Enduring effect of childhood maltreatment on cortisol and heart rate responses to stress: The moderating role of severity of experiences

Abstract

There is a relative consensus about the detrimental impact of childhood maltreatment on later mental health problems and behavioral difficulties. Prior research suggests that neurophysiological stress mechanisms may partly mediate this association. However, inconsistent findings regarding hypothalamic-pituitary-adrenal axis and sympathetic responses to stress complicate this investigation. Furthermore, the concordance in these two stress systems is not well understood. We tested whether the severity of maltreatment affected the association between maltreatment and cortisol and heart rate (HR) stress responses and the symmetry of these responses. Participants were 155 males (56 maltreated and 99 controls) aged 18 to 35 years. Cortisol and HR were measured in response to the Trier Social Stress Test. Childhood maltreatment, sociodemographic factors, and health-related factors were measured using self-reported questionnaires. Maltreated participants had higher cortisol responses to stress in comparison to controls. However, a shift from moderate to lower to higher cortisol responses was noted as the severity of the experiences increased. Participants exposed to more experiences of maltreatment also showed a greater symmetry between cortisol and HR stress responses. Our findings provide further support for persistent dysregulation of the HPA axis following childhood maltreatment, of which the expression and symmetry with the sympathetic system may change according to the severity of experiences.

Full text

Enduring effect of childhood maltreatment on cortisol and heart
rate responses to stress: The moderating role of severity
of experiences
ISABELLE OUELLET-MORIN,
a,b,c
MARIE-PIER ROBITAILLE,
a
STE
´PHANIE LANGEVIN,
a
CHRISTINA CANTAVE,
a
MARA BRENDGEN,
c,d
AND SONIA J. LUPIEN
a,b
aUniversity of Montreal; bResearch Center of the Montreal Mental Health University Institute; cUniversity of Quebec at Montreal;
and dSainte-Justine Hospital Research Center
Abstract
There is a relative consensusabout the detrimental impact of childhood maltreatment on later mental health problems and behavioral difficulties. Prior research
suggests that neurophysiological stress mechanisms may partly mediate this association. However, inconsistent findings regarding hypothalamic-pituitary-
adrenal axis and sympathetic responses to stress complicate this investigation. Furthermore, the concordance in these two stress systems is not well understood.
We tested whether the severity of maltreatment affected the association between maltreatment and cortisol and heart rate (HR) stress responses and the
symmetry of these responses. Participants were 155 males (56 maltreated and 99 controls) aged 18 to 35 years. Cortisol and HR were measured in response to
the Trier Social Stress Test. Childhood maltreatment, sociodemographic factors, and health-related factors were measured using self-reported questionnaires.
Maltreated participants had higher cortisol responses to stress in comparison to controls. However, a shift from moderate to lower to higher cortisol responses
was noted as the severity of the experiences increased. Participants exposed to more experiences of maltreatment also showed a greater symmetry between
cortisol and HR stress responses. Our findings provide further support for persistent dysregulation of the HPA axis following childhood maltreatment, of which
the expression and symmetry with the sympathetic system may change according to the severity of experiences.
A relative consensus exists regarding the consequences of
childhood maltreatment on emotional, behavioral, and social
functioning during childhood and adolescence (Ferrara et al.,
2016; Hunt, Slack, & Berger, 2016). Longitudinal studies
have also shown that the negative impact of maltreatment
may persist into adulthood and affect multiple domains of
life, such as physical and mental health, intimate relation-
ships, employment, and criminal offending (Herrenkohl,
Hong, Klika, Herrenkohl, & Russo, 2013; Mersky & Topit-
zes, 2010; Smith, Ireland, & Thornberry, 2005). Embracing
a developmental psychopathology framework could help to
understand the negative (and potentially positive) adaptations
unfolding over time (Toth & Cicchetti, 2013). While longitu-
dinal study designs for which measures of functioning and
hypothesized causal factors have been collected prospec-
tively remain ideally positioned to make a contribution to
the field, additional objectives are pursued. Among them,
the identification of the pathways by which maltreatment jeo-
pardizes health and behavioral functioning, through the
adoption of multiple levels of analysis and a transactional ap-
proach for which the biological, emotional, and psychologi-
cal processes transcend divisions between normality and ab-
normality (Beauchaine & McNulty, 2013; Cicchetti, 2016).
To date, though, the mechanisms underlying the long-lasting
impact of maltreatment on functioning remain elusive, and
are often examined in isolation and according to artificially
truncated sources of influences.
The hypothalamic–pituitary–adrenal (HPA) axis and the
sympathetic nervous system (SNS) are hypothesized to play
a central role in the association between early adversity and
health (Doom & Gunnar, 2013; Lupien, McEwen, Gunnar,
& Heim, 2009). While a flattened pattern of diurnal cortisol
secretion has been reported in maltreated children with
some consistency (Bernard, Frost, Bennett, & Lindhiem,
2017; Cicchetti, Rogosch, Gunnar, & Toth, 2010; Power,
Thomas, Li, & Hertzman, 2012), both lower (Bernard
et al., 2017; Bruce, Fisher, Pears, & Levine, 2009;Power
et al., 2012) and higher (Bruce et al., 2009; Bugental, Martorell,
& Barraza, 2003; Engert, Efanov, Dedovic, Dagher, &
Pruessner, 2011; Fries, Shirtcliff, & Pollak, 2008; Saridjan
Address correspondence and reprint requests to: Isabelle Ouellet-Morin,
School of Criminology, University of Montreal, Research Center of the Mon-
treal Mental Health University Institute and the Research Group on Child
Maladjustment, C.P. 6128, succursale Centre-ville, Montre
´al QC, H3C
3J7, Canada; E-mail: isabelle.ouellet-morin@umontreal.ca.
We are grateful to the participants who have given their time to take part in
this study. The data presented in this manuscript have been funded by the
HF Guggenheim Foundation. Isabelle Ouellet-Morin is Canada Research
Chair in the Developmental Origins of Vulnerability and Resilience, and Ste
´-
phanie Langevin is supported by the Fonds de recherche du Que
´bec–Socie
´te
´
et Culture. Mara Brendgen wassupported by the Fonds de Recherche du Que
´-
bec-Sante
´, and Sonia J. Lupien is a Canada Research Chair in Human Stress.
Development and Psychopathology 31 (2019), 497–508
#Cambridge University Press 2018
doi:10.1017/S0954579418000123
497

et al., 2010) basal cortisol levels are noted. Inconsistent find-
ings have also been reported regarding the directionality of
the association between maltreatment and cortisol responses
to psychosocial stress. Adolescents and adults who had
been maltreated as children showed either higher (Harkness,
Stewart, & Wynne-Edwards, 2011;Heimetal.,2000;Sullivan,
Bennett, & Lewis, 2013), no difference (Hagan, Roubinov,
Mistler, & Luecken, 2014; Suzuki, Poon, Papadopoulos,
Kumari, & Cleare, 2014) or lower cortisol responses to stress
than controls (Carpenter et al., 2007; Carpenter, Shattuck,
Tyrka, Geracioti, & Price, 2011; Cook, Chaplin, Sinha, Tebes,
& Mayes, 2012; Elzinga et al., 2008; Lovallo, Farag, Sorocco,
Cohoon, & Vincent, 2012;MacMillanetal.,2009; Ouellet-
Morin et al., 2011; Peckins, Dockray, Eckenrode, Heaton, &
Susman, 2012; Trickett, Gordis, Peckins, & Susman, 2014;
Voellmin et al., 2015). Mixed findings also exist in regard to
the SNS response to stress (Cook et al., 2012;DeBellis,Lefter,
Trickett, & Putnam, 1994; Gordis, Feres, Olezeski, Rabkin, &
Trickett, 2010;MacMillanetal.,2009;Voellminetal.,2015).
A common source of inconsistency among studies examin-
ing the association between maltreatment and these stress
response systems is the selected methodology. Besides the
confounding effects of factors, such as the time of day,
medications, and current symptomatology, another, more con-
cealed source of discrepancy may lie in the measure of
maltreatment. Most studies relied on data collected in partici-
pants drawn from the general population, including indi-
viduals who were maltreated (with or without official records)
and others who were not. Without the necessary precautions
(e.g., overrepresentation of participants who report maltreat-
ment), this strategy may reduce the heterogeneity of the mal-
treatment experiences captured in these samples, in terms of
frequency and severity. Moreover, the use of a dichotomous
index of maltreatment (presence vs. absence) may be prob-
lematic if the association with the stress response systems
changes direction (i.e., is not linear) as maltreatment becomes
more severe. The presence of a point of inflexion, a shift, in
cortisol response to stress along the continuum of maltreat-
ment severity echoes in part the stress inoculation model,
which proposes that moderate stress dampens cortisol re-
sponse to future stress (Parker, Buckmaster, Schatzberg, &
Lyons, 2004). However, exposure to more severe stress may
not be “inoculating” per se, but could sensitize the HPA
axis to subsequent stress (Obradovic, 2012). Consequently,
the restricted range of maltreatment captured in some studies,
because of the participants’ selection procedures or due to
how maltreatment was measured or analyzed, may not ade-
quately depict the association between maltreatment and the
stress response systems. Further tests are warranted.
The impact of these methodological concerns depends,
among other things, on whether or not the association linking
maltreatment and the stress response systems is expected to be
linear. If maltreatment is linearly associated with cortisol (i.e.,
lower or higher cortisol response as maltreatment severity in-
creases), the constrained range of maltreatment experiences
or the use of a dichotomous index bear no (or fewer) conse-
quences in understanding this association. In contrast, if a
shift in the physiological stress response exists somewhere
along the maltreatment distribution, only a partial representa-
tion of the maltreatment–cortisol association would be
revealed. Such a possibility cannot be easily assessed from
existing studies. For example, higher levels of adverse child-
hood experiences (ACEs) were associated with lower cortisol
responses to stress in a sample of young women (Voellmin
et al., 2015). However, it is not clear whether, in a sample
of participants who reported an average of 2.8 ACEs, those
who reported the highest level of adversity (i.e., 4 or more
ACEs) were confronted by moderate or higher levels of ad-
versity so that lower or higher patterns of cortisol response
could be present along the ACE distribution. As both lower
and higher cortisol responses to stress have been reported
following maltreatment, a closer look at the directionality of
this association, according to the severity of maltreatment ex-
periences, is warranted.
Another source of inconsistency may be that studies gen-
erally examine one stress response system at a time, preclud-
ing a more systematic, integrated view of how maltreatment
may have long-lasting effects on these systems (Bauer,
Quas, & Boyce, 2002). The locus coeruleus-norepinephr-
ine/SNS and the HPA axis do not always present symmetrical
(lagged) responses to stress (Allwood, Handwerger, Kiv-
lighan, Granger, & Stroud, 2011; Bae et al., 2015; Cook
et al., 2012; El-Sheikh, Erath, Buckhalt, Granger, & Mize,
2008; Gordis, Granger, Susman, & Trickett, 2006; van Goo-
zen et al., 1998). Moreover, despite their neural connections,
these stress systems have distinct secretion time course, ef-
fects on targeted tissues, and regulatory mechanisms (Sa-
polsky, Romero, & Munck, 2000). Important individual
variability in the HPA axis and SNS responses to stress
have been reported (Kudielka, Hellhammer, & Wust,
2009), so that while some individuals show marked responses
in both systems when confronted by stress, only one stress
system may be activated in others (Bauer et al., 2002). Ac-
cording to the biological sensitivity to context model (Boyce
& Ellis, 2005), genetically and environmentally mediating
factors have the potential to calibrate the stress systems. It
is thus possible that the specific genetic and environmental
etiology of the HPA axis and SNS may prompt asymmetric
responses to stress. On a related point, the biological sensitiv-
ity to context model underlines how the integrated actions and
connections of the stress systems should be understood in
their ecological contexts, past or present (Ellis & Boyce,
2008). However, the possibility that the symmetry of the
HPA and SNS responses to stress vary according to childhood
maltreatment has rarely been investigated (for an exception,
see Gordis, Granger, Susman, & Trickett, 2008). In summary,
the restricted range of maltreatment captured in some studies,
the overlook of potential nonlinear association between these
constructs as well as the omission of testing the possibility
that maltreatment severity affects the symmetry of HPA and
SNS responses to stress, may obscure how they jointly affect
later vulnerability to psychopathology.
I. Ouellet-Morin et al.498

The present study had three objectives. We examined
whether young adults exposed to childhood maltreatment,
as defined using the standardized Childhood Trauma Ques-
tionnaire (CTQ) guidelines (Bernstein & Fink, 1998), had a
disrupted pattern of stress responses in comparison to those
who did not reach that threshold, using cortisol and heart
rate (HR) as markers of HPA axis and SNS reactivity to stress.
This dichotomous index of maltreatment experiences, how-
ever, would not allow uncovering the nonlinear patterns of as-
sociations, if present. To this end, we investigated if the cor-
tisol and HR responses to stress varied according to
maltreatment severity. Here, we operationalized maltreatment
experiences so that individual variation within the CTQ-
based nonmaltreated participants could be depicted along
with their differential patterns of associations with the stress
response systems. Finally, we explored whether the symmetry
between cortisol and HR responses to stress also varied as a
function of maltreatment severity.
Method
Sample
Because the study’s general objective was to understand the
biosocial roots of general aggression, including verbal and
physical aggression, and that these behaviors are manifested
more frequently by men than by women (Archer, 2004),
the sample only comprised men. Moreover, uncertainty
remains about the existence of sex differences in cortisol
response to stress (Carpenter et al., 2009; Kudielka, Buske-
Kirschbaum, Hellhammer, & Kirschbaum, 2004) and regard-
ing the maltreatment-cortisol associations (Carpenter et al.,
2009; Negriff, Saxbe, & Trickett, 2015). Because we could
not reach the statistical power required to adequately test these
possible sexually dimorphic associations, only men were
initially investigated. Participants were recruited using ads
posted online and on public billboards inviting them to
participate in a study about early life experiences. Trained
research assistants conducted a phone interview with inter-
ested individuals, screening for health and about experi-
ences of childhood maltreatment using the short form of
the CTQ (Bernstein & Fink, 1998). The sample included
155 participants aged from 18 to 35 years (M¼24.10,
SD ¼3.70).
Procedure
We invited the participants to take part in our study, lasting
about 3 hr 30 min. During that time, the participants took
part in the Trier Social Stress Test (TSST), a well-established,
standardized stress paradigm that induces social–evaluative
threat by subjecting participants to a 5-min mock job inter-
view in front of a “panel of behavioral experts,” and followed
by 5 min of mental arithmetic. Participants communicated
with the panel using an intercom and were filmed with avideo
camera in a stand-up position in front of a one-way window
(Andrews et al., 2007). Both the “panel-in” and “panel-out”
methods have been shown to elicit reliable cortisol responses
in laboratory settings (Andrews et al., 2007). The TSST took
place in the early afternoon for all participants (M¼13:41,
SD ¼0:53). Ethical approval was granted by the Research
Center of the Montreal Mental Health University Institute
Ethics Committee (Montre
´al, Canada).
Measures
CTQ-SF. The CTQ-SF inquiries information about emo-
tional, physical, and sexual abuse and neglect that have
occurred before age 18 and have been selected because of
its demonstrated validity in community samples (Bernstein
et al., 2003). Participants responded to each of the 28 items
in the context of “when you were growing up” and answered
according to a 5-point Likert scale ranging from 1 ¼never
true to 5 ¼very often true, leading to total scores of 5 to
25 on each subscale (plus 3 items of validity). The CTQ-
SF included items such as “People in my family said hurtful
or insulting things to me” (emotional abuse) and “I was pun-
ished with a belt, a board, a cord, or some other hard object”
(physical abuse). To test the first objective of the study, we
identified 56 men (35.9%) who reported experiences suggest-
ing the occurrence of at least one type of maltreatment (i.e.,
CTQ-based maltreatment) using the manual’s recommended
classification scores (Bernstein & Fink, 1998). The experi-
ences of the remaining participants (n¼99; controls) did
not reach that threshold (i.e., CTQ-based nonmaltreatment).
Being identified as positive for a category corresponds with
endorsing a number of experiences as “often true.” The
CTQ has good internal consistency and criterion validity in
clinical and community samples and convergent reliability
with clinical assessments of abuse is high (Bernstein et al.,
2003). Acceptable internal consistency was also found in
this sample (Cronbach a¼0.78). To test the second objective
of the study, we calculated the total scale of maltreatment by
summing up all 25 items, as an index of maltreatment severity
(total sample: M¼37.43, SD ¼11.04), and derived three
equal groups of participants who reported increasing levels
of maltreatment experiences, thereafter referred to as no
(few) maltreatment experiences (CTQ total score 31);
some experiences of maltreatment (CTQ total score 32–40);
and more experiences of maltreatment (CTQ total score 
41). The groups based on the CTQ’s guidelines for maltreat-
ment, M¼30.85, SD ¼3.96 and M¼49.18, SD ¼9.81, re-
spectively; F(1, 154) ¼271.15, p,.001, as well as the
groups derived according to the total CTQ score, significantly
differed in the levels of maltreatment reported, M¼28.12, SD
¼2.00, M¼34.91, SD ¼2.63, and M¼50.78, SD ¼9.07,
respectively; F(2, 153) ¼239.02, p,.001, with post hoc
analyses showed significant differences between each group
(ps,.001).
Stress biomarkers. Cortisol was measured through the collec-
tion of five saliva samples via passive drool. The first two
Maltreatment seerity and stress response 499

samples were collected 2 and 20 min before the TSST. The
third, fourth, and fifth samples were collected 15, 25, and
35 min after the beginning of the TSST. Saliva samples
were stored in a –20 8C freezer and analyzed in a single
batch with a high sensitivity enzyme immune assay kit (Sali-
metrics State College, PA, Catalogue No. 1-3102). The range
of detection for this assay is between 0.012 and 3 ug/dl and
the intra- and interassay coefficients of variation were 4.1%
and 8.3%, respectively. All samples were assayed in dupli-
cates, Winsorized, and log-transformed prior to statistical
analyses.
HR was measured using an Omron 7 Series Plus BP765
Automatic Blood Pressure Monitor, which records blood
pressures in a noninvasive manner using a cuff placed on
the upper arm. HR was measured, at a 2-min interval, three
times prior to and six times during the TSST.
Risk factors and covariates
Information about the sociodemographic, health, and lifestyle
factors, including age, occupation, and cigarette, alcohol, and
other drugs consumption were enquired during the initial
phone interview. We also asked the participants to complete
the Beck Depression Inventory during the laboratory visit,
which is a 21-question multiple-choice self-report inventory
measuring depressive symptoms and severity (Beck, Steer,
& Brown, 1996).
Statistical analyses
Before conducting the main analyses, we identified, from a
wide range of health-related factors (e.g., medication, cigar-
ettes, alcohol and drug use, and allergies), those uniquely as-
sociated with cortisol and HR. Two were identified for corti-
sol: being a smoker and having had aflu in the past month and
one for HR: anti-inflammatory medication. These variables
were statistically controlled for in all analyses. We tested
the study hypotheses in three steps. First, we tested whether
the participants showed a distinct pattern of stress response
according to the CTQ-based maltreatment status using a re-
peated-measures analysis of variance (ANOVA; cortisol)
and growth curve analyses (HR). A repeated-measures AN-
OVA was preferred for cortisol because we had no missing
data and the saliva samples were all collected at predeter-
mined, constant times in relation to the beginning of the
TSST. Greenhouse–Geisser corrections for repeated mea-
sures were reported to correct for the violated sphericity as-
sumption. Because missing data occurred for HR due to tech-
nical difficulties, we conducted growth curve analyses using
full information maximum likelihood estimation in MPlus
(Version 6.11; Muthe
´n & Muthe
´n, 1998–2011). Second,
we wanted to expand on the previous analysis and test if dis-
tinct, nonlinear patterns of cortisol and HR responses to stress
could be detected according to the severity of maltreatment.
As described in the Method, we split the total sample in three
groups according to the continuously distributed total CTQ
score of maltreatment, yielding to participants who reported
no (few) maltreatment experiences;some experiences of mal-
treatment;ormore experiences of maltreatment. Tertiles were
chosen to allow a similar number of participants in each group
and sufficient statistical power to test the study’s hypotheses.
Third, we explored whether the symmetry between cortisol
and HR responses to stress was moderated by maltreatment
severity using the regression model included in the SPSS’s
macro PROCESS (Hayes, 2013).
Results
Did the TSST elicit a significant cortisol stress response,
and could distinct patterns of cortisol responses to stress
be detected according to the CTQ-based maltreatment
status?
A repeated measures ANOVA showed that the TSST elicited
a robust and significant increase in cortisol, time: F(2.05,
311.56) ¼57.99, p,.001. Figure 1 illustrates the patterns
of secretion for the participants for whom the experiences
reached the CTQ’s threshold for maltreatment (solid line)
and those for whom it did not (dashed line). The CTQ-based
maltreated participants had higher cortisol responses to the
TSST, Time CTQ-Based Maltreatment: F(2.08, 313.27)
¼2.89, p¼.05, and a trend for significantly higher cortisol
levels throughout the TSST, CTQ-based maltreatment:
F(1, 151) ¼3.69, p¼.06, in comparison to the CTQ-based
nonmaltreatment group. Specifically, while the two groups
did not differ prior to the TSST, –20 min: F(1, 154) ¼
1.01, p¼.32; –2 min: F(1, 154) ¼0.88, p¼.35, distinct re-
sponses emerged subsequently, F(1, 151) ¼4.60, p¼.03.
Did distinct patterns of cortisol responses to stress emerge
according to maltreatment severity?
Distinct cortisol responses were noted according to maltreat-
ment severity, F(4.17, 312.89) ¼2.84, p¼.02. Figure 2
shows that while the three groups had similar initial cortisol
levels, participants who reported more experiences of mal-
treatment had higher cortisol responses to the TSST in com-
parison to the remaining groups. We formally tested this ob-
servation by contrasting the groups two by two. Participants
who reported more experiences of maltreatment had higher
cortisol responses than those who reported some experiences,
F(2.00, 186.16) ¼5.18, p¼.006, but did not differ signifi-
cantly from the participants with no or few experiences,
F(2.10, 217.95) ¼1.45, p¼.24. Moreover, participants
who reported some experiences of maltreatment had lower re-
sponses than controls, F(1, 101) ¼3.89, p¼.05. Altogether,
these findings suggest lower responses when maltreatment
departs from the no (or few) experiences, followed by higher
cortisol levels in participants confronted to more experiences
of maltreatment, a finding hereafter referred to as a shift from
moderate to lower to higher responses as maltreatment sever-
ity increased.
I. Ouellet-Morin et al.500

Were similar patterns of findings observed for HR
response to stress?
As reported in the online-only Supplementary Table S.1, par-
ticipants showed, on average, a significant HR increase during
the TSST, B¼6.95 (0.41), critical ratio ¼16.96, p,.001,
which did not vary according to the CTQ-based maltreatment
groups, B¼–0.31 (0.85), critical ratio ¼–0.36, p¼.72
(Figure 3). In addition, no differences in HR could be detected
according to maltreatment severity, main level: B¼–0.31
(1.01), critical ratio ¼–0.31, p¼.76; stress response: B¼
–0.61 (0.48), critical ratio ¼–1.26, p¼.21 (Figure 4).
Other potential confounders
In addition to the factors affecting cortisol and HR, we ex-
plored whether other factors differed between participants
Figure 2. Cortisol responses (+SEM) to the TSST according to the severity of maltreatment. SEM, standard mean error; n, number of partic-
ipants; TSST, Trier Social Stress Test.
Figure 1. Cortisol responses (+SEM) to the TSST according to CTQ-based maltreatment status. SEM, standard mean error; n, number of par-
ticipants; TSST, Trier Social Stress Test; CTQ, Childhood Trauma Questionnaire.
Maltreatment seerity and stress response 501

who reported CTQ-based maltreatment and those who did not
(Table 1). Participants assigned to the CTQ-based maltreat-
ment group have had more flu in the previous month and
more depressive symptoms than those who did not. While
the first factor was already accounted for in the previous anal-
yses, we reran all the analyses to ensure that the depressive
symptomatology did not explain away the findings. Partici-
pants who reported maltreatment that reached the CTQ-based
threshold still showed higher cortisol responses to the TSST
in comparison to those who did not, F(1.86, 276.14) ¼
4.07, p¼.02. The distinct patterns of cortisol responses to
stress also remained according to increasing levels of mal-
treatment severity, F(3.75, 275.94) ¼3.71, p¼.007, for
which lower responses were noted for participants who re-
ported some experiences of maltreatment in comparison to
those who reported more experiences, F(1.80, 162.24) ¼
6.32, p¼.003. Findings also remained unchanged for HR.
Did the symmetry between cortisol and HR vary according
to maltreatment severity?
Maltreatment severity moderated the association between
cortisol and HR responses to stress, F(1, 146) ¼5.30, p¼
.02. To explore the direction and relative magnitude of these
associations according to maltreatment severity, we conduct
post hoc Pearson correlations. As illustrated in Figure 5,no
significant associations were observed for participants ex-
posed to no (or few; r¼–.17, p¼.22) or some experiences
of maltreatment (r¼.20, p¼.18), whereas a significant as-
sociation emerged for those who reported more experiences
of maltreatment (r¼.34, p¼.02).
Discussion
The present study examined the association between child-
hood maltreatment, cortisol, and HR responses to a psychoso-
cial stress in early adulthood. Consistent with previous find-
ings, we found indications of both lower and higher cortisol
responses to stress in the context of maltreatment. As pre-
viously hypothesized (Del Giudice, Ellis, & Shirtcliff,
2011; Obradovic, 2012), these patterns of secretion may
embody different expressions of changes made by the HPA
axis in an attempt to adapt to the perceived environmental
demands according to past experiences, such as childhood
maltreatment.
Three features of these findings are noteworthy. First, the
lower cortisol response noted in participants who reported
only some experiences of maltreatment falls in line with the
findings from studies that have recruited participants from
the general population (Carpenter et al., 2007,2011; Elzinga
et al., 2008; Lovallo et al., 2012; Ouellet-Morin et al., 2011;
Peckins et al., 2012; Peckins, Susman, Negriff, Noll, & Trick-
ett, 2015) and Child Protective Services (Trickett et al.,
2014). A direct comparison of the relative severity of mal-
treatment captured in these studies is difficult to make, how-
ever. More promising is the consideration that the association
between maltreatment and cortisol reactivity may not be lin-
ear. Many biological and psychological processes are ex-
pected to be nonlinear because of the regulating actions of
several intertwined structures and systems. Still, linear mod-
els remain the analytical strategy of choice (Mattei, 2014;
Young & Benton, 2015). HPA axis reactivity to stress is sim-
ilarly modulated by several brain structures processing the
cognitive and emotional information according to present
Figure 3. Heart rate responses (+SEM) to the TSST according to CTQ-based maltreatment status. SEM, standard mean error; n, number of
participants; TSST, Trier Social Stress Test; CTQ, Childhood Trauma Questionnaire.
I. Ouellet-Morin et al.502

and past contexts (e.g., frontal cortex, the hippocampus, and
the amygdala), which jointly regulate cortisol secretion
through excitatory and negative-feedback pathways at the
level of the hypothalamus, the pituitary, and the adrenal
glands (Gunnar & Vazquez, 2006). Multiple embedded sys-
tems also interact at a molecular level to regulate the initia-
tion, amplitude, and termination of the stress response, in-
cluding genetic and epigenetic processes, glucocorticoid
and mineralocorticoid receptors, endogenous sex steroids,
and oral contraceptives (de Kloet, 2014; Hamstra, de Kloet,
van Hemert, de Rijk, & Van der Does, 2015; Houtepen
et al., 2016; Kudielka et al., 2009; Meaney, 2010; Ouellet-
Morin et al., 2013). The shift from moderate to lower to
higher cortisol responses as maltreatment severity increased
suggests we should revisit the assumption of linearity when
investigating the association between maltreatment and
HPA axis reactivity. Nonlinear models may help to depict
more precisely the changes (e.g., directionality and strength)
of the association between maltreatment and cortisol response
to stress according to the severity of the experiences, to better
document individual variation in this change and the determi-
nants affecting it (e.g., relative severity and chronicity of ex-
posure, timing; for an in-depth discussion on how nonlinear
growth models may be helpful in developmental research,
see Grimm, Ram, & Hamagami, 2011).
Second, the lower cortisol responses in participants who
reported some experiences of maltreatment are also consistent
with the stress inoculation model, according to which dam-
Figure 4. Heart rate (+SEM) to the TSSTaccording to the severity of maltreatment. SEM, standard mean error; n, number of participants; TSST,
Trier Social Stress Test.
Table 1. Participant characteristics in the total sample and according reported experiences of maltreatment
Potential
confounders
Total sample
%(n) or mean (SD)
N¼155
CTQ-based
nonmaltreated
%(n) or mean (SD)
n¼99
CTQ-based
maltreated
%(n) or mean (SD)
n¼56 x2t
Age 24.1 (SD ¼3.7) 24.10 (SD ¼3.7) 24.0 (SD ¼3.6) — 0.08
Student (vs. other) 64.7% (n¼101) 62.0% (n¼62) 69.6% (n¼39) 0.91 —
Single (yes/no) 85.9% (n¼134) 85.0% (n¼85) 87.5% (n¼49) 0.18 —
Weight (kg) 76.4 (SD ¼14.8) 76.1 (SD ¼14.6) 76.9 (SD ¼15.4) — 20.32
Number of alcohol consumption per week 3.4 (SD ¼3.9) 3.2 (SD ¼3.8) 3.7 (SD ¼4.0) — 20.73
Smoking (yes/no) 17.9% (n¼28) 14.0% (n¼14) 25.0% (n¼14) 2.94 —
Drug consumption (yes/no) 25.0% (n¼39) 23.0% (n¼23) 28.6% (n¼16) 0.59 —
Had a flu in the last month (yes/no) 23.1% (n¼36) 17.0% (n¼17) 33.9% (n¼19) 5.79* —
Depressive symptomatology 10.48 (SD ¼8.79) 8.82 (SD ¼7.30) 13.45 (SD ¼10.39) — 22.95**
Note: SD, standard deviation; n, number of participants; kg, kilogram. *p,.05; **p,.01; ***p,.001.
Maltreatment seerity and stress response 503

pened activations of the HPA axis befall milder to moderate
exposure to stress (Crofton, Zhang, & Green, 2015; Parker
et al., 2004). Nevertheless, while lower cortisol response to
stress may protect the body against excessive exposure over
time, it may not be synonymous to resilience, which refers
to better than anticipated adaptation to detrimental environ-
mental influences (Luthar & Zelazo, 2003; Shirtcliff, Peres,
Dismukes, Lee, & Phan, 2014). Caution may also be warran-
ted given that lower basal cortisol levels and response to stress
have been associated with antisocial behaviors and posttrau-
matic stress disorder (Boks et al., 2016; Lupien et al., 2006;
Susman, 2006; van Goozen, Fairchild, Snoek, & Harold,
2007). Future studies need to identify the mechanisms by
which maltreatment confers vulnerability (or resilience) to
mental health or behavioral problems (Bowes & Jaffee,
2013).
Third, the shift from moderate to lower to higher cortisol
responses to the TSST as maltreatment increased in severity
may be better understood, in all its complexity, as diverse ex-
pressions of the HPA axis attempting to adapt to distinct mal-
treatment experiences. This is consistent with the allostatic
load (Juster, McEwen, & Lupien, 2010; McEwen, 1998)
and the adaptive calibration models (Del Giudice et al.,
2011), proposing that the HPA axis’ responses reflect long-
term individual trajectories that can be recalibrated according
to environmental circumstances and for which adaptive and
detrimental costs may ensue. Our findings also parallel Del
Giudice et al.’s (2012) model predicting a succession of mod-
erate, lower, and higher stress responses in safe, moderately
stressful and risky environments. One difference lies at the
very end of the continuum where severe and traumatic envi-
ronments are hypothesized to result in even lower (males)
and higher (females) responses (Del Giudice et al., 2011).
However, others have not found evidence for that fourth cor-
tisol profile either (Peckins et al., 2015).
More generally, other studies have also reported a shift for
basal cortisol activity, where higher morning levels were
noted in moderate adversity while lower levels were detected
Figure 5. Associations between cortisol and heart rate responses to the TSST according to the severity of maltreatment. (a) No (few) maltreatment
experiences, (b) some experiences of maltreatment, and (c) more experiences of maltreatment. TSST, Trier Social Stress Test.
I. Ouellet-Morin et al.504

in more severe conditions (Gustafsson, Anckarsater, Lichten-
stein, Nelson, & Gustafsson, 2010; van der Vegt, van der
Ende, Kirschbaum, Verhulst, & Tiemeier, 2009). Higher to
lower morning basal cortisol levels were also observed in
abused females, from adolescence to adulthood (Trickett,
Noll, Susman, Shenk, & Putnam, 2010; see also Trickett,
Noll, & Putnam, 2011)). Likewise, Doom, Cicchetti, and Ro-
gosch (2014) reported higher to lower basal cortisol levels
over time in maltreated school-aged children. This findings
may also depend, in addition to maltreatment severity, on fac-
tors such as the age, duration and type of maltreatment, as
well as time passed since the end of maltreatment, and the pre-
sence of co-occurring factors enhancing vulnerability (e.g.,
puberty) or promoting resilience (e.g., social support; Gunnar
& Vazquez, 2006; Lupien et al., 2009; Miller, Chen, & Zhou,
2007). Future studies should also investigate further whether
maltreated individuals with lower or higher patterns of re-
sponse to stress are more vulnerable to mental health prob-
lems and behavioral difficulties. Drawing from the adaptive
calibration model, the recalibration of the stress systems
may be adaptive by amplifying, or filtering the information
present in the environment, in order to avoid further aggres-
sion or to develop a sense of normality, for instance. Trade-
offs may, however, be present, such as increased sensitivity
to social judgment, taxing even further the individuals’ al-
ready solicited stress systems and coping mechanisms. The
higher risks of internalizing (e.g., depression) and externaliz-
ing (e.g., antisocial behavior) problems in individuals with
higher and lower cortisol activity, respectively, suggest the
possibility that distinct costs may arise depending of the
recalibration of the stress systems (Struber, Struber, &
Roth, 2014; Susman, 2006). Longitudinal studies investigat-
ing the recalibration of the stress response systems as they
unfold and according to the numerous intervening factors
would be uniquely suited to depict the time-varying trade-
offs following these adaptations (Mead, Beauchaine, &
Shannon, 2010).
Nevertheless, it is only among participants who reported
more experiences of maltreatment that a significant degree
of symmetry emerged between cortisol and HR responses
to stress. This finding, albeit preliminary and exploratory in
nature, echoes in part the permissive or preparative actions
of glucocorticoids on the SNS, previously suggested by Sa-
polsky, Romero, and Munck (2000). Both the permissive
and the preparative actions of glucocorticoids theoretically
enhance the body’s arousal to a new or repeated appearance
of a stressor. In this cross-sectional study for which no mea-
sure of diurnal secretion was made, we can only speculate
about the possibility that the exposure to higher levels of mal-
treatment could have also induced persistent changes in basal
secretion, so that an enhancing action of glucocorticoids on
HR and cortisol responses to the TSST may have been taken
place (i.e., permissive actions). Alternatively, the higher cor-
tisol responses to stress observed in participants who reported
more maltreatment experiences may reflect a stable pattern of
responsivity (i.e., preparative actions). The time-varying and
reciprocal nature of these influences complicates the under-
standing of the symmetry between cortisol and HR responses
to stress and its adaptive value (or cost) on health and func-
tioning. Future studies should measure both basal and reac-
tive HPA axis and SNS to disentangle the potential permis-
sive and/or preparative effects of glucocorticoids on the
stress systems in increasing levels of maltreatment.
The present findings should be considered in light of some
limitations. First, childhood maltreatment was assessed using
the CTQ-SF, a well-validated and widely used questionnaire,
for which the recall of experiences may, however, have been
tainted by memory loss and bias. Nevertheless, other findings
suggested that recall bias emerging as a result of directed
forgetting and relabeling (Epstein & Bottoms, 2002), for
instance, accounted for less than 1% of the maltreatment’s
variance and that the use of retrospective reports has little ef-
fect on the investigation of its long-term impact on function-
ing (Fergusson, Horwood, & Boden, 2011). This strategy
may even be preferable to the sole consideration of recent ex-
posure to stress that may not have lasted long enough to in-
duce persisting changes in cortisol response to stress (Peckins
et al., 2015). Second, we did not examine the possibility that
distinct associations may have emerged as a function of mal-
treatment subtypes (e.g., emotional abuse and neglect) nor
did we take into account the fact that the items included in
the CTQ are not equally severe in their impact on children
(Barnett, Manly, & Cicchetti, 1993). On a related point, our
measure could not untangle the impact of frequency from
the severity of maltreatment, two concepts shown to be differ-
entially associated with behavioral outcomes (Jackson, Gab-
rielli, Fleming, Tunno, & Makanui, 2014). Future research
with more participants who were confronted with maltreat-
ment and for whom the experiences could be operationalized
more homogenously based on the information available in the
official records holds the promise of better describing the im-
pact of this complex, multifaceted concept on the stress re-
sponse systems and functioning (see Mennen, Kim, Sang,
& Trickett, 2010). Third, since our measure of maltreatment
encompassed all experiences that have occurred before 18
years of age, we could not test whether the nature or timing
further affected cortisol responses in a nonlinear manner.
More generally, the absence of prospectively and repeatedly
collected measures in this study impeded us from investigat-
ing the developmental processes and time-varying individual
and environmental influences that may also have affected the
course of stress responses systems. Fourth, our sample was
only composed of adult males. Because sex differences in
cortisol response to stress (Carpenter et al., 2009) and
sexually dimorphic associations with maltreatment have
been reported (Negriff et al., 2015), although inconsistently
so (Kudielka et al., 2004), our findings may not be generaliz-
able to female participants. Fifth and finally, although HR is a
fairly common measure of SNS activity, it remains
highly variable and could easily be modulated by factors
such as position of the participant (Vogel, Wolpert, &
Wehling, 2004), in spite of specific instructions asking
Maltreatment seerity and stress response 505

participants to stay still at a preidentified, marked place during
the TSST.
In conclusion, this study extends prior findings regarding
the impact of childhood maltreatment on HPA axis and SNS
reactivity to stress by reporting distinct expressions of cortisol
dysregulated patterns of stress response as maltreatment in-
creased in severity. This study calls into question the linearity
assumed to exist in the association between maltreatment and
the stress response systems, as well as in regard to its impact
on health and behavioral functioning.
Supplementary Material
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