Background
In 2017, 10% of Australian women diagnosed with cancer were aged 15 to 44 years,1 and the National Cancer Institute approximates half of these occurred in young adults aged 15 to 39 years.2 Cancer treatments can significantly reduce reproductive potential in female patients3–11; across all cancer types, survivors are 38% less likely to achieve pregnancy after diagnosis.11 Women of childbearing potential (WoCBP) have been known to opt out of chemotherapy, choose one chemotherapy regimen over another, and reject or shorten endocrine therapy to preserve fertility.12 In both hematology and oncology there have been significant advances in survival rates with the advent of novel therapeutic agents, in particular monoclonal antibodies.13 This has shifted some of the focus in clinical practice from survival to survivorship issues.14 This includes the ability to bear children, and for many, an inability or lack of option to bear children can be devastating and significantly impact quality of life.15,16 Indeed, fertility preservation has been cited as one of the top 5 unmet needs for young patients with cancer.17
Anticancer therapies affect a woman’s fertility in a multitude of ways. Chemotherapy can cause ovarian cortical fibrosis and damage blood vessels, triggering local ischemia with potential destruction of oocytes.10 Chemotherapy also compromises the uterine environment’s ability to support pregnancy by reducing volume and vasculature.9 High-dose chemotherapeutic regimens6,18 or those containing alkylating agents, such as cyclophosphamides and anthracyclines, are particularly harmful.19,20 Alkylating agents create covalent bonds between strands of DNA, interfering with cleavage during replication and disrupting cell division.10 The cumulative risk for premature ovarian failure (POF) upon receiving alkylating chemotherapy is 60%, increasing by 23% per year of age at treatment.6 Larsen et al21 demonstrated that in teenage females undergoing chemotherapy the risk of POF increases by a factor of 4, whereas for women aged 21 to 25 years the risk increased by a factor of 27. High POF risk has been confirmed by lower serum anti-Müllerian hormone and transvaginal ultrasound antral follicle counts in cancer cohorts.8,22,23
Abdominal radiotherapy directly reduces hormone production, whereas cranial irradiation damages the hypothalamic-pituitary axis.4,8 Hematopoietic stem cell transplantation (HSCT) also commonly leads to POF, especially because patients are often conditioned with total body irradiation prior to transplantation.4,10 A recent meta-analysis on reproductive outcomes post-HSCT estimates a low pregnancy rate of 22.7% in patients desiring children.4
Although cancer treatment in WoCBP has these significant risks, there are excellent fertility preservation options for women, with oocyte and embryo cryopreservation routinely available (and in Australia, at no cost).24,25 Additionally, in some states there is public access to oncofertility services with clinical nurse consultants, psychologists, and practical supports. In clinical practice it may be challenging to integrate fertility preservation in the setting of life-threating malignancies and urgent need for therapy.26,27 However, the age of first pregnancy is rising,28 increasing the risk of cancer diagnosis at a time when women are contemplating family planning.29 Fertility discussions, and provision of services to preserve gametes or tissues, is acknowledged as a vital aspect of cancer care.30 The objective of this study was to examine the incidence of fertility counseling in women of childbearing age before, during, and after anticancer therapies at a large metropolitan Australian cancer center with access to no-cost oncofertility services at 3 tertiary referral hospitals in New South Wales.
Patients and Methods
Participants
We conducted a retrospective medical record review of patients diagnosed with cancer between 2017 and 2020 who were seen by oncologists, hematologists, or allied health professionals, including counselors/social workers/psychologists, pharmacists, geneticists, and clinical trial staff, at Kinghorn Cancer Centre, and therefore recorded in the Kinghorn Cancer Centre electronic medical records (EMRs). We also included scanned correspondence letters from gynecologists, endocrinologists, and other specialists to whom patients were referred. Patients were included if they met the following criteria: female, aged 18 to 49 years at the time of cancer diagnosis, premenopausal at diagnosis, had a diagnosis confirmed by tissue biopsy, treated with anticancer therapy (chemotherapy, hormonal therapy, immunotherapy, or radiation), and treated by a medical oncologist or hematologist. The number of medical record entries reviewed varied from 5 to >100. The Human Research Ethics Committee (HREC) of St Vincent’s Hospital Australia approved this study (2020/ETH03136).
Recruitment
Patients who met inclusion criteria were identified through databases including hospital records, clinic lists, the EMR (MOSAIQ, a comprehensive medical records system designed for cancer care that can be accessed by multidisciplinary teams across multiple locations), and pathology and pharmacy records at St Vincent’s Hospital Kinghorn Cancer Centre.
Measures
Data collected from chart review included age at diagnosis, primary diagnosis, stage of cancer, treatment(s) received, rates of remission or progression, documentation of contraceptive use, details of any fertility preservation discussions (wanting children vs family complete) and what was offered (eg, oocyte, embryo or gonadal tissue cryopreservation), involvement of a specialist gynecologist across different stages of care, prior reproductive history (including parity and gravidity), thromboembolic complications, fertility outcomes posttreatment (spontaneous conception vs in vitro fertilization [IVF] cycles and outcomes including confirmed intrauterine pregnancy, miscarriage, live births), and signs or diagnosis of early ovarian failure, amenorrhoea, or oligomenorrhoea. A fertility history was defined as information about past and present pregnancies (including miscarriages and terminations); family planning, including the desire to have future children versus family being complete; menses status; and fertility preservation options undertaken, including egg and embryo cryopreservation.
Results
Participant Characteristics
A total of 143 patients met inclusion criteria. Patient characteristics are presented in Table 1. The median age at diagnosis was 41 years (range, 19–49 years). Premenopausal women who did not have children and did not wish to have children were slightly older (median, 44 years [range, 38–48 years]).
Demographic and Pathologic Characteristics
| Variable | n (%) |
|---|---|
| Number of children | |
| 0 | 38 (26.6) |
| 1 | 19 (13.3) |
| ≥2 | 49 (34.3) |
| Not documented | 37 (25.9) |
| Type of cancer | |
| Breast | 76 (53.1) |
| Hematologic | 28 (19.6) |
| Gastrointestinal | 19 (13.3) |
| Head and neck | 9 (6.3) |
| Lung | 4 (2.8) |
| Melanoma | 3 (2.1) |
| Central nervous system | 2 (1.4) |
| Gynecologic | 1 (0.7) |
| Renal | 1 (0.7) |
| T stage51 | |
| T1 | 20 (14.0) |
| T2 | 37 (25.9) |
| T3 | 41 (28.7) |
| T4 | 18 (12.6) |
| Not documented | 27 (18.9) |
| Type of treatment | |
| Surgery | 101 (70.6) |
| Chemotherapy | 124 (86.7) |
| Radiotherapy | 58 (40.6) |
| Endocrine therapy | 60 (42.0) |
| Allogeneic stem cell transplant | 5 (3.5) |
| Other | 8 (5.6) |
| Disease recurrence | |
| No | 116 (81.1) |
| Yes | 27 (18.9) |
The most common cancer diagnosis was breast (53.1%), followed by hematologic (19.6%) and gastrointestinal (13.3%). Other diagnoses included head and neck cancers (6.3%), lung cancers (2.8%), melanoma (2.1%), cancers of the central nervous system (1.4%), gynecologic malignancies (0.7%), and renal carcinomas (0.7%).
Most patients (86.7%) underwent chemotherapy and 70.6% underwent surgery. Other forms of cancer therapy included radiotherapy (40.6%), endocrine therapy (42.0%), and allogeneic stem cell transplantations (3.5%), and 5.6% of patients were treated with immunotherapy alone or in combination with chemotherapy.
Fertility History
Reproductive history taking was poorly documented. Parity and gravidity were documented in only 18 (12.6%) patients during the first consultation and in 2 (1.4%) at a later visit (Table 2). Reproductive histories were more often taken by other medical staff, such as radiation oncologists, endocrinologists, and gynecologists (20.3%), than by treating physicians (14.0%), but 94 (65.7%) patients did not have their reproductive histories documented.
Documentation of Reproductive History
| Documented at First Consult n (%) |
Documented, but Not at First Consult n (%) |
Documented, but Not by Attending Physician n (%) |
Not Recorded n (%) |
|---|---|---|---|
| 18 (12.6) | 2 (1.4) | 29 (20.3) | 94 (65.7) |
Fertility Discussions
A total of 58% (n=83) of patients had fertility preservation discussions with their attending physician documented, and 1.4% (n=2) had fertility discussions with another health professional documented. This rate was slightly higher for patients with a breast cancer diagnosis (n=51; 67.1%). As a result, 37 (25.9%) patients saw a specialist gynecologist to discuss preservation options before receiving cancer treatment and 16 (11.2%) were offered a referral but declined.
At the time of data collection, the following fertility-related outcomes over 1 to 4 years were documented; 30 (21.0%) women experienced return of their menses, 22 (15.4%) had >1 oocyte cryopreserved, 13 (9.1%) stated they had already completed their families, 13 (9.1%) stated that they did not want children, 11 (7.7%) experienced premature menopause, 3 (2.1%) managed a successful pregnancy and birth (no IVF documented), 2 (1.4%) had embryos cryopreserved, and 2 (1.4%) unsuccessfully attempted to achieve pregnancy (1 using IVF). Just more than a quarter (n=37; 25.9%) had no measured fertility-related outcome documented (Table 3).
Fertility-Related Outcomes
| Outcome | n (%) |
|---|---|
| Return of menses | 30 (21.0) |
| Premature menopause | 11 (7.7) |
| Eggs cryopreserved | 22 (15.4) |
| Embryos cryopreserved | 2 (1.4) |
| Elective oophorectomy | 13 (9.1) |
| Successful pregnancy | 3 (2.1) |
| Unsuccessful pregnancy attempt | 2 (1.4) |
| Family already completed | 13 (9.1) |
| No children desired | 13 (9.1) |
| Not documented | 37 (25.9) |
For those with documented relapse, no new discussions were recorded regarding fertility.
Fertility Outcomes
In total, 5 patients had documented pregnancy posttreatment. Only 1 patient was documented to have undergone IVF and conceived, although later miscarried; 1 other patient had a documented miscarriage. Three women had pregnancies that resulted in live births at a mean age of 43 years, with the youngest at 38 years. One had documented oocyte preservation, but the mode of conception was not detailed in the notes. The possibility exists that more patients underwent IVF (≥1 cycles) and/or experienced miscarriages, but this was not captured in this retrospective chart review.
Discussion
This study investigated the frequency of documented fertility counseling in WoCBP with a cancer diagnosis treated at a major metropolitan cancer center in Australia. We identified that only 14.9% of the participants had a reproductive history recorded, with 12.6% of these at first consultation. Just more than half had a fertility preservation discussion recorded at some point with their oncologist or hematologist, and this proportion was slightly higher for patients with a breast cancer diagnosis (67% vs 58%). Elsewhere, significant variations in the incidence of fertility preservation discussions (9%–75%) have been reported,31–36 and the quality of discussion documentation is known to be poor even if fertility preservation is discussed.37
It is essential that oncologists and hematologists discuss fertility preservation at the first consultation before the administration of gonadotoxic treatment, and to furthermore allow sufficient time for an obstetric and gynecologic consultation to take place and fertility preservation processes such as egg harvesting to be performed if possible.15 If at that time a woman states that she does not wish to have children, this is not necessarily a permanent decision, particularly in younger cohorts, and efforts should be taken to discuss fertility preservation options even if patients believe they will not pursue childbearing later down the line.
Fertility preservation discussions were more common for patients with breast cancer. This is likely due to their treating physicians being more familiar with treating WoCBP38 and having more established guidelines for this population,39 the advocacy efforts of patient groups on this issue, and the rates of fertility preservation increasing at a fast rate in young patients with breast cancer.40
International uptake and utilization of fertility counseling and preservation remains unacceptably low, with only 4% to 50% of young people undertaking fertility preservation in a timely fashion.15 Gender inequality and implicit bias remains rife in research and clinical practice.41–43 The lack of attention to women’s health issues is a long-standing issue, and women’s autonomy to make independent decisions regarding their bodies is often deprioritised.41 As cancer survival rates continue to improve44 and more women delay childbearing,45 the proportion of cancer survivors wishing to bear children is increasing.
The reduced rates of reproductive history taking by treating oncologists/hematologists represents an unmet need in service delivery for women of childbearing age. There are many possible reasons for the low rate of fertility discussions with patients and/or documentation of discussions. In some cases, such as life-threatening malignancies where immediate treatment is recommended (eg, acute leukemia), advanced cancers involving the reproductive system, or life-threatening events, the urgency and time-sensitive nature of management strategies may lead to reproductive concerns and fertility implications being overlooked.46 However, these discussions are important to women and a discussion of future fertility is warranted.47 A subset of patients may not want children, but this must be clearly established and documented.48 Physicians may be distracted by competing priorities, have implicit bias in who they refer for fertility preservation,49,50 or have received limited training on options available.37,51 This may ultimately lead to decision-making regarding fertility preservation occurring with a sense of urgency and subject to the real (or perceived) prospect of mortality, causing patients to feel rushed, unprepared, dissatisfied, or regretful of their choices.52 Importantly, a WoCBP may not want to have children at the time of her cancer diagnosis, but these wishes may change, and physicians must advocate for timely consideration of fertility preservation when appropriate.
Only 58.0% of the cases in our study had discussions regarding fertility and options to preserve fertility, despite access to publicly funded oncofertility services. It is difficult to establish the reasoning for this based on analysis of medical records. Perhaps several women declined fertility preservation due to personal circumstances/desires, but this was not captured in the documentation. It is also conceivable that fertility discussions were not addressed or documented for a variety of reasons. Counseling women near the time of diagnosis is crucial to enabling informed decisions about treatment and fertility preservation. Patients and nurses53 agree that oncologists should initiate fertility discussions and provide written information to their patients.54,55 Gynecologists are thought to have the best knowledge and most confidence providing advice and referring patients for fertility preservation,56 but hematologists/oncologists need to initiate the discussion and provide information about the fertility risks associated with the planned cancer treatment, and refer patients to a fertility preservation specialist.57 An online survey revealed that women with breast cancer reported that fertility concerns influenced their decision-making,58 and cancer-related infertility has been associated with greater psychological distress.24 Indeed, in one survey of patients with cancer, more than half cited that having a child was “the most important” priority in their life and 62% were “most concerned” with the impact the cancer treatment would have on their fertility.59 ASCO highly recommends a timely gynecology referral in this setting, notwithstanding the competing urgency of initiating anticancer therapy.60 Even if patients do not ultimately pursue oocyte or embryo cryopreservation,24 referral to a fertility specialist is crucial to ensure women are fully informed regarding the implications of their cancer treatment on future fertility and have autonomy making fertility preservation decisions.
Several successful strategies translating to improved fertility preservation discussions and referral rates have been illustrated in the literature. Educating health care providers on the long-term fertility consequence of cancer treatment and the clinical value of available fertility preserving options has been shown to improve fertility referral rates.25,61 The establishment of cancer center policies specifying that oncologists/hematologist have primary responsibility for educating patients about their fertility options has also been shown to be beneficial.15 Decision aids are known to help guide fertility preservation discussions by improving patient knowledge, decreasing decisional conflict, and reducing decisional regret about fertility treatment compared with standard care not involving the provision of decision aids.62 Improved referral rates have been associated with centers promoting collaboration between cancer and fertility specialists.63 Another successful strategy has been the implementation of information technology system prompts and standardized referral pathways, and employing patient navigators to assist with this process.57,64,65
The limitations of this study include its retrospective nature and the short follow-up period of 1 to 4 years, and therefore long-term fertility outcomes may not be fully captured. Furthermore, fertility conversations may have occurred but not been documented.66
Further research combining data from multiple institutions with longer follow-up times and statistical analysis would be greatly beneficial in further characterizing routine cancer care. Guidelines need to provide sufficient detail to inform real-world application and effective strategies to reduce or avoid key implementation barriers.15 There is a role for information system solutions and telehealth in facilitating documentation, standardizing practice, and improving referral rates.57,64,65 This could include EMR prompts for question-taking, standardized templates for referrals, having “internal champions” who ensure all WoCBP are offered fertility preservation referrals and that these referrals are received, and having patient navigators actively guide patients through the process if they choose to proceed.57,65 Improved provision of education and resources for oncology and hematology staff in the medical and allied health fields would be of great value. Patients want written information and decision aids,15 and doctors could improve their knowledge of fertility preservation options through grand rounds,67 internal education sessions,68 and center-initiated online training modules.61 Resources and education could include the importance of reproductive history taking and referrals, signs of declining fertility such as amenorrhea, and options available to preserve fertility. This information should also be provided to patients in writing. Qualitative and service development research in this area should be used to develop standardized national recommendations on this topic to support the overall well-being and quality of life of female patients with cancer.
Conclusions
Findings of our study showed that in a major cancer center, only half of women of childbearing age with a new cancer diagnosis had documentation of reproductive counseling. There is certainly room for improvement to ensure women have access to fertility preservation and gynecologic input in the future, as survival rates in this age group are steadily improving. Clinicians have a moral imperative to promote and facilitate reproductive counseling and oncofertility referral where it aligns with patients’ wishes. As treating clinicians in this setting, oncologists and hematologists are well placed to initiate timely fertility discussions and oncofertility referral. Systems-based changes are required to promote early fertility discussions, with improved education, documentation, and guidelines in the oncofertility setting to ensure these important conversations occur.
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