Children's Salivary Cortisol, Internalising Behaviour

INTER NA TIO NA L JO U R NAL O F BE H A VIO R A L D EVELO PME NT, 1998, 22 (4), 707±728

Children’s Salivary Cortisol, Internalising Behavio ur Problems, and Family Environment: Results from the Concordia Longitudinal R isk Project D ouglas A . G ranger Pennsylvania State University

Lisa A . Serbin, A lex Schwartzman, Pascale Lehoux, and Jessica Cooperman Concordia University, M ontreÂal, Q ueÂbeÂc

Sandra Ikeda Pennsylvania State University

To explor e the possibility that children’s adrenocortical reactions to parentchild con¯ ict in¯ uence their vulne rability for internalising behaviour problems, we studied 62 mother-child dyads from the Concor dia Longitudina l R isk Project. Standardised measures of maternal, child, and family adjustment were collected. Mother’ s and children’ s saliva was sampled before and after a con¯ ict-oriented mother-child interaction task and was later assayed for cortisol. The children’ s pre-task cortisol scores were negatively associated with their internalising behaviour problems, their mother’s childhood levels of socially withdrawn behaviour and current psychosocial problems, as well as dimensions of family environme nt representing the open expression of aggression, anger, and con¯ ict. R equests for reprints should be sent to Dr. Douglas A . G ranger, Departme nt of Biobehavior al H ealth, The Pennsylvania State U niversity, 315 E ast H ealth and Human D evelopment Building, U niversity Park, PA 16802, U SA ; e-mail via Internet to D AG [email protected]. This research was part ially supporte d by grants from the Seagram Fund for Innovative R esearch (Concord ia University), the Strategic Fund for Children’ s Mental H ealth (Health Canada) , the National Instit ute of Mental H ealth, and the UCLA Task Force on Psychoneuro immunology. A ssays were supporte d by the Center for Interdisciplinary Study of Immunolo gy and D isease at UCLA and the Penn State U niversity Behaviora l E ndocrinology Laborat ory. We thank Claude Senneville, Xiaoming Tang, and D anny Lacroix for their assistance in data collection; Najib A ziz and E ve Schwartz for assistance with salivary immunoassays; Jessica King and Jodi H eaton for manuscript prepara tion; and the participants in the study. We very much appreciat e the thoughtful comments of two anonymous reviewers. c 1998 The International Society for the Study of Behavioura l D evelopment

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Children’ s cortisol levels after the interaction task were lowest for those raised by mothers with high childhood levels of aggressive behaviour problems, and in family environme nts characterised by rigid rules. Interrelationships between mother and child pre- and post-task cortisol levels were associated with maternal levels of childhood behaviour problems. The integration of measures of children’ s adrenocortical activity into developmental studies of children at risk for psychosocial problems may reveal important clues regarding the processes by which adverse early rearing environme nts affect children’ s internalising problem behaviour .

In this decade, there has been an emphasis on the integration of biological measures into behavioura lly oriented studies. This spirit of the times has spawned renewed interest among developmental scientists in how ``fastacting’ ’ horm onal processes affect the impact that social contextual events have on children’ s behaviour , how these processes become integrated with behaviour over time, and how the consequences of these reciprocal in¯ uences affect children’ s psychosocia l adjustment later in life (e.g. G ottlieb, 1992; Magnu sson, 1988; Susman, 1997). Studies evaluating relations among aspects of family environm ent, children’ s proble m behaviour, and the activity of the hyp othalamic-pituitary-adrenal (H PA ) axis are at the leading edge of the application of this biobehavioura l perspective. This paper addre sses an important knowle dge gap in that emerging literature. We examine whether children’ s H PA axis activity is associated with the intergenerational transfer of risk for serious psychosocial proble ms from mothe r to child. Numerous studies reveal that children who have multiple and severe behaviour problems are likely to grow up to become the parents of another generation at high risk for disadvantage and adjust ment dif® culties (e.g. Chase-Landale & Brooks-G unn, 1995; Wilson, 1987). The search for clues to the processes involve d in the transfer of risk across generations has been extensive (e.g. Cairns & Cairns, 1994; Farrington, 1991; R utter, 1987; Velez, Johnson, & Cohen, 1989). The focus has recently narrowe d on aspects of parent’ s behaviour proble ms and circumstances during their own childhoods, years prior to the conception and birth of their children (e.g. Serbin, Peters, McA ffer, & Schwa rtzman, 1991; Serbin, Mosko witz, Schwartzman, & Ledingh am, 1991). The Concor dia Longitudinal R isk Progra m (CLR P) 1 has played a central role in the effort to extend our unde rstanding of these relationships. The project began in 1976 and has followed a group of over 1700 inner city elementary school-aged children from low income neighbourh oods (see Schwartzman, Ledingham, & 1

The CLR P was originated in 1976 under the direction of Jane Ledingham and Alex Schwartzman .

CORTISOL, FAMILY CONTEXT, BEHAVIOUR PROBLEMS

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Serbin, 1985). The children were screened and selected to represent four groups: those who were aggre ssive, socially withdrawn, both aggre ssive and socially withdra wn, and a comparison group (see description of selection criterion later). In 1998, CLR P participants are in their late 20s and early 30s and many have become parents. The ® ndings from the most recent follow-up assessments reveal that mother’ s childhood rates of aggressive behaviour predict impove rished hom e environm ents, developmental lags in their young offspring, risk to their children for neglect and abuse, unre sponsive and aggressive behaviours towards their children, and children’ s aggressive behaviour towards them (Serbin et al., 1991a , b; Serbin, Peters, & Schwartzman, 1996; Serbin et al., 1998). The CLR P analyses clearly support the well established intergenerational cycle of risk for psychosocia l distress. H owever, on a more positive note, the analyses also corrobo rate that, despite poor prospe cts at birth, many children from high risk and disadvantageous backgrounds grow up to be reasonably well adjusted. The ® ndings to date unde rscore the notion that psychosocia l risk is, as the term implies, proba bilistic (e.g. R ubin, H ymel, Mills, & R ose-Krasner, 1991; R utter, 1987; Serbin et al., 1998; Werner & Smith, 1992). There remain signi® cant gaps in our unde rstanding of why when children grow up in impove rished or stressfu l family environm ents some are susceptible to risk and show serious psychosocia l proble ms whereas others appear resilient and adjust reasonably well. The overarching hypot hesis guiding the present study is that incorpora ting measures of enviro nmentally sensitive physiologica l systems (i.e. activity of the H PA axis), into existing behavioura lly oriented models of psychosocial risk will extend our unde rstanding of individual differences. U ntil recently, the application of such a ``biobe havioura l’ ’ analysis in studies of the relations among family environment, childhood stress, and risk was dif® cult. That is, the measurement of H PA axis product s (i.e. cortisol) required procedures that were either invasive (e.g. blood sampling), or dif® cult to implement in naturalistic social contexts, or unable to capture response s to time limited contextual events (i.e. 12- or 24-hour urine collection). In the last 10 years, technical advances that make the immunoa ssay of biomarkers in saliva possible (e.g. G ranger, Schwartz, Booth, & A rentz, in press; Schwa rtz, G ranger, Susman, G unna r, & Laird, in press) have created new oppor tunities by making sample collection less invasive. The ® ndings from numerous studies seem to justify integrating measures of children’ s H PA axis activity into the study of intergenerational transfer of risk, and results from two groups are particularly relevant. The ® rst research group (Finn & E ngland, 1995) used biod emograp hic methods to monitor longitudina lly relations between 247 norm ally developing children’ s (from 82 house holds in a rural Caribbean village)

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daily activities, emot ional states, interactions with caretakers, behaviour proble ms, and activity of the H PA axis (indexed by salivary cortisol) in a natural environm ent. A nalyses revealed that traumatic family events (e.g. con¯ ict, punishm ent, ``shame’ ’ , serious quarrelling, and ® ghting) were associated with elevated cortisol levels more strongly than any other factor they considered for all ages of children (range 2 months to 17 years). Further analyses revealed that children with severe caretaking proble ms during infancy exhibited either: (a) unusua lly low basal cortisol levels with occasional high spikes; or (b) chronically high cortisol levels. The form er cortisol pro® le was associated with antisocial and delinquent behaviour, whereas the latter cortisol pro® le was associated with anxiety and social withdrawal. These naturalistic observations indicate that characteristics of early childho od parenting environm ents may in¯ uence the threshold or sensitivity of the H PA axis compone nt of the psychobio logy of the stress response Ð a subsyst em with well established developm ental effects on physiology and behaviour in later life (e.g. Plotski & Meaney, 1993). The second research group used a quasi-naturalistic labora tory task to study clinic-referred children’ s cortisol reactivity to discrete con¯ ictoriented parent-child interactions (G ranger, Weisz, & Kauneckis, 1994). The children ranged in age from 7 to 18 years and had multiple and severe behaviour proble ms. Children’ s cortisol increases in response to a con¯ ictoriented discussion were associated with high levels of their social dif® culties, anxiety, and withdra wal; high levels of socially inhibited behaviour during the interaction; low levels of perceived social contingency; and high levels of external attributions for persona l success and failures (G ranger et al., 1994). The children’ s con¯ ict-related cortisol reactivity also predicted internalising behaviour proble ms, symptoms of anxiety disorde rs, and a negative pattern of control-r elated beliefs six months later (G ranger, Weisz, McCracken, Ikeda, & D ouglas, 1996). It is noteworthy that children who showe d higher cortisol responsiven ess, at the intake and six-mont h assessments, had follow-up outcomes characterised by high levels of social withdra wal. A lso, children who showed consistently high levels of anxiety/depression at intake as well as six months later had high levels of cortisol responsiven ess to the con¯ ict discussion at follow-up. In the most recent analysis, children’ s cortisol increases to the con¯ ictdiscussion task also were associated with levels of their parent-partner’ s symptoms of anxiety and depression, and dysfunct ional parenting attitudes and behaviours (G ranger, D ennig, Weisz, R udolph, & Ikeda, 1998). These clinic-based ® ndings sugge st that reciprocal relationships may exist between children’ s cortisol response s to family con¯ ict that may affect the emergence of, or continuity in, internalising behaviour proble ms. When considered together, the naturalistic and labora tory observations sugge st that perhaps initially individua l differences in H PA activation are


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closely linked to the intensity or frequency of hostile or abusive caregiverchild interactions. O ver time, repeated H PA activation may affect physiologica l or psychologica l processes that increase rates of children’ s socially withdrawn behaviours, negative affect, and low levels of controlrelated beliefs. This complex of behaviour s and cognitions may increase the likelihood that more severe symptoms of internalising behaviour disorde rs will develop. Subseq uently, persistent symptoms of internalising disorde rs may lead to a lower threshold for, or exaggerated H PA reactivity to, mildly challenging social events. A lthough far from conclusive, the accumulating ® ndings highlight the possib ility that individua l differences in links between children’ s H PA activity and parent-child con¯ ict may affect the impact of parental dysfunct ion on children’ s vulnerability to psychopa thology. In the present project, we challenged mother-child dyad s from the young families participating in the CLR P with a con¯ ict-oriented parent-child interaction task. We evaluated if these high-risk children’ s cortisol levels were associated with individua l differences in their psychosocia l adjustment, family environme nt, current levels of maternal psychopa thology, and maternal childhood levels of behaviour problems. We also examined the concordance between maternal cortisol levels measured in anticipation and respon se to the con¯ ict discussion task. We expected the children’ s cortisol levels to: (1) be associated with maternal dysfunct ion, high levels of parenting stress, and family environm ents characterised by high rates of con¯ ict and control; and (2) to predict individua l diffe rences in levels of their internalising behaviour proble ms.

METHODS Screening and Selection of the Original CLRP Sample In the school years 1976±1977 and 1977±1978, the CLR P screened 4109 Francophone schoolchildren in regular grade 1, 4, and 7 classes. These children lived in lower socioeconomic, inner-city areas of MontreÂal, Canada. Participation in the screening was volunt ary, with over 95% of students consenting to participate. In total, 1770 children met the criteria for inclusion (see below), including approxim ately equal num bers of boys (n = 861) and girls (n = 909) from each grade level. The screening process involve d the classi® cation of children along the dimensions of aggre ssion and withdrawal by means of a French translation of the Pupil E valuation Inve ntory (PE I; Pekarik, Prinz, Leibert, Weintraub, & Neale, 1976). The PEI consists of 34 items which load on to three factors: A ggre ssion, Withdra wal, and Likeability. Scale items assess not only the behaviour of the child, but also the reactions of peers

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towards the child. The children were screened only on the A ggre ssion and Withdra wal factors. Within each classroom , boys and girls were screened using the PE I in separate administrations. Children were asked to nomina te up to four boys and four girls in their class who best matched each item on the PE I. The numbe r of nom inations received by each child was summed for the A ggre ssion and Withdrawal factors. These total scores were then subjected to a square root transform ation to decrease skewness. Finally, transform ed scores were conve rted to z -scores for each gender, within each classroom to control for class size and gende r differences in base rates of aggre ssion and withdra wal. This procedure enabled appropr iate comparisons of each child against the relevant norm s for gende r and age. Percentile cut-offs were established to identify children who exhibited extreme scores on the A ggression and/or Withdrawal scales, while enabling adequate sample sizes for statistical analysis. The present study focuses exclusively on a subsam ple of the origin al 909 female participants. G irls who scored above the 95th percent ile on A ggre ssion and below the 75th percent ile on Withdra wal, relative to same-sex classmates, were selected for the aggre ssive group; the reverse criteria were used to select the withdrawn grou p. A s a function of the low proba bility of achieving extreme scores on both dimensions, more liberal criteria were used to identify a suf® cient numbe r of children to form the aggre ssive-withdra wn group. z -scores equal to or above the 75th percent ile on both A ggr ession and Withdra wal were criteria for membership in this group. Finally, agematched children for whom z -scores on A ggre ssion and Withdrawa l scales fell in the average range (i.e. between the 25th and 75th percentile) were selected for the comparison group (see Schwartzman, Ledingha m, & Serbin, 1985, for a more extensive description of the original methodolo gy).

Participants The data reported here were collected as part of the follow-up assessments of a subgroup of CLR P women who had a ® rst-born child of school age between 1994 and 1996. Sixty-two women participated together with their eldest children, 26 boys (41.9% ) and 36 girls (58.1% ) ranging in age from 5 to 11 (M = 6. 67, SD = 1. 79). Mothers ranged in age from 23 to 32 (M = 28. 21, SD = 2. 30). A t the birth of their ® rst child, women were between 14 and 27 years old. In terms of marital status, 15 (24.2% ) of these women were currently single (never married, separated, or divorce d) and 47 (75.8% ) were married or cohabiting. Census data indicates a national rate of female family headship at 10.67% and a provincia l rate for Q uebec at 11.69% . In terms of education, years of schooling ranged from 6 to 22


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years (M = 10. 98, SD = 2. 51). The average occupational prestige rating for the sample corresponded to the following jobs: cashier, ® le clerk, and hairdresser (Nock & R ossi, 1979). This is a subsample of the women who, together with their children, are thought to be at the greatest risk compared to the overall sample of women in the CLR P for psychosocia l dif® culties (Serbin et al., 1998). U sing T -scores greater than 65 as the cutoff point, 11.29% of the children had scores in the clinical ranges on both the internalising and externalising scale of the Child Behavior Checklist (CBCL; A chenbach, 1991), 69.35% had scores below clinical cut-offs on both CBCL summary scales, 8.07% had scores above the clinical criteria for the externalising but not internalising CBCL scale, and 11.29% had scores above the clinical criteria for the internalising but not the externalising CBCL scale.

Assessment The CLR P 1994±1996 follow-up interview involve d assessments of maternal and child behavioura l, emotional, and psycho logical adjustment, and family functioning. Mother-child dyad s also participated in a series of social interaction tasks around which saliva samples were collected and later assayed for cortisol. Q ualitative and quantitative ratings were scored from videotape of the mother-child interactions. A large battery of measures was administered as part of the larger study, only the instruments relevant to the present study are described here.2 Parent-child Interaction T ask . A parent-child con¯ ict discussion task was used as a psychologica lly challenging event. The rationale for the task was based on naturalistic and quasi-naturalistic evidence linking parentchild con¯ icts to individual differences increases in children’ s cortisol levels (e.g. Flinn & England, 1995; G ranger et al., 1994, 1996, 1998). A lso, procedure s for parent-child interaction tasks are well developed, and studies show that interactions during such tasks are associated with links between parental dysfunctio n and children’ s behaviour proble ms (e.g. Burge & H ammen, 1990; Cook, Kenny, & G oldstein, 1991; Serbin et al., 1998). Parent-child discord is also likely to be a particularly salient social stressor for young parents with young children, and especially for those with histories of psychosocia l problems. Finally, such a task can be used to create an individua lised, yet controllable and ecologically valid challenging event. 2

A ll measures were translated into French. Back-tran slations into E nglish were carried out to ensure that the French translations were equivalent to the original measures.

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O n arrival at the university labora tory the participants were given a brief overvie w of the schedule activities and then the children and mothers independent ly completed the Parent Child Con¯ ict Q uestionnaire. The PCCQ (G ranger et al., 1994) is a 14-item self-report rating scale of possible sources of con¯ ict between mothers and their school-a ged children (e.g. chores, bedtime, and noncom pliance). Each topic is individually rated by parent and child along a 6-point scale from ``low con¯ ict’ ’ to ``high con¯ ict’’ . Interviewers then compared the ratings and selected a topic to use during the interaction task that both parent and child evaluated as a source of con¯ ict. Four standardised observational situations, ranging from 3 to 7 minutes in length, were selected in orde r that a range of typical mother-child interaction scenarios might be observed. The orde r of the tasks was designed to move gradually mother and child from a relatively stress-free, optional interaction situation to a potentially anxiety provoking, highly interactive, confront ational task. The sequence of the activities was drawn from the work of G ranger et al. (1994). The ® rst task was intended to familiarise them with the setting and so placed few demands on either member (i.e. children were asked to free-play with age-appropr iate educational games). The second task increased the interactive demands required for the mothers and children (i.e. mothers were asked to teach the children how to plan a healthy meal). The ne xt activity required a high level of participation from both family members (i.e. they were asked to work together to generate a plan for a hypot hetical vacation they may spend together). Finally, the dyads were asked to discuss the con¯ ict topic with the goal of reaching some solution. B ehavioural O bservation. Mother-child interactions were evaluated using the H igh R isk Interaction Coding System (H -R ICS; Coope rman & Steinbach, 1995). The H -R ICS, was adapted from the Family Interaction Coding System (Patterson, R ay, Shaw, & Cobb, 1969) for use with this special popula tion. The code includes both quantitative and qualitative ratings made by trained observe rs of videotaped mother-child interaction. For the purpose s of this study, global ratings (on a 5-point scale) of ``A ggre ssive’’ behaviour (verbal and/or physical) made for mothers and children were used. Inter-obse rver agreement (r = . 96) was estimated using 22 (26% ) interaction task videotapes. M aternal Characteristics. A s described earlier, during their childhood, mothers had been screened using the Pupil E valuation Inve ntory (PEI; Pekarik et al., 1976). The PE I contains 35 items loaded on three factoranalytically derived dimensions of aggre ssion (e.g. those who are mean and


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cruel to other children), withdra wal (e.g. those who are too shy to make friends), and likeability (e.g. those whom everybody likes). A s described elsewhere, children in each of 152 classrooms were asked to rate up to four boys and girls in their class who best ® t the descriptions of the PEI items. The numbe r of nomina tions for each child was summed for each dimension, square-root transform ed, and then standardised for each sex within each classroom (see Serbin et al., 1991a ). O f the 62 pa rticipants, the breakdown by group was 12 aggre ssive, 10 withdra wn, 12 aggre ssive and withdrawn, and 28 comparison. Mothers also completed the Symptom D istress Checklist-90 (SCL-90; D erogatis, 1983; D erogatis, Lipman, & Covi, 1973) and the Parent Stress Inde x (PSI; A bidin, 1990, 1997; Loyd & A bidin, 1985). The SCL-90 is a self-report symptom checklist comprised of 90 items and generates subscale scores that re¯ ect nine symptom dimensions such as somatisation (e.g. headaches, faintness or dizziness), obsessive-compulsive (e.g. having to repeat the same action), interpersona l sensitivity (e.g. feeling critical of others, your feelings being easily hurt, feeling very self-conscious with others), depression (e.g. crying easily, feelings of worthlessness), anxiety (e.g. nervousne ss or shakiness inside, feeling fearful), phobic anxiety (e.g. feeling nervous when you are left alone, having to avoid certain things because they frighten you), and anger-host ility (e.g. easily annoye d or irritated, temper outburst s). See D erogatis et al. (1973) for infor mation on internal consistency and test-re test reliability. The PSI is a self-report scale comprised of 101 items. It generates seven subscale scores re¯ ecting parent characteristics related to the role of being a parent, such as parental attachment (e.g. mothers intrinsic investment in the role of parent), social isolation (e.g. availability of social supp ort for parenting role), depression (e.g. extent to which mother’ s emotional availability to the child is impaired), relationship with spouse (e.g. emotional and physical support , and level of con¯ ict), parental health (e.g. health in terms of ability to meet demands of parenting), and restrictions of role (e.g. negative impact associated with loss of freedom and important life roles). The PSI also generates six subscales re¯ ecting dimensions of child characteristics directly associated with parenting stre ss: adaptability (e.g. how well a child hand les change and transitions), demandingne ss (e.g. direct pressure the child places on the parent), distractability/hyperactivity (e.g. stressors that result in continuous drain on the parents energy), mood (e.g. excessive crying, withdra wal, depression), acceptability (e.g. how close the child is to the mother’ s idealised child), and reinforces parent (e.g. degree to which parent-child interaction results in positive affective response in the parents). Psychometric data for the parent and child dom ain subscales of the PSI can be found in A bidin (1990).

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Child Characteristics. Mothers were asked to evaluate the behaviours of their children using the parent-report version of the Child Behavior Checklist pro® le (A chenbach, 1991). The 1991 version of this standardised measure lists 118 child behaviour proble ms and generates T -scores that re¯ ect a child’s status relative to others of the same sex and age on internalising, externalising, and total proble ms scales, as well as in eight narrow-ba nd syndrom es: for instance, anxiety/depression (i.e. complains of loneliness, feels unha ppy, sad, or depressed), somatic complaints (i.e. physical proble ms without known medical cause), aggression (i.e. argues a lot, gets in many ® ghts), and social withdra wal (i.e. likes to be alone, shy or timid, withdra wn). E xtensive detail concerning the validity, internal consistency, and test-retest reliability of the CBCL is presented by A chenbach (1991). Fam ily Characteristics. Mothers and children completed the Family E nvironm ent Scale (FE S; Moos & Moos, 1986). The 90-item FE S is designed to assess the structure, style, and fun ctioning of the family and generates 10 subscales of which 4 were included in this study: cohesion (e.g. commitment, help and support family members provide for one another), con¯ ict (e.g. amount of openly expre ssed anger, aggre ssion, and con¯ ict), expre ssiveness (e.g. how much family members are encoura ged to openly express their feelings), and control (e.g. extent to which set rules and procedure s are used to run family life). Psychom etric inform ation for the FE S is presented in Moos (1990). Cortisol D eterm ination. Following G ranger et al. (1994, 1996), saliva samples were collected from the children and their parent-part ners before (Pre-task) and approxim ately 20 minutes after (Post-task) the parent-child interaction tasks. Saliva collection procedures were originally adapted from those used by G unna r, Mangelsdorf, Larson, and H ertsgaard (1989). Participants were asked to mouth a sterile cotton dental roll (R ichmond, NC) for 2±3min after which interviewers expresse d clear saliva from the cotton using a 10cc needleless syringe into a 2ml cyrogen ic storage vial. Following recommenda tions of Schwartz et al. (in press), an oral stimulant was not used to enhance saliva ¯ ow. Pre-task samples were used to estimate labora tory baselines in anticipation of the interaction sequence. Post-task samples were used to compute an index of task-related cortisol ``reactivity or change’ ’ in response to the interaction series. The interviews occurre d in the late afternoon and early evening. O n average pre-task samples were collected at 2.47p.m . (SD = 1h 57m in) and post-task samples at 3.57p.m. (SD = 1h 55m in). Samples were stored at ± 20 C until shipped overnigh t to the Center for the Interdisciplinary Study of Immunology and D isease at the U CLA H ealth Science Center. They were stored at ± 70 C


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until assayed using a radioimmunoa ssay for cortisol (ICN, Costa Mesa, CA ). The assay had a lower limit of sensitivity of 0. 03m g/dl, and average intra- and inter-assay coef® cients of variation less than 10% and 15% , respectively. A ll samples were tested in duplicate with samples from each dyad tested in the same assay batch. Values used in the analyses are the average of the duplicate scores. A nalytic Strategy. First, differences in cortisol levels attributable to sampling occasion (i.e. pre- vs. post-task), sample collection time, family member, and child age and gende r are explore d. Next, concorda nce between maternal and child cortisol levels measured in anticipation and response to the con¯ ict discussion task is described. Then individua l differences in children’ s cortisol levels in anticipation and response to the interaction task in relation to maternal, child, and family characteristics are examined. Finally, we evaluated if children’ s cortisol levels are associated with the transfer of risk for internalising behaviour proble ms from maternal and family environm ental characteristics.

RESULTS Sam ple Collection T ime, Sam pling O ccasion, Fam ily M em ber, G ender, and A ge. Pre-task cortisol levels were signi® cantly correlated with sample collection time [r(60) = ± . 30, P , . 018] for mothers, and approa ched signi® cance [r(60) = ± . 20, P = . 11] for children. The correlation between post-task cortisol levels and sample collection time were not signi® cant for mothers [r(60) = ± . 03, n.s.] but approa ched signi® cance for children [r(60) = ± . 21, P = . 11]. U sing cortisol ( m g/dl) as the depende nt measure, sampling occasion (pre- and post-task) and family member (parent vs. child) as repeated measures, and child gender as a blocking factor in a 2 2 2 mixed-model A NO VA (with sampling time of day and age covaried), revealed a signi® cant family member by sampling occasion interaction [F(1,53) = 8. 24, P , . 006]. The children’ s mean cortisol levels were: 0. 10m g/dl (SD = . 05) pre-task and 0. 11m g/dl (SD = . 10) post-task. The mother’ s cortisol levels were on average: 0. 19m g/dl (SD = . 12) and 0. 11m g/dl (SD = .06) pre-task and post-task, respectively. Post-hoc tests indicated pre-task cortisol levels were higher for mothers than for the children [t(61) = 5. 54, P , . 0001]. U sing an increase over pre-task levels of 15% as a criteria, 36.2% of children and 13.3% of their parent-partners showed task-related cortisol elevations. There were no signi® cant relationships between maternal or child cortisol levels and children’ s age or gender.

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Concordan ce between M aternal and Child Cortisol L evels. A s expected, pre-task and post-task cortisol levels were highly correlated [r(54) = . 51, P , . 0001] for children and [r(59) = . 50, P , . 0001] for mothers. Mother and child cortisol levels were correlated post-task [r(56) = . 37, P , . 005], but not signi® cantly related when measured before the task. Mother’s pre-task cortisol levels predicted their children’s posttask cortisol levels [r(55) = . 38, P , . 005]. Conversely, the children’ s pretask cortisol levels were associated with their mother’ s post-task cortisol levels [r(58) = . 48, P , . 0001] (see Fig. 1). When relations between the dyads’ cortisol levels were analysed separately within each behaviour proble m group an interesting difference was revealed (see Fig. 2). Within the aggre ssive-only group mother-child post-task cortisol levels were highly correlated [r(10) = . 73, P , . 007], and the mother’s [r(10) = . 66, P , . 02], but not the children’ s cortisol levels were correlated pre- to post-task. For the withdra wn-only group the children’ s pre-task cortisol levels predicted the mother’ s post-task cortisol levels [r(7) = . 85, P , . 004], but neither maternal or child cortisol levels were correlated pre- to post-task. Within the aggressive/withdrawn group both maternal [r(9) = . 80, P , . 003] and child [r(7) = . 84, P , . 005], cortisol levels were correlated from pre- to post-task, yet there was no relation between mother and child cortisol levels at either sampling occasion. Finally, for the control group the children’ s pre-task levels predicted the mother’ s post-task cortisol, [r(26) = . 43, P , . 023], but only the children’ s cortisol levels were correlated pre- to post-task [r(25) = . 58, P , . 001].

FIG. 1. A ssociations between maternal and child cort isol levels (m g/dl) pre- and postinteraction task for combined sample. ( = P ,

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de® ned using maternal levels of childhood behaviour problems. ( = P ,

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FIG. 2. A ssociations between maternal and child cortisol levels (m g/dl) pre- and post-interaction task by subgroup

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Individual D ifferences in Children’s Cortisol L evels in A nticipation and R esponse to Con¯ ict T ask . To control for nonbe haviour al factors that could in¯ uence the children’ s cortisol levels, these analyses used standardised residual pre-task and post-task cortisol scores. Following G ranger et al. (1994, 1996), regression equations were computed predicting pre-task cortisol levels from pre-task sample collection times. R esidual pre-task scores were produce d by subtracting the predicted scores from the observed pre-task cortisol levels. Standardised residual pre-task cortisol scores were used to index children’ s H PA activity before the con¯ ictdiscussion task. Similarly, residual post-task cortisol scores were produce d using linear regression and predicting post-task levels from post-task sample collection times and pre-task cortisol levels, then subtracting the predicted scores from the observed post-task levels. Standardised residual post-task cortisol scores were used to index variability in the children’ s cortisol levels that may be related to their participation in the task interaction (i.e. independe nt of sampling time of day and pre-task cortisol levels). The analyses then proceeded in two steps. First, the correlates of children’ s pre-task and post-task residualised cortisol scores were identi® ed within each measurement domain (i.e. child, maternal, and family assessments). The second step evaluated the relative and combined contributions of the signi® cant predictors from each domain. Fam ily environm ent. Children’ s pre-task cortisol scores were associated with child-reported [r(60) = ± . 35, P , . 007] and mother-reported [r(60) = ± . 28, P , . 025] levels of family con¯ ict. Children’ s ratings on the FES subscale measuring control were associated with their pre-task [r(60) = ± . 28, P , . 025] and post-task [r(60) = ± . 28, P , . 025] cortisol scores. R egression analyses (stepwise criteria PIN , .05) revealed that mother-rated (beta = ± . 34, R SQ = . 08, P , . 019), and child-rated (beta = ± . 285 , R SQ = . 12, P , . 006) levels of family con¯ ict made unique contributions to the prediction of children’ s pre-task cortisol scores [R SQ = . 20, F(2,57) = 7. 16, P , . 002]. Parenting stress. Children’ s pre-task cortisol scores were associated with the following subscales of the PSI: mood [r(60) = ± . 39, P , . 002], distractability/hyperactivity [r(60) = ± . 29, P , . 024], reinforces parent [r(60) = ± . 27, P , . 031], depression [r(60) = ± . 25, P , . 049], social isolation [r(60) = ± . 34, P , . 006], parent health [r(60) = ± . 36, P , . 004], and restrictions of role [r(60) = ± . 26, P , . 042]. A stepwise linear regression (PIN , .05) including each of these scales revealed that the PSI mood subscale (i.e. parent-perceived impact that their child’s mood has on their stress level) made a unique contribution to the prediction of children’ s pretask cortisol scores [R SQ = . 149 , F(1,59) = 10. 36, P , . 002]. Maternal perceptions of parenting stress were not associated with the children’ s post-task cortisol scores.


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Children’s behav iour problem s. Children’ s pre-task cortisol scores were correlated with the internalising [r(60) = ± . 35, P , . 006], externalising [r(60) = ± . 32, P , . 01], and total proble ms [r(60) = ± . 33, P , . 01] CBCL summary scale scores. The following narrow band behaviour proble m subscales were also associated with children’ s pre-task cortisol scores: anxiety/depression [r(60) = ± . 31, P , . 014], social withdra wal [r(60) = ± . 29, P , . 023], somatic complaints [r(60) = ± . 27, P , . 033], and aggre ssion [r(60) = ± . 28, P , . 03]. A follow-up stepwise regression (PIN , . 05) revealed that among these variables, only the CBCL internalising summary scale made a unique contribution to the prediction of children’ s pre-task cortisol scores [R SQ = . 118 , F(1,59) = 7. 92 P , . 007]. The children’ s behaviour proble ms were not associated with their post-task cortisol scores. M others’ childhood behav iour problem s. The ® rst analyses correlated maternal PE I withdra wal and aggre ssive behaviour nom ination z -scores with their children’ s pre-task and post-task cortisol scores. Children’ s pretask cortisol scores were associated with their mothers’ levels of socially withdrawn behaviour problems dur ing their childhood [r(60) = ± . 27, P , . 032]. A follow-up analysis used a repeated-measure A NO VA with planned contrasts to compare pre-task and post-task cortisol levels ( m g/dl) between each of the CLR P behaviour proble m groups (i.e. aggressive-only, withdrawn-only, and aggressive /withdrawn groups) and the comparison group. Children born to mothers from the aggre ssive-only group (M = ± . 34, SD = . 48) showe d signi® cantly (LSD tests P , . 05) lower post-task cortisol levels than did the control group (M = . 23, SD = 1. 07). No two other groups’ cortisol levels ( m g/dl) were signi® cantly different from each other. M others’ current sym ptom atology . The children’ s pre-task cortisol scores were correlated with SCL-90 subscales representing interpersona l sensitivity [r(60) = ± . 42, P , . 001], depression [r(60) = ± . 32, P , . 012], and phobic anxiety [r(60) = ± . 36, P , . 003]. A stepwise regression (PIN , . 05) revealed that among these constructs only the interpersona l sensitivity scale made a unique contribution to the prediction of children’ s pre-task cortisol scores [R SQ = . 18, F(1,60) = 13. 00, P , . 001]. R elative and com bined effects of child, m aternal, and fam ily characteristics. This series of analyses evaluates the unique and combined contribution that each predictor identi® ed earlier makes to the prediction of the children’ s residualised pre-task cortisol scores. Children’ s pre-task cortisol scores were regressed on the CBCL internalising summary scale score, the FE S mother and child-rated con¯ ict scales, the SCL interpersona l sensitivity scale, the mother’ s childhood levels of social withdrawal (PE I nomina tion z-score), and the PSI mood subscale using stepwise procedure s (PIN , . 05). The resulting equation accounted for

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40.8% of the variance [F(4,54) = 9. 32, P , . 0001]. The mother’ s interpersona l sensitivity (SCL, beta = ± . 332; R SQ = . 194 , P , . 005), the child’s perception of the level of family con¯ ict (FES, beta = ± . 266; R SQ = . 09, P , . 015), the mother’s childhood levels of socially withdrawn behaviour proble ms (PE I, beta = ± . 286; R SQ = . 075 , P , . 009), and the parents’ percept ions of stress created by the child’s negative moods (PSI, beta = ± . 244; R SQ = . 05, P , . 038) each contributed unique ly to the prediction. D oes Children’s H PA A xis A ctivity A ffect the R elationship between M aternal Interpersonal Sensitivity or Parenting Stress and their Internalising B ehaviour Problems? We observed signi® cant correlations between children’ s internalising behaviour problems and maternal interpersona l sensitivity (SCL-90) [r(60) = . 524 , P , . 001], as well as between children’ s internalising behaviour problems and parenting stress (Mood subscale from the PSI, see previous section) [r(60) = . 44, P , . 001]. There were also signi® cant associations between children’ s residualised pre-task cortisol scores and maternal interpersonal sensitivity [r(60) = ± . 422 , P , . 001], and parenting stress [r(60) = ± . 386 , P , . 001]. A s noted earlier, children’ s residualised pre-task cortisol scores and levels of their internalising behaviour proble ms were also signi® cantly correlated [r(60) = ± . 347 , P , . 006]. This pattern of associations raises the possibility that children’ s cortisol levels are mediating the relationship between maternal interpersona l sensitivity or parenting stress and their internalising behaviour proble ms. Following the logic of Baron and Kenney (1986) we comput ed two regression equations to evaluate this possibility. The ® rst equation predicted levels of the children’ s internalising behaviour proble ms (criterion variable) from the SCL-90 maternal interpersona l sensitivity subscale (predictor) and the children’ s residualised pre-task cortisol scores. The second equation predicted children’ s internalising behaviour proble ms from the PSI mood scale (predictor) and the children’ s residualised pre-task cortisol scores. In both equations the cortisol scores were entered after the predictor. If the children’ s H PA activity was mediating these relationships then the associations between maternal interpersona l sensitivity and parenting stress would be substantially reduced when the residualised cortisol scores were included in the equations. The analyses revealed signi® cant relationships between maternal interpersona l sensitivity and children’ s internalising proble ms (beta = . 478 , P , . 0001), and between children’ s internalising proble ms and parenting stress (beta = . 235, P , . 01), even after cortisol scores were included in the equa tions. Interestingly, the relationsh ip between children’ s cortisol scores and internalising behaviour problems was not signi® cant in either equation. Thus, there was no evidence that children’ s


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cortisol levels in¯ uenced the association between maternal characteristics and children’ s internalising behaviour proble ms.

DISCUSSION The present investigation revealed systematic relationships between children’ s cortisol measured prior to a con¯ ict-oriented parent-child discussion and their mother’s current psychosocia l proble ms, perceived parenting stress, and childhood levels of social withdra wal; dimensions of family context representing the open expre ssion of aggression, anger, and con¯ ict; and their internalising behaviour problems. By contrast, children’ s cortisol levels measured after the con¯ ict-discussion task were associated with family environm ents characterised by rigid rules as well as with their mother’ s childhood levels of aggressive behaviour proble ms. The ® ndings reveal for the ® rst time (to our knowle dge) an interesting difference between maternal and child adrenoco rtical responsiven ess to parent-child con¯ ict. In a companion report (G ranger, Serbin, & Schwartzman, in progress), mothers’ pre-task cortisol levels were shown to be positively correlated with levels of aggression-host ility, neglect-indifference, and rejection they directed towards their children. We also observed patterns of concordance between maternal and child cortisol levels, and in maternal and child cortisol ``stability’ ’ from pre- to post-task. These patterns varied as a funct ion of the mother’ s childhood levels of aggre ssive and socially withdrawn behaviour problems. A lthough children’ s H PA activity was associated with their internalising behaviour proble ms, we did not ® nd evidence support ing that cortisol levels mediate the intergenerational transfer of risk. Children’ s cortisol levels did not contribute to the prediction of children’ s internalising behaviour proble ms beyond that explained by maternal dysfunct ion and family environm ental characteristics. The ® ndings have several potential implications. A lthough the behavioural and contextual factors related to the children’ s cortisol levels con® rm previous research, the direction of the relationships is relatively nove l. The overwhe lming pattern is that negative dimensions of child, maternal, and family adjustment were inversely correlated with the children’ s cortisol levels. The ® ndings appear to be consistent with those described by Flinn and E ngland (1995). Children unde r chronic stress were shown to have subnorm al cortisol levels in nonst ressful conditions. H ence, these ® ndings support the possibility that high-risk early childhood rearing environments may have the potential to in¯ uence the threshold of the sensitivity of the H PA axis to social challenge. Theoretically, lower basal levels of H PA activity would be associated with increased reaction potential. H owever, studies sugge st that:

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(1) the cortisol response is stimulated by uncertainty that is perceived as signi® cant and for which behavioura l response s will have unknown effects; and (2) habituation may occur to repeated events for which a child acquires an effective cognitive and behavioural response (Levine , 1993). Thus, in this special popula tion, the children may be very familiar with parent-child con¯ ict and therefore may no longer evince a detectable H PA response to the mildly challenging social con¯ ict presented during the laboratory exercise. The observation that neither ratings of maternal or child aggressive behaviour during the interaction task were related to the children’ s cortisol reactivity support s this interpretation. It is also possible, howeve r, that children who are less aroused by con¯ ict have more interpersona l dif® culties, which in turn, lead to increased stress and insensitivity in their parents. A lternatively, H PA activation and familial con¯ ict may have reciprocal in¯ uences on each other. For instance, increased familial stress might lead to reduced child arousal in con¯ ict situations which may be an antecedent to more familial con¯ ict and stress leading subsequently to childhood behaviour proble ms. A dditional studies are clearly needed aimed towards ruling out the many alternative rival hypothe ses. A noteworthy ® nding was that aspects of behaviour proble ms and social context were predom inantly related to children’ s pre-task rather than posttask cortisol levels. A t ® rst glance, this observa tion appears inconsistent with the ® ndings presented by G ranger et al. (1994, 1996, 1998). In those studies relationships were not observe d between clinic-referred children’ s behaviour proble ms and pre-task cortisol levels. O ne possibility is that the present ® ndings hint at a developmental antecedent to the relationships described in those studies. The children in this project were young (M age = 6.68; range 5±11) and were ``at pro babilistic risk’ ’ for psychosocia l proble ms. By contrast, the sample studied by G ranger et al. were older (M age = 12.08, range 7±17) and had been recruited from the intake assessments at community-ba sed mental health clinics to which they had been referred for treatment of multiple and severe behaviour proble ms. The children were interviewed before treatment began thus their emotional and behaviour al problems were likely to be near peak intensity. It is plausible that aspects of early experience are initially associated with an atypical cortisol pro® le (low levels and reactivity) which, when integrated over time with emerging internalising behaviour proble ms, leads to exagger ated reactivity later in middle childhood and adolescence. To our knowle dge, this is the ® rst time concordance between maternal and child cortisol levels has been addressed in a high-risk sample. It is interesting that the dyads’ cortisol levels were associated post-task but not pre-task. O ne alternative explanation is that cortisol levels synchronise as the dyad engage s and focuses mutual effort toward achieving the shared


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goals of the interaction activities. It is also intriguing that differences in concordance and ``stability’ ’ were associated with maternal levels of childhood behaviour proble ms. It is tempting to speculate that maternal adjustment problems would contribute to the juxtaposition of the dyads’ cognitive and behavioural strategies. To the extent that individua l rather than shared agendas are pursue d, concordance between the dyads’ cortisol levels might be affected. A ny interpretation of these relationships would be tentative at best, as the effects look large but the magnitude of these correlations, in some instances, may result from the small sample size. Full appreciation of these ® ndings’ implications awaits their more compre hensive study. O ur intention was to contribute to the accumulating body of evidence that sugge sts the study of children’ s adrenocort ical activity may provide important clues abou t the mechanisms that regulate the effects of adverse environm ental circumstances on the development of children’ s internalising behaviour problems. Inde ed, these ® ndings are impressive in that they reveal a substantial portion of the variance (40.8% ) in children’ s cortisol levels can be explained by the simultaneous consideration of aspects of maternal, family, and child psychosocia l proble ms. Internalising behaviour proble ms were pred icted to be related to cortisol levels. Interestingly, the results indicated no unique contribution for cortisol levels after other maternal and family characteristics were included in the models. The ® ndings suggest maternal and family characteristics account for the relationship between children’ s cortisol levels and their internalising behaviour proble ms. They indicate that the important relationship may be that an adverse familial environment mediates the impact of cortisol on children’ s internalising problem behaviour. The study generated some potentially interesting results, but there are limitations which restrict the implications of the ® ndin gs. H ellhammer and Wade (1993) argue that the H PA axis is extremely sensitive to social in¯ uences and can only be investigated in an individua l’s natural environm ent. Thus, it is possible that differential sensitivity of the children or parents to the laboratory environm ent may have contributed to the observed pattern of associations. A lso, this study relied extensively on mother-report. Bias in these mothers’ self-report that may have in¯ uenced interrelationships among the measures may have affected the ® ndings. The robust pattern of ® ndings linked to pre-task cortisol levels focuses attention on whether this index represents a labora tory baseline measure or an anticipatory reaction to the discussion task. Each of these issues would be important to consider when designing future studies. Further investigations of the associations among high-risk children’ s H PA activity and behaviour proble ms, in quasi-naturalistic and everyda y social contexts seem well justi® ed. In particular, data are needed to assess

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cross-situational consistency of individual differences such as those revealed here. Carefully controlled longitudinal work is also needed to assess the tempora l relationship between the emergence of atypical H PA activity and symptoms of children’ s internalising behaviour proble ms. Manuscript received July 1998

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