Psychoneuroendocrinology (2006) 31, 209–215

Altered cortisol awakening response in posttraumatic stress disorder
` Michele Wessaa,*, Nicolas Rohlederb, Clemens Kirschbaumb, Herta Flora

Department of Clinical and Cognitive Neuroscience, Central Institute of Mental Health, University of Heidelberg, J 5, 68159 Mannheim, Germany b Department of Psychology, Technical University Dresden, Zellescher Weg 17, 01069 Dresden, Germany
Received 14 October 2004; received in revised form 2 May 2005; accepted 14 June 2005

Posttraumatic stress disorder; Salivary cortisol; Awakening response

Summary An altered function of the hypothalamic–pituitary–adrenal axis is assumed to be characteristic for Posttraumatic Stress Disorder (PTSD), although there is inconsistent empirical evidence. Only few studies examined the awakening cortisol response and a daytime profile in PTSD. Salivary cortisol levels were measured at seven intervals from awakening until 8 PM in trauma-exposed subjects with (NZ29) and without PTSD (NZ19) and in 15 non-exposed controls. While the three groups did not differ with respect to their first cortisol level immediately after awakening, the expected cortisol increase to awakening 15–60 min later was significantly lower in PTSD patients compared to non-PTSD subjects and healthy controls. This effect remained stable when trauma-exposed subjects with comorbid major depression were excluded from the analysis. A significant negative correlation between the overall cortisol secretion (AUCG) and overall PTSD symptomatology and hyperarousal symptoms was found. The findings are discussed in light of the hypothesis of a counterregulation of hyperarousal symptoms and chronic stress in PTSD. Q 2005 Elsevier Ltd. All rights reserved.

1. Introduction
Alterations in the activity of the Hypothalamic– Pituitary–Adrenal (HPA) axis are thought to be an important factor in the development of stressrelated disorders. In posttraumatic stress disorder a more sensitive negative feedback inhibition, for example, reflected by an increased number and

* Corresponding author. Tel.: C49 621 1703 6306; fax: C49 621 1703 6305. E-mail address: (M. Wessa).

sensitivity of glucocorticoid receptors (Yehuda et al., 1993), is assumed to result in diminished baseline cortisol levels (Yehuda et al., 1996). However, neuroendocrinological studies in PTSD patients yielded contradictory results showing either decreased baseline levels of cortisol (Yehuda et al., 1993), no differences between PTSD patients and controls (Young and Breslau, 2004) or even higher cortisol levels in PTSD patients (Lemieux and Coe, 1995). This conflicting evidence might be related to the fact that the studies were not comparable with respect to sample characteristics that affect HPA axis activity, such as trauma

0306-4530/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.psyneuen.2005.06.010

daily activities. Maercker and Schutzwohl. In a recent study. 1997) to assess psychiatric disorders other than PTSD. The two trauma-exposed groups were not significantly different with respect to the types of trauma they experienced and the time span since trauma onset. All participants completed . (2004) examined the awakening cortisol response and a short daytime profile in a small sample of Bosnian refugees and healthy controls. ¨ Examining the circadian rhythm of cortisol secretion in PTSD patients. the anticipatory (pre stress) and recovery phase (post-stress) of stress). violent crime (NZ12) and sexual assault or rape (NZ3). 2000).1. The PTSD diagnosis was based on the diagnostic criteria of DSM-IV TR (APA. 2. Seven female subjects were on contraceptive medications. 19 non-PTSD and 15 healthy controls) remained for the statistical analyses. the Ger¨ man version of the Center for Epidemiological Studies Depression Scale (CES-D. these subjects were equally distributed among the three groups (c2(2)Z1. drink caffeine. From this original sample two subjects with terminal illness as traumatic event and eight subjects showing incongruent data from the self-report diaries and the electronic monitoring device for the sampling of cortisol were excluded from the analyses. social conflicts. the German Version of the Structured Clinical Interview of DSM-IV (SCID-I. 1991) and the Assessment of General Stress Susceptibility (FSR. these patients remained in the final sample. This instruction was given verbally as well as through 2. German Version: Wittchen et al.. All subjects gave written informed consent and the study was approved by the local ethics committee. Participants were instructed not to smoke. forming an overall stress reactivity score as well as six subscales (stress reactivity related to work overload.2. although the increase in salivary cortisol to awakening provides a simple and reliable means of assessing the dynamic activity of the HPA axis (Prussner et al. Patients diagnosed with major depression and treated with antidepressant medication were excluded in a reanalysis of the cortisol profile. Thus.210 characteristics. 1997). 2003). sex and level of education. eat or brush their teeth in the sampling period. 2. Subjects Participants of the study were 31 trauma-exposed persons with PTSD. Yehuda et al. another five subjects took hypertension-reducing medication. a total sample of 63 subjects (29 PTSD. immediately ¨ after as well as 30. however. Rohleder et al. Wessa et al. As the exclusion of the five subjects with hypertension from the statistical analyses did not reveal a different pattern of results. 1998). Numbrecht. pZ0.2. The healthy controls did not meet any diagnostic criteria for mental disorder. The experienced traumatic events included severe accidents (NZ30). Methods and materials 2.. the present study investigated the awakening response and daytime profile of a larger and with regard to the experienced traumatic event more heterogeneous sample of trauma-exposed subjects with and without PTSD and the relationship of the cortisol response and PTSD symptoms. So far. M. Measures All trauma-exposed subjects completed the German Version of the Impact of Event Scale-Revised (IES-R.. None of the participants met diagnostic criteria for current alcohol or drug abuse/dependence or psychotic disorders. 1500 and 2000 h (short daytime profile). Based on these findings. work failure. no influences of these medications on cortisol secretion have been found. All participants were Caucasian. The questionnaire consists of 29 items. only few studies measured the circadian rhythm of cortisol secretion in PTSD. 45 and 60 min after awakening (awakening response) and at 1100.61). 1997. gender.00. 2005). Hautzinger and Bailer. social evaluation. First et al. 23 trauma-exposed subjects without PTSD and 19 healthy controls. 2004). Jansen and Schlotz. the time since trauma exposure but not PTSD diagnosis itself was found to be positively associated with an increase in saliva cortisol after awakening (Young et al. Germany). They reported lower daytime cortisol levels and no typical cortisol increase after awakening in PTSD patients compared to the controls. The 12 subjects diagnosed with major depression used antidepressant medication. who were matched for age. So far. The latter has been validated in a sample of 975 subjects and has been shown to be a valid and reliable instrument for the assessment of stress reactivity. nicotine and alcohol abuse or medication status (Rasmusson et al. (1996) reported normal cortisol levels in the morning and lower than normal levels in the later evening. HPA axis activity Saliva samples were collected into Salivette tubes (Sarstedt.1. Ten PTSD and 2 non-PTSD subjects had a comorbid major depression. Schulz.

Group differences in the awakening cortisol response between PTSD patients.58)Z6. ns).71.70.72) revealed that the three groups did not differ with regard to baseline cortisol levels immediately after awakening (F(2. 211 2000 h).39. p!.58)Z8. In addition. As comorbid depression was shown to have a significant influence on cortisol secretion. a one-way ANOVA with Bonferroni-corrected post-hoc tests was carried out. number of cigarettes smoked on a usual day or differing wake-up times.01) and nonPTSD subjects (all p!. Statistical analyses Differences in PTSD symptomatology.58)Z9. Thus. sex.001) and higher stress reactivity related to work overload (F(2. Therefore.28.58)Z2. 3Z0. ns) and post-stress situations (post-stress phase: (F(2.58)Z8. the three cortisol levels between awakening and 1 h after awakening were excluded from the AUC calculation. p!.58)Z1. p! . which among other information assessed their sleep duration the night before the sampling procedure.e.58)Z9. awakening profile). 45 and 60 min after awakening. Subjects did not differ significantly in their stress reactivity with regard to work failure (F(2.36. depressive symptoms as well as stress reactivity were calculated by one-way analyses of variance (ANOVAs) with Bonferroni-corrected post-hoc tests. p!. Germany). but that the PTSD patients exhibited a reduced increase of cortisol secretion . AUC values were based on four samples (awakening.24.82. Free cortisol levels in saliva were measured using a commercially available chemiluminescence assay (IBL. the area under curve with respect to baseline cortisol levels (AUCG) was calculated by multiplying the single cortisol samples by the time interval between the sampling points in minutes. PTSD subjects showed significantly more depressive symptoms (F(2. social conflicts (F(2. Clinical data PTSD patients and trauma-exposed subjects without PTSD were significantly different in the overall sum of PTSD symptoms and the symptom clusters re–experiencing. 4 HC) were excluded from the analysis because their selfreported and electronically monitored sampling times were not congruent. these variables were included as covariates in the ANOVAs.05. the pre-stress phase (F(2.23. social evaluation (F(2. trauma-exposed subjects without PTSD and healthy controls were calculated by a one-way repeated measures ANOVA with four within-group levels (baseline immediately after awakening as well as 30. p!. i.11.18.001) as well as overall stress reactivity (F(2.05). 1100. 1 h later. 1500 and 4. Hamburg. 5. For every subject the individual duration between 1 h after awakening and the sampling point at 1100 h was included in the calculation. In addition. Cortisol response PTSD patients showed a significantly lower cortisol awakening response than non-PTSD subjects and healthy controls (group effect: F(2. p!. A significant group by sampling time interaction (F(6. subjects were asked to complete a diary during the sampling period.60)Z 12. Eight subjects (2 PTSD. When repeated-measures ANOVAs revealed significant interactions. In addition to the awakening and day time profile. In addition. Self-reports of wake-up times as well as an electronic monitoring device (MEMS Track Cap.001).001).001). p!. different wake-up times might influence the AUC significantly.001) compared to healthy controls (all p!.180)Z3. Switzerland) were employed to control for any influence of sampling time.Cortisol Awakening Response in PTSD detailed written information accompanying the sampling tubes. 1500 and 2000 h) was performed to compute differences in the subsequent circadian profile of free cortisol levels (short daytime profile). As it is statistically problematic to combine values from dense sampling and infrequent sampling. ns).1. 2 non-PTSD. 3.60)Z8. A repeated measures ANOVA with three within-group levels (1100. Aardex.24. As the individual difference between the sample point 1 h after awakening and 1100 h enters the calculation of the AUC. intake of contraceptive medication. For differences in sleep duration the night before saliva sampling. To control for possible effects of age. the AUC was correlated with PTSD symptomatology using Pearson correlations. p!.60)Z0. one-way ANOVAs at the different sample points and Bonferroni-corrected post-hoc tests were performed. Results 4. Group differences in the AUC were calculated by a one-way ANOVA with Bonferronicorrected post-hoc tests.05). wake-up times were included as a covariate in the statistical analysis of the AUC. the ANOVAs were again computed for trauma-exposed subjects without. avoidance and hyperarousal (Table 1).

4Z60 min after awakening) and daytime profile (5Z1100 h. wake-up times and sleeping hours before the sampling day of the final sample of PTSD patients (NZ29).01.48)Z 5.06.34 (1.09 (0. p!.001 F(2. PTSD vs.73.48)Z7. nonPTSD: p!.05). comorbid depression excluded (PTSD: NZ19.96.60)Z2.01.62) 0.001. However. NPTSD: NZ19) and healthy controls (NZ15). HC: p!. The cortisol increase was significantly smaller in PTSD patients than in trauma-exposed subjects without PTSD and healthy controls (F(2. non-PTSD: p!.09. PTSD vs. The reduced awakening response in PTSD patients compared to both other groups remained when trauma-exposed subjects with comorbid depression were excluded (Fig. PTSD vs. .36. PTSD vs.04.38) 65. PTSD vs. ns F(2. 45 min (F(2.60)Z8. HC: pZ.27) 56.58)Z9.86) F-Value/p-value F(2.49. HC: p!.60)Z12.37) 0704 h (0120 h) 7.06) but a significant increase in nonPTSD subjects (tZK 4.0 (10.75) 0. Table 1 Demographic characteristic.47 (9.05. pZ.62.05).24) 3. p! . trauma-exposed persons without PTSD (NPTSD. NZ 19) and healthy controls (HC.79. range Sex (female/male) PTSD symptoms Overall score Re-experiencing Avoidance Hyperarousal Depression (ADS) Stress reactivity (FSR) Wake-up time M (SD) Sleeping hours before sampling 47. stress reactivity (FSR). p!.60)Z 2. 2Z30 min after awakening.17 p!.78 (0.212 M. p!.23 (1.73 (0.05.22 (0. ns c2Z.4) 19–71 10/9 17. PTSD vs.001 F(1.17.46)Z42.26) 2.23 (1.8) 27–65 13/16 66. Single comparisons showed that non-depressed PTSD patients exhibited a significantly reduced increase of cortisol secretion 30 min after awakening (F(2.05. p!.001).001) and healthy controls (tZK6. HC: p!.23) 54. p!.47 (13. p!.144)Z3. HC: ns) after awakening (Fig.00.05.001 F(2. depression (ADS). p!.46)Z84.01. PTSD vs. Wessa et al. HC: p!. nonPTSD: p!.01.60)Z7. p!.94) 0800 h (0132 h) 7. nonPTSD: p!. Analysis of the short daytime profile revealed no significant difference in the cortisol secretion between PTSD patients and trauma-exposed subjects without PTSD and healthy controls (F(2. PTSD vs. pZ.76 (0. ns F(1. p!.47) 3.40) 1.45.07 (8. PTSD vs. ns 30 min (F(2.25) 1. 60)Z6.46)Z36.01).05. p!.90. PTSD symptoms (IES-R).83) 0.7) 20–67 8/7 – – – – 0.46)Z66. 1(b). NZ15) and (b) traumaexposed subjects with and without PTSD. group!time interaction: F(6. NZ 29).3 (12. group effect: F(2.36.73 (0.05. PTSD vs.48)Z4.41. Paired comparisons showed a trend towards significance for the cortisol increase 30 min after awakening in PTSD patients (tZ2.89 (0.18. p! .60)Z4.72.001 F(1.00 (23.01. p!. HC: pZ.60)Z.51 ( (1. p!. 1). 6Z1500 h and 7Z2000 h) in (a) patients with posttraumatic stress disorder (PTSD. PTSD vs.01.001 F(2.00 (7.60)Z1. the typical cortisol increase after awakening was not completely absent in PTSD patients.10). PTSD vs.001 F(1. 3Z45 min after awakening. p!. non-PTSD: p!.71.95) 0705 h (0123 h) 7.001) and 45 min after awakening (F(2.01) and 60 min (F(2. PTSD vs.96) HC (NZ15) 40.33) NPTSD (NZ19) 48.39. (a) 40 Salivary Cortisol (nmol/l) 35 30 25 20 15 10 5 0 1 2 34 5 6 Healthy controls NPTSD PTSD 7 Time point of saliva collection (b) 40 Salivary Cortisol (nmol/l) 35 30 25 20 15 10 5 0 1 234 5 6 7 Time point of saliva collection Figure 1 Salivary cortisol response to awakening (1Z awakening. PTSD (NZ29) Age (in years) M (SD).32. trauma-exposed subjects without PTSD (NZ19) and healthy controls (NZ15).5 (13. nonPTSD: p!.01).

ns).21).39. one-way ANOVAs of the wakeup-times and the sleeping hours during the night before cortisol sampling showed no significant differences between the three groups (wake-up times: F(2. Some authors (e.40. 7. the analyses where repeated with the covariates age. These covariates showed no significant impact on the reported group effects or interactions. with PTSD patients showing lower values than the nonPTSD subjects (p!. Yehuda et al. Similarly.01). collected only one morning sample and they instructed the subjects to collect that sample within 30 min of awakening. p!. 2005). but has recently also been reported for patients with chronic fatigue syndrome (Roberts et al. cigarette smoking and wake-up times. However.72. separating PTSD patients with comorbid depression from those with ‘pure’ PTSD resulted in different results in Young et al. Discussion In the line with the study by Rohleder et al..g. Yet. intake of contraceptive medication. p!..60)Z 0. however. The finding of a reduced cortisol awakening response in PTSD patients as shown in the present study suggests some important and interesting implications for the development of PTSD and accompanying changes in neurobiology. Young et al. (2004). Among trauma-exposed subjects. sex.’s study: ‘pure’ PTSD patients no longer differed from nonPTSD subjects and healthy controls as it was the case in the present study when we excluded PTSD patients with comorbid major depression. 1997) have suggested ¨ that the typical cortisol increase 30–60 min after awakening usually reflects an enhanced release of ACTH and a lower cortisol awakening response is assumed to be associated with higher glucocorticoid receptor sensitivity. neither with regard to the morning profile nor overall cortisol secretion (AUC). whereas Young et al.. Wolf et al.g. There is strong evidence that the hippocampus is affected in PTSD patients (Bremner et al. (2004) reported elevated cortisol evening levels in PTSD patients compared to nonPTSD subjects and healthy controls.50. the overall PTSD symptom score and the number of hyperarousal symptoms were significantly negatively correlated with the AUCG (overall symptom score: rZK. hyperarousal: rZK. 1996). Confounding variables To control for possible confounding effects. p!. In contrast to the blunted cortisol morning response in PTSD patients.g. Hafizi and Cowen (2003) found significantly greater levels of waking salivary cortisol in recovered depressed patients compared to healthy controls. the two findings are not fully comparable as Young et al.08). avoidance: rZK. Bhagwagar. 2004) and patients with unilateral or bilateral lesions of the hippocampus (Buchanan et al. ns. These contrasting results suggest different neurobiological mechanisms in both disorders despite their overlapping symptomatology. PTSD patients showed a significantly reduced cortisol increase 30–60 min after awakening (awakening response). a relatively robust finding in PTSD research (e. intake of contraceptive medication. in line with our findings and other previous studies (e. the one-point cortisol assessment at a certain time interval after awakening might have led to blurred values. Taking into account our finding of a blunted awakening cortisol response. cortisol secretion during the day and evening was not affected in PTSD patients compared to both other group.. the blunted cortisol awakening response does not seem to be specific for PTSD patients. (2004) found no differences between PTSD patients and trauma-exposed subjects . 213 without PTSD in cortisol levels after awakening. 2004.e. In addition. In contrast to our results. they observed reduced morning cortisol levels in PTSD patients. no reduced cortisol increase after awakening in PTSD patients. cigarette smoking and wake-up time. sleeping hours: F(2.30. 1997).. In our study. sex. However.01) and the healthy controls (pZ.. 2000).Cortisol Awakening Response in PTSD The AUC was significantly different in the three groups (F(2.60)Z5. The correlation between avoidance and re-experiencing symptoms and the AUCG were not significant (re-experiencing: rZK. it is not clear whether the observed hippocampal reduction in traumaexposed subjects with PSTD is a predisposing factor or a result of the illness (Gilbertson et al.60)Z2.23. Yehuda et al. as indicated by the AUC of the morning cortisol profile.01). Neylan and colleagues (2005) found no differences between PTSD patients and trauma-exposed subjects without PTSD in the time course of cortisol.05. This effect remained stable after excluding PTSD patients with comorbid major depression and on antidepressant medication and after controlling for possible confounding variables such as age. In addition. Longitudinal studies are needed to clarify the relationship between hippocampal damage and 6. 1993). Prussner et al. i. baseline cortisol levels immediately after awakening were not significantly different between the three groups...

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