Background
Approximately 90,000 adolescents and young adults (AYAs) aged 15 to 39 years are diagnosed with cancer annually.1 The incidence of cancer in this population is increasing; however, this population has historically not witnessed the same advances in survival as their pediatric or adult counterparts.2–7 Reasons for inferior survival are varied and include differing cancer biology,8 poor clinical trial participation,9–11 unique developmental and psychosocial issues,12–14 challenges accessing oncology care,15,16 poorer socioeconomic status, and lack of insurance coverage.17–19
Identification of poor survival outcomes for AYAs was concurrently recognized in the early 2000s by the National Cancer Institute (NCI) alongside young adult survivors leading grassroots efforts advocating for advancements in their care. Together, AYA advocacy organizations and the NCI formed an AYA Oncology Progress Review Group (AYAO PRG) in 2006 that highlighted the need for increased AYA oncology (AYAO) awareness, research, education and training of providers, optimal service delivery, and patient advocacy and support.18
AYAO is now recognized as a distinct specialty. Over the past decade, all major national cancer organizations have joined in the recommendation18,20–22 that AYAs with cancer should be treated within an AYAO program and by healthcare professionals who specialize in this population. Despite awareness of AYAO patients as a distinct population, the current state of AYAO care at cancer centers across the United States is unknown. Many cancer centers have existing AYAO programs; however, the structure, design, and program resources are largely unknown and vary between institutions. This survey study sought to evaluate the current services and delivery models of AYAO specific programs at NCI-designated Cancer Centers (NCI-CCs), as well as perceptions of how well they deliver care.
Patients and Methods
Survey Development
The Institutional Review Board at Case Western Reserve University approved this study and waived requirement for informed consent. The questionnaire was constructed by multiple authors (K. Daunov, K. Noskoff, H. Gan, R.T. Lee) and reviewed by a focus group of experts in AYAO from both pediatric and internal medicine backgrounds; their feedback informed the final version of the questionnaire and assessed time for completion. The first section addressed participant and institution demographic information and assessed presence of a unique AYAO program. Participants with an established AYAO program were questioned about program makeup and design. The second section administered to all participants addressed comprehensive resources available to all oncology patients in addition to presence of providers with any amount of clinical effort (full-time equivalent [FTE] >0.1) dedicated solely to AYAO patients. The third section more specifically addressed aspects of AYAO care, including fertility preservation, sexual health, survivorship, psychosocial services, research, provider education, and palliative/supportive oncology (eAppendix 1, available with this article at JNCCN.org).
Survey Process
AYAO program contacts and cancer center directors were identified via online directory search for all clinical NCI-CCs. Surveys were not sent to NCI Basic Laboratory Cancer Centers. Teen Cancer America’s contact list was used as a cross reference to confirm the correct contact for each identified institution. An initial email introduced the purpose of the survey and asked for study participation. A follow-up email with a unique URL link for an online questionnaire was subsequently emailed to participants through the REDCap system. Weekly reminders were emailed to nonresponders for a duration of 8 weeks. A $25 Amazon eGift Card was provided upon completion of the survey. Surveys required 75% responses to questions to be considered complete and included in the analysis.
Statistical Analysis
All data were coded and checked for errors by the research team (K. Daunov, M. Daunov, R.T. Lee). Missing data were excluded from the analysis. Descriptive statistics were used to summarize survey responses. SPSS Statistics, version 16 (SPSS Inc) and STATA, version 12.0 (StataCorp LP) were used for statistical analysis.
Results
Survey Respondents
A total of 55 survey responses were received from 50 of 64 NCI-CCs, for a 78% response rate. Multiple responses were received from 4 institutions; these centers were contacted and discrepancies in their responses were clarified into a single cohesive response and/or the most appropriate respondent was identified. For 5 institutions, multiple surveys were allowed when adult and pediatric programs at a single institution were deemed separate and not unified. The majority of NCI-CC survey respondents were pediatric oncologists (53%), adult oncologists (11%), and social workers (11%), and 28% were of other backgrounds, such as AYAO program manager/director.
AYAO Programs
Overall, 51% of survey respondents reported having an existing AYAO program; 31% percent reported plans to develop a future program, 15% did not have a program, and 4% of respondents were unsure if they had an AYAO program. Most existing programs (66%) had been started in the past 5 years, with a small number (14%) in existence ≥10 years. Of existing AYAO programs, most saw patients aged 15 years (55%) to 39 years (66%). Approximately one-fourth of existing programs (24%) had a minimum age of 13 years for their AYAO program. Most AYAO programs (59%) had a program that was combined between medical and pediatric oncology. One-fourth (24%) of AYAO programs were embedded in pediatrics alone. An overwhelming majority (93%) of AYAO programs provided services to patients with all types of malignancies, and for patients on treatment or in survivorship (96%). Centers reported a range of new AYAO patients visits per month: 0–25 (35%), 25–50 (22%), 50–100 (9%), 100–300 (20%), and >300 (15%). A similar range of AYAO follow-up visits per month were also reported (Table 1).
Program Presence and Demographics
Oncology Services
Most respondents reported patient access to pediatric or medical oncology (87% for both). In regard to supportive care services available, >90% of NCI-CCs provided social work (98%), physical therapy (98%), dietician services (98%), chaplaincy (98%), oncology survivorship (96%), supportive/palliative oncology (96%), psychiatry (95%), nurse coordinator (93%), and financial services (91%). Other less available services included insurance counseling (84%), child life services (82%), art therapy (82%), music therapy (80%), integrative oncology (69%), meditation (69%), acupuncture (62%), academic support services (62%), and yoga therapy (60%).
AYAO Dedicated Providers, Services, and Spaces
In contrast, the prevalence of dedicated AYAO providers (any FTE >0.1 devoted solely to the care of AYAs) was much less. Only 60% reported a dedicated AYA pediatric oncologist and 47% for an AYA medical oncologist. Other dedicated AYA support services included program coordinator (60%), social work (58%), psychology (54%), nurse coordinator (51%), advanced practice provider (41%), research coordinator (38%), administrative assistant (31%), child life services (28%), music therapy (28%), dietician services (23%), physical therapy (17%), psychiatry (17%), and chaplaincy (17%) (Figure 1).
Comparison of comprehensive versus AYA-dedicated oncology resources.
Abbreviation: AYA, adolescent and young adult.
aPrograms not asked about general availability.
Citation: Journal of the National Comprehensive Cancer Network 21, 5; 10.6004/jnccn.2023.7001
Comparison of comprehensive versus AYA-dedicated oncology resources.
Abbreviation: AYA, adolescent and young adult.
aPrograms not asked about general availability.
Citation: Journal of the National Comprehensive Cancer Network 21, 5; 10.6004/jnccn.2023.7001
Comparison of comprehensive versus AYA-dedicated oncology resources.
Abbreviation: AYA, adolescent and young adult.
aPrograms not asked about general availability.
Citation: Journal of the National Comprehensive Cancer Network 21, 5; 10.6004/jnccn.2023.7001
Among established AYAO programs, most provided services to patients in their main campus outpatient clinic (93%), with less than one-fifth (18%) reporting a dedicated outpatient space or an outpatient satellite clinic location (18%). Seventy-five percent provided AYAO inpatient consultation, 18% reported a dedicated inpatient AYAO service, and only 7% reported presence of a dedicated inpatient unit. Eighteen percent reported a dedicated outpatient AYAO lounge, and half reported having a dedicated inpatient lounge (Table 2).
AYA Physical Space and Social Presence
Fertility Preservation and Sexual Health
All NCI respondents reported offering fertility preservation at their center. Approximately half of centers (51%) offered fertility preservation at diagnosis regardless of risk, 55% reported fertility preservation based on risk stratification, slightly more than one-quarter (26%) offered it based upon patient request, and a minority of centers (9%) reported requiring documentation of discussion/fertility preservation as being mandatory in the electronic medical record. Patients were counseled by a primary oncology provider (76%), reproductive endocrinologist (64%), advanced practice provider (47%), social workers (36%), and registered nurses (31%). Only two-thirds of NCI centers (64%) reported providing sexual health services to patients. A small number of NCI cancer centers (7%) offered referral to a community fertility clinic not affiliated with their center. Most (78%) provided services if requested by patients. To a lesser extent, respondents reported sexual health being addressed in the survivorship phase (47%) or during a routine patient appointment (36%). Less than half (44%) of centers reported having sexual health patient education materials available. Similar to fertility preservation, sexual health was primarily addressed by the primary oncology team (67%) or through referral to a sexual health provider (44%) (Table 3).
Aspects of AYAO Care
Survivorship
Most NCI respondents affirmed the presence of a survivorship clinic (94%), with most being provided in a dedicated cancer survivors clinic (82%) (Table 3). Time frame of transition to survivorship care was mixed, with 27% of centers reporting that this occurs at completion of treatment, 6% at 1 year after treatment, 31% at 2 years after treatment, 15% at 3 years after treatment, and 9% at 5 years after treatment (Table 3). A little more than half of centers (58%) had a transitional survivorship care plan, 44% offered academic support or school reintegration services in survivorship, and 42% offered peer support to cancer survivors.
Palliative and End-of-Life Care
Most NCI centers (78%) reported offering pediatric and adult palliative care services, whereas a few centers reported not providing any palliative care services to pediatric (16%) or adult patients (9%). Approximately one-half of centers offered pediatric or adult palliative care inpatient (53% and 51%, respectively) as well as outpatient (49%) services. Few had a dedicated AYA palliative care provider (11%). Pain management services were available at most centers (86%), with these services available on an inpatient basis in 60% and on an outpatient basis in 55%. Most respondents reported that palliative care providers (98%), social workers (98%), and psycho-oncology providers (86%) assisted in addressing goals of care with AYA patients. Regarding advanced care planning, 69% reported requiring documentation in the electronic medical record, 51% reported having AYA-specific advanced care planning resources, 62% offered grief counseling in end-of-life situations for family members of AYAO patients, and 56% offered legacy work at the end of life for AYAs (Table 3).
AYAO Research and Education
Most NCI survey respondents (98%) reported being affiliated with a research consortium for oncology clinical trials, with 2% reporting being uncertain of an affiliation. Most centers reported AYAs had access to pediatric oncology phase I–III studies (64%, 75%, and 80%, respectively), in addition to adult oncology phase I–III studies (71%, 75%, and 76%, respectively). Roughly three-quarters of respondents (73%) reported collaboration between adult and pediatric researchers regarding AYAO patients. Types of collaboration included joint AYA tumor boards and cross-network trial access and availability. AYAO clinical and psychosocial research was reported with similar frequency: 71% and 69%, respectively. AYAO health outcomes and translational research was performed to a lesser extent: 58% and 40%, respectively. Only approximately one-third (29%) reported training staff about the care of AYAO patients, fewer (24%) reported hosting or planning to host AYAO conferences at their respective institutions.
Opinion of AYAO Care
Most respondents (60%) reported that AYA oncology care was important/very important to their respective institution. A little more than one-half (59%) reported providing good/excellent care to AYAs with cancer. Two-thirds (66%) of respondents felt they provided good/excellent fertility preservation, survivorship care, and psychosocial care to AYA patients. Good/Excellent overall symptom management for AYAs was reported by 57% of institutions, and good/excellent end-of-life care was reported by 49%. Services rated as poor/very poor and thus are areas for improvement include sexual health services (28%) and education of staff (34%), as well as research in AYAs, which most respondents graded as only average (57%) (Figure 2).
Opinion of AYAO care provided.
Abbreviations: AYAO, adolescent and young adult oncology; EoL, end-of-life.
Citation: Journal of the National Comprehensive Cancer Network 21, 5; 10.6004/jnccn.2023.7001
Opinion of AYAO care provided.
Abbreviations: AYAO, adolescent and young adult oncology; EoL, end-of-life.
Citation: Journal of the National Comprehensive Cancer Network 21, 5; 10.6004/jnccn.2023.7001
Opinion of AYAO care provided.
Abbreviations: AYAO, adolescent and young adult oncology; EoL, end-of-life.
Citation: Journal of the National Comprehensive Cancer Network 21, 5; 10.6004/jnccn.2023.7001
Discussion
This study is the first national survey to assess presence and characteristics of AYAO programs, care delivery, and available resources for AYAs with cancer. Findings are important for not just oncology providers but all providers who may assist in cancer prevention, diagnosis, treatment, and survivorship health. Previous national surveys in this population have surveyed patients and focused on cancer experience and outcomes.23–27 National consensus guidelines recommend that AYAs with cancer be cared for by professionals with expertise in this population; however, only half of NCI-CCs reported having a dedicated program, with one-quarter of programs developed in the past year. Our data show that significant variability exists in AYAO program composition and service delivery. Additionally, less than two-thirds of centers felt they were providing good/excellent AYA care overall. AYA sexual healthcare, education for providers, and research were identified as areas for improvement.
Availability of AYAO Programs
Despite recommendations by the NCI, ASCO, and NCCN,18,20–22 only approximately half of NCI-CCs reported having an existing AYAO program, with most programs being developed in the last 5 years. These findings highlight the tremendous work that needs to be done to connect this minority population with necessary resources for optimal and developmentally appropriate oncology care. Despite the common goal of meeting the needs of AYAO patients, there was significant heterogeneity in program composition across centers. Although most AYAO programs were combined between medical and pediatric oncology, one-quarter of programs still reported being siloed in pediatric oncology, reflective of the continued care gap for AYAs created by traditional adult and pediatric care models.8,22 Effective and equitable care of AYAs requires a central yet multidisciplinary approach, and future AYAO programs should be built around collaboration between medical and pediatric oncology to best meet their unique needs.28,29 Few of the existing AYAO programs that were surveyed reported the presence of services available at satellite locations within communities surrounding NCI-CCs where most AYAO patients are diagnosed and treated.30–32 Recent studies suggest that AYAs with cancer have inferior survival when treated outside academic centers.31,33–36 Referral patterns of AYAO patients influences geography of patient care, in turn contributing to access to academic centers and clinical trials.32,33 Little is known about AYA oncology care in the community setting; this survey had a low response rate among community oncology practices. Currently, no comprehensive list exists identifying AYAO clinical programs, nor is there any systematic process for certification or evaluation. Consideration should be given to the inclusion of an AYAO research program as a requirement for designation as an NCI Comprehensive Cancer Center.
Meeting the Needs of AYAs With Cancer: Comprehensive Reproductive Health
Most survey respondents reported providing comprehensive oncology care and services to all patients. To a lesser extent, dedicated services were provided directly to AYAO patients. In contrast to the near-complete access to fertility preservation, sexual health resources were less accessible to patients, with most centers only addressing sexual health upon patient request. Reflective of the lack of availability of sexual health services, only one-quarter of respondents reported providing good/excellent sexual healthcare to AYAs with cancer. Research demonstrates that AYAO patients are sexually active during cancer care37 and that AYAO survivors experience sexual dysfunction, which affects quality of life.38–41 Reproductive health is more comprehensive than just consideration of fertility preservation—it includes intimate relationships, sexual identity and orientation, sexuality and body image, and contraceptive needs in addition to the ability to conceive children. Practice guidelines are predominantly focused on fertility preservation or are focused within the context of oncology survivorship care.21,42,43 A paucity of data and guidelines exists regarding interventions for AYAO sexual health, although literature suggests that sexual health is important to AYAO patients.44 Comprehensive reproductive healthcare for AYAs should include sexual health alongside fertility. Practice standards must be implemented to evaluate sexual and reproductive healthcare throughout treatment and survivorship for AYAs.
AYAO Education and Research
Only one-third of respondents reported good/excellent AYAO research and education of staff at NCI-CCs. Academic medical centers provide a foundation for training and education of physicians, nurses, and other healthcare professionals. A minority of NCI-CCs reported training their staff in the care of AYAO patients, and few reported hosting education or conferences about AYAO at their institution. Few academic institutions offer AYAO specialty training fellowships for physicians.45–47 AYAO training should be incorporated into medical, nursing, and healthcare provider education, as well as included in existing healthcare curricula, and provided through educational program tracts at oncology conferences.48,49 This lack of training at NCI-CCs is a missed opportunity to disseminate awareness of the unique developmental needs of this population to all healthcare providers who may come into contact with AYAO patients as a result of their health and wellness needs. In addition to healthcare provider training, education and awareness of cancer should also be targeted to AYAs themselves. Empowering AYAs and educating medical professionals may increase cancer awareness and early detection in addition to informing healthcare providers about a developmental approach to the examination and care of AYAs with illness.50
Contributing to the deficit in research is the lack of AYAO patients enrolling in clinical trials—this population has the lowest trial enrollment of any age group.9,11,51 Reasons for poor trial participation is multifactorial and include not just access, but psychosocial barriers, lack of reliable transportation, financial barriers, and type of and lack of trust in healthcare provider.16,52,53 There is a greater need to understand barriers to enrollment and perform AYA-directed research, as well as address the overall trend of poor clinical trial enrollment among AYAs. The development of an AYAO program has been shown to increase clinical trial enrollment.28,54 Targeting AYAs through a multidisciplinary approach with providers who are trained in AYAO may help overcome barriers to trial enrollment.
This survey had several limitations. The survey may not truly reflect these programs accurately because this information was self-reported by centers. Additionally, surveys were addressed to the cancer center director or director of an identified AYAO program, but unique survey links may have been shared and/or delegates may have completed the survey. Furthermore, this report focused on NCI-CCs, which limits the generalizability of the results. We attempted to include other academic cancer centers and community cancer centers but received a very low response rate.
Conclusions
Only half of participating NCI-CCs reported having a dedicated AYAO program, and significant variability exists in program composition and care delivery. In alignment with national cancer organizations and AYAO advocacy groups, we must expand AYAO care delivery and research. This should include developing comprehensive reproductive healthcare programs, expanding AYAO provider training, addressing barriers to and improving upon AYAO research, as well as enhancing awareness of the unique needs of AYAO patients among all healthcare providers. Further research is needed to understand AYAO care in the community setting, and collaboration and coordination of care between academic and community practices should be fostered to ensure that all AYAs with cancer have the opportunity to receive population-specific, comprehensive care.
References
- 1.↑
Surveillance, Epidemiology, and End Results Program. Cancer stat facts: cancer among adolescents and young adults (AYAs) (ages 15–39). Accessed June 1, 2022. Available at: https://seer.cancer.gov/statfacts/html/aya.html
- 2.↑
Scott AR, Stoltzfus KC, Tchelebi LT, et al. Trends in cancer incidence in US adolescents and young adults, 1973-2015. JAMA Netw Open 2020;3:e2027738.
- 3.↑
Bleyer WA. Cancer in older adolescents and young adults: epidemiology, diagnosis, treatment, survival, and importance of clinical trials. Med Pediatr Oncol 2002;38:1–10.
- 4.↑
Bleyer A, O’Leary M, Barr R, Ries LAG, eds. Cancer epidemiology in older adolescents and young adults 15-29 years of age, including SEER incidence and survival: 1975-2000. Accessed June 1, 2022. Available at: https://seer.cancer.gov/archive/publications/aya/aya_mono_complete.pdf
- 5.↑
Ballantine KR, Utley V, Watson H, et al. The burden of cancer in 25-29 year olds in New Zealand: a case for a wider adolescent and young adult age range? N Z Med J 2018;131:15–24.
- 6.↑
Close AG, Dreyzin A, Miller KD, et al. Adolescent and young adult oncology-past, present, and future. CA Cancer J Clin 2019;69:485–496.
- 7.↑
Keegan TH, Ries LA, Barr RD, et al. Comparison of cancer survival trends in the United States of adolescents and young adults with those in children and older adults. Cancer 2016;122:1009–1016.
- 8.↑
Bleyer A, Barr R. Cancer in young adults 20 to 39 years of age: overview. Semin Oncol 2009;36:194–206.
- 9.↑
Bleyer A, Budd T, Montello M. Adolescents and young adults with cancer: the scope of the problem and criticality of clinical trials. Cancer 2006; 107(Suppl 7):1645–1655.
- 10.↑
Roth ME, O’Mara AM, Seibel NL, et al. Low enrollment of adolescents and young adults onto cancer trials: insights from the community clinical oncology program. J Oncol Pract 2016;12:e388–395.
- 11.↑
Bleyer A, Tai E, Siegel S. Role of clinical trials in survival progress of American adolescents and young adults with cancer-and lack thereof. Pediatr Blood Cancer 2018;65:e27074.
- 12.↑
Zebrack BJ. Psychological, social, and behavioral issues for young adults with cancer. Cancer 2011;117(Suppl 10):2289–2294.
- 13.↑
Zebrack B, Butler M. Context for understanding psychosocial outcomes and behavior among adolescents and young adults with cancer. J Natl Compr Canc Netw 2012;10:1151–1156.
- 14.↑
Zebrack B, Isaacson S. Psychosocial care of adolescent and young adult patients with cancer and survivors. J Clin Oncol 2012;30:1221–1226.
- 15.↑
Liu L, Krailo M, Reaman GH, et al. Childhood cancer patients’ access to cooperative group cancer programs. Cancer 2003;97:1339–1345.
- 16.↑
Alvarez E, Keegan T, Johnston EE, et al. Adolescent and young adult oncology patients: disparities in access to specialized cancer centers. Cancer 2017;123:2516–2523.
- 17.↑
Rosenberg AR, Kroon L, Chen L, et al. Insurance status and risk of cancer mortality among adolescents and young adults. Cancer 2015;121:1279–1286.
- 18.↑
Adolescent and Young Adult Oncology Progress Review Group. Closing the gap: research and care imperatives for adolescents and young adults with cancer: report of the Adolescent and Young Adult Oncology Progress Review Group. Accessed June 1, 2022. Available at: https://www.livestrong.org/sites/default/files/what-we-do/reports/ ayao_prg_report_2006_final.pdf
- 19.↑
Cuglievan B, Berkman A, Dibaj S, et al. Impact of lagtime, health insurance type, and income status at diagnosis on the long-term survival of adolescent and young adult cancer patients. J Adolesc Young Adult Oncol 2021;10:164–174.
- 20.↑
NCI. Adolescents and young adults with cancer. Accessed June 1, 2022. Available at: https://www.cancer.gov/types/aya
- 21.↑
Bhatia S, Pappo AS, Acquazzino M, et al. NCCN Clinical Practice Guidelines in Oncology: Adolescent and Young Adult (AYA) Oncology. Version 3.2023. Accessed January 30, 2023. To view the most recent version, visit https://www.nccn.org
- 22.↑
Zebrack B, Mathews-Bradshaw B, Siegel S, et al. Quality cancer care for adolescents and young adults: a position statement. J Clin Oncol 2010;28:4862–4867.
- 23.↑
Harlan LC, Lynch CF, Keegan TH, et al. Recruitment and follow-up of adolescent and young adult cancer survivors: the AYA HOPE study. J Cancer Surviv 2011;5:305–314.
- 24.↑
Smith AW, Parsons HM, Kent EE, et al. Unmet support service needs and health-related quality of life among adolescents and young adults with cancer: the AYA HOPE study. Front Oncol 2013;3:75.
- 25.↑
Smith AW, Keegan TH, Hamilton A, et al. Understanding care and outcomes in adolescents and young adult with cancer: a review of the AYA HOPE study. Pediatr Blood Cancer 2019;66:e27486.
- 26.↑
Keegan TH, Lichtensztajn DY, Kato I, et al. Unmet adolescent and young adult cancer survivors information and service needs: a population-based cancer registry study. J Cancer Surviv 2012;6:239–250.
- 27.↑
Bellizzi KM, Smith A, Schmidt S, et al. Positive and negative psychosocial impact of being diagnosed with cancer as an adolescent or young adult. Cancer 2012;118:5155–5162.
- 28.↑
Ferrari A, Thomas D, Franklin AR, et al. Starting an adolescent and young adult program: some success stories and some obstacles to overcome. J Clin Oncol 2010;28:4850–4857.
- 29.↑
Osborn M, Johnson R, Thompson K, et al. Models of care for adolescent and young adult cancer programs. Pediatr Blood Cancer 2019;66:e27991.
- 30.↑
Albritton KH, Wiggins CH, Nelson HE, et al. Site of oncologic specialty care for older adolescents in Utah. J Clin Oncol 2007;25:4616–4621.
- 31.↑
Yeager ND, Hoshaw-Woodard S, Ruymann FB, et al. Patterns of care among adolescents with malignancy in Ohio. J Pediatr Hematol Oncol 2006;28:17–22.
- 32.↑
Parsons HM, Harlan LC, Schmidt S, et al. Who treats adolescents and young adults with cancer? A report from the AYA HOPE study. J Adolesc Young Adult Oncol 2015;4:141–150.
- 33.↑
Johnson KJ, Wang X, Barnes JM, et al. Associations between geographic residence and US adolescent and young adult cancer stage and survival. Cancer 2021;127:3640–3650.
- 34.↑
Wendt R, Gao Y, Miller BJ. Rural patients are at risk for increased stage at presentation and diminished overall survival in osteosarcoma. Cancer Epidemiol 2019;61:119–123.
- 35.↑
Keegan TH, Grogan RH, Parsons HM, et al. Sociodemographic disparities in differentiated thyroid cancer survival among adolescents and young adults in California. Thyroid 2015;25:635–648.
- 36.↑
Mobley EM, Charlton ME, Ward MM, et al. Nonmetropolitan residence and other factors affecting clinical trial enrollment for adolescents and young adults with cancer in a US population-based study. Cancer 2019;125:2283–2290.
- 37.↑
Murphy D, Klosky JL, Reed DR, et al. The importance of assessing priorities of reproductive health concerns among adolescent and young adult patients with cancer. Cancer 2015;121:2529–2536.
- 38.↑
Sopfe J, Gupta A, Appiah LC, et al. Sexual dysfunction in adolescent and young adult survivors of childhood cancer: presentation, risk factors, and evaluation of an underdiagnosed late effect: a narrative review. J Adolesc Young Adult Oncol 2020;9:549–560.
- 39.↑
Cherven B, Sampson A, Bober SL, et al. Sexual health among adolescent and young adult cancer survivors. CA Cancer J Clin 2021;71:250–263.
- 40.↑
Hovén E, Fagerkvist K, Jahnukainen K, et al. Sexual dysfunction in young adult survivors of childhood cancer. Eur J Cancer 2021;154:147–156.
- 41.↑
Wettergren L, Kent EE, Mitchell SA, et al. Cancer negatively impacts on sexual function in adolescents and young adults: the AYA HOPE study. Psychooncology 2017;26:1632–1639.
- 42.↑
Oktay K, Harvey BE, Partridge AH, et al. Fertility preservation in patients with cancer: ASCO Clinical Practice Guideline update. J Clin Oncol 2018;36:1994–2001.
- 43.↑
Children’s Oncology Group. Guideline for fertility preservation for patients with cancer. Accessed June 1, 2022. Available at: https://childrensoncologygroup.org/downloads/COG_SC_Fertility_Guideline_Document.pdf
- 44.↑
Fladeboe KM, Scott S, Bradford MC, et al. Sexual activity and substance use among adolescents and young adults receiving cancer treatment. J Adolesc Young Adult Oncol 2020;9:594–600.
- 45.↑
USC Norris Comprehensive Cancer Center. Medical professional education. Accessed June 1, 2022. Available at: https://www.aya.usc.edu/en/education/medical-fellowships
- 46.↑
OHSU Children’s Hospital. Adolescent and young adult (AYA) combined med/peds hematology/oncology fellowship. Accessed June 1, 2022. Available at: https://www.ohsu.edu/doernbecher/adolescent-and-young-adult-aya-combined-med-peds-hematology-oncology-fellowship
- 47.↑
Cincinnati Children’s Hospital Medical Center. Hematology and oncology: adolescent and young adult oncology fellowship. Accessed June 1, 20223. Available at: https://www.cincinnatichildrens.org/education/clinical/fellowship/hem-onc/adolescent-young-adult
- 48.↑
Johnson RH. AYA in the USA. International perspectives on AYAO, part 5. J Adolesc Young Adult Oncol 2013;2:167–174.
- 49.↑
Hayes-Lattin B, Mathews-Bradshaw B, Siegel S. Adolescent and young adult oncology training for health professionals: a position statement. J Clin Oncol 2010;28:4858–4861.
- 50.↑
Audino AN, Yeager ND. “Learning, Education, Awareness, Prevention (L.E.A.P.) Young Adult Cancer”: an education and outreach program. J Adolesc Young Adult Oncol 2018;7:130–133.
- 51.↑
Unger JMCE, Cook E, Tai E, et al. The role of clinical trial participation in cancer research. Am Soc Clin Oncol Educ Book 2016;35:185–198.
- 52.↑
Buchanan ND, Block R, Smith AW, et al. Psychosocial barriers and facilitators to clinical trial enrollment and adherence for adolescents with cancer. Pediatrics 2014;133(Suppl 3):S123–130.
- 53.↑
Parsons HM, Harlan LC, Seibel NL, et al. Clinical trial participation and time to treatment among adolescents and young adults with cancer: does age at diagnosis or insurance make a difference? J Clin Oncol 2011;29:4045–4053.
- 54.↑
Shaw PH, Boyiadzis M, Tawbi H, et al. Improved clinical trial enrollment in adolescent and young adult (AYA) oncology patients after the establishment of an AYA oncology program uniting pediatric and medical oncology divisions. Cancer 2012;118:3614–3617.
