Early caregiving stress exposure moderates the relation between respiratory sinus arrhythmia

14 Pages·2015·0.47 MB·English

Psychophysiology,53(2016),83–96.WileyPeriodicals,Inc.PrintedintheUSA.
CopyrightVC 2015SocietyforPsychophysiologicalResearch
DOI:10.1111/psyp.12569
Early caregiving stress exposure moderates the relation between
respiratory sinus arrhythmia reactivity at 1 month and
biobehavioral outcomes at age 3
ELISABETH CONRADT,a THEODORE BEAUCHAINE,b BEAU ABAR,c LINDA LAGASSE,d,e
SEETHA SHANKARAN,f HENRIETTA BADA,g CHARLES BAUER,h TONI WHITAKER,i
JANE HAMMOND,j AND BARRY LESTERd,e
aDepartmentofPsychology,UniversityofUtah,SaltLakeCity,Utah,USA
bDepartmentofPsychology,OhioStateUniversity,Columbus,Ohio,USA
cDepartmentsofEmergencyMedicine,Psychiatry,andPublicHealthServices,UniversityofRochesterMedicalCenter,Rochester,NewYork,USA
dDepartmentofPediatrics,WomenandInfantsHospitalofRhodeIsland,Providence,RhodeIsland,USA
eDepartmentsofPsychiatryandPediatrics,WarrenAlpertMedicalSchool,BrownUniversity,Providence,RhodeIsland,USA
fDepartmentofPediatrics,WayneStateUniversitySchoolofMedicine,Detroit,Michigan,USA
gDepartmentofPediatrics,UniversityofKentuckyCollegeofMedicine,Lexington,Kentucky,USA
hDepartmentofPediatrics,UniversityofMiamiMillerSchoolofMedicine,Miami,Florida,USA
iDepartmentofPediatrics,UniversityofTennesseeHealthScienceCenter,Memphis,Tennessee,USA
jRTIInternational,ResearchTrianglePark,NorthCarolina,USA
Abstract
Thereisagrowingscientificinterestinthepsychophysiologicalfunctioningofchildrenlivinginlow-socioeconomic
status (SES) contexts, though this research is complicated by knowledge that physiology–behavior relations often
operate differently in these environments among adults. Importantly, such research is made more difficult because
SESmaybeaproxyforawiderangeofriskfactorsincludingpoorcaregivingandexposuretoparentalsubstanceuse.
We used factor analysis to organize risk-exposure data collected from 827 children—many of whom were raised in
low-SES contexts and exposed to substances prenatally—into dissociable components including economic stress,
caregiving stress (e.g., stress the caregiver may experience, including parental psychopathology), and postnatal
substanceexposure.Thesefactors,alongwithrespiratorysinusarrhythmia(RSA)reactivityatage1month,wereused
topredictbehaviordysregulationandrestingRSAatage3years.AsignificantRSAReactivity3CaregivingStress
interaction indicated that infants who exhibited high RSA reactivity at 1 month experienced the greatest behavior
dysregulation at 3 years, but only when they were exposed to high levels of caregiving stress. Among African
Americans, the highest resting RSA at 3 years was found in infants with less RSA reactivity, but only if they also
experiencedlesscaregivingstress.Ourworkisconsistentwithbiologicalsensitivitytocontext,adaptivecalibration,
andallostaticloadmodels,andhighlightstheimportanceofstudyingPhysiology3Environmentinteractionsinlow-
SEScontextsforpredictingbehaviorandrestingRSA.
Descriptors: Individualdifferences,Infants/children, Heartrate
Socioeconomicstatus(SES)isapotentindicatorofhumanhealth, (Boyce,Sokolowski,&Robinson,2012;Kishiyama,Boyce,Jime-
with effects on both physiological and behavior development nez,Perry,& Knight,2008). However,very littleisknownabout
psychophysiologicalfunctioningamongchildrenwholiveinlow-
SES contexts, although it is recognized that physiological bio-
This work was supported by NIH grants: National Institute of Child markers may aid in the identification of who is most sensitive to
Health and Human Development (NICHD) Neonatal Research Network suchenvironments(Boyce&Ellis,2005).Mostresearchersopera-
and an inter-institute agreement with the National Institute on Drug
tionalizeSESasacompositeofincome,education,andoccupation
Abuse (NIDA) through cooperative agreements: U10-DA-024117-01
(Adleretal.,1994;Bradley&Corwyn,2002).Oftentimes,SESis
and U10-HD-21385 (to S.S.), I10-DA-024128-06 and U10-HD-2786 (to
H.S.B.),U10-DA-024119-01andU10-HD-27904(toB.M.L.),andU10- treatedasa“nuisance”variableinpsychophysiologicalresearch.In
DA-024118-01 and U10-HD-21397 (to C.R.B.); NICHD contract N01- fact, researchers often use it as a statistical control variable when
HD-2-3159(Dr.Lester);and5K08DA038959-03(toE.C.).
they examine physiology–behavioral relations. One reason that
Address correspondence to: Elisabeth Conradt, University of Utah,
SES is rarely used as a predictor of physiological processes is
380S.1530E.BEHS602,SaltLakeCity,UT84112.E-mail:elisabeth.
[email protected] because it is not directly causal. Rather, it is a proxy for
83
84 E.Conradt etal.
unmeasuredvariablesthatexertdirecteffectsonphysiologicaland caregiverwhomaybestressedisthereforeofgreatconcerngiven
behavioral functioning. Low SES is associated with risk factors its associations with impaired parasympathetic functioning and
suchasparentalmentalandphysicalhealth,exposuretoparenting psychopathology.
stress,prenatalandpostnataldrugexposure,andneighborhoodvio- Povertyisalsoofconcern.Themoretimechildrenspendliving
lenceandcriminality(Brooks-Gunn&Duncan,1997).Modelsthat inpoverty,themorebluntedtheirbloodpressureresponsesareto
include these variables are needed to identify processes through stressatage13,overandaboveeffectsofcurrentpoverty(Evans
whichsomechildrenwhoarerearedinlow-SEScontextsdevelop &Kim,2007).Furthermore,greaterhouseholddensityisrelatedto
poorbehavioralandphysiologicaloutcomes. greater blood pressure and heart rate reactivity among fifth and
Todate,mostresearchers,includingourowngroup,haveexam- sixthgraders(Johnston-Brooksetal.,1998).Althoughresearchers
ined how early-life stress affects brain and behavior development have investigated effects of parenting on PNS function among
usingacumulative-riskapproach(Conradtetal.,2014).Thisstrat- motherswholiveinpoverty(e.g.,Conradt&Ablow,2010;Prop-
egyderivesinpartfromtheobservationthatalthoughoverlapping, peretal.,2008),weknowofnostudiesthathavecomparedproxi-
riskfactors are not entirely redundant(e.g.,Conradt, Measelle, & mal (e.g., stress that may affect the caregiving environment;
Ablow, 2013; Evans & Kim, 2012). Cumulative-risk models are Propper & Holochwost, 2013), and distal (e.g., economic stress)
thereforemorepowerfulthansingle-riskmodelsinpredictingprob- risk factors on autonomic and behavioral outcomes. Such study
lembehavior,particularlyamongchildrenwithprenatalsubstance comparisonsarecriticalifwewishto(i)understandhowdiscrete
exposure (Yumoto, Jacobson, & Jacobson, 2008). Importantly, risk factorsaffect physiological and behavioraloutcomes,and(ii)
however,thetypeofearly-lifestressexperiencedmayexertunique formulate more effective prevention and intervention programs
(seeBeauchaine,Neuhaus,Brenner,&Gatzke-Kopp,2008).
effectsoncentralnervoussystem(CNS)andparasympatheticnerv-
Inadditiontoidentifyingtypesofriskfactorsthataffectphysi-
oussystem(PNS)development,evenwhencontrollingforassoci-
ologyandbehavior,wealsoseektodeterminewhichstressorsmay
ated risk factors. PNS function is indexed by respiratory sinus
be more detrimental than others at certain developmental periods
arrhythmia (RSA). RSA consists of oscillatory increases and
(Miller,Chen,&Zhou,2007).Inotherwords,thetimingofexpo-
decreasesofheartrateacrosstherespiratorycycle(seeBeauchaine,
suretolow-SESconditionsmaybeimportantinpredictingbrain–
2001,2015).Thisheartratevariabilityiscontrolledbyacardiores-
behavior outcomes. For example, poverty experienced in early
piratory source generator that projects from the CNS to the heart
childhood is particularly detrimental to emotional and behavioral
through the 10th cranial (vagus) nerve (Berntson et al., 1997;
health compared to poverty experienced in middle childhood or
Grossman,1983;Porges,2007).Intheirreviewoftheliteratureon
adolescence (Brooks-Gunn & Duncan, 1997). Mechanisms (e.g.,
proximalriskfactorsandANSdevelopment,PropperandHoloch-
malnutritionorpoorparentalcare)responsibleforsucheffectsare
wost(2013)concludedthatenvironmentalriskfactors,suchaslow
lessclear.AccordingtoHertzman(1999),stressfulearly-lifeexpe-
SES, may exert negative effects on brain and behavior through
riences may become “biologically embedded” to affect stress
more proximal risk factors, such as parenting. Among children
response system functioning and in turn behavioral responses to
withprenatalsubstanceexposure,postnatalcaregiversubstanceuse
stress. Two partially overlapping theoretical perspectives suggest
may be one such parenting behavior that is associated with poor
howsuchbiologicalembeddingmayoccur:theallostaticloadand
child behavioral outcomes (Mayet et al., 2008). For instance,
adaptivecalibrationmodels.Thepurposeofthisbriefreviewisto
Hickey, Suess, Newlin, and Spurgeon (1995) found that perform-
provide a framework from which to understand how physiology–
anceonanattentiontaskwaslowestamongboyswithprenatalopi-
physiologyandphysiology–behaviorassociationsmaybeaffected
ate exposure and boys with no prenatal drug exposure but whose
bySES.Anexcellentreviewcomparing,contrasting,andproviding
parentsusedopiatespostnatally,comparedtoboyswithnoprenatal
detaileddescriptionsofthesetheoriescanbefoundinHostinarand
orpostnatal exposure. Prenatal parental substance use is also pre-
Gunnar(2013).
dictiveofpostnataluse,whichinturnisassociatedwithchildfoster
According to these perspectives, physiological responses to
careplacement(Smith,Johnson,Pears,Fisher,&DeGarmo,2007).
stressareusuallyadaptiveintheshortterm(Boyce&Ellis,2005;
In turn, child maltreatment is a risk factor for impaired CNS and
Bush & Boyce, 2014; Del Giudice, Ellis, & Shirtcliff, 2011;
ANS functioning (see, e.g., Beauchaine & McNulty, 2013). For
McEwen & Gianaros, 2010; McEwen & Stellar, 1993), and may
instance, Skowron, Cipriano-Essel, Gatzke-Kopp, Teti, and
result from adaptations to the environment in which a child is
Ammerman (2014) found that better inhibitory control was pre- reared(Boyce&Ellis,2005;Bush&Boyce,2014).Allostaticload
dicted by RSA withdrawal, but only for nonmaltreated children. suggests that when faced with recurrent threats and stress, which
High inhibitorycontrol among childrenwho were maltreated was may occur in low-SES contexts, repeated activation of stress
insteadpredictedbyincreasedRSAfrombaselinetotask(Skowron response systems alters the functional operating ranges of neural
etal.,2014). systemsimplicatedinbehavioralimpulsivity,moodregulation,and
Anotherriskfactorcommontochildrenwithprenatalsubstance social affiliation (Beauchaine, Neuhaus, Zalewski, Crowell, &
exposure is maternal depression (Mayet et al., 2008). Depressed Potapova, 2011). These processes induce wear and tear on stress
mothers tend to interact insensitively with their children, who in and immune system functioning,resulting in greater riskfor poor
turn do not exhibit age-expected increases in resting RSA during psychologicalandphysicalhealthoutcomes(McEwen&Gianaros,
earlychildhood(Fieldetal.,2004).Inasampleofdepressedmoth- 2010). Functional operating ranges of certain neural systems may
erswhoareexposedtocontextualriskfactorssuchasfamilystress be inferred from baseline physiological functioning (e.g., Beau-
and low social support, those with chronic depression when their chaine et al., 2011; El-Sheikh & Hinnant, 2011). In other words,
childrenwereages14monthsto6.5yearshadchildrenwithgreater historiesofrepeatedadversityandstressexposurealterphysiologi-
RSA reactivity at age 6.5 (Ashman, Dawson, & Panagiotides, calfunctioningatrest(McEwen&Stellar,1993).Overtime,recur-
2008). Such patterns of RSA reactivity are frequently associated rent threatening experiences, associated vigilance, and feelings of
with internalizing and externalizing psychopathology (see Beau- helplessnesscontributetoanindividual’sperceptionofnewsitua-
chaine, 2001, 2015; Beauchaine & Thayer, 2015). Exposure to a tions as stressful, which in turn initiates a dynamic cascade of
RSAReactivityandLow-Socioeconomic Status 85
behavioral and physiological stress responses that are no longer (El-Sheikh&Hinnant,2011;Propper,2013).HighrestingRSAis
adaptive when they result in protracted or even permanent altera- thoughttoreflectneuralintegrityandreadinesstorespondtoenvi-
tions in physiological functions (El-Sheikh & Hinnant, 2011; ronmental stressors (Beauchaine, 2001, 2015; Porges, 1995).
McEwen & Stellar, 1993). The adaptive calibration model (Del ChangeinRSAinresponsetoenvironmentalstimulationandchal-
Giudiceetal.,2011)isanextensionofbiologicalsensitivitytocon- lengeistermedRSAreactivity.WestudiedeffectsofRSAreactiv-
texttheory(Boyce&Ellis,2005).Itsuggeststhatindividualdiffer- ity at age 1 month because both allostatic load and adaptive
ences in stress responding result from adaptations to particular calibration models indicate that the way in which an organism
environments in which an individual is reared. Over time, and if responds to stress may be a stronger predictor of later behavioral
environmentalconditionschange,thestressresponsesystemadapts and physiological outcomes than basal or resting physiological
andfeedsbacktorecalibrateitsfunctionaloperatingrange,ifnec- measures.Ouroutcomesincludedbehaviordysregulationandrest-
essary.Importantly,highphysiologicalreactivitymaybeadaptive inglevelsofRSAatage3years.Wecalculatedabehaviordysre-
according to this framework, if children with high reactivity are gulation composite, rather than examine internalizing and
raisedinsupportiveenvironments.Thereverseistrue,however,if externalizingbehaviorseparately,because(i)atage3,differences
high-reactive children are reared in negative, threatening, and in internalizing and externalizing behavior may not be as pro-
impoverishedcontexts(Boyce&Ellis,2005). nounced in later childhood (Essex, Klein, Cho, & Kalin, 2002;
Such effects may be direct or mediated through relationships Rose, Rose, & Feldman, 1989); and (ii) the correlation between
withprimarycaregivers.Asnotedabove,childrenrearedinlow-SES internalizingandexternalizingbehaviorwasstrongandpositive.
environmentsareoftenexposedtomaternaldepression,whichren-
ders mothers less responsive to bids for comfort and reassurance
Present Study
(Bradley & Corwyn, 2002; Harnish, Dodget, & Valente, 1995).
Theseexperiencesmayinturnresultinincreasedautonomicactiv- Beforeembarkingonourmainstudyaims,weconductedexplora-
ity/reactivity among affected children (Conradt & Ablow, 2010). toryandconfirmatoryfactoranalysesofvariablesthoughttoindex
According to the allostatic load perspective, if such experiences SES, and variables known to covary with SES, to determine
recur often enough throughout development, multiple “hits” to the whethertypeofstressexposurewasrelatedtobehavioralandphys-
ANSmayleadtoadownregulatedstressresponse(seeBeauchaine iological outcomes. Although SES itself does not cause adversity
etal.,2011;El-Sheikh&Hinnant,2011;McEwen&Stellar,1993). (see above), we included variables traditionally thought to index
Suchmodelsprovideaframeworkthroughwhichtounderstand SESinordertoexamineeffectsofourstressorsaboveandbeyond
someimportantdiscrepanciesinthepsychophysiologicalliterature. SES, and because SES may reflect variables that were not meas-
For example, although it is generally assumed that higher ured in this study (such as family discord). We hypothesized that
resting levels of RSA are adaptive throughout development (see dissociable factors would emerge, representing the range ofstres-
Beauchaine, 2001, 2015; Beauchaine, Gatzke-Kopp, & Mead, sorstowhichchildrenwithprenataldrugexposuremayexperience
2007), higher resting RSA may not predict positive outcomes in (e.g.,exposuretoparentalpsychopathology,parentalstress,lackof
low-SESsamplesorinveryyoungchildren(Conradtetal.,2013; monetary resources, postnatal substance exposure; Dong et al.,
Holochwost, Gariepy, Propper, Mills-Koonce, & Moore, 2014). 2004). Next, we examined main effects and interactions between
Such findings may support the biological sensitivity to context stress variables experienced between birth and age 1 year, and
model.Forinstance, toddlerswhoareraisedinlow-SES environ- behavior dysregulation and resting RSA at age 3 years. Although
mentswhoreceiveinsensitivecaregivinghavethehighestlevelsof
nostudieshaveexaminedeffectsofonetypeofstressor,overand
problem behavior, but only if they also exhibit high resting RSA
aboveothers,giventhecentralityofthecaregivingenvironmentin
(Conradt et al., 2013). Inattention to demographic factors may
early childhood, and the comparatively larger body of work indi-
thereforeobscurephysiology–physiologyandphysiology–behavior
cating associations between caregiving and psychophysiology in
outcomes(seeGatzke-Kopp,2016).
low-SESsamples,weexpectedthatcaregivinginsufficiencywould
Accordingly,amorecompleteunderstandingofstressrespond-
exert a stronger influence on physiological and behavioral out-
inginlow-SESenvironmentsmaybeneededtoidentifyresponses
comesinearlychildhoodthaneconomicinsufficiencyorevenpost-
that are problematic. Using the aforementioned example, in ordi-
natal caregiver drug use. Furthermore, based on both the allostatic
naryenvironments,highrestingRSAisassociatedwithbetterself-
loadandadaptivecalibrationmodels,inadditiontoworkimplicating
regulation, social competence, and empathy (Beauchaine, 2001,
prior experiences of stress reactivity with later resting physiology
2015).Incontrast,inlow-SEScontextsitmayonlypredictadapt-
(El-Sheikh& Hinnant,2011),weexpectedthatthecombinationof
ive outcomes among infants and children who are raised by sup-
exposure to stress and physiological reactivity during the first year
portivecaregivers(Conradtetal.,2013).Specificmeasuresofthe
oflifewouldpredictgreaterbehaviordysregulation,andlowerrest-
typeofenvironmentinwhichchildrenareraisedareneededtotest
ingRSAbyage3years.
processes throughwhichenvironmentsinteractwith physiological
functioning in children, which in turn may affect relevant brain/
Method
behavior relations. Such information in turn may allow us to use
physiological markers to identify children who are vulnerable to
Participants
later problem behavior, particularly in low-SES contexts (Beau-
chaineetal.,2008). We used data from participants in the Maternal Lifestyle Study
We collected measures of children’s RSA in predominantly (MLS), a multisite investigation of effects of prenatal substance
low-SES environments. Seventy-nine percent of these children exposure in a longitudinal follow-up from 1 month to 16 years.
weredrugexposedprenatally.RSAwaschosenbecausefarlessis Mother–infant dyads from singleton gestations were recruited
known about how RSA functions in low-SES environments in between May 1993 and May 1995. Maternal exclusion criteria
childhoodcomparedtothesympatheticorneuroendocrinesystems, includedage<18years,psychosisorhistoryofinstitutionalization
and past research indicates it is sensitive to stressful experiences for intellectual disability or emotional problems, and language
86 E.Conradt etal.
barriersthatpreventedthemfromgivinginformedconsentorunder- (NICU) Neonatal Network Neurobehavioral Scale (NNNS). The
standing the study. All participants spoke English. Infant inclusion NNNSwasadministeredbetween42–44weekspostmenstrualage
criteria included viable, singleton birth, birth weight of at least andisastandardizedcomprehensiveevaluationoftheneurobeha-
500g,gestationalagelessthan43weeksbybestobstetricestimate, vioral performance of high-risk term and preterm infants that
andanegativescreenforchromosomalabnormalityorTORCH(tox- includes neurologicaland behavioralmeasures andsignsofstress
oplasmosis,rubella,cytomegalovirus,herpes,andsyphilis). (Lester & Tronick, 2004). Psychometric properties of the exam
Participants were recruited from Detroit, MI; Memphis, TN; have been established (Lester & Tronick, 2004). The NNNS was
Miami, FL; and Providence, RI. A total of 19,079 mother–infant administeredbycertifiedpsychometristsblindedtoexposurestatus.
dyads were screened for study recruitment. From these, 16,988 Fortherestingperiod,RSAwasmeasuredwhiletheinfantwasina
dyads were eligible for enrollment, and 11,811 (70%) gave con- quiet awake state (state 4 on the NNNS) for at least 2 min
sent.Ofthese,1,072infantswerecocaineexposed.Alistofpossi- (M52.23 minutes). Measurement of RSA occurred during the
blecomparisoninfants(matchedonrace,sex,andgestationalage) NNNS visual attention procedure. This challenge task lasted, on
wassentbythedatacentertoeachstudysite.Motherswerecalled average,6.8minutes(62.43min)andincludesinfantvisualtrack-
on the list in sequence to confirm consent for the 1-month visit. ingtoanimateandinanimatestimuli.Wefoundnosignificantasso-
Whenaninfantinthecomparisongroupdidnotattendthe1-month ciationbetweenthelengthofthechallengetaskandeitherresting
visit,anothermatchwasgeneratedforeachexposedinfantuntila RSA (r5–.002, p5.95), or RSA during the task (r5.044,
comparison infant was successfully enrolled in the 1-month visit. p5.15).Lengthofassessmentswasnotassociatedwithanyofthe
This procedure resulted in two groups at the 1-month visit: 658 stressfactors(allrs(cid:2)–.06and(cid:3).02,allps>.06)orprenataldrug
cocaine-exposed infants (61.4% retention of the cocaine-exposed exposure (r5.05, p5.11). Estimates of RSA were averaged
group)and730infantswithoutcocaineexposure(N51,388). acrossthe attention episode.Differences inRSA measuredat rest
Mothers were approached in the hospital following delivery, andduringthevisualattention“challenge”procedurewereusedto
informedconsentwasobtained,andmotherswereinterviewedfor calculatereactivityscores.RSAreactivitywasmeasuredasRSA
vi-
history of smoking, alcohol use, and drug use during pregnancy –RSA .Therefore,positivescoresreflectincreasesin
sualattention rest
andinthelastyear.Meconiumwascollectedfromthenewbornin RSA, whereas negative scores reflect decreases (i.e., withdrawal)
ordertoconducttoxicologyscreensforcocaineoropiatemetabo- inRSA.
lites. Families were selected for the exposed group (i.e., maternal RestingRSAwasmeasuredatage3,whilechildrenwerewait-
reportofcocaineoropiateuseduringpregnancyorgaschromatog- ingfor a masterymotivation proceduretobegin.Because RSA is
raphy–mass spectrometry confirmation of presumptive positive reducedbypsychomotoractivity(Porges,2007),likeothers(Obra-
meconium screens for cocaine or opiate metabolites) or the com- dovic´, Bush, Stamperdahl, Adler, & Boyce, 2010), we assessed
parisongroup(i.e.,maternaldenialofcocaineoropiateuseduring resting RSA during a nonchallenge “control” task that paralleled
the pregnancy and a negative enzyme multiplied immunoassay themotordemandsofourchallengetask.Useofthistypeoftaskto
meconiumscreenforcocaineandopiatemetabolites).Ifawoman assessrestingphysiologyamongveryyoungchildrenisdescribed
denied use of cocaine during pregnancy but mass spectrometry byBush,Alkon,Obradovic´,Stamperdahl,andBoyce(2011).Rest-
resultswerepositiveforcocaineexposurethenthechildwascon- ingRSAwasmeasuredwhilechildrenplayedwithatoyaloneor
sidered cocaine exposed. Exposed and comparison youth were with an experimenter for an average of 164.8 s (range5135.6–
groupmatchedonrace,sex,andgestationalagewithineachstudy 199.3 s). The correlation between length of the task and resting
site. Background substances associated withcocaine use (alcohol, RSA was not significant, r5–.05, p5.22. Although this resting
tobacco, and marijuana) were present in both groups; thus, most period required some attention, which may evoke moderate vagal
participants were polysubstance exposed. However, a subset of withdrawal(seeSuess,Porges,&Plude,1994),thetoywithwhich
infants (21.3%) was not exposed to any substances in utero. thechildplayedwassimpleandnotaskdemandswereplacedon
Althoughtheoriginalintentofthestudywastoexamineeffectsof thechild.Thetypeofactivitydependedonsite;therefore,wecon-
cocaine exposure on psychosocial outcomes, the purpose of this trol for site in our analyses. Estimates of resting RSA are similar
studywastoexamineeffectsofearly-lifestressinalow-SEScon- (within1SD)tootherstudiesofinfantsandyoungchildrenofsim-
text and psychophysiology on behavioral and physiological out- ilar ages (Alkon et al., 2003; Calkins, Graziano, & Keane, 2007;
comes. We therefore included cocaine exposure and postnatal Calkins & Keane, 2004; Doussard-Roosevelt, Montgomery, &
caregiver cocaine use as covariates in all analyses but did not Porges, 2003), who have also calculated RSA using the same
exploremaineffectsofcocaineexposure.Thestudywasapproved technique.
by the institutional review board at each study site, and written Atbothtimepoints,RSAwasderivedfromtheR-Rtime-series
informed consent (from caregivers) was obtained for all partici- (ortimebetweenadjacentR-waves)collectedfromdigitizedelec-
pants. Each site had a certificate of confidentiality from the trocardiogram (ECG) recordings using Porges’s MXEdit software
NationalInstituteonDrugAbuse. (Delta-Biometrics Inc, 1988–1993). ECGs were recorded using
TheMLSsampleincludeschildreninthefollowingracialcate- three electrodes placed on the child’s chest and abdomen. The
gories:AfricanAmerican(77%),Caucasian(16%),Hispanic(6%), ECG signal was sampled at 1 kHz and stored on a computer for
and children whose parents identified other racial backgrounds later scoring. Interbeat intervals were defined by detection of R-
(1%). There were significantly more African American and His- wavestothenearestms.
panic participants in Detroit, and more Caucasians in Providence Post-processing of data took place offline by using a series of
comparedtotheothersites,v2(9)5299.42,p<.001. automated algorithms. These algorithms were written to identify
R-R intervals outside of expected values. Missed or spurious R-
waves were flagged and corrected via linear interpolation. A 21-
Measures
point moving polynomial was then applied to remove low-
Respiratory sinus arrhythmia (RSA). At 1 month, RSA was frequencytrendsintheHRsignal.Next,abandpassfilterextracted
assessed prior to and during the Neonatal Intensive Care Unit the variance in heart period within the frequency band of
RSAReactivityandLow-Socioeconomic Status 87
spontaneousrespirationinyoungchildren(0.24–1.04Hz;seeZis- Table 1. Percent of caregivers engaging in postnatal substance
ner&Beauchaine,2015).Thisprocessremovesperiodicitiesinthe use at4 or8months
ECGsignalthatareoutsidethefrequencyrangeoftherespiratory
cycle. The resulting measure ofRSA isinthe frequency rangeof Variable Percent
respiration. RSA was computed as the natural logarithm of heart Tobaccouse 58.6
periodvarianceandreportedinunitsofmssquared,ln(ms)2.This Alcoholuse 61.3
methodwasdescribedinitiallybyPorges(1985)andisoneofsev- Marijuanause 24.9
Cocaineuse 17.2
eral acceptable approaches for calculating RSA (Berntson et al.,
Opiateuse 0.6
1997).Spectraldensitieswerecalculatedin30soverlappingwin-
dows and then averaged within each episode (resting period and Note.Tobaccousedefinedaspercentofcaregiverswhosmokedatleast
one cigarette/day when infants were 4 or 8 months old, alcohol use
attentiontask).TheRSAdataforanindividualwasusedaslongas
definedasdrinkingatleast1ounceofalcoholperdayat4or8months,
therewasa30-ssegmentwithlessthan20%ofsegmentsidentified
marijuana use defined as smoking at least one joint/day when infants
with,whichistheshortestdurationrecommendedwhencalculating were 4 or 8 months old, cocaine used defined as using cocaine at least
RSA(Berntsonetal.,1997;Jenningsetal.,1981).Specifically,if oncewheninfantswere4or8months,opiateusedefinedasusingopi-
atesatleastoncewheninfantswere4or8months,n51,259.
6 s or less of RSA data were artifact, then those seconds were
deleted and the rest of the RSA data from the 30-s epoch were
averaged.Inotherwords,eachswasflaggedandremovedif20% tory (BSI; Derogatis & Coons, 1993) at 4 months (a5.96). The
ofthe beats in that 30-s window were marked as artifact, leaving rangesfortheBSIwere0–3.13andcontinuousscoreswereused.
the remaining seconds to be averaged. Thirty-s epochs are fre- Caregiver victimization was measured using the Caretaker
quently sampled in studies of infants and young children (Buss, Inventory of Substance Use (CISU; Shankaran et al., 1996). The
Goldsmith, & Davidson, 2005; Moore & Calkins, 2004). In addi- CISU is a caregiver-report questionnaire of current substance use
tion,smallamountsofartifactcanbeexpectedtohaveaminimal and personal violence sustained by the caregiver. The caregiver
effectonmeasuresofheartratevariability,includingRSA(Bernt- indicatedwhentheinfantwas4monthsand8monthswhetheror
sonetal.,1997). notthecaregiverhadexperiencedphysicalorsexualabuse(05no,
15yes). The 4- and 8-month responses were averaged to reflect
Early-life stress indicators. Twelve variables were chosen to caregiverexperienceofabuseduringtheinfant’sfirstyearoflife.
indexearly-lifestressbasedonpriorresearchindicatingthatinfants Caregiverparentingstresswasmeasuredusingthetotalscore
with prenatal drug exposure are more likely to experience these oftheParentingStressIndex(PSI;Abidin,1990)whentheinfant
stressors,andbasedonresearchwiththispopulationindicatingthat was4monthsold.ThePSIisa36-itemquestionnaire,scoredona
thesestressorsareassociatedwithprenataldrugexposureandpsy- 5-pointscale,administeredtothecaregiver.Itmeasuresparentdis-
chophysiological functioning (Conradt et al., 2013). These varia- tress,parent–childdysfunctionalinteraction,andthedifficultylevel
blesincludedthefollowing: ofthechild.
CaregiverpostnataltobaccousewasmeasuredusingtheCISU
Index of social position (ISP; Hollingshead, 1975). TheISP
(Shankaran et al., 1996) developed by the MLS. The caregiver
was calculated based on the formula provided by Hollingshead reportedthemeannumberofcigarettessmokedperday.TheCISU
(1975): Parental occupation and education were coded using a 7- was administered at the 4-month and8-month assessment. Scores
pointscale.Forparentaloccupation,thescalerangesfrom1(e.g., wereaveragedacrosstimepoints.
higher executives) to 7 (unskilled employees). For education, the Caregiver postnatal alcohol use was measured by caregiver
scale ranges from 1 (e.g., professional degree) to 7 (less than 7 report of the mean ounces the caregiver drank per day using the
yearsofschool).Iftherewasanothercontributingadultinthefam- CISU. Scores from the 4-month and 8-month assessment were
ily,thenISPwascalculatedbysummingtheaverageoftheprimary averaged.
caregiver and the contributing adult’s weighted education and Caregiverpostnatalmarijuanausewasmeasuredbythemean
occupation.TheISPwascalculatedbasedontheformula:(Occu- numberofjointsthecaregiverreportedsmokingperdayusingthe
pation x 7)1(education x 4; Hollingshead, 1975). The ISP was CISU. Scores from the 4-month and 8-month assessment were
reverse-scoredsothathighervaluesreflectedlowerISP. averaged.
Education.Adichotomousscore(15no,05yes)wascreated Caregiver postnatal cocaineuse was measured as the number
whentheinfantwas1montholdbasedonwhetherornotthepri- of days per week the caregiver reported using cocaine using the
marycaregiverhadatleastahighschooleducation. CISUat4and8months.Table1includesthepercentageofcare-
Poverty status. Poverty status was calculated when the infant giverswhoendorsedusingeachtypeofsubstanceatleastonceat
was1montholdusingthenumberofpersonslivinginthehouse- the4-or8-monthassessment.
hold andusing the Health andHuman Service Poverty guidelines
History of Child Protective Services (CPS) involvement.
for the year the assessment was conducted. A dichotomous score
CaregiverswereaskediftherewasareporttoCPSmadeonbehalf
(05no, 15yes) was created to indicate whether household
of the study child. Caregivers were interviewed by trained exam-
income wasless than$2,000/monthper householdmemberat the
iners about whether or not there had been any CPS involvement
dateoftheassessment.
sincethelastvisit,andifso,whetheritwasforsexualabuse,physi-
Caregiver symptoms of depression were assessed using the
calabuse,and/orneglect.Ifanyreporthadbeenmadeascoreof1
BeckDepressionInventory(BDI;Beck,Steer,&Brown,1996)at
wasgiven.Scoresat1,4,and8monthswereaveragedtogetherto
age4months(a5.88).TherangesfortheBDIscoreswere0–56
createthisvariable.
andthescorewasusedcontinuously.
Caregiverpsychologicaldistresswasmeasuredusingthemean Prenatal substance exposure. Dichotomousmeasuresarefre-
of total psychological symptoms from the Brief Symptom Inven- quentlyusedintestingprenatalsubstanceexposureeffects(Fisher
88 E.Conradt etal.
16 –.04 aria-less 0et,anlo.,)2p0r1e1n)a.taMllaytewrnaaslcroempoprut/tmede.cOonnieumposicnrtewenasofasdsriuggneudsefo(1r,eyaecsh;
ve
15 –.77***.04 statusandar sisubmstoarnecelikueselyd.tIofausweoamdadnitiuosneaslosnuebsstuabnscteasnc(eMwahyielteeptreagln.,an2t0,0s8h)e.
14 –.03.03–.07 conomicincome, Ftfaroollmslouwb0s–itn5agnfctohereemxwpoootrhskeurro-efrewFpiaossrhtmeerdeea(tsouarrl.ged(a2sa0sc1ha1r)osuwmmiatmthoagthtriaivspeshaiynm–dmpelxaes,rsapnsrgpenienacg--
13 –.02.06*.07*.08* Socioelower tfroormceotcryainceonofrirmopaitaiotenmofetparbeosluitmesp)tiuvesepoofsitciovceaimnee,coonpiiuamtess,cmreaernis-
12 –.36***–.03.06*.05–.01 ythmia.position, juanBae,haalcvoiohrold,yasnrdegtoublaacticoond.uTrihnegcporrergenlaatniocny.betweeninternalizing
h
11 52***40262 usarrsocial apn<d.0e0x1t.erWnaeliztihnegrefboerheavcoiomrbiwnaesd ipnotesritnivaleizianngdansdtroenxgt,ernra5liz.i7n7g,
–.0.2.0–..0.0 sinof behaviortoformalatent“behaviordysregulation”compositecom-
10 –.09**–.06.17***.04.03.04.07 espiratorywerindex pBcareirsheeagdviviooefrrseCwxhtheeercnnkalcliishztiilnd(gCreBnanCwdLe;irneAte3crnhyaeelnaizbrsiancoghld,b.e1Th9a9svc2io)o,rreasfdrfomomrineitxshtteeerrneCdahliiztldo-
**** ro
9 0**8**9**6**4464 5Aal ingandinternalizingbehaviorwereused.WeusedTscoresrather
678 0***–7*.12***–3***.13***.23***–7*.06*.12***.27*.11***.14***.102–.01.01.01.11***.42***.204.05.00.00***.09**.09**.04***.11***.10**.03–.07.03.0 ParentingStressIndex;RSsevariablesindicatehaving trslrtMhaieacmtantoiienso’redssesnisrnbwtanrcgewuohaherneDam,stnvhcaoosieortotraorvrbefeeesraroeyucbtlh/saheoeetcifdrovatefucetnohs1etitco1lrdou2wrsmeeeainpomtewavomereef-ersartectghhwheeeiidenlsdrptaeeprameresenneteso’r6tsstae,mgdbtnreeouiohnanerant,mvhcdsiseooo.sdmrmeaxpbeg.aywarCiihsnnaaegsrxtet/.gspcoihRovmipaelduewrs---
45 –.76***–.47***.46***–.30***.38***.2.10**.12***.0.09**.07*.1.08**.09**.0.09***.10***.0–.01.02–..00.06.0.02.03–..25***.28***.3.24***.31***.2–.13***–.12**.0 5otectiveServices;PSIthathigherlevelsofthe Weadtdlhixgaekapetpeetaorl3eyesacsuxthsytrai3oieelvmdayehbrrieesnaesan.vetyrwdeTmsw.ehpaedOienttnirohnfemfoecem-hpwrswiee,ielnnsadFrscyeriCeen(an6s1gPn4,Swai61Rnlh,ycS0(osa4e5Aesa60dser.)i6ldody5b%af-eatlva)ti4nwfa.dec4rhehi1aadesi,dnlnitddrpcercte5esnhasn(oerAe.t0waagNh4ngiiav,dtOehveasVernpmsodArRefiwssSwnb)saiAietirtnhrraetgedlvhfaemRedttawaoroSlueerAadg1ert
23 4***–5***.14***2***.13***0***.22***4.11***2***.049**–.014.042.040***–.041***.08**1–.021***.12***9**.10***4.04 5PSChildPre-scoredsuch ysimneegosarrbde,eaFlttiwak(ee1ael,tyn13t,c3oyh7eic9laod)rmrs5eaenn9fwd.r8oi4ftmho,upalnno5ddwt.weh0ra0itt2Sh.cEohWuSitledfearxcmetoneinrlwdineuaistlchitazesimdnmgitshesaeainnsdsguarimdenadteetarbanynwaaletlihyrzee--
correlations n1 1364–1363.47***–1344.31***.21052.18***.11051.17***.11076.27***.21259.06*.01259.17***.11259.13***.01259.11***.01259.08**.01380–.05.11388.16***.11047.01.01002.17***.11002.14***.0742.03.0 mptomInventory;Cincome)arerevers Ia1badSnn,er3ePtdw7n,o9fFepwo)eeu5i(nntn1hdc,5Cha1.nn2iP,lo36ddS6,rdw3epicn)fia5tf5hseweor.ie40utnh.2bt2c.em9aetWnw,sidspeiesne5wiannbligs.ti0hortoht4ohuee,utxatwcaanommegdmiiegiswesnhseietdno,dragfestdeamoebx.umi,orttocroheorgmlrstiaioketpeehd1lbiyacetytatdoweiaafhetfraee,3vnreFeycnehhca(aie1rldss-,
deviations,and MSD 227.829.940.340.450.420.448.698.630.600.5870.5117.420.080.226.148.650.220.620.060.280.030.170.160.331.891.380.120.7156.1210.6155.3210.365.641.29 5y;BSIBriefSyooleducation,and DTaebslceri2ptinivceluSdteastmisteiacnss,SDs,Ranesduclotsrrelationsamongallvariables.
Variablemeans,standardTable2. Variable 1.Socialposition(reverse-scored)2.Highschooleducation3.Povertystatus4.BDI5.BSI6.PSI7.Caregivervictimization8.Caregiverpostnataltobaccouse9.Caregiverpostnatalalcoholuse10.Caregiverpostnatalmarijuanause11.Caregiverpostnatalcocaineuse12.ChildCPSinvolvement13.Prenataldrugexposure14.1monthRSAreactivity15.Internalizingbehavior(age3)16.Externalizingbehavior(age3)17.RestingRSA(age3) 5.BDIBeckDepressionInventorNotebles(indexofsocialposition,highschlikelytohaveahighschooleducation.<<<*.05.**.01.***.001.ppp Tmmemstssscchtcytnaahrreoaahmrrteeeieettdossnceerpggessoearrgtii,.rnnlrovvaweCaasaemeetgtllneedrrhrisrsdesuivweylyspcwedsmcmoiasorrt.hatfthesprwiprToinooetttldhaoinongewvseemu,mgsievprsischestpsereohaeerocdowrvodsosrafsihufeiernnitadicrlrodigsaelaeevontcetltpoeapepoa,iarrodterhlceyliesnpnoooospos,swslnorsoCyirassfioeescnoPtairnlrhadntnaSboi,bii,tdveannmipucepottcgsswarlosnoymieysycprsemc.eecaoewhbPherwnsslieii,oiiiayjttkateuhtsamiwttrrevtanhrienlhepiecndeycaeamtasctovnet.asySoomoixylSnmrErpHmhrsegsEeSep,auipSrllltgvbaiieotahkeevostvsmnineetsamaotadrclrshrnyntisi,iheansca,lppaitbbgeeroabaanlvlnecrregeuheaeedstusrslawnn,ersehvprttaaaeiiieeatgbnnnneoenrndggdhyar-ft
RSAReactivityandLow-Socioeconomic Status 89
Table3. Exploratoryfactor analysissummary Preliminary Analyses
Given moderate-to-strong correlations between variables meas-
Postnatal
Caregiving Economic substance uringvariousformsofstressthechildexperiencedbetweenbirthto
Variable stress stress use 1year,weconductedexploratoryandconfirmatoryfactoranalyses
to determine whether variables could be grouped into dissociable
Indexofsocialposition .77
Highschooleducation .80 factors. Although the social position variable was comprised both
Povertystatus .61 ofincomeandeducation, we included two dichotomousvariables
Caregiversymptomsof .87 (povertystatusandeducation) becausetheymayidentifychildren
depression
inthe samplewho are atthe extremes oflow educationandpov-
Caregiverpsychological .88
distress erty.First,afterrandomlyselectinghalfofthesample,exploratory
Parentingstress .66 factor analysis (EFA) was conducted with an oblimin rotation on
Caregivervictimization .54 the12stressvariables.TheEFAproducedathree-factorsolution.
Caregiverpostnataltobaccouse .69
Associated eigenvalues accounted for 53.6% of the variance in
Caregiverpostnatalalcoholuse .70
Caregiverpostnatalmarijuana .55 variable scores (Table 3). Cross-validation on the second half of
use the sample was conducted using confirmatory factor analysis
Eigenvalue 2.65 1.44 1.27 (CFA).Thissuggestedexcellentstabilityofitemloading(seeFig-
%Varianceexplained 26.45 14.39 12.72
ure 1). The EFA and CFA revealed three factors, including (i) a
Note. Factor loadings with a weight of (cid:2).40 are reported; socioeco- “caregiving stress” factor, comprised of symptoms of depression,
nomic status variables (index of social position, high school education, psychiatric symptoms, parenting stress, and caregiver history of
andincome)arereverse-scoredsuchthathigherlevelsofthesevariables abuse;(ii)an“economicstress”factor,comprisedoftheISP,high
indicate having a lower index of social position, lower income,and are
schooleducation,andincomevariables;and(iii)a“drugexposure”
lesslikelytohaveahighschooleducation,n5512.
factor, comprised of caregiver postnatal use of alcohol, tobacco,
andmarijuana.ChildCPSinvolvementandpostnatalcocaineexpo-
sure did not load well on any one factor and were therefore
prenataldrugexposurewererelatedtoalowerindexofsocialposi- includedasindividualpredictorsinsubsequentmodels.
tion,acaregiverhavingreceivedlessthanahighschooleducation, We controlled for False Discovery among the eight tests of
lowerincome,acaregiverhistoryofabuse,andcaregiverpostnatal interaction using the Benjamini and Hochberg (1995) procedure.
substance use. These children were more likely to have an open Thismethodwasusedtodeterminethepercentageoffindingsthat
CPScase.Greaterinternalizingandexternalizingbehavioratage3 couldbeafalsediscovery.Insteadofacorrectedpvalue,aqvalue
yearswasassociatedwithlowerSESasindexedbytheISP,parent isobtained,whichrepresentstheproportionoftestsbelow,which
education, and income. It was also related to greater caregiver- arefalsepositives.Wechoseaqvalueof.10.IntheResultssec-
reportedpsychologicaldistress,asindexedbysymptomsofdepres- tion,wepresentboththepvalueandqvalues.
sion, psychiatric symptoms, and parenting stress. These children
werealsomorelikelytobeprenatallydrugexposed.Greaterrest-
Covariates
ingRSAatage3yearswasrelatedtofewercaregiversymptomsof
depression,fewercaregiverpsychiatricsymptoms,andgreaterpre- Covariates tested included birth weight, race, site, and sex. Birth
natalsubstanceexposure. weight was not related to RSA at age 1 month, age 3 years, or to
Figure1.Confirmatoryfactoranalysisofstressorsexperiencedduringthefirstyearoflife.Pathsarestandardizedbetacoefficients.v2(39)5133.59,
p<.001;Comparativefitindex(CFI)5.96;Standardizedrootmeansquareresidual(SMSR)5.04,n5694,***p<.001.
90 E.Conradt etal.
Table 4. Unstandardized parameter estimates and standard and CPS involvement experienced between birth and 1 year pre-
errors for predicting behavior dysregulation and baseline respi- dictedgreaterbehaviordysregulationatage3years.Therewasno
ratorysinus arrhythmia(RSA) at age 3years maineffectofRSAreactivityatage1monthonbehaviordysregu-
lation at age 3 years, although RSA reactivity did interact with
RestingRSAin caregiving stress to predict behavior dysregulation (Figure 2a). To
Behavior African clarify the nature of this interaction, we examined RSA reactivity
Dysregulation Americans
andcaregivingstressat1SDaboveandbelowthemeanusingonline
(n5827) (n5802)
computational tools provided by Preacher, Current, and Bauer
Predictor B SE B SE
(2006) (http://www.quantpsy.org/interact/mlr2.htm; Preacher). On
Site — — .08** .03 average,therewerenosignificantassociationsbetweenRSAreactiv-
Race 22.10** .77 — — ityat1monthandbehaviordysregulationatage3,norwastherea
Sex — — 0.18 0.12
significantassociationbetweenRSAreactivityandbehaviordysre-
Economicstressfactor 10.12 6.35 21.70 1.52
gulationamonginfantswithlowlevelsofcaregivingstressexposure.
Caregivingstressfactor 36.77*** 7.23 22.19* 1.08
Postnatalsubstance 20.33 15.61 27.68* 3.74 However,amonginfantswithhighlevelsofcaregivingstressexpo-
exposurefactor sure,greaterRSAwithdrawalwasrelatedtoelevatedsymptomsof
ChildProtective 5.24*** 1.33 20.22 0.20 behaviordysregulation.
Servicesinvolvement
Prenataldrugexposure –.24 0.35 0.03 0.05
Postnatalcocaineexposure 22.31 2.68 0.09 0.35 Resting RSA at age 3 years.1 We repeated the analyses
RSAreactivityat1month 20.48 0.47 0.17 0.09 describedabovewithrestingRSAasouroutcome.Whenracewas
RSAReactivity3 217.86** 7.07 22.37* 1.18 includedinthemodels,therewasamaineffectofcaregivingstress
Caregivingstress
on resting RSA at 3 years, with greater caregiving stress experi-
Note. Standard error and parameter estimates come from a structural encedfrombirthto1yearbeingassociatedwithlowerrestingRSA
equationmodel. at3years(b522.01,p5.04,q5.03).However,thismaineffect
*p<.05.**p<.01.***p<.001. wasqualifiedbyasignificantCaregivingStress3RSAReactivity
3 Race interaction. As shown in Table 4, among African Ameri-
internalizingorexternalizingbehavior,allps>.32.Sexwasrelated cans only, greater postnatal drug exposure and greater caregiving
torestingRSAatage3years,withfemalesexhibitinggreaterresting stressexperiencedbetweenbirthandage1yearwasrelatedtolower
RSA than males, F (1, 734)54.67, p5.03. A one-way ANOVA resting RSA at age 3 years. This main effect of caregiving stress,
however,wasqualifiedbyasignificantinteractionbetweencaregiv-
revealedsitedifferencesinRSAreactivityatage1month,withnew-
ingstressandRSAreactivityatage1month(Figure2b).Respira-
bornsinProvidenceexhibitinggreaterRSAreactivitythannewborns
torysinusarrhythmiaandcaregivingstresswereagainprobedat1
inDetroit.Therewerealsositedifferencesininternalizingandexter-
SD above and below the mean. Among children who experienced
nalizing behavior, with preschoolers in Detroit exhibiting signifi-
highlevelsofcaregiverstress,therewasnorelationbetweenRSA
cantly higher internalizing and externalizing behavior compared to
reactivityat 1monthand restingRSA at 3years. However,lower
preschoolers in Miami and Providence, and preschoolers in Mem-
levels of RSA reactivity at 1 month were related to higher resting
phisexhibitingsignificantlyhigherexternalizingbehaviorthanpre-
RSAat3years,butonlyamongchildrenwhoexperiencedlowlev-
schoolersinMiami.TherewasnomaineffectofsiteonrestingRSA
els of caregiver stress. There were no significant interactions
at3years,butwhenincludedinfullmodels,significantsiteeffects
between RSA reactivity at 1 month and the other stress variables
emergedforAfricanAmericans.Wethereforeincludesiteasacova-
(economic stress, postnatal drug exposure, or child CPS involve-
riateinmodelspredictingrestingRSAat3years.Racewasrelated
ment).Thesesamemodelsweretestedwithnon–AfricanAmericans
tointernalizingbehavior,withAfricanAmericansexhibitinggreater
only.Nosignificantmaineffectsorinteractionswerefound.
internalizing behavior compared to Caucasians. There was a main
effect of race on resting RSA at 3 years, with African Americans
Discussion
exhibitingsignificantlyhigherrestingRSAthannon–AfricanAmeri-
cans, F (1, 733)522.03, p<.001. We therefore included site and WeexaminedeffectsofSESandassociatedstressors,andStress3
race(dichotomizedasAfricanAmericanvs.non–AfricanAmerican) RSAReactivityinteractionsduringthefirstyearoflifetoidentify
as a covariate in all models. Given that children with prenatal predictors of behavior dysregulation and resting RSA at age 3
cocaineexposurewereoversampled,wealsoincludedprenatalsub- years.Ourfindingshighlighttheimportanceofstudyinghowstres-
stanceexposureasacovariateinallanalyses. sorsassociatedwithlowSEScanshedlightonhowindividualdif-
ferences in physiological reactivity associate with behavioral and
StructuralEquation Models physiological outcomes. Our factor analytic approach revealed
threedissociable,ordistinguishable,early-lifestressfactors,oneof
Behaviordysregulationat3years.Predictorsofbehaviordysre- whichinteractedwithRSAreactivitytopredictbehaviordysregu-
gulation(latentvariablecomprisedofinternalizingandexternaliz- lation in the sample as a whole, and resting RSA among African
ing behavior) included site, race, caregiving stress, economic Americans.Thefalsediscoveryrateswerelow,indicatingthatour
stress,postnataldrugusestress,CPSinvolvement,andRSAreac- results likely represent true discoveries. Below we speculate on
tivityat1month.InteractionsbetweenRSAreactivityat1month
and our four stress variables (economic stress, caregiving stress, 1. There was a significant positive correlation between resting RSA
postnatal drugexposure, andchild CPS involvement) wererun in at1monthandrestingRSAat3years(r5.10,p5.02,n5575).Rest-
ing RSAat 1 monthis not includedas a predictoror potential modera-
separatemodels.Weonlyincludemodelswithasignificantinter-
tor in our analyses as our interest was in how stress reactivity may
actionterm,butoutputfromothermodelsisavailablefromthefirst
interact with environmental conditions to predict behavior and physio-
authoruponrequest.AsshowninTable4,greatercaregivingstress logicaloutcomes,perallostaticloadandACMtheories.
RSAReactivityandLow-Socioeconomic Status 91
Figure2.Respiratorysinusarrhythmia(RSA)reactivityatonemonth3caregivingstressexposure(birth–1year)predictsbehaviordysregulationat
age3,(n5827)(a),andrestingRSAat3yearsinAfricanAmericans(n5802)(b).Simpleslopesweretestedat61SDaboveandbelowthemean
ofRSAreactivityandcaregivingstress.
potentialmechanismsthatmayunderlietheseeffects,andbroaden stress is more proximal than economic stress or postnatal drug
discussionoftheimportanceoftestingcurrenttheoriesofphysiol- exposure,theeffectsofwhichmaynotemergeuntillaterinlife
ogy–behaviorrelationsamongpopulationswhoareheterogeneous (Shonkoff, Boyce, & McEwen, 2009). Furthermore, we may
vis-(cid:2)a-visSES. have hit a floor effect with our economic stress factor, given
First,inthisarticleweexpandontheearly-lifestressliterature that the majority of children in our sample were raised in low-
bystudyinghowmultipletypesofstressorsexperiencedduringthe SES environments. Given that all three factors were signifi-
firstyearoflifeaffectphysiology–behaviorrelations.Threedisso- cantly and positively correlated, however, economic and post-
ciable factors emerged from both EFA and CFA approaches: an natal substance exposure may have exerted an indirect effect
economic stress factor, a caregiving stress factor, and a post- through caregiving stress to predict outcomes, a possibility to
natal drug exposure factor. The caregiving stress factor inter- beexploredinfuturestudies.
actedconsistentlywithRSAreactivityatage1monthtopredict Our results extend prior research by demonstrating that RSA
problem behavior and resting RSA at age 3 years. There is a reactivityat1monthoflifepredictsbehaviordysregulationatage
largeliteraturesupportingthepremisethatcaregiversaffectand 3,butonlyamonginfantswithexposuretohighlevelsofcaregiv-
areaffectedbyinfantresponsestostressduringthefirstyearof ingstress.Theseresultssuggestthatinfantswhoaremorereactive
life (Conradt & Ablow, 2010; Moore & Calkins, 2004). It is atage1monthmaybemoresensitivetoanenvironmentcharacter-
therefore less surprising that the caregiving factor was more izedbycaregiverdepression,psychologicaldistress,andparenting
closelyassociatedwithinfantphysiologicalfunctionat1month stress.Whenconfrontedbymaternalunavailability,achild’sauto-
than the other factors (Propper, 2013). Exposure to caregiving nomic reactivity may be coupled with increased behavioral
92 E.Conradt etal.
reactivity/frustration, which is adaptive in this context because it forAfricanAmericans.Therewerenosignificantdifferencesincare-
signals to the caregiver the child’s need for attention. Over time, givingstressexposurebetweenAfricanAmericansandnon–African
however, heightened behavioral and physiological reactivity may Americansinthissample,norweretheredifferencesinRSAreactiv-
downregulate the stress response system, thereby reducing the ityat1month.Differencesinthedevelopmentaltrajectoryhavebeen
child’ssensitivitytonegativeenvironments,whichmayinturnpro- found between African Americans and European Americans, with
motedisruptivebehavior(seeBeauchaineetal.,2011;DelGiudice African Americans exhibiting greater baseline RSA at age 8
etal.,2011).Ourfindingsarealsoinsupportofbiologicalsensitiv- (El-Sheikh,Hinnant,&Erath,2011),thatremainedstableacrossmid-
ity to context theory (Boyce & Ellis, 2005). The most reactive dle childhood (Hinnant, Elmore-Staton, & El-Sheikh, 2010). Given
infantsappearedtobetheoneswhoweremoresensitivetocaregiv- thatdifferencesinRSAemergedbetween1monthand3yearsinthis
ingstress,giventhatcaregivingstresswasrelatedtobehaviordys- sample,theremaybeanunexploredthirdvariablethataccountsfor
regulation among these infants, but not among infants who were differencesintheautonomicnervoussystembetweenracialgroups,
lessreactive.Thisworkalsosupportscurrenttheorizingthatstress suchasparentalexperienceofstereotypethreatorperceivedracism
experiencedearlyinlifemayaffectphysiologicalsystemsinvolved (Lepore et al., 2006). Alternatively, we may have had increased
in self-regulation, given that high-reactive infants exhibited more powertodetectthismoderationeffect,giventhatAfricanAmericans
behavior dysregulation (indicative of poor self-regulation), but representedthemajorityofthissample.
onlyifcaregivingstressexposurewashigh(Evans&Kim,2013). These results also support a fetal programming model, which
These results are important because they suggest that we may be helpstoexplainwhyaninfantwouldexhibithighRSAreactivity,a
abletoidentifywhichchildrenaremoresensitivetoenvironmental presumed risk factor for adverse behavioral and physical health
adversitybyage1month. outcomes.Inbrief,theconceptofprogrammingisbasedonepide-
We then examined whether high-reactive infants may exhibit miological studies suggesting that an adverse fetal environment
lowrestingRSAatage3,givencurrenttheorizingthatchronicacti- resulting in low birth weight in term infants was associated with
vation of the stress response system may manifest in changes to the development many decades later of adult cardiovascular and
baselinephysiology,presumablythroughloweredrestingRSA(El- metabolicdisorders(Barker,1998;Barker&Osmund,1986).This
Sheikh & Hinnant, 2011). Across numerous samples spanning was attributed to fetal adjustments to cues from the intrauterine
developmentalepochsfrominfancytoadulthood,highrestingRSA environment(programming)thatincreaseddiseasesusceptibilityin
isassociatedwithpositivementalhealthoutcomes,includingbetter adulthood (Entringer, Buss, & Wadhwa, 2010; Sandman, 2015).
self and emotion regulation, greater social competence, and Infantswhoweremorereactivemayhavebeen“preparing,”based
empathicrespondingtootherswhoareindistress(seeBeauchaine, on pregnancy conditions such as prenatal drug exposure, to enter
2001,2015).Wefoundasignificantinteractionbetweencaregiving intoamoreunpredictable,stressfulpostnatalenvironment.Prenatal
stressexposureandRSAreactivityat1month,butonlyforAfrican stress exposure may also impair prefrontal cortex development
Americans. Among African Americans, infants who were more (Kishiyamaetal.,2008)whichisknowntoexertdownstreamcon-
physiologicallyreactiveat1monthhadthelowestlevelsofresting sequences on RSA reactivity (Beauchaine, 2015). Postnatal pro-
RSA,regardlessoftheirlevelofcaregivingstressexposure.How- gramming by insensitive or unresponsive caregiving behavior
ever,childrenwithlessRSAreactivityatage1monthhadthehigh- couldinturnaffectprefrontalcortexdevelopmentandstressphysi-
est resting RSA if raised in contexts of low caregiving stress ology (Meaney, Szyf, & Seckl, 2007). This heightened reactivity
exposure,butlowrestingRSAifraisedincontextsofhighcaregiv- maybeadaptiveinthissettingasitfacilitatesattunementandsen-
ing stress exposure. These results were surprising. We expected, sitivity to changes in the environment (Boyce & Ellis, 2005;
basedontheoryandpriorwork(El-Sheikh&Hinnant,2011),that Sandman, 2015). By age 3, however, increased reactivity may
greater RSA reactivity in infancy combined with greater stress comeatacost,asinfantswiththegreatestRSAreactivityhadthe
exposure would predict lower resting RSA. However, our results highest behavior dysregulation, and lowest resting RSA if also
are not incongruent with current theory. This finding supports the raisedinenvironmentsofhighcaregivingstress.
allostatic load model as it suggests that increased RSA reactivity,
presumablyexperiencedduringthefirst3yearsoflife,comesata
Implications
“cost”intheformoflowerrestingRSAatage3,apossiblevulner-
ability for poor social competence and emotion dysregulation Our results highlight the importance of examining low SES and
(Beauchaine,2001,2015;Beauchaineetal.,2007).Inotherwords, associated stressors in psychophysiological research, as what we
lower resting RSA among infants with greater caregiving stress knowaboutpsychophysiologicalprocessesintypicallydeveloping
exposuremaybearesultofdownregulationofthestressresponse childrenmaynotnecessarilyapplyamonglow-incomepopulations.
system (El-Sheikh & Hinnant, 2011; McEwen & Stellar, 1993). Inthepast,particularlyinresearchonprenatalsubstanceexposure,
ThehighestrestingRSAwasobservedamonglessreactiveinfants, SESwasviewedasaconfoundthatneededtobecontrolledforin
butonlyiftheyexperiencedlowerlevelsofcaregivingstress.These ordertotestdirecteffectsofasubstanceonbehavioralandphysio-
resultsaremoreconsistentwithwhatisfoundintheliteraturewith logical outcomes. More recently, research suggests that prenatal
typicallydevelopingchildren.Ifstressphysiologysystemsarenot substanceexposuremaybemoreofamarkerofthequalityofthe
beingused chronically,asexpected among infantsraisedbycare- postnatal environment (Fisher et al., 2011), and that meaningful
givers who are less stressed and without psychopathology, then relations between SES and physiological outcomes are obscured
restingRSAshouldbehighercomparedtoinfantswithhighcare- whenSESisignored(Conradtetal.,2013;Fisheretal.,2011).For
givingstressexposure,whichsuggestsincreasedsocialcompetence example,althoughtherewasamaineffectofcaregivingstresson
andemotionregulation(Beauchaine,2001,2015;Beauchaineetal., physiologicalandbehavioraloutcomes,thiseffectwasqualifiedby
2007). Less caregiving stress exposure may therefore be concep- asignificantinteractionbetweencaregivingstressandRSAreactiv-
tualizedasprotectiveinthisgroupofinfants. ity.Thus,thisresearchsuggeststhateffectsofstressorsassociated
It is unclear why the interactive effects of caregiving stress and with low-SES environments on behavior dysregulation may be
RSA reactivity at 1 month were found to predict resting RSA only magnified among children with high RSA reactivity, whereas