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ORIGINAL RESEARCH |
From the Department of Obstetrics and Gynecology at the University of Iowa Roy J. and Lucille A. Carver College of Medicine, Iowa City, Iowa.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: Retrospective study of women less than 38 years of age during their first fresh IVF cycle (January 1995 to April 2005).
RESULTS: A total of 1,293 women were included in the study, with 236 obese women (body mass index [BMI] = 30–39.9) and 79 morbidly obese women (BMI 
40). The morbidly obese group had a 25.3% IVF cycle cancellation rate compared with 10.9% in normal-weight women (odds ratio 2.73, 95% confidence interval 1.49–5.0), P < .001). Morbidly obese women without polycystic ovarian syndrome had an even higher cancellation rate (33%). Women with higher BMI required significantly more days of gonadotropin stimulation but had lower peak estradiol levels (P < .001). There were no significant differences in clinical pregnancy or delivery rates between the four BMI groups. Of the women who delivered, there was a significant linear trend for risk of preeclampsia, gestational diabetes, and cesarean delivery with increasing BMI (P < .03).
CONCLUSION: We report a significantly higher risk for IVF cycle cancellation in morbidly obese patients with no effect of BMI on clinical pregnancy or delivery rate. However, obese and morbidly obese subjects had a significantly higher risk for obstetric complications. This target population should be aggressively counseled regarding their increased obstetric risk and offered treatment options for weight reduction before the initiation of fertility therapy.
LEVEL OF EVIDENCE: II-2
With the increasing prevalence of obesity, more women seeking in vitro fertilization (IVF) as a treatment for infertility are obese. The data regarding the impact of obesity on pregnancy outcomes after IVF are conflicting. A few studies have shown no effect of increasing BMI on IVF success rates, but they demonstrate higher rates of IVF cycle cancellation in overweight and obese women.13,14 In a large Dutch study, BMI greater than 27 was associated with a lower live birth rate per IVF cycle start. However, there was no significant difference when live birth rate per oocyte retrieval was compared with the normal-weight group.15 Other groups have reported decreased cumulative live birth rates after IVF. The higher rate of early pregnancy loss with increasing BMI may contribute to these findings.16 Overall, there are limited data regarding details of IVF outcome, including obstetric complications, in the strictly defined obese (BMI 30) population and no separate data for the morbidly obese (BMI 40) group. With the population of morbidly obese women increasing rapidly, it is imperative to assess the impact of morbid obesity on IVF outcomes to better counsel these women.
The primary objective of our study was to comprehensively estimate the effects of obesity and morbid obesity on IVF treatment outcomes compared with normal-weight women. We also investigated the effects of obesity on obstetric outcomes after IVF treatment. The high proportion of women with polycystic ovarian syndrome (PCOS) among the obese population may influence some of the outcomes of IVF.19 We, therefore, separately examined the outcomes of IVF in obese and morbidly obese women based on the presence or absence of PCOS.
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MATERIALS AND METHODS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Patients underwent either a standard long luteal-phase gonadotropin-releasing hormone (Gn-RH) agonist protocol or a microdose flare protocol. For the long luteal-phase Gn-RH agonist protocol, pituitary desensitization was achieved by administration of the Gn-RH agonist (leuprolide; Mallinckrodt Chemical, St. Louis, MO) from day 23 of the cycle preceding stimulation until the day of ovulation trigger. The majority of women (94.7%) used the long luteal-phase Gn-RH agonist protocol. For the microdose flare protocol, the Gn-RH agonist was administered daily starting on cycle day 2. Follicular stimulation was initiated on cycle day 3, with urinary or recombinant follicle-stimulating hormone (FSH) administered intramuscularly for 3 days. Women weighing more than 200 lb (90.7 kg) used 2-inch needles instead of 1
-inch needles. The starting dose of gonadotropin was adjusted for age, ovarian volume, or antral follicle count. Subsequent stimulation was achieved with human menopausal gonadotropins and FSH administered intramuscularly, with doses adjusted based on ovarian response as measured by estradiol levels and follicular growth by serial ultrasonograms. Human chorionic gonadotropin (hCG, 10,000 international units) was administered when at least two follicles were 18 mm or more in maximum diameter. The IVF cycle was cancelled if the estradiol level was less than 150 pg/mL on day 8 of stimulation or if there were fewer than three total follicles. For those women who underwent successful ovulation induction, length of stimulation was defined as the number of days from the first gonadotropin injection until the day of hCG administration.
Oocyte retrieval was performed by transvaginal follicular aspiration under ultrasound guidance 34 hours after hCG administration. Oocyte nuclear maturity was assessed at the time of retrieval. Oocytes were inseminated by either conventional insemination methods or ICSI, and fertilization was confirmed 14–18 hours after insemination. Fertilization rate was defined as the number of normally fertilized oocytes (diploid zygotes) divided by the number of oocytes inseminated. All embryo transfers performed before January 2000 were scheduled 72 hours after oocyte retrieval (day 3). Five or six pronuclear-stage embryos were maintained in culture for day 3 embryo transfers, and supernumerary embryos were cryopreserved at the pronuclear stage. As of January 2000, patients with 7 or more pronuclear-stage embryos were scheduled for a day 5 transfer. After confirmation of fertilization, 7–8 zygotes were maintained in culture and supernumerary zygotes were cryopreserved. Patients with fewer than 7 zygotes had all zygotes maintained in culture and were scheduled for embryo transfer on day 3. Luteal-phase support was achieved by administration of 50 mg of progesterone in oil intramuscularly daily starting on the day of oocyte retrieval.
Clinical pregnancy was defined as the presence of a gestational sac on transvaginal ultrasonography and expressed per cycle start. The implantation rate reflects the number of gestational sacs divided by the number of embryos transferred. All patients were referred for obstetric care after the observation of a viable intrauterine pregnancy by transvaginal ultrasonogram at approximately 7 weeks of gestation. Miscarriage was defined as spontaneous pregnancy loss up to 20 weeks of gestation after detection of a gestational sac and expressed per clinical pregnancy. Delivery rate was based on delivery after 20 weeks of gestation and expressed per IVF cycle start. Pregnancy complications and delivery outcome information was self-reported by patients in response to a standardized form with a self-addressed paid envelope mailed by our clinic within a month of the subject’s delivery date. The form specifically asked for details regarding first-trimester complications, obstetric complications, delivery type, and fetal outcomes. If there was no response to two reminder letters, a phone call was made by a clinic staff member.
Women were divided into BMI groups, as determined by weight and height measured at the initial IVF consultation (weight [kilograms]/height [meters]2). Body mass index groups, based on the World Health Organization and National Institutes of Health definitions, were as follows: normal weight (BMI < 25), overweight (BMI 25–29.9), obese (BMI 30–39.9), and morbidly obese (BMI 40).1,20 Women were also classified according to the cause of infertility as documented by the providing physician. These diagnosis categories included tubal factor, endometriosis, PCOS (based on National Institute of Child Health and Human Development [NICHD] criteria), male factor, unexplained, combined, and other.
We estimated our sample size based on 80% power to detect a 20% difference in clinical pregnancy rate between obese/morbidly obese women and normal-weight women (assuming a clinical pregnancy rate of 50% in normal-weight women) in a total population of 1,200 women, with morbidly obese women representing 5.5% of this population at P < .05. Data are reported as mean ± standard error. The Cochran-Armitage trend test21 or the Jonckheeere-Terpstra trend test22 was used to assess the data as a linear trend with order across all four BMI groups. The Wilcoxon rank sum test was used to evaluate differences between continuous variables and Fisher exact test and 
2 were performed for categorical variables to compare data for the morbidly obese groups with the data for the normal weight population. A trend analysis was performed for the primary outcomes over the time period of the study by using the Mantel-Haenszel 2 test. We performed multifactorial logistic regression analysis to examine the effect of BMI after adjusting for year of treatment, age, and diagnosis of PCOS on primary outcomes. Statistical significance was defined as P < .05.
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RESULTS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The detailed characteristics of the IVF cycles for all four BMI groups are shown in Table 2. We had complete data for all IVF outcomes except for two subjects did who did not provide delivery information (one normal weight and one overweight). The overall IVF cycle cancellation rate per cycle start was 11.3%, with a significantly higher cancellation rate of 25.3% in the morbidly obese group compared with normal-weight and overweight women (P < .004). Obese women had a comparable cancellation rate to that of overweight and normal-weight women. After adjusting for year of treatment, age, and diagnosis of PCOS, the odds ratio (OR) for cancellation in women with BMI of 40 or more compared with that of normal-weight women was 2.73 (95% CI 1.49–5.0). Of the 20 subjects who were cancelled in the morbidly obese group, 16 underwent a second IVF cycle using higher gonadotropin doses, and six of these cycles were again cancelled (37.5%). For the patients who did undergo oocyte retrieval, there was a significant trend toward increasing length of gonadotropin stimulation days with increasing BMI (P < .001). Despite the longer stimulation for women with increased BMI, the peak estradiol levels showed a significant linear reduction across the BMI groups (P < .001). The time required for the retrieval procedure also increased in a linear manner across the four BMI groups (P < .03), despite there being no significant difference in number of follicles aspirated in the groups. Fewer mature follicles were obtained from women with a BMI 40 or more compared with normal-weight women (P < .02). The fertilization rate and number of embryos transferred were similar among the four BMI groups. The ICSI rate was not significantly different in the four groups (range 41.4–47.2%). Because of the lower number of mature follicles, fewer embryos were frozen in the morbidly obese group although the trend was not significant. Additionally, there was no difference among the BMI groups in the proportion of patients whose embryo transfers were cancelled because of lack of fertilization or risk of ovarian hyperstimulation syndrome. However, as a reflection of their high cycle cancellation rate, women in the morbidly obese category were less likely to have an embryo transfer after initiation of ovarian stimulation than women with a BMI less than 25 (P < .001).
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The study population’s clinical pregnancy rate per cycle start was 47.6%, with no significant difference among BMI groups with regard to clinical pregnancy and embryo implantation rate (Table 3). The pregnancy rates for day 5 transfers were higher than those in day 3 transfers in all groups (overall 66.4% versus 50.7%), but the proportions of women undergoing a day 3 transfer (range 62–67%) were similar in all four groups. A trend analysis over the time period of the study showed that the clinical pregnancy rates improved significantly (P < .004). After adjusting for year of study, diagnosis of PCOS, and age with multifactorial logistic regression analysis, we did not detect a significant change in clinical pregnancy rate with BMI. The miscarriage rate was higher in the obese group than in normal-weight women, but we did not detect a similar difference with the morbidly obese group. The overall delivery or live birth rate was 41.6%. Again a trend analysis showed that the delivery rates improved over the time period of the study (P < .02). However, with multifactorial regression analysis, we did not find a change in delivery rate with BMI. Women who had a BMI of 40 or more were almost twice as likely to have a cesarean delivery (68.9%) than women with a BMI less than 25 (36%, P < .002). There was also a linear trend toward a higher risk of cesarean delivery with increasing BMI (P < .005), which persisted after adjusting for multiple gestation (P < .02, Mantel-Haenszel 2 test). Also, there was a significant trend toward increased risk of gestational diabetes (P < .01) and preeclampsia (P < .001) with increasing BMI and after adjusting for multiple gestation. Morbidly obese patients were also more likely than women with a BMI less than 25 to develop preeclampsia (21% versus 7%, P < .001) and gestational diabetes (10.3% versus 3.1%, P = .03). The risks of preterm delivery and multiple births were similar among BMI groups. The morbidly obese group had significantly higher risk for singleton fetal birth weight greater than 4,000 g than the normal-weight group (23.5% versus 9.7%, P < .05).
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Given the high prevalence of PCOS among the obese population, we compared IVF cycle outcomes for obese and morbidly obese PCOS patients with those of women who did not have PCOS (Table 4). In these two groups, 96 women were diagnosed with PCOS based on the NICHD criteria, and 219 had other infertility etiologies. The cycle cancellation rate for women with a BMI of 40 or greater who did not have PCOS was three times higher (33.3%) than the cancellation rate for the weight-matched PCOS subjects (12.9%, P < .04). These findings suggest that ovarian response to exogenous gonadotropins may be altered in obese women. Obese PCOS women had longer retrieval times, corresponding to higher numbers of follicles, compared with weight-matched subjects (P < .001). There was a threefold increased risk of overall ovarian hyperstimulation syndrome in the PCOS groups. The clinical pregnancy and delivery rates were similar in women with and those without PCOS in both BMI groups. The obstetric complications in obese and morbidly obese women with and those without PCOS are shown in Table 4.
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DISCUSSION |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Our study did not detect a significant effect of BMI on clinical pregnancy or delivery rates after one fresh cycle of IVF. Although the morbidly obese women had a slightly lower clinical pregnancy and delivery rate, these were not statistically significant. Our study population included both day 3 and day 5 transfers; however, there was a similar proportion in all four BMI groups. As mentioned in paragraph 2 above, other studies have not detected a difference in clinical pregnancy rates between obese and normal-weight women after matching for age, dose of gonadotropins, and year of treatment. Our study was not designed to examine the effects of cumulative pregnancy rates after IVF.16,18 In a large Australian study, the likelihood of achieving at least one pregnancy after assisted reproductive treatment in obese and very obese women (BMI > 35) was reported to be significantly reduced.18 Similarly, in a study from Norway, the cumulative live birth rates showed a negative trend with increase in BMI.16 However, on analysis of the first cycle only, these authors did not find a significant effect of BMI of live birth rate.
The strengths of our study include a large number of women in the obese category (n = 236), the inclusion of a separate morbidly obese group (n = 79), exclusion of women over the age of 38 years, and follow-up that included live birth and obstetric complications. We had complete data for all IVF outcomes, and only two women did not complete delivery information. The obstetric data were self-reported, but acquisition of the information soon after delivery decreases the likelihood of recall bias. We did not adjust for the effects of smoking on the clinical pregnancy rate because we had limited data (< 50%) in the earlier years of the database. The rate of current smokers in a more recent analysis in our center was only 7% and, hence, is unlikely to significantly affect the overall outcomes.
Similar clinical pregnancy rates but lower live birth rates, as reported in some studies, may be a reflection of an increased miscarriage rate.16 We detected a higher spontaneous miscarriage rate in the obese group after IVF compared with normal-weight women. This finding was not observed in the morbidly obese group and may be a reflection of the smaller group size. Our study had only 43% power to detect a 10% difference in miscarriage rates between the morbidly obese group and the normal-weight group. The data regarding the effects of obesity on miscarriage rates are controversial.12,16,24,25 Increased risk of miscarriage in women with PCOS has not been shown to be independent of obesity.24 In one study obese egg donor recipients had significantly higher miscarriage rates than normal-weight women, suggesting that oocyte quality did not contribute to the findings.26 Further, the studies that report an increased risk of miscarriage in obese subjects are not specifically designed to determine the cause of this association. Larger studies are needed, especially in the infertility population, to clearly determine the risk of miscarriage with obesity and the potential contribution of prediabetes/insulin resistance.
Mechanisms by which obesity interferes with the pathophysiology of PCOS are complex and not completely understood. Although a large number of women in the United States with PCOS are obese, it is not clear whether the reported effects of obesity on IVF outcome were independent of the effects of PCOS. The data regarding pregnancy outcomes in women with PCOS are controversial, and studies comparing PCOS women with weight-matched controls are limited.19 We, therefore, separately examined the effects of obesity, both with and without PCOS, on the outcomes of IVF. The overall cancellation rate in the non-PCOS morbidly obese women was almost three times higher than that of the PCOS women (33.3% versus 12.9%), further confirming the association between obesity and decreased ovarian response to gonadotropins. As expected, the PCOS groups had a higher risk for ovarian hyperstimulation. Overall there was no significant difference in clinical pregnancy rates, miscarriage rates, and live birth rates in these groups. A recent meta-analysis also showed similar results for clinical pregnancy rates and miscarriage rates after analyzing 9 studies comparing the outcomes of IVF in women with PCOS with that of women without PCOS.19
Our study found an increased risk of cesarean delivery in obese and morbidly obese women after IVF. The overall cesarean delivery rate is increased because of the high rate of multiple gestations in our study population. However, the cesarean delivery rate in singletons was also significantly increased in the obese and morbidly obese groups. The association between maternal BMI and cesarean delivery has been shown to be independent of fetal macrosomia.4 The same authors reported that one in seven cesarean deliveries of singleton infants was attributable to overweight and obesity. In addition, these BMI groups had a higher incidence of both gestational diabetes and preeclampsia after adjusting for multiple gestations. Our data confirm previously reported associations between obesity and obstetric complications. Analysis of a large multicenter database in the United States showed that obesity and morbid obesity had a statistically significant association with preeclampsia (ORs 1.6 and 3.3), gestational diabetes (ORs 2.6 and 4.0), and fetal birth weight greater than 4,000 g (ORs 1.7 and 1.9).27 Operative and postoperative complications in these BMI groups include increased blood loss, increased operative time, wound infections, and endometritis.28 Despite a very high response rate, our data on obstetric outcomes was self-reported and, hence, may underestimate the magnitude of the problem. Our current results highlight the obstetric risks in a population that has undergone a planned intervention to achieve pregnancy and warrants urgent attention. This is a target group that may have benefited from counseling regarding the complications of obesity in pregnancy and perhaps delaying assisted reproductive technology treatment to allow for weight loss.
The American College of Obstetricians and Gynecologists (ACOG) recommends that obstetricians provide preconception counseling and education about the specific maternal and fetal risks of obesity in pregnancy.5 Setting an initial goal of losing 5–10% of body weight over a 6-month period is realistic and achievable. The target population should include obese women seen at annual exams and also children and adolescents because childhood onset of obesity contributes to 25% of adult obesity.29 The College further recommends that referral for further evaluation and treatment should be considered when resources of the clinician are insufficient to meet the needs of obese women.30 For women with morbid obesity, a combination of medications and group lifestyle modifications results in greater weight loss than medication or lifestyle modifications alone.31 Recent studies also suggest that bariatric surgery is not associated with adverse perinatal outcomes.5 Lack of physical activity associated with obesity results in health care costs of 24 billion dollars or 2.4% of U.S. health care expenditure, whereas direct health care costs from obesity in 1995 totaled 75 billion dollars, accounting for 9.4% of the national health care expenditures in the United States.32 Not surprisingly, the epidemic of obesity seen in the pregnant population will have significant public health implications. There are currently no estimates on the economic impact of obesity on pregnancy.
In conclusion, morbidly obese women who do not have PCOS should also be counseled regarding their significantly increased risk of IVF cycle cancellation. Further studies are needed to evaluate the effects of weight loss on ovarian response to gonadotropins. However, the obstetrics risk in the obese and morbidly obese women who successfully complete an IVF cycle underscores the importance of early initiation of weight loss therapies. Once patients are referred for IVF treatment, acceptance of weight loss therapies that require delay in childbearing is difficult. Discussion initiated by primary physicians should also make women aware that some IVF centers do not offer treatment to women with a BMI greater than 35. We recommend that obese and morbidly obese women be strongly counseled regarding the importance of weight reduction and offered effective strategies during preconception visits and before initiation of an infertility work-up.
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Footnotes |
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Corresponding author: Anuja Dokras, MD, PhD, Department of Obstetrics and Gynecology, University of Iowa, 200 Hawkins Drive, Iowa City, IA 52242; e-mail: anuja-dokras{at}uiowa.edu.
doi:10.1097/01.AOG.0000219768.08249.b6
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REFERENCES |
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