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ORIGINAL ARTICLES |
From the Department of Psychiatry (S.K., T.T.), Department of Radiology (T.K.), Department of Neurology (R.P., H.I., L.H., O.T.), Turku University Hospital, Turku, Finland; and Department of Biostatistics (S.H.), Turku University, Turku, Finland; Department of Psychiatry, Kuopio University Hospital, and University of Kuopio, Kuopio, Finland (K.H., H.V.); School of Public Health, University of Tampere, and Department of Psychiatry, Tampere University Hospital, Tampere, Finland (M.J.).
Address correspondence and reprint requests to Salla Koponen, Department of Psychiatry, Turku University Hospital, PL 52, FI-20521 Turku, Finland. E-mail salla.koponen{at}utu.fi
| ABSTRACT |
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Methods: Fifty-four participants, 67% men, were evaluated after a median of 30 years since TBI. A control group was matched for age, gender, and severity of depression. Alexithymia was measured with the 20-item Toronto Alexithymia Scale (TAS-20). In patients with TBI, axis I psychiatric disorders were assessed with the Schedules for Clinical Assessment in Neuropsychiatry (SCAN, version 2.1), and axis II disorders with the Structured Clinical Interview for DSM-III-R Personality Disorders (SCID-II). MRI examinations were carried out with a 1.5 T MRI scanner.
Results: Alexithymia was significantly more common in patients with TBI than in controls (31.5% versus 14.8%; odds ratio 2.64, 95% confidence interval 1.036.80). None of the variables representing TBI, ie, severity of TBI or the presence, laterality, or location of contusions on MRI, was associated with the TAS-20 total scores. Several current axis I and II psychiatric disorders, particularly organic personality syndrome, were connected to higher TAS-20 scores.
Conclusion: Alexithymia is common, along with psychiatric disorders, in patients with TBI. Both of them may reflect dysfunction of the injured brain. In clinical practice, alexithymic features should be taken into consideration in psychosocial rehabilitation after TBI.
Key Words: alexithymia traumatic brain injury magnetic resonance imaging psychiatric disorders
Abbreviations: MRI = magnetic resonance imaging; TBI = traumatic brain injury; TAS-20 = 20-item Toronto Alexithymia Scale; OR = odds ratio; 95% CI = 95% confidence interval; BDI-13 = 13-item Beck Depression Inventory; DAI = diffuse axonal injury.
| INTRODUCTION |
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As a neurobiological model of alexithymia, a deficit in interhemispheric communication and a dysfunction of the right cerebral hemisphere have been proposed (4). In addition, a disturbance in the participation of the anterior cingulate cortex, one of the essential structures in generating the conscious awareness of feelings, during emotional arousal, has been suggested (5). The size of the right anterior cingulate gyrus has been found to correlate with alexithymia (6). Differences in anterior cingulate and mediofrontal activity during emotional stimuli processing, detected with functional magnetic resonance imaging (fMRI), have been linked to alexithymia (7). In a positron emission tomography study, subjects with alexithymia showed a lower response in the right hemisphere, a higher response in the left hemisphere, and also less activation in the anterior cingulate cortex than controls, when viewing different facial expressions (8). So far, the findings of these individual studies dealing with alexithymia and cerebral functioning seem to be somewhat inconsistent. Parker and Taylor (4) have concluded that "alexithymia is associated, at the very least, with a variation in brain organization."
Many people with traumatic brain injury (TBI) have deficits in the cognitive processing and regulation of emotions. They may present with flattened affect, have difficulties in expressing themselves verbally, become disorganized under stress, and have sudden outbursts without being able to elaborate the cause. On the basis of neurobiological studies, the cingulate gyrus and the corpus callosum, the latter being related to the interhemispheric communication deficit hypothesis, are structures associated with alexithymia (38). On the other hand, they are also regions that can often be damaged in TBI (9,10). Thus, considering the clinical observations and research findings, it can be hypothesized that traumatic changes in the brain could produce alexithymia.
To our knowledge, there are only few reports of alexithymia after TBI. One study dealt with the prevalence of alexithymia in 135 family-practice patients and its association with a self-reported history of head injury (11). Alexithymia was significantly more common in those with a history of TBI (knocked unconscious) (41%), compared with those with mild head injury (knocked dizzy/dazed) (9%) or those without TBI/head injury (10%). A single case study on "organic alexithymia" after TBI has also been published (12). In addition, alexithymia has been studied in 48 patients with stroke: 48% of subjects with right-hemisphere stroke were alexithymic, compared with 22% of subjects with left-hemisphere stroke (13). The more specific location of the lesion had no association with alexithymia.
We have earlier reported the high occurrence of psychiatric disorders in 60 patients with TBI (14). In the present study, our hypothesis was that, on the basis of the above mentioned clinical and research findings, alexithymia is more common in patients with TBI than in a control group from the general population. As several studies have found an association between alexithymia and male gender (1518), older age (15, 16, 19), and depression (17, 20), our study groups were matched for gender, age, and severity of depression. We also assumed that severity of TBI, MRI findings, and current axis I and II psychiatric disorders may modify the prevalence of alexithymia after TBI.
| METHODS |
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Of the original group of 210 patients, 76 had died. The inclusion criteria for the remaining 134 patients were (1) a head trauma severe enough to cause TBI and causing neurological symptoms (including headache and nausea) lasting at least 1 week, and (2) at least 1 of the following: loss of consciousness for at least 1 minute, posttraumatic amnesia for at least 30 minutes, neurological symptoms (excluding headache and nausea) during the first 3 days after injury, or neuroradiologic findings suggesting TBI (eg, skull fracture, intracerebral hemorrhage). The exclusion criteria were (1) neurological illness before TBI, (2) clinical symptoms of a nontraumatic neurological illness that developed after TBI (excluding dementia), (3) insufficient cooperation, or (4) unavailability of medical records.
Of the 134 patients, 13 did not meet the inclusion criteria according to medical records, 1 patient was excluded because of neurological illness before TBI, and 2 patients did not have available medical records. The remaining 118 patients were contacted by mail, and 88 of them replied. Eighty-three of them met the inclusion criteria, but 7 were excluded because of a nontraumatic neurological illness, and 16 refused to participate in the study. Of the remaining 60 subjects, 3 were excluded from the present study because of clinical dementia and 3 because of a missing questionnaire and/or MRI examination, leaving 54 subjects for the study group. Written informed consent was obtained after the procedure had been fully explained. The protocol was approved by the Ethics Committee of Turku University Hospital.
For a control group, 54 subjects were drawn from a general population sample from the District of Kuopio, eastern Finland (17). Table 1 presents the characteristics of the 54 patients with TBI and their controls. They were matched for age, gender, and severity of depression. As the age of the patients was up to 80 years and the age of the controls only up to 64 years, matching was done by aiming at equal median ages in the 2 groups. Matching for depression was carried out by using the 13-item Beck Depression Inventory (BDI-13) (21). The following categories were used: BDI-13 score 0 to 4 no or minimal depression, score 5 to 7 mild depression, score 8 to 15 moderate depression, and score
16 severe depression (21).
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The 20-item Toronto Alexithymia Scale (TAS-20) was applied as it is the most widely used and presumably the most carefully validated method for measuring alexithymia. Its internal consistency, test-retest reliability, and its convergent, discriminant, and concurrent validity have been demonstrated to be good (2225). The psychometric properties of the Finnish version of the TAS-20 have been shown to be satisfactory (26). The items are rated on a 5-point scale ranging from "strongly disagree" to "strongly agree." The TAS-20 consists of 3 subscales or factors, which reflect the 3 main facets of the alexithymia concept: TAS factor 1 assesses difficulty in identifying feelings (eg, "I have feelings that I cant quite identify"), TAS factor 2 concerns itself with difficulty in describing feelings (eg, "It is difficult for me to find the right words for my feelings"), and TAS factor 3 reflects concrete externally oriented thinking or a preoccupation with the details of external events (eg, "I prefer talking to people about their daily activities rather than their feelings"). According to the recommendation of the developers of the scale, a TAS-20 total score of >60 was used as the cutoff point for alexithymia (27).
In patients with TBI, DSM-IV diagnoses of current axis I psychiatric disorders were made using the Schedules for Clinical Assessment in Neuropsychiatry (SCAN, version 2.1) (28). Personality disorders were evaluated with the Structured Clinical Interview for DSM-III-R Personality Disorders (SCID-II) (29). Organic personality syndrome was assessed according to DSM-III-R criteria and was divided into the following subtypes: labile, aggressive, disinhibited, apathetic, and paranoid.
MRI scans were acquired with a 1.5-T Siemens Magnetom system using a standard head coil. The following sequences were used for analysis: (1) T2-weighted axial turbo spin echo (TSE) 3500/93 ms (repetition time/echo time) with 1 acquisition, slice thickness 5.0 mm, data acquisition matrix 192 x 256 and field of view (FOV) 23.0 cm; (2) T1-weighted sagittal 3-dimensional magnetization prepared rapid gradient echo; TR 10, TE 4, flip angle 10°, matrix 192 x 256, contiguous 1.5-mm slices, 1 acquisition; and (3) T2/PD-weighted coronal TSE 3500/93/19 with 1 acquisition, slice thickness 4.0 mm, data acquisition matrix 192 x 256, and FOV 23.0 cm. In selected cases, additional sequences such as gradient echo T2*-weighted sequences were obtained. The images were evaluated blindly by an experienced neuroradiologist.
For statistical analyses, all patients with contusions of a specific brain region in the right, left, or both hemispheres were combined into 1 group, as the number of patients with contusions on MRI was limited (N = 14), and contusions were bilateral in the majority of them. The frontal lobe was divided into orbital, mesial, and lateral regions. The orbital region included the orbital gyri and the gyrus rectus. The mesial region consisted of the superior and medial frontal gyri, the anterior cingulate gyrus, and the anterior paracentral gyrus. The lateral region included the inferior, middle, and precentral gyri and the opercular and triangular cortex.
Lesions were characterized as diffuse axonal injury (DAI) on the basis of their location and characteristics. In general, hemorrhagic lesions or lesions at the gray-white matter junction, in the corpus callosum, and in the dorsolateral upper brain stem were characterized as DAI. Well-defined areas of >2 mm with signal characteristics similar to cerebrospinal fluid in white matter or deep gray matter were considered lacunar infarcts.
To test for differences in continuous variables, t tests or, if more than 2 categories, ANOVA was used. To test for differences in categorical variables,
2 tests or, if necessary, Fishers exact tests were applied. Odds ratios (ORs) and 95% confidence intervals (95% CIs) are presented where feasible. A 2-sided p value of less than 0.05 was considered statistically significant. Statistical analyses were conducted with SAS System for Windows (Release 8.00).
| RESULTS |
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None of the variables representing TBI was associated with the TAS-20 total scores. Among the 4 categories of TBI severity, the differences in the TAS-20 total scores were nonsignificant (ANOVA: in mild TBI 52.5 ± 14.2, in moderate 57.6 ± 11.4, in severe 48.4 ± 10.3, in very severe 53.3 ± 14.2; p = .46). MRI detected contusions in only 14 out of 54 patients (25.9%). These were bilateral in 8 subjects, exclusively right hemisphere in 3, and exclusively left hemisphere in 3. Between the patients with contusions and patients without contusions, no differences were observed in the TAS-20 total scores (t test: 54.4 ± 14.4 and 53.0 ± 12.7; p = .73). Moreover, the differences did not even approach statistical significance for the presence of contusions of the right hemisphere (N = 11), the left hemisphere (N = 11), the frontal lobe (N = 12), the orbital frontal region (N = 12), the mesial frontal region (N = 8), the lateral frontal region (N = 10), the temporal lobe (N = 10), the parietal lobe (N = 2), and the cingulate gyrus (N = 4). No occipital contusions were found. Nor was DAI on MRI (N = 6; 5 out of 6 also had contusions) connected to the TAS-20 total scores. MRI also revealed silent infarcts (N = 8), which had no association with the TAS-20 total scores.
Table 3 presents current psychiatric disorders and their relation to the TAS-20 total scores in patients with TBI. Statistically significant associations were observed on both axis I and axis II. First, having any axis I disorder or anxiety disorder was associated with significantly higher TAS-20 total scores. Second, patients with any axis II disorder, personality disorder (particularly cluster C disorder), or organic personality syndrome (particularly the labile and disinhibited subtypes) had significantly higher TAS-20 total scores. Alexithymia was strongly associated with organic personality syndrome, as 7 out of 9 patients with this diagnosis (77.8%) were alexithymic. On the other hand, as many as 15 out of 17 patients with alexithymia (88.2%) had psychiatric disorders. No significant differences were found between men and women in terms of having any axis I disorder (men 12/36, 33.3% versus women 6/18, 33.3%;
2 = 0.00, p = 1.00), or any axis II disorder (men 12/36, 33.3% versus women 5/18, 27.8%;
2 = 0.17, p = .68).
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| DISCUSSION |
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Despite the high rate of alexithymia in our patients, none of the variables representing TBI was associated with the TAS-20 total scores. No trend was found between severity of TBI and alexithymic features. In an earlier study with family-practice patients, alexithymia was more common in subjects with a self-reported history of a more severe head injury (knocked unconscious versus knocked only dizzy/dazed) (11). Considering the MRI findings, our statistical analyses were complicated by the small number of subjects with contusions or DAI detectable with postacute MRI. Nonspecific brain atrophy, a potential late sign of DAI, was present in some subjects, but since its etiology could not be ascertained, the radiological diagnosis of DAI was not made. Because our follow-up period was long, our material undoubtedly included people whose traumatic lesions were no longer visible, as the number of lesions detectable with MRI diminishes with time (31). In a stroke study, alexithymia was associated with right-sided lesions but not with the more specific location of the lesion (13). The different quality of stroke and TBI should be kept in mind. In stroke, the laterality of the lesion is apparent and the damaged region is more clearly demarcated, whereas TBI usually affects both hemispheres and is generally more diffuse.
The role of the anterior cingulate cortex has been considered important in alexithymia (58). Furthermore, 2 functional subdivisions of the anterior cingulate cortex have been identified. Its rostral-ventral affective division processes emotional information and regulates emotional responses, whereas its dorsal cognitive division mediates, eg, response inhibition and error processing (32). In our study, the contusions of the cingulate gyrus did not have an association with the TAS-20 total scores, but the number of these patients was small. Moreover, DAI may well disrupt the connections of the cingulate gyrus without causing macroscopical lesions of the region itself (9).
The association between psychiatric disorders and alexithymic features was obvious in our patients with TBI. In fact, nearly all our alexithymic patients had some kind of psychiatric morbidity. As the rates of psychiatric disorders did not differ significantly between men and women, the gender difference in the prevalence of alexithymia does not seem to be explained by psychiatric disorders. Thus, it could be hypothesized that besides being more prone to alexithymia in general, men may have a smaller cerebral reserve capacity for emotion processing and therefore an increased susceptibility to alexithymia in the case of brain injury. Of axis I psychiatric disorders, significantly higher TAS-20 total scores were found in patients with any axis I disorder or anxiety disorder (the number of subjects in other diagnosis groups was low). This finding is in line with earlier studies, where, eg, depression and anxiety disorders have been associated with alexithymia (17,20,3335). On axis II, especially patients with cluster C personality disorders, which were all avoidant personality disorders, or with the labile and disinhibited subtypes of organic personality syndrome had significantly more alexithymic features. In an earlier study, alexithymia was connected to schizotypal, dependent, and avoidant personality traits (36). In addition, alexithymic features have been found to diminish less during recovery from depression in subjects with comorbid cluster C disorders, compared with subjects with depression only (37). Our finding concerning the strong association between organic personality syndrome and alexithymia is interesting, and further studies on patients with organic personality change are warranted. Despite the reports of the state-dependent nature of alexithymia in, eg, depression (20,38), alexithymia can also be considered a trait phenomenon (3941). After TBI, it is plausible that in some cases alexithymic features are mainly related to current psychiatric disorders, whereas in others they may be more traitlike and independent of psychiatric disorders.
In the literature, the relationships between the constructs of alexithymia and depression, and the scales measuring them, have been discussed. As was mentioned above, there are reports of the state-dependent nature of alexithymia in the presence of depression (20,38). It is possible that depressive symptomatology could endorse alexithymia items (15). In some situations, alexithymia may also be a state phenomenon secondary to the emotional distress evoked by an illness (42). Despite the connection between alexithymia and depression, these constructs have been found to be mainly distinct (43,44). However, in a subgroup of subjects with depression, an overlap has occurred between the constructs when the TAS-20 and the 21-item Beck Depression Inventory have been used as measures (44). A corresponding overlap has also been found in subjects with anxiety disorders (43). The psychometric properties of TAS may possibly need to be further developed to improve the differentiation of alexithymia and other constructs.
This is one of the few studies on the association between alexithymia and TBI. Its strengths include the use of a control group matched for age, gender, and severity of depression. Both axis I and II psychiatric disorders were assessed with standardized interviews in patients with TBI. MRI examinations were carried out, but the relatively small number of patients with lesions detectable with postacute MRI set limitations to the analyses. A more sensitive neuroimaging method may have been needed. Because the original group of 210 subjects was referred for examination on a clinical basis, our conclusions may not be generalizable to all patients with TBI.
In conclusion, alexithymia was significantly more common after TBI than among the general population. Alexithymic features were not associated with MRI findings but with psychiatric disorders. It seems that both alexithymia and psychiatric disorders may reflect dysfunction of the injured brain. In clinical practice, the identification of alexithymic features is important as they may complicate rehabilitation after TBI. Alexithymic patients cannot differentiate and express their feelings appropriately, nor can they interpret the emotional communication of others correctly. This may lead to interpersonal difficulties and isolation. To facilitate the adaptation of these patients, alexithymic features should be addressed in psychosocial rehabilitation after TBI by emphasizing elements increasing emotional awareness and teaching appropriate interpersonal communication. In addition, educating family members and health professionals about alexithymic features may also improve the social functioning of patients with TBI.
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Received for publication February 25, 2005; revision received May 15, 2005.
DOI:10.1097/01.psy.0000181278.92249.e5
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