З. Стоянов, П. Николова, Д. Ставрев, C. Трендафилова, Р. Русева «Эпидемиология правшества-левшества в Болгарии: гендерные и возрастные различия» (C. 5-12)

З. Стоянов, П. Николова, Д. Ставрев, C. Трендафилова, Р. Русева

ЭПИДЕМИОЛОГИЯ ПРАВШЕСТВА-ЛЕВШЕСТВА В БОЛГАРИИ: ГЕНДЕРНЫЕ И ВОЗРАСТНЫЕ РАЗЛИЧИЯ

Zlatislav Stoyanov*, Piareta Nikolova*, Dimitar Stavrev**, Svetla Trendafilova**, Ralica Ruseva**

Handedness Proportions in Bulgaria:

II. Sex and Age Differences

*Medical University “Prof. Paraskev Stoyanov”, Varna, Bulgaria

**Home Care Centre at Varna Branch of Bulgarian Red Cross, Varna, Bulgaria

Handedness Proportions in Bulgaria:II. Sex and Age Differences

Zlatislav Stoyanov*, Piareta Nikolova*, Dimitar Stavrev**, Svetla Trendafilova**, Ralica Ruseva**
The proportions of handedness among males and females in Bulgaria are analyzed including handedness proportions in adolescence and senescence. It is established that left-handed males are reliably more than left-handed females, 9.8% and 5.2% respectively. There is no significant difference in left-handedness incidence in young and old, 6.8% and 8.1% respectively.

Key words: left-handedness, non-right-handedness, sex, age.

Introduction.

Handedness is a behavioural manifestation of cerebral laterality. According to average data, approximately 10% of human population are left-handers (non-right-handers) (McManus, 2002; Geuze et al., 2012). Sex differences are known to exist in the lateralization of brain functions (McGlone, 1980; Grabowska et al., 1994; Toga and Thompson, 2003). For that reason, studies on population proportions of handedness pay special attention to the presence or absence of sex differences. Most publications on the problem report higher incidence of left-handedness in males (Bourassa et al., 1996; Bradley, 1992; Medland et al., 2005; Llaurens et al., 2009; Vuoksimaa et al., 2009). In Spain, for example, left-handed men present 7.9% and left-handed women 4.4%; in Italy they are 8.3% and 5.1% respectively; in Brazil 8.5% and 5.3%; in the United Kingdom 11% и 9%. Chernigovskaya et al. (2005) report that in Russia’s Northwest left-handed males are reliably more than left-handed females, 8.5% and 5% respectively. There exist, however, data that do not conform to these observations: research in France found 8.7% left-handed men against 9.8% left-handed women, the same being demonstrated in some Greek studies (see Bourassa et al., 1996). Data for the Chuvash Republic show 9.08% left-handed males and 9.98% left-handed females (Kalichman et al., 2008). Analyzing data for Sudan, De Agostini et al. (1997) do not find sex differences in the handedness frequency: 5% of the boys and 5% of the girls were left-handed. The presence of diverse data points out that there exist ethnic or geographical differences, and gives reason to analyzing the sex differences in handedness in various populations.One more aspect is naturally present in the discussions of population proportions of handedness, that of ontogenesis. Data for senescence are interesting although controversial. Some report of decrease of asymmetry in handedness and reduction of the relative share of left-handers in old age (see Bragina and Dobrohotova, 1988; Hugdahl et al., 1993). Summarizing the results of several studies, Annett (1993) reports about 11% left-handers among young people (15-24 years of age) and only about 3 % among old people (64-86 years of age). The problem is especially debatable because it serves as the basis for commenting the longevity of left-handers. Following the results of their study among players in the US baseball league, Halpern and Coren come to the conclusion that handedness is associated with reduced longevity (see Coren, 1994). Similar results are published by Ellis and Engh (2000). The discussions in a number of studies on handedness proportions or the health problems of left-handers are based speculatively on such results (see Schaafsma et al., 2012). There exist, however, definite counterpoints to the presented data. Contrary to Halpern and Coren’s findings, Hicks et al. (1994), again among baseball players, establish that right-handed players live approximately eight months less than left-handed players. A more recent study of Lawler and Lawler (2011) among basketball players does not discover a significant relation between the type of manual dominance and mean longevity.Bearing in mind the interest to sex-related and age-related differences in handedness in various nations, we decided to analyse: (1) the proportions of handedness among males and females in Bulgaria; (2) the proportions of handedness in two different age groups of Bulgarians, in adolescence and senescence. Such a study has not been carried out in Bulgaria. Moreover, in the last 25 years (the time of the democratic transition) Bulgarian society has experienced significant socio-cultural changes. They include changes in the pedagogical dogma and attitudes towards left-handed children: the practice of forced switch of hand use was abandoned. As a result, it could be expected that the proportion of the left-handers among young people is higher than in old people.
Methods.
Analyses of sex differences in handedness proportions are based on a contingent of total of 600 individuals (250 males and 350 females) born between 1981 and 1991 with average age of 19.8 years. The subjects were recruited on a volunteer basis from the secondary schools and universities in the city of Varna, Bulgaria. For the aims of the study, additional 136 individuals (46 males and 90 females) born between 1928 and 1947, with average age of 73.9 years, were recruited among participants in the target group of the “Home Care” project of the Red Cross in Varna. Recruitment was directed at obtaining an approximately equal proportions of males and females, but balance was not achieved.The evaluation of handedness was based on a handedness questionnaire, which was adapted for Bulgarian compilation from the questionnaires of Annett (the 12-item version) and of Oldfield (the 10-item version) (for details see Stoyanov, 1998; Stoyanov et al., 2010). A handedness quotient was computed on the basis of the handedness questionnaire (Fedoruk and Dobrohotova, 1980). The handedness quotient varied between –100% (strong left-handers) and +100% (strong right-handers). The zero value of HQ was used as a threshold for distinguishing between left-handers and right-handers. We also considered it relevant to carry out an analysis of handedness in the categories of non-right-handedness (HQ = –100% ¸ +35%) and right- handedness (HQ = +36% ¸ +100%). This approach allows for inclusion of switched left-handers (see McManus, 1985), a large part of whom falls into the range of HQ = 0% ¸ +35%.Fisher’s exact test was used for statistical evaluation of the data (GraphPad Prism 5 software). The differences were considered significant at p < 0.05.
Results.
The results are presented in Tables 1 and 2. Left-handers (HQ = –100% ¸ –1%) in the group of young Bulgarians are 6.8%, and in the sample from the old age group 8.1%. The difference is non-significant with p = 0.581. The proportion of left-handers among young males (24 out of 250 – 9.6%) does not differ significantly from the proportion of left-handers among old males (5 out of 46 – 10.9%) with p = 0.788. The same is valid for females: 4.9% left-handers in young women and 6.7% in old ones (p = 0.438).Table 1 shows that among the young people the share of left-handed males is significantly higher (p = 0.03) than that of left-handed females: 9.6% and 4.9% respectively. Similar sex differences in the handedness proportions are found also in the group of old age participants: 10.9% left-handed males and 6.7% left-handed females (but the difference is statistically insignificant with p = 0.508). Aggregated data of both groups show that left-handers are 29 out of 296 studied males (i.e. 9.8%) and 23 out of 440 studied females (i.e. 5.2%) and the difference is statistically significant (p = 0.02).

TABLE 1. Population proportions of handedness in categories left-handedness (HQ = –100% ¸ –1%) and right-handedness (HQ = 0% ¸ +100%).

Age category Total Left-handers(HQ = –100% ¸ –1) Right-handers(HQ = 0% ¸ +100%)
Young 600 41 (6.8%) 559 (93.2%)
males females males females males females
250 350 24(9.6%) 17(4.9%) 226(90.4%) 333(95.1%)
Old 136 11 (8.1%) 125 (91.9%)
males females males females males females
46 90 5(10.9%) 6(6.7%) 41(89.1%) 84(93.3%)
It is evident from Table 2 that non-right-handers are 13.0% of the young people and 10.3% of the old ones (p = 0.473). In young males, non-right-handers are 38 out of 250 (i.e. 15.2%), and in old males they are 8 out of 46 (i.e. 17.4%) with p = 0.662. In females, the proportions are respectively 11.4% for non-right-handed young females and 6.7% for non-right-handed old ones with p = 0.246.The share of non-right-handed young males (15.2%) is higher than that of non-right-handed young females (11.4%), although the difference does not reach statistical significance (p = 0.109). In old individuals the difference in favour of males (17.4% non-right-handed males against 6.7% non-right-handed females) is close to the statistical significance with p = 0.07. In summarised data (both young and old), 15.5% of males (46 out of 296) are non-right-handed against 10.5% of females (46 out of 440) with p = 0.05.

TABLE 2. Population proportions of handedness in categories non-right-handedness (HQ = –100% ¸ +35%) and right-handedness (HQ = +36% ¸ +100%).

Age category Total Non-right-handers (HQ = –100% up to +35%) Right-handers (HQ = +36 up to +100%)
Young 600 78 (13.0%) 522 (87.0%)
males females males females males females
250 350 38(15.2%) 40(11.4%) 212(84.8%) 310(88.6%)
Old 136 14 (10.3%) 122 (89.7%)
males females males females males females
46 90 8(17.4%) 6(6.7%) 38(82.6%) 84(93.3%)

Discussion.
One of the aims of the present study was to establish the proportions of handedness among males and females in Bulgaria. The results obtained from the studied sample of Bulgarian population (both young and old) build into the file of prevalent data about higher incidence of left-handedness (non-right-handedness) in males (for review see Papadatou-Pastou et al., 2008). We support the concept that sex differences in handedness are biological in nature: they are a result of sex-dependent manifestation of the etiologic mechanisms of handedness or sex specifics in the plasticity of lateralization (see Medland et al., 2005). We also share the idea that in its genesis handedness is an epigenetic phenomenon, i.e. it is determined by genetic mechanisms and programmes, modified by overlapping factors of the environment. For that reason we think that when searching for the causes for sex differences in the proportions of handedness, several theories about the origin of handedness should be taken into account, those of Annett, McManus and of Geschwind and Galaburda.The Right Shift Theory of Marian Annett favours the role of a single gene with two alleles (RS+ и RS–), where RS+ (factor of the “right shift”) appears to be dominant and determining the development of typical left-hemisphere dominance for language and right-handedness (Annett, 1985; 1998; 2008). Annett (1997) assumes that the RS+ gene is not sex-related but its expression is sex modified: it is more strongly expressed in females determining for more right-handers among them. Annett also attempts to associate the degree of right shift (the expression of the RS+ gene) with the degree of brain maturation during the foetal period: in more mature brains at the moment of birth (as in girls than boys) the right shift (in this case towards right-handedness) is better expressed.According to the McManus model (1985), handedness is also controlled by two alleles of one gene. One allele “D” encodes dextrality, and the other “C” encodes chance in the formation of manual preferences. To explain the higher incidence of left-handedness in males, McManus and Bryden (1992) postulate the existence of a sex-related modifier-gene. They assume that the expression of the D gene (for dextrality) may be suppressed by a relatively rare recessive gene of the X-chromosome. The effect should be more expressed in men because the “m” modifier in the X-chromosome cannot be compensated. In females, the suppression in the expression of the D gene happens only with a double dose of the modifier (“mm” from both X-chromosomes). The recessive model of Jones and Martin (2000; 2001) is very similar to this hypothesis. According to that model, left-handedness is associated recessively with a genetic variation in the X-chromosome. That explains its higher potential for expression in males (XY) than in females (XX).The hypothesis of Geschwind and Galaburda (1985a,b) is one of the theories that give attention to prenatal and perinatal factors affecting brain development. It assumes that higher than normal intrauterine levels of testosterone, operating during critical periods of foetal brain development, determine right hemisphere dominance for language, left hemisphere dominance for processing of visual-spatial relations and left-handedness. The essence of the theory of Geschwind and Galaburda somehow makes it more natural (without additional modifications) in explaining the higher left-handedness in males. The authors do not on principle reject the genetic mechanisms but they focus on testosterone as a factor for “left shift”. It is logical that the androgen production of foetal testes ensures the stronger expression of the testosterone “left shift” in male foetuses (hence the higher incidence of left-handedness in males).The second aim of the present study was to compare the proportions of handedness in two different age groups of Bulgarians, in adolescence and senescence. It was a little surprising, and in considerable discrepancy with the data of Annett (1993) and of Halpern and Coren (Coren, 1994), that we not only did not find a reduced number of left-handers and non-right-handers among the old age group, but we established the opposite: a higher incidence of left-handedness among them (despite the statistically insignicant difference). The relatively small number of individuals in the advance age group makes us restrain from drawing conclusions, still we will point out several findings. Our data allow for evidence of a certain (statistically insignificant) reduction with the advance of age in individuals who are in the category non-right-handedness and more especially those with HQ between 0% and +35%. It should also be mentioned that the reduction is at the expense of females.Some publications claim that the reported low incidence of left-handers among old people is a result of social pressure and training to use their right hand (see Annett, 1993). We, however, did not find decreased incidence of left-handedness in the group exposed to higher degree of social pressure – the people born between 1928 and 1947. This causes us to be reserved towards assertions that training may lead to total “neglect” of the left hand. Many of the population screening studies are based on evaluation of handedness according to the hand used for writing (see Annett, 1993). It is understandable that such studies note decreased incidence of left-handedness among old age people because of their early training to use the right hand for writing. The comprehensive questionnaires, however, disclose manipulations not affected by pressure and thus verify handedness. We are inclined to think that the result of the social pressure to switch the preferred hand is successful mainly in ambidextrous individuals and those with poorly expressed lateralization. Lower rate of non-right-handers among the elderly, especially among women, in our study suggests that. It is considered that the female brain is less asymmetrically organized than the male brain (McGlone, 1980; Godard and Fiori, 2010).In conclusion, there exist significant sex differences in the proportions of handedness among Bulgarians: left-handed (non-right-handed) males are more than left-handed (non-right-handed) women. It may be assumed that some hypothetical genetic mechanisms determining handedness operate in a specific way in males and in females. Overlapping effects of the sex steroids may also play a role. There are no significant differences in the incidence of left-handedness (non-right-handedness) in young and old. There are no ground for discussing differences in the longevity in left-handers (non-right-handers) and right-handers.
AcknowledgementsThe authors would like to thank Prof. Boris Gutnik, Department of Physiology, Russian State Medical University by Pyrogov, Moscow, Russian Federation, for his valuable comments on an earlier version of this text.
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