In the United States, more than 72,000 adolescents and young adults (ages 15-39 years) are diagnosed with cancer each year.1 Fortunately, advancements in early detection and treatment mean many young patients with cancer will live well beyond their cancer diagnosis. As higher rates of cancer survivorship are reached, the clinical focus has shifted from survival alone to include long-term quality-of-life issues.2 One important quality-of-life issue in young patients is the potential infertility caused by some cancer treatments.3,4 The likelihood of infertility varies according to age at diagnosis, cancer site, treatment modality, treatment agent, and other factors5; however, sustained infertility is estimated to develop in 50% to 95% of cancer survivors treated during their reproductive years.5-8
The issue of fertility subsequent to cancer treatment is a primary concern for most patients of childbearing age.9,10 Even in the face of a life-threatening illness, patients report that the loss of fertility is almost as distressing as the actual battle with cancer.11,12 Several studies have found that most cancer survivors (∼ 76%), men and women alike, are interested in having children, especially if they were childless at diagnosis.10,13-15 In fact, many patients report that their cancer experience increased the value they placed on parenthood and family ties.16,17
The long-term negative impact of infertility has also been shown among young male and female cancer survivors.18,19 More-recent studies suggest that among young women in particular, cancer-related infertility is associated with a greater risk for emotional distress and poorer quality of life.20,21 However, options are available that may preserve the ability to have biological children in the future.
Fertility Preservation Options
Although the physiologic impact on the patient's fertility may be inevitable, the practical outcome—the ability to later have biological children—might be improved by recent advances that allow fertility preservation (FP) options for both male and female patients with cancer.
FP methods that are considered established are sperm cryopreservation for men and embryo cryopreservation for women.5 These options must be started before treatment. In some cases these treatments are not suitable and experimental options may be considered, such as hormonal gonadoprotection for men and oocyte cryopreservation, ovarian transposition, ovarian downregulation (suppression), and ovarian tissue cryopreservation for women, and gonadal shielding for both men and women.5 A specialist can help patients decide which FP option is best in a particular circumstance.
Lack of Knowledge as a Barrier
Unfortunately, patients with cancer may not be aware of their fertility risk and FP options within the limited timeframe in which these options are available. A pilot study13 and a follow-up study14 showed that patients are not well informed about available FP options. Among cancer survivors who were queried about whether a health care provider had discussed the risk of infertility with them, only 50% recalled this occurrence.22 In a study of female patients alone, fewer than 35% recalled discussing the risks of infertility with a health care provider during or after cancer treatment.16
The Importance of Physician Endorsement
Although advocacy organizations, such as Fertile Hope, have been proactive in making resources related to FP available to patients with cancer and their families, research shows that patients may perceive information provided by national organizations to be a resource but not necessarily a course of action suggested for their situation.17 Instead, receiving tailored information about cancer-related support services has been shown to help patients and families recognize that the service provided is endorsed by their physician.23 Furthermore, patients report higher levels of satisfaction with integrative medicine referrals when a system is in place for receiving referrals and services and that suggests that these services are endorsed by their treating physician.24
Guidelines
In acknowledgement of these findings, the ASCO (2006) and the American Society for Reproductive Medicine (2005) guidelines, and advocacy organizations such as American Cancer Society and Fertile Hope (now part of the Lance Armstrong Foundation), recommend that patients with newly diagnosed cancer receive risk information and a referral to a reproductive endocrinologist/infertility (REI) specialist. REI and associated clinics offer counseling and FP services tailored to individual patients with consideration of age, cancer type and stage, and the therapeutic agent recommended for treatment. In addition, these specialists can assess each patient's risk for infertility, reproductive capacity, and physical health to determine which FP options are available and likely to be successful.
Despite these recommendations, a 2008 national study of oncologists showed that fewer than 50% routinely refer patients to an REI specialist.25 Studies of pediatric and adult oncologists examining referral practice patterns for fertility have found that a lack of resources regarding where or how to refer patients is a significant barrier and deterrent to discussion.26 Several large studies have found that physicians are more likely to make appropriate referrals (e.g., for palliative care) when they practice within a system that has established guidelines and processes for referrals.27-31 Furthermore, according to Fertile Hope, two-thirds of physicians would be more likely to discuss FP if detailed patient education materials and appropriate referrals were available.32
The Moffitt Referral System
To improve patient awareness of FP services and reduce the burden on oncologists of discussing and referring for a service for which they may have limited training and time, the authors' group developed a 5-step system to ensure that all patients of childbearing age received a referral to an REI (Figure 1). The goal in building a referral system at H. Lee Moffitt Cancer Center was to effectively inform patients and direct them to services, and to minimize the direct burden on their oncologists. This integrated, coordinated system was based partly on the guidelines established by the Fertile Hope organization (www.fertilehope.org) for receipt of the Center of Excellence award.
Methods
Step One: The first step in this process was to identify the institutional barriers to communicating with patients about FP options. The authors' group conducted a series of individual interviews with oncologists from each of the hospital clinics, and focus groups consisting of nurses and social workers. The primary barriers identified were lack of knowledge about need for FP, lack of awareness about where to refer patients, lack of knowledge of FP options, and a lack of time for these discussions.
Step Two: The authors' group conducted a series of in-service educational programs and Grand Rounds to educate health care professionals about the physiologic
Flowchart of 5-step process.
Abbrevation: REI, reproductive endocrinologist/infertility.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Flowchart of 5-step process.
Abbrevation: REI, reproductive endocrinologist/infertility.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Flowchart of 5-step process.
Abbrevation: REI, reproductive endocrinologist/infertility.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Step Three: The authors' group established a relationship with the University of South Florida In Vitro Fertilization (USF IVF) program (www.usfivf.com) to create a referral process. This partnership was enhanced by Moffitt's relationship with these reproductive endocrinologists who specialize in FP for patients with cancer and their ability to implement a fee structure that provides at least a 50% reduction in the standard cost of these procedures. The clinic's participation in Fertile Hope's Sharing Hope program allows for the reduced fees and other services offered at deeply discounted rates. Additionally, REI specialists from USF IVF will also travel to Moffitt for inpatient consults.
Together with USF IVF, the authors' group developed a brochure for treating physicians to provide patients, which highlights the importance of discussing the effect of cancer treatment on fertility and reproduction, and directs patients to call or ask for assistance from the clinic nurse to schedule a phone or in-person consultation with an REI specialist. (To view the brochure, visit www.insidemoffitt.com/Fertility-Preservation-What-You-Can-Do.htm.) A unique telephone number was established for patients treated at Moffitt, which guarantees a return phone call by an REI specialist within 24 hours and an appointment, if desired, within 48 hours.
Step Four: The authors' group conducted a pilot study at Moffitt. All clinic sites were included except for Senior Adult and Thoracic, because they do not see patients of reproductive age. The sarcoma clinics' staff (selected because they see the highest number of young men and women of reproductive age) were administered a pretest about current practices regarding discussion of fertility and referrals, and preferences for communication channels and information type. The process and brochure were modified based on the results of this pretest (Figure 2) and regular biweekly meetings to review the referral process. These modifications included the need for the brochure to deemphasize a discussion with the oncologist and place emphasis on a consultation with an REI specialist, and to make the phone system more patient-friendly.
The brochure was also tested with a small group of 5 survivors receiving follow-up care in the clinic. The authors' group received a waiver of need for consent from Moffitt's Institutional Review Board because they were not collecting any patient data and were asking for feedback to improve an educational resource. The patients suggested that emphasis on the window of opportunity to pursue FP options needed to be stronger, how FP services coordinated with oncology care services was not clear, and assurance should be given that patients' oncologist supported this consultation with an REI specialist.
The authors' group developed a call log with the USF IVF clinic to document calls, capturing information including patients who called from all clinics in the institution, the clinic or referring physician, patient gender, and type of service requested (phone, in-patient, or office consult). This reporting system was augmented by documentation of the disposition of the call (e.g., REI-provided phone consult, patient request of clinic consult after phone call, in-patient consult, office consult, cancellation, no-show).
Step Five: Two questions were added to the electronic patient health questionnaire, an electronic medical record completed by all new patients. Patients are asked, “Do you have all the children you wish to have? Yes/No”; “Would you like a referral to an infertility specialist? Yes/No” (Figure 3). The electronic patient questionnaire generates a report for the physician, and the response of “Yes” to either of these questions is noted in the report. This serves as a prompt for the physician to distribute a brochure to the patient during the initial visit. It is Moffitt's policy for a patient to receive a brochure if they selected “Yes.”
Results
From August 2007 to August 2008, before this pilot study was initiated, the USF IVF program received a total of 13 calls and referrals from Moffitt patients and physicians. After initiation of the study, from October 2008 to September 2009, the authors' group monitored the brochure quantities distributed to the breast, gastrointestinal, genitourinary, gynecologic, head and neck, hematology, neurology, and sarcoma clinics. The brochure was distributed with other clinic materials in the patient waiting areas of these 8 clinics. Results of the study showed that 776 patients of reproductive age (< 40 years) were seen in these clinics over the 12-month period; a total of 349 brochures were taken from these waiting rooms (although whether patients took multiple copies could not be determined) and 122 phone calls were placed by patients (or their nurses) to the USF IVF clinic. Therefore, approximately 16% of patients of reproductive age contacted the REI group. Of these calls, 77 patients wanted only to speak to an REI specialist over the phone, 45 scheduled an appointment, 38 attended an outpatient appointment, 3 were no-shows, and 4 were inpatient consults (i.e., the patients were hospitalized at Moffitt). Of the 42 attended appointments, 11 male patients chose to bank sperm (including 3 inpatients), 12 female patients chose oocyte preservation, 10 female patients chose embryo cryopreservation, and 7 female and 2 male patients opted for no services. Thus, a 12-month pilot of the brochure and referral system increased calls and consults to the REI by 9-fold.
Discussion and Conclusion
The goal of the Moffitt Referral System is to develop a structure that enhances patient quality of life and satisfaction through empowering patients to make fertility-related decisions based on relevant and timely information, and to provide patients the chance to be active in deciding whether to act.33 The 12-month pilot program showed that 16% of the eligible population is contacting the REI group for a consult, and 27% of these patients are opting
Pretest questions.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Pretest questions.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Pretest questions.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Electronic patient health questionnaire.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Electronic patient health questionnaire.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Electronic patient health questionnaire.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 9, 11; 10.6004/jnccn.2011.0102
Furthermore, nurses and social workers at Moffitt suggest that the brochure helps some patients receive the information they need to feel certain that future childbearing is not a goal for them. Staff members suggested that the brochure facilitates conversations in which patients report, “I did not plan on having any more children” or “I've never wanted children.” Thus, the brochure can be perceived as effective in helping inform these patients about potential infertility from cancer treatment, even though, in keeping with their own goals, a consultation with an infertility specialist may not be required.
Providing timely and relevant information related to FP and the opportunity for a referral to an REI specialist for consultation may reduce emotional distress and improve quality of life for patients as they transition from patient to survivor. Results from the pilot study illuminated the concept that a great need exists to ensure that all patients are aware of the window of opportunity for taking steps to preserve fertility. As a result of the pilot study, 2 questions were added to the electronic patient questionnaire prompting physicians to provide brochures directly to appropriate patients. Future plans include having an on-site clinic with a reproductive endocrinologist, and the opportunity for patients to have this consultation at the same time and place as their cancer care services is anticipated to increase consultation rates.
Oncologists often have limited time and expertise to discuss FP with patients, particularly in the context of each patient's unique medical and social history. Furthermore, FP is evolving as a critical branch of reproductive medicine, with recent advances occurring at an accelerated pace. Thus, a streamlined referral system with aids, such as the health questionnaire and brochure the group developed, along with the involvement of reproductive medicine specialists, will help oncologists meet this obligation. Cooperation from the treatment team is imperative for the referral system's success, and Moffitt's system can serve as a model that can be standardized at other institutions. Staff at varying clinics within the hospital must be informed of the referral system and educated on resources and where to direct patients for the system to operate at its full potential. Through referring patients for consultation and providing them with the information required to make informed decisions, health care teams are afforded the opportunity to participate in a movement to empower patients through information.
References
- 1↑
Ware JE Jr. Methodology in behavioral and psychological cancer research. Conceptualizing disease impact and treatment outcomes. Cancer 1984;15(Suppl 10):2316-2323.
- 2↑
Centers for Disease Control and Prevention. A national action plan for cancer survivorship: advancing public health strategies. Available at www.cdc.gov/cancer/survivorship/pdf/plan.pdf. Accessed October 13, 2011.
- 3↑
Padron OF, Sharma RK, Thomas AJ Jr, Agarwal A. Effects of cancer on spermatozoa quality after cryopreservation: a 12-year experience. Fertil Steril 1997;67:326-331.
- 4↑
Sonmezer M, Oktay K. Fertility preservation in female patients. Hum Reprod Update 2004;10:251-266.
- 5↑
Lee SJ, Schover LR, Partridge AH et al.. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol 2006;24:2917-2931.
- 6
Amory JK. Case 15-2004: cancer therapy and sperm banking. N Engl J Med 2004;351:510; author reply 510.
- 7
Kelleher S, Wishart SM, Liu PY et al.. Long-term outcomes of elective human sperm cryostorage. Hum Reprod 2001;16:2632-2639.
- 8↑
Lass A, Akagbosu F, Brinsden P. Sperm banking and assisted reproduction treatment for couples following cancer treatment of the male partner. Hum Reprod Update 2001;7:370-377.
- 9↑
Knobf MT. The influence of endocrine effects of adjuvant therapy on quality of life outcomes in younger breast cancer survivors. Oncologist 2006;11:96-110.
- 10↑
Schover LR. Motivation for parenthood after cancer: a review. J Natl Cancer Inst Monogr 2005;2005:2-5.
- 11↑
Surbone A, Petrek JA. Childbearing issues in breast carcinoma survivors. Cancer 1997;79:1271-1278.
- 13↑
Schover LR, Rybicki LA, Martin BA, Bringelsen KA. Having children after cancer. A pilot survey of survivors' attitudes and experiences. Cancer 1999;86:697-709.
- 14↑
Schover LR, Brey K, Lichtin A et al.. Knowledge and experience regarding cancer, infertility, and sperm banking in younger male survivors. J Clin Oncol 2002;20:1880-1889.
- 15↑
Schover LR, Brey K, Lichtin A et al.. Oncologists' attitudes and practices regarding banking sperm before cancer treatment. J Clin Oncol 2002;20:1890-1897.
- 16↑
Partridge AH, Gelber S, Peppercorn J et al.. Web-based survey of fertility issues in young women with breast cancer. J Clin Oncol 2004;22:4174-4183.
- 17↑
Bryant CA, Forthofer MS, McCormack K et al.. A social marketing approach to increasing breast cancer screening. J Health Educ 2000;31:320-328.
- 18↑
Hammond C, Abrams JR, Syrjala KL. Fertility and risk factors for elevated infertility concern in 10-year hematopoietic cell transplant survivors and case-matched controls. J Clin Oncol 2007;25:3511-3517.
- 19↑
Green D, Galvin H, Horne B. The psycho-social impact of infertility on young male cancer survivors: a qualitative investigation. Psychooncology 2003;12:141-152.
- 20↑
Ganz PA, Greendale GA, Petersen L et al.. Breast cancer in younger women: reproductive and late health effects of treatment. J Clin Oncol 2003;21:4184-4193.
- 21↑
Ganz PA, Rowland JH, Desmond K et al.. Life after breast cancer: understanding women's health-related quality of life and sexual functioning. J Clin Oncol 1998;16:501-514.
- 22↑
Schover LR. Psychosocial aspects of infertility and decisions about reproduction in young cancer survivors: a review. Med Pediatr Oncol 1999;33:53-59.
- 23↑
McPherson CJ, Higginson IJ, Hearn J. Effective methods of giving information in cancer: a systematic literature review of randomized controlled trials. J Public Health 2001;23:227-234.
- 24↑
Koithan M, Bell IR, Caspi O et al.. Patients' experiences and perceptions of a consultative model integrative medicine clinic: a qualitative study. Integr Cancer Ther 2007;6:174-184.
- 25↑
Quinn GP, Vadaparampil ST, Lee JH et al.. Physician referral for fertility preservation with oncology patients: a national study of practice behaviors. J Clin Oncol 2009;27:5952-5957.
- 26↑
Goodwin T, Oosterhuis B, Kiernan M et al.. Attitudes and practices of pediatric oncology providers regarding fertility issues. Pediatr Blood Cancer 2007;48:80-85.
- 28
Webb C, Kevern J. Focus groups as a research method: a critique of some aspects of their use in nursing research. J Adv Nurs 2001;33:798-805.
- 29
Morgan D. The Focus Group Guidebook. Thousand Oaks, CA: Sage; 1988.
- 30
McGrath P, Holewa H. Missed opportunities: nursing insights on end-of-life care for haematology patients. Int J Nurs Pract 2006;12:295-301.
- 31↑
Lorenz KA, Lynn J, Dy SM et al.. Evidence for improving palliative care at the end of life: a systematic review. Ann Intern Med 2008;148:147-159.
- 33↑
Andersen MR, Bowen DJ, Morea J et al.. Involvement in decision-making and breast cancer survivor quality of life. Health Psychol 2009;28:29-37.
- 34↑
Klock S, Zhang J, Kazer R. Fertility preservation for female cancer patients: early clinical experience. Fertil Steril 2010;94:149-155.
- 35↑
Rowan K. Fertility preservation during treatment is a growing issue for women. J Natl Cancer Inst 2010;102:294-296.
- 36
Quinn GP, Vadaparampil ST, Gwede CK et al.. Discussion of fertility preservation with newly diagnosed patients: oncologists' views. J Cancer Survivorship 2007;1:146-155.
- 37↑
Wallace WH, Anderson RA, Irvine DS. Fertility preservation for young patients with cancer: who is at risk and what can be offered? Lancet Oncol 2005;6:209-218.
