Centre for Research in Health & Social Statistics, The Danish National Research Foundation, Sejrøgade 11, DK-2100 Copenhagen Ø, Denmark
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Abstract |
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Key words: birth order/parental age/sex composition/sex ratio/twins
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Introduction |
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The largest natural variation in the human sex ratio is found between ethnic groups, where Asian populations have the highest sex ratio and black populations the lowest (James, 1984, 1985a
; Ruder, 1985
). The intra-population variation in the sex ratio is generally smaller in magnitude (Ullizzi and Zonta, 1995) and has been associated with various natural factors such as maternal parity (`Poisson association'), paternal age, maternal age, the sexes of previously born children in the family (James, 1975
) and season (e.g. Lerchl, 1998). Most large-scale studies on parity and parental ages suggest an effect on the sex ratio of birth order and paternal age, and in some studies, also of maternal age (Table I
). One possible biological explanation for the decrease in sex ratio with maternal age and birth order is an increase in female gonadotrophin concentration with age (James, 1980a
,b
, 1985b
). The decline in sex ratio with paternal age is suggested to be due to decreasing coital rates with age (James, 1980b
).
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Children from multiple births have been shown to have a lower sex ratio than singletons (Pollard, 1969). The proportion of multiple births has increased in Denmark in the period, 19801994 (Westergaard et al., 1997
) and we were therefore curious to examine the sex ratio among Danish multiple born children.
In the present study, using data on more than 800 000 births in Denmark, 19801993, we address the hypothesis that sex ratio in the Danish population varies with multiple birth, birth order, ages of parents and with the sexes of preceding siblings.
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Materials and methods |
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To examine the sex ratio of multiple born infants, 795 027 singletons and 18 991 multiple born children representing 9406 pregnancies were compared. For 1873 children, there was no information on the mother or on number of children per multiple birth. Information on zygocity of the multiple born children was not available. Therefore the comparison with singletons was done on an expected sex ratio among the multiple born similar to singletons, while keeping in mind that we were making an underestimation of the expected sex ratio for twins, triplets and quadruplets.
For the 795 027 singletons, the effects of maternal and paternal ages and birth order were analysed by logistic regression. The proportion of males born was calculated as a function of the sexes of preceding siblings with the same mother for 204 815 second, 40 433 third and 5279 fourth born children. Only firstborn children and their siblings within the period 19801993 were used in the analysis on the sexes of preceding siblings, due to missing information on the children born before 1980. For the rest of the analysis inclusion of children with siblings born before 1980 were included, as information on the previous siblings did not have any influence on the analysis. The analyses of the proportion of males as a function of the sex of previous siblings were done by contingency tables, 2 tests and by logistic regression.
From all logistic regression analyses, odds ratios and 95% confidence intervals were calculated; a statistical test (two-sided) for trend over categories was performed by assigning values 1, 2, 3, etc. to successive categories and including the resulting variable in the analysis.
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Results |
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Multiple born children
Table II presents the comparison between singletons and children from different categories of multiple births. Overall, the sex ratio decreased with increasing number of children per plural birth, and the sex ratios for twins and triplets were significantly lower than that of singletons (P < 0.05). Same-sexed twins had a sex ratio close to that of singletons (51.1 versus 51.3). Twins with different sex had a lower sex ratio than singletons (50, P = 0.04; Table II
) and the overall sex ratio for twins was 50.6. If only one of the twins was alive at the time of birth, the sex ratio was 47.9. Overall, triplets had a significantly lower (P < 0.05) sex ratio than singletons (47.0 versus 51.3). This was due to a lower sex ratio for all groups of triplets. Triplets with different sex had the highest sex ratio within triplets (49.8), same-sexed triplets the second (42.8) and triplets with one or two dead in the birth the lowest (41.7). The seven sets of quadruplets had an apparently lower sex ratio than singletons (42.9 versus 51.3), but this was not significant.
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Discussion |
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Multiple born children
The overall lower sex ratio for multiple born children compared with singletons is in accordance with previous findings (Pollard, 1969) and illustrates the importance of considering explicitly multiple births in sex ratio analysis, i.e. by exclusion of multiple born children from the analysis or by identification of multiple births as a separate group. Zygocity information was not available and the expected sex ratios for multiple born children in relation to zygocity could not be directly calculated. Therefore the direct comparison with the sex ratio of singletons probably underestimates the difference between multiple born children and singletons. For example, same sexed dizygous twins have an expected probability of 0.237 (0.487x0.487) for a girlgirl combination and 0.263 (0.513x0.513) for a boyboy combination, with a resulting sex ratio of 52.6, whereas monozygotic twins have an expected sex ratio of 51.3. Thus, for twins the sex ratio is expected to be between 51.3 and 52.6, suggesting that the lower sex ratio observed in the present study is even more significant. The same calculations could be performed for same sexed dizygous triplets and quadruplets resulting in an expected sex ratio value in the range 51.353.9 for triplets and 51.355.2 for quadruplets, further suggesting a higher significance of the present results. The observed decrease in sex ratio with increase in number of children per plural birth is most likely due to an increased prenatal mortality of the male fetus in multiple births (Zahálková, 1978
; Rydström, 1990
).
Parental ages and birth order
Contradictory results are found in the literature for the effects of paternal age, maternal age and birth order, ranging from no effect at all to significant effects of one, two or all three factors. It has been suggested (James and Rostron, 1985) that the paternal age effect is stronger than the maternal effect, and illustrated that the observation of no effect of maternal age in a study could be due to a low sample size. If this suggestion is right, this could explain why no effect of maternal age was found in the present study, whereas the stronger effect of paternal age was correctly identified. Indeed, all studies of relatively low numbers of births (<2x106) have failed to identify the effect of maternal age (Table I
), whereas larger studies seem to identify the effect. The results from studies examining all three factors (Table I
) suggest that the number of factors identified increases with study size, such that the paternal effect is identified by most studies, birth order is the next most frequently identified and maternal age is identified only in very large studies. However, it should be noted that the results from the three studies that found an effect of maternal age (Takahashi, 1954
; Pollard, 1969
; James and Rostron, 1985
) differed. Sex ratio has variously been reported to decrease (Pollard, 1969
; James and Rostron, 1985
) or increase (Takahashi, 1954
) with maternal age. A possible explanation for this difference in results could be false registration of children by elderly women in Japan (James, 1972
) or perhaps the lack of adjustment for birth order and paternal age in Takahashi's analysis. Recently, the sex ratio among children of grand-grand-multiparous women was examined in relation to maternal age (Juntunen et al., 1997
). A significantly lower sex ratio with age was found among grand-grand-multiparous women in Finland, supporting previous findings (James and Rostron, 1985
), whereas no such association was found in a study (Almagor et al., 1998
) on Jewish Orthodox and Muslim women in Israel. This supports the idea that cultural, ethnic and environmental variables may be of importance in relation to the effect of maternal age (James, 1972
; Almagor et al., 1998
).
Suggestions have been made of underlying biological effects leading to a decrease in sex ratio with increasing paternal age, including decline in male androgen concentrations with age (James, 1987). This suggestion seems to be supported by the observation that the HLA gene can affect androgen levels and thus the sex ratio (review in James, 1992, 1996). Such a hormone-induced effect could imply a skewed ratio of Y- and X-bearing spermatozoa, a reduced probability of fertilization by a Y-bearing spermatozoon or differential mortality of XX and XY fetuses with increasing paternal age. Analysis of the primary sex ratio measured as the ratio of X- and Y-bearing spermatozoa in semen samples showed no significant effect of age (Martin and Rademaker, 1992
; Martin et al., 1995
). However, no alteration was found in the normal X:Y sperm ratio (Bowman et al., 1998
) but a significantly higher number of in-vitro fertilized male (n = 20) than female (n = 8) cleavage-stage embryos, when doing preimplantation analysis, indicating that the binding of Y-bearing or X-bearing spermatozoa to the oocyte has an effect on the primary sex ratio. Another line of speculation is that the decrease in the sex ratio with paternal age is due to less frequent sexual intercourse with increase in paternal age (James, 1975
; Hilsenrath et al., 1997
), thus decreasing the probability for male offspring, since the probability of males is suggested to be lower near ovulation (James, 1980b
). However, a recent study found no relationship between timing of insemination and day of ovulation on the secondary sex ratio (Gray et al., 1998
). This discrepancy in results is difficult to explain, but factors such as effects on precise reporting of intercourse, measurement errors and small scale studies with little power for detecting differences have been suggested (Gray et al., 1998
). One line of speculation is that precise reporting of intercourse could be influenced by the wish of couples in some cultural groups to indicate higher coital rates than in reality.
Sexes of preceding siblings
The suggestion that some individuals or some couples have a natural tendency towards having children of one or the other sex (James, 1975) is not supported by the present study. Indeed, no association was seen with the sex of the previous born child (`Markovian dependency') and no significant predisposition was found of couples or individuals to have children of a particular sex (`Lexis association'). It has been suggested (James, 1975
) that if the sex ratio after one firstborn boy is lower than after two firstborn boys, this indicates Lexis association. In the present study this was not the case as the sex ratio was 1% lower after two firstborn boys than after one firstborn boy. Using the same argument for girls, but with the opposite expectation for the trend of the sex ratio, our analysis also failed to indicate Lexis association as the sex ratios following one firstborn girl and two firstborn girls were the same.
Taking into account the large number of births analysed in the present study and the lack of association found with previously born children and the sex ratio, we conclude that no strong relationship is present between sexes of adjacent sibs in Danish sibships in the period analysed. The lack of statistically significant correlation does not mean that some couples cannot have a higher probability of having children of a particular sex, just that such couples are a small fraction of the Danish population. One may see an indication of Lexis association in the observation of excesses of large sibships of only one sex when regarding all children born after the same-sex combination. However, the conditional probability of a particular sex of the immediately next born child, following a given sex combination of previous born children, would not be influenced by sex preference. For example, in Denmark, a preference for having children of both sexes in families has been found with increasing fertility rates in families with only children of one sex (Jacobsen et al., 1999). This effect increased fertility rates following same-sexed children, for example for the fourthborn children. However, the higher number of fourthborn children could not influence conditional probability for a particular sex among these children. The analysis of incomplete families of decreasing family size, when compared to previous studies based on larger and completed families, may be contributing to the discrepancy between this study and some previous studies (Edwards, 1966
; James, 1975
).
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Notes |
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References |
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Submitted on June 14, 1999; accepted on August 27, 1999.