Ann Surg Oncol DOI 10.1245/s10434-016-5423-9
ORIGINAL ARTICLE – BREAST ONCOLOGY
Oncofertility Knowledge, Attitudes, and Practices of Canadian Breast Surgeons Ellen Warner, MD, MSc1,2, Samantha Yee, PhD3, Erin Kennedy, MD, PhD2,4, Karen Glass, MD2,3, Shu Foong, MD5,6, Maureen Seminsky, RN1, and May Lynn Quan, MD, PhD6,7 Division of Medical Oncology, Sunnybrook Odette Cancer Centre, Toronto, ON, Canada; 2University of Toronto, Toronto, ON, Canada; 3CReATe Fertility Centre, Toronto, ON, Canada; 4Mount Sinai Hospital, Toronto, ON, Canada; 5 Regional Fertility Program, Calgary, AB, Canada; 6University of Calgary, Calgary, AB, Canada; 7Tom Baker Cancer Centre, Calgary, AB, Canada 1
ABSTRACT Background. Guidelines recommend that oncologists discuss treatment-related fertility issues with young cancer patients as early as possible after diagnosis and, if appropriate, expedite referral for fertility preservation (FP). This study sought to determine the attitudes and practices of Canadian breast surgeons regarding fertility issues, as well as barriers to and facilitators of fertility discussion and referrals. Methods. Semistructured telephone interviews were conducted with 28 site lead surgeons (SLSs) at 28 (97 %) of 29 centers (25 % cancer centers, 64 % teaching hospitals) across Canada participating in RUBY, a pan-Canadian research program for young women with breast cancer. In addition, 56 (65 %) of 86 of their surgical colleagues (nonsite lead surgeons [NSLSs]) completed an online survey of their oncofertility knowledge, attitudes, and practices. Results. Of the 28 SLSs (43 % male, 36 % in practice\10 years), 46 % had inadequate oncofertility knowledge, 25 % discussed fertility only if mentioned by the patient, 21 % believed fertility discussion and referral were the mandate of the medical oncologist, and 45 % did not know of an FP center in their area. More than 80 % of the NSLSs (54 % male, 30 % in practice \10 years) were unfamiliar with oocyte or embryo cryopreservation; 36 % never or rarely discussed fertility issues; and 51 % thought referral to a fertility specialist was not their responsibility.
Ó Society of Surgical Oncology 2016 First Received: 31 March 2016 E. Warner, MD, MSc e-mail:
[email protected]
Conclusions. Oncofertility knowledge was low among the SLSs, especially the NSLSs, and barriers to referral were identified. An oncofertility knowledge translation intervention specifically for breast surgeons is being developed to increase surgeon knowledge and awareness of oncofertility issues and referral.
For many young breast cancer patients, the effect of treatment on their fertility is of utmost concern, second only to fear of recurrence.1–3 Chemotherapy is toxic to the oocyte-containing primordial follicles, frequently leading to immediate or premature infertility,4 and the required delay in attempting conception after anti-estrogen therapy also reduces fertility due to the natural effects of aging. Treatment-related infertility has become an increasingly important issue because of the progressive delay in childbearing in developed countries,5 higher breast cancer survival rates,6 confirmatory evidence of the safety of pregnancy after breast cancer,7,8 recent data that 10 years of tamoxifen is more effective than 5 years,9 and improvements in fertility preservation (FP) techniques. The American Society of Clinical Oncology (ASCO) issued guidelines in 2006,10 updated in 2013,11 recommending that health care providers discuss the risk of infertility with cancer patients and refer patients to reproductive specialists as soon as possible after diagnosis if treatment is expected to affect future fertility (key recommendations summarized in Appendix 1). The most common methods of FP chosen by women with breast cancer are embryo or oocyte cryopreservation. The latter is generally preferred by women without a partner.12 Early referral to a fertility clinic has a threefold benefit: minimum systemic therapy delay,13 maximum
E. Warner et al.
time for difficult decision making,14 and sufficient time for additional FP cycles if necessary.15 Studies have consistently found that many oncologists do not follow the ASCO guidelines.16–18Assessment by a surgeon usually is the first step in the management of breast cancer. Therefore, an opportunity exists for early referral for FP by the surgical team. However, in our review of the literature, we found no studies examining breast surgeon awareness and attitudes toward oncofertility counseling, barriers to communication with young women with breast cancer (YWBC), or facilitators of such communication. The Reducing the bUrden of Breast cancer in Young women (RUBY) study is a pan-Canadian research program targeting YWBC. The backbone of this program, which has four substudies, is the assembly of a prospective cohort of 1200 women, 40 years of age or younger, with newly diagnosed breast cancer at 29 sites across Canada during 4 years. One of the RUBY substudies, Surgeon and Patient Oncofertility Knowledge Enhancement (SPOKE), is a fertility knowledge translation intervention based on the principles outlined by Cabana et al.19 for Canadian general surgeons and surgical oncologists who treat YWBC. The goals of SPOKE are to increase the probability that a fertility discussion will take place between every young woman with a new diagnosis of potentially curable breast cancer and her surgeon and that each of these women who did not definitely complete her family before the diagnosis will be offered a referral for an FP consultation. The SPOKE intervention will include a comparison of the preand post-intervention oncofertility knowledge, attitudes, and practice patterns of the breast surgeons. This report describes the results of the pre-intervention assessment of SPOKE. The post-intervention assessment will be reported in a subsequent publication. METHODS The study was approved by the Sunnybrook Health Science Centre Research Ethics Board. A phone interview guide was developed by the study investigators, with topics examining surgeons’ demographics and oncofertility knowledge together with their attitudes and practice regarding fertility discussion and FP referral. The interview guide content was adapted into a 10-min online survey covering similar topics (Appendix 2). Three surgical oncologists provided feedback on the interview guide and pilot-tested the survey before data collection. Site Lead Surgeon Interviews The 29 RUBY sites represent a sample from across Canada in a variety of practice settings. A site lead surgeon
(SLS) had been identified previously from among the general surgeons at each of the sites, who voluntarily took on the role of leading the clinical research at that center for RUBY. These 29 SLSs were invited by e-mail to participate in a pre-intervention 30-min semistructured telephone interview. The participants were told that after a future interview (after an oncofertility knowledge translation intervention) they would receive a $250 honorarium to cover both interviews. The pre-intervention interviews, conducted between November 2014 and February 2015 by a single interviewer, were audio-recorded and transcribed verbatim. Non-Site Lead Surgeon Surveys Each RUBY site hosts one to nine general surgeons in addition to the SLS. The SLSs were asked to provide contact information for the other surgeons in the clinic/ office, who were then invited via e-mail to participate in SPOKE and complete the online survey. Because these non-site lead surgeons (NSLSs) had not previously committed to participate in RUBY, a higher rate of response to the survey than to an interview invitation was anticipated. Repeated reminders were sent during a 4-month period between February and May 2015. The participants were offered a $25 gift certificate. Statistical Analysis The transcribed interviews were kept anonymous before evaluation. Each transcript was independently analyzed by two investigators (S.Y. and M.S.) through an iterative process of coding recurrent themes using constant comparative methods20 to discern commonalities and deviations in experiences. The SLS oncofertility knowledge was assessed by seven questions, with answers graded as ‘‘good knowledge’’ or ‘‘inadequate knowledge’’ by two independent investigators (S.Y. and E.W.) blinded to the other responses. ‘‘Good knowledge’’ was defined as an answer that was either correct and complete or almost complete with no misinformation. ‘‘Inadequate knowledge’’ was defined as either no answer or misinformation. Differences in scoring were resolved by consulting other investigators in the SPOKE team to reach consensus. The questions with examples of good and inadequate answers are shown in Table 2. Descriptive statistics, cross-tabulation, and Fisher’s exact tests were conducted using SPSS v23 (IBM Analytics). A cutoff p value lower than 0.05 indicated statistical significance. Extracts from interviews are used to illustrate the major themes arising from this analysis. Texts within square brackets are editorial notes for clarification purposes. Three dots (. . .) indicate omitted text.
Oncofertility and Breast Surgeons TABLE 1 Characteristics of site lead surgeons and non-site lead surgeons
Response rate
Site lead surgeons (n = 28) n (%)
Non-site lead surgeons (n = 56) n (%)
28 / 29 (97)
56 / 86 (65)
Gender 12 (43)
30 (54)
Female
16 (57)
26 (46)
6 (21)
13 (23)
Age (years) 12 (43)
19 (34)
50–59
9 (32)
16 (29)
60?
1 (4)
8 (14)
Years in practice \10 10–19 20? Location of practice Atlantic
19 (34)
9 (32)
20 (36)
3 (11)
7 (12)
4 (14)
8 (14)
Ontario
11 (39)
26 (46)
Prairies
5 (18)
8 (14)
West Coast
4 (14)
5 (9)
Northern Territories
1 (4)
2 (4)
7 (25)
20 (36)
18 (64)
32 (57)
3 (11)
4 (7)
Type of facility Cancer center University-affiliated teaching hospital Non-teaching hospital or health center
2 (7)
10 (18)
25–49
7 (25)
15 (27)
50–75
4 (14)
15 (27)
15 (54)
16 (29)
No. of breast surgeons at center 5 (18)
16 (29)
4–5
17 (61)
33 (59)
C7
6 (21)
7 (12)
No. of YWBC seen per month 1–2
Site Lead Surgeons (n=28)
0.005 0 (0)
10 (18)
18 (64)
38 (68)
3–4
5 (18)
7 (12)
C5
5 (18)
1 (2)
Fisher’s exact test
Often or Routinely
Non-Site Lead Surgeons (n=56)
FIG. 1 Site lead surgeons were significantly more likely to have a fertility discussion with their young breast cancer patients than nonsite lead surgeons (Fisher’s exact test, p = 0.002)
The 29 RUBY sites represent a geographic sample from across Canada. Of these sites, 25 % were cancer centers, 64 % were university-affiliated or academic centers, and 11 % were non academic or rural centers. The distance from a site to the nearest fertility center was less than 10 km for 65 % of the sites, 11–49 km for 8 % of the sites, 50–99 km for 4 % of the sites, and 150 km or more for 23 % of the sites.The demographics of the 28 interviewed SLSs (97 % response rate) and the 56 surveyed NSLSs (65 % response rate) are shown in Table 1. SLS Interviews
NS not significant; YWBC young women with breast cancer Bage 40 years a
Sometimes
RESULTS
NS
1–3
Close to none
0%
NS
\25
[75
4%
Frequency of fertility discussion
NS
% Breast cancer of practice
20%
Never or Rarely
NS
Quebec
25%
20% 10%
17 (30)
9 (32)
44% 36%
30%
NS 10 (36)
60%
40%
NS
40–49
71%
70%
50%
NS
Male
30–39
p valuea
80%
Most of the SLSs (89 %) were unaware of the ASCO oncofertility guidelines. Although 71 % of the SLSs usually or routinely discussed the potential negative impact of adjuvant systemic therapy on fertility (Fig. 1), 25 % did so only when the patient initiated the discussion. Only 18 % were aware of a FP referral protocol at their clinic. Table 2 summarizes the SLS oncofertility knowledge assessed by seven questions with illustrative quotes. Overall, more than half of the SLSs were not fully aware of available FP options, estimated FP success rates, or the implications of tamoxifen on future fertility, and about one third were not aware of factors affecting the success of FP or the time it takes a woman to undergo FP. Among the 15 SLSs rated as having good knowledge (Table 2), 80 % usually or routinely discussed fertility issues with their patients compared with 62 % of the 13 SLSs with inadequate knowledge. In addition, good knowledge was found to be significantly associated with surgeons who had 50 % or more of their practice devoted to
E. Warner et al. TABLE 2 Examples of ‘‘good’’ and ‘‘inadequate’’ oncofertility knowledge of site lead surgeons Question
Good knowledge n (%)
Illustrative quote
(a) Do you think postcancer pregnancy would affect prognosis?
25 (89)
‘‘Nope. Only if it means stopping their treatment. But getting pregnant after having breast cancer does not increase your risk per se. But if you don’t take your tamoxifen for years to get pregnant, that may affect things. [Interviewer: Does it depend on ER status?] I guess so; it depends on what the patient is doing to get pregnant.’’ [#111]
3 (11)
‘‘My gut instinct is yes, but I do not know the numbers. Biologically it would make sense if you throw all those hormones at someone who might have a growing cancer, it will make their cancer worse. Probably for the study, I should say no; honest opinion is yes.’’ [#110]
(b) What are the possible 23 (82) side effects of chemotherapy on fertility?
‘‘It will lower their chance of being pregnant after receiving chemotherapy. The older they are, the least chance they will be able to conceive afterward. The younger they are, the more chances they have for ovarian function to come back. So there is a relationship, but even very young women have a lower chance afterward.’’ [#103]
5 (18)
‘‘Short term, because they are systemically unwell; they would have a harder time getting pregnant while they are on chemotherapy, which is not a good idea. From a long-term point of view, if they are on hormonal treatment, that could be a problem.’’ [#125]
(c) Do women who get only tamoxifen but not chemotherapy have fertility issues?
8 (29)
‘‘Most women are on it for at least 5 years, 20 (71) and so you have a time span where they are not going to get pregnant. With the newer guidelines, some of the women are staying on this drug even longer. The biggest thing with tamoxifen is while you are on it, you are blocking estrogen, and you are getting older. The older you get, the less the fertility.’’ [#109]
‘‘Tamoxifen also affects fertility, I think it can do something to the oocyte, or there are increasing abnormalities or something.’’ [#122]
(d) Do you know what FP 13 (46) options are available to YWBC?
‘‘I know there is egg preservation and 15 (54) embryo preservation, sperm donor versus partner.’’ [#114]
‘‘Yes. You can stimulate the ovaries and follicles with Lupron, or you can do removal and cryopreservation.’’ [#113]
(e) What are your estimation of the FP success rate?
‘‘I would say 50 %. I think the age of the 22 (79) patient is a factor for sure. Probably the pre-morbid health of the patient would have an impact on that as well, and I suppose if there is a history of failed or delayed reproduction when trying, either because of any gynaecologic issues, they may impact.’’ [#116]
‘‘Not as much as we would like, I don’t know if it is 10 % or 20 %. Most people who have done FP, I can tell you I don’t remember any of them who actually gave birth afterwards.’’ [#112]
(f) What factors affect the 19 (68) FP success rate?
‘‘I would assume general medical condition, obesity, previous problems with fertility, polycystic ovary, stress of surgery, general stress of a chronic illness, cancer, and age of the patient obviously.’’ [#113]
‘‘I would think that stress would be one, general health another, specifics no.’’ [#114]
(g) How much time do 18 (64) you think would be required for patients to undergo FP?
‘‘It usually depends on where they are in 10 (36) their cycle. . . . If they have to wait for a cycle, then it can slow things down. If they are going onto chemo, they might have to wait. If they are going to have surgery, they might have to wait a month anyway, so it won’t really affect things.’’ [#111]
6 (21)
Inadequate knowledge n (%)
9 (32)
Illustrative quote
‘‘Probably a minimum of 2 to 3 months I would anticipate. I am not exactly sure; that is my own judgment.’’ [#116]
YWBC young women with breast cancer Bage 40 years, FP fertility preservation
breast cancer (p = 0.03) or saw three or more YWBC per month (p = 0.04). Statistical trends associated with the female gender of the SLS (p = 0.07) and age younger than 45 years (p = 0.06) also were observed.
The key themes with illustrative quotes associated with the barriers to fertility discussion and FP referral identified by the SLSs are summarized in Table 3.
Oncofertility and Breast Surgeons TABLE 3 Site lead surgeons’ perceived barriers to initiating a fertility discussion Key themes
Illustrative quotes
Clinical factors Advanced cancer stage or aggressive tumor
‘‘Metastatic cancer. I get really nervous in terms of how much we should be counseling about fertility preservation. . . . I think if they are metastatic it changes my approach.’’ [#113]
Urgency to start treatment
‘‘If they [patients] had a very aggressive tumor and needed neoadjuvant treatment. If we were to send them to a center to be assessed and it may take weeks and weeks to do the egg harvesting when they should be starting chemotherapy.’’ [#105]
Patient factors Demographics (being single, ‘‘Sometimes with young single women that are there with their parents, I am probably a little more careful belongs to certain ethnic groups, with what I say. So someone in their 30s who’s there with their mom, it might be a bit of a different and same-sex relationship) conversation than if they were there with their partners.’’ [#113] ‘‘Also certain ethnic groups where this is not discussed as easily. With white Anglo-Saxons, it’s easier; with others, I don’t know how to say it; ‘traditional’ groups it’s not talked about as easily. You kind of have to read the patient.’’ [#107] ‘‘Sexual preference: some of my patients come in with same sex-partners. I find I can’t have the conversation even though they may be interested in it and that option.’’ [#121] Perceived emotional barriers
‘‘I think the biggest ones are the emotional barriers where they have to think about that and the mortality and treatments for their breast cancer. Often they are not ready to talk about both things at once. ’’ [#115]
Perceived information overload
‘‘Sometimes I don’t mention it because the patient is just too overwhelmed and it’s just too much. . . . Every patient has a certain tolerance to what they are absorbing. . . . there is only so much information you can give at one time.’’ [#128]
Perceived reluctance to consider ‘‘They [patients] feel like they don’t have any time to wait. Most women think that if they are going to wait, FP they are going to die. So to see a fertility, it’s a delay;it does not matter how much you tell them, that it’s okay you can wait to get things done; it’s not going to affect anything. They don’t want to delay the surgery.’’ [#122] Physician factors Attitudes
‘‘I know at our tumor boards, there have been some attitudes discussed by other people that ‘‘why is a woman even worried about this. She should be worried about her survival, not her fertility.’’ If any health professional has this attitude, that could be a barrier.’’ [#109]
Knowledge
‘‘It’s [fertility preservation] very rarely brought up, and I generally would refrain from this discussion. I don’t have the expertise. I don’t like giving out information if I am not entirely clear with what I am discussing. I don’t like to give out information that I am not the expert on.’’ [#101]
Logistic factors Lack of time for discussion
‘‘Probably just time; you are seeing them for 10 to 15 min, and there is a lot to get through. . . . With the young patients, I find they are so overwhelmed with so much, for so many other reasons, it may fall off the list.’’ [#106]
Accessibility of FP services
‘‘Distance is the main issue . . . timely access to consultation. Even if the patient has the ways and means to travel to a place like that, it would also be important they could be seen before treatments get set and started.’’ [#116]
Time required to complete FP
‘‘I feel if they think there will be a delay in treatment, it is very stressful; waiting for treatments is stressful. The majority of people think it’s a magic bullet; there will be one stop and you are done. But there is a process, counseling, procedures, and some may decide not to go through with it because of this.’’ [#109]
Affordability of FP services
‘‘I think there are significant barriers to the patient in cost. . . . I think the hindrance and a barrier to some of the women who might want to, is the fact they know they have to pay.’’ [#104]
FP fertility preservation
NSLS Surveys Of the 56 NSLSs, 95 % were unaware of the ASCO oncofertility guidelines, and 36 % rarely or never discussed fertility issues with their patients (Fig. 1). Furthermore, 22 NSLSs (39 %) believed the evidence was insufficient to support FP referral, and 23 (41 %) never or rarely referred patients for FP.
Almost half of the NSLSs were unaware that breast cancer treatment was likely to damage oocytes permanently (45 %), impair ovaries’ ability to make hormones (43 %), or cause infertility (43 %), and 39 % did not think that chemotherapy was likely to cause premature ovarian failure. Only a minority were familiar with oocyte cryopreservation (18 %) or embryo (20 %) cryopreservation, and 48 % thought the waiting time to see a fertility specialist
E. Warner et al. TABLE 4 Factors non-site lead surgeons (n = 56) would consider when deciding whether to make a fertility preservation referral More likely to refer (%)
Less likely to refer (%)
No effect (%)
Sociodemographic factors a. Patient is married/partnered
27
2
b. Patient is single
14
7
78
0
49
51
d. Patient is \25 years old
54
4
42
e. Patient is [35 years old
13
46
42
0 0
14 11
86 89
0
41
59
c. Patient already has children
f. Patient is in a same-sex relationship g. Patient has low socioeconomic status
71
Clinical factors a. Patient is HIV-positive b. Patient has infectious disease (e.g., hepatitis B or C)
0
37
63
c. Patient has an aggressive form of cancer
2
48
50
d. Patient has a poor prognosis
4
65
32
e. Patient urgently needs to start cancer treatment
7
54
38
f. Patient has preexisting fertility problems before cancer diagnosis g. Patient is highly anxious and stressed about cancer diagnosis
28
13
59
6
26
68
Institutional factors a. Availability of fertility preservation educational materials within facility
32
6
63
b. Availability of assistance from colleagues (e.g., nurses and allied health) to make referral
44
6
50
c. Availability of institutional referral protocols
46
4
50
PUB1 because YWBC includes the plural noun ‘‘women,’’ I didn’t add an ‘‘s’’ when it was used in the plural form, but this makes awkward reading. You decide if YWBCs would be a proper usage. If so, then you will need to change YWBC to YWBCs at some places in this file
was 2 weeks or more. Almost half stated they did not know how long FP would take, and a significant proportion of the remaining NSLSs thought oocyte cryopreservation (7/32, 22 %) or embryo cryopreservation with partner sperm (14/ 30, 47 %) or donor sperm (17/30, 57 %) would take 5 weeks or longer. A total of 22 NSLSs (40 %) believed it was the duty of the medical oncology team rather than the surgeons to initiate fertility discussions. Compared with the surgeons who assumed responsibility for fertility discussion, the surgeons who did not think FP was their clinical responsibility were significantly less familiar with oocyte cryopreservation (24 % vs 64 %; p = 0.003) and embryo cryopreservation (35 % vs 73 %; p = 0.005), significantly less comfortable discussing oocyte cryopreservation (p = 0.006) and embryo cryopreservation (p = 0.017) with their YWBC, and significantly less likely to think the clinical evidence was sufficient to support referring their YWBC for FP (p = 0.028). As shown in Table 4, the three most common patient factors deterring NSLSs from FP referral were poor prognosis (65 %), urgent need to start chemotherapy (54 %), and already having children (49 %). One fourth of NSLSs indicated they would be less likely to refer a highly anxious YWBC for FP.
Surgeon Recommendations The most common suggestions of the SLSs and NSLSs for increasing the frequency of FP referrals were providing training for surgeons to improve their knowledge base and confidence in fertility discussion, involving other disciplines such as nursing and social work in the fertility discussion and FP referral process, and using clinical tools such as a checklist and a prompt sheet. DISCUSSION It is unusual in medicine, and certainly counterintuitive, for a medical specialist to be asked to take an active role to prevent toxicity of a treatment that will be administered by a physician in a different specialty. Yet, in the case of preventing chemotherapy-related infertility, an opportunity exists for the surgeon, usually the first specialist consulted by a young woman with breast cancer, to initiate fertility discussions and make FP referrals. For women with breast cancer, this may be the most efficient way to fulfill the recommendations of the ASCO11 guidelines. Frequently, FP can be conveniently performed during the weeks between the completion of surgery and the start of chemotherapy, obviating any treatment delay.
Oncofertility and Breast Surgeons
To the best of our knowledge, this is the first study to focus specifically on the oncofertility attitudes, practices, and knowledge of breast surgeons. Because the SLSs in the RUBY study were often opinion leaders for their centers, were more likely to have a higher percentage of their practice devoted to breast cancer, and generally saw more YWBC than their colleagues, one expects the SLSs to be more knowledgeable about oncofertility issues, more likely to discuss fertility with their patients, and more likely to take responsibility for FP referral. Unfortunately, the different approaches used to survey the two groups (interviews vs online surveys) precluded us from making direct comparisons for most items. However, the question about frequency of fertility discussion was worded similarly in the interview and the online survey, and, indeed, the SLSs were significantly more likely to have such discussions (p = 0.002). It is also important to note that even the SLSs showed room for improvement in following the oncofertility recommendations set by ASCO. For example, 29 % of the SLSs only occasionally discussed fertility issues if ever, and another 18 % did so only if the discussion was initiated by the patient. Our study demonstrated several practical ways to facilitate universal implementation of the ASCO guidelines. Oncofertility Knowledge Translation In both the SLS interviews and the NSLS surveys, the surgeons with greater knowledge concerning the harmful effects of systemic cancer treatments on fertility and those who had greater familiarity with FP procedures were more likely to discuss fertility issues with patients and more likely to take responsibility for FP referral. Moreover, some of the surgeons (e.g., surgeon 101; Table 3) specifically mentioned inadequate oncofertility knowledge as a barrier to fertility discussion. Increasing surgeons’ knowledge of FP not only will lead to increased referrals to oncofertility experts but also will increase surgeons’ comfort level in discussing fertility and minimize the risk of patients receiving misinformation. Specific knowledge deficits of surgeons that should be addressed include safety of pregnancy after breast cancer, time required for FP, and the negative effect of patient age on the success of FP.
Written Materials for Patients Describing FP Options Written materials describing FP options not only would shorten the discussion time needed by the surgical team but also would facilitate patient decision making about FP. During a long initial consultation in which many new concepts and complex decisions are discussed, take-home literature such as a brochure may assist in providing information that can be read by the patient at home when she has time to focus on it. The strengths of our study included the mixed methods design, the very high SLS response rate, and the relatively high NSLS response rate. However, our study had several limitations. Because 88 % of the surgeons worked at teaching hospitals or cancer centers, our results are not as generalizable to community or rural surgeons. A study by Yee et al.18 evaluating FP practice in Ontario found nonacademic clinicians to be even less informed about oncofertility issues than their academic counterparts, which is likely the case among surgeons as well. In the next phase of SPOKE, we plan to create a knowledge translation intervention for all the RUBY study surgeons based on information identified in the current study. All the SLSs have participated in a 90-min seminar given by an oncofertility expert. The seminar has been videotaped and is available online for repeat viewing of the SLSs and for sharing with their colleagues. We have created a one-page FP option grid for surgeons, with a simplified version for patients. In addition, we are issuing reminders to surgeons about fertility discussion as soon as they recruit a patient to RUBY. Interviews and surveys with surgeons will be repeated in 2 years to determine whether attitudes and practices have changed. Ideally, at least a cursory mention of fertility will become part of the routine ‘‘script’’ of information that surgeons share with newly diagnosed YWBC. Many studies have shown that the act of having a fertility discussion with the patient itself improves her well-being and quality of life.21 Such discussions deliver the strongest possible positive message about her cancer—that she is expected to live long enough to raise a future child. ACKNOWLEDGMENT This study was supported by a Grant from the Canadian Breast Cancer Foundation and Canadian Institutes of Health Research (#OBW139590). DISCLOSURE
There are no conflict of interest.
Fertility Consultation Referral Protocols Suggestions from the SLSs and NSLSs to improve the logistics of fertility referral included checklists for the surgeon or surgical team, availability of nurses or other staff to whom the discussion and/or referral could be delegated, and a designated fertility specialist willing to expedite referrals.
APPENDIX 1: KEY RECOMMENDATIONS OF ASCO ONCOFERTILITY GUIDELINES11,12 –
Discuss fertility preservation with all patients of reproductive age (and with parents or guardians of adolescents) if infertility is a potential risk of therapy.
E. Warner et al.
–
Refer patients who express an interest in fertility preservation (and patients who are ambivalent) to reproductive specialists. Address fertility preservation as soon as possible, before treatment starts. Document fertility preservation discussions in the medical record. Answer basic questions about whether fertility preservation may have an impact on successful cancer treatment. Refer patients to psychosocial providers if they experience distress about potential infertility. Encourage patients to participate in registries and clinical studies.
– – –
– –
11.
a. Oocyte cryopreservation b. Embryo cryopreservation using partner sperm c. Embryo cryopreservation using donor sperm d. Ovarian tissue cryopreservation 12.
YWBC refers to newly diagnosed Young Women With Breast Cancer 40 years of age or older.
3. 4.
5. 6.
7. 8.
9.
10.
Gender: male or female Age (i.e., \30, 30–39, 44–49, 50–59, 60–69, 70? years) Number of years in practice as a breast surgeon after training. What percentage of your practice is breast cancer surgery? (i.e., \25 %, 25–49 %, 50–74 %, [75 %, 100 %) Location of facility (i.e., Atlantic, Que´bec, Ontario, Prairies, West Coast, Northern Territories) What type of facility do you work at? (i.e., specialized cancer center, university-affiliated teaching hospital, non-teaching hospital or health center, or other, please specify) Number of staff surgeons at your center performing breast cancer surgery. What is your level of familiarity with the following fertility preservation options for YWBC on a scale from 1 (not familiar at all) to 5 (highly familiar): (a) Oocyte cryopreservation. (b) Embryo cryopreservation. (c) Ovarian tissue cryopreservation. How comfortable are you discussing the following fertility preservation options with your YWBC on a scale from 1 (not comfortable at all) to 5 (very comfortable): (a) Oocyte cryopreservation. (b) Embryo cryopreservation. (c) Ovarian tissue cryopreservation. Do you think there is enough clinical evidence in the research literature to support referring YWBC for fertility preservation? Please respond on a scale from 1 (strongly disagree) to 5 (strongly agree).
Which of the following are possible side effects of cancer treatment on YWBC? (i.e., extremely unlikely, unlikely, neutral, likely, extremely likely, not sure) a. Damage and destroy egg supply permanently b. Impairs ovaries ability to make hormones. c. Menstrual periods stopped temporarily d. Infertility e. Premature ovarian failure (premature menopause) f. Subfertility g. Birth defects in future offspring h. Higher risk for miscarriage
APPENDIX 2: NON-SITE LEAD SURGEON QUESTIONNAIRE
1. 2.
How much time do you think would be required for a patient to complete the following fertility preservation procedures? (i.e., \1 week, 1–2 weeks, 3–4 weeks, 5–6 weeks, [6 weeks, not sure)
13. 14.
15.
16.
17.
18.
19.
How many YWBC do you see per month? (i.e., 0, 1– 2, 3–4, 5, or more) What percentage of your YWBC inquire about the side effects of cancer treatment on their capacity to have children post-treatment? (i.e., 0 %, B25 %, 26– 50 %, 51–75 %, 76–100 %) How often do you initiate a discussion mentioning the effects of cancer treatment on fertility? (i.e., never, rarely, sometimes, most of the time, routinely) How often do you discuss fertility preservation options? (i.e., never, rarely, sometimes, most of the time, routinely, only if asked by patient) What percentage of your YWBC at risk for infertility do you refer for fertility preservation consultation with an infertility specialist? (i.e., 0 %, B25 %, 26–50 %, 51–75 %, 76–100 %) Typically when do you refer your YWBC patients for fertility preservation consultation? (i.e., as soon as breast cancer is suspected even if pathology is pending, as soon as a cancer diagnosis is confirmed even if biomarkers are pending, after cancer diagnosis and biomarkers are confirmed but before surgery, after surgery when final pathology is available, typically I do not refer for fertility preservation consultation) Do you know where to refer your YWBC for the following fertility preservation options? (i.e., yes, no, not sure)
Oncofertility and Breast Surgeons
f. Node negative, triple negative, [2 cm g. All other node-negative patients who may require systemic therapy
a. Oocyte or embryo cryopreservation b. Ovarian tissue cryopreservation 20.
21.
22.
23.
Do you know a fertility clinic with expertise in fertility preservation for YWBC within your area? (i.e., no, not sure, if yes, please specific distance from your center in km) How long do you think YWBC have to wait to see a fertility specialist after a referral is made? (i.e., a few days, 1 week, 1.5 weeks, 2 week, 2.5 weeks, C3 weeks) Does your clinic have guidelines or protocols for referring YWBC for fertility preservation procedures? (i.e., no, not sure, if yes, please elaborate) What factors would you consider when deciding whether to refer YWBC for fertility preservation? (i.e., more likely to refer, less likely to refer, no effect) a. b. c. d. e. f. g. h. i. j. k. l. m. n. o. p. q. r.
24.
Patient is married/partnered Patient is single Patient already has children Patient is \25 years old Patient is [35 years old Patient is in a same-sex relationship Patient is HIV positive Patient has infectious disease (e.g., hepatitis B, C) Patient has an aggressive form of cancer Patient has a poor prognosis Patient urgently needs to start cancer treatment Patient has low socioeconomic status Patient has preexisting fertility problems before cancer diagnosis Patient is highly anxious and stressed about cancer diagnosis Availability of fertility preservation educational materials within facility Availability of assistance from colleagues (e.g., nurses and allied health) to make referral Availability of institutional referral protocols Others, please specify
What is your level of support or opposition for recommending fertility preservation to YWBC with the following cancer stage? (i.e., strongly oppose, somewhat oppose, neutral, somewhat favor, strongly favor, no opinion). Please elaborate in the space provided. a. Oligometastatic (i.e., 1 or 2 bone mets) b. Locally advanced or inflammatory c. 10 or more positive lymph nodes d. 4–9 positive lymph nodes e. 1–3 positive lymph nodes
25.
With regard to providing fertility preservation to YWBC, who at your center (i.e., staff surgeon, surgical fellow or resident, clinic nurse, social worker, medical oncology team, family physician) is primarily responsible for a. Initiating the fertility discussion b. Referring patient to see a fertility specialist
26.
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28.
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Do you think there are psychological benefits for YWBC receiving a fertility preservation consultation? Rate on a scale from 1 (strongly disagree) to 5 (strongly agree) Are you aware of any clinical practice guidelines on fertility preservation for cancer patients published by medical societies? (i.e., no, don’t know, if yes, please specify) Are you aware of any Canadian organizations that provide information, services and/or resources on fertility preservation to health care providers and cancer patients? (i.e., no, don’t know, if yes, please specify) Any other comments about this topic?
REFERENCES 1. Partridge AH, Gelber S, Peppercorn J, et al. Web-based survey of fertility issues in young women with breast cancer. J Clin Oncol. 2004;22:4174–83. 2. Peate M, Meiser B, Hickey M, Friedlander M. The fertility-related concerns, needs, and preferences of younger women with breast cancer: a systematic review. Breast Cancer Res Treat. 2009;116:215–23. 3. Gorman JR, Usita PM, Madlensky L, Pierce P. Young breast cancer survivors: their perspectives on treatment and fertility concerns. Cancer Nurs. 2011;34:32–40. 4. Stearns V, Schneider B, Henry NL, Hayes DF, Flockhart DA. Breast cancer treatment and ovarian failure: risk factors and emerging genetic determinants. Nat Rev Cancer. 2006;6:886–93. 5. Mathews TJ, Hamilton BE. Delayed Childbearing: More Women Are Having Their First Child Later in Life. NCHS Data Brief, no. 21. NationalCenter for Health Statistics, Hyattsville, MD, 2009. 6. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin. 2007;57:43–66. 7. Azim Jr HA, Santoro L, Pavlidis N, Gelber S, Kroman N, Azim H, Peccatori FA. Safety of pregnancy following breast cancer diagnosis: a meta-analysis of 14 studies. Eur J Cancer. 2011;47:74–83. 8. Pagani O, Partridge A, Korde L, et al. Breast International Group; North American Breast Cancer Group Endocrine Working Group. Pregnancy after breast cancer: if you wish, ma’am. Breast Cancer Res Treat. 2011;129:309–17. 9. Davies C, Pan H, Godwin J, et al .Adjuvant Tamoxifen: Longer Against Shorter (ATLAS) Collaborative Group. Long-term effects of continuing adjuvant tamoxifen to 10 years vs stopping
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at 5 years after diagnosis of estrogen receptor positive breast cancer: ATLAS, a randomised trial. Lancet. 2013:381:805–16. Lee SJ, Schover LR, Partridge AH, et al. American Society of Clinical Oncology. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24:2917–31. Loren AW, Mangu PB, Beck LN, et al. American Society of Clinical Oncology. Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2013;31:2500–10. Kim SS, Klemp J, Fabian C. Breast cancer and fertility preservation. Fertil Steril. 2011;95:1535–43 Kim, J, Oktay K, Gracia C, Lee S, Morse C, Mersereau J. Which patients pursue fertility preservation treatments? A multicenter analysis of the predictors of fertility preservation in women with breast cancer. Fertil Steril. 2012;97:671–6. Hill KA, Nadler T, Mandel R, Burlein-Hall S, Librach C, Glass K, Warner E. Experience of young women diagnosied with breast cancer who undergo fertility preservation consultation. Clin Breast Cancer. 2012;12:127–32. Lee S, Ozkavukcu S, Heytens E, Moy F, Oktay K. Value of early referral to fertility preservation in young women with breast cancer. J Clin Oncol. 2010;28:4683–6.
16. Quinn GP, Vadaparampil ST, Lee J-H, et al. Physician referral for fertility preservation in oncology patients: a national study of practice behaviours. J Clin Oncol. 2009;27:5952–7. 17. Adams E, Hill E, Watson E. Fertility preservation in cancer survivors: a national survey of oncologists’ current knowledge, practice and attitudes. Br J Cancer. 2013;108:1602–15. 18. Yee S, Fuller-Thompson E, Lau A, Greenblatt EM. Fertility preservation practices among Ontario oncologists. J Cancer Educ. 2012;27:362–8. 19. Cabana MD, Rand CS, Powe NR, Wu AW, Wilson MD, Abboud P-A C, Rubin HR. Why don’t physicians follow clinical practice guidelines? A framework for improvement. JAMA. 1999;282:1458–65. 20. Strauss, A. Basics of qualitative research: techniques and procedures for developing grounded theory. Sage, Thousand Oaks, CA, 1998. 21. Dashpande NA, Braun IM, Meyer FL. Impact of fertility preservation counseling and treatment on psychological outcomes among women with cancer: a systematic review. Cancer. 2015;121:3938–47.