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Julien J. Stirnemann, 1 Department of Obstetrics and Maternal Fetal Medicine , Hôpital Necker-Enfants Malades, AP-HP, Université Paris Descartes , Paris , France 2 Applied Mathematics and Statistics, MAP5, UMR CNRS 8145 , Université Paris Descartes , Paris , France *Correspondence address. Maternité et médecine materno-foetale, GHU Necker-Enfants Malades, 149 rue de Sèvres, 75015 Paris, France. Tel: +33-1-44-49-40-30; Fax: + 33-1-44-49-40-18 ; E-mail: Search for other works by this author on: Adeline Samson,2 Applied Mathematics and Statistics, MAP5, UMR CNRS 8145 , Université Paris Descartes , Paris , France Search for other works by this author on: Jean-Pierre Bernard,1 Department of Obstetrics and Maternal Fetal Medicine , Hôpital Necker-Enfants Malades, AP-HP, Université Paris Descartes , Paris , France 3 Centre Européen de Diagnostic et d'Exploration de la Femme (C.E.D.E.F.), Le Chesnay , France Search for other works by this author on: Jean-Christophe ThalabardJean-Christophe Thalabard 2 Applied Mathematics and Statistics, MAP5, UMR CNRS 8145 , Université Paris Descartes , Paris , France 4 Centre de Diagnostic, Hôtel-Dieu , AP-HP, Université Paris Descartes , Paris , France Search for other works by this author on: Revision received: 28 November 2012 Accepted: 07 December 2012 Published: 22 January 2013
Close Navbar Search Filter Microsite Search Term Search AbstractSTUDY QUESTION When, within the female cycle, does conception occur in spontaneously fertile cycles? SUMMARY ANSWER This study provides reference values of day-specific probabilities of date of conception in ongoing pregnancies. The maximum probability of being within a 5-day fertile window was reached on Day 12 following the last menstrual period (LMP). WHAT IS KNOWN ALREADY The true date of conception is not observable and may only be estimated. Accuracy of these estimates impacts on obstetric management of ongoing pregnancies. Timing of ovulation and fertility has been extensively studied in prospective studies of non-pregnant fertile women using error-prone proxies, such as hormonal changes, body-basal temperature and ultrasound, yielding day-specific probabilities of conception and fertile windows. In pregnant women, date of conception may be retrospectively estimated from early pregnancy fetal measurement by ultrasound. STUDY DESIGN, SIZE, DURATION Retrospective analysis of consecutive pregnancies in women referred for routine first-trimester screening, over a 3-year period (2009–2011) in a single ultrasound center (n = 6323). PARTICIPANTS/MATERIALS, SETTING, METHODS Within the overall population, 5830 cases with a certain date of last menses were selected for analysis. The date of conception was estimated using a crown-rump length biometry and an equation derived from IVF/ICSI pregnancies. Day-specific probabilities of conception were estimated across several covariates, including age, cycle characteristics and ethnicity, using deconvolution methods to account for measurement error. MAIN RESULTS AND THE ROLE OF CHANCE Overall, the day-specific probability of conception sharply rises at 7 days after the LMP, reaching its maximum at 15 days and returning to zero by 25 days. Older women tend to conceive earlier within their cycle, as did women with regular cycles and white and black women compared with Asian ethnicity. The probability of being within the fertile window was 2% probability at Day 4, a maximum probability of 58% at Day 12 and a 5% probability by Day 21 of the cycle. LIMITATIONS, REASONS FOR CAUTION Although conception is believed to occur within hours following ovulation, a discrepancy is theoretically possible. However, when comparing our results to those of prospective studies, no such difference was found. The equation used for estimating the date of pregnancy was estimated in IVF/ICSI pregnancies, which could lead to potential bias in spontaneous pregnancies. However, in our population, the observed bias was negligible. Non-fertile cycles and early pregnancy losses are necessarily overlooked because of the nature of our data. WIDER IMPLICATIONS OF THE FINDINGS Because of the wider access to retrospective data and the potential bias in prospective studies of ovulation monitoring, this study should broaden the perspectives of future epidemiologic research in fertility and pregnancy monitoring. STUDY FUNDING/COMPETING INTERESTS None. IntroductionExcept in the specific case of assisted reproduction technologies (ART), such as IVF or ICSI, the exact date of conception is unknown. Although ovulation generally occurs at around 14 days following the first day of last menses, a wide variation in the timing of ovulation has been found in prospective studies. Such studies generally rely upon hormonal changes (Wilcox et al., 1995, 2000; Dunson et al., 1999, 2001; Behre et al., 2000; O'Connor et al., 2006; Venners et al., 2006; Cole et al., 2009) and physiological changes, such as basal body temperature (Royston, 1982; Royston et al., 1984; Dunson et al., 1999) or ultrasound (Queenan et al., 1980; Marinho et al., 1982; Luciano et al., 1990; Ecochard et al., 2001), to detect ovulation in healthy non-pregnant women monitored intensively in an experimental setting. However, although some methods may be more accurate than others, any indirect method aiming to detect ovulation or conception is prone to measurement error (Dunson and Weinberg, 2000; Dunson et al., 2001; Lynch et al., 2006). In pregnant women, the date of conception may be estimated from early fetal growth using sonographic biometry (Robinson, 1973). This method has been proved more reliable than last menstrual period (LMP) for dating the onset of pregnancies (Gardosi et al., 1997; Mongelli and Gardosi, 1997; Gardosi and Geirsson, 1998; Mustafa and David, 2001) and most national guidelines now consider early biometry as the method of choice for dating conception in routine practice (NICE, 2008; ACOG, 2009). However, dating of conception using first trimester biometry remains an indirect observation of conception and therefore prone to error due to measurement error or biological variability in growth dynamics (Smith et al., 1998, 2002). Prospective estimation of date of ovulation in fertile women and retrospective estimation of date of conception in pregnant women are closely related since conception occurs within hours following ovulation, if ever (Royston, 1982; Wilcox et al., 1995). Therefore, in pregnant women, the true day of conception may be safely considered as the true day of ovulation, although neither one is directly observed. Therefore, day-specific probabilities of conception are defined as the probability that conception occurs on a given day of the cycle (Lynch et al., 2006), provided the cycle is fertile (see Supplementary datafor a formal presentation). Since a cycle may either be non-fertile or lead to an early loss, day-specific probabilities of conception should not be interpreted as the overall probability of clinical pregnancy. Precise knowledge of the timing of conception, however, has important clinical implications: (i) for counseling regarding fertility. In this context, hormonal ovulation monitoring methods have been made commercially available to help optimize the chances of conception (Behre et al., 2000). (ii) For the follow-up of pregnancies regarding growth monitoring, screening for birth defects and management of delivery. With regard to these clinical implications, the objective of this study is to provide estimates of day-specific probabilities of conception in fertile cycles, using ultrasound fetal biometry in the first trimester as a proxy in a large cohort of spontaneous singleton pregnancies. A specific statistical method is used to take into account the measurement error inherent to ultrasound estimates of date of conception (Comte et al., 2011; Stirnemann et al., 2012). The estimated distribution allows the calculation of the day-specific probability that conception occurs within a ‘fertile window’, as defined by Wilcox et al. (2000). MethodsPopulation and data collectionGeneral inclusion criteriaThe overall population comprised all consecutive pregnancies referred for a routine first trimester ultrasound, over a 3-year period (2009–2011) in a single ultrasound screening center. In this center, women either self-refer or are referred by another practitioner without restriction regarding gestational age or indication. However, women are scheduled at around 12 weeks following LMP unless otherwise requested. General exclusion criteriaAll multiple pregnancies were excluded as well as patients referred on the basis of a specific condition (i.e. second-line examination, threatened miscarriage, acute pelvic pain or bleeding, fever or abnormal vaginal discharge). Pregnancies originating from ART were also excluded as their cycles may be disturbed by infertility treatment. No further selection was made on the basis of ultrasound findings or measurements. Therefore, the study population is an unselected sample from the general population of spontaneous singleton pregnancies ongoing in the first trimester at 11–14 weeks. For the analysis of day-specific probabilities, patients with an unknown or uncertain date of LMP were excluded as well as those with amenorrhea or recent (<3 months) pregnancy, breastfeeding or prior contraception use without return to normal cycles. In addition, an ancillary sample was composed of all the ongoing pregnancies originating from non-donor, non-frozen egg IVF or ICSI within the initial population. This ancillary sample was used for estimating a dating equation based upon a crown-rump length (CRL), as explained later. Demographic characteristics as well as information regarding cycle characteristics were collected upon referral and recorded prospectively. All the data, including demographic characteristics, medical records and ultrasound results, were stored in a dedicated database (Astraia GmbH, Germany). Within this population, a proportion of women had an additional early first-trimester ultrasound on parental demand for psychological reassurance prior to the routine fetal assessment at 11–14 weeks. This subgroup of patients with two observations was handled specifically in the course of statistical modeling. No approval from the Institutional Review Board was required for this study. Ultrasound measurementsAll ultrasound examinations were performed according to French national guidelines (CTE, 2005) and according to the guidelines of the Fetal Medicine Foundation (FMF, 2012). Dating of pregnancy was based upon CRL. All ultrasound examinations were performed using a Voluson E8 (General Electric, GE Medical System Europe, Buc, France). Quality control of ultrasound measurements is routinely performed in this pregnancy screening center and was ongoing throughout the study period, using standardized imaging quality assessments and scoring, statistical checks and external audits. Ultrasound measurements together with the corresponding covariates were collected under the responsibility of an obstetrician (J.P.B.) as part of the routine follow-up and were stored in a clinical database with the patient's consent. The database was secondarily accessed only by J.P.B., who extracted anonymously the routine data, which were retrospectively analyzed in the present study. All the data were manipulated according to the French regulation on both protection of privacy (law #2004-801,08/06/2004) and biomedical research (law# 2004-806, 08/08/2004). Unbiased ultrasound predictions of date of pregnancyAll published reference dating equations displayed some bias when tested in the spontaneous conception as well as in the IVF/ICSI population. Although overall bias was found to be as small as 0.5 days with some equations—which is consistent with previous reports (Sladkevicius et al., 2005)—it would have strongly hampered the final estimation of day-specific probabilities. Therefore, to rule out the impact of ultrasound prediction bias, in a preliminary analysis we estimated a new dating equation based upon the IVF/ICSI data set comprising 286 pregnancies with a median CRL of 63.6 mm [interquartile range (IQR) = 55.1–68.8]. The date of IVF/ICSI fertilization was considered as the date of conception. The final predictive model was the following equation with fetal age in days and CRL in mm, estimated using fractional polynomials (Royston and Sauerbrei, 2008) (Supplementary data, SA): (1) Statistical analysis and correction for error-in-measurementThe first day of the menstrual cycle was defined by the onset of menstrual bleeding. The date of pregnancy predicted from ultrasound measurements of CRL was considered as a noisy observation of the true underlying date using an additive noise model given by equation (1), Z = X + ɛ, where Z is the observed time interval between LMP and the predicted date of pregnancy based upon CRL measurement, X is the unknown true time interval between LMP and true date of conception, i.e. without measurement error and ɛ is an unknown error. The probability distribution function (p.d.f.) of X (true time since LMP) was estimated using non-parametric deconvolution methods that are described elsewhere (Comte et al., 2011; Stirnemann et al., 2012). The assumptions regarding the distribution of the error ɛ were checked (Supplementary data, SB). This estimation algorithm makes use of the repeated measurements in the subset of pregnancies with an early first-trimester additional ultrasound to yield a smooth estimation of the error-free p.d.f. of X. The estimated distribution provides day-specific probabilities in fertile cycles defining the probability that a given day of the cycle is the true date of conception. Day-specific probabilities were calculated according to cycles reported as regular or irregular, according to maternal age group and ethnicity. Finally, in the overall population, we used the previous estimation of day-specific probabilities to calculate the probability that a given day of the cycle falls within a ‘fertile window’, defined by the probability that a given day of the cycle falls within the 5-day window preceding conception (Wilcox et al., 1995, 2000). All analyses were implemented in R v2.15.0 (R Development Core Team), using the ‘deamer’ library. ResultsOver the study period, 6323 women were referred for a routine ultrasound examination with a singleton spontaneous pregnancy. In this population, women reported their LMP with certainty in 5830 (92%) cases. In 397 (6%) cases, women were uncertain or could not remember the date of their last menses. In 96 (2%) cases, the present pregnancy occurred shortly after a previous pregnancy, interruption of contraception or amenorrhea without return to normal cycles. Only women with a certain date of LMP were selected for further analysis. The demographic characteristics of this population are presented in Table I. Table I Demographic characteristics of the study population (n = 5830).
Results are presented as n (%) unless otherwise specified. IQR, inter-quartile range. Table I Demographic characteristics of the study population (n = 5830).
Results are presented as n (%) unless otherwise specified. IQR, inter-quartile range. Routine ultrasound examinations were performed at a median of 86 days following LMP (or equivalently 12 weeks and 2 days, IQR = 85–89 days). Within the study population, 939 women had an additional early first-trimester ultrasound for psychological reassurance prior to the scheduled 11–14 weeks routine ultrasound. In this subgroup, the first ultrasound was performed at a median of 57 days (IQR = 51–64 days) following LMP. This subgroup was used to correct for measurement error in the estimation of day-specific probabilities (Supplementary data, SB). Figure 1 presents the error-free estimates of day-specific probabilities of conception in fertile cycles across the female cycle in the overall population. This distribution is right skewed, showing a sharp rise from 7 days onwards, reaching its maximum of 13% at 15 days and decreasing to zero by 25 days following LMP. Figure 1 Day-specific probabilities of conception in fertile cycles in the overall population. LMP, last menstrual period. Maternal ageDay-specific probabilities in fertile cycles were calculated for the three groups of maternal age presented in Table I. Figure 2 shows that the distribution is narrower and that pregnancies occur earlier in women aged >35 years. The maximum probability occurred at 15 days for women aged <25 years and at 14 days for women aged >25 years. Furthermore women aged <25 years displayed more variation with higher probabilities of onset of pregnancy around 21 days. Figure 2 Day-specific probabilities of conception in fertile cycles according to maternal age (years). Characteristics of female cyclesWithin the group with certain date of LMP, 5035/5830 (86%) reported regular cycles and 795/5830 (14%) reported irregular cycles. Compared with women with reportedly regular cycles, women with irregular cycles displayed more variation in timing of onset of pregnancy (Fig. 3), with an increased likelihood of pregnancies occurring later in the cycle. Figure 3 Day-specific probabilities of conception in fertile cycles according to menstrual cycle characteristics. EthnicityLittle difference in the day-specific probabilities of conception was found across ethnic groups as demonstrated by the overlap of distributions in Fig. 4. However, white women were found to have the least variable dates of conception, whereas Asian women displayed the greatest variability, mostly due to later onset of pregnancies in their third week. Figure 4 Day-specific probabilities of conception in fertile cycles according to ethnicity. Smoking status did not show any significant difference regarding the distribution of day-specific probabilities (data not shown). A numerical table of the day-specific probabilities plotted in Figs 1–4 is provided in Supplementary data, Table SB. Probability of falling within the fertile windowThe fertile window was defined by the 5 days preceding the day of conception. Figure 5 displays the probability that a given day of the cycle falls within this fertile window for each day of the cycle in the overall population. The probability of being within a fertile window rises from 2% on Day 4 onwards and reaches 58% by Day 12. By Day 21, the probability falls down to 5%. Figure 5 Day-specific probabilities of being within the ‘fertile window’ (the 5-day window preceding conception). DiscussionUsing retrospective data from pregnant women for estimating day-specific probabilities of conception in fertile cyclesThis study provides reference values for the probability that conception occurs on a given day of the cycle, provided the cycle is fertile. A formal presentation of the relationship between day-specific probabilities in prospective and retrospective designs is presented in Supplementary data. Although our results are similar to prospective studies of timing of ovulation (Wilcox et al., 1995, 2000; Dunson et al., 1999, 2001; O'Connor et al., 2006; Venners et al., 2006), they differ in several ways: (i) we were interested in the date of conception rather than ovulation. A discrepancy in timing is likely although of little clinical relevance since fertilization is believed to occur within hours following ovulation (Royston, 1982; Wilcox et al., 1995). Therefore, in our study, the day-specific probabilities of conception are a close approximation of the day-specific probabilities of ovulation estimated in a sample of fertile cycles leading to a clinical pregnancy; (ii) since we considered only pregnant women, our results are obviously conditional on the occurrence of a clinical pregnancy ongoing throughout the first trimester. Therefore, by design, only fertile cycles were selected, necessarily overlooking potentially non-fertile cycles. However, it has been hypothesized that the timing of ovulation does not impact on fertility nor on the probability that a given cycle will yield a pregnancy (Wilcox et al., 2000). Conversely, the same authors suggest a relationship between late implantation and early pregnancy loss (Wilcox et al., 1999). This effect is also overlooked by design in our study. Fetal biometry as a proxy for estimating the date of conceptionUsing fetal biometry as a proxy for determining day-specific probabilities may raise concerns regarding potential bias and magnitude of measurement error compared with previously used hormonal tests. Moreover, we used IVF/ICSI pregnancies to determine a dating equation, which could further limit the application of our dating equation, given the long-standing debate regarding growth disorders associated with IVF/ICSI (Dumoulin et al., 2010; Le Bouc et al., 2010; Eaton et al., 2012). However, this dating method showed negligible bias (−0.02 day) in spontaneous pregnancies within the time frame of first-trimester ultrasound. Furthermore, the magnitude of the error (SD = 1.52 day) was similar to reported precisions of urinary hormonal detection of ovulation in optimal experimental settings (see Supplementary data, SB) (Dunson et al., 1999; O'Connor et al., 2006). Comparison with the results of prospective studiesMost studies aiming to determine the timing of ovulation involve intensive longitudinal monitoring of women using study-specific diagnostic methods, which is likely to induce some selection bias. In contrast, our study uses routine cross-sectional clinical observations in a general population setting. Therefore, our results are less likely to be prone to selection bias or to any impact of follow-up design on measurements, especially since observations are performed only after natural conception occurring outside a research setting. Furthermore, this allows for much larger samples and easier access to data than prospective experimental studies. Regardless of these differences, our findings regarding the timing of the fertile window closely match those of previous reports. Indeed, our estimates (Fig. 5) are strikingly similar to those reported by Wilcox et al. (2000): the maximum probability was reached by Day 12, displaying a probability of 58% compared with the 54% probability reported by Wilcox et al. (2000). However, whereas our results showed a probability of <1% by Day 28 and onward, Wilcox et al. (2000) found a 4–6% probability remaining in the fifth week. Two independent hypotheses are likely to explain this difference: (i) the estimates given by Wilcox et al. (2000) are not corrected for measurement error and a biased error (i.e. the mean error is not zero) could cause such an effect and (ii) it may also be hypothesized that these late ovulations are non-fertile or at high risk of early pregnancy loss and therefore excluded in our data. Our results regarding the effect of maternal age and ethnicity are also consistent with previous reports showing a shortening of cycle length in women aged >35 years and a longer cycle in Asian women compared with white women (Liu et al., 2004), although we acknowledge the difference between groups is small. Our results are also consistent with Wilcox et al. (2000), showing that conception occurs relatively later in women with reportedly irregular cycles compared with women with reportedly regular cycles. Clinical implications and relevance for epidemiology studiesWe wish to emphasize that achieving a description of the physiological variability in onset of pregnancy using simple routine clinical data in a large-scale sample should help to broaden the perspectives of future research regarding the understanding of the relationship between physiological characteristics and fertility. Furthermore, with regard to the clinical implications of dating accuracy discussed in the Introduction section, this study yields measurement-error free values for day-specific probabilities of conception according to several covariates which should be useful for fertility counseling as well as for dating pregnancy. In the context of fertility counseling, considering day-specific probabilities of conception rather than day-specific probabilities of ovulation may appear as a more pragmatic and clinically relevant concept since it rules out the association between timing of ovulation and fertility and the association between timing of ovulation and early pregnancy loss. In the context of obstetric management of pregnancy, our results could help practitioners in refining the estimated date of pregnancy given by an early pregnancy ultrasound measurement. Reporting the date of conception predicted by a CRL equation within a table of day-specific probabilities provides some measure of the likelihood that this estimate, derived from an ultrasound measurement, is actually the true date of conception. Furthermore, reference values provided in Supplementary data, Table SB would allow prenatal care-providers to implement maternal characteristics, such as age, cycle characteristics and ethnicity, in their appraisal of the most likely date of conception. Authors' rolesJ.J.S. initiated the study, analyzed the data, interpreted the results and wrote the manuscript. A.S. participated in the statistical analysis of the data and reviewed the manuscript. J.-P.B. leads the screening center and made the data available. He participated in the design as well as in the interpretation of the results. J.-C.T. initiated the study, actively participated in the analysis and the interpretation of the results. He reviewed all versions of the manuscript. FundingNo external funding was either sought or obtained for this study. Conflict of interestNone declared. AcknowledgementsWe thank Pr. Bouyer (Inserm, CESP, UMRS 1018 Université Paris Sud) for his insightful comments and his critical help in reviewing the final manuscript. We thank Pr. Ville (Obstetrics and Maternal—Fetal Medicine, Hôpital Necker-Enfants Malades, APHP and Université Paris Descartes) for his help in establishing the rationale for this study. ReferencesACOG (American Congress of Obstetricians and Gynecologists) Practice Bulletin No. 101: ultrasonography in pregnancy , Obstet Gynecol , 2009 , vol. 113 2 Pt 1 (pg. 451 - 461 ) , , , , , , . Prediction of ovulation by urinary hormone measurements with the home use ClearPlan Fertility Monitor: comparison with transvaginal ultrasound scans and serum hormone measurements , Hum Reprod , 2000 , vol. 15 (pg. 2478 - 2482 ) , , . 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More from Oxford Academic How likely is it to get pregnant on your most fertile day?If she has sex five days before she ovulates, her probability of pregnancy is about 10 percent. If she has sex on the day of ovulation, or the two days before, the chance of getting pregnant is around 30 percent. These are average figures and depend on a woman's age.
Can you get pregnant any day in your fertile window?As shown in the graph, conception is only possible from about five days before ovulation through to the day of ovulation. These six days are the “fertile window” in a woman's cycle and reflect the lifespan of sperm (five days) and the lifespan of the egg (24 hours).
Should you try everyday during fertile window?Couples who tried to get pregnant were previously told to have sex once every other day during their fertile days. But studies have shown you can improve your chances if you have sex once a day every day (as long as his sperm are OK) during the fertile 4-5 days prior to, and the day of, ovulation.
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Chances of getting pregnant each day of fertile window
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