; Rauh-Hain, J.A.; Woodard, T. Fertility Preservation in Women with Early-Stage Gynecologic Cancer: Optimizing Oncologic and Reproductive Outcomes. Int. J. Gynecol. Cancer 2021, 31, 345–351. [Google Scholar] [CrossRef] [PubMed]
- Lambertini, M.; Blondeaux, E.; Bruzzone, M.; Perachino, M.; Anderson, R.A.; de Azambuja, E.; Poorvu, P.D.; Kim, H.J.; Villarreal-Garza, C.; Pistilli, B.; et al. Pregnancy After Breast Cancer: A Systematic Review and Meta-Analysis. J. Clin. Oncol. 2021, 39, 3293–3305. [Google Scholar] [CrossRef] [PubMed]
- Natsuhara, K.H.; Chien, A.J. Impact of Systemic Therapy on Fertility in Women with Early-Stage Breast Cancer. Curr. Breast Cancer Rep. 2024, 16, 61–68. [Google Scholar] [CrossRef]
- United States Cancer Statistics (USCS). Gynecologic Cancer Incidence, United States—2012–2016; United States Cancer Statistics (USCS): Washington, DC, USA, 2019.
- Riggan, K.A.; Rousseau, A.C.; DSouza, K.N.; Woodward, K.T.; Lue, J.; Phelan, S.M.; Allyse, M.A.; Shenoy, C.C. Patient Perceptions of Body Mass Index Restrictions Limiting Fertility Care for Women with High Body Mass Index. Reprod. Biomed. Online 2023, 47, 103210. [Google Scholar] [CrossRef]
- Kaye, L.; Sueldo, C.; Engmann, L.; Nulsen, J.; Benadiva, C. Survey Assessing Obesity Policies for Assisted Reproductive Technology in the United States. Fertil. Steril. 2016, 105, 703–706.e2. [Google Scholar] [CrossRef] [PubMed]
- Quinn, G.P.; Vadaparampil, S.T.; Lee, J.-H.; Jacobsen, P.B.; Bepler, G.; Lancaster, J.; Keefe, D.L.; Albrecht, T.L. Physician Referral for Fertility Preservation in Oncology Patients: A National Study of Practice Behaviors. J. Clin. Oncol. 2009, 27, 5952–5957. [Google Scholar] [CrossRef] [PubMed]
- Carter, J.; Penson, R.; Barakat, R.; Wenzel, L. Contemporary Quality of Life Issues Affecting Gynecologic Cancer Survivors. Hematol. Oncol. Clin. N. Am. 2012, 26, 169–194. [Google Scholar] [CrossRef]
- Jemal, A.; Bray, F.; Center, M.M.; Ferlay, J.; Ward, E.; Forman, D. Global Cancer Statistics. CA Cancer J. Clin. 2011, 61, 69–90. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.J.; Schover, L.R.; Partridge, A.H.; Patrizio, P.; Wallace, W.H.; Hagerty, K.; Beck, L.N.; Brennan, L.V.; Oktay, K. American Society of Clinical Oncology American Society of Clinical Oncology Recommendations on Fertility Preservation in Cancer Patients. J. Clin. Oncol. 2006, 24, 2917–2931. [Google Scholar] [CrossRef] [PubMed]
- Lawrenz, B.; Jauckus, J.; Kupka, M.S.; Strowitzki, T.; von Wolff, M. Fertility Preservation in >1,000 Patients: Patient’s Characteristics, Spectrum, Efficacy and Risks of Applied Preservation Techniques. Arch. Gynecol. Obs. 2011, 283, 651–656. [Google Scholar] [CrossRef]
- Kim, J.; Oktay, K.; Gracia, C.; Lee, S.; Morse, C.; Mersereau, J.E. Which Patients Pursue Fertility Preservation Treatments? A Multicenter Analysis of the Predictors of Fertility Preservation in Women with Breast Cancer. Fertil. Steril. 2012, 97, 671–676. [Google Scholar] [CrossRef]
- Wnuk, K.; Świtalski, J.; Miazga, W.; Tatara, T.; Religioni, U.; Olszewski, P.; Augustynowicz, A. The Usage of Cryopreserved Reproductive Material in Cancer Patients Undergoing Fertility Preservation Procedures. Cancers 2023, 15, 5348. [Google Scholar] [CrossRef]
Factor | Total (N = 410) | No Referral (N = 350) | Referral Placed (N = 60) | p-Value |
---|---|---|---|---|
Age at diagnosis (median) IQR (when was first abnormal imaging or biopsy found) | 35.0 [31.0, 39.0] | 36.0 [32.0, 39.0] | 32.0 [28.5, 35.5] | <0.001 b |
Age at Diagnosis n (%) | <0.001 c | |||
18–34 | 180 (43.9) | 139 (39.7) | 41 (68.3) | |
35–41 | 230 (56.1) | 211 (60.3) | 19 (31.7) | |
Living children > 0 | <0.001 c | |||
No | 204 (49.8) | 156 (44.6) | 48 (80.0) | |
Yes | 206 (50.2) | 194 (55.4) | 12 (20.0) | |
Race | 0.22 d | |||
White | 327 (79.8) | 277 (79.1) | 50 (83.3) | |
African American | 61 (14.9) | 56 (16.0) | 5 (8.3) | |
Asian | 8 (2.0) | 6 (1.7) | 2 (3.3) | |
Multiracial/Multicultural | 14 (3.4) | 11 (3.1) | 3 (5.0) | |
Ethnicity | 0.65 d | |||
Not Hispanic | 385 (93.9) | 329 (94.0) | 56 (93.3) | |
Hispanic | 13 (3.2) | 10 (2.9) | 3 (5.0) | |
Unknown | 12 (2.9) | 11 (3.1) | 1 (1.7) | |
Marital Status at time of diagnosis | 0.019 d | |||
Married | 198 (48.3) | 178 (50.9) | 20 (33.3) | |
Single | 198 (48.3) | 158 (45.1) | 40 (66.7) | |
Widowed | 5 (1.2) | 5 (1.4) | 0 (0.00) | |
Unknown | 9 (2.2) | 9 (2.6) | 0 (0.00) | |
Med hx: type 2 diabetes | 37 (9.0) | 36 (10.3) | 1 (1.7) | 0.031 c |
Med hx: hypertension | 60 (14.6) | 54 (15.4) | 6 (10.0) | 0.27 c |
Med hx: asthma | 33 (8.0) | 27 (7.7) | 6 (10.0) | 0.61 d |
Med hx: kidney disease | 4 (0.98) | 4 (1.1) | 0 (0.00) | 0.99 d |
Med hx: GI disease | 20 (4.9) | 20 (5.7) | 0 (0.00) | 0.056 d |
Med hx: obesity (BMI > 30) | 148 (36.1) | 135 (38.6) | 13 (21.7) | 0.012 c |
Med hx: mental health illness | 76 (18.5) | 72 (20.6) | 4 (6.7) | 0.010 c |
Med hx: other malignancy | 13 (3.2) | 11 (3.1) | 2 (3.3) | 0.99 d |
Med hx: none | 170 (41.5) | 132 (37.7) | 38 (63.3) | <0.001 c |
Pelvic hx: ovarian cystectomy | 19 (4.6) | 12 (3.4) | 7 (11.7) | 0.012 d |
Pelvic hx: none | 255 (62.2) | 217 (62.0) | 38 (63.3) | 0.84 c |
Factor | Total (N = 410) | No Referral (N = 350) | Referral Placed (N = 60) | p-Value |
---|---|---|---|---|
Cancer: Cervical | 152 (37.1) | 134 (38.3) | 18 (30.0) | 0.22 c |
Cancer: Epithelial/Ovarian/Peritoneal/Tubal | 101 (24.6) | 80 (22.9) | 21 (35.0) | 0.044 c |
Borderline ovarian tumor | 25 (6.1) | 14 (4.0) | 11 (18.3) | <0.001 c |
Cancer: Sex cord stromal/germ cell | 11 (2.7) | 10 (2.9) | 1 (1.7) | 0.60 c |
Cancer: Gestational trophoblastic | 26 (6.3) | 24 (6.9) | 2 (3.3) | 0.30 c |
Cancer: Uterine | 83 (20.2) | 75 (21.4) | 8 (13.3) | 0.15 c |
Cancer: Vaginal/vulvar | 15 (3.7) | 15 (4.3) | 0 (0.00) | 0.10 c |
Cancer: Other ovary (i.e., neuroendocrine) | 5 (1.2) | 5 (1.4) | 0 (0.00) | 0.35 c |
Gyn Onc gender | 0.010 c | |||
female | 80 (19.5) | 61 (17.4) | 19 (31.7) | |
male | 330 (80.5) | 289 (82.6) | 41 (68.3) | |
Gyn Onc Start Year | 2006 [1989, 2015] | 2004 [1989, 2015] | 2010 [2004, 2015] | 0.032 b |
Desire for future fertility at time of gyn onc visit? | <0.001 c | |||
yes | 134 (32.7) | 77 (22.0) | 57 (95.0) | |
no | 53 (12.9) | 53 (15.1) | 0 (0.00) | |
not documented | 223 (54.4) | 220 (62.9) | 3 (5.0) | |
Was fertility sparing treatment offered by a GO? | <0.001 c | |||
No | 235 (57.3) | 218 (62.3) | 17 (28.3) | |
Yes | 175 (42.7) | 132 (37.7) | 43 (71.7) | |
Treatment Plan—first definitive step | 0.28 c | |||
Chemo | 23 (5.6) | 22 (6.3) | 1 (1.7) | |
Chemo/RT | 34 (8.3) | 30 (8.6) | 4 (6.7) | |
Radiation | 7 (1.7) | 7 (2.0) | 0 (0.00) | |
Surgery | 346 (84.4) | 291 (83.1) | 55 (91.7) | |
Days between contact and treatment | 18.5 [8.0, 35.0] | 19.0 [8.0, 34.0] | 17.0 [7.0, 56.5] | 0.44 b |
Factor | N | Referral Placed (N = 60) |
---|---|---|
Was REI visit attended? | 60 | |
No | 11 (18.3) | |
Yes | 49 (81.7) | |
Patient offered fertility treatment? | 49 | |
No | 4 (8.2) | |
Yes | 45 (91.8) | |
Did patient elect to undergo fertility testing? | 45 | |
No | 17 (37.8) | |
Yes | 28 (62.2) | |
Did patient elect to undergo fertility preservation? | 45 | |
No | 24 (53.3) | |
Yes | 21 (46.7) | |
Fertility treatment: medication preservation | 21 | |
No | 16 (76.2) | |
Yes | 5 (23.8) | |
Fertility treatment: oocyte preservation | 21 | |
No | 10 (47.6) | |
Yes | 11 (52.4) | |
Fertility treatment: embryo preservation | 21 | |
No | 21 (100.0) | |
Fertility treatment: ovarian tissue preservation | 21 | |
No | 14 (66.7) | |
Yes | 7 (33.3) | |
Pregnancy after fertility preservation? | 21 | |
No | 19 (90.5) | |
Yes | 2 (9.5) |
Pregnancy after onc diagnosis/intervention (regardless of REI referral)? | 410 | 0.99 d | |||
No | 392 (95.6) | 334 (95.4) | 58 (96.7) | ||
Yes | 18 (4.4) | 16 (4.6) | 2 (3.3) | ||
Days between contact and last follow-up | 410 | 1405.0 [547.0, 2767.0] | 1405.0 [541.0, 2818.0] | 1427.5 [747.5, 2525.0] | 0.77 b |
Factor | OR | 95% CI | p-Value |
---|---|---|---|
Living children | -Reference- | ||
No living children | 11.46 | (2.28, 57.61) | 0.004 |
Past medical history | -Reference- | ||
No past medical history | 6.69 | (1.71, 26.23) | 0.007 |
Male Gyn Onc | -Reference- | ||
Female Gyn Onc | 3.80 | (1.04, 13.85) | 0.043 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 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
Frisch, E.H.; Yao, M.; Kim, H.; Neumann, O.; Chau, D.B.; Richards, E.G.; Beffa, L. Window of Opportunity: Rate of Referral to Infertility Providers among Reproductive-Age Women with Newly Diagnosed Gynecologic Cancers. J. Clin. Med. 2024, 13, 4709. https://doi.org/10.3390/jcm13164709
Frisch EH, Yao M, Kim H, Neumann O, Chau DB, Richards EG, Beffa L. Window of Opportunity: Rate of Referral to Infertility Providers among Reproductive-Age Women with Newly Diagnosed Gynecologic Cancers. Journal of Clinical Medicine. 2024; 13(16):4709. https://doi.org/10.3390/jcm13164709
Chicago/Turabian StyleFrisch, Emily H., Meng Yao, Hanna Kim, Olivia Neumann, Danielle B. Chau, Elliott G. Richards, and Lindsey Beffa. 2024. "Window of Opportunity: Rate of Referral to Infertility Providers among Reproductive-Age Women with Newly Diagnosed Gynecologic Cancers" Journal of Clinical Medicine 13, no. 16: 4709. https://doi.org/10.3390/jcm13164709