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Development and Psychopathology, 13 (2001), 653–676

Copyright  2001 Cambridge University Press


Printed in the United States of America

Can poverty get under your skin?


Basal cortisol levels and cognitive
function in children from low and high
socioeconomic status

S. J. LUPIEN,a,b S. KING,a M. J. MEANEY,a AND B. S. MCEWENc


a b
Douglas Hospital/McGill University; Montreal Geriatric Institute; and
c
Rockefeller University

Abstract
It is well known that individuals from more advantaged social classes enjoy better mental and physical health than
do individuals within lower classes. Various mechanisms have been evoked to explain the association between
socioeconomic status (SES) and health. One mechanism that has received particular attention in recent years is
stress. It has been shown that individuals lower in SES report greater exposure to stressful life events and a greater
impact of these events on their life than individuals higher in SES. In order to measure whether the development of
the relationship between SES and mental health is sustained by exposure to high levels of glucocorticoids, we
measured morning salivary cortisol levels as well as cognitive function (memory, attention, and language) in 307
children (from 6 to 16 years of age) from low versus high SES in the Montreal area in Canada. The results revealed
that low SES children from 6 to 10 years old present significantly higher salivary cortisol levels when compared to
children from high SES. This difference disappears at the time of school transition, and no SES differences are
observed in salivary cortisol levels during high school. However, children from low and high SES do not differ with
regard to memory or to attentional and linguistic functions. Also, mothers of low SES children reported higher
feelings of depression and more unhealthy behaviors, while mothers of high SES children reported higher stress
related to work or family transitions. Altogether, these results show that low SES in young children is related to
increased cortisol secretion, although the impact of SES on cortisol secretion is absent after transition to high
school. These data are interpreted within the context of the equalization process of class patterning. Four social
explanatory factors are suggested to explain the disappearance of SES differences in basal cortisol levels after
school transition, taking into account the influence of family environment on the child’s secretion of stress
hormones.

It is well known that individuals from more than do individuals from disadvantaged envi-
advantaged backgrounds enjoy better health ronments (Anderson & Armstead, 1995; An-
tonovsky, 1967). In the health literature, the
terms “social class” and “socioeconomic sta-
tus (SES)” are often used interchangeably.
This study was supported by a grant from the John D.
However, in disciplines such as sociology,
and Catherine T. MacArthur Foundation. S.J.L.’s work
was supported by a scientist award from the Fonds de la
they bear different meanings. “Social class” is
recherche en santé du Québec (FRSQ) and by a Young a term widely used in theories of social order-
Investigator Award from the National Alliance for Re- ing and class categories, such as Marx’s the-
search on Schizophrenia and Depression (NARSAD). ory (Wright & Perrone, 1977) and others.
Address correspondence and reprint requests to: “SES,” as used in the sociological literature,
Sonia Lupien, PhD, Director, Laboratory of Human Psy-
choneuroendocrine Research, Douglas Hospital/McGill is function of education, income, or occupa-
University, 6875 Boulevard Lasalle, Montréal PQ H4H tion (Dutton & Levine, 1989). Epidemiologic
1R3 Canada; E-mail: Lupson@douglas.mcgill.ca. studies and census data have provided the

653
654 S. J. Lupien et al.

most well known associations between SES high versus low SES: children from low SES
and health. It has been shown that the risk of showed deficits in language, memory, and at-
mortality, the prevalence and course of dis- tentional capacities when compared with chil-
ease (Pincus, Callahan, & Burkhauser, 1987), dren from high SES.
and blood pressure (Dyer, Stamler, & Shek-
elle, 1976) increase significantly as employ-
Mechanisms Underlying the Association
ment grade (Marmot, Shipley, & Rose, 1984),
Between SES and Health
occupational status (Adelstein, 1980), income
(Pappas, Queen, Hadden, & Fisher, 1993), Various mechanisms have been evoked to ex-
and years of education (Adelstein, 1980) de- plain the association between SES and health.
crease. A link has also been observed between Three of them have received particular atten-
SES and the prevalence and course of disease tion in recent years (for a review, see Adler,
(Pincus et al., 1987). Finally, it has been Boyce, Chesney, Folkman, & Syme, 1993;
shown that blood pressure is higher in indi- Boyce, Chesney, Cohen, Folkman, Kahn, &
viduals lower on the SES hierarchy (Dyer et Syme, 1994). First, it has been proposed that
al., 1976; Keil, Tyroler, & Sanfider, 1977; the empirical link between SES and health is
Matthews, Kelsey, & Meilahn, 1989; Syme, due to underlying genetic factors. Genetically
Oakes, & Friedman, 1974) and that this asso- based physical or mental factors might lead
ciation is closely related to race, which in it- to lower social position and poorer health. As
self is closely associated with SES (Bureau of noted by many researchers (see Adler et al.,
Labor Statistics, 1967; Kahn, Williamson, & 1994; Anderson & Armstead, 1995), this ex-
Stevens, 1991; Keil et al., 1977; Susser, Wat- planation is plausible but improbable because
son, & Hopper, 1985). Although most of the the association between SES and health per-
literature on the association between SES and sists even after adjusting for factors such as
health has concentrated on systemic disease, height, body mass index, and cognitive flexi-
other studies have shown a significant rela- bility. Second, it is suggested that the associa-
tionship between SES and mental health. In- tion between SES and health is due to the in-
verse associations have been reported be- fluence of illness on SES, rather than of SES
tween SES and prevalence of schizophrenia on illness. It has been reported that, although
(Dohrenwend, 1990), as well as between SES there is evidence that mental and physical dis-
and depression (Hirschfeld & Cross, 1982). turbances may lead to lower SES, available
The relationship between SES and health data on this association does not explain it in
begins at the earliest stages of life (Ander- its totality (see Anderson & Armstead, 1995).
son & Armstead, 1995). According to Star- The third explanation for the association be-
field (1982), who reviewed the literature on tween SES and health is that SES may lead to
SES and child health, a SES–health linkage behaviors that, in turn, will influence health
has been found with the following health status. Income, education, and occupation,
problems: lead poisoning, vision problems, which are all components of SES, may shape
otitis media and hearing loss, cytomegalic in- an individual’s life course and determine his
clusion disease, and iron deficiency anemia. or her health outcome. The physical environ-
Langford, Watson, and Douglas (1968) have ment in which one lives, the social environ-
reported results on 1,765 high school girls and ment and associated vulnerability to interper-
showed that the lower the SES of the parents, sonal aggression and violence, and the health
the higher the blood pressure of the girls. In behaviors related to a particular lifestyle, as
addition, mental retardation, learning disor- well as socialization and experiences, may all
ders, and emotional and behavioral problems be candidate variables that may contribute to
occur at greater frequency among children of the association between SES and health (see
lower SES (Anderson & Armstead, 1995). McLeod & Kessler, 1990). For example, ciga-
Another study by Ardila and Rosselli (1995) rette smoking (Winkleby, Fortmann, & Bar-
in Columbia reported significant develop- rett, 1990) and lack of physical activity
mental differences between children from (Cauley, Donfield, Laporte, & Warhaftig,
Basal cortisol levels in low and high SES children 655

1991) are inversely related to SES and are events on their life than individuals from
positively associated with poor health out- higher SES (Dohrenwend, 1973). This sug-
comes (Winkleby et al., 1990). Moreover, gests that individuals from lower SES may
psychological characteristics such as anger have greater vulnerability to stress and, subse-
and hostility, emotional suppression, depres- quently, to disease.
sion, and pessimism or fatalism (for a review, The association between SES and stress
see Scheier & Bridges, 1995) relate to both may stem from environmental and social–
SES and disease risk (Barefoot, Dodge, & Pe- psychological factors. With regard to environ-
terson, 1989; Murphy, Olivier, Monson, & mental factors, it is known that, as one moves
Sobol, 1991). down the SES ladder, residential choices be-
Although behavioral or personality traits come more limited and many of the environ-
may shed some light on the association be- ments in which individuals lower on the SES
tween SES and health, they do not explain the hierarchy live are associated with increased
significant relationships observed between mortality rate and crime (Haan, Kaplan, &
SES and health in children (Langford et al., Syme, 1989). It has been suggested that these
1968), in whom such risk behaviors or per- differences in environments vary objectively
sonality traits may not yet be developed. Most in chronic exposures to stressor events (Har-
of the research performed on the association burg, Erfurt, Chape, Hauenstein, Schull, &
between SES and health suggest that we Schork, 1973). With regard to sociological–
should see the largest socioeconomic differ- psychological factors, it has been shown that
ences in health during middle and early old higher SES decreases the likelihood of expo-
age because these age groups are most likely sure to negative events such as social aggres-
to be characterized by sizable socioeconomic sion and risk behaviors (Dohrenwend & Doh-
differentials in exposure to risk factors (see renwend, 1970). Individuals of lower SES are
House, Kepkowski, Kinney, Mero, Kessler, & exposed to a higher rate of change or instabil-
Herzog, 1994; West, 1997). ity in their lives, and this instability has been
found to produce a higher level of individual
distress in lower SES individuals (Broadhead,
Stress as the Missing Link?
Kaplan, & James, 1983; Dohrenwend & Doh-
So, health behaviors and personality traits renwend, 1970).
represent two pathways by which SES may This association between SES and stress
influence health, but they do not account for has led researchers to look for the effects of
all of the association. Other potential path- stress on health as the possible missing link
ways by which SES may influence health are in the global association between SES and
through differential exposure of the individu- health. It has been shown that prior life stress
als to physical and social contexts that may is related to cardiovascular disease (Bros-
be damaging for their health. A factor that has schot, Benschop, Godaert, De Smet, Olff,
received a great deal of attention in recent Heijnen, & Ballieux, 1994), sudden cardiac
years is stress (for recent reviews, see Mar- death (Rahe & Lind, 1971), birth complica-
mot & Feeney, 2000; Steptoe, 2000). Stress is tions (Gorsuch & Key, 1974), seriousness of
generally defined as previous or actual expo- chronic illness (Wyler, Masuda, & Holmes,
sure to life events that require adaptation from 1971), and the exacerbation of symptoms
the individual (Selye, 1950), or else as a state among persons with chronic illness (Bedell,
occurring when an individual perceives that Giordani, Amour, Tavormina, & Boll, 1977).
the demands of the environment exceeds his Prior stressful life events, as well as perceived
or her ability to cope (see Adler et al., 1994). stress, have also been shown to alter immune
The association between SES and health may function (Calabrese, Kling, & Gold, 1987;
result in part from differential exposure to Jemmott & Locke, 1984; Kennedy, Kiecolt–
stress. It has been shown that individuals from Glaser, & Glaser, 1988; Kiecolt–Glaser &
lower SES report greater exposure to stressful Glaser, 1991, 1995; McKinnon, Weisse, &
life events and a greater impact of these Reynolds, 1989; Naliboff, Benton, Solomon,
656 S. J. Lupien et al.

Morley, Fahey, Bloom, Makinodan, & Gil- also been reported on mood or cognitive pro-
more, 1991; Schleiffer, Keller, & Camerino, cessing. Breier, Albus, Pickar, Zahn, Wol-
1983; Ursin, Mykletun, & Tonder, 1984), and kowitz, and Paul (1987) have exposed healthy
stress has been reported to affect mood or human volunteers to the stress of loud noise
cognitive processing (for a review, see Lu- under controllable and uncontrollable condi-
pien & McEwen, 1997). Direct effects of tions. Subjects submitted to the uncontrollable
stress on the immune function have been re- stress conditions reported higher self-ratings
ported by Brosschot, Benschop, Godaert, De of helplessness, lack of control, tension, un-
Smet, Olff, Heijnen, and Ballieux (1992), happiness, anxiety, and depression than sub-
who submitted young male subjects to a mild jects submitted to the controllable stress con-
and potentially uncontrollable interpersonal dition.
stress situation. They showed that, in contrast
to control subjects, experimental subjects
SES, Stress, and Health in Children
showed a significant increase in numbers of
natural killer cells after the stress period. In children, it has been hypothesized that the
There is some other direct evidence that psy- child’s response to stress experienced in the
chological stress also increases the risk of ver- early years may have long-term effects upon
ified acute infectious respiratory diseases future development of psychosomatic diseases
(Boyce, Jensen, Cassel, Collior, Smith, & Ra- (Tennes & Kreye, 1985). However, immediate
mey, 1977; Graham, Douglas, & Ryan, 1986). effects of stress on children’s health have also
Cohen, Tyrell, and Smith (1991) have studied been reported (Gunnar, Gonzales, Goodlin, &
the relationship between psychological stress Levine, 1981; Gunner, Connors, & Isensee,
and the frequency of documented clinical 1989, 1992; Knight, Atkins, Eagle, Evans, Fin-
colds among subjects intentionally exposed to kelstein, Fukushima, Katz, & Weiner, 1979).
respiratory virus. They showed that the rates Cohen, Evans, Krantz, and Stokols (1980) mea-
of both respiratory infection and clinical colds sured the blood pressure of children in ele-
increased in a dose–response manner with in- mentary schools that differed in terms of
creases in the degree of previously reported amount of noise in the environment. They
psychological stress. compared children from schools that were be-
Stress has also been shown to affect mood or neath the flight path of the Los Angeles Inter-
cognitive processing (for reviews, see Lupien, national Airport with children from schools of
Lecours, Schwartz, Sharma, Meaney, & Nair, quieter areas. They showed that children from
1995; Lupien, Gandreau, Tchiteya, Mahue, the noisy school areas presented a higher blood
Sharma, Nair, Hauger, McEwen, & Meaney, pressure than children from the quieter school
1997; Lupien & McEwen, 1997; Lupien et al., areas. Moreover, they reported that children
1994). Life stress has been found to be corre- from the noisy areas were more distractable
lated with psychiatric symptomatology (Dek- and had more difficulty with problem-solving
ker & Webb, 1974), and several researchers tasks than the other children. More impor-
have found life stress scores to correlate with tantly, children from the noisy areas presented
measures of anxiety and depression (Vino- trouble learning how to discriminate between
kur & Selzer, 1975), as well as with indices irrelevant noise and the relevant task, which
of academic (Harris, 1972) and work perfor- supposes that stress may affect selective atten-
mance (Carranza, 1972). A variety of other tion (i.e., the ability to discriminate between
studies have suggested that high levels of anx- relevant and irrelevant information).
iety and arousal as induced by stress are nega- Similar findings have been reported by Co-
tively related to performance on complex hen, Glass, and Singer (1973). Although
tasks (Eysenck, 1976), to the ability to utilize adults can adapt to stressful events, stress in
semantic cues in recall (Mueller, 1976), and itself may have the most detrimental effects
to a lesser degree of cue utilization in atten- on children. They studied the effects of living
tional tasks (Bacon, 1974; Easterbrook, 1959). in apartments built directly over congested
More direct and acute effects of stress have highways in New York City. They showed
Basal cortisol levels in low and high SES children 657

that, despite the relatively higher noise levels liams, 1995). In this regard, the hypothala-
on lower floors of the buildings, residents of mic–pituitary–adrenal (HPA) system plays a
lower floors did not differ from neighbors on key role in coordinating an organism’s physi-
upper floors in ratings of noise level or annoy- ologic reactions to environmental challenges
ance. However, the ability of children living and has received a great deal of attention in
on lower floors to discriminate between simi- recent years. The adrenal glucocorticoid hor-
lar sounds was lower than that displayed by mone cortisol is the principal effector in this
children living on upper floors. Thus, children system and is thought to be responsible for
on the lower floor adapted to the noise by both adaptational and maladaptational pro-
“tuning out” sounds which resulted in a lower cesses in response to perturbing situations
responsiveness to differences in spoken words. (Munck, Guyre, Holbrook, 1984).
This further affected their reading ability and The secretion of glucocorticoids from the
this latter fact was apparent in long-term read- adrenal cortex is under the control of the adre-
ing impairments. nocorticotrophin hormone (ACTH), which in
These results suggest that stress in early turn is released from the anterior lobe of the
age may affect health (blood pressure), as pituitary. Adrenocorticotrophin secretion is
well as cognitive processing. Moreover, stress regulated by corticotropin releasing factor
in school has widely been perceived as having (CRF) and other secretagogues from the hy-
an impact on the developing socioemotional pothalamus (Keller–Wood & Dallman, 1984).
life of children (Bower, 1964; Phillips, 1978; Several closed feedback mechanisms regulate
Rutter, 1980). Given that urban socioecologi- the secretion of glucocorticoids. Circulating
cal areas vary in rates of stressor conditions glucocorticoids act on the pituitary directly to
(see Harburg et al., 1973), it is possible that inhibit ACTH secretion, and on the hypothal-
schools in low SES areas lead to more stress- amus to suppress secretion of CRF (Keller–
ful conditions in children than schools in Wood & Dallman, 1984). These feedback
higher SES areas. The long-term effects of loops enable the organism to maintain a stable
these differences may have an impact on the blood level of glucocorticoids at all times,
SES–health relationship. while simultaneously providing an emergency
override, via the central nervous system, to re-
spond to stressors.
Impact of Stress Hormones on
When the HPA system is functioning un-
Physical Health
der basal conditions, cortisol levels generally
So, stress is one major factor that has been follow a circadian rhythm with elevations of
proposed in order to explain the association cortisol levels in the morning and decreases
between SES and health. Individuals from in cortisol over the day. Following the onset
lower SES areas may be subjected to more of a stressor, however, cortisol levels raise
stressful events and have less ability and re- rapidly (in a range of 10–15 min), initiating
sources to cope with them, which will eventu- the peripheral catabolic processes required for
ally lead to disease. Although this proposal mobilizing energy reserves to meet the meta-
may help one understand part of the associa- bolic demands imposed by the stressor (Bax-
tion between SES and health, it does not offer ter & Tyrrell, 1987). Although it is well docu-
an explanation as to the physiological mecha- mented that other steroid hormones are also
nisms by which differences in stress environ- affected by stress, cortisol is still considered
ments may alter physical and mental function. one of the best markers of altered physiologi-
For this reason, a second-order class of mech- cal states in response to stressful stimulation
anisms is now evoked in order to explain the (for reviews, see Kirschbaum & Hellhammer,
SES–stress–health relationship, namely the 1989, 1994). As early as 1943, it was shown
potentiation of disease as a result of behavior- that flight in test pilots and instructor pilots
ally stress-evoked perturbations of the body’s leads to an elevation in urinary cortisol excre-
principal axes of neuroendocrine response tion (Pincus & Hoagland, 1943). Further stud-
(see Manuck, Marshland, Kaplan, & Wil- ies showed increases in cortisol excretion in
658 S. J. Lupien et al.

race-car drivers (Frost, Dryer, & Kohlstaedt, Although short-term glucocorticoid re-
1951), parachute jumpers (Basowitz, Persky, sponse to stress serves an adaptative function,
Korchin, & Grinker, 1955), and subjects tak- chronic exposure to elevated glucocorticoid
ing final college examinations (Markkanen, concentrations contributes to the onset of pa-
Pekkarinen, Pulkkinen, & Simola, 1956). Bliss, thology, ranging from an increased resistance
Migeon, Branch, and Samuels (1956) sur- to insulin, hypertension, hypercholesterol-
veyed the literature on cortisol excretion in emia, arteriosclerosis, and immunosuppres-
studies measuring the relatives of emergency- sion (Munck et al., 1984). Glucocorticoids ex-
room patients, medical students taking final ert multiple and complex effects on the
examinations, and normal subjects in day-to- immunologic apparatus. At plasma levels gen-
day events, as well as through a number of erally achieved during stress, glucocorticoids
laboratory techniques of eliciting emotional exert immunosuppressive and antiinflamma-
disturbances, and concluded that the emotional tory effects (Bateman, Singh, Kral, & Solo-
disturbances associated with most of these situ- mon, 1989; Calabrese et al., 1987; Munck et
ations caused modest but consistent increases al., 1984). It is known that natural killer cells
in plasma and urinary cortisol levels. and cytotoxic T cells play a pivotal role in
Cortisol can now be measured easily and defending the organism against viral infection
noninvasively in small samples of saliva. The (Sheridan, Feng, Bonneau, Allen, Huney-
measurement of steroid concentrations in sa- cutt, & Glaser, 1991). Stress has been shown
liva has a number of potential advantages to influence the development of viral infec-
over the more conventionally used total serum tion (for a review, see Cohen, 1988; Cohen &
concentrations. These advantages include a Wills, 1985; Cohen et al., 1991), and it has
stress-free and noninvasive collection proce- been suggested that adrenal steroids are in-
dure and the measurement of a parameter volved in the stress effects on immunity
which is believed to reflect the biologically (Rabin, Cunnick, & Lysle, 1990).
active, serum-unbound steroid concentration Even if glucocorticoids act primarily at a
(Mendel, 1989; Robbins & Rall, 1957). High peripheral level to maintain homeostasis, the
correlation coefficients have been reported brain represents one of the principal targets
between plasma and salivary cortisol in el- for these steroid hormones. Circulating gluco-
derly, in adults (Harris, Watkins, Cook, corticoids easily cross the blood–brain barrier
Walker, Read, & Riad–Fahmy, 1990; Mc- and exert their actions in the central nervous
Cracken & Poland, 1989; Woodside, Win- system at steroids receptor sites. In the brain,
ter, & Fisman, 1991), and in children (Bober, glucocorticoids exert their actions primarily
Weller, Weller, Tait, Fristad, & Preskorn, on the hippocampus, which is the brain area
1988; Gunnar, Hertsgaard, Larson, & Riga- richest in glucocorticoids receptors (McEwen,
tuso, 1992). A wide variety of studies have Weiss, & Schwartz, 1968). Two types of re-
shown significant increases in saliva cortisol ceptors have been described, according to
in the same stress conditions as those showing their affinity for different glucocorticoids
increases in plasma cortisol levels (for a re- (Reul & deKloet, 1985). Type I receptors (or
view, see Kirschbaum & Hellhammer, 1994). mineralocorticoid receptors) show a high af-
Due to the noninvasive nature of samplings, finity for glucocorticoids and appear to serve
several studies have recently emerged on sali- as the major receptor that, when occupied,
vary cortisol stress responses among new- regulates normal basal activity in the HPA
borns and infants. Increases in saliva cortisol axis. Type II receptors (or glucocorticoid re-
in newborns have been observed during dis- ceptor) show a low affinity for glucocorti-
charge examinations (Gunnar et al., 1989), in- coids and is occupied during the diurnal peak
oculation of infants by a pediatrician (Lewis of cortisol or in response to stress (Reul &
& Thomas, 1990), a brief maternal separation deKloet, 1985).
(Larson, Gunnar, & Hertsgaard, 1991). These Prolonged exposure to elevated glucocorti-
results indicate that the human HPA system is coid levels under endogenous or exogenous
highly responsive from a very early postnatal conditions has been shown to lead to hippo-
period. campal neuronal dysfunction or neuron loss
Basal cortisol levels in low and high SES children 659

(Landfield, Baskin, & Pitler, 1981). Sapolsky, chological stimuli. This reaction is in part de-
Krey, and McEwen (1986) exposed young termined by social context and the social sta-
rats to stresslike levels of glucocorticoids for tus of the individual. Second, the stimulus
3 months and compared these animals to old, will have an effect on the individual’s infor-
untreated controls. They showed that the two mation processing system (the “processor”),
groups exhibited similar anatomical sequelae, and the response of the processor will be de-
including a significant loss of neurons in the termined by genetic makeup, stage of biologi-
hippocampal regions and increases in the den- cal development, gender, past learning, and
sity of microglia. Thus, exposure to high lev- social history. If, at this point, the stimulus is
els of glucocorticoids appeared to accelerate perceived as a threat, and the source of the
the brain aging process in young rats. In order threat is unknown, the individual will become
to see if endogenous elevations of glucocorti- highly vigilant and try to determine the real
coids induced by stress may have the same nature (threat vs. nonthreat) of the stimuli. If,
effects upon hippocampal cells, Kerr, Camp- on the contrary, the stimulus is perceived as a
bell, Applegate, Brodish, and Landfield (1991) threat and the source of it is known, the indi-
applied stress to young, middle-aged, and old vidual will try to find a coping response to the
rats for 6 months and measured hippocampal threat. If no response is available, helpless-
changes. The results showed that the younger ness or hopelessness may appear, with its al-
groups under stress exhibited increased evi- tered physiologic responses. If a response is
dence of aginglike neurophysiological changes. available, the outcome of it will depend on the
So, the possibility that stress-induced long- cost of that response. If a low-cost response is
term elevations of endogenous corticosteroids appropriate, no stress response will be initi-
levels might accelerate or induce brain aging- ated. If a high-cost response is needed, it may
like neuropathology may have considerable necessitate the appearance of aggression or
implications for human health. thrill-seeking or risk-taking behaviors. How-
ever, the available response can also be
thwarted, which will eventually lead to dis-
The Model of Allostatic Load
placed frustration or aggression. So, percep-
This suggestion goes along with a recent tions of threat and choice of response are cen-
model of stress and health developed by tral aspects of the assessment of risk and
McEwen and Stellar (1993). Their model, making choices leading to health-damaging or
called the “allostatic load” model, is based on health-promoting behaviors. The biological
the concept of allostasis—the ability of the side of the allostatic load model can be di-
body to increase or decrease vital functions to vided into mediators, effectors, and disease
a new steady state following a challenge— outcomes. The mediators of the stressful stim-
proposed by Sterling and Eyer (1988). In or- uli are the brain, the autonomic nervous sys-
der to define allostatic load, McEwen and tem, and the neuroendocrine system. We
Stellar (1993) give the analogy of two heavy know that all three are affected by chronic
versus two light weights on a seesaw. Al- stress leading to allostatic load (for a review,
though both heavy and light weights are well see McEwen, 1998). The effectors are the
balanced on the seesaw, the see-saw itself ex- main organ systems, the immune and cardio-
periences more strain with the two heavy vascular systems, adipose tissue, and muscle,
weights than with the two light weights. Allo- responding to the mediators.
static load refers to the strain put on an other- This model can be used to explain part of
wise balanced system. Thus, the strain pro- the association between SES and health. Indi-
duced by repeated assaults to physiologic viduals from lower SES areas may be submit-
response, as well as that produced by elevated ted to a greater amount of environmental, so-
activity of physiologic systems under chal- ciological, and psychological challenges, and
lenge, will, by increasing the allostatic load, these events will increase the probability that
predispose an organism to disease. The first the individual will process more incoming in-
factor in McEwen and Stellar’s model is the formation as being threatening (real or fic-
reaction of the individual to physical and psy- tive). Individuals from lower SES areas are
660 S. J. Lupien et al.

also known to have fewer coping resources adolescents was gathered using the school
for stressful events, which will also increase system, within only one school board com-
the probability that the individual will come mission (Commission des Ecoles Catholiques
to the conclusion that he or she has no re- de Montreal: [CECM]). This was done in or-
source to cope with the stressor and that a der to ensure a similar schooling procedure
costly response will have to be taken. This for all subjects. The CECM governs the ma-
latter path may lead to more frequent and jority of French-speaking schools in the Mon-
larger increases in cortisol levels or to a treal urban community. With the help of cen-
greater probability of establishing risk behav- sus data, and in conjunction with the CECM,
ior or personality traits that will, eventually, we chose schools for the study according to
lead to disease. the SES levels of the neighborhoods in which
the schools are located (low and high SES)
and according to grade level (elementary: 1,
Goal of the Study
3, 5; high school: 1, 3, 5). The CECM uses a
The main goal of the present descriptive study criterion for SES using parents’ income and
was to measure salivary cortisol levels in chil- education level, and this criterion has been
dren of low and high SES and from different shown to be a reliable one for description of
age groups in order to measure whether SES the socioeconomic background of these chil-
differences in salivary cortisol exist and if dren. Within each of these schools, students
these differences vary according to age. The were sampled randomly within grade levels
second goal of the study was to measure the from a list provided by the school. A total of
relationship between salivary cortisol levels 307 children of low and high SES were stud-
and cognitive function in this population, as ied, and there were no significant differences
well as possible changes in this relation as a between ages of children from same grades
function of age. Finally, the third goal of this but of different SES. Every child was in good
study was to measure whether scores of chil- general health as reported in school records.
dren’s parents on various stress questionnaires The only exclusion criteria for the present
differed with regard to SES. study was the presence of asthma or the use
of corticosteroids as treatment.
Written consent was obtained from the
Material and Method
mothers. Consenting mothers were also asked
if they would be interested in participating in
Population
a 40-min phone interview in which they
A cross-sectional experimental design was would be asked to answer two questionnaires
used, with six age groups (ranging from 6 to measuring environmental and family stres-
16 years old) and two categories of SES (low, sors, as well as to answer questions relative
high1). The age groups were determined ac- to income, education, and so forth. Mothers
cording to grade—that is, elementary school had the choice of participating in the study
(Grades 1 [mean age: 6 years], 3 [mean age: in conjunction with their child or refusing to
8 years], and 5 [mean age: 10 years]) and high participate although they consented their child
school (Grades 1 [mean age: 12 years], 3 to participate. The demographic questions re-
(mean age: 14 years], and 5 [mean age: 16 lated to both mothers and fathers were put to
years]). The entire population of children and the mothers in order to verify SES as obtained
from the CECM. The sample of children and
1. Note that the high SES group was defined as families parents from low and high SES who were
with an income higher than $50,000. In Quebec, Can- tested is presented in Table 1. Fifty-three per-
ada, the average family income is between $30,000 and cent of low SES parents and 61% of high SES
$35,000. Children from higher SES (higher than parents consented to the 40-min phone inter-
$100,000) were not tested given that the majority of
these children are placed in private schools, which view, which allowed us to measure various
were not part of the CECM School Board of Montreal stressors in the parents using a representative
(see below). sample.
Basal cortisol levels in low and high SES children 661

Table 1. Sample of children and parents from low and high socioeconomic status (SES)

Low SES High SES

Number of Number of Participation Number of Number of Participation


Children Parents (%) Children Parents (%)

Children’s grade level


Elementary 1 36 22 61.1 12 10 83.3
Elementary 3 25 11 44 18 12 66.7
Elementary 5 35 22 62.8 15 12 80
High school 1 20 11 55 26 19 73.1
High school 3 27 13 48.1 35 21 60
High school 5 24 10 41.6 34 12 35.3
Total 167 89 53.2 140 86 61.4

Children’s assessment session that measured memory, attention, and


linguistic functions. The neuropsychological
Cortisol levels. Saliva samples for cortisol
session lasted for about 1 hr and was per-
levels determination were taken in the morn-
formed in the classroom, using a group-test-
ing, at 8:00 a.m., at the beginning of the neu-
ing method. Presentation of stimuli to the
ropsychological session (see section below),
children was performed using a computer and
and 60 min later (9:00 a.m.), at the end of the
a LCD projector. This device permitted for
session. Rectangular filter papers (3.5 × 5 cm)
presentation of stimuli to all students, with
were used for salivettes. One centimeter of the
possibilities of computer-controlled presenta-
salivette was used for handling while the
tion time of the stimuli.
other 4 cm were used for saliva sampling.
This method has proven to yield reliable cor-
tisol measurements in adult and elderly sub- Declarative memory test. The distinction be-
jects (Lupien et al., 1997; Lupien, DeLeon, tween declarative and nondeclarative memory
DeSanti, Convit, Tarshish, Nair, McEwen, revolves mainly around whether conscious
Hauger, & Meaney, 1998). The subjects were recollection of previously learned information
asked to put the filter paper in their mouth is necessary for performance. Thus, tests of
until it was saturated with saliva. Saliva sam- declarative memory depend on conscious rec-
plings have proven to be an easy and reliable ollection of previously learned information,
method in children (Stansbury & Gunnar, while tests of nondeclarative memory refer
1994). Coding of saliva samples was made subjects to a processing task and measure the
during saliva sampling. Once saliva was sam- extent to which previous exposure to the ma-
pled, the examiners wrote the name, date, and terial changes the speed or the accuracy of
hour of the sample on the handling part of the performance on the processing task. In this
salivette, and the filter paper was then clipped study, declarative memory was measured by
on a drying device. Cortisol levels were mea- an immediate and 30-min delayed free recall
sured using radioimmunoassay with tritiated test, and nondeclarative memory was mea-
cortisol and a highly specific antibody (B-63; sured by an implicit recall test. Fifteen line
Endocrine Science Tarzana, CA) that cross- drawings of animals were presented, one at a
reacts with corticosterone has 4% and has less time, on the screen, and the task of the child
than 1% cross-reactivity with deoxycorticos- was to say whether the gender of the animal
terone and deoxycortisol and less than 0.5% was “feminine” or “masculine” (which is a
cross-reactivity with any other adrenal steroid. normative form of language in French). Im-
Intra- and interassay variability is 3.5 and 5%. mediately after and 30 min later, children
were asked to freely recall all the animals of
Child’s cognitive processing. Children were the list, in any given order. Given the absence
submitted to a neuropsychological assessment of writing–reading capacity in 6-year-old
662 S. J. Lupien et al.

children, they were tested using a recognition Parents’ assessment


task in which they were presented with the
line drawing of two animals and asked to cir- Environmental stressors. Environmental stres-
cle the animal they had seen previously. For sors were measured using the Derogatis Stress
children 8 or more years old, declarative Profile (DSP; Derogatis & DellaPietra, 1994)
memory was tested using a free recall task in questionnaire. The DSP is a multidimensional
which they were asked to write down the psychological self-report scale designed to
name of the animals they had seen previously, measure various subcomponents of stress. It
in any given order. Given this important dif- reflects the three principal components of
ference in the methods for testing memory stress and their interaction: environmental
performance, data from 6-year-old children events, personality mediators, and emotional
were not analyzed in the same analysis of responses. Collectively, these measures pro-
variance as data from older children. vide a comprehensive screening assessment of
current stress levels. The DSP consists of 77
items that are divided into 11 subscales, or
Nondeclarative memory. Nondeclarative mem-
domains, that measure the salient aspects of
ory was tested by asking children to write
each of the three principal stress domains (en-
down all the animal names they knew in a
vironmental events’ subscale: vocational/
45-s period. Nondeclarative memory was cal-
work, family, health; personality mediators’
culated as the number of animal names from
subscale: time pressure, driven behavior, atti-
the previously studied list that were given by
tude posture, relaxation potential, role defini-
the child. In order to prevent children from
tion; emotional response’s subscale: hostility,
making a link between the declarative and
anxiety, depression). The DSP has been eval-
nondeclarative memory tasks, the nondeclara-
uated on two measures of reliability, homoge-
tive memory test was given 15 min after the
neity and repeated measures, and has demon-
declarative memory task and was embedded
strated very acceptable reliability coefficients.
within a larger verbal fluency task for which
Test–retest coefficients range from .92 to .72,
children had to provide names for vegetables,
and internal consistency for the three princi-
jobs, and animals (nondeclarative memory
pal domain scores ranged from .88 to .83.
task). Given the absence of writing–reading
capacity in 6-year-old children, they were not
Family stressors. Family stressors were mea-
tested for nondeclarative memory function.
sured using the Family Inventory Life Experi-
ence (FILE; McCubbin, Patterson, & Wilson,
Selective attention. Selective attention refers 1980) survey. The FILE questionnaire is an
to the ability to discriminate relevant from ir- objective measure that assesses the buildup of
relevant information (Rabbitt, 1964). This life events experienced by a family, and is an
was measured by a visual detection task with index of family stress. The FILE is a 72-item
stimuli presented for 50 ms. In this task, the self-report instrument designed to record the
target was the digit “2,” and this target was normative and nonnormative life events and
inserted in simple visual displays comprised changes experienced by a family unit. Since
of letters (easy detection; e.g., R J 2 X) or it is a family life change inventory, all events
digits (difficult detection; e.g., 3 9 2 1). There experienced by any member of the family are
were 60 stimuli presented to the children; 30 recorded. Each item is worded to reflect a
of them were absent-target trials (target was change of sufficient magnitude to require
absent from the display), and 30 others were some adjustments in the regular pattern of in-
present-target trials (target was present in the teraction of family members. The emphasis is
display). Half of each set was comprised of on change, which may be either positive or
15 easy and 15 difficult detection stimuli. The negative. The FILE comprises nine subscales
number of targets correctly detected consti- (intrafamily strains; marital strains; pregnancy
tuted the dependent variable. or childbearing strains; finance and business
Basal cortisol levels in low and high SES children 663

strains; work–family transitions and strains; As a compensation for the children’s par-
illness and family care strains, losses, and ticipation in the study, each school received
transition; and legal strains). The reliability $350.00, which was deposited in the school’s
coefficient ranges from .73 to .30, and test– foundation for children’s social activities.
retest reliability ranges from .77 to .72.
Analyses of results
Procedure
Data were first examined for normal distribu-
Four examiners tested groups on each occa- tions and means, and standard errors were cal-
sion. Such a high number of examiners was culated (descriptive study). Data were then
used in order to ensure an adequate cortisol analyzed using a univariate or multivariate
sampling for the group of children, as well as analysis of variance (ANOVA or MANOVA),
to ensure a valid environment (e.g., absence with SES (low vs. high) and age (6–16 years)
of noise) for the neuropsychological testing. as the between-subject factors and with the
The four examiners used for the study were specific dependent variable of each test as the
the same for each class tested. within-subject factor. Given the number of
A particular session was as follows: when dependent variables used for neuropsycholog-
the examiners arrived, the consented children ical assessment, we used a Bonferroni correc-
had already been gathered in a room by the tion with an alpha set to p < 0.01. For the
school director. The principal investigator of memory (declarative vs. nondeclarative), the
the project (S.J.L.) served as the “presentator” performance of 6-year-old was not compared
of the study and introduced the procedure of to that of other children, so these data were
testing to the children, while the other exam- compared using a t test. For salivary cortisol
iners prepared the material for testing and data, the average of the two morning cortisol
placed the answer sheets (response booklet) samples was used as a measure of basal morn-
on the desk of each student. Any questions ing cortisol levels, because this procedure
were answered at that time. The presentator takes into account intra- and intersubjects
then showed how to take a saliva sample and variability in salivary cortisol samplings (Lu-
took one in front of the children in order to pien et al., 1998) and has been shown to be
ensure that everyone understood. Afterward, highly correlated with personality variables
a first sample of saliva was taken. Saliva sam- (Bossert et al., 1988; Bridges, 1974; Steptoe,
pling in the classroom using four examines 2000). Preliminary analyses were performed
lasted an average of 10 min. The neuropsy- in order to test the existence of gender differ-
chological testing was then introduced to the ences on the biological and cognitive factors.
children, and task order was counterbalanced No differences between boys and girls were
across classrooms. observed for any variables tested, so data
For the declarative memory task, children were collapsed across subsequent analyses.
were presented with words or images on the
screen and then asked to recall as many of
Results
them as possible on a specific page of the re-
sponse booklet. For the selective attention
Representativity of the sample of
task, stimuli were presented on the wall
children and parents
screen for 50 ms and children were asked to
write on a specific page of the booklet Annual salary, education level, and employ-
whether the target was present or not in the ment type and time (full-time vs. part-time)
display they saw. For the verbal fluency task were assessed during the semistructured
and nondeclarative memory task, children phone interview with mothers in order to ver-
were given a specific category and then asked ify the accuracy of SES (defined by the
to write as many items as possible that related CECM) as a grouping factor for the analysis
to the criterion in a 45-s session. of cortisol levels in children. Table 2 gives
664 S. J. Lupien et al.

Table 2. Demographic data on parents of children from low and high socioeconomic status
(SES) in Montreal (data obtained on 175 families)

Low SES High SES

N Data N Data Difference

Family
Salary 91 $24.000 ± 11 82 $56.000 ± 12 p < 0.001
Family type 94 47.8% (45) single mom 88 22.7% (20) single mom χ2 = 12.51
52.2% (49) both parents 77.3% (68) both parents p < .001
Number of children 94 2.48 ± 0.10 88 2.36 ± 0.08 ns
Rank of tested child 94 1.67 ± 0.09 88 1.58 ± 0.08 ns
Mothers
Education 92 12.56 ± 0.68 86 18.89 ± 1.07 p < 0.001
Employment type 92 51.1% (47) occasional/ 86 24.4% (21) occasional/ χ2 = 27.01
unemployed unemployed p < .0001
44.6% (41) clerical/ 44.2% (38) clerical/
technical technical
4.2% (4) professional/ 31.4% (27) professional/
career career
Employment time 92 52.2% (48) unemployed 86 26.7% (23) unemployed χ2 = 12.9
22.8% (21) part-time 19.8% (17) part-time p < .01
25% (23) full-time 53.5% (46) full-time
Alcohol consumption 92 0.025 ± 0.01 87 0.10 ± 0.04 p < 0.07
Cigarette consumption 92 0.45 ± 0.05 87 0.19 ± 0.04 p < 0.001
Fathers
Education 63 13.03 ± 0.8 79 19.56 ± 1.13 p < 0.001
Employment type 63 20.6% (13) occasional/ 79 9.5% (6) occasional/ χ2 = 20.9
unemployed unemployed p < .0001
73.1% (46) clerical/ 70.8% (43) clerical/
technical technical
6.3% (4) professional/ 19.7% (30) professional/
career career
Employment time 63 20.6% (13) unemployed 79 0% (0) unemployed χ2 = 17.78
7.9% (5) part-time 6.3% (5) part-time p < .001
71.5% (45) full-time 93.7% (72) full-time
Alcohol consumption 59 0.05 ± 0.03 77 0.18 ± 0.06 p < 0.08
Cigarette consumption 60 0.56 ± 0.08 77 0.17 ± 0.04 p < 0.001

the information gathered in CECM criterion was a tendency for both mothers and fathers
for low- and high-SES parents. There were of high SES to report a higher intake of alco-
significant differences between the annual sal- hol (mothers: t (176) = −1.82, p = .07; fathers:
ary of low- and high-SES parents, t (171) = t (137) = −1.73, p = .086). Finally, both moth-
−7.41; p < .0001, as well as a higher educa- ers and fathers of low SES reported a higher
tion level for both mothers, t (176) = −5.03; intake of nicotine (mothers: t (176) = 4.03,
p < .0001, and fathers, t (140) = −4.14; p < p < .0001; fathers: t (135) = 4.42, p < .0001).
.0001, of high SES, when compared to low-
SES parents. Parents of high SES had a sig-
Children’s cortisol levels
nificantly higher employment type than low-
SES parents (mothers: χ2 = 27.01, p < .0001; Figure 1 presents the mean morning saliva
fathers: χ2 = 20.0, p < .0001), and were signif- cortisol levels for low- and high-SES children
icantly more employed full time, when com- from 6 to 16 years of age. The ANOVA per-
pared to low-SES parents (mothers: χ2 = 12.9, formed on salivary cortisol data revealed sig-
p < .01; fathers: χ2 = 17.78, p < .001). There nificant main effects of SES, F (1, 307) =
Basal cortisol levels in low and high SES children 665

Figure 1. Mean morning salivary cortisol levels (±SE) in children from low and high SES
ranging from 6 to 16 years of age.

6.62, p < .01, and age, F (5, 307) = 21.23, sults were observed for the effect of age per-
p < .001, as well as a significant interaction formance on the delayed memory task, F (4,
between SES and age, F (5, 307) = 4.78, p < 259) = 26.8, p < .0001. Children from the 6-
.0001. We then broke down the interaction by year-old group were tested using an immedi-
age. An a posteriori comparison of means re- ate and delayed picture recognition task, due
vealed significant SES differences in children to the lack of writing skills in these children.
6, 8, and 10 years old (p < .0001), with chil- Again, no SES differences were observed on
dren of low SES showing significantly higher immediate (p > .2) or delayed (p > .1) mem-
salivary cortisol levels than children of high ory performance in 6-year-old children. The
SES. There were no significant SES differ- ANOVA performed on nondeclarative mem-
ences in salivary cortisol levels for children ory performance revealed a significant main
from high school (12–16 years of age; p > .1). effect of age, F (4, 259) = 23.11, p < .0001,
Interestingly, the SES differences in cortisol with no main effect of SES, F (1, 259) = 3.1,
levels disappeared at the time of school transi- p > .08, or interaction between SES and age
tion, with SES differences in cortisol levels in (p > .2). Thus, declarative and nondeclarative
elementary school and a disappearance of memory performance increased with age, but
these differences during high school. SES did not have any effect on this change
across age in children.
Cognitive function
Verbal fluency. The ANOVA performed on
Table 3 presents the cognitive performance of this data set revealed a significant main effect
low- and high-SES children for each cogni- of age, F (4, 259) = 66.7, p < .0001, as well
tive task performed. as a tendency toward a significant interaction
between SES and age, F (4, 259) = 2.4, p =
Memory. The ANOVA performed on immedi- .051. However, due to the use of a Bonferroni
ate declarative memory performance (children correction set at p < 0.01, this interaction was
8–16 years old) revealed a significant age dif- not further decomposed.
ference, F (4, 259) = 40.97, p < .0001, with
no main effect of SES (p > .2) or interaction Selective attention. The ANOVA performed
between SES and age (p < .1). The same re- on the number of correctly detected targets
Table 3. Cognitive performance of low and high SES children as a function of age

Elementary 1 Elementary 3 Elementary 5 High School 1 High School 3 High School 5

Low High Low High Low High Low High Low High Low High

Declarative memory (no. words


recalled)
Immediate 9.1 9.4 4.7 4.8 6.1 5.3 7.7 8.2 7.6 8.3 7.7 7.6
(0.19) (0.26) (0.27) (0.28) (0.27) (0.37) (0.51) (0.39) (0.24) (0.23) (0.32) (0.24)
Delayed 9.1 9.6 4.4 4.0 5.3 5.3 6.7 7.2 6.7 6.8 7.6 7.4
(0.16) (0.26) (0.23) (0.35) (0.26) (0.35) (0.44) (0.46) (0.28) (0.31) (0.43) (0.32)
Nondeclarative memory (no. words — — 1.6 2.4 2.7 2.7 3.7 4.5 3.9 4.1 4.3 4.1
recalled) (0.22) (0.27) (0.23) (0.32) (0.31) (0.29) (0.28) (0.22) (0.34) (0.26)
Verbal fluency (no. words given — — 3.9 4.6 6.1 6.9 8.1 7.4 8.6 9.7 9.9 9.5
in 45 s) (0.32) (0.51) (0.28) (0.44) (0.30) (0.31) (0.42) (0.34) (0.51) (0.24)
Selective attention (no. of targets 8.0 10.6* 13.4 14.0 18.2 17.1 20.2 21.2 22.9 24.2 28.2 22.9*
detected in 45 s) (0.30) (1.08) (0.65) (0.80) (0.65) (0.80) (0.92) (0.68) (0.86) (0.59) (1.24) (0.72)
*Significant difference (p < .05) between low and high SES children.
Basal cortisol levels in low and high SES children 667

Figure 2. Scores (calculated as t scores ± SE) of low and high SES children on the 11 stress
subscales of the Derogatis Stress Profile: 1, anxiety; 2, hostility; 3, time pressure; 4, depres-
sion; 5, attitude; 6, relaxation; 7, role definition; 8, driven behavior; 9, vocational status; 10,
domestic; 11, health attitude. **Significant group difference at p < .05.

revealed a main effect of age, F (5, 306) = higher feelings of depression and higher un-
46.23, p < .0001, as well as a significant inter- healthy behaviors when compared to high-
action between SES and age, F (5, 306) = 3.8, SES parents.
p < .003. An a posteriori comparison of means
revealed significant SES differences on the FILE. Figure 3 presents the scores of chil-
selective attention task for 6-year-old and 16- dren’s parents on the nine subscales of the
year-old subjects. Among 6-year-olds, high- FILE questionnaire. The MANOVA performed
SES children performed significantly better on the FILE scores of the parents revealed
than low-SES children (p < .05), while low- significant SES differences on the subscales
SES 16-year-olds performed significantly bet- of family transitions, F (1, 173) = 4.52, p <
ter than high-SES 16-year-olds (p < .05). No .03, and work-related stressors, F (1, 173) =
other age groups showed significant SES dif- 3.8, p < .04. These differences revealed that
ferences with regard to selective attention per- high-SES parents scored higher for stress re-
formance. lated to work and family transition (e.g., child
leaving the house) when compared to low-
SES parents.
Environmental and family stressors

DSP. Figure 2 presents the scores of low- and Discussion


high-SES parents on the subscales of the DSP
questionnaires. The MANOVA performed on The results obtained in this study revealed
the DSP scores of the parents revealed signifi- significant developmental SES differences in
cant SES differences on the subscales of de- cortisol levels during childhood, which tended
pression, F (1, 170) = 3.92, p < .05, and to equalize during youth. Children from ele-
health, F (1, 170) = 17.8, p < .0001. An a pos- mentary schools (ages 6–10 years) presented
teriori comparison of means showed that low- significantly higher basal salivary cortisol lev-
SES parents scored significantly higher on els when compared to children from high
these subscales when compared to high-SES SES. However, after school transition, when
parents, showing that low-SES parents report children are 12–16 years of age, there are no
668 S. J. Lupien et al.

Figure 3. Scores (±SE) of low and high SES children on the nine stress subscales of the
Derogatis Stress Profile: 1, marital; 2, intrafamily; 3, pregnancy; 4, finance; 5, work;
6, illness; 7, losses; 8, transitions; 9, legal. **Significant group difference at p < .05.

significant differences in basal cortisol levels ences in basal cortisol levels do not impact on
in children of low and high SES. These results cognitive performance on tests of memory
raise some interesting questions as to the im- and linguistic abilities in this population. The
pact of school transition on stress reactivity in only SES difference to emerge with regard to
low- and high-SES children. cognitive function was observed on the test of
We also report a significant increase of selective attention. At 6 years of age, high-
cortisol levels with age, with the largest SES children performed better than low-SES
change occurring between 10 and 12 years of children, while this tendency reversed at 16
age, which corresponds to the onset of pu- years of age, with low-SES children outper-
berty. Similar findings of increased cortisol forming children of high SES. Such an effect
levels at the time of puberty have been re- of SES at different ages was also observed
ported previously (see Weinstein, Diforio, by Ardila and Rosselli (1995), who reported
Schiffman, Walker, & Borsall, 1999). This in- significant developmental differences in cog-
creased cortisol secretion at the time of pu- nitive processing between children of high
berty corresponds to the significant increase versus low SES. However, these results have
in gonadal hormone secretion (estrogen and to be taken with caution, given the limited
testosterone). Since gonadal hormones are se- sample size of children tested at these age
creted by the adrenal glands, interaction be- ranges. Also, selective attrition of subjects
tween puberty-induced gonadal hormone may have influenced the results. Indeed, it
changes and cortisol secretion is highly proba- might be possible that low-SES children with
ble. Also, melatonin (which is coregulated cognitive deficits are more likely to drop out
with cortisol levels) is involved in regulation of school or to refuse to participate in the re-
of puberty onset (see Reiter, 1973), which search. This possibility would have the poten-
could also be a significant factor in the occur- tial to mask the existence of SES-related se-
rence of the significant increase of cortisol lective attention throughout the age ranges
around the age of 10–12 years. tested.
We have further shown that SES differ- With regard to the children’s mothers, we
Basal cortisol levels in low and high SES children 669

have found that low SES in the family is gen- school transition, with no SES differences ob-
erally related to high levels of environmental served during high school. This difference in
stressors, while high SES is significantly basal cortisol levels as a function of SES and
more related to familial stressors. Indeed, age could be due to the school environments
low-SES mothers showed a higher score on in which children are exposed as a function of
the depressive subscale of the DSP and a SES. A study performed by Tennes and Kreye
lower score on healthy behaviors of the same (1985) on children’s adrenocortical responses
questionnaire. With regard to family stressors, to classroom activities reported that in second
high-SES mothers scored higher on the graders cortisol levels are influenced by social
FILE’s subscale of family stress related to interactions with peers and teachers at school.
work and family transitions. These results It might thus be possible that the school envi-
give us a very interesting view of the familial ronment in low-SES areas differ from those
environment of the low- and high-SES chil- in high-SES areas in such a way that they act
dren tested. The mothers of low-SES children on the basal secretion of stress hormones in
tend to complain more about depression and the children attending these schools. How-
unhealthy behaviors, while the mothers of ever, we have previously reported data from
high-SES children tend to complain more another subset of this study (Lupien, King,
about stress related to work and to transitions Meaney, & McEwen, 2000) in which we were
in the family, such as their children leaving able to obtain salivary cortisol levels in ele-
home. mentary school children of medium SES. In
Altogether, these results go along with data this data set, children 6–10 years of age were
showing that school transition in low- and tested in the same school of a low-, medium-,
high-SES children may act as an equalization or high-SES area, and significant SES differ-
process for SES impact on health (West, ences still emerged as a function of age in
1997). This “equalization process” refers to medium-SES children. These data suggest
the observed changes in class patterning be- that if the school environment plays a signifi-
tween childhood and youth, with SES differ- cant role in cortisol differences as a function
ences tending to disappear during youth and of SES, its impact is concomitant with other
reemerge during adulthood (for a complete re- environmental variables associated with age.
view, see West, 1997). Four major explana- The second explanatory factor within the
tory factors have been suggested in the litera- educational system relates to the importance
ture to explain the equalization of SES of school transition itself. Transition to high
difference in health during youth (see West, school marks the first major change in status
1997). What is very interesting is that all for a child. The child then moves from a rela-
these factors have been shown to be signifi- tively small, community-based school to a
cant variables in activating the HPA axis. We larger impersonal unit, and also moves from
will discuss each of these variables in turn being the oldest of the school (elementary
and relate them to HPA activation data. school, Grade 5) to being the youngest (high
school, Grade 1). The work of Sapolsky, Al-
berts, and Altmann (1997) on primates re-
Educational system vealed the importance of the hierarchical sta-
tus in determining basal cortisol levels. In his
The first explanatory factor for the equaliza- studies, Sapolsky has shown that in a stable
tion of SES differences during youth is related social hierarchy, basal cortisol levels are sig-
to the educational system itself, with impor- nificantly higher in subordinates than in
tant differences relating to the school environ- leader baboons. These results have been con-
ments. In our study, we have found that basal firmed in human army recruits (Hellhammer,
cortisol levels are significantly higher in low- Buchtal, Gutberlet, & Kirschbaum, 1997; see
SES children of elementary grades but that also Kessler, 1979). These data could be used
differences tend to disappear at the time of to interpret the school transition effect on
670 S. J. Lupien et al.

basal salivary cortisol levels. Indeed, it is pos- ary) gives rise to higher cortisol levels in low-
sible that the change of SES differences in SES children when compared to high-SES
cortisol levels observed at the time of school children. However, at the time of school tran-
transition may be due to the change of status sition, when peer relationships become more-
of the children and to the advantage of this important than family relationship, this transi-
changing status for low-SES children when tion might have a more significant impact on
compared to high-SES children. basal cortisol levels in low-SES children
when compared to high-SES children.

Influence of peers
Youth culture
The second influencing factor that could ex-
plain the equalization of cortisol levels at the The third influence that could explain the
time of school transition is related to the influ- equalization of basal cortisol levels during
ence of the peer system (for a review, see youth is closely related to the second one and
West, 1997). It is known that during youth, concerns the influence of the youth culture it-
peer-based relationships have a more impor- self (for a review, see West, 1997). It is
tant influence than family-based relationships known that the youth culture permeates both
(see West, 1997). It has further been shown school-based and peer group experiences and
that the significance of the peer group in- gives meaning to a particular membership to
creases markedly around 12–13 years of age the social culture of youth. This influence will
(Claes, 1992), which is the age at which we go beyond that of the school and the peer
report the disappearance of the SES difference group and may explain the equalization of
in cortisol levels. Based on this assumption, it SES differences during youth. The youth cul-
could be suggested that the absence of SES ture has a potential influence on identity and
differences observed during youth are due to the behavior of the teen, and this youth cul-
the decrease of the family influence on the ture may assume greater significance for
low-SES teen’s life and the increase in the in- young people than family or peer-based rela-
fluence of peers in these children. Given that tionships. Now, it may also be possible that
low-SES mothers tended to be more de- the feeling of membership to the youth culture
pressed than high-SES mothers, we can postu- has advantageous effects for low-SES young
late that the high levels of cortisol in low-SES people, while it has more disadvantageous ef-
children during elementary school might be fects for high-SES young people. Going along
related to the family environment in which with this hypothesis is the significant SES dif-
they live. In our previous report of a subset of ference observed between low- and high-SES
these data in low-, medium-, and high-SES parents on the family transition subscale of
elementary school children (Lupien et al., the FILE questionnaire. High-SES parents
2000), we reported the presence of a signifi- scored higher on stress related to family tran-
cant positive relationship between the moth- sitions (e.g., child leaving the house) than
er’s score on the depressive subscale of the low-SES parents, and it may thus be possible
DSP and her own child’s cortisol levels. We that young people of high SES place more
interpreted this data as suggesting that chil- weight on parents’ expectations than young
dren may be reactive, in terms of adrenocorti- people of low SES, giving rise to higher cor-
cal activation, to the family environment in tisol levels in high-SES teenagers than
which they live. The frequent presence of dis- low-SES teenagers. If this is the case, then it
cord and disorganization in families with a must be suggested that the absence of SES
depressed parent (Brown & Harris, 1978) or differences in terms of cortisol levels during
in low-SES families (see Adler et al., 1994) youth may be due to the increase of cortisol
is well known. It is thus be possible that the levels in high-SES teenagers, rather than the
family setting in which a child is raised (other decrease of cortisol levels in low-SES teen-
than pure environmental factors like low sal- agers.
Basal cortisol levels in low and high SES children 671

Resilience studies that have shown that prenatal stress


increases emotionality and stress hormone re-
Finally, there is a fourth influencing factor activity for the life of the individual. Con-
that could explain the equalization of SES dif- versely, postnatal “handling” of neonates leads
ferences in terms of basal cortisol levels dur- to reduced emotionality and reduced stress hor-
ing youth, and this last factor relates to resil- mone reactivity for the lifetime of the individ-
ience. It is known that low-SES teenagers ual (Anisman, Zaharia, Meaney, & Merali,
tend to quit school at a lower ages than high- 1998; Caldji, Tannenbaum, Sharma, Francis,
SES teenagers. It may thus be possible that Plotsky, & Meaney, 1998; DeNelsky & De-
the absence of SES differences in terms of nenberg, 1967; Denenberg & Zarrow, 1971;
cortisol levels observed during youth may be Francis, Champagne, Liu, & Meaney, 1999;
due to the fact that the teenagers studied in Francis, Diorio, Liu, & Meaney, 1999; Le-
our experiment were the “resilient” ones (i.e., vine, Haltmeyer, Karas, & Denenberg, 1967;
those who have decided to stay in school). Meaney, Aitken, Sharma, Viau, & Sarrieau,
Many vulnerability factors (e.g., personality 1989; Meaney, Aitken, Van Berkel, Bhatna-
traits) have been shown to be related to basal gar, & Sapolsky, 1989). In animal models,
cortisol levels (Mason, 1968), so it may be brain aging is increased by elevated stress re-
suggested that the absence of SES differences activity and reduced by lowered stress reactiv-
observed during youth are due to a population ity (Dellu, Mayo, Vallee, LeMoal, & Simon,
bias, which means that the low cortisol levels 1994; Escorihuela, Tobena, & Fernandez–
of the resilient low-SES teenagers who stayed Teruel, 1995; Liu, Diorio, Tannenbaum, Caldji,
in school—thus being “available” for our Francis, Freedman, Sharma, Pearson, Plot-
study—created an artificial absence of SES sky, & Meaney, 1997). There are also data
differences in terms of cortisol levels. from an animal model that increased stress re-
activity increases propensity for substance
abuse (Dellu et al., 1994), and this finding
Conclusion needs to be studied for its implications and
relevance to human drug abuse. In addition,
At the present time, all these influencing fac- studies in infrahuman primates have shown
tors carry equal weight in explaining the that early maternal deprivation reduces brain
equalization of SES differences during youth. serotonin levels and increases alcohol prefer-
However, this descriptive study has shed ence and aggressive behavior and decreases
some light on the physiological differences affiliative behaviors (Higley, King, Hasert,
existing between low- and high-SES children Champoux, Suomi, & Linnoila, 1996; Higley,
and teenagers. Mehlman, Higley, Fernald, Vickers, Lindell,
The susceptibility of an individual to Taub, Suomi, & Linnoila, 1996). This data is
stress-related disorders is likely to reflect de- to be put in line with recent human evidence
velopmental influences as well as genetic risk showing that low SES in adult men and
factors. In this perspective, creators of models women is significantly related with a blunted
such as the allostatic load model (for a re- serotoninergic responsitivity similar to what is
view, see McEwen, 1998) are to be congratu- observed in endogenous depression (Mat-
lated on their attempt at providing a multisys- thews, Flory, Muldoon, & Manuck, 2000).
temic view about the cumulative impact of From all these animal and human studies,
wear and tear on physical and mental health. it becomes clear that future longitudinal stud-
Indeed, a major advance in behavioral neuro- ies of children of low and high SES are ur-
science during the past decade has been the gently needed, as well as others measuring
establishment of a lifelong perspective for en- basal cortisol levels in the mothers of low-
vironmental influences on stress reactivity and high-SES children and teenagers. Such
during development that persist for a lifetime studies should yield very valuable data as to
(for a review, see McEwen & Lupien, in the possible origin of SES differences in
press). In this line of work, we can cite animal physical and mental health.
672 S. J. Lupien et al.

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