Racial disparities in in vitro fertilization outcomes Dana B. McQueen, M.D., M.A.S.,a Ann Schufreider, M.D.,a Sang Mee Lee, Ph.D.,b Eve C. Feinberg, M.D.,a,c,d and Meike L. Uhler, M.D.d a
Department of Obstetrics and Gynecology and b Department of Public Health Sciences, University of Chicago, Chicago; Department of Obstetrics and Gynecology, North Shore University Health System, Evanston; and d Fertility Centers of Illinois, Chicago, Illinois c
Objective: To evaluate the impact of race on in vitro fertilization (IVF) outcomes. Design: Retrospective analysis. Setting: Private practice. Patient(s): All women who underwent a first autologous IVF cycle at Fertility Centers of Illinois from January 2010 to December 2012. Intervention(s): Information was collected on baseline characteristics, cycle parameters, and outcomes. Race was self-reported. Main Outcome Measure(s): Clinical intrauterine pregnancy and live birth rates. Result(s): A total of 4,045 women were included: 3,003 white (74.2%), 213 black (5.3%), 541 Asian (13.4%), and 288 Hispanic women (7.1%). A multivariable logistic regression was performed to control for confounders. Compared with white women, the adjusted odds ratio for clinical intrauterine pregnancy was 0.63 (95% confidence interval [CI] 0.44–0.88) in black women, 0.73 (95% CI 0.60–0.90) in Asian women, and 0.82 (95% CI 0.62–1.07) in Hispanic women. The adjusted odds ratio for live birth was 0.50 (95% CI 0.33–0.72) in black women, 0.64 (95% CI 0.51–0.80) in Asian women, and 0.80 (95% CI 0.60–1.06) in Hispanic women compared with white women. The spontaneous abortion rate was 14.6% in white women versus 28.9% in black women, 20.6% in Asian women, and 15.3% in Hispanic women. Conclusion(s): Black and Asian women had lower odds of clinical intrauterine pregnancy and live birth and higher rates of spontaneous abortion compared with white women. Further research is needed to better characterize the mechanisms associated with this racial disparity and to improve treatment options for black Use your smartphone and Asian women. (Fertil SterilÒ 2015;104:398–402. Ó2015 by American Society for Reproducto scan this QR code tive Medicine.) and connect to the Key Words: Racial disparity, infertility, in vitro fertilization Discuss: You can discuss this article with its authors and with other ASRM members at http:// fertstertforum.com/mcqueend-racial-disparities-ivf-outcomes/
R
esearch on predictors of in vitro fertilization (IVF) success is an area of concentrated interest. Factors known to be associated with IVF outcomes include age, ovarian reserve, oocyte quality, body mass index, endometrial receptivity, and male factors (1). In recent years, there have been several publications that suggest racial disparities in IVF outcomes. The study of racial disparity is complex
and subject to a considerable number of confounders, including socioeconomic status. A large data set with a heterogeneous patient population is needed to reach meaningful conclusions, and therefore several studies on this topic have used the Society of Assisted and Reproductive Technology (SART) data set. In 2006, Purcell et al. analyzed the SART dataset and included 25,843 white and 1,429 Asian
Received January 27, 2015; revised May 10, 2015; accepted May 11, 2015; published online June 11, 2015. D.B.M. has nothing to disclose. A.S. has nothing to disclose. S.M.L. has nothing to disclose. E.C.F. has nothing to disclose. M.L.U. has nothing to disclose. Supported by the University of Chicago Department of Obstetrics and Gynecology. Presented as a poster at the American Society for Reproductive Medicine Meeting, Honolulu, Hawaii, October 18–22, 2014. Reprint requests: Meike L. Uhler, M.D., Fertility Centers of Illinois, 1S224 Summit Avenue, Ste. 302, Oakbrook Terrace, Illinois 60181 (E-mail: [email protected]). Fertility and Sterility® Vol. 104, No. 2, August 2015 0015-0282/$36.00 Copyright ©2015 American Society for Reproductive Medicine, Published by Elsevier Inc. http://dx.doi.org/10.1016/j.fertnstert.2015.05.012 398
discussion forum for this article now.*
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women (2). After controlling for several confounders, Asian ethnicity was found to be an independent risk factor for worse outcomes with an adjusted odds ratio (OR) for live birth of 0.76 (95% confidence interval [CI] 0.66– 0.88). In 2007, Seifer et al. performed an analysis of the same SART data set, focusing on IVF outcomes in black women (3). There were 3,666 black and 68,606 white women included in the analysis. The relative risk of not achieving a live birth was found to be 1.21 in black women compared to white women. These findings were confirmed by several other studies that have also used the SART database (4, 5). A major criticism of these SART database studies is that there are wide differences in IVF success rates among clinics. It has also been argued VOL. 104 NO. 2 / AUGUST 2015
Fertility and Sterility® that minority access to care may be limited to clinics with worse outcomes. A study conducted in a single IVF program would therefore have the advantage of being able to better control for confounders and may eliminate some of the differences in access to care for minority patients. One such single-site study was conducted by Feinberg et al. evaluating IVF outcomes in the military setting, with service members of all ranks and races having equal access to care (6). This study revealed no statistical difference in the live birth rate between black women (29.6%) and white women (35.8%). These findings suggested that eliminating access to care issues might lessen differences in outcomes. However, because there was a trend toward worse outcomes among black women it is possible that even though the study had the highest number of minority patients in any published single-site study, it still may not have been adequately powered to detect differences. A significant challenge for single-site studies is lack of an adequate sample size, and previously published single-site studies have included only 27–197 minority women (7–11). Fertility Centers of Illinois (FCI) is a large private practice in the Chicago area that has ten offices in diverse neighborhood settings and performs more than 3,000 IVF cycles annually. Illinois is one of 15 states with mandated insurance coverage for IVF, and Illinois law allows for four cycles of IVF to achieve a first live birth. More than 80% of all patients at FCI have at least partial insurance coverage, and access to care is increased greatly by the state mandate. Chicago is racially diverse, and therefore FCI is an excellent candidate for a single-site study. The objective of the present research was to perform a comprehensive review of IVF outcomes data in a racially diverse private practice setting. Specifically, the primary goal was to evaluate the impact of race on IVF outcomes. We hypothesized that with increased access to care and uniform treatment by a single IVF program, outcome disparities would be reduced.
MATERIALS AND METHODS Study Design Institutional Review Board (IRB) approval was granted by New England IRB. Women who underwent their first autologous fresh IVF cycle from January 2010 to December 2012 were included in the analysis. To limit heterogeneity among participants, donor oocyte cycles, oocyte vitrification, and embryo banking cycles were excluded. Additionally, all cycles for preimplantation genetic diagnosis were excluded. Information was collected on baseline characteristics, as well as IVF cycle parameters and outcomes. Race was self-reported and included categories developed by SART. Women who self-reported race as black, Asian, Hispanic, or white were included in the analysis, and women reporting more than one race were excluded. A clinical pregnancy was defined as an intrauterine gestational sac visible on ultrasound after the 6th week of pregnancy. Clinical pregnancy rate was defined as the proportion of women with an intrauterine gestational sac among all women who received IVF stimulation. Live birth rate was defined as the proportion of women whose IVF treatment VOL. 104 NO. 2 / AUGUST 2015
was followed by the birth of one or more living infants. Spontaneous abortion rate was the proportion of women with a fetal loss before 20 weeks among those women with a clinical intrauterine gestation. Multiple pregnancy rate was defined as the proportion of women with more than one live born infant among all women with a clinical intrauterine gestation. Outcomes in each racial group were compared with all other groups and with white women as a reference.
Data Analysis Statistical analysis was performed with the use of R software version 3.0.1. To assess the contribution of race to IVF outcome, a multivariable logistic regression analysis was performed to control for age, body mass index (BMI), day 3 FSH levels, smoking status, and primary infertility diagnosis. The adjusted and unadjusted ORs are reported with 95% CIs to indicate statistical precision. To account for missing values, a multiple imputation technique was used based on an iterative regression imputation. Data on antim€ ullerian hormone (AMH) and number of embryos transferred were missing for a significant portion of the subjects; therefore, rather than perform imputation for those variables, we excluded them from the regression. This should not have affected our results, because there was no clinically significant difference in AMH or number of embryos transferred across the races. Continuous variables were compared with the use of Student t test. Categoric variables were compared with the use of chisquare test and Fischer exact test. A two-sided P value of < .05 was considered to be statistically significant.
RESULTS Clinical information was collected on 4,155 consecutive women presenting for their first autologous IVF cycle. In this group, 110 women were excluded: 66 (1.6%) of unknown race, 12 (0.3%) American Indian or Alaskan Native, 15 (0.4%) Native Hawaiian or Pacific Islander, and 17 (0.4%) who selfreported multiple races. Information on the race of the partner was not collected. Data from the remaining 4,045 women were analyzed: 3,003 white (74.2%), 213 black (5.3%), 541 Asian (13.4%), and 288 Hispanic women (7.1%). Although mean age was similar among Hispanic, Asian, and white women, black women were slightly older than white women (36.0 vs. 35.2 years; P¼ .02; Table 1). BMI was significantly higher in black and Hispanic women (27.9 and 27.6 kg/m2, respectively) compared with white women (25.1 kg/m2). Asian women had a significantly lower BMI (23.3 kg/m2). Black women were significantly more likely to have tubal factor or uterine factor as their primary infertility diagnosis compared with white women. Hispanic women were also significantly more likely to have tubal factor as their primary diagnosis (Supplemental Table 1, available online at www.fertstert.org). All other baseline characteristics were similar between groups. There were several differences noted during IVF stimulation and embryo transfer between black and white women. Although the response to stimulation and number of oocytes retrieved were similar, black women had fewer mature oocytes, fewer fertilized oocytes, fewer day 5 transfers, fewer 399
ORIGINAL ARTICLE: ENVIRONMENT AND EPIDEMIOLOGY
TABLE 1 Group characteristics (n [ 4,045). Characteristic Mean age (SD), y Mean day 3 FSH (SD), IU/L Mean AMH (SD), ng/mL Mean BMI (SD), kg/m2 Smokers Mean no. of embryos transferred (SD)
White (n [ 3,003)
Black (n [ 213)
Asian (n [ 541)
Hispanic (n [ 288)
P value
35.2 (4.6) (n ¼ 3,003) 10.3 (7.7) (n ¼ 2,974) 2.2 (3.0) (n ¼ 1,282) 25.1 (5.8) (n ¼ 3,003) 9.4% (n ¼ 2,720) 1.9 (0.7) (n ¼ 2,298)
36.0 (5.0) (n ¼ 213) 10.2 (7.8) (n ¼ 211) 2.0 (2.4) (n ¼ 79) 27.9 (6.0)d (n ¼ 213) 5.2%c (n ¼ 202) 2.1 (0.8)c (n ¼ 150)
34.9 (4.5) (n ¼ 541) 9.6 (6.3)c (n ¼ 526) 2.4 (2.8) (n ¼ 232) 23.3 (4.3)d (n ¼ 541) 3.0%d (n ¼ 525) 1.9 (0.7) (n ¼ 416)
34.7 (5.0) (n ¼ 288) 8.8 (4.8)d (n ¼ 281) 2.3 (2.5) (n ¼ 129) 27.6 (6.3)d (n ¼ 288) 9.4% (n ¼ 261) 2.0 (0.8) (n ¼ 216)
.006a .002a .676a < .0001a < .0001b .033a
c
Note: AMH ¼ antim€ ullerian hormone; BMI ¼ body mass index. a Calculated by means of analysis of variance. b Calculated by means of chi-square test. c P< .05 compared with white group. d P< .0001 compared with white group. McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
surplus blastocysts for cryopreservation, and higher cancellation rates compared with white women (Table 2). Outcomes in black women were markedly worse compared with white women. The clinical pregnancy rate was significantly lower (24.4% vs. 36.2%; P¼ .001) and the spontaneous abortion rate significantly higher (28.9% vs. 14.6%; P¼ .01). Black women were less likely to have a multiple pregnancy (7.7% vs. 21.9%; P¼ .02) compared with white women. Most important, the live birth rate among black women was almost half that of white women (16.9% vs. 30.7%; P< .0001; Table 3). Racial disparities were present, but not as marked, in the Asian population. Asian women required a longer duration of stimulation (10.3 vs. 9.9 days; P¼ .001), had a higher mean peak E2 level, had fewer oocytes retrieved, and had fewer surplus blastocysts available for cryopreservation (1.5 vs. 2.0; P< .0001) compared with white women (Table 2). The clinical pregnancy rate was significantly lower (31.4% vs. 36.2%; P¼ .04) in Asian than in white women, and the spontaneous abortion rate was similar (20.6% vs. 14.6%; P¼ .059). The live birth rate among Asian women was significantly lower than in white women (24.0% vs. 30.7%; P¼ .002; Table 3). Outcomes in Hispanic women were similar to those in white women. Despite having a higher cancellation rate, His-
panic women had similar clinical pregnancy rates (34% vs. 36%; P¼ .50), spontaneous abortion rates (15.3% vs. 14.6%; P¼ .97), and live birth rates (28.5% vs. 30.7%; P¼ .48) compared with white women (Table 3). Pregnancy outcomes were significantly worse in both black and Asian populations. The crude ORs, without adjustment for confounders, were calculated to evaluate the odds of clinical intrauterine pregnancy and live birth among black, Asian, and Hispanic women compared with white women. In black women, the unadjusted OR for clinical intrauterine pregnancy was 0.56 (95% CI 0.41–0.78), in Asian women 0.81 (95% CI 0.66–0.98), and in Hispanic women 0.91 (95% CI 0.70–1.17) compared with white women. In black women, the unadjusted OR for live birth was 0.45 (95% CI 0.31–0.66), in Asian women 0.72 (95% CI 0.58– 0.88), and in Hispanic women 0.90 (95% CI 0.69–1.17) compared with white women. A multivariable logistic regression analysis was performed to evaluate the odds of both clinical intrauterine pregnancy and live birth while controlling for age, BMI, day 3 FSH, smoking, and primary infertility diagnosis. In black women, the adjusted OR for clinical intrauterine pregnancy was 0.63 (95% CI 0.44– 0.88), in Asian women 0.73 (95% CI 0.60–0.90), and in
TABLE 2 IVF and pregnancy outcomes (n [ 4,045). Outcome Stimulation (d), mean (SD) Peak E2, mean (SD) Ocytes retrieved (n), mean (SD) Matured oocytes, % Fertilized oocytes, % Day 5 embryo transfer, % Vitrified embryos (n), mean (SD) Cancellations, %
White (n [ 3,003) 9.9 (1.9) 2,388.6 (1,145.5) 13.6 (8.3) 70.8 83.0 47.9 2.0 (3.3) 13.6
Black (n [ 213) 10.0 (2.0) 2,547.4 (1,320.1) 13.7 (9.3) 65.8d 77.6d 37.1d 1.5 (3.3)c 22.0d
Asian (n [ 541) d
10.3 (2.8) 2,694.0e (1,192.8) 12.1e (6.9) 70.0 84.1 47.9 1.5 (2.5)e 13.9
Hispanic (n [ 288)
P value
9.8 (2.1) 2,521.1 (1,218.4) 13.1 (7.6) 73.1 81.4 46.2 1.7 (2.8)c 18.8c
.00034a < .0001a .0043a .0013a .0609a .0225b .0004a .001b
a
Calculated by means of analysis of variance. Calculated by means of chi-square test. P< .05 compared with white group. d P< .01 compared with white group. e P< .0001 compared with white group. b c
McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
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TABLE 3 Pregnancy outcomes (n [ 4,045). Outcome
White (n [ 3,003)
Clinical pregnancy rate Spontaneous abortion rate Multiple pregnancy rate Live birth rate
36.2 14.6 21.9 30.7
Black (n [ 213) c
Asian (n [ 541) b
31.4 20.6 21.8 24.0c
24.4 28.9c 7.7b 16.9d
Hispanic (n [ 288)
P value
34.0 15.3 19.4 28.5
.001a .0136a .1019a < .0001a
Note: Values presented as percent. a Calculated by means of chi-square test. b P< .05 compared with white group. c P< .01 compared with white group. d P< .0001 compared with white group. McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
Hispanic women 0.82 (95% CI 0.62–1.07) compared with white women. Additionally, the adjusted OR for live birth in black women was 0.50 (95% CI 0.33–0.72), in Asian women 0.64 (95% CI 0.51–0.80), and in Hispanic women 0.80 (95% CI 0.60–1.06) compared with white women (Table 4).
DISCUSSION These results show significant racial disparity in IVF outcomes. Although we controlled for multiple confounders, black and Asian women had lower clinical pregnancy rates and lower live birth rates compared with white women. There was also a significantly higher rate of spontaneous abortion among black women compared with white women. This study showed that black women had fewer mature oocytes, fewer fertilized oocytes, lower blastocyst development rates, higher cancellation rates, and higher spontaneous abortion rates compared with white women. Feinberg et al. reported a higher prevalence of leiomyomas in black women compared with white women (30.8% vs. 10.7%) and hypothesized that this may have accounted for a higher spontaneous abortion rate (6). The present data set unfortunately did not include detailed information on leiomyomas or the mean gestational age at the time of miscarriage. Interestingly, the results suggested that black women in our cohort had worse oocyte quality. This may be attributed to the significantly higher BMI in the black women. Research from Moley et al. suggests that the developmental competence of the oocyte is negatively affected by obesity (14). Moreover, high-fatdiet mouse models demonstrate oocyte mitochondrial dysfunction and spindle defects (15). Although our multivariate analysis controlled for BMI, the impact of weight on IVF
outcomes may have overarching effects that could not be isolated in this analysis. Asian women in this study were more likely to have a longer stimulation time, a greater peak E2 level, and a lower number of oocytes retrieved. Although the lower number of oocytes is suggestive of an ovarian etiology for the disparate outcomes, it is possible that the longer stimulation time and greater peak E2 may have adversely affected implantation. Elevated E2 levels created by stimulation might negatively affect endometrial receptivity. This hypothesis was supported by Fujimoto et al., who showed that Asian recipients of donor oocytes who avoided exposure to ovarian stimulation protocols and resultant high E2 levels, had similar pregnancy rates to white women (16). A future study could evaluate the impact of autologous freeze-all cycles with subsequent frozen embryo transfers in Asian women as a means of improving pregnancy rates by potentially enhancing endometrial receptivity. A strength of this study was its large sample size. The inclusion of 3,003 white, 213 black, 541 Asian, and 288 Hispanic women made this study the largest single-site study to date on racial disparities in IVF outcomes. This study is further strengthened by the high percentage of women who reported race (98.4%), with only 1.6% missing racial data. This is in contrast to the 35% of women in the SART dataset who are missing racial information. Indeed, the authors of a systematic review cautioned that firm conclusions on racial disparity can not be made from SART data, because so many practices that submitted their data to SART did not reliably report on race (12). Race was inclusively reported in our cohort, yet our findings are concordant with those of studies based on the SART database. The present study is also strengthened by the inclusion of BMI, a variable not included in previous SART analyses.
TABLE 4 Adjusted odds ratios (95% CI; n [ 4,045). Outcome Clinical pregnancy Live birth
White (n [ 3,003)
Black (n [ 213)
Asian (n [ 541)
Hispanic (n [ 288)
1.0 1.0
0.63 (0.44–0.88) 0.50 (0.33–0.72)
0.73 (0.60–0.90) 0.64 (0.51–0.80)
0.82 (0.62–1.07) 0.80 (0.60–1.06)
Note: Data presented as adjusted odds ratio (95% confidence interval). Adjustment factors: age, body mass index, day 3 FSH, smoking, and primary infertility diagnosis. McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
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ORIGINAL ARTICLE: ENVIRONMENT AND EPIDEMIOLOGY This study was limited in that we were not able to control for additional possible confounders, such as duration of infertility, doses and protocols for stimulation, quality of the embryo transferred, and potential comorbidities, including hypertension or diabetes. Additionally, we did not examine the race of the partner in this study, and the impact of race on male infertility could certainly be a subject of further research. In an effort to create homogeneity in our data, we excluded donor oocyte cycles, and future studies could examine the impact of race on donor oocyte success rates. Additionally, our study lacked data on income and socioeconomic status. The impact of socioeconomic status on IVF outcomes is complex and expands beyond access to health care. In the field of maternal fetal medicine, Geronimus et al. developed the ‘‘weathering hypothesis’’ that asserts that cumulative social stressors lead to adverse health effects and negative birth outcomes (13). It is certainly plausible that chronic stress from background disadvantage could also affect IVF success rates. In conclusion, we showed that marked racial disparities in IVF outcomes persisted even though all care was received at a single center and inequities in access were eased by statemandated insurance coverage. Multiple confounders were controlled for without a reduction in the outcomes gap. Further research is needed to confirm these findings and to better understand the underlying mechanisms associated with racial disparity so that strategies can be developed to improve treatment outcomes for black and Asian women. Acknowledgments: The authors thank the physicians, nurses, staff, and embryologists at Fertility Centers of Illinois for the excellence in patient care that made this work possible. The authors are also grateful to Dr. Ernst Lengyel at the University of Chicago for his critical reading of the manuscript and to Dr. Alicia Armstrong and Dr. James Segars for their mentorship.
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American Society for Reproductive Medicine. Testing and interpreting measures of ovarian reserve; a committee opinion. Fertil Steril 2012;98:1407–15. Purcell K, Schembri M, Frazier LM, Rall MJ, Shen S, Croughan M. Asian ethnicity is associated with reduced pregnancy outcomes after assisted reproductive technology. Fertil Steril 2007;87:297–302.
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Seifer DB, Frazier LM, Grainger DA. Disparity in assisted reproductive technologies outcomes in black women compared with white women. Fertil Steril 2008;90:1701–10. Fujimoto VY, Luke B, Brown MB, Jain T, Armstrong A, Grainger DA. Racial and ethnic disparities in assisted reproductive technology outcomes in the United States. Fertil Steril 2010;93:382–90. Baker VL, Luke B, Brown MB, Alvero R, Frattarelli JL, Usadi R. Multivariate analysis of factors affecting probability of pregnancy and live birth with in vitro fertilization: an analysis of the Society for Assisted Reproductive Technology Clinic Outcomes Reporting System. Fertil Steril 2010;94: 1410–6. Feinberg EC, Larsen FW, Catherino WH, Zhang J, Armstrong AY. Comparison of assisted reproductive technology utilization and outcomes between Caucasian and African American patients in an equal-access-to-care setting. Fertil Steril 2006;85:888–94. Sharara F, McClamrock HD. Differences in in vitro fertilization (IVF) outcome between white and black women in an inner-city, university based IVF program. Fertil Steril 2000;73:1170–3. Nichols JE, Higdon HL, Crane MM, Boone WR. Comparison of implantation and pregnancy rates in African American and white women in an assisted reproductive technologies practice. Fertil Steril 2001;76: 80–4. Dayal MB, Gindoff P, Dubey A, Spitzer TL, Bergin A, Peak D. Does ethnicity influence in vitro fertilization (IVF) birth outcomes? Fertil Steril 2009;91: 2414–8. Langen ES, Shahine LK, Lamb JD, Lathi RB, Milki AA, Fujimoto VY, et al. Asian ethnicity and poor outcomes after in vitro fertilization blastocyst transfer. Obstet Gynecol 2010;115:591–6. Csokmay JM, Hill MJ, Maguire M, Payson MD, Fujimoto VY, Armstrong AY. Are there ethnic differences in pregnancy rates in African American Women versus white women undergoing frozen blastocyst transfers? Fertil Steril 2011;95:89–93. Wellons MF, Fujimoto VY, Baker VL, Barrington DS, Broomfield D, Catherino WH, et al. Race matters: a systematic review of racial/ethnic disparity in Society for Assisted Reproductive Technology reported outcomes. Fertil Steril 2012;98:406–9. Geronimus AT. Black/white differences in the relationship of maternal age to birthweight: a population-based test of the weathering hypothesis. Soc Sci Med 1996;42:589–97. Purcell SH, Moley KH. The impact of obesity on egg quality. J Assist Reprod Genet 2011;28:514–24. Grindler NM, Moley KH. Maternal obesity, infertility and mitochondrial dysfunction: potential mechanisms emerging from mouse model systems. Mol Hum Reprod 2013;19:486–94. Huddleston HG, Rosen MP, Lamb JD, Modan A, Cedars MI, Fujimoto VY. Asian ethnicity in anomymous oocyte donors is associated with increased estradiol levels but comparable recipient pregnancy rates compared with Caucasians. Fertil Steril 2010;94:2059–63.
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SUPPLEMENTAL TABLE 1 Primary infertility diagnosis (n [ 4,045). Diagnosis Diminished ovarian reserve Ovulatory Tubal Endometriosis Uterine Male factor Unexplained Unknown
White (n [ 3,003)
Black (n [ 213)
Asian (n [ 541)
Hispanic (n [ 288)
P value
22.7 (682/3,003) 17.2 (516/3,003) 3.9 (116/3,003) 3.0 (90/3,003) 1 (29/3,003) 17.7 (530/3,003) 24.2 (727/3,003) 10.4 (313/3,003)
23.4 (50/213) 9.4a (20/213) 14.6c (31/213) 3.8 (8/213) 3.3b (7/213) 19.3 (41/213) 17.9 (38/213) 8.5 (18/213)
20.1 (109/541) 19.2 (104/541) 4.1 (22/541) 3.3 (18/541) 1.0 (5/541) 13.5 (73/541) 26.8 (145/541) 12.0 (65/541)
19.4 (56/288) 17.0 (49/288) 11.5c (33/288) 3.8 (11/288) 1.4 (4/288) 16.0 (46/288) 22.9 (66/288) 8.0 (23/288)
.553 .046 < .0001 .824 .040 .191 .224 .330
Note: Data presented as percent (n/n). Calculated by means of chi-square or Fischer exact test. a P< .05 compared with white group. b P< .01 compared with white group. c P< .0001 compared with white group. McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
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402.e1
Department of Obstetrics and Gynecology and b Department of Public Health Sciences, University of Chicago, Chicago; Department of Obstetrics and Gynecology, North Shore University Health System, Evanston; and d Fertility Centers of Illinois, Chicago, Illinois c
Objective: To evaluate the impact of race on in vitro fertilization (IVF) outcomes. Design: Retrospective analysis. Setting: Private practice. Patient(s): All women who underwent a first autologous IVF cycle at Fertility Centers of Illinois from January 2010 to December 2012. Intervention(s): Information was collected on baseline characteristics, cycle parameters, and outcomes. Race was self-reported. Main Outcome Measure(s): Clinical intrauterine pregnancy and live birth rates. Result(s): A total of 4,045 women were included: 3,003 white (74.2%), 213 black (5.3%), 541 Asian (13.4%), and 288 Hispanic women (7.1%). A multivariable logistic regression was performed to control for confounders. Compared with white women, the adjusted odds ratio for clinical intrauterine pregnancy was 0.63 (95% confidence interval [CI] 0.44–0.88) in black women, 0.73 (95% CI 0.60–0.90) in Asian women, and 0.82 (95% CI 0.62–1.07) in Hispanic women. The adjusted odds ratio for live birth was 0.50 (95% CI 0.33–0.72) in black women, 0.64 (95% CI 0.51–0.80) in Asian women, and 0.80 (95% CI 0.60–1.06) in Hispanic women compared with white women. The spontaneous abortion rate was 14.6% in white women versus 28.9% in black women, 20.6% in Asian women, and 15.3% in Hispanic women. Conclusion(s): Black and Asian women had lower odds of clinical intrauterine pregnancy and live birth and higher rates of spontaneous abortion compared with white women. Further research is needed to better characterize the mechanisms associated with this racial disparity and to improve treatment options for black Use your smartphone and Asian women. (Fertil SterilÒ 2015;104:398–402. Ó2015 by American Society for Reproducto scan this QR code tive Medicine.) and connect to the Key Words: Racial disparity, infertility, in vitro fertilization Discuss: You can discuss this article with its authors and with other ASRM members at http:// fertstertforum.com/mcqueend-racial-disparities-ivf-outcomes/
R
esearch on predictors of in vitro fertilization (IVF) success is an area of concentrated interest. Factors known to be associated with IVF outcomes include age, ovarian reserve, oocyte quality, body mass index, endometrial receptivity, and male factors (1). In recent years, there have been several publications that suggest racial disparities in IVF outcomes. The study of racial disparity is complex
and subject to a considerable number of confounders, including socioeconomic status. A large data set with a heterogeneous patient population is needed to reach meaningful conclusions, and therefore several studies on this topic have used the Society of Assisted and Reproductive Technology (SART) data set. In 2006, Purcell et al. analyzed the SART dataset and included 25,843 white and 1,429 Asian
Received January 27, 2015; revised May 10, 2015; accepted May 11, 2015; published online June 11, 2015. D.B.M. has nothing to disclose. A.S. has nothing to disclose. S.M.L. has nothing to disclose. E.C.F. has nothing to disclose. M.L.U. has nothing to disclose. Supported by the University of Chicago Department of Obstetrics and Gynecology. Presented as a poster at the American Society for Reproductive Medicine Meeting, Honolulu, Hawaii, October 18–22, 2014. Reprint requests: Meike L. Uhler, M.D., Fertility Centers of Illinois, 1S224 Summit Avenue, Ste. 302, Oakbrook Terrace, Illinois 60181 (E-mail: [email protected]). Fertility and Sterility® Vol. 104, No. 2, August 2015 0015-0282/$36.00 Copyright ©2015 American Society for Reproductive Medicine, Published by Elsevier Inc. http://dx.doi.org/10.1016/j.fertnstert.2015.05.012 398
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women (2). After controlling for several confounders, Asian ethnicity was found to be an independent risk factor for worse outcomes with an adjusted odds ratio (OR) for live birth of 0.76 (95% confidence interval [CI] 0.66– 0.88). In 2007, Seifer et al. performed an analysis of the same SART data set, focusing on IVF outcomes in black women (3). There were 3,666 black and 68,606 white women included in the analysis. The relative risk of not achieving a live birth was found to be 1.21 in black women compared to white women. These findings were confirmed by several other studies that have also used the SART database (4, 5). A major criticism of these SART database studies is that there are wide differences in IVF success rates among clinics. It has also been argued VOL. 104 NO. 2 / AUGUST 2015
Fertility and Sterility® that minority access to care may be limited to clinics with worse outcomes. A study conducted in a single IVF program would therefore have the advantage of being able to better control for confounders and may eliminate some of the differences in access to care for minority patients. One such single-site study was conducted by Feinberg et al. evaluating IVF outcomes in the military setting, with service members of all ranks and races having equal access to care (6). This study revealed no statistical difference in the live birth rate between black women (29.6%) and white women (35.8%). These findings suggested that eliminating access to care issues might lessen differences in outcomes. However, because there was a trend toward worse outcomes among black women it is possible that even though the study had the highest number of minority patients in any published single-site study, it still may not have been adequately powered to detect differences. A significant challenge for single-site studies is lack of an adequate sample size, and previously published single-site studies have included only 27–197 minority women (7–11). Fertility Centers of Illinois (FCI) is a large private practice in the Chicago area that has ten offices in diverse neighborhood settings and performs more than 3,000 IVF cycles annually. Illinois is one of 15 states with mandated insurance coverage for IVF, and Illinois law allows for four cycles of IVF to achieve a first live birth. More than 80% of all patients at FCI have at least partial insurance coverage, and access to care is increased greatly by the state mandate. Chicago is racially diverse, and therefore FCI is an excellent candidate for a single-site study. The objective of the present research was to perform a comprehensive review of IVF outcomes data in a racially diverse private practice setting. Specifically, the primary goal was to evaluate the impact of race on IVF outcomes. We hypothesized that with increased access to care and uniform treatment by a single IVF program, outcome disparities would be reduced.
MATERIALS AND METHODS Study Design Institutional Review Board (IRB) approval was granted by New England IRB. Women who underwent their first autologous fresh IVF cycle from January 2010 to December 2012 were included in the analysis. To limit heterogeneity among participants, donor oocyte cycles, oocyte vitrification, and embryo banking cycles were excluded. Additionally, all cycles for preimplantation genetic diagnosis were excluded. Information was collected on baseline characteristics, as well as IVF cycle parameters and outcomes. Race was self-reported and included categories developed by SART. Women who self-reported race as black, Asian, Hispanic, or white were included in the analysis, and women reporting more than one race were excluded. A clinical pregnancy was defined as an intrauterine gestational sac visible on ultrasound after the 6th week of pregnancy. Clinical pregnancy rate was defined as the proportion of women with an intrauterine gestational sac among all women who received IVF stimulation. Live birth rate was defined as the proportion of women whose IVF treatment VOL. 104 NO. 2 / AUGUST 2015
was followed by the birth of one or more living infants. Spontaneous abortion rate was the proportion of women with a fetal loss before 20 weeks among those women with a clinical intrauterine gestation. Multiple pregnancy rate was defined as the proportion of women with more than one live born infant among all women with a clinical intrauterine gestation. Outcomes in each racial group were compared with all other groups and with white women as a reference.
Data Analysis Statistical analysis was performed with the use of R software version 3.0.1. To assess the contribution of race to IVF outcome, a multivariable logistic regression analysis was performed to control for age, body mass index (BMI), day 3 FSH levels, smoking status, and primary infertility diagnosis. The adjusted and unadjusted ORs are reported with 95% CIs to indicate statistical precision. To account for missing values, a multiple imputation technique was used based on an iterative regression imputation. Data on antim€ ullerian hormone (AMH) and number of embryos transferred were missing for a significant portion of the subjects; therefore, rather than perform imputation for those variables, we excluded them from the regression. This should not have affected our results, because there was no clinically significant difference in AMH or number of embryos transferred across the races. Continuous variables were compared with the use of Student t test. Categoric variables were compared with the use of chisquare test and Fischer exact test. A two-sided P value of < .05 was considered to be statistically significant.
RESULTS Clinical information was collected on 4,155 consecutive women presenting for their first autologous IVF cycle. In this group, 110 women were excluded: 66 (1.6%) of unknown race, 12 (0.3%) American Indian or Alaskan Native, 15 (0.4%) Native Hawaiian or Pacific Islander, and 17 (0.4%) who selfreported multiple races. Information on the race of the partner was not collected. Data from the remaining 4,045 women were analyzed: 3,003 white (74.2%), 213 black (5.3%), 541 Asian (13.4%), and 288 Hispanic women (7.1%). Although mean age was similar among Hispanic, Asian, and white women, black women were slightly older than white women (36.0 vs. 35.2 years; P¼ .02; Table 1). BMI was significantly higher in black and Hispanic women (27.9 and 27.6 kg/m2, respectively) compared with white women (25.1 kg/m2). Asian women had a significantly lower BMI (23.3 kg/m2). Black women were significantly more likely to have tubal factor or uterine factor as their primary infertility diagnosis compared with white women. Hispanic women were also significantly more likely to have tubal factor as their primary diagnosis (Supplemental Table 1, available online at www.fertstert.org). All other baseline characteristics were similar between groups. There were several differences noted during IVF stimulation and embryo transfer between black and white women. Although the response to stimulation and number of oocytes retrieved were similar, black women had fewer mature oocytes, fewer fertilized oocytes, fewer day 5 transfers, fewer 399
ORIGINAL ARTICLE: ENVIRONMENT AND EPIDEMIOLOGY
TABLE 1 Group characteristics (n [ 4,045). Characteristic Mean age (SD), y Mean day 3 FSH (SD), IU/L Mean AMH (SD), ng/mL Mean BMI (SD), kg/m2 Smokers Mean no. of embryos transferred (SD)
White (n [ 3,003)
Black (n [ 213)
Asian (n [ 541)
Hispanic (n [ 288)
P value
35.2 (4.6) (n ¼ 3,003) 10.3 (7.7) (n ¼ 2,974) 2.2 (3.0) (n ¼ 1,282) 25.1 (5.8) (n ¼ 3,003) 9.4% (n ¼ 2,720) 1.9 (0.7) (n ¼ 2,298)
36.0 (5.0) (n ¼ 213) 10.2 (7.8) (n ¼ 211) 2.0 (2.4) (n ¼ 79) 27.9 (6.0)d (n ¼ 213) 5.2%c (n ¼ 202) 2.1 (0.8)c (n ¼ 150)
34.9 (4.5) (n ¼ 541) 9.6 (6.3)c (n ¼ 526) 2.4 (2.8) (n ¼ 232) 23.3 (4.3)d (n ¼ 541) 3.0%d (n ¼ 525) 1.9 (0.7) (n ¼ 416)
34.7 (5.0) (n ¼ 288) 8.8 (4.8)d (n ¼ 281) 2.3 (2.5) (n ¼ 129) 27.6 (6.3)d (n ¼ 288) 9.4% (n ¼ 261) 2.0 (0.8) (n ¼ 216)
.006a .002a .676a < .0001a < .0001b .033a
c
Note: AMH ¼ antim€ ullerian hormone; BMI ¼ body mass index. a Calculated by means of analysis of variance. b Calculated by means of chi-square test. c P< .05 compared with white group. d P< .0001 compared with white group. McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
surplus blastocysts for cryopreservation, and higher cancellation rates compared with white women (Table 2). Outcomes in black women were markedly worse compared with white women. The clinical pregnancy rate was significantly lower (24.4% vs. 36.2%; P¼ .001) and the spontaneous abortion rate significantly higher (28.9% vs. 14.6%; P¼ .01). Black women were less likely to have a multiple pregnancy (7.7% vs. 21.9%; P¼ .02) compared with white women. Most important, the live birth rate among black women was almost half that of white women (16.9% vs. 30.7%; P< .0001; Table 3). Racial disparities were present, but not as marked, in the Asian population. Asian women required a longer duration of stimulation (10.3 vs. 9.9 days; P¼ .001), had a higher mean peak E2 level, had fewer oocytes retrieved, and had fewer surplus blastocysts available for cryopreservation (1.5 vs. 2.0; P< .0001) compared with white women (Table 2). The clinical pregnancy rate was significantly lower (31.4% vs. 36.2%; P¼ .04) in Asian than in white women, and the spontaneous abortion rate was similar (20.6% vs. 14.6%; P¼ .059). The live birth rate among Asian women was significantly lower than in white women (24.0% vs. 30.7%; P¼ .002; Table 3). Outcomes in Hispanic women were similar to those in white women. Despite having a higher cancellation rate, His-
panic women had similar clinical pregnancy rates (34% vs. 36%; P¼ .50), spontaneous abortion rates (15.3% vs. 14.6%; P¼ .97), and live birth rates (28.5% vs. 30.7%; P¼ .48) compared with white women (Table 3). Pregnancy outcomes were significantly worse in both black and Asian populations. The crude ORs, without adjustment for confounders, were calculated to evaluate the odds of clinical intrauterine pregnancy and live birth among black, Asian, and Hispanic women compared with white women. In black women, the unadjusted OR for clinical intrauterine pregnancy was 0.56 (95% CI 0.41–0.78), in Asian women 0.81 (95% CI 0.66–0.98), and in Hispanic women 0.91 (95% CI 0.70–1.17) compared with white women. In black women, the unadjusted OR for live birth was 0.45 (95% CI 0.31–0.66), in Asian women 0.72 (95% CI 0.58– 0.88), and in Hispanic women 0.90 (95% CI 0.69–1.17) compared with white women. A multivariable logistic regression analysis was performed to evaluate the odds of both clinical intrauterine pregnancy and live birth while controlling for age, BMI, day 3 FSH, smoking, and primary infertility diagnosis. In black women, the adjusted OR for clinical intrauterine pregnancy was 0.63 (95% CI 0.44– 0.88), in Asian women 0.73 (95% CI 0.60–0.90), and in
TABLE 2 IVF and pregnancy outcomes (n [ 4,045). Outcome Stimulation (d), mean (SD) Peak E2, mean (SD) Ocytes retrieved (n), mean (SD) Matured oocytes, % Fertilized oocytes, % Day 5 embryo transfer, % Vitrified embryos (n), mean (SD) Cancellations, %
White (n [ 3,003) 9.9 (1.9) 2,388.6 (1,145.5) 13.6 (8.3) 70.8 83.0 47.9 2.0 (3.3) 13.6
Black (n [ 213) 10.0 (2.0) 2,547.4 (1,320.1) 13.7 (9.3) 65.8d 77.6d 37.1d 1.5 (3.3)c 22.0d
Asian (n [ 541) d
10.3 (2.8) 2,694.0e (1,192.8) 12.1e (6.9) 70.0 84.1 47.9 1.5 (2.5)e 13.9
Hispanic (n [ 288)
P value
9.8 (2.1) 2,521.1 (1,218.4) 13.1 (7.6) 73.1 81.4 46.2 1.7 (2.8)c 18.8c
.00034a < .0001a .0043a .0013a .0609a .0225b .0004a .001b
a
Calculated by means of analysis of variance. Calculated by means of chi-square test. P< .05 compared with white group. d P< .01 compared with white group. e P< .0001 compared with white group. b c
McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
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TABLE 3 Pregnancy outcomes (n [ 4,045). Outcome
White (n [ 3,003)
Clinical pregnancy rate Spontaneous abortion rate Multiple pregnancy rate Live birth rate
36.2 14.6 21.9 30.7
Black (n [ 213) c
Asian (n [ 541) b
31.4 20.6 21.8 24.0c
24.4 28.9c 7.7b 16.9d
Hispanic (n [ 288)
P value
34.0 15.3 19.4 28.5
.001a .0136a .1019a < .0001a
Note: Values presented as percent. a Calculated by means of chi-square test. b P< .05 compared with white group. c P< .01 compared with white group. d P< .0001 compared with white group. McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
Hispanic women 0.82 (95% CI 0.62–1.07) compared with white women. Additionally, the adjusted OR for live birth in black women was 0.50 (95% CI 0.33–0.72), in Asian women 0.64 (95% CI 0.51–0.80), and in Hispanic women 0.80 (95% CI 0.60–1.06) compared with white women (Table 4).
DISCUSSION These results show significant racial disparity in IVF outcomes. Although we controlled for multiple confounders, black and Asian women had lower clinical pregnancy rates and lower live birth rates compared with white women. There was also a significantly higher rate of spontaneous abortion among black women compared with white women. This study showed that black women had fewer mature oocytes, fewer fertilized oocytes, lower blastocyst development rates, higher cancellation rates, and higher spontaneous abortion rates compared with white women. Feinberg et al. reported a higher prevalence of leiomyomas in black women compared with white women (30.8% vs. 10.7%) and hypothesized that this may have accounted for a higher spontaneous abortion rate (6). The present data set unfortunately did not include detailed information on leiomyomas or the mean gestational age at the time of miscarriage. Interestingly, the results suggested that black women in our cohort had worse oocyte quality. This may be attributed to the significantly higher BMI in the black women. Research from Moley et al. suggests that the developmental competence of the oocyte is negatively affected by obesity (14). Moreover, high-fatdiet mouse models demonstrate oocyte mitochondrial dysfunction and spindle defects (15). Although our multivariate analysis controlled for BMI, the impact of weight on IVF
outcomes may have overarching effects that could not be isolated in this analysis. Asian women in this study were more likely to have a longer stimulation time, a greater peak E2 level, and a lower number of oocytes retrieved. Although the lower number of oocytes is suggestive of an ovarian etiology for the disparate outcomes, it is possible that the longer stimulation time and greater peak E2 may have adversely affected implantation. Elevated E2 levels created by stimulation might negatively affect endometrial receptivity. This hypothesis was supported by Fujimoto et al., who showed that Asian recipients of donor oocytes who avoided exposure to ovarian stimulation protocols and resultant high E2 levels, had similar pregnancy rates to white women (16). A future study could evaluate the impact of autologous freeze-all cycles with subsequent frozen embryo transfers in Asian women as a means of improving pregnancy rates by potentially enhancing endometrial receptivity. A strength of this study was its large sample size. The inclusion of 3,003 white, 213 black, 541 Asian, and 288 Hispanic women made this study the largest single-site study to date on racial disparities in IVF outcomes. This study is further strengthened by the high percentage of women who reported race (98.4%), with only 1.6% missing racial data. This is in contrast to the 35% of women in the SART dataset who are missing racial information. Indeed, the authors of a systematic review cautioned that firm conclusions on racial disparity can not be made from SART data, because so many practices that submitted their data to SART did not reliably report on race (12). Race was inclusively reported in our cohort, yet our findings are concordant with those of studies based on the SART database. The present study is also strengthened by the inclusion of BMI, a variable not included in previous SART analyses.
TABLE 4 Adjusted odds ratios (95% CI; n [ 4,045). Outcome Clinical pregnancy Live birth
White (n [ 3,003)
Black (n [ 213)
Asian (n [ 541)
Hispanic (n [ 288)
1.0 1.0
0.63 (0.44–0.88) 0.50 (0.33–0.72)
0.73 (0.60–0.90) 0.64 (0.51–0.80)
0.82 (0.62–1.07) 0.80 (0.60–1.06)
Note: Data presented as adjusted odds ratio (95% confidence interval). Adjustment factors: age, body mass index, day 3 FSH, smoking, and primary infertility diagnosis. McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
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ORIGINAL ARTICLE: ENVIRONMENT AND EPIDEMIOLOGY This study was limited in that we were not able to control for additional possible confounders, such as duration of infertility, doses and protocols for stimulation, quality of the embryo transferred, and potential comorbidities, including hypertension or diabetes. Additionally, we did not examine the race of the partner in this study, and the impact of race on male infertility could certainly be a subject of further research. In an effort to create homogeneity in our data, we excluded donor oocyte cycles, and future studies could examine the impact of race on donor oocyte success rates. Additionally, our study lacked data on income and socioeconomic status. The impact of socioeconomic status on IVF outcomes is complex and expands beyond access to health care. In the field of maternal fetal medicine, Geronimus et al. developed the ‘‘weathering hypothesis’’ that asserts that cumulative social stressors lead to adverse health effects and negative birth outcomes (13). It is certainly plausible that chronic stress from background disadvantage could also affect IVF success rates. In conclusion, we showed that marked racial disparities in IVF outcomes persisted even though all care was received at a single center and inequities in access were eased by statemandated insurance coverage. Multiple confounders were controlled for without a reduction in the outcomes gap. Further research is needed to confirm these findings and to better understand the underlying mechanisms associated with racial disparity so that strategies can be developed to improve treatment outcomes for black and Asian women. Acknowledgments: The authors thank the physicians, nurses, staff, and embryologists at Fertility Centers of Illinois for the excellence in patient care that made this work possible. The authors are also grateful to Dr. Ernst Lengyel at the University of Chicago for his critical reading of the manuscript and to Dr. Alicia Armstrong and Dr. James Segars for their mentorship.
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Seifer DB, Frazier LM, Grainger DA. Disparity in assisted reproductive technologies outcomes in black women compared with white women. Fertil Steril 2008;90:1701–10. Fujimoto VY, Luke B, Brown MB, Jain T, Armstrong A, Grainger DA. Racial and ethnic disparities in assisted reproductive technology outcomes in the United States. Fertil Steril 2010;93:382–90. Baker VL, Luke B, Brown MB, Alvero R, Frattarelli JL, Usadi R. Multivariate analysis of factors affecting probability of pregnancy and live birth with in vitro fertilization: an analysis of the Society for Assisted Reproductive Technology Clinic Outcomes Reporting System. Fertil Steril 2010;94: 1410–6. Feinberg EC, Larsen FW, Catherino WH, Zhang J, Armstrong AY. Comparison of assisted reproductive technology utilization and outcomes between Caucasian and African American patients in an equal-access-to-care setting. Fertil Steril 2006;85:888–94. Sharara F, McClamrock HD. Differences in in vitro fertilization (IVF) outcome between white and black women in an inner-city, university based IVF program. Fertil Steril 2000;73:1170–3. Nichols JE, Higdon HL, Crane MM, Boone WR. Comparison of implantation and pregnancy rates in African American and white women in an assisted reproductive technologies practice. Fertil Steril 2001;76: 80–4. Dayal MB, Gindoff P, Dubey A, Spitzer TL, Bergin A, Peak D. Does ethnicity influence in vitro fertilization (IVF) birth outcomes? Fertil Steril 2009;91: 2414–8. Langen ES, Shahine LK, Lamb JD, Lathi RB, Milki AA, Fujimoto VY, et al. Asian ethnicity and poor outcomes after in vitro fertilization blastocyst transfer. Obstet Gynecol 2010;115:591–6. Csokmay JM, Hill MJ, Maguire M, Payson MD, Fujimoto VY, Armstrong AY. Are there ethnic differences in pregnancy rates in African American Women versus white women undergoing frozen blastocyst transfers? Fertil Steril 2011;95:89–93. Wellons MF, Fujimoto VY, Baker VL, Barrington DS, Broomfield D, Catherino WH, et al. Race matters: a systematic review of racial/ethnic disparity in Society for Assisted Reproductive Technology reported outcomes. Fertil Steril 2012;98:406–9. Geronimus AT. Black/white differences in the relationship of maternal age to birthweight: a population-based test of the weathering hypothesis. Soc Sci Med 1996;42:589–97. Purcell SH, Moley KH. The impact of obesity on egg quality. J Assist Reprod Genet 2011;28:514–24. Grindler NM, Moley KH. Maternal obesity, infertility and mitochondrial dysfunction: potential mechanisms emerging from mouse model systems. Mol Hum Reprod 2013;19:486–94. Huddleston HG, Rosen MP, Lamb JD, Modan A, Cedars MI, Fujimoto VY. Asian ethnicity in anomymous oocyte donors is associated with increased estradiol levels but comparable recipient pregnancy rates compared with Caucasians. Fertil Steril 2010;94:2059–63.
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SUPPLEMENTAL TABLE 1 Primary infertility diagnosis (n [ 4,045). Diagnosis Diminished ovarian reserve Ovulatory Tubal Endometriosis Uterine Male factor Unexplained Unknown
White (n [ 3,003)
Black (n [ 213)
Asian (n [ 541)
Hispanic (n [ 288)
P value
22.7 (682/3,003) 17.2 (516/3,003) 3.9 (116/3,003) 3.0 (90/3,003) 1 (29/3,003) 17.7 (530/3,003) 24.2 (727/3,003) 10.4 (313/3,003)
23.4 (50/213) 9.4a (20/213) 14.6c (31/213) 3.8 (8/213) 3.3b (7/213) 19.3 (41/213) 17.9 (38/213) 8.5 (18/213)
20.1 (109/541) 19.2 (104/541) 4.1 (22/541) 3.3 (18/541) 1.0 (5/541) 13.5 (73/541) 26.8 (145/541) 12.0 (65/541)
19.4 (56/288) 17.0 (49/288) 11.5c (33/288) 3.8 (11/288) 1.4 (4/288) 16.0 (46/288) 22.9 (66/288) 8.0 (23/288)
.553 .046 < .0001 .824 .040 .191 .224 .330
Note: Data presented as percent (n/n). Calculated by means of chi-square or Fischer exact test. a P< .05 compared with white group. b P< .01 compared with white group. c P< .0001 compared with white group. McQueen. Racial disparities in IVF outcomes. Fertil Steril 2015.
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