Abstract
Study Objective
Adolescent and young adult (AYA) women undergoing cancer treatment face unique reproductive health risks. This study aimed to assess the prevalence of sexual health counseling and contraception use in the oncology setting, and to identify patient factors associated with these outcomes.
Design
Retrospective chart review.
Setting
Yale New Haven Hospital from 2013 to 2018.
Participants
Female patients 15-25 years of age receiving cancer treatment, excluding those treated with surgery only.
Interventions
None.
Main Outcome Measures
Outcomes of documented sexual health counseling and contraception use were assessed for frequency. Associations between patient factors and these outcomes were assessed using Pearson χ2 and Fisher exact tests, and multivariate logistic regression was used to identify predictors of these outcomes.
Results
In this cohort (n = 157), the median age was 20.5 years, and the most common diagnoses were hematologic (40.8%) and thyroid (31.2%) malignancies. Of the patients, 33.1% were documented as receiving sexual health counseling, and 48.4% used contraception. Younger patients (15-20 years of age) were less likely to receive counseling (OR 0.31, 95% CI 0.14-0.70, P = .005). Receiving counseling (OR 3.36, 95% CI 1.35-8.34, P = .009) and sexual activity (OR 4.18, 95% CI 1.80-9.68, P = .001) were significantly associated with contraception use.
Conclusions
Sexual health counseling was documented infrequently during oncologic care for AYA women, especially for younger patients. However, such conversations were associated with a higher likelihood of contraception use. There is a need to improve rates of counseling in this high-risk setting, in which adolescents may be more vulnerable with regard to sexual health.
Key Words: Cancer, Adolescent, Young adult, Contraception, Sexual health, Reproductive health, Counseling
Introduction
Cancer among adolescents and young adults (AYAs) is relatively rare. In 2016, there were a total 1,658,716 new cases of cancer in the United states, of which 0.31% were among individuals 15-19 years of age, 0.49% were among those 20-24 years of age, and 0.83% were among those 25-29 years of age.1 Despite the rarity of cancer diagnoses in this population, because of their age and sex, adolescent and young adult female cancer patients face unique challenges, especially with regard to sexual and reproductive health.
According to data from the Centers for Disease Control and Prevention (CDC) national Youth Risk Behavior Survey, 55.8% of female adolescents report having had sexual intercourse by the 12th grade.2 It has been shown that AYAs with cancer engage in sexual relationships, often without consistent contraception or protection from sexually transmitted infections (STIs).3 Among adolescents with cancer who report having had sexual intercourse in their lifetime, there is an increased rate of early-onset sexual intercourse, a greater number of partners, more current sexual activity, and less use of protection.4 Even among those using contraception, many in this population use less effective methods.5
Women undergoing cancer treatment face significant reproductive health issues. Chemotherapy and radiation can have toxic effects on oocytes and embryos, potentially leading to infertility, spontaneous abortion, or fetal anomalies.6, 7, 8, 9 Education and counseling about reproductive and sexual health and access to contraception are therefore critical in the context of oncology care.
There is a need to better understand current patient and provider practices surrounding sexual health in this high-risk patient population. The aims of this study were, in a large tertiary care center, to determine the frequency of sexual health counseling provided by oncology providers to female AYA cancer patients receiving therapy; to determine the rates of contraception use in these patients; and to ascertain whether certain patient characteristics were associated with an increased or decreased likelihood of receiving such counseling or of using contraception. Although other studies have looked at rates of sexual health counseling and contraception use in groups of AYA cancer patients,5 , 10 , 11 none to our knowledge have examined how patient characteristics relate to both of these outcomes in this specific population. Obtaining information about the care currently provided to female AYA cancer patients will lead to a clearer understanding of unmet needs and will highlight possible opportunities for intervention.
Materials and Methods
Study Population
Approval was obtained from the Yale Institutional Review Board, after which a retrospective chart review was conducted. The Joint Data Analytics Team at Yale compiled a list of medical records fitting inclusion criteria for the study using information such as age, sex, and International Classification of Diseases, Tenth Revision (ICD-10) diagnosis codes for any type of cancer. Electronic medical records (EMR) were then manually reviewed to confirm eligibility and to gather data. Only patients who met all eligibility criteria based on manual medical record review were included in the final analysis.
Inclusion criteria for the study required patients to be female, between the ages of 15.0 and 25.99 years, with a new diagnosis of malignancy between the years 2013 and 2018, and receiving initial cancer directed therapy at Yale New Haven Hospital. Cancer treatment modalities included surgery, radiation, chemotherapy, hormone-based therapy, targeted or biologic treatments, and bone marrow transplantation. Patients treated with surgery alone were excluded from this study. Other exclusion criteria included a history of hysterectomy or removal of both ovaries and/or fallopian tubes prior to cancer diagnosis or as the first stage of treatment, as well as being pregnant at the time of the cancer diagnosis.
Variables and Data Collection
Primary outcomes assessed in this study included documented sexual health counseling by an oncology provider, as well as contraception use. Sexual health counseling was defined as documentation in the EMR of a conversation related to contraception use or pregnancy prevention during cancer treatment. Contraception use was defined as documentation of condoms and/or prescription contraception of any kind being used during the treatment period.
Other information gathered from the EMR, and included in this analysis as independent variables, included demographic data, types of cancer diagnosis and treatments received, obstetric history, specific contraceptive methods used, and sexual history. Documented sexual health counseling was considered in this study both as a dependent variable and as an independent variable in its relation to contraceptive use.
Medical records were reviewed starting from the initial diagnostic workup through remission or death, whichever occurred first. To extract data from the medical records, provider notes were reviewed, as well as designated areas of the EMR for sexual history. In addition, the medical records were searched using predetermined search terms to ensure that information was not missed. These search terms included the following: sex, sexual, sexually, sexual activity, sexually active, condom, barrier, contraception, contraceptive, birth control, OCP, IUD, Mirena, Paragard, Depo, implant, Nexplanon, pregnant, and pregnancy.
Statistical Analysis
Frequencies were calculated for all independent and dependent variables. Bivariate associations between each independent variable and the outcome variable of documented sexual health counseling were assessed using Pearson χ2 and Fisher exact tests. Multivariate logistic regression models were then constructed to identify predictors of the outcome of documented sexual health counseling. Variables with P values <0.2 on univariate analysis were entered into the multiple logistic regression model. The variable of age was also included in the multivariate analysis on the basis of clinical significance. The same process was repeated for the dependent variable of contraception use.
Associations in the multivariate model between independent variables and the outcomes of receiving counseling or using contraception were reported as odds ratios (OR) with 95% confidence intervals (CI), and level of significance considered to be at α = .05. Statistical analysis was completed using Stata version 15.0 (StataCorp, College Station, TX).
Sample size adequacy was determined based on the rule of thumb for logistic regression that for each independent variable included, the sample must contain a minimum of 10 events per variable.12 In this study, 157 eligible patient medical records were identified, of which there were 52 cases of patients who received sexual health counseling and 76 cases of patients using contraception. Therefore, the 2 logistic regression models for these 2 dependent variables could contain up to 5 and 7 independent variables, respectively. Fewer independent variables entered the final models based on the process described above; therefore, the sample size was considered adequate.
Results
A total of 157 eligible patient medical records were identified. Table 1 describes the demographics and clinical characteristics of these patients. All patients were female, and the mean age was 20.5 years. Of the patients, 70.1% were white/Caucasian, 81.5% were non-Hispanic, and 89.8% were single. The most common type of cancer was hematologic, comprising 40.8% of the patients, followed by thyroid cancer in 31.2%. For treatment, 52.2% underwent surgery, 60.5% received chemotherapy, and 52.2% received radiation.
Table 1.
Patient Demographics and Clinical Characteristics (n = 157)
n | % | |
---|---|---|
Age range, y | ||
15-20 | 80 | 51.0 |
21-25 | 77 | 49.0 |
Race | ||
Asian | 11 | 7.0 |
Black or African American | 13 | 8.3 |
White or Caucasian | 110 | 70.1 |
Other/not listed | 23 | 14.6 |
Ethnicity | ||
Hispanic or Latina | 29 | 18.5 |
Not Hispanic or Latina | 128 | 81.5 |
Marital Status | ||
Single | 141 | 89.8 |
Married or other | 16 | 10.2 |
Cancer type | ||
Breast | 9 | 5.7 |
Gynecologic | 8 | 5.1 |
Hematologic | 64 | 40.8 |
Neurologic | 15 | 9.6 |
Sarcoma | 8 | 5.1 |
Thyroid | 49 | 31.2 |
Other | 4 | 2.5 |
Treatment | ||
Surgery | 82 | 52.2 |
Chemotherapy | 95 | 60.5 |
Radiation | 82 | 52.2 |
Bone marrow transplant | 8 | 5.1 |
Hormone therapy | 7 | 4.5 |
Targeted/biologic therapy | 28 | 17.8 |
Prior pregnancy | ||
Yes | 13 | 8.3 |
No | 144 | 91.7 |
Sexually active | ||
Yes | 56 | 35.7 |
No | 56 | 35.7 |
Not documented | 45 | 28.7 |
Contraception use | ||
Yes | 76 | 48.4 |
No | 81 | 51.6 |
Sexual health counseling | ||
Yes | 52 | 33.1 |
No | 105 | 66.9 |
In all, 91.7% of patients had never been pregnant, and 28.7% did not have sexual activity status documented anywhere in the medical record. Of those who did have documented sexual activity status (71.3% of the total cohort), half were sexually active. Of those documented as sexually active, 82.1% had male partners and 7.1% had female partners. The remaining sexually active patients did not have the sex of their partner(s) documented.
Only 33.1% of patients in this study received sexual health counseling. Table 2 shows associations between patient characteristics and documented sexual health counseling based on Pearson χ2 or Fisher exact tests. Table 3 shows the variables that were found to be statistically significant predictors of having documented sexual health counseling based on multivariate logistic regression. Younger age (age 15-20 years) was significantly associated with a lower likelihood of documented sexual health counseling (OR 0.31, 95% CI 0.14-0.70, P = .005), and Hispanic or Latina ethnicity was associated with a greater likelihood (OR 6.07, 95% CI 1.81-20.40, P = .004). Having had at least 1 prior pregnancy also had a significant association (OR 4.93, 95% CI 1.31-18.57, P = .018).
Table 2.
Frequency of Documented Sexual Health Counseling and Contraception Use Across Patient Characteristics
Characteristic | Documented Sexual Health Counseling |
Contraception Use |
||
---|---|---|---|---|
n (%) | P value∗ | n (%) | P value∗ | |
Age, y | .011 | .581 | ||
15-20 (n = 80) | 19 (23.8) | 37 (46.3) | ||
21-25 (n = 77) | 33 (42.9) | 39 (50.6) | ||
Race | .070 | .778 | ||
Asian (n = 11) | 1 (9.1) | 6 (54.5) | ||
Black or African American (n = 13) | 3 (23.1) | 6 (46.2) | ||
White or Caucasian (n = 110) | 36 (32.7) | 55 (50.0) | ||
Other/not specified (n = 23) | 12 (52.2) | 9 (39.1) | ||
Ethnicity | .001 | .987 | ||
Hispanic or Latino (n = 29) | 17 (58.6) | 14 (48.3) | ||
Not Hispanic or Latino (n = 128) | 35 (27.3) | 62 (48.4) | ||
Marital Status | .340 | .508 | ||
Married/other (n = 16) | 7 (43.8) | 9 (56.3) | ||
Single (n = 141) | 45 (31.9) | 67 (47.5) | ||
Cancer Type | .595 | .785 | ||
Breast (n = 9) | 3 (33.3) | 4 (44.4) | ||
Gynecologic (n = 8) | 2 (25.0) | 5 (62.5) | ||
Hematologic (n = 64) | 21 (32.8) | 29 (45.3) | ||
Neurologic (n = 15) | 3 (20.0) | 7 (46.7) | ||
Sarcoma (n = 8) | 4 (50.0) | 6 (75.0) | ||
Thyroid (n = 49) | 19 (38.8) | 23 (46.9) | ||
Other (n = 4) | 0 (0.0) | 2 (50.0) | ||
Surgery | .775 | .824 | ||
Yes (n = 82) | 28 (34.1) | 39 (47.6) | ||
No (n = 75) | 24 (32.0) | 37 (49.3) | ||
Chemotherapy | .594 | .741 | ||
Yes (n = 95) | 33 (34.7) | 47 (49.5) | ||
No (n = 62) | 19 (30.6) | 29 (46.8) | ||
Radiation | .532 | .824 | ||
Yes (n = 82) | 29 (35.4) | 39 (47.6) | ||
No (n = 75) | 23 (30.7) | 37 (49.3) | ||
Bone marrow transplant | .441 | 1.000 | ||
Yes (n = 8) | 4 (50.0) | 4 (50.0) | ||
No (n = 149) | 48 (32.2) | 72 (48.3) | ||
Hormone therapy | .686 | .713 | ||
Yes (n = 7) | 3 (42.9) | 4 (57.1) | ||
No (n = 150) | 49 (32.7) | 72 (48.0) | ||
Targeted/biologic therapy | .314 | .852 | ||
Yes (n = 28) | 7 (25.0) | 14 (50.0) | ||
No (n = 129) | 45 (34.9) | 62 (48.1) | ||
Prior pregnancy | .010 | .682 | ||
Yes (n = 13) | 9 (69.2) | 7 (53.8) | ||
No (n = 144) | 43 (29.9) | 69 (47.9) | ||
Sexual activity | .327 | .000 | ||
Yes (n = 56) | 23 (41.1) | 39 (69.6) | ||
No (n = 56) | 18 (32.1) | 20 (35.7) | ||
Documented sexual health counseling | 0.003 | |||
Yes (n = 52) | — | — | 34 (65.4) | |
No (n = 105) | — | — | 42 (40.0) |
Unadjusted comparisons, P values based on Pearson χ2 and Fisher exact tests.
Table 3.
Predictors of Sexual Health Counseling Based on Multivariate Logistic Regression
Characteristic | OR | 95% CI | P Value | ||
---|---|---|---|---|---|
Age | |||||
15-20 | 0.31 | 0.14-0.70 | .005 | ||
21-25 | |||||
Ethnicity | |||||
Hispanic or Latina | 6.07 | 1.81-20.40 | .004 | ||
Not Hispanic or Latina | |||||
Prior Pregnancy | |||||
Yes | 4.93 | 1.31-18.57 | .018 | ||
No |
CI, confidence interval; OR, odd ratio.
In all, 48.4% of patients were documented as using a contraceptive method during their cancer treatment. Contraceptive methods used are shown in Figure 1 . The most popular method used was combination oral contraceptive pills (COCP), with 24.2% of all patients (50.0% of those using contraception) using this method. Long-acting reversible contraceptive (LARC) methods, including intrauterine devices (IUD) and implants, were used by 5.7% of all patients (11.8% of those using contraception).
Fig. 1.
Contraceptive methods used by patients undergoing cancer treatment (n = 157). When a patient was documented as using more than 1 method (simultaneously or sequentially), the most effective type based on World Health Organization tiers of contraceptive effectiveness13 is listed. If 2 methods of the same efficacy were used sequentially, the first method used is listed.
Table 2 shows associations between patient characteristics and any contraception use based on Pearson χ2 and Fisher exact tests. In all, 69.6% of patients who were sexually active were documented as using contraception. Table 4 shows the variables that were found to be statistically significant predictors of contraception use based on multivariate logistic regression. Sexual activity was significantly associated with contraception use (OR 4.18, 95% CI 1.80-9.68, P = .001). Having documented sexual health counseling was associated with more than 3 times the likelihood of using contraception compared to not having documented counseling (OR 3.36, 95% CI 1.35-8.34, P = .009). There were no pregnancies or positive pregnancy tests during cancer treatment documented in the medical records of this cohort.
Table 4.
Predictors of Contraception Use Based on Multivariate Logistic Regression
Characteristic | OR | 95% CI | P Value |
---|---|---|---|
Sexual activity | |||
Yes | 4.18 | 1.80-9.68 | .001 |
No | |||
Received Sexual health Counseling | |||
Yes | 3.36 | 1.35-8.34 | .009 |
No |
CI, confidence interval; OR, odd ratio.
Discussion
The goal of this study was to assess the frequency of sexual health counseling and contraception use among AYA female cancer patients, whether there is an unmet need in this area, and whether certain factors make patients more or less likely to receive these services.
The National Comprehensive Cancer Network (NCCN) notes that reproductive health and contraception should be discussed with AYA patients prior to starting treatment.14 However, results of this study show that a minority of patients (only 33.1%) have any such counseling documented. This is a larger percentage compared to other retrospective studies looking at different subsets of the AYA cancer population.10 , 11
Commonly cited barriers to sexual health counseling for AYA cancer patients include limited provider knowledge about contraception, severity of patient illness, the belief that sick patients are not sexually active, time constraints, or the assumption that patients will bring the topic up if needed.15, 16, 17 This study showed that the younger subset of AYA patients were less likely to be counseled. Potential reasons for this include false assumptions about sexual activity in this age group,18 a focus on survivorship,17 parental influence,19, 20, 21 and patient reluctance to discuss sexual health with their oncology providers.3 , 22
Approximately half of the patients in this cohort had documentation demonstrating contraception. Of the patients without documented contraception use, although some were not sexually active, many were (including specifically documented as sexually active with men), and many did not have sexual activity status documented. It is likely that there were patients who had unmet contraceptive needs. The most common birth control method in this cohort was COCP, with LARC options being less common, similar to patterns seen in the general population of healthy women23 , 24 and in other cohorts of cancer patients.5 It is recommended that adolescents be counseled on the range of reversible contraceptive methods, including LARC, and that all contraceptives options be readily accessible to them.25 Although the reason for the lower rate is unknown, our findings may demonstrate another unmet need and a possible area for intervention, as LARC options have several benefits in this population including highly effective contraception and, in some cases, reduction of menstrual blood loss.26
In this study, not surprisingly, sexual activity was associated with increased rates of contraception. However, sexual activity was not associated with higher rates of sexual health counseling. Controlling for sexual activity, however, the data did show that documented sexual health counseling was associated with increased rates of contraception use. This is an encouraging finding, showing that counseling is associated with a clinically meaningful benefit. This finding is corroborated by other research, including survey research in AYA cancer patients among whom contraceptive counseling was associated with higher rates of more effective contraception.5
The impact of cancer treatment on fertility is more commonly discussed in this population. The potential loss of fertility can be a major source of psychosocial distress for AYA cancer patients; and women of reproductive age with gynecologic malignancies face additional distress, as these diagnoses and their treatment may uniquely affect fertility, sexuality, and identity.27 , 28 Education about options for fertility preservation is key. Embryo and oocyte cryopreservation may be options for women facing potential infertility secondary to treatment for any type of malignancy. Newer methods of fertility-sparing surgery now exist for certain gynecologic malignancies, and oophropexy may be an option to shield reproductive organs from radiation therapy.6 , 29
Discussions of fertility are critically important for their own sake, but also as they relate to other aspects of sexual health. Conversations about fertility preservation may lead AYA patients to develop incorrect beliefs about their fertility and underestimate their risk of pregnancy.30 Studies have shown that young adult female cancer survivors were significantly more likely to have unintended pregnancies compared to the general population, to have pregnancies ending in medical abortions compared to healthy age-matched siblings, and to use emergency contraception more than the general population.31, 32, 33 Of those survivors with a history of chemotherapy, having the perception of infertility is predictive of contraception nonuse, even without clinical evidence of infertility.34 As such, discussions about fertility preservation provide an ideal opportunity to provide education about the continued need for contraception.
This study had several strengths. Although there is an existing body of literature examining the intersection between gynecology and adolescent and young adult oncology as it relates to infertility and fertility preservation, little is known about sexual health counseling and contraception use in this population. This study adds to the existing limited body of literature by examining a population with a wide age range and diversity in cancer type. Importantly, our study identifies characteristics of patients who are less likely to receive sexual health counseling and less likely to use contraception. This, in turn, identifies potential opportunities for intervention.
There are several limitations of this study. As a retrospective chart review, these data are based on documentation, which may not always be accurate. It is possible that some patients received counseling, but those conversations were not documented. Documentation of contraception prescriptions do not necessarily translate into contraception use, and rates of condom use may have been underestimated. Sexual activity status was often missing from the medical record, and it is possible that the documented information was sometimes inaccurate, as sexual activity can change over time. Despite these limitations, it is important to highlight what is and is not documented; as such, this study is informative about the current landscape of sexual health care for female AYA patients undergoing cancer treatment.
In conclusion, this study showed that a majority of AYA female patients undergoing cancer treatment did not have documented sexual health counseling, and that many did not have documentation indicating contraception use. However, patients who received counseling were more likely to use contraception. There appears to be a need for increased rates of sexual health counseling in female AYA cancer patients. Efforts should be made to explore and to overcome current barriers, especially for the younger, adolescent patients, who may represent an especially vulnerable subset of this population. Addressing the major barriers that limit the provision of sexual health care in the oncology context may optimize comprehensive care for these patients.
Footnotes
Neither of the authors has any disclosures or conflicts of interest.
No funding was received for this work.
Accepted for poster presentation at the American College of Obstetricians and Gynecologists Annual Clinical and Scientific Meeting, Seattle, WA, April 24-27, 2020 (conference canceled due to COVID-19).
References
- 1.Centers for Disease Control and Prevention United States cancer statistics: data visualizations. 2019. www.cdc.gov/cancer/dataviz Available at:
- 2.Kann L., McManus T., Harris W.A. Youth risk behavior surveillance; United States, 2017. MMWR Surveill Summ. 2018;67:1. doi: 10.15585/mmwr.ss6708a1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Rosenberg A.R., Bona K., Ketterl T. Intimacy, substance use, and communication needs during cancer therapy: a report from the "resilience in adolescents and young adults" study. J Adolesc Health. 2017;60:93. doi: 10.1016/j.jadohealth.2016.08.017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Carpentier M.Y., Mullins L.L., Elkin T.D. Prevalence of multiple health-related behaviors in adolescents with cancer. J Pediatr Hematol Oncol. 2008;30:902. doi: 10.1097/MPH.0b013e318186533f. [DOI] [PubMed] [Google Scholar]
- 5.Maslow B.S., Morse C.B., Schanne A. Contraceptive use and the role of contraceptive counseling in reproductive-aged women with cancer. Contraception. 2014;90:79. doi: 10.1016/j.contraception.2014.03.002. [DOI] [PubMed] [Google Scholar]
- 6.Rodriguez-Wallberg K.A. Principles of cancer treatment: impact on reproduction. In: Quinn G.P., Vadaparampil S.T., editors. Reproductive Health and Cancer in Adolescents and Young Adults. Springer; Dordrecht: 2012. pp. 1–8. [Google Scholar]
- 7.Laurence V., Rousset-Jablonski C. Contraception and cancer treatment in young persons. In: Quinn G.P., Vadaparampil S.T., editors. Reproductive Health and Cancer in Adolescents and Young Adults. Springer; Dordrecht: 2012. pp. 41–60. [Google Scholar]
- 8.Leslie K.K., Koil C., Rayburn W.F. Chemotherapeutic drugs in pregnancy. Obstet Gynecol Clin North Am. 2005;32:627. doi: 10.1016/j.ogc.2005.08.009. [DOI] [PubMed] [Google Scholar]
- 9.Silva C., Chung F.S. Pregnancy and cancer. In: Quinn G.P., Vadaparampil S.T., editors. Reproductive Health and Cancer in Adolescents and Young Adults. Springer; Dordrecht: 2012. pp. 89–102. [Google Scholar]
- 10.Johansen S.L., Lerma K., Shaw K.A. Contraceptive counseling in reproductive-aged women treated for breast cancer at a tertiary care institution: a retrospective analysis. Contraception. 2017;96:248. doi: 10.1016/j.contraception.2017.06.004. [DOI] [PubMed] [Google Scholar]
- 11.Wang Y., Chen L., Ruan J.Y. Discussions about reproductive and sexual health among young adult survivors of cancer. Cancer Med. 2016;5:1037. doi: 10.1002/cam4.666. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Peduzzi P., Concato J., Kemper E. A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol. 1996;49:1373. doi: 10.1016/s0895-4356(96)00236-3. [DOI] [PubMed] [Google Scholar]
- 13.World Health Organization Department of Reproductive Health and Research (WHO/RHR) and Johns Hopkins Bloomberg School of Public Health/Center for Communication Programs (CCP) CCP and WHO; Baltimore and Geneva: 2018. Knowledge for Health Project: Family planning: a global handbook for providers (2018 update) [Google Scholar]
- 14.Coccia P.F., Pappo A.S., Beaupin L. Adolescent and young adult oncology, version 2.2018, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2018;16:66. doi: 10.6004/jnccn.2018.0001. [DOI] [PubMed] [Google Scholar]
- 15.Frederick N.N., Campbell K., Kenney L.B. Barriers and facilitators to sexual and reproductive health communication between pediatric oncology clinicians and adolescent and young adult patients: the clinician perspective. Pediatr Blood Cancer. 2018;65:e27087. doi: 10.1002/pbc.27087. [DOI] [PubMed] [Google Scholar]
- 16.Eisenberg D.L., Stika C., Desai A. Providing contraception for women taking potentially teratogenic medications: a survey of internal medicine physicians’ knowledge, attitudes and barriers. J Gen Intern Med. 2010;25:291. doi: 10.1007/s11606-009-1215-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Murphy D., Klosky J.L., Reed D.R. The importance of assessing priorities of reproductive health concerns among adolescent and young adult patients with cancer. Cancer. 2015;121:2529. doi: 10.1002/cncr.29466. [DOI] [PubMed] [Google Scholar]
- 18.Dobinson K.A., Hoyt M.A., Seidler Z.E. A grounded theory investigation into the psychosexual unmet needs of adolescent and young adult cancer survivors. J Adolesc Young Adult Oncol. 2016;5:135. doi: 10.1089/jayao.2015.0022. [DOI] [PubMed] [Google Scholar]
- 19.Stinson J.N., Jibb L.A., Greenberg M. A qualitative study of the impact of cancer on romantic relationships, sexual relationships, and fertility: perspectives of Canadian adolescents and parents during and after treatment. J Adolesc Young Adult Oncol. 2015;4:84. doi: 10.1089/jayao.2014.0036. [DOI] [PubMed] [Google Scholar]
- 20.Quinn G.P., Knapp C., Murphy D. Congruence of reproductive concerns among adolescents with cancer and parents: pilot testing an adapted instrument. Pediatrics. 2012;129:e930. doi: 10.1542/peds.2011-2568. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Murphy D., Klosky J.L., Termuhlen A. The need for reproductive and sexual health discussions with adolescent and young adult cancer patients. Contraception. 2013;88:215. doi: 10.1016/j.contraception.2012.08.041. [DOI] [PubMed] [Google Scholar]
- 22.Frederick N.N., Revette A., Michaud A. A qualitative study of sexual and reproductive health communication with adolescent and young adult oncology patients. Pediatr Blood Cancer. 2019;66:e27673. doi: 10.1002/pbc.27673. [DOI] [PubMed] [Google Scholar]
- 23.Daniels K., Abma J.C. NCHS Data Brief, no 327, Hyattsville, MD: National Center for Health Statistics; 2018. Current contraceptive status among women ages 15-49: United States, 2015-2017. [Google Scholar]
- 24.Kavanaugh M.L., Jerman J. Contraceptive method use in the United States: trends and characteristics between 2008, 2012 and 2014. Contraception. 2018;97:14. doi: 10.1016/j.contraception.2017.10.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.American College of Obstetricians and Gynecologists: ACOG committee opinion no 735: adolescents and long-acting reversible contraception: implants and intrauterine devices. Obstet Gynecol. 2018;131:e130. doi: 10.1097/AOG.0000000000002632. [DOI] [PubMed] [Google Scholar]
- 26.American College of Obstetricians and Gynecologists: Committee opinion no 606: options for prevention and management of heavy menstrual bleeding in adolescent patients undergoing cancer treatment. Obstet Gynecol. 2014;124:397. doi: 10.1097/01.AOG.0000452745.44206.c3. [DOI] [PubMed] [Google Scholar]
- 27.Lagana A.S., La Rosa V.L., Rapisarda A.M. Psychological impact of fertility preservation techniques in women with gynaecological cancer. Ecancermedicalscience. 2017;11:ed62. doi: 10.3332/ecancer.2017.ed62. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Vitale S.G., La Rosa V.L., Rapisarda A.M.C. Fertility preservation in women with gynaecologic cancer: the impact on quality of life and psychological well-being. Hum Fertil (Camb) 2018;21:35. doi: 10.1080/14647273.2017.1339365. [DOI] [PubMed] [Google Scholar]
- 29.La Rosa V.L., Shah M., Kahramanoglu I. Quality of life and fertility preservation counseling for women with gynecological cancer: an integrated psychological and clinical perspective. J Psychosom Obstet Gynaecol. 2020;41:86. doi: 10.1080/0167482X.2019.1648424. [DOI] [PubMed] [Google Scholar]
- 30.Wright C.I., Coad J., Morgan S. ‘Just in case’: the fertility information needs of teenagers and young adults with cancer. Eur J Cancer Care (Engl) 2014;23:189. doi: 10.1111/ecc.12137. [DOI] [PubMed] [Google Scholar]
- 31.Green D.M., Whitton J.A., Stovall M. Pregnancy outcome of female survivors of childhood cancer: a report from the Childhood Cancer Survivor Study. Am J Obstet Gynecol. 2002;187:1070. doi: 10.1067/mob.2002.126643. [DOI] [PubMed] [Google Scholar]
- 32.Medica A.C.O., Stark S.S., Hadnott T.N. Use of emergency contraception among female young adult cancer survivors. Fertil Steril. 2018;109:1114. doi: 10.1016/j.fertnstert.2018.02.136. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Quinn M.M., Letourneau J.M., Rosen M.P. Contraception after cancer treatment: describing methods, counseling, and unintended pregnancy risk. Contraception. 2014;89:466. doi: 10.1016/j.contraception.2014.01.014. [DOI] [PubMed] [Google Scholar]
- 34.Hadnott T.N., Stark S.S., Medica A. Perceived infertility and contraceptive use in the female, reproductive-age cancer survivor. Fertil Steril. 2019;111:763. doi: 10.1016/j.fertnstert.2018.12.016. [DOI] [PMC free article] [PubMed] [Google Scholar]