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clinmed/2000080008v1 (August 22, 2000)
Contact author(s) for copyright information

Dr Sebastian Kraemer
Consultant Child and Adolescent Psychiatrist
Tavistock Clinic and Whittington Hospital, London

Address for correspondence
Child & Family Department 
Tavistock & Portman NHS Trust
120 Belsize Lane
London NW3 5BA
tel   020  7435 7111 
fax  020  7447 3733


The human male is on most measures, more vulnerable than the female. Part of the explanation is the biological fragility of the male fetus, which is little understood, and not widely known. A typical attitude to boys is that they are, or must be made, more resilient than girls. This adds 'social insult to biological injury'. Culture, and class, make a difference to the health and survival of boys. The data presented here have implications for the clinical management of male patients as well as for the upbringing of boys.

Downhill from conception to  birth
At conception there are more male embryos than female ones. This may be because the spermatozoa carrying the Y chromosome swim faster. The male's pole position is, however, immediately challenged. External stress around the time of conception is associated with a reduction in the male:female sex ratio, consistent with a more vulnerable male embryo[1]. From this point on it is downhill all the way. The male fetus is more likely to suffer the consequences almost all the catastrophes that can happen before birth - spontaneous abortion (male:female ratio - 1.3:1), antepartum haemorrhage (1.6:1), placenta praevia (1.2:1), abruptio placentae (2:1), toxaemia (1.3:1) and anoxia. Premature birth and stillbirth are commoner in boys. During birth the boy's brain is more vulnerable to damage and by the time he is born it is on average developmentally some days or even weeks behind his sister's: "A newborn girl is the physiological equivalent of a 4-to-6-week old boy". The new born male brain is "more completely lateralised, it is heavier, its oxygen requirements are higher _ it is an androgenized female brain"[2]. Similar differences have been observed in chimpanzees[3] .

Perinatal brain damage, cerebral palsy and congenital deformities of the genitalia, limbs and face are commoner in boys. Of course X-linked disorders such as haemophilia, Duchenne muscular dystrophy, G6PD deficiency are by definition expressed only in the male but, apart from these relatively rare conditions, why is the male so much more vulnerable? There are a number of theories. It was argued by Gualtieri & Hicks (op cit, 2)  that the male fetus has "a lower threshold of liability to neurodevelopmental problems" because it is somehow antigenic in utero. This, they suggest, is probably related to the sex-linked H-Y antigen, widespread in vertebrate males. Female developmental damage is more often genetic, while male disorders more often result from environmental deficits in combination with genetic ones. In support of this (extensively argued) hypothesis is the fact that later born boys in a family are at greater risk. Ounsted and Taylor[4] believed that the Y chromosome carried very little genetic information and suggested that antigenic dissimilarity would create a greater challenge to the developing fetus (and make it bigger). The basic model is female. "Males are attempting something extra all through life".[5]  Alongside these theories is the well-known Lyon hypothesis: mosaicism provides the female with greater biological resilience. The cells of a normal female (46,XX) contain X chromosomes from both parents but one or other is (randomly) inactivated[6]. Potential genetic defects could be diminished in their effects by being only partially present in the individual. In any case, the conception of  more males than females makes sense, given the outcome. At term the excess of male conceptions has been reduced from around 120 per 100 females to 105 per 100[7].

The male excess of developmental and behavioural  disorders
By the time a boy is born the pattern seems set. Infant death is commoner in boys[8].. Boys are more often affected by developmental disorders although girls, when they have them, may be more severely affected. Many of the developmental disorders, signs and symptoms familiar to paediatricians and child psychiatrists have a biological basis, yet the environmental contribution is often evident to the clinician. In the aetiology of specific language and reading delays (male:female ratio - 4:1), left handedness, clumsiness, stammering (4:1), autism and Asperger syndrome (4:1), attention deficit/hyperactivity disorder (4:1), conduct and oppositional disorders (5:1), tics (4:1), seizures (1.3:1) and nocturnal enuresis, genetic factors play a part, varying from a low heritability in conduct disorder to a high one in autism[9]. Why are they all commoner in boys? Few of these conditions are thought to be sex-linked in the classical sense. But Skuse et al[10] offer the intriguing possibility that the X chromosome does carry some of the burden of the social and cognitive deficits that are common to many (but not all) of these disorders. He found that phenotypically identical XO subjects with Turner's syndrome (45,X - all of whom appear to  be girls) divide into two distinct behavioural and cognitive clusters which turn out to be dependent on which parent's X chromosome they carry. Boys get their X chromosome only from their mothers, and it is the maternally derived X that is associated in Skuse's study with male-like deficits in the Turners subjects, such as hyperactivity, attention deficits, and poorer social and emotional expressivity. These results are supported by Scourfield[11] et al's twin study which shows a significant genetic influence on social cognition to the disadvantage of males. 

Social and cultural attitudes
Until birth, given that the sex of most fetuses is unknown to the parents, social attitudes and prejudices about gender cannot make any difference, but as soon as the child is born, these can amplify pre-existing biological disadvantage (or indeed reduce them, such as in traditional patriarchal societies where males are strongly favoured. In rural Bangladesh, for example, more girls than boys die during infancy and early childhood[12].) Many studies show how cultural expectations about masculinity shape the experience of  boys as they grow up. The most vulnerable are the "boys who don't talk"[13]. They become "ashamed of being ashamed"[14], seeming invulnerable, even to themselves. If parents were more aware of male sensitivity, they might change the way they treat their sons. 

Danger and despair  
The excess of accidents, including fatal ones, among boys seems to be part of a pattern of poor motor and cognitive regulation in the developing male, leading to misjudgement of risk. In adolescence the nature of risk-taking can change and may lead to dangerous experiments with drugs and alcohol, or to violence against the self and others. As is now well known, the suicide rate in young men is several times higher than in young women, and had from the late 1970s until recently[15] risen alarmingly in Britain and several other western nations. The dramatic rise in this statistic (which goes in parallel with a soaring rate in violent crime - also largely due to males[16]) implicates powerful social factors, rather than biological ones, at work here. For example the male to female ratio of suicides in the 15-24 age group varies from 7.1:1 in Ireland to 1.1:1 in Mauritius. (The only recorded female excess in this age group is 1.4:1 in Tajikistan.[17]) There is similar social variation within countries in death rates from all causes. For example in England and Wales the death rate in boys under 16 is 41% greater than in girls, yet the social class differences are even greater, with more than twice as many dead boys in social class V than in social class I [18].

Educational disadvantage
Co-education has exposed another difference which may have been less evident (even though paradoxically more pronounced[19]) in the past: that girls are better at most academic subjects than boys. The English General Certificate of Secondary Education (GCSE) exam results (taken at age 16) only relatively recently collected on a nation-wide scale, show a significant gap between the sexes in scholastic achievement (42,8% boys vs 53.4% girls get A*-C grades at GCSE[20]). It may be that disruptive ('boyish') behaviour is less tolerated in modern schools than it was in the past, or that there is more of it[21]. As with the effects of postnatal depression (below), however, there is also a strong social effect. The male-female academic gap is wider in lower social classes[22]. 

Males are better at throwing and map reading, but more out of touch 
Males, meanwhile, tend to have superior skills in maths and other non-verbal tasks, fitting in with Labarthe's interesting finding that 2 year old boys are on average already better than girls at building a bridge with toy bricks[23]. Other data confirm the superiority of males in spatial and navigational skills, such as throwing, map reading[24], chess and architecture. Yet even these are not fixed qualities. Spatial ability, for example, is better in females of the Inuit (Eskimo).[25]  One specific spacial skill seems less changeable. Males have on average consistently maintained a superior ability to match figures rotated at different angles[26]. 

The psychosocial correlates of these differences are well known. Girls have better literary skills and are more articulate at expressing themselves, while boys tend to clam up, especially when there is high emotion, and just feel uncomfortable and awkward without knowing why. The much studied quality 'alexithymia' - the lack of an emotional vocabulary - is much commoner in boys[27], and it is not difficult to see how such a quality could lead to adverse outcomes when a boy is under social, academic, or emotional (especially sexual) stress. Alexithymia is associated with deficits in interhemispheric transfer across the brain[28], a feature also noted in Hopkins and Bard's study of infant chimpanzees (op cit,  3) 

Even though almost all the most powerful positions in politics and business are still occupied by men, recent social changes in post-industrial societies do not favour the majority of males. (Meanwhile in the rest of the world men retain social advantages. Of 960 million illiterate people in the world, two thirds are female[29].) Disorders of addiction, particularly substance abuse, are commoner in males. Even when ill, men may not notice signs of illness[30],  and when they do, they are less likely to seek help from doctors[31]. This tendency no doubt accounts for some of the excess suicides in males. In his despair the victim believes that no help is available, that talking is useless. If baby boys are typically harder to care for  (see below) it is arguable that they will as adults be more likely to feel alone.

More lethal diseases
Later in life the process continues unabated. Circulatory disorders, diabetes, alcoholism, duodenal ulcer, lung cancer are all commoner in men[32] (while women have significantly higher rates of depressive, eating and rheumatic disorders).  Male suicide rates continue to exceed female ones throughout life and, as is universally known, women survive men by several years in almost all countries, and the gap is widening. Androgens could be implicated in the earlier death of males, but recent studies suggest that female mosaicism may enhance lifespan.[33]  

There is unlikely to be a single explanation for all the foregoing differences, but it is worth exploring the period in life where inborn qualities may interact with environmental ones.  

Infant boys are more sensitive 
If new-born baby boys tend to be less mature then they probably require more attentive care. Trevarthen[34] observed that parents tend to imitate new-born boy babies more than they do girl babies, suggesting that caregivers have to work harder with boys. Tronick and Weinberg state "infant boys are more emotionally reactive than girls. They display more positive as well as negative affect, focus more on the mother, and display more_distress and demands for contact than do girls. Girls show more interest in objects, a greater constancy of interest, and better self regulation of emotional states"[35]. At six months mothers in Malatesta and Haviland's non-clinical study had a wider repertoire of communication about emotional states with girls than with boys. "..... very significant sex difference for the expression of interest, with female infants displaying interest expressions more frequently than males .... female infants have more open eyes and higher brow placements than male infants [which] may serve to lead observers to quite different overall impressions about male and female sociability"[36]. Boys tended to be too excitable and mothers did all they could to soothe and settle them, at some cost to their development.  One of the findings of Murray[37],[38] and her colleagues is that boys are more affected by maternal postnatal depression than girls, extending into nursery school years, long after the depression has lifted. One of the most notable effects is inattentiveness and hyperactivity, especially in boys from lower social class families. In Fivush's study of  communication styles of mothers with their almost three year old children, the mothers did not attribute anger to any of their daughters, only to their sons[39] suggesting that significant differences in managing emotional states are already established before 3 years. Apart from anger boys show less, but may feel more, emotion than girls, as shown by  physiological measures, such as heart rate variability, taken when a group of six year old girls and boys were listening to the sound of a crying baby. Many more girls than boys spoke kindly to what they assumed was a real infant, while more than twice as many boys simply turned the speaker off[40]. 

Thirty years ago Rutter showed how vulnerable boys are to chronic stress in the home.[41] In a recent study of the effects of early significant losses, although the numbers were about equal in both sexes, boys dismissed the experiences as of little concern more often than girls, while girls were more often overpreoccupied by them.[42]. Neither of these are healthy responses, but this finding is consistent with the male habit of not asking for help when it is needed. In a sample of British GPs, male doctors showed more anxiety and depression than female doctors (and more than the average male population) and were more likely to to avoid contact with other people when stressed[43]. 

The care of boys is generally more difficult and therefore more likely to go wrong, adding to the deficits already existing before birth. Since most of the growth of the human brain takes place after birth, some early environmental stressors could lead to disadvantage for boys being 'wired in'. In any case in boys the formation of secure attachment to a caregiver is more subject to parental unavailability, insensitivity or depression: insecure attachment is more common in boys[44]. Consistent with this is the observation that male rhesus monkeys partially or totally isolated from maternal care are more likely to 'freeze' in test situations than matched females, who are more active and curious[45].

Before concluding that maleness is a genetic disorder it is important to note that the foregoing data (which is in any case mostly British or American) is embedded in social values about normality. A hominid male of, say, half a million years ago may have needed all the opportunities for risk taking he could get, just in order to procreate. Darwin noted this[46]. Many male mammals fail in their primary biological goal, which is to reproduce. They risk instead being excluded, wounded or killed by rivals. Rivalries in human societies are more complex, and it may  be that one of the features of the historical process of which we are a part is that competition for females is replaced by competition with them[47]. Survival skills required by modern people are not very similar to those required by our ancestors, even if we still have most of the same genes. Male advantages in physical strength and spatial skill were probably more useful in the past. In contrast, while the preeminence of the few men who reach to the very top of public life is barely dented by women, the modern male is now more often seen as lacking female qualities, such as self regulation and reflectiveness.

It is clear that the male is more vulnerable from the beginning of life. Where caregivers assume that from birth a boy ought always to be tougher than a girl, his inborn disadvantage will be amplified. (Yet where males are more highly valued, as the Bangladesh study shows[48], they get relatively better care, probably because girls are neglected). The data presented here have implications both for the clinical management of male patients (especially, perhaps, by male doctors), and for the upbringing of boys in general. The more developmental problems there are, the more sensitive care is required. Yet difficult babies often receive less good care, precisely because they are more difficult to look after. Biological and social constraints work together against the interests of the male.

Most discussions (with a few honourable exceptions[49],[50]) tend to ignore one side or the other of the story. While there is plenty written about gender from a social and philosophical perspective, and about sexual differences from a Darwinian and biological point of view, there is little evidence of discussion between them, and apparently little curiosity as to why boys are vulnerable to so many stressors that might confront them. The implicit assumption of the majority of scientific writers (most of whom until this generation were themselves men) has probably been that 'boys will be boys'. Perhaps they will, but the matter needs exploring in a more coherent way. 

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