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Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members
YGYNO-976888; No. of pages: 6; 4C: Gynecologic Oncology xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members Jaimin S. Shah a,⁎, Rosa Guerra a, Diane C. Bodurka b, Charlotte C. Sun b, Gary B. Chisholm b, Terri L. Woodard b,c a b c
Department of Obstetrics and Gynecology, UT Health, The University of Texas at Houston, McGovern Medical School, United States Department of Gynecologic Oncology and Reproductive Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, United States Department of Obstetrics and Gynecology, Division of Reproductive Endocrinology and Infertility, Baylor College of Medicine, Houston, TX, United States
H I G H L I G H T S • • • •
Number of reproductive aged women seen may influence fertility sparing treatment. Geographic region and practice setting also influences fertility sparing treatment. Most of the gynecologic oncologists felt collaborating with a RE was important. Collaboration can help optimize treatment planning for women considering a FST.
a r t i c l e
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Article history: Received 21 July 2017 Received in revised form 15 September 2017 Accepted 18 September 2017 Available online xxxx Keywords: Fertility sparing treatment Fertility preservation Early gynecologic cancer Provider attitudes Practice patterns Health care disparities
a b s t r a c t Objectives. This study aims to examine practice patterns of gynecologic oncologists (GO) regarding fertilitysparing treatments (FST) for gynecology malignancies and explores attitudes toward collaboration with reproductive endocrinologists (RE). Methods. An anonymous 23-question survey was sent to 1087 GO with a 14.0% completion rate. Descriptive statistics, Fisher's exact test, and Chi-square tests were used for data analysis. Results. The majority of GOs offer FST for gynecologic malignancies. Providers seeing larger numbers of reproductive age women were more likely to consider cancer prognosis (p b 0.03) and cancer stage (p b 0.01) as key factors. Providers in the Midwestern US considered socioeconomic status more often when offering FST than those in the South (p b 0.04). Those practicing in urban settings were more likely to feel that collaborating with a RE prior to treatment could improve treatment planning for women considering FST (p b 0.02). Finally, providers in urban or suburban areas more often felt collaboration with a RE improves pregnancy outcomes in women who pursue FST (p b 0.01, p b 0.02) compared to rural practitioners. Conclusions. While FST offers women the chance to pursue pregnancy after cancer, there are minimal data on factors that influence whether FST is offered and if collaboration with a RE is sought in the management of these patients. The number of reproductive age women seen, geographic location, and practice setting are important variables that may influence current practice. Understanding these factors can help identify opportunities to improve oncologic and reproductive outcomes of this patient population. © 2017 Elsevier Inc. All rights reserved.
1. Introduction Advances in cancer treatment have increased the number of reproductive aged (RA) survivors, many of whom have questions and concerns about fertility and family planning. The American Society of Clinical Oncology (ASCO) recommends that providers discuss the risk of cancer-related infertility and refer patients who are interested in ⁎ Corresponding author at: 6431 Fannin St, Suite 3.214, Houston, TX 77030, United States. E-mail address: [email protected] (J.S. Shah).
fertility preservation (FP) to reproductive specialists early in the course of treatment planning [1]. While practice guidelines encourage fertility counseling, there are limited data on the quality of these discussions. In addition, the type of information provided to patients is not well characterized and referral rates to reproductive endocrinologist remain low. Fertility sparing treatments (FST) of early gynecologic cancers offer women the opportunity to preserve fertility potential while effectively treating their disease. However, as with other cancers, conservative management of gynecologic cancers may still negatively impact fertility and reproductive outcomes. For example, conservative surgical
https://doi.org/10.1016/j.ygyno.2017.09.019 0090-8258/© 2017 Elsevier Inc. All rights reserved.
Please cite this article as: J.S. Shah, et al., Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members, Gynecol Oncol (2017), https://doi.org/10.1016/j.ygyno.2017.09.019
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management of women with ovarian cancer may compromise ovarian reserve and women receiving trachelectomies for early stage cervical cancer may be at increased risk of cervical stenosis, preterm labor, and difficulties trying to conceive, even with assisted reproductive technology [2–4]. In addition, there may be comorbidities that warrant additional management, such as women with endometrial cancer who often present with anovulation and/or polycystic ovarian syndrome. Because conservative management of early gynecologic cancers is viewed as “fertility-sparing”, the need for comprehensive fertility counseling and evaluation by a reproductive endocrinologist (RE) is often overlooked. Gynecologic oncologists (GO) often perceive fertility counseling as a lower priority; lack of training in FP counseling, being pressed for time in clinic and unfamiliar with new national guidelines pertaining to FP are other reasons why infertility risks may be disregarded [5]. However, a RE can contribute to treatment planning by assessing a woman's baseline fertility status, making reasonable estimates of likelihood for successful pregnancy and live birth, and counseling patients on fertility treatments that may be needed in the future [4]. Lack of initiating the conversation about fertility goals at the time of diagnosis and not providing patients with quality discussions regarding FP may affect how patients choose treatment options [6,7]. The impact of potential cancer-related infertility has important implications for a patient's quality of life and survivorship experience. Discussions about fertility concerns prior to cancer treatment have been shown to decrease regret scores, whether a woman chooses to preserve fertility or not [8]. RA patients who receive a FST have been shown to have a reduced risk of regret about fertility goals [9]. Providing these patients options for fertility preservation has been proven to be worthwhile and safe [10]. FST in eligible patients has been shown to result in survival rates similar to conventional therapy [11–15]. The purpose of this study was to examine practice patterns of GOs with regard to FST of gynecologic malignancies and explore their attitudes toward collaboration with REs. The purpose of our study was to understand how FST practice tendencies varied amongst providers and examine their thoughts toward collaboration with REs. Understanding FST factors such as the size of the provider's practice, geographic region, and practice setting may identify opportunities to improve counseling and promote collaboration to optimize oncologic and reproductive outcomes in this patient population. 2. Materials and methods The study was approved by the Institutional Review Board at The University of Texas MD Anderson Cancer Center. An anonymous 23question survey was developed and tested by the study team (Appendix A). The survey was tested for face validity by administering it to ten gynecologic oncologists at our institution and eliciting their feedback about the clarity and appropriateness of the questions. The survey was reiteratively edited until the majority agreed on wording. Once finalized, it was sent by email to Full and Candidate members (N = 1087) of the Society of Gynecologic Oncology (SGO); the only inclusion criteria were that participants must be a GO and a member of SGO. A free text area was provided where participants could leave comments. The study data were collected and managed using REDCap™ (Research Electronic Data Capture) tools hosted at MD Anderson [16]. Descriptive statistics, Fisher's exact test, and Chi-square tests were used for data analysis. 3. Results 3.1. Demographics A total of 163 surveys were received. Of the surveys received, 152 were eligible for inclusion, yielding a completion rate of 14.0% (152/ 1087). Data analysis was restricted to surveys that were partially (75%
Table 1 Provider characteristics. Variable Sex (N = 146) Female Male Years in practice (N = 150) 0–10 11–20 21–30 31+ Type of practice (N = 152) Private Academic Private + Academic Military Other Geographic distribution (N = 152) Northeast Midwest South West Outside US
N
%
71 75
48.6% 51.4%
74 36 27 13
49.3% 24.0% 18.0% 8.7%
25 80 40 4 3
16.4% 52.6% 26.5% 2.6% 2.0%
41 30 51 29 1
27% 19.7% 33.6% 19.1% 0.7%
of the questions) or entirely completed. Table 1 shows the demographics of the GOs. The characteristics of the participants included a relatively even split of male and female providers, approximately 50% have been in practice for N10 years, providers seeing a wide range of RA women, and at least 75% solely work at or are affiliated with an academic institution. There was a broad but yet relatively even geographic distribution of GOs with the South reporting the highest percentage (33%); 27% of participants practice in the Northeast, 19.7% in the Midwest, 19.1% in the West, and 0.7% outside the United States. The majority of providers (70.2%) practiced in an urban setting while others were in a suburban (25.8%) or rural (4.0%) setting. Many of the GOs (84.2%, 128/152) are involved with training residents/fellows and 83.6% (107/ 128) reported that they incorporate lessons into their curricula about how to discuss fertility issues with patients diagnosed with a gynecologic cancer. 3.2. Assessment of fertility status, referral to a RE, and collaboration Sixty-eight percent (68%) of GOs reported they always assess fertility status prior to initiation of cancer treatment while 18% “often” and 8.7% “sometimes” perform an assessment (Table 2). The method of fertility assessment reported varied amongst providers. Many GOs (74.2%) preferred using a reproductive specialist for this assessment (Table 3). However, when referring patients to a RE for FP counseling prior to offering a FST, only 16% of the GOs reported they “always” do this while 44% stated they “often” and 26% “sometimes” refer their patients Table 2 How often do GOs assess fertility status? (N = 150). How often do GOs refer to or consult a RE for FP counseling prior to offering FST? (N = 150). Variable Assessment of fertility status Always Often Sometimes Rarely Never Referral to RE Always Often Sometimes Rarely Never
N
%
102 27 13 5 3
68.0% 18.0% 8.7% 3.3% 2.0%
24 66 39 19 2
16.0% 44.0% 26.0% 12.7% 1.3%
GO, gynecologic oncologist; RE, reproductive endocrinologist.
Please cite this article as: J.S. Shah, et al., Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members, Gynecol Oncol (2017), https://doi.org/10.1016/j.ygyno.2017.09.019
J.S. Shah et al. / Gynecologic Oncology xxx (2017) xxx–xxx Table 3 What tools do GOs use to assess or determine fertility status? (N = 151). What factors do GOs consider when offering FST? (N = 151). Variable Fertility status assessment method Never assess fertility Reproductive specialist TVUS FSH Estradiol (E2) Inhibin B AMH HSG or sonohysterogram Estimation based on age Other method Factors to consider for FST Patient age Number of current children Socioeconomic status History of infertility Cancer prognosis PMH Cancer stage Cancer histology Patient's wishes Other
N
%
3 115 33 54 30 11 39 6 79 8
2.0% 74.2% 21.3% 34.8% 19.4% 7.1% 25.2% 3.9% 51.0% 5.2%
142 86 19 80 140 74 133 120 149 1
94.0% 57.0% 12.6% 53.0% 92.7% 49.0% 88.1% 79.5% 98.7% 0.7%
Abbreviations: GO, gynecologic oncologist; TVUS, transvaginal ultrasound; FSH, follicle stimulating hormone; AMH, anti-mullerian hormone; HSG, hysterosalpingogram; PMH, past medical history.
(Table 2). Providers considered several indicators when assessing patients' fertility function; approximately 51% of providers considered the patient's age, 34.8% used serum follicle stimulating hormone level and 25.2% used serum anti-mullerian hormone level (Table 3). Many GOs strongly agreed (64.9%) or agreed (21.9%) that it is easy to refer gynecologic cancer patients to a RE (Table 4). The majority of providers (94%) felt that collaboration with a RE can improve the treatment planning for women considering FST. In addition, 83.4% of participants felt that working with a RE (strongly agree/agree) can improve pregnancy outcomes for patients that pursue conservative management (Table 4). 3.3. Fertility sparing treatment for gynecologic cancers Approximately 98.0% of providers (148/151) offer some form of FST for early gynecologic cancers. For providers who offered FSTs, Fig. 1 Table 4 Is it easy to refer patients to a RE? (N = 151). Collaborating with a RE can improve treatment planning for women considering FST (N = 150). Collaborating with a RE can improve pregnancy outcomes in women who pursue conservative management (N = 151). Variable Referral is easy Strongly agree Agree Neutral Disagree Strongly disagree Collaboration improves treatment planning Strongly agree Agree Neutral Disagree Strongly disagree Collaboration improves pregnancy outcomes Strongly agree Agree Neutral Disagree Strongly disagree RE, reproductive endocrinologist.
N
%
98 33 7 8 5
64.9% 21.9% 4.6% 5.3% 3.3%
101 40 8 1 0
67.3% 26.7% 5.3% 0.7% 0.0%
92 34 24 1 0
60.9% 22.5% 15.9% 0.7% 0.0%
3
shows breakdown of all the treatment types. Table 3 highlights the factors providers consider when offering FST to eligible patients. Most commonly, the patient's wishes (98.7%), patient age (94%), cancer prognosis (92.7%), cancer stage (88.1%), and histology (79.5%) are factors evaluated. Many providers (38.4%) reported that they have a maximum age after which they do not offer FST. While the survey results yielded a wide range as to what this age is, most providers (60.4%) reported an age cutoff between 46 and 50 years of age. Providers seeing larger numbers of RA women were more likely to consider cancer prognosis (p b 0.004) and cancer stage (p b 0.02) as critical factors when considering FST (Table 5). Providers in an urban setting were more likely to report that collaborating with a RE prior to treatment could improve treatment planning for women considering FST (p b 0.02). Compared to rural practitioners, providers in urban or suburban areas more often felt that collaborating with a RE improved pregnancy outcomes in women who pursue FST (p b 0.01, p b 0.02). There were 106, 38, and 6 providers in an urban, suburban, and rural practice setting, respectively. 3.4. Feedback from study participants Interestingly, several GOs completed the free text field (N = 16) within the survey and shared additional thoughts about the topic. Some themes that emerged included: 1) the challenges that many face in trying to coordinate care with REs; 2) the recognition of the importance in trying to coordinate medical care; and 3) the assumption fertility would not be affected by a FST. These themes are summarized below with supporting quotes. 1. The challenges that many face in trying to coordinate care with REs 1.1. “There isn't a RE at our hospital and patients have limited access to private practitioners in the area due to high rates of poverty in our patient population.” 1.2. “I think it would be great to refer all patients who desire fertility preservation to a RE. However, we have such limited resources in our rural community. We have no RE associated with the university and all private REs do not take insurance. It is very challenging to coordinate care with private REs when planning cancer care.” 1.3. “We have only private practice REs in our area. Costs for IVF, harvesting storing etc. are prohibitive for anyone in low middle class and below.” 2. The recognition of the importance in trying to coordinate medical care 2.1. “I think a referral to a RE for treatment is critical given the timing of ovulation induction and treatment for cancer.” 3. The assumption fertility would not be affected by a FST 3.1. “The vast majority of my fertility sparing surgeries are for young women without a history of infertility with early stage disease.” 4. Discussion The purpose of our study was to examine practice patterns of GOs regarding FST for gynecology malignancies and explores attitudes toward collaboration with REs. Within our study population, most of the GOs felt collaborating with a RE was important as it can help optimize treatment planning for women considering a FST and improve pregnancy outcomes. Many GOs utilized various methods to assess fertility status. The majority of participants stated they offer some FSTs in their practice; we concluded the size of the provider's practice, geographic region, and practice location were potentially key variables that influenced FST consideration (Table 5). The study indicated many providers refer their patients to a RE but this was not the case for everyone. The lack of RE referrals can be attributed to various barriers. Of note, the free response portion of the survey raised concerns for socioeconomic barriers to access a RE. Identifying and understanding the barriers to collaboration between GOs and REs are important first steps toward improving access to fertility counseling and treatment.
Please cite this article as: J.S. Shah, et al., Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members, Gynecol Oncol (2017), https://doi.org/10.1016/j.ygyno.2017.09.019
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J.S. Shah et al. / Gynecologic Oncology xxx (2017) xxx–xxx
Fig. 1. Fertility sparing treatments offered by providers (N = 148).
Our results showed many GOs perform various FSTs for early stage gynecologic cancers. This offers the opportunity for women who would otherwise be infertile from conventional treatment; however, it is not fail-proof. Some women may unknowingly be infertile or subfertile at the time of presentation to the GO. Our study reported that if FST was successful, 94.0% (141/150) of GOs stated they would then refer the patient to a RE for further evaluation and treatment. It is possible that by the GO providing timely information about treatment impacts on fertility and increasing the quality and quantity of FP discussions with patients, an increase in RE referrals prior to initiation of a FST would be observed. Early collaboration with an RE can complement oncological care by providing patients with data on baseline fertility potential, discussing how cancer treatment may affect future fertility, reviewing options for fertility preservation strategies, providing support and realistic expectations, and initiating fertility treatment, if desired. As a result, patients may be more informed and prepared to make decisions about whether they want to pursue FST or not, depending on their risk tolerance for likelihood of cancer recurrence versus the likelihood of pregnancy. By determining specific factors that influence FST practice patterns, it may be possible to improve access to FST for women with early Table 5 Predictors that influenced fertility sparing treatment consideration. Predictor Outcome 2
Comparison
N
100+ vs. b100 100+ vs. b100 Midwest vs. South
152 5.6 (1.7, 18.3) 152 3.3 (1.2, 9.3) 151 0.23 (0.57, 0.90) 111 10.2 (1.6, 66.7) 151 11.8 (2.0, 68.6)
Volume Volume2 Region
Prognosis Stage SES3
Setting
Treatment Urban vs. Rural
Setting
Pregnancy Urban + Suburban vs. Rural
1 2 3
Wald Chi-square Test. Number of reproductive aged women seen. SES, socioeconomic status.
OR (95% CI)
P-Value1 0.0049 0.0229 0.0344 0.0156 0.0060
gynecologic malignancies who desire fertility preservation. Despite some GOs seeing many RA women in their practice every year, their comfort level in FP counseling or collaboration with a RE may be low [17]. Regardless of one's practice volume, many GOs report a lack of formal training on how to discuss FP, a tendency for FP being low on their priority list, and not being aware of updated guidelines as barriers to counseling patients on FP [8,17,18]. Studies have shown that providers reportedly did not have the materials or resources they felt they needed to have a thorough conversation with their patients [17] but if they had updated, readily available institutional guidelines on FP, many would gladly implement this into their practice [18]. In addition, practice setting was another factor that influenced collaboration beliefs and RE referral frequency. Providers in large academic centers or teaching hospitals have more resources and access to REs than those within community settings or non-teaching institutions [19]. If providers were able to have a network of accessible and collaborative REs in the surrounding area and if this process was efficient and simplistic, it is likely more GOs would refer patients [19]. Due to the small number of rural providers in this study, no definitive conclusions can be made regarding geographic trends, however, this warrants further study. Providers wrote about barriers to access a RE in terms of geography, socioeconomics, financial burden, and patients who lack or have poor insurance coverage as significant concerns. Health care disparities are known to be present pertaining to gender, race, ethnicity, annual income, and education level [6,20]. Many studies have shown that Caucasian women, non-Hispanic women, and patients with a female GO provider were more likely to receive FP counseling [6,20,21]. It has also been shown that women with higher health literacy and education levels were more likely to bring up the topic of FP on their own to their GO [6]. Many providers assume patients may not be interested in FP because of perceived economic status, language barriers, health literacy, and cultural disparity [5,6,20,22,23]. Given that REs may not be accessible in all types of communities, an alternative solution is having oncologists disseminate information to patients pertaining to FP and FST through other mechanisms such as: navigators, educational tools, and
Please cite this article as: J.S. Shah, et al., Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members, Gynecol Oncol (2017), https://doi.org/10.1016/j.ygyno.2017.09.019
J.S. Shah et al. / Gynecologic Oncology xxx (2017) xxx–xxx
pamphlets. Other resources such as educational materials, decision aids, and organizational websites can be alternative tactics to educate patients about FP options [5,21,24]. Since patients typically recall b50% of information providers give to them verbally, some of these written tools of communication may be particularly advantageous. Tools can be tailored to meet the educational needs of specific populations, including those with low literacy. While there are multiple challenges in providing and coordinating care, there are some novel attempts to improve the care of women considering FST. The European Society of Gynecological Oncology is trying to implement a centralization of cancer centers that would allow certain locations to have trained providers in FP and FST [25]. This implementation would help create a registry of gynecology malignancies to allow for further research and create evidence-based guidelines that GOs can consult when giving FST recommendations to their patients [26]. As a result, patients may be offered more consistent, comprehensive medical management that could help them make more informed FST decisions. To our knowledge, this is one of the first studies that have examined the factors associated with FST of gynecologic malignancies. We have identified factors that may influence GO practice. Using the SGO membership allowed the inclusion of GOs with diverse backgrounds and demographics, which potentially helped capture practice patterns that are representative nationwide. Some limitations to our study include selection bias; GOs from academic practices were over-represented in our sample. It is possible that GOs interested in FP or FST may have been more likely to complete the survey. This may have decreased the generalizability of the result and caused an overestimation in responses. Despite capturing a relatively small sample size with a completion rate of 14.0%, this was comparable to other published survey studies of SGO providers [27–29]. While the survey design allowed for a self-report format that may have provided more desirable answers than actually capturing providers' true practice patterns, the anonymity of the survey likely decreased the risk of having social response bias [5]. Furthermore, the survey design allowed us to capture qualitative data that provided a deeper understanding of practice patterns than purely quantitative data would. In conclusion, while FST offers women the chance to pursue pregnancy after cancer, there are multiple factors that may influence if and when it is offered and whether consultation with a RE is considered or pursued in the management of these patients. It appears that the number of RA women seen by a GO, geographic location, and practice setting are potentially important variables that may influence current practice. While further research is needed to confirm these findings, the variability observed in practice suggests that educating GO's about the relevance and benefits of RE consultation might be a useful strategy to encourage collaboration. Our data also highlighted barriers to collaboration, especially access to RE care. Further research is needed to develop solutions to minimize these barriers that prevent optimization of oncologic and obstetrical outcomes.
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Conflict of interest statement There are no conflicts of interest or disclosures from any authors.
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Appendix A. Supplementary data [23]
Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.ygyno.2017.09.019.
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Contents lists available at ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members Jaimin S. Shah a,⁎, Rosa Guerra a, Diane C. Bodurka b, Charlotte C. Sun b, Gary B. Chisholm b, Terri L. Woodard b,c a b c
Department of Obstetrics and Gynecology, UT Health, The University of Texas at Houston, McGovern Medical School, United States Department of Gynecologic Oncology and Reproductive Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, United States Department of Obstetrics and Gynecology, Division of Reproductive Endocrinology and Infertility, Baylor College of Medicine, Houston, TX, United States
H I G H L I G H T S • • • •
Number of reproductive aged women seen may influence fertility sparing treatment. Geographic region and practice setting also influences fertility sparing treatment. Most of the gynecologic oncologists felt collaborating with a RE was important. Collaboration can help optimize treatment planning for women considering a FST.
a r t i c l e
i n f o
Article history: Received 21 July 2017 Received in revised form 15 September 2017 Accepted 18 September 2017 Available online xxxx Keywords: Fertility sparing treatment Fertility preservation Early gynecologic cancer Provider attitudes Practice patterns Health care disparities
a b s t r a c t Objectives. This study aims to examine practice patterns of gynecologic oncologists (GO) regarding fertilitysparing treatments (FST) for gynecology malignancies and explores attitudes toward collaboration with reproductive endocrinologists (RE). Methods. An anonymous 23-question survey was sent to 1087 GO with a 14.0% completion rate. Descriptive statistics, Fisher's exact test, and Chi-square tests were used for data analysis. Results. The majority of GOs offer FST for gynecologic malignancies. Providers seeing larger numbers of reproductive age women were more likely to consider cancer prognosis (p b 0.03) and cancer stage (p b 0.01) as key factors. Providers in the Midwestern US considered socioeconomic status more often when offering FST than those in the South (p b 0.04). Those practicing in urban settings were more likely to feel that collaborating with a RE prior to treatment could improve treatment planning for women considering FST (p b 0.02). Finally, providers in urban or suburban areas more often felt collaboration with a RE improves pregnancy outcomes in women who pursue FST (p b 0.01, p b 0.02) compared to rural practitioners. Conclusions. While FST offers women the chance to pursue pregnancy after cancer, there are minimal data on factors that influence whether FST is offered and if collaboration with a RE is sought in the management of these patients. The number of reproductive age women seen, geographic location, and practice setting are important variables that may influence current practice. Understanding these factors can help identify opportunities to improve oncologic and reproductive outcomes of this patient population. © 2017 Elsevier Inc. All rights reserved.
1. Introduction Advances in cancer treatment have increased the number of reproductive aged (RA) survivors, many of whom have questions and concerns about fertility and family planning. The American Society of Clinical Oncology (ASCO) recommends that providers discuss the risk of cancer-related infertility and refer patients who are interested in ⁎ Corresponding author at: 6431 Fannin St, Suite 3.214, Houston, TX 77030, United States. E-mail address: [email protected] (J.S. Shah).
fertility preservation (FP) to reproductive specialists early in the course of treatment planning [1]. While practice guidelines encourage fertility counseling, there are limited data on the quality of these discussions. In addition, the type of information provided to patients is not well characterized and referral rates to reproductive endocrinologist remain low. Fertility sparing treatments (FST) of early gynecologic cancers offer women the opportunity to preserve fertility potential while effectively treating their disease. However, as with other cancers, conservative management of gynecologic cancers may still negatively impact fertility and reproductive outcomes. For example, conservative surgical
https://doi.org/10.1016/j.ygyno.2017.09.019 0090-8258/© 2017 Elsevier Inc. All rights reserved.
Please cite this article as: J.S. Shah, et al., Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members, Gynecol Oncol (2017), https://doi.org/10.1016/j.ygyno.2017.09.019
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management of women with ovarian cancer may compromise ovarian reserve and women receiving trachelectomies for early stage cervical cancer may be at increased risk of cervical stenosis, preterm labor, and difficulties trying to conceive, even with assisted reproductive technology [2–4]. In addition, there may be comorbidities that warrant additional management, such as women with endometrial cancer who often present with anovulation and/or polycystic ovarian syndrome. Because conservative management of early gynecologic cancers is viewed as “fertility-sparing”, the need for comprehensive fertility counseling and evaluation by a reproductive endocrinologist (RE) is often overlooked. Gynecologic oncologists (GO) often perceive fertility counseling as a lower priority; lack of training in FP counseling, being pressed for time in clinic and unfamiliar with new national guidelines pertaining to FP are other reasons why infertility risks may be disregarded [5]. However, a RE can contribute to treatment planning by assessing a woman's baseline fertility status, making reasonable estimates of likelihood for successful pregnancy and live birth, and counseling patients on fertility treatments that may be needed in the future [4]. Lack of initiating the conversation about fertility goals at the time of diagnosis and not providing patients with quality discussions regarding FP may affect how patients choose treatment options [6,7]. The impact of potential cancer-related infertility has important implications for a patient's quality of life and survivorship experience. Discussions about fertility concerns prior to cancer treatment have been shown to decrease regret scores, whether a woman chooses to preserve fertility or not [8]. RA patients who receive a FST have been shown to have a reduced risk of regret about fertility goals [9]. Providing these patients options for fertility preservation has been proven to be worthwhile and safe [10]. FST in eligible patients has been shown to result in survival rates similar to conventional therapy [11–15]. The purpose of this study was to examine practice patterns of GOs with regard to FST of gynecologic malignancies and explore their attitudes toward collaboration with REs. The purpose of our study was to understand how FST practice tendencies varied amongst providers and examine their thoughts toward collaboration with REs. Understanding FST factors such as the size of the provider's practice, geographic region, and practice setting may identify opportunities to improve counseling and promote collaboration to optimize oncologic and reproductive outcomes in this patient population. 2. Materials and methods The study was approved by the Institutional Review Board at The University of Texas MD Anderson Cancer Center. An anonymous 23question survey was developed and tested by the study team (Appendix A). The survey was tested for face validity by administering it to ten gynecologic oncologists at our institution and eliciting their feedback about the clarity and appropriateness of the questions. The survey was reiteratively edited until the majority agreed on wording. Once finalized, it was sent by email to Full and Candidate members (N = 1087) of the Society of Gynecologic Oncology (SGO); the only inclusion criteria were that participants must be a GO and a member of SGO. A free text area was provided where participants could leave comments. The study data were collected and managed using REDCap™ (Research Electronic Data Capture) tools hosted at MD Anderson [16]. Descriptive statistics, Fisher's exact test, and Chi-square tests were used for data analysis. 3. Results 3.1. Demographics A total of 163 surveys were received. Of the surveys received, 152 were eligible for inclusion, yielding a completion rate of 14.0% (152/ 1087). Data analysis was restricted to surveys that were partially (75%
Table 1 Provider characteristics. Variable Sex (N = 146) Female Male Years in practice (N = 150) 0–10 11–20 21–30 31+ Type of practice (N = 152) Private Academic Private + Academic Military Other Geographic distribution (N = 152) Northeast Midwest South West Outside US
N
%
71 75
48.6% 51.4%
74 36 27 13
49.3% 24.0% 18.0% 8.7%
25 80 40 4 3
16.4% 52.6% 26.5% 2.6% 2.0%
41 30 51 29 1
27% 19.7% 33.6% 19.1% 0.7%
of the questions) or entirely completed. Table 1 shows the demographics of the GOs. The characteristics of the participants included a relatively even split of male and female providers, approximately 50% have been in practice for N10 years, providers seeing a wide range of RA women, and at least 75% solely work at or are affiliated with an academic institution. There was a broad but yet relatively even geographic distribution of GOs with the South reporting the highest percentage (33%); 27% of participants practice in the Northeast, 19.7% in the Midwest, 19.1% in the West, and 0.7% outside the United States. The majority of providers (70.2%) practiced in an urban setting while others were in a suburban (25.8%) or rural (4.0%) setting. Many of the GOs (84.2%, 128/152) are involved with training residents/fellows and 83.6% (107/ 128) reported that they incorporate lessons into their curricula about how to discuss fertility issues with patients diagnosed with a gynecologic cancer. 3.2. Assessment of fertility status, referral to a RE, and collaboration Sixty-eight percent (68%) of GOs reported they always assess fertility status prior to initiation of cancer treatment while 18% “often” and 8.7% “sometimes” perform an assessment (Table 2). The method of fertility assessment reported varied amongst providers. Many GOs (74.2%) preferred using a reproductive specialist for this assessment (Table 3). However, when referring patients to a RE for FP counseling prior to offering a FST, only 16% of the GOs reported they “always” do this while 44% stated they “often” and 26% “sometimes” refer their patients Table 2 How often do GOs assess fertility status? (N = 150). How often do GOs refer to or consult a RE for FP counseling prior to offering FST? (N = 150). Variable Assessment of fertility status Always Often Sometimes Rarely Never Referral to RE Always Often Sometimes Rarely Never
N
%
102 27 13 5 3
68.0% 18.0% 8.7% 3.3% 2.0%
24 66 39 19 2
16.0% 44.0% 26.0% 12.7% 1.3%
GO, gynecologic oncologist; RE, reproductive endocrinologist.
Please cite this article as: J.S. Shah, et al., Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members, Gynecol Oncol (2017), https://doi.org/10.1016/j.ygyno.2017.09.019
J.S. Shah et al. / Gynecologic Oncology xxx (2017) xxx–xxx Table 3 What tools do GOs use to assess or determine fertility status? (N = 151). What factors do GOs consider when offering FST? (N = 151). Variable Fertility status assessment method Never assess fertility Reproductive specialist TVUS FSH Estradiol (E2) Inhibin B AMH HSG or sonohysterogram Estimation based on age Other method Factors to consider for FST Patient age Number of current children Socioeconomic status History of infertility Cancer prognosis PMH Cancer stage Cancer histology Patient's wishes Other
N
%
3 115 33 54 30 11 39 6 79 8
2.0% 74.2% 21.3% 34.8% 19.4% 7.1% 25.2% 3.9% 51.0% 5.2%
142 86 19 80 140 74 133 120 149 1
94.0% 57.0% 12.6% 53.0% 92.7% 49.0% 88.1% 79.5% 98.7% 0.7%
Abbreviations: GO, gynecologic oncologist; TVUS, transvaginal ultrasound; FSH, follicle stimulating hormone; AMH, anti-mullerian hormone; HSG, hysterosalpingogram; PMH, past medical history.
(Table 2). Providers considered several indicators when assessing patients' fertility function; approximately 51% of providers considered the patient's age, 34.8% used serum follicle stimulating hormone level and 25.2% used serum anti-mullerian hormone level (Table 3). Many GOs strongly agreed (64.9%) or agreed (21.9%) that it is easy to refer gynecologic cancer patients to a RE (Table 4). The majority of providers (94%) felt that collaboration with a RE can improve the treatment planning for women considering FST. In addition, 83.4% of participants felt that working with a RE (strongly agree/agree) can improve pregnancy outcomes for patients that pursue conservative management (Table 4). 3.3. Fertility sparing treatment for gynecologic cancers Approximately 98.0% of providers (148/151) offer some form of FST for early gynecologic cancers. For providers who offered FSTs, Fig. 1 Table 4 Is it easy to refer patients to a RE? (N = 151). Collaborating with a RE can improve treatment planning for women considering FST (N = 150). Collaborating with a RE can improve pregnancy outcomes in women who pursue conservative management (N = 151). Variable Referral is easy Strongly agree Agree Neutral Disagree Strongly disagree Collaboration improves treatment planning Strongly agree Agree Neutral Disagree Strongly disagree Collaboration improves pregnancy outcomes Strongly agree Agree Neutral Disagree Strongly disagree RE, reproductive endocrinologist.
N
%
98 33 7 8 5
64.9% 21.9% 4.6% 5.3% 3.3%
101 40 8 1 0
67.3% 26.7% 5.3% 0.7% 0.0%
92 34 24 1 0
60.9% 22.5% 15.9% 0.7% 0.0%
3
shows breakdown of all the treatment types. Table 3 highlights the factors providers consider when offering FST to eligible patients. Most commonly, the patient's wishes (98.7%), patient age (94%), cancer prognosis (92.7%), cancer stage (88.1%), and histology (79.5%) are factors evaluated. Many providers (38.4%) reported that they have a maximum age after which they do not offer FST. While the survey results yielded a wide range as to what this age is, most providers (60.4%) reported an age cutoff between 46 and 50 years of age. Providers seeing larger numbers of RA women were more likely to consider cancer prognosis (p b 0.004) and cancer stage (p b 0.02) as critical factors when considering FST (Table 5). Providers in an urban setting were more likely to report that collaborating with a RE prior to treatment could improve treatment planning for women considering FST (p b 0.02). Compared to rural practitioners, providers in urban or suburban areas more often felt that collaborating with a RE improved pregnancy outcomes in women who pursue FST (p b 0.01, p b 0.02). There were 106, 38, and 6 providers in an urban, suburban, and rural practice setting, respectively. 3.4. Feedback from study participants Interestingly, several GOs completed the free text field (N = 16) within the survey and shared additional thoughts about the topic. Some themes that emerged included: 1) the challenges that many face in trying to coordinate care with REs; 2) the recognition of the importance in trying to coordinate medical care; and 3) the assumption fertility would not be affected by a FST. These themes are summarized below with supporting quotes. 1. The challenges that many face in trying to coordinate care with REs 1.1. “There isn't a RE at our hospital and patients have limited access to private practitioners in the area due to high rates of poverty in our patient population.” 1.2. “I think it would be great to refer all patients who desire fertility preservation to a RE. However, we have such limited resources in our rural community. We have no RE associated with the university and all private REs do not take insurance. It is very challenging to coordinate care with private REs when planning cancer care.” 1.3. “We have only private practice REs in our area. Costs for IVF, harvesting storing etc. are prohibitive for anyone in low middle class and below.” 2. The recognition of the importance in trying to coordinate medical care 2.1. “I think a referral to a RE for treatment is critical given the timing of ovulation induction and treatment for cancer.” 3. The assumption fertility would not be affected by a FST 3.1. “The vast majority of my fertility sparing surgeries are for young women without a history of infertility with early stage disease.” 4. Discussion The purpose of our study was to examine practice patterns of GOs regarding FST for gynecology malignancies and explores attitudes toward collaboration with REs. Within our study population, most of the GOs felt collaborating with a RE was important as it can help optimize treatment planning for women considering a FST and improve pregnancy outcomes. Many GOs utilized various methods to assess fertility status. The majority of participants stated they offer some FSTs in their practice; we concluded the size of the provider's practice, geographic region, and practice location were potentially key variables that influenced FST consideration (Table 5). The study indicated many providers refer their patients to a RE but this was not the case for everyone. The lack of RE referrals can be attributed to various barriers. Of note, the free response portion of the survey raised concerns for socioeconomic barriers to access a RE. Identifying and understanding the barriers to collaboration between GOs and REs are important first steps toward improving access to fertility counseling and treatment.
Please cite this article as: J.S. Shah, et al., Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members, Gynecol Oncol (2017), https://doi.org/10.1016/j.ygyno.2017.09.019
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Fig. 1. Fertility sparing treatments offered by providers (N = 148).
Our results showed many GOs perform various FSTs for early stage gynecologic cancers. This offers the opportunity for women who would otherwise be infertile from conventional treatment; however, it is not fail-proof. Some women may unknowingly be infertile or subfertile at the time of presentation to the GO. Our study reported that if FST was successful, 94.0% (141/150) of GOs stated they would then refer the patient to a RE for further evaluation and treatment. It is possible that by the GO providing timely information about treatment impacts on fertility and increasing the quality and quantity of FP discussions with patients, an increase in RE referrals prior to initiation of a FST would be observed. Early collaboration with an RE can complement oncological care by providing patients with data on baseline fertility potential, discussing how cancer treatment may affect future fertility, reviewing options for fertility preservation strategies, providing support and realistic expectations, and initiating fertility treatment, if desired. As a result, patients may be more informed and prepared to make decisions about whether they want to pursue FST or not, depending on their risk tolerance for likelihood of cancer recurrence versus the likelihood of pregnancy. By determining specific factors that influence FST practice patterns, it may be possible to improve access to FST for women with early Table 5 Predictors that influenced fertility sparing treatment consideration. Predictor Outcome 2
Comparison
N
100+ vs. b100 100+ vs. b100 Midwest vs. South
152 5.6 (1.7, 18.3) 152 3.3 (1.2, 9.3) 151 0.23 (0.57, 0.90) 111 10.2 (1.6, 66.7) 151 11.8 (2.0, 68.6)
Volume Volume2 Region
Prognosis Stage SES3
Setting
Treatment Urban vs. Rural
Setting
Pregnancy Urban + Suburban vs. Rural
1 2 3
Wald Chi-square Test. Number of reproductive aged women seen. SES, socioeconomic status.
OR (95% CI)
P-Value1 0.0049 0.0229 0.0344 0.0156 0.0060
gynecologic malignancies who desire fertility preservation. Despite some GOs seeing many RA women in their practice every year, their comfort level in FP counseling or collaboration with a RE may be low [17]. Regardless of one's practice volume, many GOs report a lack of formal training on how to discuss FP, a tendency for FP being low on their priority list, and not being aware of updated guidelines as barriers to counseling patients on FP [8,17,18]. Studies have shown that providers reportedly did not have the materials or resources they felt they needed to have a thorough conversation with their patients [17] but if they had updated, readily available institutional guidelines on FP, many would gladly implement this into their practice [18]. In addition, practice setting was another factor that influenced collaboration beliefs and RE referral frequency. Providers in large academic centers or teaching hospitals have more resources and access to REs than those within community settings or non-teaching institutions [19]. If providers were able to have a network of accessible and collaborative REs in the surrounding area and if this process was efficient and simplistic, it is likely more GOs would refer patients [19]. Due to the small number of rural providers in this study, no definitive conclusions can be made regarding geographic trends, however, this warrants further study. Providers wrote about barriers to access a RE in terms of geography, socioeconomics, financial burden, and patients who lack or have poor insurance coverage as significant concerns. Health care disparities are known to be present pertaining to gender, race, ethnicity, annual income, and education level [6,20]. Many studies have shown that Caucasian women, non-Hispanic women, and patients with a female GO provider were more likely to receive FP counseling [6,20,21]. It has also been shown that women with higher health literacy and education levels were more likely to bring up the topic of FP on their own to their GO [6]. Many providers assume patients may not be interested in FP because of perceived economic status, language barriers, health literacy, and cultural disparity [5,6,20,22,23]. Given that REs may not be accessible in all types of communities, an alternative solution is having oncologists disseminate information to patients pertaining to FP and FST through other mechanisms such as: navigators, educational tools, and
Please cite this article as: J.S. Shah, et al., Factors influencing fertility-sparing treatment for gynecologic malignancies: A survey of Society of Gynecologic Oncology members, Gynecol Oncol (2017), https://doi.org/10.1016/j.ygyno.2017.09.019
J.S. Shah et al. / Gynecologic Oncology xxx (2017) xxx–xxx
pamphlets. Other resources such as educational materials, decision aids, and organizational websites can be alternative tactics to educate patients about FP options [5,21,24]. Since patients typically recall b50% of information providers give to them verbally, some of these written tools of communication may be particularly advantageous. Tools can be tailored to meet the educational needs of specific populations, including those with low literacy. While there are multiple challenges in providing and coordinating care, there are some novel attempts to improve the care of women considering FST. The European Society of Gynecological Oncology is trying to implement a centralization of cancer centers that would allow certain locations to have trained providers in FP and FST [25]. This implementation would help create a registry of gynecology malignancies to allow for further research and create evidence-based guidelines that GOs can consult when giving FST recommendations to their patients [26]. As a result, patients may be offered more consistent, comprehensive medical management that could help them make more informed FST decisions. To our knowledge, this is one of the first studies that have examined the factors associated with FST of gynecologic malignancies. We have identified factors that may influence GO practice. Using the SGO membership allowed the inclusion of GOs with diverse backgrounds and demographics, which potentially helped capture practice patterns that are representative nationwide. Some limitations to our study include selection bias; GOs from academic practices were over-represented in our sample. It is possible that GOs interested in FP or FST may have been more likely to complete the survey. This may have decreased the generalizability of the result and caused an overestimation in responses. Despite capturing a relatively small sample size with a completion rate of 14.0%, this was comparable to other published survey studies of SGO providers [27–29]. While the survey design allowed for a self-report format that may have provided more desirable answers than actually capturing providers' true practice patterns, the anonymity of the survey likely decreased the risk of having social response bias [5]. Furthermore, the survey design allowed us to capture qualitative data that provided a deeper understanding of practice patterns than purely quantitative data would. In conclusion, while FST offers women the chance to pursue pregnancy after cancer, there are multiple factors that may influence if and when it is offered and whether consultation with a RE is considered or pursued in the management of these patients. It appears that the number of RA women seen by a GO, geographic location, and practice setting are potentially important variables that may influence current practice. While further research is needed to confirm these findings, the variability observed in practice suggests that educating GO's about the relevance and benefits of RE consultation might be a useful strategy to encourage collaboration. Our data also highlighted barriers to collaboration, especially access to RE care. Further research is needed to develop solutions to minimize these barriers that prevent optimization of oncologic and obstetrical outcomes.
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Conflict of interest statement There are no conflicts of interest or disclosures from any authors.
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Appendix A. Supplementary data [23]
Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.ygyno.2017.09.019.
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