Disparities among infertility patients regarding genetic carrier screening, sex selection, and gene editing.

Purpose The purpose of this study is to evaluate the perspectives of infertility patients regarding genetic carrier screening, embryo sex selection, embryo research, and gene editing.

An anonymous 32-question survey was distributed electronically to all patients who seen at a single academic fertility center for at least one visit between June 2018 and September 2019. Survey questions evaluated patient perspectives on genetic carrier screening, embryo sex selection, embryo research, and gene editing.

There were 1460 survey responses (32.0% response rate). There were significant differences in the proportion of respondents receiving genetic carrier screening between racial groups, 73.1% of White, 45.5% of Black, 49.4% of Hispanic, and 62.8% of Asian respondents. The likelihood of having genetic carrier screening was also significantly influenced by respondent income, insurance status, and religion. Religion significantly influenced the acceptance of embryonic research and embryonic sex selection. While only 8.9% felt that genetically modifying embryos for physical traits should be allowed, 74.1% felt that genetic modification to correct disease should be allowed.

Racial, religious, and socioeconomic factors significantly impacted respondents’ likelihood to have genetic carrier screening and views on embryo sex selection, embryo research, and gene editing. These findings highlight the importance of tailoring genetic counseling to the individual, acknowledging individual and cultural differences in agreement with genetic testing and emerging genetic therapies. Supplementary Information The online version contains supplementary material available at 10.1007/s10815-021-02261-7.

Genetic counseling, Gene editing, Sex selection, Genetic carrier screening

In 2020, the Nobel Prize in Chemistry was awarded to Emmanuelle Charpentier and Jennifer Doudna for their discovery of CRISPR-Cas9 genome editing [1]. This novel technology has been revolutionary and opened the door to an array of applications including the genetic modification of embryos to correct or prevent disease. While the potential applications of CRISPR-Cas9 have excited the scientific community, the early use of the technology on viable embryos led to an outcry regarding the ethics and safety of gene editing. In September 2020, an international panel announced that gene editing should not yet be used in human embryos [2]. Due to these rapid advances in genetic technologies and diagnostic and therapeutic capabilities, it is important to understand what influences patients’ views on genetic screening, embryo research, and new technologies to genetically modify the genome. These perspectives will help inform the design of educational materials and be critical to shaping policies and regulations [3]. Past studies of genetic carrier screening showed that patients overwhelmingly wanted to be offered the choice of screening. However, while some patients felt the information provided a sense of control, others felt it detracted from the natural experience of pregnancy and led to increased anxiety [4]. Education and counseling must therefore be tailored to meet the needs of diverse patients with differing viewpoints. There is evidence that some providers currently recommend this “extra” genetic testing only when requested by the patient [5]. Therefore, gaining a better understanding of what patients want could help shape policies and encourage providers to initiate these conversations rather than waiting for patients to request testing. Genetic carrier screening mostly identifies recessive disease traits in those screened, identifying women that have a normal phenotype but are silent carriers for a recessive genetic condition [10]. Carrier prevalence varies by race and disease. In addition, carrier screening can also serve to identify X-linked recessive carrier status in women who choose screening. When both a patient and partner screen positive for the same heritable recessive condition, they have the option of prenatal diagnosis to detect the condition in the fetus or in vitro fertilization with preimplantation genetic testing to considerably reduce the likelihood of an affected pregnancy. With the discovery of CRISPR-Cas9, it may eventually be possible to alter the embryonic genome to correct disease. While genome editing may appear to be the next frontier in combating genetic disease, this new technology will likely not be acceptable to all patients. One study showed when asked about using CRISPR-Cas9 to reduce the burden of sickle cell disease, patients reported increased anxiety about uncertainty of outcomes and concerns such as inequities in care, access issues, religious conflicts, or cultural conflicts [6]. We sought to identify perspectives of patients presenting for infertility evaluation and treatment in the topics of genetic carrier screening, embryo sex selection, embryonic research, and genetic modification of embryos (for medical and non-medical reasons). Prior investigations into these fields have been limited, especially among an infertility population that is increasingly utilizing assisted reproductive technologies and genetic testing [7].

Study design Institutional Review Board approval was obtained. This was a single center cross-sectional study performed in the Division of Reproductive Endocrinology and Infertility at Northwestern University Feinberg School of Medicine. Patients were seen at one of three clinical sites. A 32-question survey (Supplemental Figure 1) was adapted from previous work [8] and programmed into REDCap, a secure, HIPAA-compliant, data collection platform. Modifications were made to improve understanding of patient experiences with infertility and to account for recent technological advancements in fertility care. Prior to distribution, the survey was piloted and reviewed by an infertility physician, a non-infertility physician, a clinical psychologist, and five research study staff. The survey instrument collected information regarding demographics, infertility history, and patient perspectives on genetic testing and modification. The survey was distributed in September 2019 to patients who presented to the Northwestern Center for Fertility and Reproductive Medicine (FRM) for at least one visit between June 2018 and September 2019. Patient emails were obtained from the Northwestern Enterprise Data Warehouse (NEDW). The electronic consent form and survey were emailed using REDCap, and responses were collected for 1 month. To encourage survey completion, reminder emails were sent to non-respondents. Baseline demographic data were obtained from the invited individuals via the NEDW to compare the demographics between survey responders and non-responders and evaluate potential non-response bias. Data analysis Descriptive statistics were calculated for all variables of interest. Categorical variables were summarized with the use of counts and percentages, and continuous variables with mean and standard deviation. Statistical tests were conducted using Stata 16. Multiple logistic regression analyses were performed to examine covariate-adjusted determinants of patient attitudes and beliefs by patient race, age, parity, income, religion, education, past fertility treatment, insurance coverage, history of miscarriage, history of anxiety, and history of depression. All available survey data were included in the present analyses. Each individual survey item had < 4% missingness.

Sample There were 5000 unique female patients who presented to the Northwestern Center for Fertility and Reproductive Medicine (FRM) for at least one visit between June 2018 and September 2019 and were eligible to participate. There were 377 undeliverable emails due to incorrect addresses. From the remaining 4623 patients invited, 1460 survey responses were obtained (32.0% response rate). Survey respondents had a mean age of 36.2 years (range 20–58, SD 4.4). The majority of respondents in our sample were White (72.2%), in a heterosexual relationship (86.8%), had an advanced degree (59.6%), and reported an annual household income > $100,000 (81.2%) (Table 1). 54.7% of the sample reported having ever undergone (or currently undergoing IVF treatment). The physician-diagnosed causes of infertility were unexplained (37.2%), advanced age/decreased ovarian reserve (26.6%), ovulatory dysfunction (21.0%), male factor (16.0%), uterine factor (6.9%), blocked fallopian tubes (6.2%), endometriosis (6.1%), genetic factor (2.5%), fertility preservation for cancer (2.3%), same-sex couple (2.2%), and elective fertility preservation (1.2%). Table 1. | N (%) | | |---|---| | Age (N = 1410) | | | 42 years | 107 (7.4%) | | Race or ethnicity (N = 1460) | | | White | 1054 (72.2%) | | Black or AA | 102 (7.0%) | | Hispanic/Latinx | 79 (5.4%) | | Asian | 146 (10.0%) | | Multiple/other | 79 (5.4%) | | Relationship status (N = 1457) | | | Single | 99 (6.8%) | | Heterosexual relationship | 1264 (86.8%) | | Divorced or separated | 16 (1.1%) | | Same-sex relationship | 74 (5.1%) | | Other | 4 (.3%) | | Religion (N = 1418) | | | Catholic | 531 (37.5%) | | Protestant | 212 (15.0%) | | Other Christian | 102 (7.2%) | | Judaism | 122 (8.6%) | | Hinduism | 48 (3.4%) | | Non-religious | 360 (25.4%) | | Other | 43 (3.0%) | | Education (N = 1458) | | | Less than a Bachelor’s degree | 76 (5.2%) | | 4-year college (Bachelor’s degree) | 512 (35.1%) | | Master’s degree | 591 (40.5%) | | Professional degree | 279 (19.1%) | | Annual household income (N = 1440) | | | $400,000 | 155 (10.8%) | There was diversity in patient religion with 37.5% Catholic, 22.2% other Christian, 8.6% Jewish, 3.4% Hindu, 25.4% non-religious, and 3.0% other. The age distribution of our analytic sample [M = 36.0 (SD 4.5)] was similar to that of the entire invited sample [M = 36.2 (SD 4.4)]. In addition, the representation of racial/ethnic minority patients within the analytic sample was comparable to that of the invited sample (7.0% vs 8.2% Black; 5.4% vs 4.5% Hispanic; 10% vs 9.7% Asian). Racial, religious, and socioeconomic factors significantly impacted respondents’ views on genetic carrier screening, embryo sex selection, embryonic research, and the genetic modification of embryos. Genetic carrier screening One thousand one (68.7%) stated that they had undergone genetic carrier screening. Of these, 318 (31.9%) were carriers for a heritable condition. Seven hundred eight (48.9%) stated that their spouse/partner had undergone genetic carrier screening. Eighteen respondents reported that they and their partner were both carriers for the same heritable condition (1.8% of those who received screening). There were significant differences in the proportion of respondents receiving genetic carrier screening between racial groups. 73.1% of White, 45.5% of Black, 49.4% of Hispanic, and 62.8% of Asian respondents reported having had screening, P < 0.001. Similarly, the proportion that reported their spouse had received screening also varied significantly by race: 53.3% of White, 27.7% of Black, 41.7% of Hispanic, and 51.3% of Asian respondents, P < 0.001. After controlling for confounders in a multivariable regression using White as reference, the odds of receiving genetic carrier screening was significantly lower among Black and Latinx women, aOR 0.54 (95% CI 0.31, 0.91) for Black, 0.50 (95% CI 0.29, 0.87) for Latinx, 0.84 (95% CI 0.49, 1.45) for Asian, and 1.07 (95% CI 0.59, 1.94) for other (Fig. 1). The likelihood of electing genetic carrier screening also varied significantly by income, with an increased likelihood of screening at higher income levels. 50.4% of those with an income $200,000 received such screening, P < 0.001. In a multivariable regression, there remained a significantly higher odds of receiving screening by income. Compared to those earning $200,000 (aOR 3.21, 95% CI 2.19, 4.72). Insurance status also significantly impacted the odds of having genetic carrier screening. 53.8% of those with no insurance coverage for infertility had genetic carrier screening, compared to 59.8% of those with < 50% coverage, 71.9% of those with 50–74% coverage, and 74.2% of those with 75–100% coverage. After adjusting for confounders, compared to those with no insurance coverage, those with 50–74% coverage and > 75% coverage were significantly more likely to have had genetic carrier screening (aOR 2.22, 95% CI 1.48, 3.34 and aOR 2.31, 95% CI 1.65, 3.23, respectively). Religion also significantly affected the likelihood of electing genetic carrier screening, with Jewish respondents being the most likely to elect such screening. Of the participants in our study, 83.6% of Jewish, 68.3% of Catholic, 66.5% of Protestant, 61.8% of other Christian, 64.6% of Hindu, and 70.5% of non-religious respondents reported either having had genetic carrier screening or chose to undergo such screening. In a multivariable regression with non-religious as reference, Jewish respondents were significantly more likely to have had genetic carrier screening, aOR 1.88 (95% CI 1.03, 3.42). Sex selection Respondents were divided on the subject of sex selection, with 54.6% of respondents stating that couples should able to choose the sex of their child. After controlling for confounders, Black respondents were significantly more likely to agree with sex selection compared to White respondents, aOR 1.88 (95% CI 1.12, 3.15). Religion was also a factor in the acceptance of embryo sex selection. When asked if it should be acceptable to choose the sex of your child, 60.8% of non-religious, 51.7% of Catholic, 51.0% of Protestant, 64.4% of other Christian, 62.8% of Jewish, and 58.3% of Hindu respondents agreed (P = 0.008). Compared to non-religious, Christians were less likely to agree with sex selection with an aOR of 0.69 (95% CI 0.51, 0.93) in Catholic, 0.62 (95% CI 0.43, 0.90) in Protestant, and 0.50 (95% CI 0.30, 0.84) in other Christian respondents (Fig. 2). In a sub-analysis stratifying patients who did or did not undergo genetic carrier screening, significantly fewer patients felt that couples should be able to choose the sex of their child in the group that did not undergo carrier screening (43.9% vs 59.7%, P < 0.001). Embryonic research When queried as to whether embryos not used by couples could be used for research purposes, 83.4% of respondents agreed that using left-over embryos for research should be allowed. This response varied significantly by race, with 87.7% of White, 66.7% of Black, 64.1% of Hispanic, and 76.6% of Asian respondents agreeing with embryonic research (P < 0.001). After controlling for covariates, Black and Latinx respondents were significantly less likely to agree with using left-over embryos for research, aOR 0.48 (95% CI 0.27, 0.86) and aOR 0.34 (95% CI 0.19, 0.62), respectively (Table 2). Table 2. | Characteristic | Overall | White | Black | Hispanic | Asian | Multiple/other | P value | |---|---|---|---|---|---|---|---| | Genetic carrier screening | 1001 (68.7%) | 770 (73.1%) | 46 (45.5%) | 39 (49.4%) | 91 (62.8%) | 55 (69.6%) | <0.001 | | Sex selection | 786 (54.6%) | 568 (54.5%) | 59 (59.6%) | 38 (48.7%) | 77 (52.7%) | 44 (58.7%) | 0.59 | | Embryonic research | 1202 (83.4%) | 914 (87.7%) | 66 (66.7%) | 50 (64.1%) | 111 (76.6%) | 61 (79.2%) | <0.001 | | Genetically modifying embryos for physical traits | 128 (8.9%) | 81 (7.7%) | 14 (14.1%) | 8 (10.4%) | 14 (9.6%) | 11 (14.5%) | 0.08 | | Genetically modifying embryos to correct disease | 1061 (74.1%) | 782 (75.6%) | 65 (65.0%) | 54 (69.2%) | 107 (74.3%) | 53 (70.7%) | 0.14 | Agreement increased significantly with increasing income, with 72.9% of those earning $400,000 agreeing with embryonic research. Compared to those earning < $100,000, the odds of agreeing with using left-over embryos for research was significantly higher for those at higher incomes, aOR 1.79 (95% CI 1.18, 2.73) at incomes of $100,000–$200,000 and aOR 2.69 (95% CI 1.70, 4.27) at incomes > $200,000. While religion also influenced the acceptance of embryonic research, overall most respondents agreed that embryonic research should be allowed. When ask if it should be acceptable to use left-over embryos for research, 80.9% of Catholic, 90.1% of Protestant, 63.4% of other Christian, 95% of Jewish, 79.2% of Hindu, and 91.7% of non-religious respondents agreed (P < 0.001). Compared to non-religious individuals, Christians were less likely to agree with using left-over embryos for research, with an aOR of 0.47 (95% CI 0.29, 0.76) in Catholic, 0.36 (95% CI 0.21, 0.62) in Protestant, and 0.25 (95% CI 0.13, 0.48) in other Christian respondents. In a sub-analysis stratifying patients who did or did not undergo genetic carrier screening, significantly fewer patients felt that left-over embryos could be used for research in the group that did not undergo carrier screening (76.2% vs 87.0%, P < 0.001). Gene editing The majority of respondents (91.1%) reported that genetically modifying embryos for physical traits (e.g., eye color, hair color, height, etc.) should not be allowed. Upon covariate adjustment, responses did not vary significantly by race, income, or religion. Those with > 75% coverage were less likely to agree compared to those with no coverage, aOR 0.59 (95% CI 0.35, 0.98). In contrast, the majority of respondents (74.1%) reported that genetically modifying embryos to correct disease should be allowed. After covariate adjustment, responses did not vary significantly by race, income, or insurance status. Protestant and other Christian respondents were less likely to agree with genetically modifying for disease compared to non-religious, aOR 0.52 (95% CI 0.35, 0.79) and 0.53 (95% CI 0.31, 0.91), respectively. In contrast, Hindu respondents were significantly more likely to agree with genetically modifying embryos for disease, aOR 4.51 (95% CI 1.22, 16.59). In a sub-analysis stratifying patients who did or did not undergo genetic carrier screening, a slightly higher (but not statistically significant) percentage of patients felt that modifying embryos for physical traits should be allowed in the group that did not undergo carrier screening (9.2% vs 8.7%, P = 0.93). In contrast, a significantly lower percentage of patients felt that modifying embryos to correct disease should be allowed in the group that did not undergo carrier screening (67.0% vs 77.2%, P = 0.93). Impact of views on likelihood of genetic carrier screening The likelihood of having had genetic carrier screening was significantly associated with respondent views on embryonic research, sex selection, and genetic modification of embryos. Those respondents that agreed with using left-over embryos for research, sex selection, and genetically modifying embryos to modify disease risk were also significantly more likely to have had genetic carrier screening, P < 0.001 for all comparisons.

We show in this study that racial, religious, and socioeconomic factors considerably influence respondents’ views on genetic carrier screening, embryo sex selection, embryonic research, and the genetic modification of embryos. We show that Jewish respondents were significantly more likely to have had genetic carrier screening, with an adjusted odds ratio of 1.88 compared to non-religious respondents. This finding likely reflects the success of efforts by the Jewish community to increase awareness and performance of carrier screening, beginning 30 years ago with the introduction of screening for Tay-Sachs disease. Indeed, carrier screening has been met with overwhelming acceptance by all sectors of the Jewish community in the USA and worldwide [9]. While the successful screening of the majority of Jewish respondents is reassuring, we must now work to improve acceptance of genetic carrier screening in other communities. Ethnicity-based carrier screening can be limited by inaccurate knowledge of ancestry, and so pan-ethnic screening for some conditions is reasonable. A shift from an opt-in to an opt-out approach to screening may be beneficial for infertile couples for whom this information can lead to better outcomes with the use of preimplantation genetic testing, with the goal of improving participation while maintaining patient autonomy regarding which testing to undergo or forego. The American College of Obstetricians and Gynecologists (ACOG) recommends that information about carrier screening be provided to every pregnant woman and that counseling should ideally be performed preconception [10]. In addition, ACOG recommends universal screening be offered to all couples for spinal muscular atrophy, cystic fibrosis, and hemoglobinopathies. We found that universal genetic carrier screening was not achieved among our sample, with significantly less screening performed in Black and Hispanic patients. While 73.1% of White patients received genetic carrier screening, only 45.5% of Black and 49.4% of Hispanic patients had been screened. This study also revealed a concerning trend toward decreased genetic carrier screening for patients with lower income and insurance coverage for infertility. While 82% of respondents with an income > $200,000 received genetic carrier screening, only 50.4% of those with an income 75% insurance coverage received screening, compared to only 52.8% of those with no insurance coverage. These findings suggest that patients’ decision to pursue genetic carrier screening is influenced by cost rather than their desire for testing. Our clinic routinely offers and performs expanded carrier screening which costs $349 if not covered by insurance. Further research is needed to determine if patients are electing not to have screening due to fear that insurance will not cover screening or high deductibles. These data highlight the need to offer alternative, less expensive options for carrier screening if a patient declines screening, rather than assuming that screening is not desired. While our clinic policy does not allow for sex selection for non-medical purposes, over half of respondents felt that couples should be able to choose the sex of their child. This finding persisted in all races, income, and insurance groups and is consistent with prior literature on views of sex selection among infertility patients [8, 11, 12]. The majority of US fertility clinics do offer non-medical sex selection. In a 2017 survey, 72.7% of fertility clinics offered sex selection. Of those, 93.6% offered sex selection for family balancing (to have a child of the opposite sex of previous offspring) and 81.2% offered elective sex selection [13]. Sex selection for non-medical purposes is an ethical challenge in our field, as the practice could encourage gender bias and lead to gender imbalances in society [14]. As new technologies for gene editing continue to advance, embryonic research will likely be necessary. While the majority of respondents (83%) agreed with using left-over embryos for research, this response varied significantly by race, income, and religion. Black, Latinx, and Christian respondents were significantly less likely to agree, while those at higher incomes were significantly more likely to agree with embryonic research. While we hypothesized that Catholic respondents would be less likely to agree with embryonic research, it is reassuring that the majority (80.9%) felt it should be allowed. The overwhelming majority of respondents (91%) in our study did not agree with genetically modifying embryos for physical traits (eye color, hair color, height, etc.). In contrast, the majority of respondents (74%) did agree with genetically modifying embryos to correct for disease. Interestingly, Hindu respondents were significantly more likely to support genetically modifying embryos for disease, aOR 4.51 relative to their non-religious/secular counterparts. It is unclear if this agreement is due to a greater acceptance of the technology or a greater concern regarding genetic diseases that may impact offspring. We found that the likelihood of having had genetic carrier screening was significantly associated with respondents’ views on embryonic research, sex selection, and genetic modification of embryos to modify disease. Given that views on the role of genetics in ART are significantly intertwined with the likelihood of carrier screening highlight the importance of patient education to improve acceptance of recommended screening practices. This study is strengthened by the inclusion of a large sample (N = 1460) with diverse ethnicity, religion, income, and insurance coverage. This enabled us to identify factors that may influence respondents’ views on genetic carrier screening, embryonic research, and genetic modification of embryos. We are limited by a response rate of 32% and therefore it is possible that our findings were impacted by non-response bias. In an effort to improve the response rate, reminder emails were sent to eligible subjects. In addition, in a post-hoc analysis, we found that the analytic sample was comparable to the invited sample, with a similar representation of racial/ethnic minority patients and similar age distribution. In conclusion, we found that racial, religious, and socioeconomic factors affected respondents’ views on genetic carrier screening, embryo sex selection, embryonic research, and the genetic modification of embryos. In addition, the likelihood of genetic carrier screening was significantly associated with respondents’ views on the role of embryonic genetics in ART. Further research is needed to understand how we can improve education and counseling on the use of genetic testing. Our findings highlight the importance of tailoring genetic counseling to the individual, acknowledging individual and cultural differences in electing genetic testing modalities and considering the use of emerging genetic therapies. Supplementary Information Acknowledgments Availability of data and material Available upon request. Code availability N/A. Declarations Ethics approval IRB approval was obtained. Consent to participate Subjects gave written consent. Consent for publication Subjects gave written consent. Conflict of interest The authors declare no competing interests. Footnotes Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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