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Hum. Reprod. Advance Access originally published online on September 25, 2006
Human Reproduction 2007 22(2):407-413; doi:10.1093/humrep/del374
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© The Author 2006. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Time to pregnancy and multiple births

R.M. Ferrari1, M.A. Cooney2, A. Vexler3, A. Liu3 and G.M. Buck Louis2,4

1 Department of Maternal and Child Health, University of North Carolina at Chapel Hill, Chapel Hill, NC 2 Epidemiology Branch and 3 Biometry Branch, National Institute of Child Health and Human Development, Rockville, MD, USA

4 To whom correspondence should be addressed at: Epidemiology Branch, National Institute of Child Health and Human Development, 6100 Executive Blvd., Room 7B03, Rockville, MD 20852, USA. E-mail: louisg{at}mail.nih.gov


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
BACKGROUND: Mothers of multiples are alleged to be more fecund than mothers of singletons. Some authors have suggested monitoring twinning rates for assessing temporal changes in a population’s reproductive health. METHODS: Using a nested case-control design, we estimated the odds of a multiple birth in relation to fecundity in the US Collaborative Perinatal Project inclusive of 8546 pregnant women who reported a known time-to-pregnancy (TTP) upon enrolment in the cohort, 1959–1966. Case mothers comprised 81 women giving birth to twins/triplets; control mothers comprised 243 women giving birth to singletons matched to case mothers on maternal age at a ratio of 3:1. The odds ratio (OR) for a multiple birth within 6 months of trying adjusting for maternal age and prior pregnancies was estimated using logistic regression. Discrete time Cox regression analysis was also utilized to estimate the fecundability OR. RESULTS: Women with a TTP of ≤6 months were more likely to have a multiple birth than women reporting a TTP of >6 months [OR = 1.95; 95% confidence interval (95% CI) = 1.09–3.51]. Excluding pregnancies after 13+ months resulted in a loss of precision (OR = 2.14; 95% CI = 0.90–5.04). CONCLUSIONS: These data support higher fecundity among mothers of multiples than mothers of singletons.

Key words: fecundity/multiple births/time-to-pregnancy/twinning


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
Twin and higher order conceptions remain an intriguing reproductive end-point with the implicit promise of enhancing our understanding of human reproduction and development. Biologic and/or environmental mechanisms underlying spontaneous twinning remain largely unknown save for a few demographically established population factors such as parental ages and race/ethnicity (Bulmer, 1970Go; Allen, 1977Go). Individual level determinants of twinning are reported to include familial history (Parazzini et al., 1994Go; Lichtenstein et al., 1996Go) including a woman’s prior history of multiple births (Eriksson, 1990Go). Dizygotic (DZ) twinning is also associated with non-white race and increasing maternal age and reproductive history as measured with gravidity or parity (Ventura et al., 1999Go). Monozygotic (MZ) twinning is typically considered a random reproductive event with a relatively stable prevalence (Derom et al., 1995Go; Hur et al., 1995Go; Dunn and Macfarlane, 1996Go). Currently, MZ twinning is being investigated in relation to genetic susceptibility or predisposition, given the 2-fold increased risk in MZ twin birth rates among women receiving ovulation-inducing medications (Derom et al., 1987Go) and, more recently, by assisted hatching techniques aimed at enhancing implantation rates during assisted reproductive technology (Schieve et al., 1999Go).

With growing worldwide speculation that human fecundity is declining (Toppari et al., 1996Go), tools for monitoring a population’s reproductive health are needed for the early identification of toxicants detrimental to human reproduction and development. Joffe (2003)Go and Olsen and Rachootin (2003)Go have suggested using time-to-pregnancy (TTP) as a proxy of fecundity for monitoring reproductive health, although other authors challenge the feasibility of this approach (Sallmen et al., 2005Go). Some authors have suggested using twinning rates to monitor the reproductive health of populations, in part, given its rarity and ease of identification (James, 1982Go). Tong and Short (1998)Go have suggested monitoring the ratio of DZ/MZ twins, given that the former may reflect environmental factors and is, thereby, subject to greater population variation in comparison to relatively stable MZ twinning rates. These approaches are feasible provided that multiple pregnancies can be qualified and quantified with regard to the use of fertility-related treatment. The secular increase in the use of ovulation-inducing agents has resulted in a marked increase in multiple births (Derom et al., 1995Go; Schieve et al., 1999Go; Reynolds et al., 2003Go), as has the transfer of multiple embryos, challenging researchers’ ability to correctly categorize multiple births for surveillance of reproductive and/or developmental toxicants. A few countries such as Denmark are able to perform linkage studies to identify populations of children conceived with or without fertility-related treatments for aetiologic research purposes. In the United States, plurality of birth is included on birth certificates, but only a few states are currently capturing fertility-related treatments.

The purpose of this article is to assess fecundity of mothers by plurality of birth, an important component for understanding how twinning may be used for population-based monitoring of reproductive health. A second aim is to stimulate renewed interest in the determinants of twinning (or higher order births) in particular with regard to zygosity and the absence of fertility-related treatment. Such cumulative research efforts will be informative for answering questions about environmental reproductive and/or developmental toxicants.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 Acknowledgements
 References
 
Study population and sample
The study population comprises 48197 women enrolled into the US Collaborative Perinatal Project (CPP) upon presenting for prenatal care between 1959 and 1965 at 12 participating medical centres, i.e. Baltimore, Boston, Buffalo, New Orleans, New York (two sites), Memphis, Minneapolis, Philadelphia, Portland, Providence and Richmond. Women were recruited from obstetrical and paediatric departments of the 12 universities with added attention to ensuring the unbiased selection of women, although representative sampling was not an a priori goal of the CPP (Niswander and Gordon, 1972Go). Some clinical centres recruited all women seeking care, whereas others randomly selected women. To date, no internal selection biases have been identified (Hardy, 2003Go). There were 54390 pregnancies captured by the CPP among participating women. This included women with multiple births or those who contributed more than one singleton birth in the CPP. Women were followed throughout pregnancy, and offspring were followed through age 8 years. The original intent of the CPP was to assess the role of intrauterine events in children’s neurodevelopment. A more complete description of the original CPP is available elsewhere (Niswander and Gordon, 1972Go).

For study purposes, the sample was restricted to 8546 women who reported that the index pregnancy was planned and for whom a TTP was reported by the mother in response to the following questions asked upon enrolment:

Have you been trying to become pregnant? (yes/no)
If yes, how long did it take for you to become pregnant? (# months)

To the best of our knowledge, the CPP was the first study to define and use TTP in epidemiologic research. The large reduction in the size of the study sample reflects the preponderance of unplanned pregnancies during the time frame of the CPP study, presumably related to the limited availability of contraceptive options in the United States.

Study design
We used a nested case-control design. Case mothers comprised 80 women giving birth to twins and one woman giving birth to triplets. None of the case or control mothers contributed more than one pregnancy to the analysis. The case women represented all women in the CPP with planned pregnancies and a reported TTP and their pregnancy resulted in multiple births. Twenty-seven mothers were reported to have had MZ twins, and 38 were reported to have had DZ twins. Zygosity was determined in the CPP by an indirect method including gender, gross and microscopic examination of the placenta and analysis of nine blood type systems (ABO, MNS, Rh, P, Kell, Lewis, Lutheran, Duffy and Kidd) (Myrianthopoulos, 1975Go; Reddy et al., 2005Go). Zygosity was unknown for 15 twins largely because of death of the neonates before tests could be performed, the inability to perform placental examinations for deliveries outside participating clinical centres or subject refusal. Control mothers comprised 243 women giving birth to singletons and were selected at random and individually matched to case mothers on maternal age at the index pregnancy upon enrolment into the cohort at a ratio of 3:1.

Data analysis
All data were derived from in-person interviews with mothers at enrolment and medical records abstracted for the study. Complete data were available for most study covariates. Family history of multiple births was missing for more than half of all women and, hence, was not further considered.

Our original intent was to assess conception delay, defined as a TTP of >6 months (Cooney et al., 2006Go), and risk of multiple birth. This threshold point is supported by several prospectively performed TTP studies that report that ~80% of women becoming pregnant do so within 6 months of trying (Ellish et al., 1996Go; Gnoth et al., 2003Go; Wang et al., 2003Go). Given the potential for digit preference, we also used the empirical density function of TTP to investigate the dependence of TTP by case/control status. For the categories TTP≥3 and ≥6, we subsequently truncated TTP to 13+ months to address its potential misclassification after a long interval. We used conditional logistic regression analysis to estimate the odds ratio (OR) of a multiple birth along with 95% confidence intervals (95% CIs) adjusted for maternal age and prior pregnancies as determined on an a priori basis. Lastly, we used Cox proportional hazards model for discretely observed data to estimate the fecundity OR (FOR) defined as cycle-specific odds of conceiving among mothers of multiples versus mothers of singletons. TTP was used as a continuous variable in this analysis, and the proportional hazard assumptions were checked using log (-log) curves and adding interactions with time to the model. The assumption that the hazard ratio is constant over time was met. Confounders included prior pregnancies and maternal age.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 Acknowledgements
 References
 
Table I provides a description of the study sample by status and reflects the absence of significant differences with regard to sociodemographic characteristics, lifestyle or reproductive history. One exception is the observation that case mothers were significantly more likely than control mothers to report use of contraception at the time of conception of the index pregnancy, that is 3 and 0%, respectively (P = 0.01). A slightly higher percentage of control mothers reported having had a sterility investigation for their index pregnancy in comparison to case mothers, that is 13 and 10%, respectively, but this difference was not significant.


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  		Table I. Comparison of case and control mothers by select characteristics

 
A comparison of the maternal characteristics listed in Table I by zygosity of twin births is presented in Table II. In comparison to mothers of MZ twins, DZ twin mothers were more likely to report having a previous pregnancy (63 versus 84%, respectively, P = 0.05).


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  		Table II. Comparison of case mothers by zygosity and select characteristics

 
Figure 1 illustrates the empirical density function for TTP in relation to plurality of birth. The proportion of case mothers who became pregnant in the first 6 months is consistently higher than that of control mothers, that is 78 and 64%, respectively (P = 0.02). However, a comparable proportion of case and control mothers became pregnant within the first 12 months of trying, that is 86 and 79%, respectively (P = 0.16). The continuous distribution of TTP illustrated in Figure 1 further suggests that there may be three distinct time periods of interest for TTP—before 6 months, from 6 to 12 months and after 12 months. Figure 2 reflects a consistently higher cumulative pregnancy distribution for mothers of multiples in comparison to mothers of singletons.


Figure 1
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  		Figure 1. Distribution of time-to-pregnancy (TTP) by plurality, US Collaborative Perinatal Project 1959–1966.

 

Figure 2
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  		Figure 2. Cumulative distribution of time-to-pregnancy (TTP) by plurality, US Collaborative Perinatal Project 1959–1966.

 
Table III presents the logistic regression results by varying threshold points of TTP in relation to the odds of a multiple birth to assess the consistency of findings given the potential for digit preference in recalling and reporting. Of note is the observation that all ORs were consistently ≥1 regardless of TTP threshold point used. The FOR obtained with discrete time Cox regression analysis truncated after 13 months and adjusted for maternal age and gravidity suggested little difference by mother’s twinning status (FOR = 1.26; 95% CI= 0.96–1.66). Thus, the cycle-specific odds for pregnancy among women who had multiples were 1.26 times the cycle-specific odds for pregnancy among women who had singletons. Combined, these results suggest that fecundity may differ with regard to maternal twinning status but that the effects are largely limited to the first 6 months (or fewer) of trying to become pregnant. Zygosity data were missing for 14 women in the case group; however, Figure 3 suggests that DZ twinning may occur more frequently than MZ twinning in women who have TTPs of <4 months.


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  		Table III. Odds of multiple pregnancy by varying threshold points of time-to-pregnancy (TTP)a

 

Figure 3
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  		Figure 3. Time-to-pregnancy (TTP) by zygosity among women with planned multiple pregnancies, CPP 1959–1966. DZ, dizygotic twinning; MZ, monozygotic twinning.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
Acknowledgements
 References
 
The results of this nested case-control study suggest that fecundity is higher among women who give birth to multiples than among women giving birth to singletons as measured with self-reported TTP. An important aspect of this finding is that the difference is only observed during the first 6 months of trying to conceive. No difference was found across the entire distribution of TTP, as assessed by discrete time Cox regression analysis. This suggests that women or couples with mild underlying fecundity impairments may have both diminished fecundity as measured by TTP and a lower likelihood of conceiving multiples.

Evidence for a shorter TTP among mothers of multiples was first reported by Bulmer (1959)Go. He reported that twins were more likely than singletons to be conceived within the first 3 months of marriage. Basso et al. (2004)Go addressed the relation between TTP and twinning using the Danish National Birth Cohort. The highest odds of twinning were among women with a TTP of ≤2 months decreasing thereafter with increasing TTP. Specifically, women conceiving within 2 months had an 82% higher risk of giving birth to twins in comparison to women requiring 12+ months. The findings remained, although somewhat weaker, when women defined as having partly planned their pregnancies were included in the analysis. We attempted to corroborate these findings by classifying TTP into the following categories: ≤2, 3–5, 6–12 and >12 months. ORs for multiple birth remained consistently below 1 when the referent category was set at ≤2 months supporting a work by Basso et al. (2004)Go, although CIs included one (ORs = 0.8, 0.7 and 0.5, respectively). Now that this section of text is over two pages and separated by figures, it may not be clear to the reader that the numbers refer to the OR not confidence interval. Recently, Axmon and Hagmar (2005)Go reported that pregnancies ending in live multiple births tended to have shorter TTPs than those ending in live singleton births (FOR = 1.62; 95% CI = 1.41–2.27). These data were pooled from three Swedish studies with TTP information, and the results did not change when adjusted for confounders. Thus, our study results contribute to the limited body of evidence suggesting higher fecundity among mothers of multiple births.

Cautious interpretation of these results is needed given the observational nature of this study and our reliance on retrospectively collected TTP. This study is subject to many of the limitations associated with retrospectively reported TTP ascertained from women or couples with detected pregnancies or the so-called pregnancy-based approach (Joffe et al., 2005Go). In such scenarios, women with diminished or impaired fecundity may be underrepresented in the sampling frameworks. This has prompted investigators to seek alternative approaches for capturing unsuccessful attempts such as the current duration design (Keiding et al., 2002Go; Slama et al., 2006Go). Briefly, a cross-sectional sample of sexually active women or couples not using contraception is queried about the interval between discontinuation of contraception and interview. If desired, couples can be prospectively followed for pregnancy. We were restricted in our ability to evaluate the potential effect of subfecundity on our findings given the original design and intent of the CPP. Without exception, women who failed to become pregnant whether actively trying or not were not included in the cohort.

While women were queried about TTP upon first seeking prenatal care and before their knowledge about plurality of birth, we recognize the potential for error associated with reporting. TTP is reported to be a reliable measure when retrospectively collected even after extended periods of recall (Joffe et al., 1993Go; Nguyen and Baird, 2005Go). In addition, we have little reason to assume bias in reporting given that women did not know their twinning status upon enrolment in the CPP, which preceded the use of ultrasonography as a part of antenatal care. Consistent with earlier literature, we observed some digit preference in reporting TTP particularly for later months, i.e. 6, 12, 24 and 36 (Baird et al., 1991Go; Ridout and Morgan, 1991Go; Joffe et al., 1993Go). It is possible that our ORs are elevated because of digit preference as it was observed at 6, 12 and 24 months. However, the direction of the ORs remained above 1 even after varying the TTP threshold points. Another limitation of our study is the limited number of women who reported having planned their pregnancy and for whom a TTP (in months) was reported. The extent to which planners differ from non-planners by twinning or higher order birth status remains relatively understudied, especially at the population level. While all women were queried about a family history and whether they were a twin, family history was largely missing and only eight women (including six controls) reported having been a twin. Thus, we were unable to assess these potentially important effects. We also could not address the possibility of spontaneous reductions of multiple to singleton pregnancies, given the absence of ultrasonography in the clinical management of pregnant women during the CPP time frame. A last noteworthy limitation is our relatively crude information on zygosity, which was possibly subjected to misclassification. Despite this limitation, many of the associations observed by case status and zygosity are in the expected direction lending credence to our observed results. While provisional, there is a suggestion that women with DZ twins had a shorter TTP than women with MZ twins suggesting higher fecundity. These findings await corroboration.

The time frame of the CPP is advantageous for study purposes given that it largely preceded widespread use of fertility treatments. For example, clomiphene citrate was one of the first available medications for ovulation induction and was introduced in the United States in 1960 (Kennedy and Adashi, 1987Go). We identified only two women in our sample who reported having received clomiphene citrate, and both delivered singleton infants. As such, we have no evidence suggesting that our case status was affected by ovulation-inducing medications.

In sum, our findings provide further empirical evidence that fecundity is higher among women with multiples than women with singletons. Reasons for this heightened fecundity remain largely unknown, but careful enquiry into this area, especially with regard to zygosity, may offer promise for identifying the determinants of human fecundity and fertility. Such research will be challenged by contemporary societal behaviours such as intentionally delaying childbirth, changing paternity over a woman’s reproductive life and use of ovulation-induction agents for fertility-related treatments. Spontaneous twinning and higher order births may prove useful in assessing temporal patterns of human fecundity and fertility and offer insight into the determinants of fecundity.


   Acknowledgements
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
References
 
This research was supported by the Intramural Research Program of the National Institute of Child Health and Human Development. The authors are grateful for the comments provided on an earlier version of this paper by Drs Courtney D. Lynch and Joseph B. Stanford.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
Allen G and Nance WE. (1977) The parity effect and fertility in mothers of twins. Twin Research: Biology and Epidemiology(A.R. Liss, New York) pp. 89–97.

Axmon A and Hagmar L. (2005) Time to pregnancy and pregnancy outcome. Fertil Steril 84:966–974.[CrossRef][Web of Science][Medline]

Baird DD, Weinberg CR, Rowland AS. (1991) Reporting errors in time-to-pregnancy data collected with a short questionnaire. Am J Epidemiol 133:1282–1290.[Abstract/Free Full Text]

Basso O, Christensen K, Olsen J. (2004) Fecundity and twinning. A study within the Danish National Birth Cohort. Human Reprod 19:2222–2226.[Abstract/Free Full Text]

Bulmer MG. (1959) The effect of parental age, parity and duration of marriage on the twinning rate. Ann Hum Genet 23:454–458.[Web of Science][Medline]

Bulmer MG. (1970) The Biology of Twinning in Man(Clarendon Press, Oxford).

Cooney MA, Buck Louis GM, Klebanoff MA, Sun W, Rice MM. (2006) Is conception delay a risk factor for diminished gestation or birth weight? Paediatr Perinat Epidemiol 20:3201–209.[CrossRef][Web of Science][Medline]

Derom C, Derom R, Vlietinck R, Van den Berghe H, Thiery M. (1987) Increased monozygotic twinning rate after ovulation induction. Lancet I:1236–1238.

Derom R, Orlebeke J, Eriksson A, Thiery M. (1995) The epidemiology of multiple births in Europe. In Keith LG, Papiernik E, Keith DM (Eds.), et al. Multiple Pregnancy. Epidemiology, Gestation and Perinatal Otucome(Parthenon, New York) pp. 145–162.

Dunn A and Macfarlane A. (1996) Recent trends in the incidence of multiple births and associated mortality in England and Wales. Arch Dis Child 75:F10–F19.

Ellish NJ, Saboda K, O’Connor J, Nasca PC, Stanek EJ, Boyle C. (1996) A prospective study of early pregnancy loss. Hum Reprod 11:406–412.[Abstract/Free Full Text]

Eriksson AW. (1990) Twinning in families of triplets. Acta Genet Med Gemellol 39:279–293.[Medline]

Gnoth C, Godehardt D, Godehardt E, Frank-Herrmann P, Fredul G. (2003) Time to pregnancy: results of the German prospective study and impact on the management of infertility. Hum Reprod 18:1959–1966.[Abstract/Free Full Text]

Hardy JB. (2003) The Collaborative Perinatal Project: Lessons and legacy. Ann Epidemiol 13:303–311.[CrossRef][Web of Science][Medline]

Hur YM, McGue M, Iacono WG. (1995) Unequal rate of monozygotic and like-sex dizygotic twin birth: evidence from the Minnesota twin family study. Behav Genet 25:337–340.[CrossRef][Web of Science][Medline]

James WH. (1982) Second survey of secular trends in twinning rates. J Biosoc Sci 14:481–497.[Web of Science][Medline]

Joffe M. (2003) Invited commentary: the potential for monitoring of fecundity and the remaining challenges. Am J Epidemiol 157:89–93.[Abstract/Free Full Text]

Joffe M, Villard L, Li Z, Plowman R, Vessey M. (1993) Long-term recall of time-to-pregnancy. Fertil Steril 60:99–104.[Medline]

Joffe M, Key J, Best N, Keiding N, Scheike T, Jensen TK. (2005) Studying time to pregnancy by use of a retrospective design. Am J Epidemiol 162:115–124.[Abstract/Free Full Text]

Keiding N, Kvist K, Hartvig H, Tvede M, Juul S. (2002) Estimating time to pregnancy from current durations in a cross-sectional sample. Biostatistics 3:565–578.[Abstract]

Kennedy JL and Adashi EY. (1987) Ovulation induction. Obstet Gynecol Clin North Am 14:831–864.[Web of Science][Medline]

Lichtenstein P, Olausson PO, Kallen AJB. (1996) Twin births to mothers who are twins: a registry based study. Br Med J 312:879–881.[Abstract/Free Full Text]

Myrianthopoulos NC. (1975) Congenital malformations in twins: epidemiologic survey. Birth Defects Orig Artic Ser 11:1–39.[Medline]

Nguyen RHN and Baird DD. (2005) Accuracy of men’s recall of their partner’s time to pregnancy. Epidemiology 16:694–698.[CrossRef][Web of Science][Medline]

Niswander KR and Gordon M. (1972) The Women and Their Pregnancies(W.B. Saunders, Philadelphia).

Olsen J and Rachootin P. (2003) Monitoring fecundity over time – if we do it, then let’s do it right [Invited Commentary]. Am J Epidemiol 157:94–97.[Abstract/Free Full Text]

Parazzini F, Villa A, Moroni S, Tozzi L, Restelli S. (1994) The epidemiology of multiple pregnancies. Acta Genet Med Gemellol 43:17–23.[Medline]

Reddy U, Branum A, Klebanoff M. (2005) Relationship of maternal body mass index and height to twinning. Obstet Gynecol 105:593–597.[Web of Science][Medline]

Reynolds MA, Schieve LA, Martin J, Jeng G, Macaluso M. (2003) Trends in multiple births conceived using assisted reproductive technology, United States, 1997–2000. Pediatrics 111:1159–1162 (Suppl.).[Abstract/Free Full Text]

Ridout MS and Morgan BJT. (1991) Modelling digit preference in fecundability studies. Biometrics 47:1423–1433.[CrossRef][Web of Science][Medline]

Sallmen M, Weinberg CR, Baird DD, Lindbohm ML, Wilcox AJ. (2005) Has human fertility declined over time? Why we may never know. Epidemiology 16:494–499.[CrossRef][Web of Science][Medline]

Schieve LA, Peterson HB, Meikle SF, Jeng G, Danel I, Burnett NM, Wilcox LS. (1999) Live-birth rates and multiple-birth risk using in vitro fertilization. JAMA 282:1832–1838.[Abstract/Free Full Text]

Slama R, Ducot B, Carstensen L, Lorente C, de La Rochebrochard E, Leridon H, Keiding N, Bouyer J. (2006) Feasiblity of the current-duration approach to studying human fecundity. Epidemiology 17:440–449.[CrossRef][Web of Science][Medline]

Tong S and Short RV. (1998) Dizygotic twinning as a measure of human fertility. Hum Reprod 13:95–98.[Abstract/Free Full Text]

Toppari J, Larsen JC, Christiansen P, Giwercman A, Grandjean P, Guillette LJ Jr, Jegou B, Jensen TK, Jouannet P, Keiding N, et al. (1996) Male reproductive health and environmental xenoestrogens. Environ Health Perspect 104:741–803.

Ventura SJ, Martin JA, Curtain SC, Matthews TJ. (1999) National Vital Statistics Report. 47, No. 18. 81–83.

Wang X, Chen C, Wang L, Chen D, Guang W, French J. (2003) Conception, early pregnancy loss, and time to clinical pregnancy: a population-based prospective study. Fertil Steril 79:577–584.[CrossRef][Web of Science][Medline]

Submitted on May 26, 2006; resubmitted on July 18, 2006; resubmitted on August 18, 2006; accepted on August 25, 2006.


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