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Worse than sticks and stones? Bullying is associated with altered HPA axis functioning and poorer health
Brain and Cognition 77 (2011) 183–190
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Brain and Cognition journal homepage: www.elsevier.com/locate/b&c
Worse than sticks and stones? Bullying is associated with altered HPA axis functioning and poorer health Jennifer M. Knack a,⇑, Lauri A. Jensen-Campbell b,⇑, Andrew Baum b a b
Clarkson University, 8 Clarkson Ave Potsdam, NY 13699-5825, United states University of Texas at Arlington, 501 S. Nedderman Drive Arlington, TX 76019-0528, United States
a r t i c l e
i n f o
Article history: Available online 11 August 2011 We dedicate this paper to Dr. Andy Baum whose mentorship and friendship has significantly impacted our lives and research; we will always remember you Keywords: Peer victimization Bullying Cortisol HPA axis Adolescence
a b s t r a c t Adolescents (N = 107; M = 12.23 years, SD = 1.09 months) participated in a two-part study examining peer victimization, neuroendocrine functioning, and physical health. In phase 1, adolescents completed questionnaires assessing peer victimization and health. They returned for phase 2 which consisted of two sessions. In session 1, adolescents learned to collect salivary cortisol samples; they collected four samples over 2 non-sports school days. In session 2, adolescents completed the Trier Social Stress Test (TSST) in which they prepared and delivered a speech while cortisol was collected. Peer victimization predicted poor health outcomes and a flattened cortisol awakening response (CAR); this CAR was linked with health problems. During the TSST, victims reported more stress and exhibited altered cortisol levels. Higher cortisol immediately after the stressor and lower cortisol 30 min after the stressor were associated with more health problems. This study provides evidence that the relationship between peer victimization and poor physical health may be explained by differences in neuroendocrine functioning. Ó 2011 Elsevier Inc. All rights reserved.
1. Introduction ‘‘Sticks and stones may break my bones but words will never hurt me.’’ Peer victimization, defined as being the habitual target of peers’ aggression, is not a new phenomenon. Also known as being bullying, peer victimization is intended to be hurtful to another person of lesser status (Olweus, 1993). Contrary to the notion that words do not hurt, both physical and relational forms of peer victimization have negative developmental and mental health outcomes in adolescence including poorer school performance, higher school absences, more adjustment problems and suicide attempts for adolescents who are bullied compared to those who are not bullied (e.g., Egan & Perry, 1998; Hodges & Perry, 1996). Bullied individuals also experience more physical health problems than those who are not bullied (Greco, Freeman, & Dufton, 2007; Williams, Chambers, Logan, & Robinson, 1996). Moreover, fall reports of victimization predict worse physical health in the spring whereas poor physical health in the fall does not predict increased victimization in the spring (Nishina, Juvonen, & Withkow, 2005; Knack, Iyer, &
⇑ Corresponding authors. E-mail addresses: [email protected] (J.M. Knack), [email protected] (L.A. Jensen-Campbell). 0278-2626/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2011.06.011
Jensen-Campbell, in press). Taken together, the literature suggests being bullied is associated with physical health problems. However, little research has examined why such a link exists. The emergence of physical health problems following repeated experiences of bullying suggests that changes in biological processes may occur as a result of being bullied; these biological changes may be an underlying mechanism that can explain the link between experiences of victimization and poor physical health. As a stressor, bullying would be expected to have predictable effects including altered cortisol production (Hansen, Hogh, & Persson, 2011; Hansen et al., 2006; Vaillancourt et al., 2008). The central goal of this study was to examine whether altered HPA axis activation may help explain why the link between peer victimization and poor health exists. 1.1. Stress and health Stress has a direct effect on a number of physiological systems including the HPA axis (e.g., Dougall & Baum, 2001). Cortisol, one of the end products of HPA activation, can be beneficial in response to acute stressors because cortisol helps mobilize the body to deal with the stressor. However, chronically high levels of cortisol can be maladaptive (e.g., McEwen, 2000; Vaillancourt et al., this issue). Surprisingly, in adolescents (Vaillancourt et al., 2008) and adults (Hansen et al., 2006, 2011) peer victimization has been associated with lower diurnal cortisol levels than in those not victimized.
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These findings are consistent with the link between stressors (e.g., childhood maltreatment or PTSD) and lower cortisol levels (Johnson, Delahanty, & Pinna, 2008; Pervanidou, 2008). Researchers have begun to focus on the cortisol awakening response (CAR). The CAR is defined by an increase in cortisol roughly 20–30 min after waking and is the peak in the diurnal pattern; cortisol levels gradually drop throughout the remainder of the day. Some researchers conceptualize the awakening response as a ‘‘cortisol mobilization response’’ during which the body mobilizes its resources for the day (e.g., Tops, Riese, Oldehinkel, Rijsdijke, & Ormel, 2008, p. 553). Following this theory, we predict adolescents with a blunted CAR will be less physiologically equipped to handle threats to their immune system resulting in more reports of health problems. Acute social stressors have been found to increase cortisol reactivity. In a meta-analysis of 208 studies, Dickerson and Kemeny (2004) found that uncontrollable tasks involving a social evaluative threat produced a larger cortisol change and had a longer recovery time compared to uncontrollable tasks without a social evaluative threat. One such common laboratory social stressor, the Trier Social Stress Test (TSST), has repeatedly been used to activate the HPA axis (Kirschbaum, Pirke, & Hellhammer, 1993). As part of the TSST, participants give a 5 min speech and then count backward by 13 from a large number (e.g., 1379). Throughout the TSST, salivary cortisol samples are collected. These acute periods of social stress have produced increases in levels of salivary cortisol. We found only two studies to date that examined peer victimization and cortisol reactivity (see Hamilton, Newman, Delville, & Delville, 2008; Rudolph, Troop-Gordon, & Granger, 2010); we expect acute social stressors are likely to elicit different HPA responses in early adolescents who are bullied versus those who are not bullied. Social stressors may be especially influential during adolescence given the number of physiological changes that occur (e.g., puberty, alterations in HPA axis activity, rapid brain maturation; Spear, 2000; Walker, Walder, & Reynolds, 2001). Moreover, bullying should be especially evocative and disruptive as adolescents place more emphasis on peer relationships rather than primarily relying on parents for companionship and support (Harris, 1995; Hartup, 1996; Teicher, Samson, Sheu, Polcari, & McGreenery, 2010). Adolescence may be a time of increased vulnerability to stressful events which ultimately lead to a change in how stress is experienced (Walker et al., 2001). 1.2. Current study This research examined whether HPA activation, as assessed by repeated assay of salivary cortisol levels, may be a mechanism underlying long-term physical health effects of peer victimization. First, we expected that peer victimization would predict poorer physical health for those victimized than those not victimized. Second, we expected being bullied would influence cortisol levels; that is, victimized adolescents would exhibit lower patterns of daily cortisol than would nonvictimized adolescents and that victimization would be related to a flattened CAR. In addition, we anticipated that victimized adolescents would have a different cortisol reaction to an acute social stressor compared to nonvictimized adolescents. Given that this paper was one of the first studies to examine bullied adolescents’ stress reactivity, we did not make specific predictions about the direction of the effect. Third, we predicted these differences in cortisol would predict poorer physical health for victimized adolescents compared to nonvictimized adolescents. We examined whether diurnal pattern and cortisol reactivity predicted health outcomes. Finally, we expected daily cortisol levels and cortisol reactivity would mediate the victimization-health link.
2. Method 2.1. Participants Adolescents (5–8th grades) and their parent participated in a two-part research study on friendship, peer relationships, and health (N = 107). Participants were girls (56.1%) and boys (43.9%) in the Dallas/Fort Worth area (M = 12.23 years; SD = 1.09 months). The racial composition included 66.4% Caucasian, 15.9% Hispanic/Latino, 11.2% Black/African American, 3.7% Asian, 1.9% American Indian/Alaskan Native, and 0.9% Hawaiian/Pacific Islander participants. Information on socioeconomic status was not collected. 2.2. Participant recruitment We mailed home project information to people who were randomly selected from mailing lists from local school districts and private child organizations. We also recruited adolescents from a large public school, several small private schools, a local dance company, and several summer camps. We targeted adolescents with meaningful histories of being bullied (i.e., adolescents who scored at least one standard deviation above the mean on victimization). Adolescents were paid $5.00 and entered into a raffle for participating in Phase I. Adolescents and parents were each paid a total of $40.00 for participating in two sessions in Phase II. 2.3. Assessment of victimization 2.3.1. Children’s self-experiences questionnaire – self- and parentreport (CSEQ-SR, CSEQ-PR) The CSEQ-SR/CSEQ-PR assessed peer-related instances of victimization (Crick & Grotpeter, 1995). This survey measured physical and relational victimization (see Knack, 2009 for details). Each subscale was comprised of five items which measured the frequency adolescents experienced an event on a scale of 1 (never) to 5 (all the time). High reliability was found for both self and parental reports of overt (a = 0.81, 0.84) and relational victimization (a = 0.84, 0.86). 2.3.2. Direct and indirect aggression scales – victim version (DIAS) The DIAS (Bjorkqvist, Lagerspetz, & Osterman, 1992) is a 24item measure comprised of three subscales that assess frequency of physical, verbal, and indirect aggression/victimization. The questions were answered on a Likert-type scale ranging from 1 (never) to 5 (very often). High reliability was found for self and parental reports of physical (a = 0.85, 0.89), verbal (a = 0.86, 0.90), and indirect (a = 0.89, 0.91) victimization, respectively. 2.3.3. Creating the victimization composite Adolescents and parents completed assessments of the adolescent’s experiences of victimization given that multiple informants of bullying are advantageous in obtaining the best estimates of bullying (Ladd & Kochenderfer-Ladd, 2002; Totura, Green, Karver, & Gesten, 2009). The subscales were correlated across parent- and self-reports (range of correlations = 0.25–0.54, M = 0.40). No systematic differences were found between types of bullying and cortisol by type of victimization or rater, so we created an overall composite of bullying comprised of all parent- and self-reports for all the victimization subscales to remove biases associated with child- versus parent-raters. We used a variable-centered approach (i.e., treating victimization as a continuous variable) and a person-centered approach (i.e., creating dichotomized groups based on victimization scores).
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We included the person-centered approach because other researchers (e.g., Solberg & Olweus, 2003; Vaillancourt et al., 2008) treated their victimization data as distinct groups; we wanted our data to be easily comparable with previous work. However, creating distinct groups reduces statistical power and the richness of the data set (Aiken & West, 1991). We therefore also included a variable-centered approach. To create groups of victimized versus nonvictimized adolescents we conducted agglomerative hierarchical cluster analyses with victimization measures as our clustering variables and chose a two-cluster solution.1 On the second step, we used k-cluster means analysis with normalized Euclidean distance as the distance metric to confirm the two cluster group solution. Using McNemar’s test, there were no significant changes in group membership between the two classification methods, p = 0.50. The victimized group (n = 31) was significantly more victimized (M = 0.99, SD = 0.43) than the nonvictimized group (n = 76; M = 0.04, SD = 0.39) on the overall victimization composite, F(1, 105) = 234.85, p < 0.01, g2 = 0.69.
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2.7. Procedure In phase one, adolescents completed surveys either at school or online assessing peer victimization and health problems. Adolescents and their parent returned to the laboratory for phase two (which consisted of two parts). During session one, adolescents and their parents completed several questionnaires (e.g., health) and learned how to collect saliva samples and how to use a Palm Pilot. Adolescents were instructed to collect four saliva samples over each of two non-sport school days immediately upon waking, 30 min after waking, immediately upon returning home from school, and 30 min before going to bed. Session two was held between 4:00 pm and 7:00 pm to control for diurnal cycles. Parents completed several questionnaires about their child’s social experiences and health. Adolescents then completed a modified version of the TSST in which they had 10 min to prepare for a 5 min speech (see Knack, 2009 for details). After the speech, adolescents completed the post-TSST survey. Four saliva samples were collected during the TSST.
2.4. Physical health assessments 3. Results A health survey was used to assess how frequently and severely adolescents experienced health problems linked with stress (e.g., stomach aches, flu, mouth sores, sore throats, fatigue). Fourteen Likert-type questions ranging from 1 (not at all) to 4 (all the time) assessed the frequency of symptoms (a = 0.72), and 14 Likert-type questions ranging from 1 (does not hurt at all) to 4 (unbearable pain) assessed the severity of symptoms (a = 0.67). This survey also measured of how often adolescents went to the school nurse and doctor (a = 0.74). Next, The Abdominal Pain Index consisted of five Likert-type questions that assessed experiences of abdominal pain over the past 2 weeks. Questions examined the frequency of abdominal pain, length of the pain, and intensity of the pain. Only adolescents completed this questionnaire, a = 0.86. Several composites of parent- and self-reports served as measures of health including (1) frequency of health problems; (2) severity of health problems; (3) frequency of adolescent’s visits to the school nurse/doctor; (4) abdominal pain; and (5) all health problems.
3.1. Does peer victimization predict poorer health outcomes? We expected peer victimization would predict physical health. In a series of regression analyses using a continuous composite of peer victimization, victimization was associated with more frequent and severe health problems, increased abdominal pain, and more frequent health visits (ts(105) = 7.31, 6.76, 4.98, 3.86, p < 0.01, sr2 = 0.34, 0.30, 0.19, 0.12, respectively). 3.2. Does being victimized influence the daily diurnal pattern of cortisol production? We expected victimized adolescents would show lower daily levels of cortisol than their non-victimized peers, especially in the morning (i.e., a flattened CAR). See Fig. 1 for cortisol diurnal patterns. We conducted multi-level modeling (Raudenbush & Bryk,
2.5. Experimental questionnaires 2.5.1. Trier Social Stress Test (TSST) post-survey questionnaire An 18-item survey comprised of Likert-type questions ranging from 1 (not at all) to 7 (very much) was administered after the TSST. First, we created a composite score for how accepted adolescents felt while giving their speech (e.g., ‘‘did you feel liked during the task?’’), a = 0.85. Second, we created a composite score for stress by averaging how stressful and challenging adolescents viewed the task (r = 0.62, p < 0.001). We also examined how evaluated and in control participants felt during the speech. 2.6. Cortisol data collection and analysis Cortisol samples were collected in salivettes (Starstedt™) nested tubes following standard collection procedures (see Knack, 2009 for details) and tested with salivary cortisol kits from Salimetrics (State College, PA). Palm Pilots recorded the date and time and prompted the adolescent to ensure samples were collected correctly When examining a subsample of participants (n = 72) we found a mean correlation of 0.99 between the Palm Pilot times and the times recorded on the cortisol tubes (range: 0.45–1.00). 1 We also examined the three-factor solution for completeness. The fit of this solution was not acceptable based on the K-mean cluster results and McNemar’s test.
Fig. 1. Daily diurnal salivary cortisol patterns during two school days.
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2002; Snijders & Bosker, 2002) using a two level model with variations in change parameters in cortisol levels within a child at level 1 and variation among children on victimization at level 2 (i.e., cortisol assessments were nested within the adolescent). On the first step, we calculated regression equations that estimated the diurnal pattern based on time of assessment. In addition to the linear trend for time of day predicting cortisol levels, we also modeled the quadratic function for time since diurnal pattern often takes a quadratic shape.2 In the second step, the first-step regression coefficients (both b0 and b1) were regressed on the level of victimization of the child (see Raudenbush & Bryk, 2002). We report analyses for standardized victimization scores which produced identical results to analyses using unstandardized centered scores. There was an overall linear decline in cortisol throughout the day (t(769) = 38.60, p < 0.001) and a victimization linear slope interaction, t(769) = 2.13, p < 0.05. For high victimization levels, the slope was not as steep as it was for medium and low levels of victimization (bs = 0.98, 0.93, 0.87 for low, medium, and high levels, respectively, ts > 25.88, ps < 0.01). There was also an overall quadratic function of the slope (t(769) = 2.67, b = 0.10, p < 0.01) and a victim quadratic interaction (t(769) = 2.20, p < 0.05). When victimization was at low levels, the quadratic function was strong, t(769) = 3.52, b = 0.20, p < 0.01. When victimization was at high levels, there was no quadratic slope, t(769) = 0.18, b = 0.01, ns. We then examined differences between time 1 and time 2 to specifically look at the CAR. We found a significant linear increase from time 1 (i.e., upon waking) to time 2 (i.e., 30 min later), t(392) = 8.67, b = 0.21, p < 0.01, and a victimization linear function interaction, t(392) = 3.36, b = 0.08, p < 0.001. The CAR was significant for low victimized adolescents, t(392) = 8.06, b = 0.29, p < 0.001; for high victimized adolescents, the slope was weaker, t(392) = 4.29, b = 0.13, p < 0.001. In summary, victimized adolescents exhibited a flattened CAR. We then examined the change in cortisol from time 2 (i.e., 30 min after waking) to time 3 (after school). As expected, we found a drop in cortisol, t(375) = 33.24, b = 1.09, p < 0.001, and a victimization slope interaction, t(375) = 2.91, b = 0.10, p < 0.01. For high levels of victimization, the slope was weaker, t(375) = 21.90, b = 1.00, p < 0.001, whereas for low levels of victimization, the slope was stronger, t(375) = 24.88, b = 1.19, p < 0.001. That is, although the slope was significant for both groups, adolescents who are not victimized evidenced a sharper drop in cortisol from time 2 to time 3 than did victimized adolescents. From time 3 (i.e., after school) to time 4 (i.e., 30 min before bed) there was an overall linear trend, t(372) = 10.55, b = 0.73, p < 0.001; however, we did not find a victimization linear function, t(372) = 1.75, b = 0.13, p = 0.08. Finally, we collapsed across time points from day 1 and day 2 to get average levels of cortisol at each of the four time points throughout the day. Using independent sample t-tests, we found that victimized adolescents had significantly lower cortisol levels at 30 min after waking (t(105) = 2.71, p < 0.01) and 30 min before bed (t(105) = 2.03, p = 0.045).
in cortisol levels within children (level 1). We were most interested in whether health was related with the CAR. There was an overall health linear time interaction, t(769) = 1.93, p = 0.05, but no health quadratic time interaction, t = 0.09, ns. When the child had few health problems, the expected increase in cortisol from T1 to T2 was significant, t(392) = 8.04, b = 0.28, p < 0.05. When the child had more health problems, the slope from T1 to T2 was significant, t(392) = 4.61, b = 0.14, p < 0.05, but the magnitude was smaller. That is, the expected CAR was associated with better physical health. Other areas of the curve were not related with health. 3.4. Does CAR mediate the link between victimization and health problems? It is possible that the CAR mediates the link between victimization and health. We controlled for age, internalizing problems, and the area under the curve with reference to 0 or ground (AUCg). Following procedures outlined in Preacher and Hayes (2008), we found victimization was related to the average slope of CAR, t(107) = 2.08, p = 0.04, b = 0.16. In addition, the slope was marginally related to health problems, t(107) = 1.73, p = 0.87, b = 0.20. The direct path of victimization to health problems was still significant after controlling for the CAR slope, t(107) = 4.90, p < 0.01, b = 0.45. Using bootstrapping procedures with 1000 bootstraps, there was a marginally significant indirect effect (see Fig. 2). 3.5. Are victimized adolescents with health problems showing the greatest CAR flattening? We expected that victimized adolescents who reported poor physical health would have a flatter CAR than victimized adolescents who did not have poor health. As such, we examined whether victimization amplified this health-cortisol association for CAR. Again we ran a multi-level model. There was a victimization health time interaction, b = 0.09, t(388) = 4.10, p < 0.01. Using procedures outlined by Aiken and West (1991), we conducted simple effects analyses. At high levels of victimization and high levels of health problems, the CAR slope was significant but smallest in magnitude, b = 0.14, t(388) = 4.65, p < 0.01; when victimization and health problems were low, the relation between time and cortisol was nearly twice the magnitude, b = 0.24, t(288) = 6.32, p < 0.01. Interestingly, when there was either high victimization/low health problems or low victimization/high health problems, the magnitude of the CAR slope was the largest, bs = 0.37, 0.39, ts(388) = 4.96, 5.32, ps < 0.01. Using a person-centered approach, we explored classifications of our victims and non-victims on health. There were two health groups; 51 adolescents reported having good health, and 56
3.3. Do daily diurnal cortisol levels predict physical health outcomes? We expected daily cortisol levels would predict health outcomes. Using multi-leveling modeling, we again constructed a two level model. For this analysis, we used an overall composite of health problems among children (level 2) to predict variations 2 Cubic and higher trends were examined as well. They were dropped from the final model because they were not significant. Moreover, their variance inflation factors were not acceptable (>10.0).
Fig. 2. CAR slope mediates link between peer victimization and health problems.
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adolescents reported stress-related health problems. Of the 51 adolescents who reported good health, only 3 were classified as victims (compared to the 28 victims who reported stress-related health problems). That is, over 90% of victims reported having stress-related health problems. Conversely, only 36% of nonvictimized children reported have stress-related health problems. This differential pattern of health problems for victims and nonvictims was statistically significant, v2(1) = 25.25, p < 0.001. Taking these patterns of results together, our research suggests that the majority of bullied adolescents report health problems; moreover, adolescents who are high on victimization and health problems show the flattest CAR response. 3.6. Does being victimized influence self-reported reactions to the TSST? We examined correlations between victimization and self-reported reactions to the TSST. Adolescents who were victimized reported feeling less accepted during the TSST and that the TSST was more stressful than non-victimized adolescents (rs = 0.20, 0.28, ps < 0.05, respectively). Conversely, victimized and nonvictimized adolescents felt similarly evaluated and perceived similar degrees of control (rs = 0.09, 0.18, ns, respectively) during their speech. 3.7. Does being victimized influence cortisol reactivity during the TSST? Next, we examined whether victimization predicted cortisol levels during the TSST. There was no overall main effect for time, b = 0.02, t(404) = 1.35, p = 0.18. However, there was an overall victim time interaction for cortisol, b = 0.04, t(404) = 2.41, p < 0.02. To explore this trend, we examined changes in slope between time points. There was no evidence that victimization influenced the slope between T1 and T2 (t(205) = 0.29, p = 0.78). There was a marginally significant increase in cortisol from T2 to T3 (t(199) = 1.79, p = 0.074); however, there was no victim time interaction, t(199) = 0.04, ns. When examining the change in slope from T3 to T4, there was a victim time interaction for cortisol, t(195) = 2.95, p < 0.01. When victimization was high, there was a significant decrease in cortisol between T3 and T4, t(195) = 2.32, p = 0.02. When victimization levels were low, there was marginal increase in cortisol, t(195) = 1.86, p = 0.06. Overall, the pattern suggested that cortisol increased from T2 and T3 for both victims and non-victims. However, victims showed a decrease in cortisol between T3 and T4 whereas nonvictims showed a continued increase in cortisol. Using a person-centered approach and a repeated measures analysis, we examined this pattern to determine whether victimization predicted cortisol levels across the TSST (controlling for age and sex). There was an overall cubic effect for time predicting cortisol, F(1, 102) = 8.52, p < 0.01, g2 = 0.08. There was a significant quadratic victimization assessment interaction (F(1, 102) = 4.72, p < 0.03, g2 = 0.04) again indicating that the pattern of cortisol production throughout the TSST differed for victimized and nonvictimized adolescents (see Fig. 3). We then conducted simple effects analyses in which we examined whether levels of sequential cortisol levels differed (i.e., T1 versus T2, T2 versus T3, T3 versus T4). There was an overall increase in cortisol from T1 to T2, F(1, 102) = 4.60, p < 0.01. There was no victimization time interaction, F(1, 102) = 0.57, ns. There was no increase in cortisol from T2 and T3, F(1, 102) = 0.54, ns. There was also no victimization time interaction, F(1, 102) = 0.33, ns. There was no overall change in cortisol from T3 to T4, F(1, 102) = 2.42, p = 0.12. However, there was a significant victimization time interaction, F(1, 102) = 5.00, p < .05, g2 = 0.047; there was a significant increase in cortisol from T3
Fig. 3. Cortisol reactivity for victimized and nonvictimized adolescents during the TSST.
and T4 for nonvictimized adolescents (F(1, 72) = 6.99, p < 0.01, g2 = 0.09) whereas for victimized adolescents, there was a significant decrease in cortisol (F(1, 27) = 6.98, p < 0.01, g2 = 0.21). 3.8. Does cortisol reactivity during an acute social stressor predict physical health? Using regression, we examined whether adolescents who were more reactive to the TSST (i.e., less able to cope with stressors) would exhibit more health problems. Age, sex, and average daily cortisol were entered on step 1 and the four lab assessment points were entered on step 2. First, cortisol levels at T3 (immediately after delivering speech) predicted more health problems (t(99) = 1.68, p = 0.097, sr2 = 0.03) whereas cortisol levels at T4 (30 min after delivering their speech) negatively predicted health problems (t(99) = 2.21, p = 0.03, sr2 = 0.05). Second, higher cortisol levels at time 3 predicted more frequency health problems (t(99) = 2.28, p < 0.05, sr2 = 0.05) whereas lower cortisol levels at time 4 predicted more frequency health problems (t(99) = 2.16, p < 0.05, sr2 = 0.04). Third, higher cortisol levels at time 3 predicted more frequent visits to the doctor/nurse (t(99) = 2.54, p < 0.01, sr2 = 0.06); lower levels of cortisol at time 4 predicted more frequent office visits (t(99) = 2.89, p < 0.01, sr2 = 0.07). 3.9. Does cortisol reactivity mediate the link between victimization and health? We again used procedures outlined in Preacher and Hayes (2008) to examine whether cortisol during the TSST mediated the link between victimization and health problems. In this analysis, victimization was the predictor, the four lab cortisol assessments were mediators, and frequency of health visits was the outcome measure. Age, sex, daily cortisol levels, and internalizing problems were entered as control variables. Although there was no overall total indirect effect across the four mediators, cortisol levels 30 min after the speech marginally mediated the victimization-health effect when controlling for the other lab assessments of cortisol. Preacher and Hayes (2008) note that it is not only possible but acceptable to find specific indirect effects even when the total indirect effect is nonsignificant. This
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Fig. 4. Do cortisol levels during an acute social stressor mediate the link between victimization and visits to the doctor/nurse?
finding suggests that victimization was related to lower recovery cortisol levels which, in turn, led to more visits to health professionals (see Fig. 4). For acute reactivity, the data suggest that something is responsible for a shift in cortisol and its relationship with health. Up to T4 (i.e., 30 min after giving the speech), the curve is exactly what one would expect; the deviation for victims occurs only at T4. There was no evidence of a mediation effect of cortisol reactivity for frequency or severity of symptoms. 4. Discussion Although research has shown an association between peer victimization and health problems, this link has largely been based on self- and parent-reports. Most studies on the victimization-health link have looked at either health outcomes or cortisol patterns. This study was the first to examine health outcomes and cortisol patterns simultaneously when examining victimization’s influence on health. As expected, more frequent peer victimization was associated with greater frequency and severity of health problems, more visits to health professionals, and more abdominal pain. Notably, peer victimization accounted for large amounts of the variance in health problems (i.e., 34% in frequency of problems, 30% in severity of problems, 12% in frequency of visits to health professionals, and 21% in abdominal pain) suggesting that victimized children may not be avoiding school simply because they want to avoid interacting with their peers. Rather, their absences from school may be due, in part, to actual illnesses. 4.1. Exploring the links between victimization, daily cortisol patterns, and health outcomes Although Vaillancourt et al. (2008) examined the link between daily cortisol and victimization, they included only two assessments per day and did not assess physical health. The current study allowed for better examination of the diurnal pattern by including four assessment points per day for 2 days. We found the expected diurnal pattern for nonvictimized adolescents where cortisol levels peaked 30 min after waking and then decreased over the day. However, victimized adolescents had lower levels of cortisol 30 min after waking and 30 min before bed than nonvictim-
ized adolescents. This finding is consistent with other findings that lower levels of cortisol are linked with peer victimization (Hansen et al., 2006, 2011; Vaillancourt et al., 2008). Lower cortisol levels, specifically hypocortisolism, have also been linked with PTSD (Heim et al., 2000). Our research suggests victimization is not merely typical school-yard behavior or a normal part of growing up. Rather, peer victims have similar diurnal patterns to people who have experienced stressful events (e.g., Kliewer, 2006). We also found evidence for a blunted CAR in victimized adolescents. A flattened CAR has been linked with the occurrence and prevalence of stressors. For example, Tops et al. (2008) found that women with a high fear of negative social evaluation (i.e., higher stress) had a lower CAR than women with a lower fear of negative social evaluation. Moreover, we found that the CAR slope mediated the link between victimization and health problems. Taken together, the data suggest that victimization is linked with a flattened CAR which in turn predicted poorer health. If the ‘‘cortisol mobilization response’’ theory of the CAR response is correct (Tops et al., 2008, p. 553), victimized children (who had a blunted CAR) would be less equipped for biological processes to run efficiently and effectively (e.g., immune responses) leaving the body more susceptible to illness. Additional research is needed to more fully understand how salivary cortisol levels impact health outcomes for victimized adolescents. 4.2. Exploring the links between victimization, cortisol reactivity, and health outcomes Cortisol levels gradually increased over the course of the TSST and peaked 30 min after speech delivery among nonvictimized adolescents, but for victimized adolescents there was a significant drop in cortisol 30 min following their speech delivery. This drop in cortisol was surprising given other researchers have found cortisol levels stay elevated after the TSST. Our findings, however, are similar to those of Roy (2004); lower cortisol levels after a stressful lab task were linked with a higher incidence of real-life stressors prior to participating in the lab task. Taken together, our findings converge with previous research suggesting victimized adolescents are experiencing more daily social stress than nonvictimized adolescents and that this heightened exposure is impacting their HPA
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axis functioning. That said, we are still unsure why cortisol levels dropped for victimized adolescents 30 min after giving their speech. Since it takes time for cortisol to show up in saliva, the last sample should reflect the cortisol response to stress experienced while delivering the speech. It may be that victimized adolescents are less reactive than nonvictimized adolescents in socially stressful situations. Alternatively, victimized adolescents may recover faster after a social stressor than nonvictimized adolescents. To examine this possibility, an additional saliva sample would be needed; our data do not allow us to test these predictions. Research suggests consistent high reactivity is linked with negative mental and physical health outcomes (e.g., Lovallo & Gerin, 2003). We found that peer victimization predicted lower cortisol levels 30 min after delivering the speech which predicted more frequent visits to the doctor. This finding is slightly different to what we expected; we anticipated that initial cortisol reactivity would also mediate the victimization-health link. As discussed above, including an additional saliva sample may help shed light on these findings. It is possible that the sample 30 min after speech delivery may actually reflect early reactivity to the speech rather a recovery response. Future research should investigate this link. 4.3. Limitations and future directions Caution must be exercised in generalizing the results of this study. Due to the small sample size (i.e., 31 victims), our results need to be replicated. Given the low sample size, we did not examine whether types of peer victimization (e.g., relational versus overt) differentially alter HPA axis functioning. We also did not explore whether these links differed by participant sex. However, it is reasonable to expect that sex differences may occur (Kudielka, Hellhammer, & Wust, 2009; Paris et al., 2009); future research should explore sex differences. We did not include a number of psychological controls in our statistical models that are potential confounds with cortisol levels. Previous research found that cortisol levels can be affected by depression (e.g., Van den Bergh & Van Calster, 2009), aggression (e.g., McBurnett, Lahey, Rathouz, & Loeber, 2000), adjustment problems (e.g., McBurnett et al., 2000), puberty (Adam, 2006), and participant sex (Kudielka et al., 2009; Paris et al., 2009). Because we did not find that cortisol was associated with depression or adjustment problems in preliminary analyses, we did not include additional psychological controls in our models. In addition, we did not measure whether adolescents had experienced prior abuse or maltreatment. That being said, we did closely control the collection of cortisol samples. First, all cortisol reactivity samples were collected between 4:00 pm and 7:00 pm to control for diurnal patterns. Second, participants were instructed not to eat or drink 30 min before sampling. Third, diurnal samples were collected on non-sports days to ensure that levels were not inflated due to exercise. Fourth, although we cannot ensure that morning samples were collected immediately upon waking, self-reports of collection times matched the times recorded by the Palm Pilots which suggests that participants followed the instructions. Future research should also record time of waking. Moreover, this study was correlational in nature. Even though the statistical models and theoretical framework imply a clear causal relationship, care must be taken not to interpret the findings as causal since such statements cannot be deduced from correlational studies. Although our theoretical model suggests that being bullied causes HPA axis dysregulation which in turn leads to poor reports of health, alternative explanations are possible. For example, children with altered HPA axis functioning or poor health may be more likely to be targeted as victims by their peers. Likewise, the relationship could be circular in that children with poor health or altered HPA axis activation are targeted as victims leading to
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worse health outcomes or more pronounced dysregulation. Future work is needed to determine whether causal paths exist. 4.4. Concluding comments We expect a developmental trend where the links between victimization, cortisol, and physical health become more prominent as children progress through adolescence. Given that peer victimization peaks during early adolescence, it is possible that the negative effects of victimization have not yet fully impacted the HPA axis. Moreover, alterations to the HPA axis do not occur overnight (Putnam, 2007). A shift in cortisol production is somewhat expected given that elevated cortisol is beneficial in the short-term (i.e., mobilize resources) whereas chronically high levels of cortisol have detrimental effects on health (e.g., suppressed immune functioning). It is plausible that the trends found in the current sample mark the beginning of a shift in cortisol production for victimized adolescents. For approximately 10–30% of children, peer victimization is not merely part of ‘‘normal everyday kid’’ behavior. The current study advances the field, in part, by demonstrating that the negative effects of victimization are not solely confined to psychological and mental health outcomes. Rather, the findings provide early evidence that peer victimization in adolescence is linked with altered HPA axis functioning. Moreover, there are links between victimization, cortisol, and health problems that call for further exploration. We postulate that the link between peer victimization and poor health is due, in part, to altered biological functioning. The results from this project are exciting in that it moves the field another step closer to understanding why the link between peer victimization and negative health outcomes exists. Acknowledgments This paper was funded by a grant awarded to Jennifer M. Knack and Lauri A. Jensen-Campbell by Timberlawn Psychiatric Research Foundation, Inc. Data reported in this paper were collected as part of Jennifer M. Knack’s dissertation. We thank Melissa Muenzler for conducting the cortisol assays and Shaun Campbell for his computer assistance. We also thank members of the UTA Personality and Social Behavior Research Lab, especially Aubrey Thompson, Sarah Ziegler, Cintly Celis-de Hoyos, Tony Kutcha, and Ana Gonzalez. Special thanks to the principals, schools, and organizations in the Dallas/Fort Worth area for working with us. References Adam, E. K. (2006). Transactions among adolescent trait and state emotion and diurnal and momentary cortisol activity in naturalistic settings. Psychoneuroendocrinology, 31, 664–679. Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park, CA: Sage. Bjorkqvist, K., Lagerspetz, K. M. J., & Osterman, K. (1992). The direct and indirect aggression scales. Finland: Abo Akademi University. Crick, N. R., & Grotpeter, J. K. (1995). Relational aggression, gender, and socialpsychological adjustment. Child Development, 66, 710–722. Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355–391. Dougall, A. L., & Baum, A. (2001). Stress, health, and illness. In A. Baum, T. A. Revenson, & J. E. Singer (Eds.), Handbook of health psychology (pp. 321–337). Mahwah, NJ: Lawrence. Egan, S. K., & Perry, D. G. (1998). Does low self-regard invite victimization? Developmental Psychology, 34, 299–309. Greco, L. A., Freeman, K. E., & Dufton, L. (2007). Overt and relational victimization among children with frequent abdominal pain: Links to social skills, academic functioning, and health service use. Journal of Pediatric Psychology, 32, 319–329. Hamilton, L. D., Newman, M. L., Delville, C. L., & Delville, Y. (2008). Physiological stress response of young adults exposed to bullying during adolescence. Physiology and Behavior, 95, 617–624.
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Hansen, A. M., Hogh, A., & Persson, R. (2011). Frequency of bullying at work, physiological response, and mental health. Journal of Psychosomatic Research, 70, 19–27. Hansen, A. M., Hogh, A., Persson, R., Karlson, B., Garde, A. H., & Orbaek, P. (2006). Bullying at work, health outcomes, and physiological stress response. Journal of Psychosomatic Research, 60, 63–72. Harris, J. R. (1995). Where is the child’s environment? A group socialization theory of development. Psychological Review, 102, 458–489. Hartup, W. W. (1996). The company they keep: Friendships and their developmental significance. Child Development, 67, 1–13. Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., et al. (2000). Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA, 284, 592–597. Hodges, E. V. E., & Perry, D. G. (1996). Victimization is never just child’s play. National School Safety Center News Journal, 4, 7. Johnson, D. M., Delahanty, D. L., & Pinna (2008). The cortisol awakening response as a function of PTSD severity and abuse chronicity in sheltered battered women. Journal of Anxiety Disorders, 22, 793–800. Kirschbaum, C., Pirke, K. M., & Hellhammer, D. H. (1993). The ‘‘Trier Social Stress Test’’: A tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28, 76–81. Kliewer, W. (2006). Violence exposure and cortisol responses in urban youth. International Journal of Behavioral Medicine, 13, 109–120. Knack, J. M. (2009). Influence of peer victimization and social support on cortisol production. Dissertation Abstracts International: Section B: The Sciences and Engineering, 70(5-B), 3205. Knack, J. M., Iyer, P. A., & Jensen-Campbell, L. A. (in press). Not simply ‘‘in their heads:’’ Being bullied predicts health problems above and beyond known individual differences associated with victimization and health. Journal of Applied Social Psychology. Kudielka, B. M., Hellhammer, D. H., & Wust, S. (2009). Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge. Psychoneuroendocrinology, 34, 2–18. Ladd, G. W., & Kochenderfer-Ladd, B. (2002). Identifying victims of peer aggression from early to middle childhood: Analysis of cross-informant data for concordance, estimation of relational adjustment, prevalence of victimization, and characteristics of identified victims. Psychological Assessment, 14, 74–96. Lovallo, W. R., & Gerin, W. (2003). Psycholphysiological reactivity: Mechanisms and pathways to cardiovascular disease. Psychosomatic Medicine, 65, 36–45. McBurnett, K., Lahey, B. B., Rathouz, P. J., & Loeber, R. (2000). Low salivary cortisol and persistent aggression in boys referred for disruptive behavior. Archival of General Psychiatry, 57, 38–43. McEwen, B. S. (2000). The neurobiology of stress: From serendipity to clinical relevance. Brain Research, 886, 172–189. Nishina, A., Juvonen, J., & Withkow, M. R. (2005). Sticks and stones may break my bones, but names will make me feel sick: The psychosocial, somatic, and scholastic consequences of peer harassment. Journal of Clinical Child and Adolescent Psychology, 34, 37–48. Olweus, D. (1993). Bullying at school: What we know and what we can do. Cambridge, MA: Blackwell (ED 384 437).
Paris, J. J., Franco, C., Sodano, R., Freidenberg, B., Gordis, E., Anderson, D. A., et al. (2009). Sex differences in salivary cortisol in response to acute stressors among healthy participants, in recreational or pathological gamblers, and in those with posttraumatic stress disorder. Hormones and Behavior. doi:10.1016/ j.yhbeh.2009.06.003. Pervanidou, P. (2008). Biology of post-traumatic stress disorder in childhood and adolescence. Journal of Neuroendocrinology, 20, 632–638. Preacher, K. J., & Hayes, A. F. (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods, 40, 879–891. Putnam, F. W. (2007). The psychobiological effects of sexual abuse: A 20 year prospective study. In Second International Conference of Child Abuse and Neglect, the Facts, May 9-10, Leuven. Raudenbush, S. W., & Bryk, A. S. (2002). Hierarchical linear models (2P Nd P ed.). Thousand Oaks, CA: Sage. Roy, M. P. (2004). Patterns of cortisol reactivity to laboratory stress. Hormones and Behavior, 46, 618–627. Rudolph, K. D., Troop-Gordon, W., & Granger, D. A. (2010). Peer victimization and aggression: Moderation by individual differences in salivary cortisol and alphaamylase. Journal of Abnormal Child Psychology, 38, 843–856. Snijders, T., & Bosker, R. (2002). Multilevel analysis: An introduction to basic and advanced multilevel modeling. Thousand Oaks, CA: Sage Publications. Spear, L. P. (2000). Neurobehavioral changes in adolescence. Current Directions in Psychological Science, 9, 111–114. Solberg, M. E., & Olweus, D. (2003). Prevalence estimation of school bullying with the Olweus bully/victim questionnaire. Aggressive Behavior, 29, 239–268. Teicher, M. H., Samson, J. A., Sheu, Y. S., Polcari, A., & McGreenery, C. E. (2010). Hurtful words: Association of exposure to peer verbal abuse with elevated psychiatric symptom scores and corpus callosum abnormalities. American Journal of Psychiatry, 167, 1464–1471. Tops, M., Riese, H., Oldehinkel, A. J., Rijsdijke, F. V., & Ormel, J. (2008). Rejection sensitivity relates to hypocortisolism and depressed mood state in young women. Psychoneuroendocrinology, 33, 551–559. Totura, C. M. W., Green, A. E., Karver, M. S., & Gesten, E. L. (2009). Multiple informants in the assessment of psychological, behavioral, and academic correlates of bullying and victimization in middle school. Journal of Adolescence, 32, 193–211. Vaillancourt, T., Duku, E., Decatanzaro, D., Macmillan, H., Muir, C., & Schmidt (2008). Variation in hypothalamic-pituitary-adrenal axis activity among bullied and non-bullied children. Aggressive Behavior, 34, 294–305. Van den Bergh, B. R. H., & Van Calster, B. (2009). Diurnal cortisol profiles and evening cortisol in post-pubertal adolescents scoring high on the children’s depression inventory. Psychoneuroendocrinology, 34, 791–794. Walker, E. F., Walder, D. J., & Reynolds, F. (2001). Developmental changes in cortisol secretion in normal and at-risk youth. Development and Psychopathology, 13, 721–732. Williams, K., Chambers, M., Logan, S., & Robinson, D. (1996). Association of common health symptoms with bullying in primary school children. British Medical Journal, 3, 17–19.
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Brain and Cognition journal homepage: www.elsevier.com/locate/b&c
Worse than sticks and stones? Bullying is associated with altered HPA axis functioning and poorer health Jennifer M. Knack a,⇑, Lauri A. Jensen-Campbell b,⇑, Andrew Baum b a b
Clarkson University, 8 Clarkson Ave Potsdam, NY 13699-5825, United states University of Texas at Arlington, 501 S. Nedderman Drive Arlington, TX 76019-0528, United States
a r t i c l e
i n f o
Article history: Available online 11 August 2011 We dedicate this paper to Dr. Andy Baum whose mentorship and friendship has significantly impacted our lives and research; we will always remember you Keywords: Peer victimization Bullying Cortisol HPA axis Adolescence
a b s t r a c t Adolescents (N = 107; M = 12.23 years, SD = 1.09 months) participated in a two-part study examining peer victimization, neuroendocrine functioning, and physical health. In phase 1, adolescents completed questionnaires assessing peer victimization and health. They returned for phase 2 which consisted of two sessions. In session 1, adolescents learned to collect salivary cortisol samples; they collected four samples over 2 non-sports school days. In session 2, adolescents completed the Trier Social Stress Test (TSST) in which they prepared and delivered a speech while cortisol was collected. Peer victimization predicted poor health outcomes and a flattened cortisol awakening response (CAR); this CAR was linked with health problems. During the TSST, victims reported more stress and exhibited altered cortisol levels. Higher cortisol immediately after the stressor and lower cortisol 30 min after the stressor were associated with more health problems. This study provides evidence that the relationship between peer victimization and poor physical health may be explained by differences in neuroendocrine functioning. Ó 2011 Elsevier Inc. All rights reserved.
1. Introduction ‘‘Sticks and stones may break my bones but words will never hurt me.’’ Peer victimization, defined as being the habitual target of peers’ aggression, is not a new phenomenon. Also known as being bullying, peer victimization is intended to be hurtful to another person of lesser status (Olweus, 1993). Contrary to the notion that words do not hurt, both physical and relational forms of peer victimization have negative developmental and mental health outcomes in adolescence including poorer school performance, higher school absences, more adjustment problems and suicide attempts for adolescents who are bullied compared to those who are not bullied (e.g., Egan & Perry, 1998; Hodges & Perry, 1996). Bullied individuals also experience more physical health problems than those who are not bullied (Greco, Freeman, & Dufton, 2007; Williams, Chambers, Logan, & Robinson, 1996). Moreover, fall reports of victimization predict worse physical health in the spring whereas poor physical health in the fall does not predict increased victimization in the spring (Nishina, Juvonen, & Withkow, 2005; Knack, Iyer, &
⇑ Corresponding authors. E-mail addresses: [email protected] (J.M. Knack), [email protected] (L.A. Jensen-Campbell). 0278-2626/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2011.06.011
Jensen-Campbell, in press). Taken together, the literature suggests being bullied is associated with physical health problems. However, little research has examined why such a link exists. The emergence of physical health problems following repeated experiences of bullying suggests that changes in biological processes may occur as a result of being bullied; these biological changes may be an underlying mechanism that can explain the link between experiences of victimization and poor physical health. As a stressor, bullying would be expected to have predictable effects including altered cortisol production (Hansen, Hogh, & Persson, 2011; Hansen et al., 2006; Vaillancourt et al., 2008). The central goal of this study was to examine whether altered HPA axis activation may help explain why the link between peer victimization and poor health exists. 1.1. Stress and health Stress has a direct effect on a number of physiological systems including the HPA axis (e.g., Dougall & Baum, 2001). Cortisol, one of the end products of HPA activation, can be beneficial in response to acute stressors because cortisol helps mobilize the body to deal with the stressor. However, chronically high levels of cortisol can be maladaptive (e.g., McEwen, 2000; Vaillancourt et al., this issue). Surprisingly, in adolescents (Vaillancourt et al., 2008) and adults (Hansen et al., 2006, 2011) peer victimization has been associated with lower diurnal cortisol levels than in those not victimized.
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These findings are consistent with the link between stressors (e.g., childhood maltreatment or PTSD) and lower cortisol levels (Johnson, Delahanty, & Pinna, 2008; Pervanidou, 2008). Researchers have begun to focus on the cortisol awakening response (CAR). The CAR is defined by an increase in cortisol roughly 20–30 min after waking and is the peak in the diurnal pattern; cortisol levels gradually drop throughout the remainder of the day. Some researchers conceptualize the awakening response as a ‘‘cortisol mobilization response’’ during which the body mobilizes its resources for the day (e.g., Tops, Riese, Oldehinkel, Rijsdijke, & Ormel, 2008, p. 553). Following this theory, we predict adolescents with a blunted CAR will be less physiologically equipped to handle threats to their immune system resulting in more reports of health problems. Acute social stressors have been found to increase cortisol reactivity. In a meta-analysis of 208 studies, Dickerson and Kemeny (2004) found that uncontrollable tasks involving a social evaluative threat produced a larger cortisol change and had a longer recovery time compared to uncontrollable tasks without a social evaluative threat. One such common laboratory social stressor, the Trier Social Stress Test (TSST), has repeatedly been used to activate the HPA axis (Kirschbaum, Pirke, & Hellhammer, 1993). As part of the TSST, participants give a 5 min speech and then count backward by 13 from a large number (e.g., 1379). Throughout the TSST, salivary cortisol samples are collected. These acute periods of social stress have produced increases in levels of salivary cortisol. We found only two studies to date that examined peer victimization and cortisol reactivity (see Hamilton, Newman, Delville, & Delville, 2008; Rudolph, Troop-Gordon, & Granger, 2010); we expect acute social stressors are likely to elicit different HPA responses in early adolescents who are bullied versus those who are not bullied. Social stressors may be especially influential during adolescence given the number of physiological changes that occur (e.g., puberty, alterations in HPA axis activity, rapid brain maturation; Spear, 2000; Walker, Walder, & Reynolds, 2001). Moreover, bullying should be especially evocative and disruptive as adolescents place more emphasis on peer relationships rather than primarily relying on parents for companionship and support (Harris, 1995; Hartup, 1996; Teicher, Samson, Sheu, Polcari, & McGreenery, 2010). Adolescence may be a time of increased vulnerability to stressful events which ultimately lead to a change in how stress is experienced (Walker et al., 2001). 1.2. Current study This research examined whether HPA activation, as assessed by repeated assay of salivary cortisol levels, may be a mechanism underlying long-term physical health effects of peer victimization. First, we expected that peer victimization would predict poorer physical health for those victimized than those not victimized. Second, we expected being bullied would influence cortisol levels; that is, victimized adolescents would exhibit lower patterns of daily cortisol than would nonvictimized adolescents and that victimization would be related to a flattened CAR. In addition, we anticipated that victimized adolescents would have a different cortisol reaction to an acute social stressor compared to nonvictimized adolescents. Given that this paper was one of the first studies to examine bullied adolescents’ stress reactivity, we did not make specific predictions about the direction of the effect. Third, we predicted these differences in cortisol would predict poorer physical health for victimized adolescents compared to nonvictimized adolescents. We examined whether diurnal pattern and cortisol reactivity predicted health outcomes. Finally, we expected daily cortisol levels and cortisol reactivity would mediate the victimization-health link.
2. Method 2.1. Participants Adolescents (5–8th grades) and their parent participated in a two-part research study on friendship, peer relationships, and health (N = 107). Participants were girls (56.1%) and boys (43.9%) in the Dallas/Fort Worth area (M = 12.23 years; SD = 1.09 months). The racial composition included 66.4% Caucasian, 15.9% Hispanic/Latino, 11.2% Black/African American, 3.7% Asian, 1.9% American Indian/Alaskan Native, and 0.9% Hawaiian/Pacific Islander participants. Information on socioeconomic status was not collected. 2.2. Participant recruitment We mailed home project information to people who were randomly selected from mailing lists from local school districts and private child organizations. We also recruited adolescents from a large public school, several small private schools, a local dance company, and several summer camps. We targeted adolescents with meaningful histories of being bullied (i.e., adolescents who scored at least one standard deviation above the mean on victimization). Adolescents were paid $5.00 and entered into a raffle for participating in Phase I. Adolescents and parents were each paid a total of $40.00 for participating in two sessions in Phase II. 2.3. Assessment of victimization 2.3.1. Children’s self-experiences questionnaire – self- and parentreport (CSEQ-SR, CSEQ-PR) The CSEQ-SR/CSEQ-PR assessed peer-related instances of victimization (Crick & Grotpeter, 1995). This survey measured physical and relational victimization (see Knack, 2009 for details). Each subscale was comprised of five items which measured the frequency adolescents experienced an event on a scale of 1 (never) to 5 (all the time). High reliability was found for both self and parental reports of overt (a = 0.81, 0.84) and relational victimization (a = 0.84, 0.86). 2.3.2. Direct and indirect aggression scales – victim version (DIAS) The DIAS (Bjorkqvist, Lagerspetz, & Osterman, 1992) is a 24item measure comprised of three subscales that assess frequency of physical, verbal, and indirect aggression/victimization. The questions were answered on a Likert-type scale ranging from 1 (never) to 5 (very often). High reliability was found for self and parental reports of physical (a = 0.85, 0.89), verbal (a = 0.86, 0.90), and indirect (a = 0.89, 0.91) victimization, respectively. 2.3.3. Creating the victimization composite Adolescents and parents completed assessments of the adolescent’s experiences of victimization given that multiple informants of bullying are advantageous in obtaining the best estimates of bullying (Ladd & Kochenderfer-Ladd, 2002; Totura, Green, Karver, & Gesten, 2009). The subscales were correlated across parent- and self-reports (range of correlations = 0.25–0.54, M = 0.40). No systematic differences were found between types of bullying and cortisol by type of victimization or rater, so we created an overall composite of bullying comprised of all parent- and self-reports for all the victimization subscales to remove biases associated with child- versus parent-raters. We used a variable-centered approach (i.e., treating victimization as a continuous variable) and a person-centered approach (i.e., creating dichotomized groups based on victimization scores).
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We included the person-centered approach because other researchers (e.g., Solberg & Olweus, 2003; Vaillancourt et al., 2008) treated their victimization data as distinct groups; we wanted our data to be easily comparable with previous work. However, creating distinct groups reduces statistical power and the richness of the data set (Aiken & West, 1991). We therefore also included a variable-centered approach. To create groups of victimized versus nonvictimized adolescents we conducted agglomerative hierarchical cluster analyses with victimization measures as our clustering variables and chose a two-cluster solution.1 On the second step, we used k-cluster means analysis with normalized Euclidean distance as the distance metric to confirm the two cluster group solution. Using McNemar’s test, there were no significant changes in group membership between the two classification methods, p = 0.50. The victimized group (n = 31) was significantly more victimized (M = 0.99, SD = 0.43) than the nonvictimized group (n = 76; M = 0.04, SD = 0.39) on the overall victimization composite, F(1, 105) = 234.85, p < 0.01, g2 = 0.69.
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2.7. Procedure In phase one, adolescents completed surveys either at school or online assessing peer victimization and health problems. Adolescents and their parent returned to the laboratory for phase two (which consisted of two parts). During session one, adolescents and their parents completed several questionnaires (e.g., health) and learned how to collect saliva samples and how to use a Palm Pilot. Adolescents were instructed to collect four saliva samples over each of two non-sport school days immediately upon waking, 30 min after waking, immediately upon returning home from school, and 30 min before going to bed. Session two was held between 4:00 pm and 7:00 pm to control for diurnal cycles. Parents completed several questionnaires about their child’s social experiences and health. Adolescents then completed a modified version of the TSST in which they had 10 min to prepare for a 5 min speech (see Knack, 2009 for details). After the speech, adolescents completed the post-TSST survey. Four saliva samples were collected during the TSST.
2.4. Physical health assessments 3. Results A health survey was used to assess how frequently and severely adolescents experienced health problems linked with stress (e.g., stomach aches, flu, mouth sores, sore throats, fatigue). Fourteen Likert-type questions ranging from 1 (not at all) to 4 (all the time) assessed the frequency of symptoms (a = 0.72), and 14 Likert-type questions ranging from 1 (does not hurt at all) to 4 (unbearable pain) assessed the severity of symptoms (a = 0.67). This survey also measured of how often adolescents went to the school nurse and doctor (a = 0.74). Next, The Abdominal Pain Index consisted of five Likert-type questions that assessed experiences of abdominal pain over the past 2 weeks. Questions examined the frequency of abdominal pain, length of the pain, and intensity of the pain. Only adolescents completed this questionnaire, a = 0.86. Several composites of parent- and self-reports served as measures of health including (1) frequency of health problems; (2) severity of health problems; (3) frequency of adolescent’s visits to the school nurse/doctor; (4) abdominal pain; and (5) all health problems.
3.1. Does peer victimization predict poorer health outcomes? We expected peer victimization would predict physical health. In a series of regression analyses using a continuous composite of peer victimization, victimization was associated with more frequent and severe health problems, increased abdominal pain, and more frequent health visits (ts(105) = 7.31, 6.76, 4.98, 3.86, p < 0.01, sr2 = 0.34, 0.30, 0.19, 0.12, respectively). 3.2. Does being victimized influence the daily diurnal pattern of cortisol production? We expected victimized adolescents would show lower daily levels of cortisol than their non-victimized peers, especially in the morning (i.e., a flattened CAR). See Fig. 1 for cortisol diurnal patterns. We conducted multi-level modeling (Raudenbush & Bryk,
2.5. Experimental questionnaires 2.5.1. Trier Social Stress Test (TSST) post-survey questionnaire An 18-item survey comprised of Likert-type questions ranging from 1 (not at all) to 7 (very much) was administered after the TSST. First, we created a composite score for how accepted adolescents felt while giving their speech (e.g., ‘‘did you feel liked during the task?’’), a = 0.85. Second, we created a composite score for stress by averaging how stressful and challenging adolescents viewed the task (r = 0.62, p < 0.001). We also examined how evaluated and in control participants felt during the speech. 2.6. Cortisol data collection and analysis Cortisol samples were collected in salivettes (Starstedt™) nested tubes following standard collection procedures (see Knack, 2009 for details) and tested with salivary cortisol kits from Salimetrics (State College, PA). Palm Pilots recorded the date and time and prompted the adolescent to ensure samples were collected correctly When examining a subsample of participants (n = 72) we found a mean correlation of 0.99 between the Palm Pilot times and the times recorded on the cortisol tubes (range: 0.45–1.00). 1 We also examined the three-factor solution for completeness. The fit of this solution was not acceptable based on the K-mean cluster results and McNemar’s test.
Fig. 1. Daily diurnal salivary cortisol patterns during two school days.
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2002; Snijders & Bosker, 2002) using a two level model with variations in change parameters in cortisol levels within a child at level 1 and variation among children on victimization at level 2 (i.e., cortisol assessments were nested within the adolescent). On the first step, we calculated regression equations that estimated the diurnal pattern based on time of assessment. In addition to the linear trend for time of day predicting cortisol levels, we also modeled the quadratic function for time since diurnal pattern often takes a quadratic shape.2 In the second step, the first-step regression coefficients (both b0 and b1) were regressed on the level of victimization of the child (see Raudenbush & Bryk, 2002). We report analyses for standardized victimization scores which produced identical results to analyses using unstandardized centered scores. There was an overall linear decline in cortisol throughout the day (t(769) = 38.60, p < 0.001) and a victimization linear slope interaction, t(769) = 2.13, p < 0.05. For high victimization levels, the slope was not as steep as it was for medium and low levels of victimization (bs = 0.98, 0.93, 0.87 for low, medium, and high levels, respectively, ts > 25.88, ps < 0.01). There was also an overall quadratic function of the slope (t(769) = 2.67, b = 0.10, p < 0.01) and a victim quadratic interaction (t(769) = 2.20, p < 0.05). When victimization was at low levels, the quadratic function was strong, t(769) = 3.52, b = 0.20, p < 0.01. When victimization was at high levels, there was no quadratic slope, t(769) = 0.18, b = 0.01, ns. We then examined differences between time 1 and time 2 to specifically look at the CAR. We found a significant linear increase from time 1 (i.e., upon waking) to time 2 (i.e., 30 min later), t(392) = 8.67, b = 0.21, p < 0.01, and a victimization linear function interaction, t(392) = 3.36, b = 0.08, p < 0.001. The CAR was significant for low victimized adolescents, t(392) = 8.06, b = 0.29, p < 0.001; for high victimized adolescents, the slope was weaker, t(392) = 4.29, b = 0.13, p < 0.001. In summary, victimized adolescents exhibited a flattened CAR. We then examined the change in cortisol from time 2 (i.e., 30 min after waking) to time 3 (after school). As expected, we found a drop in cortisol, t(375) = 33.24, b = 1.09, p < 0.001, and a victimization slope interaction, t(375) = 2.91, b = 0.10, p < 0.01. For high levels of victimization, the slope was weaker, t(375) = 21.90, b = 1.00, p < 0.001, whereas for low levels of victimization, the slope was stronger, t(375) = 24.88, b = 1.19, p < 0.001. That is, although the slope was significant for both groups, adolescents who are not victimized evidenced a sharper drop in cortisol from time 2 to time 3 than did victimized adolescents. From time 3 (i.e., after school) to time 4 (i.e., 30 min before bed) there was an overall linear trend, t(372) = 10.55, b = 0.73, p < 0.001; however, we did not find a victimization linear function, t(372) = 1.75, b = 0.13, p = 0.08. Finally, we collapsed across time points from day 1 and day 2 to get average levels of cortisol at each of the four time points throughout the day. Using independent sample t-tests, we found that victimized adolescents had significantly lower cortisol levels at 30 min after waking (t(105) = 2.71, p < 0.01) and 30 min before bed (t(105) = 2.03, p = 0.045).
in cortisol levels within children (level 1). We were most interested in whether health was related with the CAR. There was an overall health linear time interaction, t(769) = 1.93, p = 0.05, but no health quadratic time interaction, t = 0.09, ns. When the child had few health problems, the expected increase in cortisol from T1 to T2 was significant, t(392) = 8.04, b = 0.28, p < 0.05. When the child had more health problems, the slope from T1 to T2 was significant, t(392) = 4.61, b = 0.14, p < 0.05, but the magnitude was smaller. That is, the expected CAR was associated with better physical health. Other areas of the curve were not related with health. 3.4. Does CAR mediate the link between victimization and health problems? It is possible that the CAR mediates the link between victimization and health. We controlled for age, internalizing problems, and the area under the curve with reference to 0 or ground (AUCg). Following procedures outlined in Preacher and Hayes (2008), we found victimization was related to the average slope of CAR, t(107) = 2.08, p = 0.04, b = 0.16. In addition, the slope was marginally related to health problems, t(107) = 1.73, p = 0.87, b = 0.20. The direct path of victimization to health problems was still significant after controlling for the CAR slope, t(107) = 4.90, p < 0.01, b = 0.45. Using bootstrapping procedures with 1000 bootstraps, there was a marginally significant indirect effect (see Fig. 2). 3.5. Are victimized adolescents with health problems showing the greatest CAR flattening? We expected that victimized adolescents who reported poor physical health would have a flatter CAR than victimized adolescents who did not have poor health. As such, we examined whether victimization amplified this health-cortisol association for CAR. Again we ran a multi-level model. There was a victimization health time interaction, b = 0.09, t(388) = 4.10, p < 0.01. Using procedures outlined by Aiken and West (1991), we conducted simple effects analyses. At high levels of victimization and high levels of health problems, the CAR slope was significant but smallest in magnitude, b = 0.14, t(388) = 4.65, p < 0.01; when victimization and health problems were low, the relation between time and cortisol was nearly twice the magnitude, b = 0.24, t(288) = 6.32, p < 0.01. Interestingly, when there was either high victimization/low health problems or low victimization/high health problems, the magnitude of the CAR slope was the largest, bs = 0.37, 0.39, ts(388) = 4.96, 5.32, ps < 0.01. Using a person-centered approach, we explored classifications of our victims and non-victims on health. There were two health groups; 51 adolescents reported having good health, and 56
3.3. Do daily diurnal cortisol levels predict physical health outcomes? We expected daily cortisol levels would predict health outcomes. Using multi-leveling modeling, we again constructed a two level model. For this analysis, we used an overall composite of health problems among children (level 2) to predict variations 2 Cubic and higher trends were examined as well. They were dropped from the final model because they were not significant. Moreover, their variance inflation factors were not acceptable (>10.0).
Fig. 2. CAR slope mediates link between peer victimization and health problems.
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adolescents reported stress-related health problems. Of the 51 adolescents who reported good health, only 3 were classified as victims (compared to the 28 victims who reported stress-related health problems). That is, over 90% of victims reported having stress-related health problems. Conversely, only 36% of nonvictimized children reported have stress-related health problems. This differential pattern of health problems for victims and nonvictims was statistically significant, v2(1) = 25.25, p < 0.001. Taking these patterns of results together, our research suggests that the majority of bullied adolescents report health problems; moreover, adolescents who are high on victimization and health problems show the flattest CAR response. 3.6. Does being victimized influence self-reported reactions to the TSST? We examined correlations between victimization and self-reported reactions to the TSST. Adolescents who were victimized reported feeling less accepted during the TSST and that the TSST was more stressful than non-victimized adolescents (rs = 0.20, 0.28, ps < 0.05, respectively). Conversely, victimized and nonvictimized adolescents felt similarly evaluated and perceived similar degrees of control (rs = 0.09, 0.18, ns, respectively) during their speech. 3.7. Does being victimized influence cortisol reactivity during the TSST? Next, we examined whether victimization predicted cortisol levels during the TSST. There was no overall main effect for time, b = 0.02, t(404) = 1.35, p = 0.18. However, there was an overall victim time interaction for cortisol, b = 0.04, t(404) = 2.41, p < 0.02. To explore this trend, we examined changes in slope between time points. There was no evidence that victimization influenced the slope between T1 and T2 (t(205) = 0.29, p = 0.78). There was a marginally significant increase in cortisol from T2 to T3 (t(199) = 1.79, p = 0.074); however, there was no victim time interaction, t(199) = 0.04, ns. When examining the change in slope from T3 to T4, there was a victim time interaction for cortisol, t(195) = 2.95, p < 0.01. When victimization was high, there was a significant decrease in cortisol between T3 and T4, t(195) = 2.32, p = 0.02. When victimization levels were low, there was marginal increase in cortisol, t(195) = 1.86, p = 0.06. Overall, the pattern suggested that cortisol increased from T2 and T3 for both victims and non-victims. However, victims showed a decrease in cortisol between T3 and T4 whereas nonvictims showed a continued increase in cortisol. Using a person-centered approach and a repeated measures analysis, we examined this pattern to determine whether victimization predicted cortisol levels across the TSST (controlling for age and sex). There was an overall cubic effect for time predicting cortisol, F(1, 102) = 8.52, p < 0.01, g2 = 0.08. There was a significant quadratic victimization assessment interaction (F(1, 102) = 4.72, p < 0.03, g2 = 0.04) again indicating that the pattern of cortisol production throughout the TSST differed for victimized and nonvictimized adolescents (see Fig. 3). We then conducted simple effects analyses in which we examined whether levels of sequential cortisol levels differed (i.e., T1 versus T2, T2 versus T3, T3 versus T4). There was an overall increase in cortisol from T1 to T2, F(1, 102) = 4.60, p < 0.01. There was no victimization time interaction, F(1, 102) = 0.57, ns. There was no increase in cortisol from T2 and T3, F(1, 102) = 0.54, ns. There was also no victimization time interaction, F(1, 102) = 0.33, ns. There was no overall change in cortisol from T3 to T4, F(1, 102) = 2.42, p = 0.12. However, there was a significant victimization time interaction, F(1, 102) = 5.00, p < .05, g2 = 0.047; there was a significant increase in cortisol from T3
Fig. 3. Cortisol reactivity for victimized and nonvictimized adolescents during the TSST.
and T4 for nonvictimized adolescents (F(1, 72) = 6.99, p < 0.01, g2 = 0.09) whereas for victimized adolescents, there was a significant decrease in cortisol (F(1, 27) = 6.98, p < 0.01, g2 = 0.21). 3.8. Does cortisol reactivity during an acute social stressor predict physical health? Using regression, we examined whether adolescents who were more reactive to the TSST (i.e., less able to cope with stressors) would exhibit more health problems. Age, sex, and average daily cortisol were entered on step 1 and the four lab assessment points were entered on step 2. First, cortisol levels at T3 (immediately after delivering speech) predicted more health problems (t(99) = 1.68, p = 0.097, sr2 = 0.03) whereas cortisol levels at T4 (30 min after delivering their speech) negatively predicted health problems (t(99) = 2.21, p = 0.03, sr2 = 0.05). Second, higher cortisol levels at time 3 predicted more frequency health problems (t(99) = 2.28, p < 0.05, sr2 = 0.05) whereas lower cortisol levels at time 4 predicted more frequency health problems (t(99) = 2.16, p < 0.05, sr2 = 0.04). Third, higher cortisol levels at time 3 predicted more frequent visits to the doctor/nurse (t(99) = 2.54, p < 0.01, sr2 = 0.06); lower levels of cortisol at time 4 predicted more frequent office visits (t(99) = 2.89, p < 0.01, sr2 = 0.07). 3.9. Does cortisol reactivity mediate the link between victimization and health? We again used procedures outlined in Preacher and Hayes (2008) to examine whether cortisol during the TSST mediated the link between victimization and health problems. In this analysis, victimization was the predictor, the four lab cortisol assessments were mediators, and frequency of health visits was the outcome measure. Age, sex, daily cortisol levels, and internalizing problems were entered as control variables. Although there was no overall total indirect effect across the four mediators, cortisol levels 30 min after the speech marginally mediated the victimization-health effect when controlling for the other lab assessments of cortisol. Preacher and Hayes (2008) note that it is not only possible but acceptable to find specific indirect effects even when the total indirect effect is nonsignificant. This
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Fig. 4. Do cortisol levels during an acute social stressor mediate the link between victimization and visits to the doctor/nurse?
finding suggests that victimization was related to lower recovery cortisol levels which, in turn, led to more visits to health professionals (see Fig. 4). For acute reactivity, the data suggest that something is responsible for a shift in cortisol and its relationship with health. Up to T4 (i.e., 30 min after giving the speech), the curve is exactly what one would expect; the deviation for victims occurs only at T4. There was no evidence of a mediation effect of cortisol reactivity for frequency or severity of symptoms. 4. Discussion Although research has shown an association between peer victimization and health problems, this link has largely been based on self- and parent-reports. Most studies on the victimization-health link have looked at either health outcomes or cortisol patterns. This study was the first to examine health outcomes and cortisol patterns simultaneously when examining victimization’s influence on health. As expected, more frequent peer victimization was associated with greater frequency and severity of health problems, more visits to health professionals, and more abdominal pain. Notably, peer victimization accounted for large amounts of the variance in health problems (i.e., 34% in frequency of problems, 30% in severity of problems, 12% in frequency of visits to health professionals, and 21% in abdominal pain) suggesting that victimized children may not be avoiding school simply because they want to avoid interacting with their peers. Rather, their absences from school may be due, in part, to actual illnesses. 4.1. Exploring the links between victimization, daily cortisol patterns, and health outcomes Although Vaillancourt et al. (2008) examined the link between daily cortisol and victimization, they included only two assessments per day and did not assess physical health. The current study allowed for better examination of the diurnal pattern by including four assessment points per day for 2 days. We found the expected diurnal pattern for nonvictimized adolescents where cortisol levels peaked 30 min after waking and then decreased over the day. However, victimized adolescents had lower levels of cortisol 30 min after waking and 30 min before bed than nonvictim-
ized adolescents. This finding is consistent with other findings that lower levels of cortisol are linked with peer victimization (Hansen et al., 2006, 2011; Vaillancourt et al., 2008). Lower cortisol levels, specifically hypocortisolism, have also been linked with PTSD (Heim et al., 2000). Our research suggests victimization is not merely typical school-yard behavior or a normal part of growing up. Rather, peer victims have similar diurnal patterns to people who have experienced stressful events (e.g., Kliewer, 2006). We also found evidence for a blunted CAR in victimized adolescents. A flattened CAR has been linked with the occurrence and prevalence of stressors. For example, Tops et al. (2008) found that women with a high fear of negative social evaluation (i.e., higher stress) had a lower CAR than women with a lower fear of negative social evaluation. Moreover, we found that the CAR slope mediated the link between victimization and health problems. Taken together, the data suggest that victimization is linked with a flattened CAR which in turn predicted poorer health. If the ‘‘cortisol mobilization response’’ theory of the CAR response is correct (Tops et al., 2008, p. 553), victimized children (who had a blunted CAR) would be less equipped for biological processes to run efficiently and effectively (e.g., immune responses) leaving the body more susceptible to illness. Additional research is needed to more fully understand how salivary cortisol levels impact health outcomes for victimized adolescents. 4.2. Exploring the links between victimization, cortisol reactivity, and health outcomes Cortisol levels gradually increased over the course of the TSST and peaked 30 min after speech delivery among nonvictimized adolescents, but for victimized adolescents there was a significant drop in cortisol 30 min following their speech delivery. This drop in cortisol was surprising given other researchers have found cortisol levels stay elevated after the TSST. Our findings, however, are similar to those of Roy (2004); lower cortisol levels after a stressful lab task were linked with a higher incidence of real-life stressors prior to participating in the lab task. Taken together, our findings converge with previous research suggesting victimized adolescents are experiencing more daily social stress than nonvictimized adolescents and that this heightened exposure is impacting their HPA
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axis functioning. That said, we are still unsure why cortisol levels dropped for victimized adolescents 30 min after giving their speech. Since it takes time for cortisol to show up in saliva, the last sample should reflect the cortisol response to stress experienced while delivering the speech. It may be that victimized adolescents are less reactive than nonvictimized adolescents in socially stressful situations. Alternatively, victimized adolescents may recover faster after a social stressor than nonvictimized adolescents. To examine this possibility, an additional saliva sample would be needed; our data do not allow us to test these predictions. Research suggests consistent high reactivity is linked with negative mental and physical health outcomes (e.g., Lovallo & Gerin, 2003). We found that peer victimization predicted lower cortisol levels 30 min after delivering the speech which predicted more frequent visits to the doctor. This finding is slightly different to what we expected; we anticipated that initial cortisol reactivity would also mediate the victimization-health link. As discussed above, including an additional saliva sample may help shed light on these findings. It is possible that the sample 30 min after speech delivery may actually reflect early reactivity to the speech rather a recovery response. Future research should investigate this link. 4.3. Limitations and future directions Caution must be exercised in generalizing the results of this study. Due to the small sample size (i.e., 31 victims), our results need to be replicated. Given the low sample size, we did not examine whether types of peer victimization (e.g., relational versus overt) differentially alter HPA axis functioning. We also did not explore whether these links differed by participant sex. However, it is reasonable to expect that sex differences may occur (Kudielka, Hellhammer, & Wust, 2009; Paris et al., 2009); future research should explore sex differences. We did not include a number of psychological controls in our statistical models that are potential confounds with cortisol levels. Previous research found that cortisol levels can be affected by depression (e.g., Van den Bergh & Van Calster, 2009), aggression (e.g., McBurnett, Lahey, Rathouz, & Loeber, 2000), adjustment problems (e.g., McBurnett et al., 2000), puberty (Adam, 2006), and participant sex (Kudielka et al., 2009; Paris et al., 2009). Because we did not find that cortisol was associated with depression or adjustment problems in preliminary analyses, we did not include additional psychological controls in our models. In addition, we did not measure whether adolescents had experienced prior abuse or maltreatment. That being said, we did closely control the collection of cortisol samples. First, all cortisol reactivity samples were collected between 4:00 pm and 7:00 pm to control for diurnal patterns. Second, participants were instructed not to eat or drink 30 min before sampling. Third, diurnal samples were collected on non-sports days to ensure that levels were not inflated due to exercise. Fourth, although we cannot ensure that morning samples were collected immediately upon waking, self-reports of collection times matched the times recorded by the Palm Pilots which suggests that participants followed the instructions. Future research should also record time of waking. Moreover, this study was correlational in nature. Even though the statistical models and theoretical framework imply a clear causal relationship, care must be taken not to interpret the findings as causal since such statements cannot be deduced from correlational studies. Although our theoretical model suggests that being bullied causes HPA axis dysregulation which in turn leads to poor reports of health, alternative explanations are possible. For example, children with altered HPA axis functioning or poor health may be more likely to be targeted as victims by their peers. Likewise, the relationship could be circular in that children with poor health or altered HPA axis activation are targeted as victims leading to
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worse health outcomes or more pronounced dysregulation. Future work is needed to determine whether causal paths exist. 4.4. Concluding comments We expect a developmental trend where the links between victimization, cortisol, and physical health become more prominent as children progress through adolescence. Given that peer victimization peaks during early adolescence, it is possible that the negative effects of victimization have not yet fully impacted the HPA axis. Moreover, alterations to the HPA axis do not occur overnight (Putnam, 2007). A shift in cortisol production is somewhat expected given that elevated cortisol is beneficial in the short-term (i.e., mobilize resources) whereas chronically high levels of cortisol have detrimental effects on health (e.g., suppressed immune functioning). It is plausible that the trends found in the current sample mark the beginning of a shift in cortisol production for victimized adolescents. For approximately 10–30% of children, peer victimization is not merely part of ‘‘normal everyday kid’’ behavior. The current study advances the field, in part, by demonstrating that the negative effects of victimization are not solely confined to psychological and mental health outcomes. Rather, the findings provide early evidence that peer victimization in adolescence is linked with altered HPA axis functioning. Moreover, there are links between victimization, cortisol, and health problems that call for further exploration. We postulate that the link between peer victimization and poor health is due, in part, to altered biological functioning. The results from this project are exciting in that it moves the field another step closer to understanding why the link between peer victimization and negative health outcomes exists. Acknowledgments This paper was funded by a grant awarded to Jennifer M. Knack and Lauri A. Jensen-Campbell by Timberlawn Psychiatric Research Foundation, Inc. Data reported in this paper were collected as part of Jennifer M. Knack’s dissertation. We thank Melissa Muenzler for conducting the cortisol assays and Shaun Campbell for his computer assistance. We also thank members of the UTA Personality and Social Behavior Research Lab, especially Aubrey Thompson, Sarah Ziegler, Cintly Celis-de Hoyos, Tony Kutcha, and Ana Gonzalez. Special thanks to the principals, schools, and organizations in the Dallas/Fort Worth area for working with us. References Adam, E. K. (2006). Transactions among adolescent trait and state emotion and diurnal and momentary cortisol activity in naturalistic settings. Psychoneuroendocrinology, 31, 664–679. Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park, CA: Sage. Bjorkqvist, K., Lagerspetz, K. M. J., & Osterman, K. (1992). The direct and indirect aggression scales. Finland: Abo Akademi University. Crick, N. R., & Grotpeter, J. K. (1995). Relational aggression, gender, and socialpsychological adjustment. Child Development, 66, 710–722. Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355–391. Dougall, A. L., & Baum, A. (2001). Stress, health, and illness. In A. Baum, T. A. Revenson, & J. E. Singer (Eds.), Handbook of health psychology (pp. 321–337). Mahwah, NJ: Lawrence. Egan, S. K., & Perry, D. G. (1998). Does low self-regard invite victimization? Developmental Psychology, 34, 299–309. Greco, L. A., Freeman, K. E., & Dufton, L. (2007). Overt and relational victimization among children with frequent abdominal pain: Links to social skills, academic functioning, and health service use. Journal of Pediatric Psychology, 32, 319–329. Hamilton, L. D., Newman, M. L., Delville, C. L., & Delville, Y. (2008). Physiological stress response of young adults exposed to bullying during adolescence. Physiology and Behavior, 95, 617–624.
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