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Gynecology & Obstetrics

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Annual Trend in Zygotic Twinning Rates and their Association with Maternal Age in Japan, 1999-2008

Yoko Imaizumi* and Kazuo Hayakawa

Department of Health Sciences, Graduate School of Medicine, Osaka University, Suita City, Osaka, Japan

*Corresponding Author:
Yoko Imaizumi
Professor, Department of Health Sciences
Graduate School of Medicine, Osaka University, A-1302
Kokubo 120-55, Akashi City, Hyogo Prefecture 673-0005, Japan
Tel: +81-78-928-6027
E-mail: [email protected]

Received date: October 19, 2013; Accepted date: December 02, 2013; Published date: December 09, 2013

Citation: Imaizumi Y, Hayakawa K (2013) Annual Trend in Zygotic Twinning Rates and their Association with Maternal Age in Japan, 1999-2008. Gynecol Obstet 3:189. doi:10.4172/2161-0932.1000189

Copyright: © 2013 Imaizumi Y, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

 

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Abstract

Objective: We aimed to determine the recent trend in monozygotic (MZ) and dizygotic (DZ) twinning rates and their association with maternal age (MA).

Study design: The MZ and DZ twinning rates were estimated using Japanese vital statistics from 1999 to 2008.

Results: The DZ twinning rate per 1000 deliveries increased from 5.10 in 1999 to 7.66 in 2005 and decreased thereafter (5.98 in 2008). The MZ twinning rate increased significantly with an increase in MA in 2002, 2003, 2006, and 2008. Both the DZ and overall twinning rates increased significantly with an increase in MA in each year. From 1960- 1967 to 1999-2008, the DZ twinning rates increased 280% for MA 30-34 years, 290% for MA 35-39, and 370% for MA 40 and over. On the contrary, the MZ twinning rates remained nearly constant with MA for both periods.

Conclusion: The DZ twinning rate increased till 2005 and decreased thereafter. The rate in 2005 (7.66) was 339% higher than that between 1955 and 1967 (2.26) whereas the MZ twinning rate remained constant before and after the introduction of reproductive technology.

Keywords

Trend; Monozygotic; Dizygotic; Twinning rates; Maternal age

Introduction

In Japan hormonal stimulation of ovulation has been used since 1966 [1]. In July 1975, the “Survey on Socio-Economic Aspects of Vital Events–Plural Births in 1975” was conducted by the Health and Welfare Statistics and Information Department, Ministry of Health and Welfare [2]. Questionnaires were distributed directly to all mothers with multiple births through January 1 to June 30, 1974. This Survey examined the proportion of mothers treated with hormonal stimulation. Based on the data from this survey, Imaizumi and Inouye determined that the proportion of mothers treated with hormonal stimulation, was 4.5% (158/3485) for like-sexed pairs and 9.2% (72/786) for unlike-sexed pairs [3]. In February 1996, the Japan Society of Obstetrics and Gynecology recommended that only 3-4 eggs or embryos should be transferred per treatment cycle. In May 2008, the Japan Society of Obstetrics and Gynecology decided that a single embryo should be transferred per treatment cycle as a general rule.

Dizygotic (DZ) twinning rate has increased since the introduction of reproductive technology in many countries [4-9]. Japan witnessed an increase in the DZ twinning rate from 1987 to 1998 [6,10]. According to vital statistics in Japan, the overall twinning rates increased till 2005 and decreased thereafter (http://www.e–stat.go.jp/SG1/estat). In the US, the rate has stabilized in 2006 [11]. On the contrary, the monozygotic (MZ) twinning rate increased following the introduction of ovulation induction and assisted reproductive technology (ART) and increased the risk of monochorionic twinning associated with the ART [12-14]. However, the recent trend in the MZ twinning rates in Japan is unknown. The summary incidence (27 studies) of monozygotic twins after the ART was 0.9% (0.8–0.9%) [15]. In Japan, the estimated MZ twinning rate after single embryo transfer was around 2% from 2007 to 2009 [16].

This study therefore aimed to estimate the MZ and DZ twinning rates during the period 1999-2008. It also deals with comparison of the MZ and DZ twinning rates before and after the introduction of reproductive treatments.

Materials and Methods

Data on live births (LBs) and fetal deaths (FDs) were obtained from vital statistic records maintained by the Health and Welfare Statistics and Information Department, Ministry of Health, Labour and Welfare (Tokyo, Japan) for the years 1999-2008. These data cover the entire population of Japan. LB certificates contain information concerning the decedents’ nationality, sex, dates of birth, birth weight, gestational age, parental dates of birth and age, single or multiple births, birth order in multiple births, and other details. FD certificates contain the same information, including the date and cause of FD, but not the parental dates of birth.

Twin pairs were estimated using three record pairings: LB-LB (2LB), FD-FD (2FD), and LB-FD. 2LB and 2FD cases were obtained from the LB and FD certification records, respectively. The LB-FD cases were obtained from LB and FD certification records that excluded 2LB and 2FD twin pairs. We identified 122,758 pairs of twins (99.9% of the total twin births).

The numbers of MZ and DZ twins were estimated by Weinberg’s method [17]. The maternal age (MA) of twin is not always the same because twin pairs could be born on different dates. Then numbers of like- or unlike-sexed twin pairs were comprised of even numbers of twin pairs according to MA and odds numbers of twin pairs.

The parameters of the linear regression model (y=αx+β) were estimated by the least squares method. The linear regression coefficient (α) of the twinning rate (y) on the year (x) was used to determine the trend from 1999 to 2008. The linear regression coefficient for MA (x) was also assessed (19, 22.5, 27.5, 32.5, 37.5, 42.5, and, 47.5 years). The rates are described as per 1000 births.

In addition, we compared the MZ and DZ twinning rates before (1955-1967) and after (1975-1998) the introduction of reproductive treatments [3,7,10]. To enable comparison of the twinning rates, the rates determined in the present study were combined with the results of Imaizumi and Inouye and recomputed using the total number of births as denominators (Table 3 in their report) [3].

Results

Annual change in the twinning rate by zygosity

Table 1 shows the annual change in MZ, DZ, and overall twinning rates from 1999 to 2008. The MZ twinning rates remained fairly constant (3.60-4.34) over this period, while the DZ twinning rate increased from 5.10 in 1999 to 7.66 in 2005, before decreasing to 5.98 in 2008. The overall twinning rates in 1999, 2005, and 2008 were 9.65, 11.51, and 10.37, respectively. Linear regression coefficients (p-values) of the twinning rates on the year were -0.015 (0.544) for MZ twins, 0.165 (0.046) for DZ twins, and 0.151 (0.037) for overall twins. The latter two coefficients were significant at the 5% level (Table 1).

Year   Monozygotic twin deliveries   Dizygotic twin deliveries   Overall twin deliveries4 Total number
  2LB1 LB–FD 2FD2 Total TR3 2LB LB–FD 2FD Total TR3 2LB LB–FD 2FD Total TR3 of deliveries
1999 4723 136 341 5200 4.33 5914 88 128 6130 5.10 10637 273 679 11589 9.65 1201381
2000 4683 100 334 5117 4.21 6528 102 90 6720 5.53 11211 263 618 12092 9.94 1216168
2001 4536 98 323 4957 4.15 6518 82 96 6696 5.60 11054 233 622 11909 9.96 1195616
2002 4628 130 290 5048 4.29 7082 80 142 7304 6.20 11710 287 624 12621 10.72 1177562
2003 4550 121 273 4944 4.32 7306 80 128 7514 6.56 11856 278 595 12729 11.11 1145592
2004 4359 93 273 4725 4.18 7650 98 122 7870 6.95 12009 274 598 12881 11.38 1131567
2005 3514 91 288 3893 3.60 8100 72 108 8280 7.66 11614 237 592 12443 11.51 1081393
2006 4267 100 285 4652 4.19 7528 78 84 7690 6.93 11795 264 564 12623 11.37 1110448
2007 4395 103 259 4757 4.30 7196 66 92 7354 6.65 11591 270 525 12386 11.20 1106288
2008 4322 89 236 4647 4.20 6492 62 68 6622 5.98 10814 219 452 11485 10.37 1107467
Linear regression coefficient (p–value) of twinning rate on the year                  
  MZ twins: –0.015 (0.544)     DZ twins: 0.165 (0.046)     Overall twins: 0.151 (0.037)    

Table 1: Monozygotic (MZ) and dizygotic (DZ) twin deliveries according to survival states of twins and twinning rates for zygotic and overall twins, 1999-2008.

Zygotic and overall twinning rates by MA

Table 2 shows the MZ, DZ, and overall twinning rates according to MA from 1999 to 2008. In general, the twinning rates slightly increased in each MA group (DZ and overall twins), but did not reach significance at the 5% level. The DZ twinning rate for MA 20-24 years and overall rate for MA ≥ 40 years between 1999 and 2008 were exceptions. Figure 1 shows the annual change in the MZ twinning rate according to MA. In the youngest MA group (<20 years), the MZ twinning rate was approximately 4 throughout the period. The rate for MA ≥ 40 years increased from 3.64 in 1999 to 5.40 in 2008, with a twinning rate linear regression coefficient (p–value) of 0.099 (0.189); this was not statistically significant at the 5% level. The MZ twinning rate significantly increased according to MA in 2002 (α=0.042, p=0.012), 2003 (0.032, 0.047), 2006 (0.072, 0.004), and 2008 (0.073, 0.003). The DZ and overall twinning rates significantly increased according to MA annually (Table 2 and Figure 1).

MA 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 RC1 (p-value)
MZ twins
<20 85 98 117 95 91 84 61 61 67 67  
20–24 769 669 650 655 635.5 596 447 506 515 473  
25–29 1956 2090 1945 1778 1622.5 1549 1238 1448 1408 1263  
30–34 1793 1663.5 1659 1840 1842 1778 1448.5 1712 1784 1736  
35–39 533 529.5 523 595 666 615 624 804 878 947  
≥ 40 63 67 63 85 87 103 74.5 121 105 161  
DZ twins
<20 34 30 32 26 28 32 51 28 22 26  
20–24 372 418 406 380 364 364 423 388 320 367  
25–29 2124 2128 2012 2116 1998 1842 1955 1584 1557 1458  
30–34 2540 2850 2880 3148 3262 3540 3711 3540 3208 2791  
35–39 962 1170 1238 1490 1678 1876 1850 1958 1986 1744  
≥ 40 98 124 128 144 184 216 290 192 261 236  
Overall twin pairs
<20 129 142 163 134 129 125 119 98 93 101  
20–24 1168 1113 1085 1069 1037.5 987 899 932 868 862  
25–29 4178 4314 4034 3980 3705.5 3468 3257 3102 3038 2769  
30–34 4423 4593.5 4620 5075 5195 5424 5268.5 5335 5082 4601.5  
35–39 1522 1732.5 1808 2127 2383 2550 2522 2831 2930 2744.5  
≥ 40 168 197 199 236 279 327 377.5 325 375 406  
MZ twinning rate per 1000 births
<20 3.55 3.80 4.32 3.47 3.66 3.63 3.00 3.14 3.66 3.64 –0.046 (0.274)
20–24 4.41 3.95 3.95 4.09 4.26 4.15 3.32 3.71 3.91 3.64 –0.065 (0.057)
25–29 4.02 4.35 4.23 4.09 4.01 4.10 3.57 4.23 4.26 3.90 –0.019 (0.462)
30–34 4.54 4.11 4.06 4.43 4.42 4.19 3.51 4.02 4.25 4.22 –0.032 (0.351)
35–39 4.42 4.05 3.97 4.39 4.62 3.97 3.95 4.57 4.58 4.61 0.039 (0.246)
≥ 40 3.99 3.95 3.69 4.67 4.46 4.92 3.40 5.11 3.93 5.40 0.099 (0.189)
DZ twinning rate per 1000 births
<20 1.42 1.16 1.18 0.95 1.13 1.38 2.50 1.44 1.20 1.41 0.039 (0.439)
20–24 2.13 2.47 2.46 2.37 2.44 2.54 3.14 2.84 2.43 2.82 0.062* (0.041)
25–29 4.37 4.43 4.38 4.87 4.94 4.87 5.64 4.62 4.71 4.50 0.041 (0.368)
30–34 6.43 7.04 7.06 7.59 7.82 8.34 8.99 8.31 7.63 6.78 0.111 (0.224)
35–39 7.97 8.94 9.40 11.00 11.64 12.10 11.70 11.14 10.36 8.49 0.157 (0.365)
≥ 40 6.21 7.31 7.50 7.91 9.43 10.31 13.22 8.11 9.77 7.91 0.318 (0.158)
Overall twinning rate per 1000 births
<20 5.39 5.50 6.02 4.89 5.19 5.39 5.84 5.05 5.09 5.48 –0.023 (0.577)
20–24 6.69 6.56 6.59 6.68 6.95 6.88 6.68 6.83 6.60 6.63 0.005 (0.752)
25–29 8.59 8.97 8.78 9.15 9.17 9.18 9.40 9.06 9.19 8.55 0.020 (0.548)
30–34 11.20 11.34 11.32 12.23 12.46 12.78 12.76 12.53 12.09 11.17 0.078 (0.309)
35–39 12.61 13.24 13.73 15.70 16.54 16.45 15.95 16.11 15.28 13.36 0.203 (0.238)
≥40 10.64 11.61 11.65 12.96 14.29 15.61 17.20 13.72 14.03 13.61 0.413* (0.047)
Linear regression coefficient (p–value) of twinning rate on the MA
Year 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008  
MZ twins 0.015 0.004 –0.019 0.042* 0.032* 0.035 0.022 0.072** 0.019 0.073**  
  (0.488) (0.698) (0.078) (0.012) (0.047) (0.089) (0.182) (0.004) (0.288) (0.003)  
DZ twins 0.258* 0.313** 0.327** 0.376* 0.429** 0.458** 0.495** 0.495** 0.415** 0.308**  
  (0.016) (0.009) (0.009) (0.016) (0.006) (0.004) (<0.001) (<0.001) (0.001) (0.002)  
Overall twins 0.276* 0.314** 0.311* 0.418* 0.462** 0.498** 0.527** 0.444** 0.439** 0.379**  
  (0.019) (0.009) (0.012) (0.010) (0.005) (0.001) (<0.001) (0.007) (0.002) (<0.001)  

Table 2: Number of twin pairs and twinning rates by zygosity and overall twins by maternal age (MA), 1999-2008

gynecology-obstetrics-twinning-rate

Figure 1: Yearly change of MZ twinning rate per 1000 births by maternal age, 1999-2008.

Comparison of twinning rates before and after introduction of reproductive technology

Figure 2 shows the annual change in the MZ and DZ twinning rates during 1955-1967 and 1974-2008. The MZ twinning rates remained approximately constant (3.56-4.43) for the overall period, whereas the DZ twinning rates were consistent from 1955 to 1987 (1.86-2.47) and gradually increasing up to 2005 (7.57) and finally decreasing slightly in 2008 (5.92). The DZ twinning rate was 2.02-fold higher in 1997 (4.56) than that for the period 1955-1967 (2.26). In 1997 the twinning rate was similar for both MZ (4.40) and DZ twins. The DZ rate was 3.35-fold higher in 2005 than that during 1955-1967 (Figure 2).

gynecology-obstetrics-Yearly-change

Figure 2: Yearly change of MZ and DZ twinning rates, 1955-1967and 1974- 2008.

Figure 3 shows comparison of the MZ and DZ twinning rates according to MA for the period 1999-2008 vs. 1960-1967. The MZ and DZ twinning rates in Figure 3 are a composite of those obtained from Table 3 of the report by Imaizumi and Inouye and from the present study (Table 2) [3]. The MZ twinning rate was constant with MA between the two periods: 0.9-fold for MA <20 years; and 1.0-fold for MA 20-24 years to ≥ 40 years. Conversely, the DZ twinning rate increased with MA between the two periods: 1.2-fold for MA <20 years, gradually increasing to 3.7-fold for MA ≥ 40 years (Figure 3).

gynecology-obstetrics-maternal-age

Figure 3: Comparison of MZ and DZ twinning rates according to maternal age (MA) for the period 1999-2008 vs. 1960-1967. RR: Comparison of twinning rates for the period 1999-2008 vs. 1960-1967.

Discussion

The MZ twinning rate remained fairly constant from 1999 to 2008. The rate for MA ≥ 40 years slightly increased during the period where the regression coefficient was 0.099 (p=0.19). The fact may have reflected the increase in the number of older mothers (≥ 35 years) undergoing fertility treatment in recent years. The DZ twinning rate increased from 1999 to 2005 and decreased thereafter. The number of twin cases delivered by ART in Japan was 1975 cases in 1999, which increased to 3559 cases in 2005 and decreasing to 2099 cases in 2008 [18]. Saito reported that restriction of the number of embryos transferred certainly takes effect. This reflected on the decline in the DZ twinning rate after 2005 in the present study [19]. Thus, the DZ twinning rate in Japan may be slowly decreasing to near the levels achieved with natural fertility.

Data on multiple pregnancies from vital statistics are very useful information which covers the entire population of Japan. However, there was no information of pregnancies achieved by ART and pregnancy outcomes.

It is very important to reduce twinning rates regarding to stillbirth and infant mortality rates. In Japan, stillbirth rates were more than two times higher in MZ twins than in singletons and in DZ twins during 1986-1994 [20]. The infant mortality rate was also 4.6 times higher in twins than in singletons during 1999-2008 [21]. Then It is very good policy that a single embryo should be transferred per treatment cycle as a general rule by the Japan Society of Obstetrics and Gynecology.

Acknowledgements

We are grateful to the staff of Statistics and Information Department, Ministry of Health, Labour and Welfare in Japan.

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