**2. Twinning rates in São Paulo city**

The USP Twin Panel (*Painel USP de Gêmeos*), based in the Institute of Psychology—University of Sao Paulo since 2015, has investigated the live birth twinning rate from São Paulo city (Brazil) using public data and additional information during the years 2003–2014 [22]. The public data on the singleton, twin, and higher order multiple live-born births were drawn from the Health Department database of Live Births Information System of São Paulo (SINASC) and included all deliveries registered between the years 2003 and 2014, from all 140 hospitals (56 public and 84 private) of the 31 districts of the city. We contacted SINASC and upon agreement from the Human Research Ethics Committee at the Institute of Psychology, University of São Paulo (Protocol Number 1,418,827), we received a more detailed database that included infants' sex, identification of the mother, date and hour of the delivery, place of the delivery, and register number. Based on these refined data, we determined the sex composition of twin maternities using Weinberg's differential method, which is a populational equation based on the sex ratio and the proportion of same-sex and opposite-sex twins. The validity of Weinberg's rule has been debated over the years. Using large samples and applying statistical assumptions may improve its utility; see [39]. As standard in the literature, we computed maternity rates per 1,000 (‰): individual twin births were divided by two and individual higher order multiple births were divided by three, assuming that the far majority of higher order multiple births were triplets. Mothers' age was recoded into eight classes (<15, 15–19, 20–24, 25–29, 30–34, 35–39, 40–44 and >45 years) (for details see, [22]).

For the first time in Brazil, we could establish live-birth rates in a decade-long, large-scale population sample encompassing 24,589 twin deliveries and 736 multiple deliveries out of a total of 2,056,016 deliveries during the studied time period. Precisely, the average rate of twin deliveries was 11.96‰, while the average of singletons was 987.42‰ and multiple births was 0.36‰. This was the largest study so far to calculate twinning rates in Brazil, which is in general in agreement with results from other countries [69], for example, Spain [70].

Interestingly, we found a strong positive correlation between the period (2003–2014) and twinning rate percentage and a strong negative correlation between the time period and both singleton rates and higher order multiple rates. This shows that while singletons and higher order multiple rates are diminishing, twinning rates are increasing. The twin birth rate rose 30.8% from 2003 to 2014, increasing from 10.19 to 13.33‰ [22]. Many factors may lead to this increase, such as increasing body mass index in women, improvement of quality of life, increase in social support, postponement of pregnancies until higher ages, use of assisted reproduction technologies and an increase in air pollution [22]. The pattern obtained in São Paulo city is aligned with the pattern in earlier decades in São Paulo [71] and with the worldwide increase in twinning rates (e.g., [42, 72, 73]), especially over the last several decades [68].

## **2.1. Twinning as a function of mothers' age in São Paulo**

with maternal age, but dizygotic twinning increases more than monozygotic twinning, then both hypotheses would receive support. However, both of these theories focus mostly on DZ twinning, which has a very different origin than MZ twinning. Therefore, while the MZ results may be consistent with what the theories predict, a causal interpretation in terms of

The USP Twin Panel (*Painel USP de Gêmeos*), based in the Institute of Psychology—University of Sao Paulo since 2015, has investigated the live birth twinning rate from São Paulo city (Brazil) using public data and additional information during the years 2003–2014 [22]. The public data on the singleton, twin, and higher order multiple live-born births were drawn from the Health Department database of Live Births Information System of São Paulo (SINASC) and included all deliveries registered between the years 2003 and 2014, from all 140 hospitals (56 public and 84 private) of the 31 districts of the city. We contacted SINASC and upon agreement from the Human Research Ethics Committee at the Institute of Psychology, University of São Paulo (Protocol Number 1,418,827), we received a more detailed database that included infants' sex, identification of the mother, date and hour of the delivery, place of the delivery, and register number. Based on these refined data, we determined the sex composition of twin maternities using Weinberg's differential method, which is a populational equation based on the sex ratio and the proportion of same-sex and opposite-sex twins. The validity of Weinberg's rule has been debated over the years. Using large samples and applying statistical assumptions may improve its utility; see [39]. As standard in the literature, we computed maternity rates per 1,000 (‰): individual twin births were divided by two and individual higher order multiple births were divided by three, assuming that the far majority of higher order multiple births were triplets. Mothers' age was recoded into eight classes (<15, 15–19, 20–24, 25–29, 30–34,

For the first time in Brazil, we could establish live-birth rates in a decade-long, large-scale population sample encompassing 24,589 twin deliveries and 736 multiple deliveries out of a total of 2,056,016 deliveries during the studied time period. Precisely, the average rate of twin deliveries was 11.96‰, while the average of singletons was 987.42‰ and multiple births was 0.36‰. This was the largest study so far to calculate twinning rates in Brazil, which is in

Interestingly, we found a strong positive correlation between the period (2003–2014) and twinning rate percentage and a strong negative correlation between the time period and both singleton rates and higher order multiple rates. This shows that while singletons and higher order multiple rates are diminishing, twinning rates are increasing. The twin birth rate rose 30.8% from 2003 to 2014, increasing from 10.19 to 13.33‰ [22]. Many factors may lead to this increase, such as increasing body mass index in women, improvement of quality of life, increase in social support, postponement of pregnancies until higher ages, use of assisted reproduction technologies and an increase in air pollution [22]. The pattern obtained in São Paulo city is

general in agreement with results from other countries [69], for example, Spain [70].

their origin may not be warranted.

34 Multiple Pregnancy - New Challenges

**2. Twinning rates in São Paulo city**

35–39, 40–44 and >45 years) (for details see, [22]).

We documented a positive influence of mothers' age on twinning rates, in particular, women aged 25 years or more have more twins than younger women. The opposite pattern appeared to characterize the singleton mothers. Mothers' age was the strongest positive predictor, with the time period also positively, although weakly, predicting the twinning rates. Together, age of the mother and the time period explained 63% of the total variation. The model for higher order multiple rates was also significant, explaining 25% of the total variation, and mothers' age was its only positive predictor [22].

Furthermore, we used the Weinberg's differential method in order to estimate the average frequency of MZ and DZ twinning rates. We found that the average twinning rate for the whole period was 4.42‰ for MZ and 7.15‰ for DZ twins [22]. These rates were comparably increasing throughout the time period (2003–2014). The mothers' age positively and significantly correlated with both MZ and DZ birth rates. The model for DZ twinning rates was highly significant, explaining 61.3% of the total variation. Mothers' age was the strongest positive predictor, with the time period also positively, although weakly predicting the twinning rates. The model for MZ twinning rates was also significant, explaining 17.1% of the total variation. Mothers' age was the only positive predictor of the MZ twinning rates [22]. This general finding, regardless of the zygosity, agrees with the literature both in Brazil [56, 71] and in other countries [58].

We found that women aged 45 or more had almost three times more DZ twins than mothers aged between 40 and 44 years and seven times more DZ twins than women aged between 20 and 24 years [22] (see **Figure 3**). This finding agrees with the view that polyovulation is a major cause of twinning in older ages as predicted by the insurance ova hypothesis. Moreover, we found that women aged 45 or more had two times more MZ twins than mothers aged between 40 and 44 years, and women aged between 20 and 24 years. This increase in MZ twinning in older mothers was predicted by the relaxed-screening hypothesis. Both hypotheses and proposed mechanisms can, thus, explain higher rates of DZ twinning in older mothers. Thus, our data support both evolutionary hypotheses for higher twinning near menopause, but the specific reasons behind MZ and DZ twinning at older maternal ages most likely differ. Importantly, different countries around the world have already sparsely but consistently found that not only DZ but also to a smaller degree MZ twinning rates were higher in mothers closer to menopause, in the U.S.A. population [74], in a Jewish population [75], in a Jewish and Bedouin populations [76], in rural and urban Chinese populations [77], and also in Spanish populations [70]. This cross-cultural convergence adds support to both evolutionary hypotheses, particularly to the relaxed-screening hypothesis [60, 61].

#### **2.2. Variation in twinning rates in different city districts of São Paulo**

Additionally, we closely investigated how twinning rates are distributed within various subregions of the city of São Paulo, the biggest metropolis of Brazil. Considering mothers' home

**Figure 3.** Dizygotic (DZ) and monozygotic (MZ) twin rates per 1,000 births as a function of mother's age; from [22].

addresses at the time of delivery, we found a large variance in the twinning rates among the 31 subregions of São Paulo: from 9.85 (district Itaim Paulista) to 24.32‰ (district Pinheiros). **Figure 4** shows the overall rate of twins' geographical distribution between 2003 and 2015 by the 31 subregions of the city. In **Figure 4**, we clearly show that in the central regions there are more twins born than in peripheral districts. This centralized distribution does not simply reflect the places where most hospitals are available, because we accessed the mothers' addresses and not the address of the maternity hospitals. Thus, this indicates that a real demographic factor is driving this distribution.

status. Further studies should attempt to disentangle the web of salient influential factors by accessing and integrating indicators such as nutrition, education, socioeconomic status, and

**Figure 4.** Overall geographical distribution of twinning rates between 2003 and 2015 by the 31 districts of the city. The darker the color, the higher the twinning rate. We used percentiles to create low, mid-low, mid-high, and high rates.

Twinning as an Evolved Age-Dependent Physiological Mechanism…

http://dx.doi.org/10.5772/intechopen.79907

37

Most recently, the USP Twin Panel (*Painel USP de Gêmeos*) has expanded the investigation of twinning rates to the entire country of Brazil between the years of 2002 and 2013. The data were drawn from TABNET within DATASUS, an official public governmental database and transformed into rates of maternities the same way it was done for the city of São Paulo [22]. A multivariate general linear model was used to explore the effects of region, maternal age, and time period on singleton, twin and higher order multiple birth rates. We obtained a total of 35,051,790 maternities between 2002 and 2013, 329,006 twinning maternities and 8,005 higher order maternities. Considering all regions of Brazil, the overall average rate of twins was 9.39‰ and higher order births were 0.23‰. These data show that the Brazilian countrywide twinning and multiple birth rates are lower than the twinning rates in the city

**3. Twinning rates across the entire country of Brazil**

assisted reproduction.

There was a pronounced positive correlation between the average income of each city district according to the 2010 Demographic census from Brazilian Institute of Geography and Statistics (IBGE) and the average twinning rates during the period from 2003 to 2015. The same result was found for the higher order multiple birth rates. This indicates that, in richer regions, there is a higher chance of twin and multiple births. This new finding from the USP Twin Panel can explain the centralized distribution of higher twinning rates shown in **Figure 4**. Many factors could be interacting to produce this result. Women with higher socioeconomic status tend to study longer and delay reproduction; thus, having offspring in higher age increases the chance of multiple pregnancies. Also those women can afford assisted reproduction technologies which increase the chance of multiple pregnancies. Moreover, those women have a richer and more diverse nutritional diet which, as found for nonhuman primates [1, 20], could increase the chance of multiple pregnancies. Colletto et al. [78] also found increased twinning rates as a function of women's higher socioeconomic Twinning as an Evolved Age-Dependent Physiological Mechanism… http://dx.doi.org/10.5772/intechopen.79907 37

**Figure 4.** Overall geographical distribution of twinning rates between 2003 and 2015 by the 31 districts of the city. The darker the color, the higher the twinning rate. We used percentiles to create low, mid-low, mid-high, and high rates.

status. Further studies should attempt to disentangle the web of salient influential factors by accessing and integrating indicators such as nutrition, education, socioeconomic status, and assisted reproduction.
