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L. Yu and others, Knowledge, attitudes, and intentions toward fertility awareness and oocyte cryopreservation among obstetrics and gynecology resident physicians, Human Reproduction, Volume 31, Issue 2, February 2016, Pages 403–411, https://doi.org/10.1093/humrep/dev308
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Abstract
What knowledge, attitudes and intentions do US obstetrics and gynecology (OB/GYN) residents have toward discussing age-related fertility decline and oocyte cryopreservation with their patients?
Most OB/GYN residents believe that age-related fertility decline, but not oocyte cryopreservation, should be discussed during well-woman annual exams; furthermore, nearly half of residents overestimated the age at which female fertility markedly declines.
Oocyte cryopreservation can be utilized to preserve fertility potential. Currently, no studies of US OB/GYN residents exist that question their knowledge, attitudes, and intentions toward discussing age-related fertility decline and oocyte cryopreservation with patients.
A cross-sectional online survey was conducted during the fall of 2014 among residents in American Council for Graduate (ACOG) Medical Education-approved OB/GYN residency programs. Program directors were emailed via the ACOG Council on Resident Education in Obstetrics and Gynecology server listing and asked to solicit resident participation.
Participants included 238 residents evenly distributed between post-graduate years 1–4 with varied post-residency plans; 90% of residents were women and 75% were 26–30 years old. The survey was divided into three sections: demographics, fertility awareness, and attitudes toward discussing fertility preservation options with patients. Descriptive and inferential statistics were conducted.
A strong majority of residents (83%) believed an OB/GYN should initiate discussions about age-related fertility decline with patients (mean patient age 31.8), and 73% percent believed these discussions should be part of an annual exam. One third of residents overestimated the age at which there is a slight decline in female fertility, while nearly half of residents overestimated the age at which female fertility markedly declines. Over three-quarters of residents (78.4%) also overestimated the likelihood of success using assisted reproductive treatments (ARTs). Residents were likely to support oocyte cryopreservation in cancer patients irrespective of the woman's age, but much less likely to support elective oocyte cryopreservation. For elective oocyte cryopreservation, 40% believed OB/GYNs should initiate discussions with patients (mean age 31.1), while only 20% believed this topic should be part of an annual exam.
Because the study invitation was sent through US OB/GYN residency program directors rather than directly to residents, it is possible that some residents did not receive the invitation to participate. This limits the generalizability of the findings.
Within the USA, there appears to be a critical need for improved education on fertility decline in OB/GYN residency programs. To promote informed reproductive decision-making among patients, efforts should be made to help OB/GYNs provide comprehensive fertility education to all women, while also respecting patient choices.
None.
Introduction
Studies assessing the relationship between female fertility and aging have utilized a variety of approaches, including observational data on study populations, statistical modeling, and biochemical assays (Howe et al., 1985; Menken and Larken, 1986; Dunson et al., 2002; Broekmans et al., 2006; Eijkemans et al., 2014). Although the specified age of onset of fertility decline varies among studies, there is widespread agreement that female fertility begins to decline by a woman's early 30s, and that the rate of decline markedly increases at age 37 and thereafter (Howe et al., 1985; Dunson et al., 2002; Te Velde and Pearson, 2002; ASRM, 2013; ACOG, 2014). However, a large number of international studies have consistently found that people who are likely to delay childbearing underestimate the impact of age on fertility as a potential risk factor for involuntary childlessness (Lampic et al., 2006; Tyden et al., 2006; Bretherick et al., 2010; Hashiloni-Dolev et al., 2011; Virtala et al., 2011; Peterson et al., 2012; Wyndham et al., 2012; Chan et al., 2015). These studies also found that participants overestimate the effectiveness of assisted reproductive treatments (ARTs) to overcome age-related infertility (Leridon, 2004; Ferraretti et al., 2013; Center for Disease Control & Prevention, 2014). It is therefore particularly important that women of childbearing age have access to accurate information regarding the impact of age on fertility, as well as the success rates of both ARTs and fertility preservation, so that they are empowered to make informed reproductive decisions.
Most women who want children report that their health care provider is the preferred and most reliable source of information about reproductive health, rather than other sources such as the media, peers, and the Internet (Peterson et al., 2012; Wyndham et al., 2012; Hodes-Wertz et al., 2013; Lundsberg et al., 2014; Azhar et al., 2015). However, women typically wait to seek information from their health care providers on fertility and conception until they are older, when their fertility may already be declining or compromised (Lundsberg et al., 2014). Furthermore, not all health care providers are familiar with or comfortable counseling their patients about age-related fertility decline. This combination of patient and physician factors may lead to a relatively low percentage of patients who actually receive reproductive health-related information directly from their health care providers (Lundsberg et al., 2014). Primary care physicians, and to a greater extent obstetric and gynecology (OB/GYN) specialists in hospitals and general practice, have an important role to play in educating patients about the relationship between age and fertility. They are also in a position to discuss the implications of oocyte cryopreservation such as cost, risk, and the estimated number of eggs needed to give women a reasonable chance of having a baby as a result (Dondorp et al., 2012). For example, doctors can present the possibility of freezing one's eggs for future use at a time of maximum reproductive potential. Although oocyte cryopreservation is clearly gaining acceptance for use in patients diagnosed with cancer (Mertes and Pennings, 2011; Noyes et al., 2011), considerable controversy exists regarding the use of oocyte cryopreservation for non-medical reasons (Stoop et al., 2011, 2014). In October 2012, the American Society for Reproductive Medicine (ASRM) removed the experimental label from oocyte cryopreservation for medical reasons, given that it has similar obstetric and perinatal outcomes compared with procedures using fresh oocytes (Oktay et al., 2006; Grifo and Noyes, 2010; Herrero et al., 2011; Rienzi et al., 2012; ASRM, 2013; Levi Setti et al., 2013; Cobo et al., 2014). However, because of the newness of the procedure, total success rates after long-term freezing remain unclear making it is difficult to counsel women in either group on the minimum number of oocytes required to have a reasonable chance of birth after oocyte cryopreservation.
To provide a more neutral and accurate description of this technology, we will refer to oocyte cryopreservation for non-medical reasons as ‘elective oocyte cryopreservation’ (EOC). Although EOC has the potential to alter the landscape of female fertility decision-making, it is of paramount importance to assess whether OB/GYNs—considered the first-line providers of comprehensive reproductive health education—feel that they have a responsibility to educate patients about fertility decline and EOC, and whether they have the necessary education to perform this function. As fertility preservation technologies become more available in the USA, OB/GYN awareness of these technologies may have a major impact on whether fertility decline is discussed, and if EOC options are presented to women during their routine gynecologic exams.
OB/GYN residents, currently in post-graduate training, may be the most likely physicians to integrate new evidence-based medicine and technologies into their practice. Thus, this study was designed to examine the knowledge, attitudes, and intentions of US OB/GYN residents in providing patients with information on age-related fertility decline and oocyte cryopreservation. Our study aims to assess OB/GYN residents' knowledge and beliefs regarding age-related fertility decline and the use and availability of oocyte cryopreservation. It is based on three key research questions: (i) Do OB/GYN residents believe that it is the role of OB/GYNs to initiate discussions about age-related fertility decline and oocyte cryopreservation with their patients, and if so, at what ages and how frequently? (ii) Do OB/GYN residents possess accurate knowledge regarding the relationship between female fertility decline and age, as well as the success rates of ARTs? And (iii) Do OB/GYN residents differ in their attitudes toward oocyte cryopreservation for patients diagnosed with cancer or other medical conditions versus EOC? To our knowledge, this is the first study to examine these issues in a sample of US OB/GYN resident physicians.
Materials and Methods
The study used a cross-sectional design to examine the knowledge, attitudes, and intentions of US OB/GYN residents. The study was reviewed and approved by the Yale University Human Investigation Committee (HIC#1409014546). All 232 residency program directors listed on the website of the American College of Obstetrician Gynecologists (ACOG) were sent a hyperlink to an online survey and asked to forward this link to their residents. Resident participants had an opportunity to enter a raffle for one of six $50 incentives at the completion of the survey. Between September and October 2014, an initial invitation email and two reminder emails were sent to each program director with a request to forward the invitation to all residents.
Instrument design
The survey was based on existing instruments measuring fertility awareness (Lampic et al., 2006), and the clinical experiences of the study authors in the fields of obstetrics and gynecology, reproductive endocrinology, psychology, and anthropology. The instrument was pre-tested on a small group of graduate students for clarity and wording, and was refined through discussion with this focus group as well as a literature review examining the published research on fertility awareness, preconception counseling, and oocyte cryopreservation. The survey included demographic background questions and questions about residents' attitudes towards discussing age-related fertility decline and oocyte cryopreservation. Questions took the form of ‘yes/no’ responses (e.g. ‘Should an OB/GYN initiate discussions with patients regarding childbearing intentions?’), and open-ended numerical questions (e.g. ‘If you answered YES to [the previous question], at what age would you initiate this discussion with patients?’). Participants were also asked whether these conversations were appropriate for annual well-woman exams, and data were collected regarding the reasons for or against discussing childbearing intentions at well-woman exams. Options for open-ended qualitative responses using an ‘other’ category were also given to more thoroughly assess residents' attitudes. As in previous studies of fertility awareness, knowledge-based questions included age of ‘slight’ versus ‘marked’ decline in a woman's ability to become pregnant, and the average success rate for couples undergoing a single round of in vitro fertilization (IVF) (Lampic et al., 2006; Peterson et al., 2012; Chan et al., 2015). Participants were asked to assess their own familiarity with oocyte cryopreservation, and whether oocyte cryopreservation was offered at their training institution. They were also asked whether they would initiate discussions of oocyte cryopreservation with their patients, at what ages they would initiate such discussions, and whether such discussions should be part of a well-woman annual exam. Finally, residents were asked how likely they would be to discuss oocyte cryopreservation and support insurance coverage for the technology in different clinical situations (e.g. ‘A 25-year-old with cancer’) or for non-medical reasons (e.g. ‘A 25-year-old who wants a career first’).
Statistical analysis
Data from the online survey were analyzed using SPSS (Version 21). Characteristics of study participants were first analyzed with descriptive statistics. Next, descriptive analyses regarding issues related to fertility awareness, preconception planning, and oocyte cryopreservation were conducted. OB/GYN residents' knowledge of fertility issues was then examined with analyses of variance (ANOVAs), which tested whether knowledge differed based on participants' year in residency. Gender differences were not examined due to the small sample size of male residents.
Results
Sample characteristics
Two hundred thirty nine residents participated in the online survey, or approximately 5% of all OB/GYN residents in the United States (based on 5021 total OB/GYN residents reported by the Accreditation Council for Graduate Medical Education) (ACGME, 2014). As shown in Table I, approximately 75% of residents were between the ages of 26 and 30. In addition, a significantly higher percentage of respondents were women (90.3% versus. 81%, z = 3.72, P < 0.0001) and white (71.7% versus 54%, z = 5.46, P < 0.0001) when compared with the overall population of residents (ACGME, 2014). Respondents were nearly equally split across year of residency and slightly more hailed from the northeastern and southern regions of the USA compared with the western and mid-western regions. Half of respondents (50.2%) intended to pursue general practice in the future.
Characteristics of the sample.
| Characteristic . | N . | % . |
|---|---|---|
| Age | ||
| 18–25 | 7 | 2.9 |
| 26–30 | 179 | 74.9 |
| 31–35 | 51 | 21.3 |
| 36–40 | 2 | 0.8 |
| 41–45 | 0 | 0 |
| Gender | ||
| Female | 214 | 90.3 |
| Male | 23 | 9.7 |
| Other | 0 | 0 |
| Racial/ethnic background | ||
| White/Caucasian | 170 | 71.7 |
| Black/African American | 16 | 6.8 |
| Asian and Pacific Islander | 27 | 11.4 |
| Hispanic/Latino | 12 | 5.1 |
| Middle Eastern | 3 | 1.3 |
| Multiracial | 6 | 2.5 |
| Other | 3 | 1.3 |
| Post-graduate year | ||
| 1 | 62 | 25.9 |
| 2 | 66 | 27.6 |
| 3 | 53 | 22.2 |
| 4 | 57 | 23.8 |
| Other | 1 | 0.4 |
| Geographic location | ||
| West | 35 | 14.8 |
| Midwest | 45 | 19 |
| Northeast | 90 | 38 |
| South | 59 | 24.9 |
| Other | 8 | 3.4 |
| Professional plans | ||
| Maternal fetal medicine | 18 | 7.5 |
| Reproductive endocrinology and infertility | 18 | 7.5 |
| Urogynecology | 17 | 7.1 |
| Gynecologic oncology | 26 | 10.9 |
| Family planning | 12 | 5 |
| Other fellowship | 10 | 4.2 |
| General practice | 120 | 50.2 |
| Other | 18 | 7.5 |
| Characteristic . | N . | % . |
|---|---|---|
| Age | ||
| 18–25 | 7 | 2.9 |
| 26–30 | 179 | 74.9 |
| 31–35 | 51 | 21.3 |
| 36–40 | 2 | 0.8 |
| 41–45 | 0 | 0 |
| Gender | ||
| Female | 214 | 90.3 |
| Male | 23 | 9.7 |
| Other | 0 | 0 |
| Racial/ethnic background | ||
| White/Caucasian | 170 | 71.7 |
| Black/African American | 16 | 6.8 |
| Asian and Pacific Islander | 27 | 11.4 |
| Hispanic/Latino | 12 | 5.1 |
| Middle Eastern | 3 | 1.3 |
| Multiracial | 6 | 2.5 |
| Other | 3 | 1.3 |
| Post-graduate year | ||
| 1 | 62 | 25.9 |
| 2 | 66 | 27.6 |
| 3 | 53 | 22.2 |
| 4 | 57 | 23.8 |
| Other | 1 | 0.4 |
| Geographic location | ||
| West | 35 | 14.8 |
| Midwest | 45 | 19 |
| Northeast | 90 | 38 |
| South | 59 | 24.9 |
| Other | 8 | 3.4 |
| Professional plans | ||
| Maternal fetal medicine | 18 | 7.5 |
| Reproductive endocrinology and infertility | 18 | 7.5 |
| Urogynecology | 17 | 7.1 |
| Gynecologic oncology | 26 | 10.9 |
| Family planning | 12 | 5 |
| Other fellowship | 10 | 4.2 |
| General practice | 120 | 50.2 |
| Other | 18 | 7.5 |
Characteristics of the sample.
| Characteristic . | N . | % . |
|---|---|---|
| Age | ||
| 18–25 | 7 | 2.9 |
| 26–30 | 179 | 74.9 |
| 31–35 | 51 | 21.3 |
| 36–40 | 2 | 0.8 |
| 41–45 | 0 | 0 |
| Gender | ||
| Female | 214 | 90.3 |
| Male | 23 | 9.7 |
| Other | 0 | 0 |
| Racial/ethnic background | ||
| White/Caucasian | 170 | 71.7 |
| Black/African American | 16 | 6.8 |
| Asian and Pacific Islander | 27 | 11.4 |
| Hispanic/Latino | 12 | 5.1 |
| Middle Eastern | 3 | 1.3 |
| Multiracial | 6 | 2.5 |
| Other | 3 | 1.3 |
| Post-graduate year | ||
| 1 | 62 | 25.9 |
| 2 | 66 | 27.6 |
| 3 | 53 | 22.2 |
| 4 | 57 | 23.8 |
| Other | 1 | 0.4 |
| Geographic location | ||
| West | 35 | 14.8 |
| Midwest | 45 | 19 |
| Northeast | 90 | 38 |
| South | 59 | 24.9 |
| Other | 8 | 3.4 |
| Professional plans | ||
| Maternal fetal medicine | 18 | 7.5 |
| Reproductive endocrinology and infertility | 18 | 7.5 |
| Urogynecology | 17 | 7.1 |
| Gynecologic oncology | 26 | 10.9 |
| Family planning | 12 | 5 |
| Other fellowship | 10 | 4.2 |
| General practice | 120 | 50.2 |
| Other | 18 | 7.5 |
| Characteristic . | N . | % . |
|---|---|---|
| Age | ||
| 18–25 | 7 | 2.9 |
| 26–30 | 179 | 74.9 |
| 31–35 | 51 | 21.3 |
| 36–40 | 2 | 0.8 |
| 41–45 | 0 | 0 |
| Gender | ||
| Female | 214 | 90.3 |
| Male | 23 | 9.7 |
| Other | 0 | 0 |
| Racial/ethnic background | ||
| White/Caucasian | 170 | 71.7 |
| Black/African American | 16 | 6.8 |
| Asian and Pacific Islander | 27 | 11.4 |
| Hispanic/Latino | 12 | 5.1 |
| Middle Eastern | 3 | 1.3 |
| Multiracial | 6 | 2.5 |
| Other | 3 | 1.3 |
| Post-graduate year | ||
| 1 | 62 | 25.9 |
| 2 | 66 | 27.6 |
| 3 | 53 | 22.2 |
| 4 | 57 | 23.8 |
| Other | 1 | 0.4 |
| Geographic location | ||
| West | 35 | 14.8 |
| Midwest | 45 | 19 |
| Northeast | 90 | 38 |
| South | 59 | 24.9 |
| Other | 8 | 3.4 |
| Professional plans | ||
| Maternal fetal medicine | 18 | 7.5 |
| Reproductive endocrinology and infertility | 18 | 7.5 |
| Urogynecology | 17 | 7.1 |
| Gynecologic oncology | 26 | 10.9 |
| Family planning | 12 | 5 |
| Other fellowship | 10 | 4.2 |
| General practice | 120 | 50.2 |
| Other | 18 | 7.5 |
Attitudes toward discussing preconception planning and fertility
Findings regarding residents' tendencies to discuss preconception planning and fertility with patients are shown in Table II. Nearly all respondents (91.7%) indicated that OB/GYNs should initiate discussion with patients about childbearing intentions at a patient's mean age of 20.8 (SD = 5.4). A majority of respondents also thought that OB/GYNs should initiate discussions about age-related fertility decline (82.9%), although beginning at a patients' mean age of 31.8 (SD = 3.5). Furthermore, 72.4% thought that discussing age-related fertility decline should be part of a well-woman annual exam with an OB/GYN, as this would help to educate women about making informed reproductive decisions. Of the 27.6% of residents who did not think that discussing age-related fertility decline should be part of a well-woman annual exam, 53% explained that an annual exam was too frequent, 53% did not want to be perceived as pushing childbearing on their patients, and 40% reported that such discussions might lead to emotional distress in patients.
OB/GYN residents' attitudes toward discussing preconception planning and fertility.
| Item . | . | N . | % . |
|---|---|---|---|
| Should an OB/GYN initiate discussions with patients about their potential childbearing intentions? | |||
| Yes | 198 | 91.7 | |
| No | 18 | 8.3 | |
| Should an OB/GYN initiate discussions about age-related fertility decline with patients? | |||
| Yes | 180 | 82.9 | |
| No | 37 | 17.1 | |
| Should discussing the natural decline in fertility with age be part of a well-woman annual exam with a gynecologist? | |||
| Yes | 157 | 72.4 | |
| No | 60 | 27.6 | |
| Reasons for yes | Educating women about this helps women make informed reproductive decisions | 141 | 89.8 |
| I want to provide comprehensive health education to my patients | 127 | 80.9 | |
| Women should be aware of the correct relationship between fertility and age | 112 | 71.3 | |
| I can help dispel many of the myths in society/media regarding fertility and age | 85 | 54.1 | |
| Other | 0 | 0 | |
| Reasons for no | Bringing this issue up annually is too frequent, but I am not opposed to discussing this issue with patients every three to four years | 32 | 53.3 |
| I don't want to be perceived as pushing childbearing on patients | 32 | 53.3 | |
| Bringing up this issue annually may lead to emotional distress in my patients | 24 | 40 | |
| I want to be able to fully respect patient choices | 23 | 38.3 | |
| I don't have enough time | 7 | 11.7 | |
| Other | 7 | 11.7 | |
| It is not my primary responsibility | 2 | 3.3 | |
| Item . | . | N . | % . |
|---|---|---|---|
| Should an OB/GYN initiate discussions with patients about their potential childbearing intentions? | |||
| Yes | 198 | 91.7 | |
| No | 18 | 8.3 | |
| Should an OB/GYN initiate discussions about age-related fertility decline with patients? | |||
| Yes | 180 | 82.9 | |
| No | 37 | 17.1 | |
| Should discussing the natural decline in fertility with age be part of a well-woman annual exam with a gynecologist? | |||
| Yes | 157 | 72.4 | |
| No | 60 | 27.6 | |
| Reasons for yes | Educating women about this helps women make informed reproductive decisions | 141 | 89.8 |
| I want to provide comprehensive health education to my patients | 127 | 80.9 | |
| Women should be aware of the correct relationship between fertility and age | 112 | 71.3 | |
| I can help dispel many of the myths in society/media regarding fertility and age | 85 | 54.1 | |
| Other | 0 | 0 | |
| Reasons for no | Bringing this issue up annually is too frequent, but I am not opposed to discussing this issue with patients every three to four years | 32 | 53.3 |
| I don't want to be perceived as pushing childbearing on patients | 32 | 53.3 | |
| Bringing up this issue annually may lead to emotional distress in my patients | 24 | 40 | |
| I want to be able to fully respect patient choices | 23 | 38.3 | |
| I don't have enough time | 7 | 11.7 | |
| Other | 7 | 11.7 | |
| It is not my primary responsibility | 2 | 3.3 | |
OB/GYN residents' attitudes toward discussing preconception planning and fertility.
| Item . | . | N . | % . |
|---|---|---|---|
| Should an OB/GYN initiate discussions with patients about their potential childbearing intentions? | |||
| Yes | 198 | 91.7 | |
| No | 18 | 8.3 | |
| Should an OB/GYN initiate discussions about age-related fertility decline with patients? | |||
| Yes | 180 | 82.9 | |
| No | 37 | 17.1 | |
| Should discussing the natural decline in fertility with age be part of a well-woman annual exam with a gynecologist? | |||
| Yes | 157 | 72.4 | |
| No | 60 | 27.6 | |
| Reasons for yes | Educating women about this helps women make informed reproductive decisions | 141 | 89.8 |
| I want to provide comprehensive health education to my patients | 127 | 80.9 | |
| Women should be aware of the correct relationship between fertility and age | 112 | 71.3 | |
| I can help dispel many of the myths in society/media regarding fertility and age | 85 | 54.1 | |
| Other | 0 | 0 | |
| Reasons for no | Bringing this issue up annually is too frequent, but I am not opposed to discussing this issue with patients every three to four years | 32 | 53.3 |
| I don't want to be perceived as pushing childbearing on patients | 32 | 53.3 | |
| Bringing up this issue annually may lead to emotional distress in my patients | 24 | 40 | |
| I want to be able to fully respect patient choices | 23 | 38.3 | |
| I don't have enough time | 7 | 11.7 | |
| Other | 7 | 11.7 | |
| It is not my primary responsibility | 2 | 3.3 | |
| Item . | . | N . | % . |
|---|---|---|---|
| Should an OB/GYN initiate discussions with patients about their potential childbearing intentions? | |||
| Yes | 198 | 91.7 | |
| No | 18 | 8.3 | |
| Should an OB/GYN initiate discussions about age-related fertility decline with patients? | |||
| Yes | 180 | 82.9 | |
| No | 37 | 17.1 | |
| Should discussing the natural decline in fertility with age be part of a well-woman annual exam with a gynecologist? | |||
| Yes | 157 | 72.4 | |
| No | 60 | 27.6 | |
| Reasons for yes | Educating women about this helps women make informed reproductive decisions | 141 | 89.8 |
| I want to provide comprehensive health education to my patients | 127 | 80.9 | |
| Women should be aware of the correct relationship between fertility and age | 112 | 71.3 | |
| I can help dispel many of the myths in society/media regarding fertility and age | 85 | 54.1 | |
| Other | 0 | 0 | |
| Reasons for no | Bringing this issue up annually is too frequent, but I am not opposed to discussing this issue with patients every three to four years | 32 | 53.3 |
| I don't want to be perceived as pushing childbearing on patients | 32 | 53.3 | |
| Bringing up this issue annually may lead to emotional distress in my patients | 24 | 40 | |
| I want to be able to fully respect patient choices | 23 | 38.3 | |
| I don't have enough time | 7 | 11.7 | |
| Other | 7 | 11.7 | |
| It is not my primary responsibility | 2 | 3.3 | |
Awareness of fertility issues
Residents' knowledge about the ages when female fertility declines and their estimate of chance of success with IVF are shown in Table III. One third overestimated the age when fertility starts to decline and almost half of residents (46.5%) overestimated when fertility declines markedly. Estimates of slight and marked decline in fertility did not differ based on year in residency.
Obstetrics and gynecology (OB/GYN) residents' awareness of fertility issues.
| Fertility issue . | All residents (N = 217) . | 1st year residents (N = 55) . | 2nd year residents (N = 58) . | 3rd year residents (N = 51) . | 4th year residents (N = 53) . | P . |
|---|---|---|---|---|---|---|
| At what age is there a slight decrease in women's ability to become pregnant? | 31.67 (3.10) | 31.55 (3.47) | 31.43 (2.74) | 31.37 (2.95) | 32.36 (3.21) | 0.32 |
| 15–24 | 0.9% | 1.8% | 0% | 0% | 1.9% | |
| 25–29* | 9.7% | 9.1% | 10.3% | 15.7% | 3.8% | |
| 30–34* | 53.0% | 50.9% | 60.3% | 54.9% | 45.3% | |
| 35–59 | 33.1% | 38.2% | 29.3% | 29.4% | 49.1% | |
| At what age is there a marked decrease in women's ability to become pregnant? | 37.58 (2.53) | 37.95 (2.54) | 37.17 (2.62) | 37.20 (2.51) | 38.00 (2.39) | 0.15 |
| 25–34 | 0% | 0% | 0% | 0% | 0% | |
| 35–39* | 52.5% | 47.3% | 60.3% | 58.8% | 43.4% | |
| 40–44 | 46.5% | 50.9% | 37.9% | 41.2% | 56.6% | |
| 45–59 | 0.9% | 1.8% | 1.7% | 0% | 0% | |
| What is the overall chance, on average, that a couple who undergoes treatment with in vitro fertilization will have a child after one treatment? | 42.30 (18.37) | 41.20 (19.52) | 45.02 (18.75) | 42.02 (18.61) | 40.75 (16.62) | 0.61 |
| 0–19% | 5.1% | 7.3% | 1.7% | 5.9% | 5.7% | |
| 20–29%* | 16.6% | 16.4% | 17.2% | 13.7% | 18.9% | |
| 30–39% | 24.0% | 29.1% | 19.0% | 29.4% | 18.9% | |
| 40–100% | 54.4% | 47.3% | 62.1% | 51.0% | 56.6% |
| Fertility issue . | All residents (N = 217) . | 1st year residents (N = 55) . | 2nd year residents (N = 58) . | 3rd year residents (N = 51) . | 4th year residents (N = 53) . | P . |
|---|---|---|---|---|---|---|
| At what age is there a slight decrease in women's ability to become pregnant? | 31.67 (3.10) | 31.55 (3.47) | 31.43 (2.74) | 31.37 (2.95) | 32.36 (3.21) | 0.32 |
| 15–24 | 0.9% | 1.8% | 0% | 0% | 1.9% | |
| 25–29* | 9.7% | 9.1% | 10.3% | 15.7% | 3.8% | |
| 30–34* | 53.0% | 50.9% | 60.3% | 54.9% | 45.3% | |
| 35–59 | 33.1% | 38.2% | 29.3% | 29.4% | 49.1% | |
| At what age is there a marked decrease in women's ability to become pregnant? | 37.58 (2.53) | 37.95 (2.54) | 37.17 (2.62) | 37.20 (2.51) | 38.00 (2.39) | 0.15 |
| 25–34 | 0% | 0% | 0% | 0% | 0% | |
| 35–39* | 52.5% | 47.3% | 60.3% | 58.8% | 43.4% | |
| 40–44 | 46.5% | 50.9% | 37.9% | 41.2% | 56.6% | |
| 45–59 | 0.9% | 1.8% | 1.7% | 0% | 0% | |
| What is the overall chance, on average, that a couple who undergoes treatment with in vitro fertilization will have a child after one treatment? | 42.30 (18.37) | 41.20 (19.52) | 45.02 (18.75) | 42.02 (18.61) | 40.75 (16.62) | 0.61 |
| 0–19% | 5.1% | 7.3% | 1.7% | 5.9% | 5.7% | |
| 20–29%* | 16.6% | 16.4% | 17.2% | 13.7% | 18.9% | |
| 30–39% | 24.0% | 29.1% | 19.0% | 29.4% | 18.9% | |
| 40–100% | 54.4% | 47.3% | 62.1% | 51.0% | 56.6% |
*Asterisk indicates the correct category based on published literature. For the slight decline in fertility, literature suggests this decline can begin in the late 20s to early 30s. Note. Means and standard deviations are presented in the first row for each fertility issue; percentages are presented in subsequent rows. Significance values come from one-way analyses of variance testing for differences based on year in residency.
Obstetrics and gynecology (OB/GYN) residents' awareness of fertility issues.
| Fertility issue . | All residents (N = 217) . | 1st year residents (N = 55) . | 2nd year residents (N = 58) . | 3rd year residents (N = 51) . | 4th year residents (N = 53) . | P . |
|---|---|---|---|---|---|---|
| At what age is there a slight decrease in women's ability to become pregnant? | 31.67 (3.10) | 31.55 (3.47) | 31.43 (2.74) | 31.37 (2.95) | 32.36 (3.21) | 0.32 |
| 15–24 | 0.9% | 1.8% | 0% | 0% | 1.9% | |
| 25–29* | 9.7% | 9.1% | 10.3% | 15.7% | 3.8% | |
| 30–34* | 53.0% | 50.9% | 60.3% | 54.9% | 45.3% | |
| 35–59 | 33.1% | 38.2% | 29.3% | 29.4% | 49.1% | |
| At what age is there a marked decrease in women's ability to become pregnant? | 37.58 (2.53) | 37.95 (2.54) | 37.17 (2.62) | 37.20 (2.51) | 38.00 (2.39) | 0.15 |
| 25–34 | 0% | 0% | 0% | 0% | 0% | |
| 35–39* | 52.5% | 47.3% | 60.3% | 58.8% | 43.4% | |
| 40–44 | 46.5% | 50.9% | 37.9% | 41.2% | 56.6% | |
| 45–59 | 0.9% | 1.8% | 1.7% | 0% | 0% | |
| What is the overall chance, on average, that a couple who undergoes treatment with in vitro fertilization will have a child after one treatment? | 42.30 (18.37) | 41.20 (19.52) | 45.02 (18.75) | 42.02 (18.61) | 40.75 (16.62) | 0.61 |
| 0–19% | 5.1% | 7.3% | 1.7% | 5.9% | 5.7% | |
| 20–29%* | 16.6% | 16.4% | 17.2% | 13.7% | 18.9% | |
| 30–39% | 24.0% | 29.1% | 19.0% | 29.4% | 18.9% | |
| 40–100% | 54.4% | 47.3% | 62.1% | 51.0% | 56.6% |
| Fertility issue . | All residents (N = 217) . | 1st year residents (N = 55) . | 2nd year residents (N = 58) . | 3rd year residents (N = 51) . | 4th year residents (N = 53) . | P . |
|---|---|---|---|---|---|---|
| At what age is there a slight decrease in women's ability to become pregnant? | 31.67 (3.10) | 31.55 (3.47) | 31.43 (2.74) | 31.37 (2.95) | 32.36 (3.21) | 0.32 |
| 15–24 | 0.9% | 1.8% | 0% | 0% | 1.9% | |
| 25–29* | 9.7% | 9.1% | 10.3% | 15.7% | 3.8% | |
| 30–34* | 53.0% | 50.9% | 60.3% | 54.9% | 45.3% | |
| 35–59 | 33.1% | 38.2% | 29.3% | 29.4% | 49.1% | |
| At what age is there a marked decrease in women's ability to become pregnant? | 37.58 (2.53) | 37.95 (2.54) | 37.17 (2.62) | 37.20 (2.51) | 38.00 (2.39) | 0.15 |
| 25–34 | 0% | 0% | 0% | 0% | 0% | |
| 35–39* | 52.5% | 47.3% | 60.3% | 58.8% | 43.4% | |
| 40–44 | 46.5% | 50.9% | 37.9% | 41.2% | 56.6% | |
| 45–59 | 0.9% | 1.8% | 1.7% | 0% | 0% | |
| What is the overall chance, on average, that a couple who undergoes treatment with in vitro fertilization will have a child after one treatment? | 42.30 (18.37) | 41.20 (19.52) | 45.02 (18.75) | 42.02 (18.61) | 40.75 (16.62) | 0.61 |
| 0–19% | 5.1% | 7.3% | 1.7% | 5.9% | 5.7% | |
| 20–29%* | 16.6% | 16.4% | 17.2% | 13.7% | 18.9% | |
| 30–39% | 24.0% | 29.1% | 19.0% | 29.4% | 18.9% | |
| 40–100% | 54.4% | 47.3% | 62.1% | 51.0% | 56.6% |
*Asterisk indicates the correct category based on published literature. For the slight decline in fertility, literature suggests this decline can begin in the late 20s to early 30s. Note. Means and standard deviations are presented in the first row for each fertility issue; percentages are presented in subsequent rows. Significance values come from one-way analyses of variance testing for differences based on year in residency.
Residents also overestimated the overall chance of success in having a child after undergoing one IVF treatment cycle, as more than three-quarters of residents (78.4%) believed that the success rate was 30% or higher. The respondents' mean estimate of overall success was 42.3% (SD = 18.4%; minimum = 5%; maximum = 80%). Estimates for success after IVF did not differ by residency year.
Familiarity with oocyte cryopreservation and attitudes toward use
Residents' attitudes towards the use of oocyte cryopreservation are presented in Table IV. Only one in four residents (25.1%) indicated that they were either ‘familiar’ or ‘very familiar’ with oocyte cryopreservation. However, six in ten residents (62.6%) worked at a training institution that offered oocyte cryopreservation to patients, suggesting a lack of education within US institutions' OB/GYN residency programs about these new technologies.
Obstetrics and gynecology (OB/GYN) residents' attitudes toward use of oocyte cryopreservation.
| Item . | . | N . | % . |
|---|---|---|---|
| Should an OB/GYN initiate discussions regarding oocyte cryopreservation with female patients? | |||
| Yes | 83 | 39.9 | |
| No | 125 | 60.1 | |
| Should discussing oocyte cryopreservation be part of a well-woman annual exam with a gynecologist? | |||
| Yes | 42 | 20.4 | |
| No | 164 | 79.6 | |
| Reasons for yes | Educating women about this issue helps women make more informed reproductive decisions | 33 | 78.6 |
| Understanding the implications of oocyte cryopreservation increases women's childbearing choices | 31 | 73.8 | |
| I want to provide comprehensive health education to all my patients | 28 | 66.7 | |
| Other | 1 | 2.4 | |
| Reasons for no | Bringing this issue up annually is too frequent, but I am not opposed to discussing this issue with patients every three to four years | 79 | 48.2 |
| I don't want to be perceived as pushing childbearing on patients | 49 | 29.9 | |
| Other | 45 | 27.4 | |
| Bringing up this issue annually may lead to emotional distress in my patients | 44 | 26.8 | |
| I want to be able to fully respect patient choices | 40 | 24.4 | |
| It is not my primary responsibility | 28 | 17.1 | |
| I don't have enough time | 25 | 15.2 | |
| Item . | . | N . | % . |
|---|---|---|---|
| Should an OB/GYN initiate discussions regarding oocyte cryopreservation with female patients? | |||
| Yes | 83 | 39.9 | |
| No | 125 | 60.1 | |
| Should discussing oocyte cryopreservation be part of a well-woman annual exam with a gynecologist? | |||
| Yes | 42 | 20.4 | |
| No | 164 | 79.6 | |
| Reasons for yes | Educating women about this issue helps women make more informed reproductive decisions | 33 | 78.6 |
| Understanding the implications of oocyte cryopreservation increases women's childbearing choices | 31 | 73.8 | |
| I want to provide comprehensive health education to all my patients | 28 | 66.7 | |
| Other | 1 | 2.4 | |
| Reasons for no | Bringing this issue up annually is too frequent, but I am not opposed to discussing this issue with patients every three to four years | 79 | 48.2 |
| I don't want to be perceived as pushing childbearing on patients | 49 | 29.9 | |
| Other | 45 | 27.4 | |
| Bringing up this issue annually may lead to emotional distress in my patients | 44 | 26.8 | |
| I want to be able to fully respect patient choices | 40 | 24.4 | |
| It is not my primary responsibility | 28 | 17.1 | |
| I don't have enough time | 25 | 15.2 | |
Obstetrics and gynecology (OB/GYN) residents' attitudes toward use of oocyte cryopreservation.
| Item . | . | N . | % . |
|---|---|---|---|
| Should an OB/GYN initiate discussions regarding oocyte cryopreservation with female patients? | |||
| Yes | 83 | 39.9 | |
| No | 125 | 60.1 | |
| Should discussing oocyte cryopreservation be part of a well-woman annual exam with a gynecologist? | |||
| Yes | 42 | 20.4 | |
| No | 164 | 79.6 | |
| Reasons for yes | Educating women about this issue helps women make more informed reproductive decisions | 33 | 78.6 |
| Understanding the implications of oocyte cryopreservation increases women's childbearing choices | 31 | 73.8 | |
| I want to provide comprehensive health education to all my patients | 28 | 66.7 | |
| Other | 1 | 2.4 | |
| Reasons for no | Bringing this issue up annually is too frequent, but I am not opposed to discussing this issue with patients every three to four years | 79 | 48.2 |
| I don't want to be perceived as pushing childbearing on patients | 49 | 29.9 | |
| Other | 45 | 27.4 | |
| Bringing up this issue annually may lead to emotional distress in my patients | 44 | 26.8 | |
| I want to be able to fully respect patient choices | 40 | 24.4 | |
| It is not my primary responsibility | 28 | 17.1 | |
| I don't have enough time | 25 | 15.2 | |
| Item . | . | N . | % . |
|---|---|---|---|
| Should an OB/GYN initiate discussions regarding oocyte cryopreservation with female patients? | |||
| Yes | 83 | 39.9 | |
| No | 125 | 60.1 | |
| Should discussing oocyte cryopreservation be part of a well-woman annual exam with a gynecologist? | |||
| Yes | 42 | 20.4 | |
| No | 164 | 79.6 | |
| Reasons for yes | Educating women about this issue helps women make more informed reproductive decisions | 33 | 78.6 |
| Understanding the implications of oocyte cryopreservation increases women's childbearing choices | 31 | 73.8 | |
| I want to provide comprehensive health education to all my patients | 28 | 66.7 | |
| Other | 1 | 2.4 | |
| Reasons for no | Bringing this issue up annually is too frequent, but I am not opposed to discussing this issue with patients every three to four years | 79 | 48.2 |
| I don't want to be perceived as pushing childbearing on patients | 49 | 29.9 | |
| Other | 45 | 27.4 | |
| Bringing up this issue annually may lead to emotional distress in my patients | 44 | 26.8 | |
| I want to be able to fully respect patient choices | 40 | 24.4 | |
| It is not my primary responsibility | 28 | 17.1 | |
| I don't have enough time | 25 | 15.2 | |
Sixty percent of respondents did not think that OB/GYNs should initiate discussion of oocyte cryopreservation with their female patients. Of the 40% of respondents who did think that OB/GYNs should initiate discussion, the mean patient age at which such discussions would occur was 31.1 (SD = 4.2). Even fewer respondents (20.4%) thought that discussion of oocyte cryopreservation should be part of an annual well-woman exam. Reasons given for discussing oocyte cryopreservation during an annual exam included educating women to make informed reproductive choices and helping them understand the implications of oocyte cryopreservation. Reasons against discussing this issue during an annual exam included wanting to be respectful of patient choices and not wanting to be perceived as pushing childbearing.
Likelihood of discussing or supporting oocyte cryopreservation for different patient situations
When presented with different patient scenarios, residents showed varying levels of support for discussing oocyte cryopreservation. As shown in Fig. 1, residents were very likely to discuss oocyte cryopreservation with patients who had received a cancer diagnosis, regardless of whether that patient was 25 or 35 years of age. In contrast, residents were either somewhat or very unlikely to discuss EOC with patients who wanted to pursue a career before starting a family, especially for younger patients. Similar patterns were evident for residents' support of insurance coverage of oocyte cryopreservation, with many more residents likely to support insurance coverage for patients who had received a cancer diagnosis versus those who wished to pursue a career prior to starting a family (data not shown).
Likelihood of discussing medically indicated and elective oocyte cryopreservation by age.
Discussion
To our knowledge, this is the first study to examine the attitudes, knowledge, and intentions regarding fertility awareness and oocyte cryopreservation among US OB/GYN residents. Nearly all residents (92%) who completed the survey believed that an OB/GYN should initiate discussions regarding their patients' childbearing intentions. Furthermore, 83% of residents said that they believed an OB/GYN should initiate discussions about age-related fertility decline with female patients, and 72% said that these discussions should be a part of an annual well-woman exam. These findings are encouraging, as numerous international studies have shown that women who are likely to delay childbearing also lack awareness of age-related fertility decline. A recent study sampling fertility patients from 79 countries found that accurate fertility knowledge was reported by only 56.9% of patients, supporting the need for more education (Bunting et al., 2013). Although physicians and other health care providers should be the first-line reproductive health educators for women (Peterson et al., 2012; Wyndham et al., 2012; Hodes-Wertz et al., 2013), studies show that many women report never having discussed the effect of age on their ability to conceive, even though they identify their health care providers as their top source of information on fertility and reproductive health (Lundsberg et al., 2014).
Although it is encouraging that the majority of OB/GYN residents believe that physicians should initiate discussions about fertility decline with their patients, a surprisingly large percentage of the residents surveyed were misinformed about fertility decline themselves. For example, 33% of residents believed female fertility slightly declines at age 35 or after, and nearly half (46.5%) of residents indicated that fertility declines markedly at age 40 or after—when, in fact, the marked decline occurs on average around the age of 37 (Dunson et al., 2002; ASRM, 2013). Given that OB/GYNs are the gatekeepers of the dissemination of correct reproductive knowledge, it is concerning that nearly half of the residents in this study were so uninformed about these basic reproductive facts. Furthermore, given that prior studies suggest that provision of fertility information impacts patient knowledge and intentions toward delaying childbearing (Williamson et al., 2014), these findings highlight a critical need for improved education and curricular offerings on age-related fertility decline in OB/GYN residency programs in the USA.
In addition to misconceptions about age-related infertility, residents in this study were also misinformed about the success rates of ARTs. Over three-quarters of residents (78.4%) overestimated the likely success of IVF in treating infertility. OB/GYN residents seem to share the common misconceptions—perpetuated by inaccurate media reports, especially of ‘celebrity moms’—that women can delay having children until after 40, and that any difficulties can be overcome through IVF (Wyndham et al., 2012). It is important to educate practitioners that ARTs such as IVF can only make up for half of the births lost by postponing a first attempt to conceive from age 30 to 35, so that they may correct any misperceptions that patients may have (Leridon, 2004; Wyndham et al., 2012; ASRM, 2013). ART success rates are directly related to the age of the patient. For example, women under 35 in the United States have a 41.5% chance for a live birth using IVF. However, for older women—who may have intentionally postponed childbearing under the false impression that ARTs could correct any difficulties with fertility—only 11.7% of women aged 41–42, and only 4.5% of women ages 43–44 had a live birth (CDC, 2014). In other words, women who use ART in their 40s are much less likely than younger women to have a live birth as a result.
When OB/GYN residents in this study were asked whether they should initiate discussions regarding oocyte cryopreservation with patients, less than half (40%) believed that OB/GYNs should, and only one-fifth (20%) reported that it should be a part of an annual well-woman exam. In a 2013 study of 183 women who had undergone at least one oocyte cryopreservation cycle, the mean age of patients who cryopreserved their oocytes was 38, an age at which oocytes already have reduced quality and reproductive potential (Hodes-Wertz et al., 2013). Furthermore, 79% of the women wished they had undergone EOC at an earlier age, and only one-third had discussed EOC with their gynecologist prior to the procedure. In the current study, residents believed OB/GYNs should initiate discussions about EOC with patients starting at age 31, an age when a woman's reproductive potential is greater than the current norm among actual EOC users, who are on average freezing their oocytes in their late 30s. Recent data from decision-analysis models propose that the highest probability of achieving a live birth may be when women undertake EOC at <34 years of age (Mesen et al., 2015). Also, cost-effectiveness studies show that freezing oocytes by age 35 in women who plan to delay childbearing until age 40 effectively reduces the cost per live birth (Devine et al., 2015).
In considering the role of physicians in discussing these issues with patients, it is important to note that childbearing decisions are also influenced by relational circumstances or other factors that are beyond a patient's immediate control. For example, in a study of women who underwent EOC to preserve their fertility, 161 (88%) had delayed childbearing because they lacked a partner (Hodes-Wertz et al., 2013). OB/GYNs should be sensitive to these possibilities while delivering information about fertility decline and EOC. However, EOC may offer some women relief from the pressure of entering into an unwanted relationship ‘for the sake of children,’ or to have children before they are ready. Counseling women about their fertility and the possibility of EOC requires both maximal sensitivity and respect for patients' reproductive autonomy. Yet, ideally, OB/GYNs should be initiating such discussions with their patients at an age when patients' reproductive potential can be maximized (the late 20s to early 30s) and when women may have the greatest flexibility in reproductive decision making.
We acknowledge an absence of studies that examine how women may respond to such discussions. However, we support the conclusions of other studies that call for research to investigate if patients want physicians to initiate these types of discussions, and under what circumstances they would like them to take place (Buske et al., 2015). The results of such research would be useful for OB/GYN training programs around the world, in order to teach residents how to deliver information about age-related fertility decline and oocyte cryopreservation in a way that respects patient circumstances, while providing education required for informed decision-making.
Examining the attitudes and knowledge of physicians regarding fertility preservation is critical, and this need has been highlighted in several international studies. For example, in Germany, a survey of 120 oncologists found that while nearly all of the physicians felt fertility preservation was an important issue, only half reported having a thorough understanding of it, and only 40% reported discussing it with patients routinely (Buske et al., 2015). A recent study of breast cancer specialists in Japan found that physicians who had more positive attitudes toward fertility preservation were more likely to discuss this with patients, and calls were made to improve interdisciplinary communication between physicians and infertility specialists to improve patient care (Shimizu et al., 2013). Countries around the world are also beginning to incorporate EOC into standard fertility care, with some nations considering oocyte cryopreservation to be cost effective and thus potentially covered by insurance or national health plans (Shkedi-Rafid et al., 2011; Van Loendersloot et al., 2011). In the current study, residents suggested that they would be more likely to support insurance coverage for oocyte cryopreservation in cancer patients than for age-matched patients seeking EOC. Thus, future studies must examine how financial coverage of these technologies might impact attitudes toward and uses of both medical oocyte cryopreservation and EOC in countries throughout the world.
Finally, it is important to note that women do not typically make their reproductive decisions alone, and often include male partners. Men have also been found to significantly overestimate the ages at which female fertility declines (Peterson et al., 2012). Furthermore, some data have shown that women's desire for childbearing may be related in part to whether a male partner desires children (Holton, et al., 2011). Given that reproductive health and the impact of fertility treatments have increasingly been conceptualized as a couple's issue (Peterson et al., 2009, 2011), it is important that providers of men's health care also be encouraged to seek appropriate education regarding age-related fertility decline. As noted in a recent review, men are often the ‘forgotten partner’ when couples are diagnosed with infertility – even in cases of male-factor infertility (Petok, 2015). Once a couple is diagnosed with infertility, both partners participate in the help seeking process (Johnson and Johnson, 2009). Thus, leaving men out of reproductive counseling overlooks the significant contribution that men make to reproduction (Inhorn et al., 2009). Discussions of fertility decline and oocyte cryopreservation can include men as well as women, so that both individuals and couples are better informed about their full range of reproductive options (Azhar et al., 2015).
Limitations
The findings of this study must also be interpreted in light of the study's limitations. First, due to our sampling methods, we were unable to calculate the exact number of residents who actually received a recruitment email. Because residents completed the survey in an online, anonymous questionnaire format, we must take into account the possibility for bias in the study findings. Inherent to email-based sampling is self-selection bias; we were unable to evaluate characteristics of non-respondents and thus cannot be sure that our findings may therefore not be generalizable to all residents. In addition, female residents were slightly over-represented in our sample when compared with the proportion of female OB/GYN residents in the USA (AAMC, 2014; ACGME, 2014). The study also did not address residents' attitudes and intentions regarding the education of men about fertility decline and oocyte cryopreservation. Finally, due to the small number of male respondents, analyses lacked sufficient power to explore gender differences among the study responses.
Conclusion
This study is the first of its kind to examine the knowledge, attitudes, and intentions of US OB/GYN residents in providing patients with information on age-related fertility decline and oocyte cryopreservation. The findings highlight a critical need for improved education among US OB/GYN residents about issues related to age-related fertility decline and the use of oocyte cryopreservation for both medical and elective reasons. Although our study focused on OB/GYN residents in the USA, topics of reproductive health and fertility are universal; thus, further research is needed to explore the role of education across cultures and in countries where OB/GYN training programs may differ in duration and method. If OB/GYNs are taught to present fertility decline and oocyte cryopreservation to patients in a way that is both respectful of individual patient autonomy and informative about new reproductive technologies, then they will maximize their patients' ability to make the most informed reproductive decisions possible.
Authors' roles
P.P. proposed the study, design and reviewed and analyzed data; L.Y. and B.P. designed the study instrument, implemented the study, analyzed data, and prepared the initial manuscript; J.K.B. conducted data analysis and statistics and assisted with manuscript preparation; M.C.I. edited the manuscript and further enhanced data analysis.
Funding
No external funding was either sought or obtained for this study.
Conflict of interest
None declared.
Acknowledgements
Special thanks to Ashley Hodgson for her help in preparing the manuscript.
References
