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ORIGINAL ARTICLE
Variations in Heritability of Cortisol Reactivityto Stress as a Function of Early Familial AdversityAmong 19-Month-Old Twins
Isabelle Ouellet-Morin, MPs; Michel Boivin, PhD; Ginette Dionne, PhD; Sonia J. Lupien, PhD; Louise Arsenault, PhD;Ronald G. Barr, MDCM, FRCPC; Daniel Pe´russe, PhD; Richard E. Tremblay, PhD
Context
:
Cortisolreactivityisamarkerofvulnerabilityforavarietyofstress-relateddiseasesthatlikelyarisefromthe contributions of both genetic and environmentalsourcesofinfluence.However,littleisknownaboutgene-environment interplay in early cortisol reactivity.
Objectives
:
To examine the genetic and environmen-talcontributionstoearlycortisolreactivityinapopulation-based sample of 19-month-old twins and to determinewhether these contributions vary as a function of earlyfamilial adversity.
Design
:
A variant of the twin method, with genetic andenvironment contributions to cortisol reactivity esti-matedasafunctionoffamilialadversity.Familialadver-sity was defined as the presence of 7 risk factors duringperinatal and postnatal development (eg, at 6 and 19monthsofage):maternalsmokingduringpregnancy,lowbirth weight, low family income, low maternal educa-tionallevel,singleparenthood,youngmotherhood,andmaternalhostileorreactivebehaviors.Twinsexposedto4 or more risk factors at either time were considered ashaving been exposed to high (vs low) familial adversity(23.4% of the sample).
Setting
:
CentredeRechercheFernand-SeguinattheHoˆ-pital Louis-Hyppolite Lafontaine, Montre´al, Quebec.
Patients
:
Participants were families of twins from theQue´bec Newborn Twin Study recruited between April1, 1995, and December 31, 1998, in the greater Mon-tre´alarea.Atotalof346twins,130monozygoticand216dizygotic, were included in the study.
Main Outcome Measures
:
Salivary cortisol sampleswerecollectedbeforeandaftertheparticipatingtwinshadbeen exposed to unfamiliar situations; change in cortisolover time was used as a measure of cortisol reactivity.
Results
:
Distinct patterns of genetic and environmentalcontributionstocortisolreactivitywereevidencedasafunc-tion of familial adversity, suggesting a possible gene-environmentinterplay.Inlow–familialadversitysettingsthatcharacterizedmostfamilies,bothgeneticanduniquebutnotsharedenvironmentalfactorsaccountedforindi-vidualdifferencesincortisolreactivity,withsharedgenesexplaining the similarity observed within twin pairs. Bycontrast,inconditionsofhighfamilialadversity,bothsharedand unique environmental factors, but not genetic fac-tors, accounted for the variance in cortisol reactivity.
Conclusion
:
This pattern of differing genetic and envi-ronmentalcontributionsaccordingtofamilialadversitysug-geststhat,earlyinlife,highfamilialadversitymayhaveaprogrammingdevelopmentaleffectoncortisolreactivity.
 Arch Gen Psychiatry. 2008;65(2):211-218
T
HE HYPOTHALAMIC
-
PITU
-itary-adrenal(HPA)axisun-derlies both adaptive andmaladaptive responses tostress.
1,2
Adaptiveresponsesto stress are characterized by relativelyrapid activation and inhibition of corti-sol secretion,
1,3
a glucocorticoid hor-mone produced by the HPA axis. How-ever, responses to stress may becomemaladaptivewhentheyareprolonged,failto habituate, are repeatedly activated, orare quiescent when needed.
4
Large individual differences in cortisolsecretionhavebeenobservedduringstress-fulconditions.
5,6
Substantialdeviationsfromnormativecortisolresponsestostressmayresult from dysfunctional HPA axis reac-tivityandhavedamagingeffectsovertime.
1,3
Disrupted cortisol reactivity has been as-sociated with behavior problems and psy-chiatric disorders, such as anxiety,
7-9
de-pression,
10,11
behavioral inhibition,
12,13
posttraumaticstressdisorder,
14,15
andcon-ductproblems.
16,17
Cortisolreactivityisthusa marker of vulnerability for a variety of 
Author Affiliations
are listed atthe end of this article.
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stress-relateddiseases.
2
Understandingtheetiologyofcor-tisol reactivity early in development may clarify the roleofearlyvulnerabilitytostressduringlateronsetofstress-related diseases.The interindividual variability in cortisol reactivitylikely arises from the joint contributions of genetic andenvironmental sources of influence. However, researchhas mainly documented the association between ad-verse environments and cortisol reactivity during child-hood and adolescence.
18-20
Cortisol reactivity has beenassociated with low socioeconomic status,
21-23
maternaldepression,
24,25
maltreatment and abuse,
26-29
and expo-sure to community violence.
30
Only a handful of studies
28,31,32
have documented therelationshipbetweenadverseenvironments,suchasharshand insensitive parenting, and cortisol reactivity duringthe preschool years. These studies suggest a likely con-tribution of early adverse environments to cortisol reac-tivity.However,becausetheyremainblindtotheroleof geneticfactorsinthatassociation,itisdifficulttoclearlyestablish the nature of this contribution.
33-36
Twin stud-ies are useful to this end, but few twin studies have ex-amined the genetic and environmental contributions tocortisolreactivity.Kirschbaumetal
37
showedthatmono-zygotic twins were more similar than dizygotic twins incortisolresponsetocorticotropin-releasingfactorinjec-tion but not with respect to physical and psychologicalstress. Pritchard et al
38
found no genetic contribution tocortisolresponsetooverfeedinginyoungadulttwinpairs.However,thesmallsamplesizes(ie,fewerthan25pairs)andthefactthatthesestudieswereconductedwithyoungadultsprecludeanyconclusionaboutpossiblegeneticcon-tributions to cortisol reactivity in early childhood. Thegenetic and environmental contributions to cortisol re-activity in early childhood have yet to be documented.Genetic and environmental factors may contribute toearlycortisolreactivityinvariousways.Oneprevailinghy-pothesisstatesthatgeneticandenvironmentalfactorsarelikely to combine nonlinearly to affect cortisol reactiv-ity.
39
Gene-environment interplay has been documentedthrough different approaches, including variations in ge-netic and environmental contributions according to en-vironmental circumstances.
39,40
Accordingly, 2 forms of gene-environmentinterplaymaybeanticipatedfrompre-vious research. First, as suggested by a diathesis-stressmodel,
41
genetic factors could predispose a child to reactwithanincreasedcortisolresponseifexposedtostressfulenvironments.
42
Inthiscase,ageneticvulnerabilitytostresswouldbemorelikelytobeexpressedduringadversitythanwith favorable conditions. Results showing higher heri-tabilityofcortisolreactivityinconditionsofenvironmen-talconstraints,suchashighvslowfamilialadversity(FA),would be consistent with such a model. The findings byCaspi et al
43,44
that genetic liabilities (ie, low monoamineoxidase A level or serotonin transporter short allele) ex-acerbated the impact of adverse environments (ie, mal-treatment or life stress events) on later psychopathologicconditions(ie,antisocialbehaviorordepression)arecon-sistent with this form of genes
environment process.A second possibility is that of a developmental pro-gramming effect on the HPA axis, taking the form of areduced genetic influence on cortisol reactivity in earlyadverse conditions.
45,46
This idea is consistent with thewell-documentedincreasedsensitivityofstress-reactivesystems to environmental influences in early develop-ment.
47-50
Inrodents,prolongedperiodsofmaternalsepa-ration have been associated with increased corticoste-rone reactivity.
51-53
Cross-fostering studies
54,55
have alsoshownthatHPAaxisreactivityismodulatedbyearlyma-ternal care through epigenetic processes. Confirmationthat these processes operate among humans awaits, al-thoughamarkedbrainplasticitytoenvironmentduringinfancy has been documented.
10,56,57
In a twin design, afindingshowing(1)reducedgeneticcontributionstocor-tisol reactivity among twin siblings exposed to high FAand (2) higher genetic contributions among twins ex-posed to low FA would be consistent with this model.Themaingoalsofthepresentstudyweretoanalyzethegeneticandenvironmentalcontributionstocortisolreac-tivitytoanunfamiliarcontextin19-month-oldtwinsandto examine variations in genetic and environmental con-tributions to cortisol reactivity according to early FA. Atthis age, children typically react with marked anxiety tounfamiliar situations and adults, but large individual dif-ferencesinbehavioralandphysiologicresponseshavebeendocumented.
58-60
Familialadversitywasdefinedasafunc-tion of prenatal and postnatal risk factors previously as-sociated with cortisol reactivity to reflect the cumulativeeffects of stressful environments in children’s lives.
40
METHODS
SAMPLE
This study was conducted under controlled conditions at theCentre de Recherche Fernand-Seguin at the Hoˆpital Louis-Hyppolite Lafontaine in Montre´al, Que´bec. Participants werefamilies of twins from the Que´bec Newborn Twin Study re-cruited between April 1, 1995, and December 31, 1998, in thegreater Montre´al area. A total of 989 families were contacted,of which 672 agreed to participate (68.0%). Twins were firstseen when they were 6 months of age and then prospectivelyassessed for a variety of child and family characteristics. Afterinformedconsentwasobtainedfromtheparents,salivasampleswerecollectedat19months(mean[SD],18.85[0.74]months)for 466 twins before testing, 474 twins after testing, and 423childrenatbothtimes.Interviewsregardingenvironmentalvari-ables were conducted with the mother in 99.7% of cases.Zygosity was determined through the Zygosity Question-naire for Young Twins when the twins were 6 and 19 monthsof age,
61
using independent ratings of the twins’ physical simi-larities.TheDNA-basedzygositywasdeterminedfor31.3%of thesame-sextwinpairsrandomlyselected,using8to10highlypolymorphic microsatellite markers. The 2 methods yielded aconcordance of 93.8%.
62
THE STRESSFUL CONTEXT:EXPOSURE TO UNFAMILIAR SITUATIONS
At 19 months of age, each participating twin was successivelybrought into the laboratory and exposed to 2 unfamiliar situa-tions known to be moderately stressful at that age.
59,63,64
In thefirstsituation,1twinandthemotherwerealoneinacornerofaroomwhenawomandressedasaclownenteredtheroom,wentto the opposite corner, and invited the child to approach by of-feringasetoffamiliartoys.Inthesecondsituation,anoisy,odd-
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looking, moving toy robot was placed on a platform in the op-posite corner of the room. Each session lasted 280 secondsseparated by 5 minutes of mother-child free play. For the first140 seconds, the mother was asked to remain passive and nottointeractwithherchild,respondingonlytochild-initiatedtalkwithbriefstatements(eg,“It’sokay,”“It’saclown”).Forthelast140seconds,themotherwasallowedtodowhatevershethoughtwas needed to help her child be at ease with the stimulus.
SALIVA COLLECTION
Salivarycortisolsamplingisanoninvasiveandvalidwaytoas-sessHPAaxisactivity.
65,66
Allsalivasampleswereobtainedbe-tween 8:05
AM
and 12:15
PM
during the 19 months of labora-tory visits. Mothers were instructed not to give their childanythingtoeatordrink20minutesbeforeeachsamplingtime.Saliva was collected before and after the unfamiliar situations(Salivette;Sarstedt,Nu¨mbrecht,Germany)andstoredat−80°Cuntil analysis. The posttest sample was obtained 20 minutesafter the end of the procedure to capture the peak cortisol re-sponse.
67
All samples were analyzed in a single batch using ra-dioimmunoassay (Diagnostic Systems Laboratories Inc, Web-ster, Texas). The technician was blind to the zygosity status of the samples. Intra-assay variability was less than 10%.
ASSESSMENT OF FA
Familial adversity was assessed to reflect the putative cumu-lative adverse effects of environmental risk factors on chil-dren’sadjustment.
18
Inthepresentstudy,anFAindexwascre-ated by combining information about 7 risk factors: maternalsmoking during pregnancy, low birth weight, low family in-come,lowmaternaleducationallevel,singleparenthood,youngmotherhood, and maternal hostile or reactive behaviors. In-formation about these risk factors was collected prospectivelywhenthetwinswere6and19monthsofage,allowingchangesin some risk factors (eg, low family income) to be taken intoaccount.Ascoreof1wascountedforthepresenceofeachriskfactor at each time. The scores were summed to reflect the cu-mulativeimpactoftheseriskfactorsovertime,assumingequalweight for each risk factor. The FA score could thus vary from0to12.Ariskfactorwasscoredifthemothersmokedcigarettesacrossalltrimesters(24.9%ofthefamilies),birthweightwaslowerthan 2500 g (46.5%), family income was below CaD $20000(19.2%and15.4%at6and19months,respectively),themotherhadnotcompletedhighschool(19.0%atboth6and19months),the twins were not living with both of their biological parents(5.5% and 11.0% at 6 and 19 months, respectively), and themother was younger than 20 years when she gave birth to thetwins (3.2%). Finally, a 7-item, 10-point (0 indicatingnot at allto 10 indicatingexactly) Likert-type self-report scale was usedat 6 and 19 months to assess the mother’s hostile or reactiveparenting toward the twins (eg, “I have shaken my baby whenheorshewasparticularlyfussy”or“Ihavelostmytemperwhenhe or she was particularly fussy”) (Cronbach
=0.77 and 0.73at6and19months,respectively).
33
Themother’sscoresforbothtwinswereaveraged,andariskwascountedifthematernalhos-tile or reactive behaviors were above the median.TheresultingFAindexwasdistributedasfollows:FAindexof0,16.6%;FAindexof1,21.7%;FAindexof2,21.9%;FAin-dex of 3, 16.4%; FA index of 4, 10.0%; FA index of 5, 5.1%; FAindex of 6, 4.5%; FA index of 7, 1.4%; FA index of 8, 0.8%; FAindexof9,0.5%;FAindexof10,0.8%;andFAindexof11,0.3%.TheFAindexwasthendichotomizedforthegeneticmodeling:familieswithanFAindexof4orabovewereconsideredtohavehigh levels of FA (23.4%), whereas those who scored below 4were considered to have low levels of FA (76.6%).
STATISTICAL ANALYSIS
Areactivecortisolratiowascomputedaccordingtothelawofini-tialvalues,
68
whichtakesintoaccountthedependencyofthepost-testvaluesontheinitialvalues.Accordingtothelawofinitialval-ues,thechangescoreshouldbeadjustedifthecorrelationbetweenthe initial value (t1) and the change score (t
2
t
1
or
t) is nega-tive,whichwasthecase(
348
=−0.74;
P
.001).
67-69
Acortisolre-activityratiowasthuscomputedbydividing
tbyt1.
11
Thisscorewas examined for outliers, defined as values ±3 standard devia-tionsfromthemean.
67,70,71
Fourchildren(1monozygoticand3dizygotic)wereexcludedfromthesubsequentanalyses.Cortisolreactivityratioswerepositivelyskewedandwerenormalizedusinga log transformation before statistical analysis.
72
Differences in mean cortisol values according to zygosityand sex were investigated through analyses of variance. TheassociationbetweenFAandcortisolreactivitywastestedusinga2-tailed
2
test,andmultinomiallogisticregressionswereper-formed on the discrete patterns of cortisol reactivity. For thelatter, children in the second and third quartiles were clus-tered as the reference category. All statistical tests, except forthe genetic modeling, were conducted on a subsample com-posed of only 1 twin, selected at random, per family.Genetic(A),sharedenvironment(C),anduniqueenviron-ment(E)contributionswereestimatedthroughstructuralequa-tionmodelingofvarianceandcovariancepatternsamongmono-zygotic and dizygotic pairs, using the MX software package.
73
AlltwinpairswereconcordantforFA.Modelsthatallowedpara-meters to vary according to FA were compared with modelsthatconstrainedparameterstobeequalacrossFAgroups.Bestmodelswereselectedaccordingtogoodnessoffit(
2
test)andparsimony indices such as Akaike information criteria (AIC)and the root mean squared error of approximation (RMSEA).
RESULTS
Table 1
presents means and standard deviations for thepretest cortisol levels, the posttest cortisol levels, and thecortisol reactivity ratio for the total sample and as a func-tion of zygosity and sex. The reactivity ratio did not varyaccordingtozygosity(
F
1,211
=0.37;
P
=.54),sex(
F
1,211
=0.98;
P
=.32),orethnicity(ie,whitevsother;
F
1,158
=0.08;
P
=.59).Thetimeofdaywhensalivawascollectedwasnotassoci-ated with pretest or posttest cortisol levels (pretest:
F
1,220
=0.37;
P
=.54; posttest:
F
1,233
=1.06;
P
=.30). The FA
Table 1. Raw Cortisol Values and the Ratio of Changefor the Total Sample According to Zygosity and Sex
VariableMean (SD)BaselineCortisolLevel, µg/dLMean (SD)PosttestCortisolLevel, µg/dLMean (SD)Ratio ofChange
Monozygotictwins0.36 (0.26)(n=182)0.35 (0.22)(n=197)0.33 (1.08)(n=163)Dizygotic twins 0.41 (0.33)(n=284)0.38 (0.27)(n=277)0.26 (0.97)(n=255)Male twins 0.40 (0.31)(n=234)0.37 (0.26)(n=234)0.25 (0.96)(n=212)Female twins 0.39 (0.30)(n=232)0.37 (0.24)(n=240)0.33 (1.08)(n=206)Total sample 0.39 (0.30)(n=466)0.37 (0.25)(n=474)0.29 (1.07)(n=418)SI conversion factor: To convert cortisol to nanomoles per liter, multiplyby 27.588.
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