Abstract
Background
Breast cancer is the most common non-skin cancer in women and an increasing number of people are living as breast cancer survivors. While the prognosis of breast cancer continues to improve, the rates of sexual dysfunction and the risk related to cancer treatments have not been well characterized in a population-based study.
Methods
We identified a cohort of 19,709 breast cancer survivors diagnosed between 1997 and 2017 from the Utah Cancer Registry, and 93,389 cancer-free women who were matched by age and birth state from the Utah Population Database. Sexual dysfunction diagnoses were identified through ICD-9 and ICD-10 codes from electronic medical records and statewide healthcare facilities data. Cox proportional hazard models were used to estimate hazard ratios for risk of sexual dysfunction.
Results
Breast cancer survivors were at higher risk of sexual dysfunction diagnosis (9.1% versus 6.9%, HR 1.60, 95% CI 1.51–1.70) compared to the general population. This risk increased 2.05-fold within 1 to 5 years after cancer diagnosis (95% CI 1.89–2.22) and 3.05-fold in individuals diagnosed with cancer at < 50 years of age (95% CI 2.65–3.51). Cancer treatments including endocrine therapy, chemotherapy and radiation therapy were associated with an increased risk of sexual dysfunction among breast cancer survivors.
Conclusions
Risk of sexual dysfunction in breast cancer survivors is higher than in the general population, but may be underdiagnosed in the clinical setting. Health care professionals should be encouraged to address the topic of sexual health early on in the treatment of breast cancer, and routinely screen patients for symptoms of sexual dysfunction.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available upon request with appropriate approval from the Resource for Genetic and Epidemiologic Research (RGE) and IRB approval. The data are not publicly available due to privacy or ethical restrictions.
References
American Cancer Society (2021) Breast cancer facts & figures 2019–2020. American Cancer Society Inc, Atlanta
Centers for Disease Control and Prevention (2021) United States cancer statistics breast cancer stat bite. Centers for Disease Control and Prevention, US Department of Health and Human Services, Atlanta
US Cancer Statistics Working Group (2021) US cancer statistics data visualizations tool, based on 2020 submission data. U.S. Department of Health and Human Services Centers for Disease Control and Prevention and National Cancer Institute, Atlanta
Barni S, Mondin R (1997) Sexual dysfunction in treated breast cancer patients. Ann Oncol 8:149–153. https://doi.org/10.1023/a:1008298615272
Boswell EN, Dizon DS (2015) Breast cancer and sexual function. Transl Androl Urol 4:160–168. https://doi.org/10.3978/j.issn.2223-4683.2014.12.04
Ganz PA, Rowland JH, Desmond K, Meyerowitz BE, Wyatt GE (1998) Life after breast cancer: understanding women’s health-related quality of life and sexual functioning. J Clin Oncol 16:501–514. https://doi.org/10.1200/jco.1998.16.2.501
Panjari M, Bell RJ, Davis SR (2011) Sexual function after breast cancer. J Sex Med 8:294–302. https://doi.org/10.1111/j.1743-6109.2010.02034.x
Schover LR (2019) Sexual quality of life in men and women after cancer. Climacteric 22:553–557. https://doi.org/10.1080/13697137.2018.1526893
Thors CL, Broeckel JA, Jacobsen PB (2001) Sexual functioning in breast cancer survivors. Cancer Control 8:442–448. https://doi.org/10.1177/107327480100800508
Wiggins DL, Wood R, Granai CO, Dizon DS (2007) Sex, intimacy, and the gynecologic oncologists: survey results of the New England association of gynecologic oncologists (NEAGO). J Psychosoc Oncol 25:61–70. https://doi.org/10.1300/J077v25n04_04
Brédart A, Dolbeault S, Savignoni A, Besancenet C, This P, Giami A, Michaels S, Flahault C, Falcou MC, Asselain B, Copel L (2011) Prevalence and associated factors of sexual problems after early-stage breast cancer treatment: results of a French exploratory survey. Psychooncology 20:841–850. https://doi.org/10.1002/pon.1789
Fouladi N, Feizi I, Nadermohammadi M, Mehrara E, Adldoosti R, Alimohammadi S (2021) The predictors of sexual satisfaction among iranian women with breast cancer. Asian Pac J Cancer Prev 22:391–396. https://doi.org/10.31557/apjcp.2021.22.2.391
Ooi PS, Draman N, Muhamad R, Yusoff SSM, Noor NM, Haron J, Hadi ISA (2021) Sexual dysfunction among women with breast cancer in the northeastern part of West Malaysia. Sex Med 9:100351. https://doi.org/10.1016/j.esxm.2021.100351
Basson R (2001) Female sexual response: the role of drugs in the management of sexual dysfunction. Obstet Gynecol 98:350–353. https://doi.org/10.1016/s0029-7844(01)01452-1
Sand M, Fisher WA (2007) Women’s endorsement of models of female sexual response: the nurses’ sexuality study. J Sex Med 4:708–719. https://doi.org/10.1111/j.1743-6109.2007.00496.x
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders. American Psychiatric Press, Arlington
Krychman M, Millheiser LS (2013) Sexual health issues in women with cancer. J Sex Med 10(Suppl 1):5–15. https://doi.org/10.1111/jsm.12034
Sears CS, Robinson JW, Walker LM (2018) A comprehensive review of sexual health concerns after cancer treatment and the biopsychosocial treatment options available to female patients. Eur J Cancer Care 27:e12738. https://doi.org/10.1111/ecc.12738
Sekse RJ, Råheim M, Gjengedal E (2015) Shyness and openness–common ground for dialogue between health personnel and women about sexual and intimate issues after gynecological cancer. Health Care Women Int 36:1255–1269. https://doi.org/10.1080/07399332.2014.989436
Dizon DS, Suzin D, McIlvenna S (2014) Sexual health as a survivorship issue for female cancer survivors. Oncologist 19:202–210. https://doi.org/10.1634/theoncologist.2013-0302
Marwick C (1999) Survey says patients expect little physician help on sex. JAMA 281:2173–2174. https://doi.org/10.1001/jama.281.23.2173
Aerts L, Christiaens MR, Enzlin P, Neven P, Amant F (2014) Sexual functioning in women after mastectomy versus breast conserving therapy for early-stage breast cancer: a prospective controlled study. Breast 23:629–636. https://doi.org/10.1016/j.breast.2014.06.012
Biglia N, Moggio G, Peano E, Sgandurra P, Ponzone R, Nappi RE, Sismondi P (2010) Effects of surgical and adjuvant therapies for breast cancer on sexuality, cognitive functions, and body weight. J Sex Med 7:1891–1900. https://doi.org/10.1111/j.1743-6109.2010.01725.x
Gandhi C, Butler E, Pesek S, Kwait R, Edmonson D, Raker C, Clark MA, Stuckey A, Gass J (2019) Sexual dysfunction in breast cancer survivors: is it surgical modality or adjuvant therapy? Am J Clin Oncol 42:500–506. https://doi.org/10.1097/coc.0000000000000552
Chang CP, Chen Y, Blackburn B, Abdelaziz S, Rowe K, Snyder J, Dodson M, Deshmukh V, Newman M, Stanford JB, Porucznik CA, Ose J, Fraser A, Smith K, Doherty J, Gaffney D, Hashibe M (2020) Genitourinary disease risks among ovarian cancer survivors in a population-based cohort study. Gynecol Oncol 157:529–535. https://doi.org/10.1016/j.ygyno.2020.02.028
Hu Q, Chang CP, Rowe K, Snyder J, Deshmukh V, Newman M, Fraser A, Smith K, Gren LH, Porucznik C, Stanford JB, Gaffney D, Henry NL, Lopez I, Hashibe M (2021) Disparities in cardiovascular disease risk among hispanic breast cancer survivors in a population-based cohort. JNCI Cancer Spectr. https://doi.org/10.1093/jncics/pkab016
Isac C, Lee P, Arulappan J (2021) Older adults with chronic illness: caregiver burden in the Asian context: a systematic review. Patient Educ Couns. https://doi.org/10.1016/j.pec.2021.04.021
Hernan MA, Hernandez-Diaz S, Werler MM, Mitchell AA (2002) Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Am J Epidemiol 155:176–184. https://doi.org/10.1093/aje/155.2.176
Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383
Lambert PC, Royston P (2009) Further development of flexible parametric models for survival analysis. Stata J 9:265–290. https://doi.org/10.1177/1536867x0900900206
Orsini N (2013) Review of flexible parametric survival analysis using stata: beyond the Cox model by Patrick Royston and Paul C. Lambert Stata J 13:212–216. https://doi.org/10.1177/1536867x1301300115
Gass JS, Onstad M, Pesek S, Rojas K, Fogarty S, Stuckey A, Raker C, Dizon DS (2017) Breast-specific sensuality and sexual function in cancer survivorship: does surgical modality matter? Ann Surg Oncol 24:3133–3140. https://doi.org/10.1245/s10434-017-5905-4
Sbitti Y, Kadiri H, Essaidi I, Fadoukhair Z, Kharmoun S, Slimani K, Ismaili N, Ichou M, Errihani H (2011) Breast cancer treatment and sexual dysfunction: Moroccan women’s perception. BMC Womens Health 11:29. https://doi.org/10.1186/1472-6874-11-29
Baumgart J, Nilsson K, Evers AS, Kallak TK, Poromaa IS (2013) Sexual dysfunction in women on adjuvant endocrine therapy after breast cancer. Menopause 20:162–168. https://doi.org/10.1097/gme.0b013e31826560da
Albornoz CR, Matros E, McCarthy CM, Klassen A, Cano SJ, Alderman AK, VanLaeken N, Lennox P, Macadam SA, Disa JJ, Mehrara BJ, Cordeiro PG, Pusic AL (2014) Implant breast reconstruction and radiation: a multicenter analysis of long-term health-related quality of life and satisfaction. Ann Surg Oncol 21:2159–2164. https://doi.org/10.1245/s10434-014-3483-2
Szegda KL, Whitcomb BW, Purdue-Smithe AC, Boutot ME, Manson JE, Hankinson SE, Rosner BA, Bertone-Johnson ER (2017) Adult adiposity and risk of early menopause. Hum Reprod 32:2522–2531. https://doi.org/10.1093/humrep/dex304
Tao X, Jiang A, Yin L, Li Y, Tao F, Hu H (2015) Body mass index and age at natural menopause: a meta-analysis. Menopause 22:469–474. https://doi.org/10.1097/gme.0000000000000324
Desmedt C, Fornili M, Clatot F, Demicheli R, De Bortoli D, Di Leo A, Viale G, de Azambuja E, Crown J, Francis PA, Sotiriou C, Piccart M, Biganzoli E (2020) Differential benefit of adjuvant docetaxel-based chemotherapy in patients with early breast cancer according to baseline body mass index. J Clin Oncol 38:2883–2891. https://doi.org/10.1200/jco.19.01771
Pajares B, Pollán M, Martín M, Mackey JR, Lluch A, Gavila J, Vogel C, Ruiz-Borrego M, Calvo L, Pienkowski T, Rodríguez-Lescure Á, Seguí MA, Tredan O, Antón A, Ramos M, Cámara Mdel C, Rodríguez-Martín C, Carrasco E, Alba E (2013) Obesity and survival in operable breast cancer patients treated with adjuvant anthracyclines and taxanes according to pathological subtypes: a pooled analysis. Breast Cancer Res 15:R105. https://doi.org/10.1186/bcr3572
Cornell LF, Mussallem DM, Gibson TC, Diehl NN, Bagaria SP, McLaughlin SA (2017) Trends in sexual function after breast cancer surgery. Ann Surg Oncol 24:2526–2538. https://doi.org/10.1245/s10434-017-5894-3
Carter J, Lacchetti C, Andersen BL, Barton DL, Bolte S, Damast S, Diefenbach MA, DuHamel K, Florendo J, Ganz PA, Goldfarb S, Hallmeyer S, Kushner DM, Rowland JH (2018) Interventions to address sexual problems in people with cancer: American society of clinical oncology clinical practice guideline adaptation of cancer care Ontario guideline. J Clin Oncol 36:492–511. https://doi.org/10.1200/jco.2017.75.8995
Halley MC, May SG, Rendle KA, Frosch DL, Kurian AW (2014) Beyond barriers: fundamental “disconnects” underlying the treatment of breast cancer patients’ sexual health. Cult Health Sex 16:1169–1180. https://doi.org/10.1080/13691058.2014.939227
Rosen R, Brown C, Heiman J, Leiblum S, Meston C, Shabsigh R, Ferguson D, D’Agostino R Jr (2000) The female sexual function index (FSFI): a multidimensional self-report instrument for the assessment of female sexual function. J Sex Marital Ther 26:191–208. https://doi.org/10.1080/009262300278597
Taylor S, Harley C, Ziegler L, Brown J, Velikova G (2011) Interventions for sexual problems following treatment for breast cancer: a systematic review. Breast Cancer Res Treat 130:711–724. https://doi.org/10.1007/s10549-011-1722-9
Steinauer J, LaRochelle F, Rowh M, Backus L, Sandahl Y, Foster A (2009) First impressions: what are preclinical medical students in the US and Canada learning about sexual and reproductive health? Contraception 80:74–80. https://doi.org/10.1016/j.contraception.2008.12.015
Warner C, Carlson S, Crichlow R, Ross MW (2018) Sexual health knowledge of U.S. medical students: a national survey. J Sex Med 15:1093–1102. https://doi.org/10.1016/j.jsxm.2018.05.019
Rubin ES, Rullo J, Tsai P, Criniti S, Elders J, Thielen JM, Parish SJ (2018) Best practices in North American pre-clinical medical education in sexual history taking: consensus from the summits in medical education in sexual health. J Sex Med 15:1414–1425. https://doi.org/10.1016/j.jsxm.2018.08.008
Shindel AW, Parish SJ (2013) Sexuality education in North American medical schools: current status and future directions. J Sex Med 10:3–17. https://doi.org/10.1111/j.1743-6109.2012.02987.x. (Quiz 18)
Bober SL, Reese JB, Barbera L, Bradford A, Carpenter KM, Goldfarb S, Carter J (2016) How to ask and what to do: a guide for clinical inquiry and intervention regarding female sexual health after cancer. Curr Opin Support Palliat Care 10:44–54. https://doi.org/10.1097/spc.0000000000000186
Flynn KE, Lindau ST, Lin L, Reese JB, Jeffery DD, Carter J, Baron SR, Abramsohn E, Weinfurt KP (2015) Development and validation of a single-item screener for self-reporting sexual problems in U.S. Adults J Gen Intern Med 30:1468–1475. https://doi.org/10.1007/s11606-015-3333-3
McGahuey CA, Gelenberg AJ, Laukes CA, Moreno FA, Delgado PL, McKnight KM, Manber R (2000) The arizona sexual experience scale (ASEX): reliability and validity. J Sex Marital Ther 26:25–40. https://doi.org/10.1080/009262300278623
Funding
This work was supported by grants from the NIH (R21 CA185811, R03 CA159357, M.Hashibe, PI), the Huntsman Cancer Institute, and the Cancer Control and Population Sciences Program (HCI Cancer Center Support Grant P30CA042014). This research was supported by the Utah Cancer Registry, which is funded by the National Cancer Institute's SEER Program, Contract No. HHSN261201800016I, the US Center for Disease Control and Prevention's National Program of Cancer Registries, Cooperative Agreement No. NU58DP007131, with additional support from the University of Utah and Huntsman Cancer Foundation. Research was supported by the NCRR grant, “Sharing Statewide Health Data for Genetic Research” (R01 RR021746, G. Mineau, PI) with additional support from the Utah Department of Health and Human Services and the University of Utah. Partial support for all datasets within the Utah Population Database is provided by the University of Utah, Huntsman Cancer Institute and the Huntsman Cancer Institute Cancer Center Support grant, P30 CA2014 from the National Cancer Institute, and Intermountain Healthcare. We thank the Utah Clinical and Translational Science Institute (CTSI) (funded by NIH Clinical and Translational Science Awards), the Pedigree and Population Resource, University of Utah Information Technology Services and Biomedical Informatics Core for establishing the Master Subject Index between the Utah Population Database and the University of Utah Health Sciences Center. The computational resources used were partially funded by the NIH Shared Instrumentation Grant 1S10OD021644-01A1.
Author information
Authors and Affiliations
Contributions
Conceptualization: CC, TH. Formal Analysis: CC. Funding Acquisition: MH. Investigation: CC, TH, MH. Methodology: CC, TH, MH. Writing (original draft): CC, TH, MH. Writing (review and editing): CC, TH, JS, MD, VD, MN, AD, NLH, MH.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chang, CP., Ho, T.F., Snyder, J. et al. Breast cancer survivorship and sexual dysfunction: a population-based cohort study. Breast Cancer Res Treat 200, 103–113 (2023). https://doi.org/10.1007/s10549-023-06953-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-023-06953-9