Timing of Oocyte Retrieval and Embryo Transfer with Pregnancy Duration

Abstract

Background:

Recent studies have suggested that assisted reproductive technology (ART) may be associated with a shorter pregnancy duration, possibly due to various aspects of the ART procedure. The purpose of this study was to examine whether pregnancy duration is affected by timing of oocyte retrieval and embryo transfer with respect to the first day of the last menstrual period (LMP) among pregnancies achieved through in vitro fertilization with or without intracytoplasmic sperm injection.

Methods:

A retrospective study was conducted at an academic center in Norfolk, Virginia, with analyses based on 294 ART cycles.

Results:

Median and interquartile range for pregnancy duration was estimated at 38.2±3.4 weeks. Similarly, median and interquartile ranges for days between LMP and day of oocyte retrieval (27.0±2.0) and between LMP and embryo transfer (29.8±2.2) differed significantly from the standard of 14 days. Timing of oocyte retrieval and embryo transfer with respect to LMP were accelerated among multiple compared with single gestations. For single gestations, pregnancy duration was positively associated with time duration between LMP and embryo transfer (β=0.14, p=0.036). The number of days between oocyte retrieval and embryo transfer was marginally associated with a shorter pregnancy duration in women with multiple gestations (β=−3.70, p=0.083). Controlling for patient characteristics, timing of oocyte retrieval and embryo transfer were not significantly associated with pregnancy duration.

Conclusions:

With few exceptions, timing of oocyte retrieval or embryo transfer did not affect pregnancy duration among ART-conceived live births.

Introduction

Assisted reproductive technology (ART), which include in vitro fertilization (IVF) and intracellular sperm injection (ICSI), are procedures that entail the handling of human gametes outside of the body for the express purpose of creating a pregnancy.^1,2 During an ART cycle, multiple steps are taken, which include ovarian stimulation, oocyte retrieval, fertilization in a liquid medium, embryo selection, and embryo transfer into a uterine environment.^3,4 ART has been associated with adverse pregnancy outcomes including a shortened pregnancy duration, which may be partly attributed to various aspects of the procedures.^5,6

Pregnancy duration, also known as gestational age, is generally defined as the number of completed weeks between the first day of the last normal menstrual period (LMP) and the date of delivery.⁷ For naturally conceived deliveries, the exact timing of ovulation, fertilization, and implantation resulting in clinical pregnancy is frequently unknown and cannot be controlled by clinical practitioners. For ART-conceived deliveries, pregnancy duration may be partly explained by various aspects of the ART procedure, including the timing of oocyte retrieval and embryo transfer with respect to the LMP date. These aspects of the ART procedure are often known precisely and controlled by clinical practitioners. Therefore, timing of oocyte retrieval and embryo transfer could potentially be manipulated to improve ART-associated pregnancy outcomes.

The purpose of this study was to examine whether pregnancy duration is affected by timing of oocyte retrieval and embryo transfer with respect to the LMP date, among live-born infants conceived through ART. First, we characterized variation in the time durations between LMP and oocyte retrieval and between LMP and embryo transfer in the context of a clinical population of live-born infants conceived through IVF with or without ICSI. Second, we estimated these time periods according to selected patient characteristics. Third, we evaluated whether pregnancy duration was influenced by time durations between LMP, oocyte retrieval, and embryo transfer.

Materials and Methods

Data source

A retrospective study was conducted at a major fertility treatment center located in Norfolk, Virginia. Demographic, diagnostic, treatment, and outcomes data were obtained on ART cycles from a clinical database. Patient identifiers recorded in this clinical database were requested to establish a list of subjects whose data could be linked with an Excel sheet (“baby book”) that stores data on all live-born infants conceived through ART at the center. The clinical database, which includes cycle number, patient name, age at cycle initiation, LMP date, date of oocyte retrieval, hours to embryo transfer, type of gestation, and pregnancy outcome, was linked to the baby book, which contains patient's name, date of delivery, and other newborn data obtained through follow-up phone calls. Subjects were included in the study if they had achieved a pregnancy and delivered at least one live-born infant after fresh nondonor IVF/ICSI treatment cycle initiated between January 1, 1998, and December 31, 2006. Published data from the Society for Assisted Reproductive Technologies indicate that, in 2003, pregnancy, live birth, and miscarriage/stillbirth rates per fresh nondonor cycle at this fertility treatment center were 31.1%, 25.2%, and 5.8%, respectively. Additionally, subjects were excluded from the study if no record linkage could be established between the clinical database and the baby book or if they had missing data on key variables, namely LMP date, date of oocyte retrieval, hours to embryo transfer, and date of delivery. Study procedures were approved by an institutional review board.

Measures

LMP date, date of oocyte retrieval, and hours to embryo transfer were obtained from the clinical database and the date of delivery was obtained from the baby book. The outcome of interest was pregnancy duration defined as LMP-based gestational age. Accordingly, LMP date was subtracted from the date of delivery and the resulting number of days was subsequently converted to completed weeks of gestation. The main exposures of interest were timing of oocyte retrieval and embryo transfer with respect to LMP date.

Accordingly, the number of days between LMP date and date of oocyte retrieval and the number of days between LMP date and date of embryo transfer were computed. We further assessed the number of days between oocyte retrieval and embryo transfer (number of hours to embryo transfer divided by 24) as a secondary exposure. We evaluated whether the main outcome and exposures varied according to patient characteristics, namely age (<30 years; 30–34 years;>34 years), infertility diagnosis (male, endometriosis, anovulatory, other), and type of gestation (single, multiple). The same patient characteristics were considered as potential confounders and/or effect modifiers when evaluating hypothesized exposure–outcome relationships.

Statistical analysis

All analyses were conducted using SAS version 9.2 (SAS Institute, Inc.). Kruskal–Wallis test was used to compare pregnancy duration across levels of patient characteristics. Wilcoxon's signed rank test was used to evaluate whether median differences between (1) LMP date and date of oocyte retrieval and (2) LMP date and date of embryo transfer were equal to a standard value of 14 days, before and after stratifying by patient characteristics. Regression models were constructed to assess whether median differences differed by patient characteristics. Next, we constructed regression models for predicting LMP-based gestational age by (1) the difference between date of oocyte retrieval and LMP date (minus 14 days); (2) the difference between date of embryo transfer and LMP date (minus 14 days); and (3) the difference between embryo transfer and oocyte retrieval dates. These analyses were performed before and after stratifying by patient characteristics. Finally, multivariate regression models were constructed to evaluate hypothesized exposure–outcome relationships after adjustment for patient age, infertility diagnoses, and type of gestation. Because of the potential for outliers, median regression (PROC QUANTREG) rather than ordinary least squares (PROC REG) models were constructed. Two-sided statistical significance was assessed at α level of 0.05.

Results

A total of 480 ART cycles (IVF with or without ICSI) that resulted in live births were initiated at the clinic between January 1, 1998, and December 31, 2006. All cycles had a known LMP date, whereas one (0.2%) had a missing date of oocyte retrieval from the clinical database and 182 (37.9%) did not have self-reported date of delivery recorded in the baby book. There were no missing data on the number of hours between oocyte retrieval and embryo transfer. We compared patient characteristics of the 298 ART cycles with known dates to the 182 IVF cycles with unknown dates. No group differences were noted with respect to age, infertility diagnosis, or type of gestation (data not shown). An additional four cycles were excluded because their LMP date was not biologically plausible. Thus, our analyses were restricted to a sample of 294 ART cycles. The mean (±standard deviation) patient age at ART cycle initiation was 33.4 (±4.1), ranging from 23 to 42 years. The distribution of ART cycles by patient age was as follows: <30 years (18.4%), 30–34 years (38.4%), and ≥35 years (43.2%). Similarly, the distribution of ART cycles by infertility diagnosis was as follows: male (53.2%), endometriosis (17.6%), anovulatory (9.7%), and other (19.4%). Of 294 ART cycles, 70.4% resulted in single births and 29.6% resulted in multiple births.

The median (±interquartile range) pregnancy duration was 38.2 (±3.4) weeks, ranging from 23.9 to 44.7 weeks (Fig. 1A). Whereas 66.6% of ART cycles resulted in term deliveries (≥37 weeks), 33.3% resulted in preterm (<37 weeks) deliveries. Pregnancy duration differed significantly according to type of gestation (single: 38.8±2.0 weeks vs. multiple: 35.6±4.3 weeks; Kruskal–Wallis test; p<0.0001). In contrast, pregnancy duration did not differ according to patient age or infertility diagnosis (data not shown).

FIG. 1.

(A) Histogram of pregnancy duration in weeks (N=294). (B) Histogram of number of days between last menstrual period and oocyte retrieval minus 14 days (N=294). (C) Histogram of number of days between last menstrual period and embryo transfer minus 14 days (N=294). (D) Histogram of number of days between oocyte retrieval and embryo transfer (N=294).

Table 1 describes timing of oocyte retrieval with respect to the LMP date and its relationship with patient characteristics. The number of days between the first day of the last menstrual cycle and the day of oocyte retrieval minus the standard value of 14 days ranged between 11 and 16 days, with a median of 13 days and an interquartile range of 2.0 days (Fig. 1B). This time duration did not differ by patient age or infertility diagnosis. When compared with single gestations, multiple gestations were associated with a marginally significant reduction in time between LMP date and oocyte retrieval (12.0±2.0 vs. 13.0±2.0; β_m=−1.00, p=0.052).

Table 1.

Number of Days Between First Day of Last Menstrual Period and Day of Oocyte Retrieval Minus 14 Days by Patient Characteristics

	N (%)	Median±IQR ^a	p^b	β1 (SE1), p1 ^c
Overall	294 (100)	13.0±2.0	<0.0001	—
Patient age (years)
<30	54 (18.4)	13.0±3.0	<0.0001	Reference
30–34	113 (38.4)	13.0±2.0	<0.0001	−0.00 (0.35), 1.00
≥35	127 (43.2)	13.0±2.0	<0.0001	−0.00 (0.33), 1.00
Infertility diagnosis
Male	115 (53.2)	13.0±1.0	<0.0001	Reference
Endometriosis	38 (17.6)	13.0±2.0	<0.0001	0.00 (0.20), 1.00
Anovulatory	21 (9.7)	13.0±3.0	<0.0001	−0.00 (0.57), 1.00
Other	42 (19.4)	13.0±1.0	<0.0001	−0.00 (0.29), 1.00
Type of gestation
Single	207 (70.4)	13.0±2.0	<0.0001	Reference
Multiple	87 (29.6)	12.0±2.0	<0.0001	−1.00 (0.51), 0.052

IQR, interquartile range.

Significance level of Wilcoxon's signed-rank test comparing the number of days between first day of last menstrual period and day of oocyte retrieval to a hypothetical value of 14 days.

β1, median regression slope coefficient; SE1, standard error of β1; p1, significance level associated with β1.

Table 2 describes timing of embryo transfer with respect to the LMP date and its relationship with patient characteristics. The number of days between the first day of the last menstrual cycle and the day of embryo transfer minus the standard value of 14 days ranged between 13.8 and 18.9 days, with a median of 15.8 days and an interquartile range of 2.0 days (Fig. 1C). This time duration did not differ by patient age or infertility diagnosis. When compared with single gestations, multiple gestations were associated with significantly decreased time between LMP date and embryo transfer (14.9±2.0 vs. 15.8±2.0; β_m=−0.83, p=0.023).

Table 2.

Number of Days Between First Day of Last Menstrual Period and Day of Embryo Transfer Minus 14 Days by Patient Characteristics

	N (%)	Median±IQR	p^a	β1 (SE1), P1 ^b
Overall	294 (100)	15.8±2.0	<0.0001	—
Patient age
<30	54 (18.4)	15.8±2.9	<0.0001	Reference
30–34	113 (38.4)	15.8±1.4	<0.0001	−0.00 (0.29), 1.00
≥35	127 (43.2)	15.8±2.0	<0.0001	0.00 (0.25), 1.00
Infertility diagnosis
Male	115 (53.2)	15.7±1.3	<0.0001	Reference
Endometriosis	38 (17.6)	15.8±2.0	<0.0001	0.063 (0.29), 0.83
Anovulatory	21 (9.7)	15.9±3.0	<0.0001	0.13 (0.59), 0.83
Other	42 (19.4)	15.8±1.9	<0.0001	−0.00 (0.27), 1.00
Type of gestation
Single	207 (70.4)	15.8±2.0	<0.0001	Reference
Multiple	87 (29.6)	14.9±2.0	<0.0001	−0.83 (0.36), 0.023

Significance level of Wilcoxon's signed-rank test comparing the number of days between first day of last menstrual period and day of embryo transfer to a hypothetical value of 14 days.

β1, median regression slope coefficient; SE1, standard error of β1; p1, significance level associated with β1.

Table 3 presents median regression models for the time periods between LMP date and oocyte retrieval (minus 14 days) and the time period between LMP date and embryo transfer (minus 14 days) as predictors of pregnancy duration, before and after stratifying by patient characteristics. Overall, pregnancy duration was not significantly associated (p>0.05) with the time elapsing between LMP date and oocyte retrieval or between LMP date and embryo transfer. Similar findings were obtained after stratifying by patient age and infertility diagnosis. However, a significantly positive association was observed between timing of embryo transfer and pregnancy duration among single (but not multiple) births (β_m=0.14, p=0.036).

Table 3.

Median Regression Models for Number of Days Between First Day of Last Menstrual Period and Days of Oocyte Retrieval or Embryo Transfer (Minus 14 Days) as a Predictor of Total Pregnancy Duration by Patient Characteristics

		Median regression
	N	Ovulation induction ^a β (SE), p	Embryo transfer ^b β (SE), p
Overall	294	0.071 (0.13), 0.58	0.094 (0.12), 0.45
Patient age
<30	54	0.11 (0.20), 0.60	0.11 (0.19), 0.57
30–34	113	−0.18 (0.23), 0.44	−0.24 (0.22), 0.29
≥35	54	0.17 (0.18), 0.35	0.17 (0.16), 0.29
Infertility diagnosis
Male	115	0.048 (0.26), 0.86	0.051 (0.25), 0.84
Endometriosis	38	0.072 (0.22), 0.74	0.24 (0.22), 0.28
Anovulatory	21	−0.26 (0.38), 0.49	−0.27 (0.34), 0.44
Other	42	0.14 (0.37), 0.70	0.00 (0.35), 1.00
Type of gestation
Single	207	0.14 (0.077), 0.065	0.14 (0.065), 0.036
Multiple	87	−0.048 (0.28), 0.86	−0.32 (0.28), 0.27

Number of days between first day of last menstrual period and day of oocyte retrieval.

Number of days between first day of last menstrual period and day of embryo transfer; β, slope coefficient; SE, standard error of β; p, significance level associated with β. Stratum-specific models are not adjusted for other covariates of interest.

Table 4 presents median regression models for number of days between oocyte retrieval and embryo transfer as a predictor of pregnancy duration, before and after stratifying by patient characteristics. The number of days between oocyte retrieval and embryo transfer ranged between 0.9 and 4.8 days, with a median of 2.8 days and an interquartile range of 0.1 days (Fig. 1D). Overall, pregnancy duration was not significantly associated (p>0.05) with the number of days between oocyte retrieval and embryo transfer. However, after stratifying by patient characteristics, a marginally significant inverse relationship was observed among women having multiple gestations (β_m=−3.70, p=0.083).

Table 4.

Median Regression Models for Number of Days Between Oocyte Retrieval and Embryo Transfer as a Predictor of Total Pregnancy Duration by Patient Characteristics

	n	Ovulation induction to embryo transfer ^a median regression β (SE), p
Overall	294	0.15 (0.52), 0.77
Patient age
<30	54	0.16 (1.35), 0.90
30–34	113	0.16 (1.48), 0.91
≥35	54	−0.57 (0.77), 0.46
Infertility diagnosis
Male	115	−0.68 (0.71), 0.33
Endometriosis	38	3.01 (2.24), 0.19
Anovulatory	21	−0.78 (5.51), 0.88
Other	13	−1.14 (2.26), 0.61
Type of gestation
Single	207	−0.084 (0.33), 0.79
Multiple	87	−3.70 (2.11), 0.083

Number of days between oocyte retrieval and embryo transfer. β, slope coefficient; SE, standard error of β; p, significance level associated with β. Stratum-specific models are not adjusted for other covariates of interest.

Table 5 presents median regression models for the hypothesized relationships after adjustment for patient age, infertility diagnosis, and type of gestation. Clearly, timing of oocyte retrieval, timing of embryo transfer, and the number of days between oocyte retrieval and embryo transfer were not significantly associated with pregnancy duration in multivariate regression models. In these models, type of gestation was the only significant predictor of pregnancy duration (data not shown).

Table 5.

Multiple Regression Models for Predictors of Total Pregnancy Duration

	Total pregnancy duration median regression ^a β (SE), p
Model I: ovulation induction^b	0.071 (0.084), 0.39
Model II: embryo transfer^c	0.072 (0.094), 0.44
Model III: ovulation induction to embryo transfer^d	0.084 (0.37), 0.82

β, slope coefficient; SE, standard error of β; p, significance level associated with β.

All regression models are adjusted for patient age, infertility diagnosis, and type of gestation.

Number of days between first day of last menstrual period and day of oocyte retrieval (minus 14 days).

Number of days between first day of last menstrual period and day of embryo transfer (minus 14 days).

Number of days between oocyte retrieval and embryo transfer.

Discussion

In this study, we characterized the time duration between LMP, oocyte retrieval, and embryo transfer and how it may affect pregnancy duration in the context of an ART-conceived population. Our results can be summarized as follows:

1. LMP generally preceded oocyte retrieval by approximately 27 days and embryo transfer by approximately 30 days.

2. Timing of oocyte retrieval and embryo transfer with respect to the LMP date were accelerated among multiple gestations.

3. Stratified analyses suggest that extended time duration between the first day of the last menstrual period and embryo transfer was associated with increased pregnancy duration among single births.

4. The number of days between oocyte retrieval and embryo transfer was negatively but marginally associated with pregnancy duration among women delivering multiple births.

5. Pregnancy duration was unaffected by variations in timing of oocyte retrieval or embryo transfer, after adjustment for patient age, infertility diagnoses, and type of gestation.

It is worth noting that ART populations represent a selected group of women and their live-born infants. Compared with the general population, women who conceive through ART are substantially older and more likely to experience multiple gestations and preterm deliveries. The 2005 National Vital Statistics Reports estimates mean maternal age to be consistently less than 28 years, with multiple gestations affecting 3%–4% of all mothers. Additionally, preterm delivery affects 12% of all live births in the United States.⁸ In this study, mean maternal age (33 years), multiple gestation rate (29.6%), and preterm delivery rate (33.3%) estimates were considerably higher than those in the general population of the United States. Therefore, study findings cannot be extrapolated to a broader population of pregnant women who conceived naturally or through ART.

Whereas dates of oocyte retrieval and embryo transfer are accurately measured in ART populations, accuracy of the LMP date is dependent on the infertile patient's ability to recall past events for both naturally and ART-conceived live births. In a study by Wegienka and Baird,⁹ data on 385 women ages 35–49 years were used to construct menstrual segments from a prospective daily menstrual record and compare the first day of a menstrual segment to a woman's recollected LMP date at a subsequent clinic appointment. More than half of the women (56%) accurately recalled their LMP date, 74% were within 1 day, and 81% were within 2 days. Women tended to underreport (25%) the length of time since their LMP rather than over-report the length of time (19%).⁹ Nevertheless, women who undergo ART procedures are often concerned about achieving a pregnancy and are closely monitored by their health-care practitioners, thus reducing the potential for recall issues.

A 2-week interval between the first day of the last menstrual period and an ovulatory event is assumed for natural conceptions but may not be applicable in the context of ART populations whereby ovulation is replaced with oocyte retrieval. The observed difference between LMP date and dates of oocyte retrieval and embryo transfer is not unexpected in the context of an ART population. In fact, controlled ovarian hyperstimulation (COH) for oocyte recruitment is not determined by the same physiologic processes that dictate potential for spontaneous ovulation and conception. Rather, oocyte recruitment by COH is determined by combinations of medications used, dosing of those medications, and any underlying disorders of ovulation including anovulation and amenorrhea due to either hypothalamic hypogonadism or polycystic ovary syndrome that may be indications for a patient to undergo ART procedures. Consequently, the length of time needed for oocyte retrieval in the ART process often depends on nuances of the COH.

The finding that an extended time between oocyte retrieval and embryo transfer may be detrimental to the health of ART-conceived infants has been previously reported through nationwide ART surveillance systems.^2,10 Since the birth of the first IVF-conceived U.S. infant in 1981, use of these treatments has increased dramatically and the number of medical centers providing ART has steadily increased over the years. In 1992, Congress passed the Fertility Clinic Success Rate and Certification Act, which requires each medical center in the United States that performs ART to report annually to the Centers for Disease Control and Prevention (CDC) on every ART procedure initiated.^2,10 In general, women who undergo ART are more likely to deliver multiple-birth infants than those who conceive naturally. Multiple births are associated with increased health risks for mothers and infants, including preterm delivery. ART procedures are sought by patients with a wide range of infertility diagnoses, namely tubal factor, ovulatory dysfunction, diminished ovarian reserve, endometriosis, uterine factor, male factor, other causes, unexplained cause, and multiple factors.^2,10 Other patient characteristics that can influence ART success include patient age, number of previous ART procedures, and number of previous births.^2,10 ART characteristics include the use of ICSI, number of days of embryo culture, and number of embryos transferred.^2,10 In 2006, a total of 138,198 ART procedures were reported to the CDC; 44% of these procedures resulted in a pregnancy and 36% in a live-birth delivery.^2,10 Of 54,656 infants born through ART, 48% were multiple-birth deliveries, and the risk of multiple births varied according to patient's age, type of ART procedure, number of embryos available for transfer, number of embryos transferred, and day of transfer (day 3 or 5).^2,10 Preterm delivery rates were 14%, 65%, and 97% among ART singletons, twins, and triplets, respectively.^2,10 Our findings are consistent with the idea that prolonged embryo culture can increase the likelihood of multiple birth, thereby, reducing pregnancy duration.^2,10 Further studies are needed to establish whether the observed stratum-specific relationships between prolonged embryo culture and pregnancy duration according to type of gestation are valid or merely chance findings.

Knowledge of pregnancy duration is critical for identifying preterm delivery, a condition of multi-factorial etiology and an important cause of perinatal morbidity and mortality.^11,12 So far, a limited number of studies have examined timing of oocyte retrieval and embryo transfer as determinants of ART success.^13,14,15 To our knowledge, this study is the first to examine timing between LMP, oocyte retrieval, and embryo transfer in relation to pregnancy duration among ART-conceived live births. Our study findings should, nevertheless, be interpreted with caution and in light of several limitations. First, the study was conducted at one academic institution, limiting sample size and generalization in terms of racial, ethnic, and socioeconomic factors to other institutions within the United States. Second, the low variability in the difference between LMP, oocyte retrieval, and embryo transfer may be an artifact due to treatment protocols that are typical of ART populations. Third, missing data on date of delivery resulted in incomplete record linkage between the clinical database and the baby book, potentially leading to selection bias. Fourth, for women who conceive through ART and deliver after a planned cesarean section or induction of labor, pregnancy duration may be completely determined by this obstetric procedure, which was not assessed in this study. Fifth, stratified analyses by patient characteristics were exploratory in nature and cannot be ruled out as chance findings due to sample size limitations. Finally, reliance of existing data precluded adjustment for other important demographic, socioeconomic, lifestyle and health characteristics that may affect pregnancy duration.

Conclusions

With few exceptions, the timing of oocyte retrieval or embryo transfer does not seem to have an effect on overall pregnancy duration among ART-conceived infants. Further research is needed to better elucidate preterm delivery risk in the context of various aspects of the ART procedure.

Footnotes

Acknowledgments

We would like to thank Ms. Debi Jones from the Jones Institute of Reproductive Medicine for providing us with a listing of potentially eligible patients.

Disclosure Statement

No competing financial interest exists.

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