J Head Trauma Rehabil Vol. 30, No. 3, pp. E24–E32 c 2015 Wolters Kluwer Health, Inc. All rights reserved. Copyright
Resilience Is Associated With Fatigue After Mild Traumatic Brain Injury ¨ Heidi Losoi, MA Psych; Minna Waljas, Psych L; Senni Turunen, MA Psych; Antti Brander, MD, PhD; Mika Helminen, MSc; Teemu M. Luoto, MD; ¨ ¨ Eija Rosti-Otajarvi, PhD; Juhani Julkunen, PhD; Juha Ohman, MD, PhD Objective: To examine resilience as a predictor of change in self-reported fatigue after mild traumatic brain injury (MTBI). Participants: A consecutive series of 67 patients with MTBI and 34 orthopedic controls. Design: Prospective longitudinal study. Main Measures: Resilience Scale, Beck Depression Inventory–Second Edition, and Pain subscale from Ruff Neurobehavioral Inventory 1 month after injury and Barrow Neurological Institute Fatigue Scale 1 and 6 months after injury. Results: Insomnia, pain, and depressive symptoms were significantly correlated with fatigue, but even when these variables were controlled for, resilience significantly predicted the change in fatigue from 1 to 6 months after MTBI. In patients with MTBI, the correlation between resilience and fatigue strengthened during follow-up. In controls, significant associations between resilience and fatigue were not found. Conclusion: Resilience is a significant predictor of decrease in self-reported fatigue following MTBI. Resilience seems to be a relevant factor to consider in the management of fatigue after MTBI along with the previously established associated factors (insomnia, pain, and depressive symptoms). Key words: depressive symptoms, fatigue, head injury, insomnia, pain, resilience, traumatic brain injury
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ATIGUE is one of the most frequently reported symptoms after mild traumatic brain injury (MTBI).1 It is a very common symptom, especially in the beginning of the recovery, but can also remain a persistent problem.2 Fatigue is associated with limitations in daily functioning1 and can have complex, interwoven, and wholly or partially treatable underlying causes.3 It has been suggested that fatigue after MTBI is unrelated to injury severity,1,4 number of days from injury to assessment, or cognitive impairment.4 Fatigue has been linked with psychological factors and associated with depression in numerous studies.2,3,5,6 However, the nature or direction of the causality between depression and fatigue has not been established.3 It is also possible that the sensation of fatigue over an extended period may cause depression and anxiety.5 Author Affiliations: Department of Neurosciences and Rehabilitation ¨ ¨ (Mss Losoi, Waljas, and Turunen and Drs Luoto, Rosti-Otajarvi, and ¨ Ohman), and Medical Imaging Center, Department of Radiology (Dr Brander), Tampere University Hospital, Tampere, Finland; University of Helsinki, Institute of Behavioural Sciences, Helsinki, Finland (Ms Losoi and Dr Julkunen); School of Health Sciences, University of Tampere, Tampere, Finland (Mr Helminen); and Science Center, Pirkanmaa Hospital District, Tampere, Finland (Mr Helminen). The authors thank research assistants Anne Simi and Marika SuopankiErvasti for their contribution in data collection. The authors declare no conflicts of interest. Corresponding Author: Heidi Losoi, MA Psych, Tampere University Hospital, PO Box 2000, FI-33521 Tampere, Finland ([email protected]). DOI: 10.1097/HTR.0000000000000055
Patients with traumatic brain injury (TBI) are also particularly likely to experience psychosocial stressors, such as inability to return to work or financial restraints, which can precipitate insomnia7 and exacerbate fatigue.2 Perceived chronic stress has been found to be a significant explanatory factor of fatigue after mild to moderate TBI. This supports the idea that fatigue may have a psychological component that is different from depression or pain.8 Resilience, which has been defined as an ability to recover from adversity,9 is a psychological construct that has received considerable attention recently.10 Resilience moderates the effects of stress and improves adaptation and thus can be one potential psychological component affecting fatigue after MTBI.11 Results from other health conditions, such as cancer12 and Parkinson disease,13 suggest that fatigue could be associated with resilience. In patients with cancer undergoing radiation therapy, resilience was found to be the best predictor of initial fatigue, but it could not be determined as a predictor of changes in fatigue during treatment.12 This study did not include a measure of depression and thus the possibility that depression could drive the association between resilience and fatigue could not be ruled out. In patients with Parkinson disease, resilience was found to correlate with fatigue and depression, along with less disability and better health-related quality of life. Since this association did not yet imply causality, prospective studies were suggested to clarify the nature of the relationship.13 Resilient individuals are suggested
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Resilience Is Associated With Fatigue After MTBI to have the tendency to manifest adaptive behavior also in the area of somatic health,11 and its association with well-being has been proposed to be mediated by positive view of the self, the world, and the future.14 Previous studies on non-TBI populations have found resilience to have a positive correlation with life satisfaction, selfesteem, self-rated health, self-actualization, stress management, and social support and a negative correlation with depressive symptoms and anxiety.9–11,14–17 Resilience has not been widely studied as a predictor of recovery from MTBI, but preliminary findings in an ongoing study18 found it to be a significant contributor to the severity of postinjury anxiety and postconcussive symptoms. On the basis of these prior findings, it can be hypothesized that resilience could be associated with fatigue in patients with MTBI. This association has not been, to the best of our knowledge, previously studied. Apart from depression, fatigue has also been linked to sleep disorders and pain. Sleep disorders are common after TBI.7 Patients with a milder injury are even more likely to have sleep disturbances than the patients with a severe TBI.19 After MTBI, the prevalence of insomnia complaints has been reported to range widely from 21% to 93%.20 Brain regions and systems regulating alertness, attention, and sleep are known to be vulnerable to the effect of TBI.5 Nevertheless, it has been stated that more research on the potential associations between fatigue and sleep disturbance in relation to specific neuroanatomical lesions is required.5,21 Psychological and environmental factors may also have a role in explaining the high prevalence of sleep disturbances after TBI.7 Many of the precipitating factors of insomnia, such as pain, brain lesions, and psychosocial stressors related to TBI, may be chronic in nature. Despite this, it has been suggested that mainly the individual’s responses (eg, adaptiveness of sleep habits, dysfunctional beliefs, and attitudes) to the initial sleep problem determine whether the sleep disturbance will cease or become chronic.7 The details of the causal relationship between sleep disturbance and fatigue is unclear.22 Pain is also a common symptom after TBI and is being reported even more frequently after MTBI than in more severe injuries.23,24 It has been well acknowledged that postconcussive symptoms, such as disturbed sleep, fatigue, and irritability, are reported frequently by patients with chronic pain.25,26 Because of this overlap in symptoms, pain has been suggested to be taken into account when assessing patients with MTBI.23,25,27 This is especially important when studying fatigue, since pain is strongly associated with sleep problems27 and can affect both the initiation and maintenance of sleep.7 Medication has also been suggested as a possibly controllable factor in fatigue studies. Also, hospital-related variables potentially impacting fatigue have been proposed to be controlled by using a medical control group.4
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According to the previous literature, fatigue, sleep disturbance, pain, and emotional distress are common and strongly intertwined symptoms after TBI. Many of the studies of fatigue after TBI have been cross-sectional in nature, and longitudinal research has been considered necessary to disentangle the causal relationships between the variables associated with fatigue.1 Additional research to better understand the interactions of these conditions and the contributing factors to fatigue has been considered essential in order to develop more systematic approaches to its management and intervention planning.8,22,28,29 The aim of this study was to examine resilience as a predictor of the recovery from fatigue after MTBI. We controlled for the aforementioned confounding variables (depression, sleep disorders, and pain) known to interfere with fatigue symptoms and used a longitudinal study design. To differentiate general illness/injury effects from MTBI-specific fatigue and to compare the rates and course of fatigue, patients with orthopedic trauma were used as controls. METHODS Study frame and ethics This study is a part of the prospective Tampere Traumatic Head and Brain Injury Study that aims to identify factors affecting the long-term outcome of MTBI. The study group includes researchers from the areas of neuropsychology, neurology, neurosurgery, neuroradiology, and emergency department (ED). This particular substudy is one of the studies focusing on the psychological aspects of MTBI outcome. Ethics approval for the study was obtained from the Ethics Committee of Pirkanmaa Hospital District, Finland. Participants Participants were enrolled consecutively from the ED of the Tampere University Hospital, between August 2010 and July 2012. All consecutive patients with head computed tomography due to acute head injury (n = 3023) were screened to obtain a sample of working aged adults without preinjury medical, psychiatric, or neurological problems who sustained an MTBI, who probably could be reached for an outcome visit, and who were without known communication problems. Criteria for treatment in the ED, and indication for acute head computed tomography, were based on the Scandinavian guidelines for initial management of minimal, mild, and moderate head injuries.30 Subjects were included in the study if they (i) met MTBI criteria of the World Health Organization’s Collaborating Centre for Neurotrauma Task Force,31 (ii) were aged between 18 and 60 years, and (iii) were residents of the hospital www.headtraumarehab.com
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district. Subjects were excluded if they had (i) premorbid neurological problems, (ii) prior psychiatric problems, (iii) past TBI, (iv) regular psychoactive medication use, (v) neurosurgery, (vi) problems with vision or hearing, (vii) first language was not Finnish, (viii) the time interval between injury and arrival to the ED was more than 72 hours, and/or (ix) they declined to participate in the study. The major causes of exclusion were (i) age criteria not met (n = 1552; 51.3%), (ii) MTBI criteria not met (n = 942; 31.2%), (iii) psychiatric problems (n = 860; 28.4%), and/or (iv) neurological problems (n = 744; 24.6%). It should however be considered that there was major overlap in the causes of exclusion because some patients had multiple reasons. Patient enrollment details are discussed thoroughly in our previous publication.32 Control subjects were orthopedically injured patients evaluated in the same ED as the patients with MTBI. All consecutive patients (n = 609) with ankle injury (bone fracture or distension) were screened for inclusion. The same study criteria used with the MTBI sample were applied in the enrollment of the controls when applicable. Control subjects were enrolled in an ageand sex-stratified manner, with 5 men and 5 women in the following age groups: (i) 18-30 years, (ii) 31-40 years, (iii) 41-50 years, and (iv) 51-60 years. By applying the aforementioned inclusion and exclusion criteria 75 patients with MTBI and 40 trauma controls were recruited. Sixty-seven patients with MTBI and 35 trauma controls completed both assessments at 1 and 6 months and thus formed the final sample of this study. Because of a possible confounding effect, one control subject was later excluded from the analysis because of untreated severe obstructive sleep apnea. ED assessment and neuroimaging In the ED, a clinical assessment of the patients in the final sample was performed by a physician (T.M.L.). The assessment included a thorough interview of past health, diagnosed medical conditions, medication use, head injury history, alcohol consumption, and drug and narcotics abuse history. None of the patients in this study had regular psychoactive medication use. Injury-related data consisted of time of injury, mechanism of injury, and alcohol intoxication at the time of injury. Presence and duration of possible loss of consciousness and posttraumatic amnesia and also Glasgow Coma Scale scores were recorded. The cranial and spinal nerves, as well as coordination and balance, were examined. The overall severity of physical injuries was also assessed. All patients with MTBI and controls underwent 3-T magnet resonance (MR) imaging of the brain (Siemens Trio; Siemens AG Medical Solutions, Erlangen, Germany). The MR imaging protocol included sagittal T1-weighted 3-dimensional infrared-prepared gradient echo, axial T2
turbo spin echo, conventional axial and high-resolution sagittal FLAIR (fluid-attenuated inversion recovery), axial T2∗ , axial SWI (susceptibility weighted imaging), and DWI (diffusion weighted imaging) series. All MR images were analyzed and systematically coded by a neuroradiologist (A.B.). Participants filled out self-report questionnaires about demographic variables, fatigue, insomnia, pain, and resilience as part of a larger Internet-based questionnaire at 1 month postinjury. Fatigue was also assessed with the same Internet-based questionnaire at 6 months after injury. Depressive symptoms were evaluated at a neuropsychological follow-up visit at 1 month postinjury.
Key measures Barrow Neurological Institute Fatigue Scale The Barrow Neurological Institute Fatigue Scale (BNIFS) is an 11-item self-report questionnaire designed to assess fatigue during the early stages of recovery after TBI.33 Subjects rate the extent to which each of the items has been a problem for them since the injury on a 7-point scale (0-1 = rarely a problem; 2-3 = occasional problem, but not frequent; 4-5 = frequent problem; 6-7 = a problem most of the time). The item 11 is an overall rating of the level of fatigue on a scale from 0 (no problem) to 10 (severe problem). The total BNI-FS score is the sum of the first 10 items (min = 0; max = 70). In this study, we examined the change in fatigue by calculating the difference in the total score from 1 to 6 months after injury. The BNI-FS has been shown to be a reliable and valid measure of fatigue after MTBI.3
Injury Severity Score The Injury Severity Score34 (ISS) is an internationally recognized anatomical scoring system that provides an overall score for patients with multiple injuries. Injuries are allocated to 6 body regions: (i) head, (ii) face, (iii) chest, (iv) abdomen, (v) extremities (including pelvis), (vi) external. The ISS ranges from 0 to 75.
Insomnia Severity Index The Insomnia Severity Index35 (ISI) is a reliable and valid36 7-item self-report questionnaire measuring the patient’s perception of his or her insomnia. It evaluates, on a 5-point Likert scale, the severity of sleep onset, sleep maintenance, early morning awakening problems, sleep dissatisfaction, interference of sleep difficulties with daytime functioning, noticeability of sleep problems by others, and distress caused by the sleep difficulties.36 The total score ranges from 0 to 28.
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Resilience Is Associated With Fatigue After MTBI Ruff Neurobehavioral Inventory Pain was assessed by the Pain subscale of the Ruff Neurobehavioral Inventory,37 which comprises of 6 items on a 4-point scale, the score thus ranging from 6 to 24. Reliability and validity of the Ruff Neurobehavioral Inventory have been reported adequate.37 Beck Depression Inventory The Beck Depression Inventory–Second Edition38 (BDI-II) self-report questionnaire was used to assess depressive symptoms. In the questionnaire, subjects are asked to rate 21 items on a 4-point scale ranging from 0 to 3. The total score of the scale ranges from 0 to 63. To address the overlap effect of BDI-II with the BNI-FS and the ISI, the analysis in this study was conducted with a reduced item set for BDI-II. Three potentially confounding items (15, “loss of energy”; 16, “changes in sleeping patterns”; and 20, “tiredness or fatigue”) were removed from the BDI-II total score. Resilience Scale Resilience was assessed using the Resilience Scale11 (RS). It comprises 25 items, wherein the respondents are asked to state the degree to which they agree or disagree on a 7-point Likert scale from 1 (strongly disagree) to 7 (strongly agree). The possible total scores thus range from 25 to 175, with higher scores reflecting higher resilience. In this study, resilience was analyzed as a categorical variable using the following scoring for the total score presented by the original author9 : 25100 = very low; 101-115 = low; 116-130 = on the low end; 131-145 = moderate; 145-160 = moderately high; and 161-175 = high. The RS has been reported to be a reliable and valid tool to measure resilience.11 The psychometric properties of the Finnish version of the scale have been previously published by our group.39 Data analysis Differences between the MTBI and control groups were analyzed by using the Mann-Whitney U and Fisher exact tests. This was done to describe and examine the characteristics of the MTBI group in reference to controls and to examine whether the groups differed in symptoms and the course of fatigue. Adjustment for multiple comparisons was not considered necessary.40 Cohen d values were used to illustrate clinical significance. The coefficient correlations between the BNI-FS and the predictive variables were then calculated using the Spearman correlation analysis to demonstrate how the variables are associated and to examine whether the associations are different in patients and controls. Finally, multiple linear regression analysis was conducted to determine eventual independent predictors of the
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change in fatigue from 1 to 6 months. Variables with clinical interest and relevance were included in the regression model. This analysis was conducted only for the MTBI group, because the aim of this study was to examine the association of fatigue and resilience following MTBI. In addition, the amount of reported fatigue among controls was practically unchangeable throughout the follow-up period. The 3 demographic variables (age, gender, and education) and physical injuries (ISS) were controlled for by entering them into to the regression analysis first. In a second step, insomnia, pain, and depressive symptoms were simultaneously added to the model. After controlling for these factors, resilience was added to the model in the third step. Residuals of the regression analysis were found to be normally distributed. The statistical significance level was set to .05 for all the analyses. Statistical analyses were conducted using SPSS for Windows (version 20.0; SPSS Inc, Chicago, Illinois) with the supervision and help of a statistician (M.H.). RESULTS There were no statistically significant differences between the MTBI and control groups in age, education, gender, ISS, or the time interval from injury to 1 month questionnaires. The difference in days from injury to 6 months questionnaires between the MTBI (186 days) and control (193 days) groups was statistically significant. The difference in days is, however, subtle (7.7 days in a follow-up period of 6 months), and the finding can be considered clinically irrelevant. The characteristics of patients with MTBI and the control group are presented in Table 1. In the MTBI group, 15 patients (22.4%) had an acute traumatic lesion on the MR image. The MR images of all the controls were interpreted normal. The MTBI group tended to report more symptoms of insomnia than the control group, but the difference between the groups was not statistically significant. The MTBI and control groups did not significantly differ on pain, depressive symptoms, or resilience. The group differences between the MTBI and control groups on the predictive variables (ISI, Ruff Neurobehavioral Inventory, BDI-II, and RS) and fatigue variables (BNI-FS) are presented in Table 2. The patients with MTBI had a significantly higher level of fatigue at 1 month postinjury than the controls. However, there was a decrease in the level of fatigue in the patients with MTBI during follow-up. In the controls, no significant change in fatigue occurred. At 6 months after injury the difference on fatigue between the patients with MTBI and controls was not statistically significant. At 1 month postinjury, fatigue correlated significantly with insomnia, pain, and depressive symptoms in both the MTBI and control groups. However, significant correlation between resilience and fatigue was found only www.headtraumarehab.com
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JOURNAL OF HEAD TRAUMA REHABILITATION/MAY–JUNE 2015
Characteristics of patients with MTBI and orthopedic controls Patients with MTBI (n = 67)
Controls (n = 34)
Cohen d
Pa
25 (37.3)/42 (62.7) 37.0 (12.0) 14.3 (3.1) 25.3 (4.4) 185.7 (11.5) 3.7 (3.1)
19 (44.1)/15 (55.9) 39.1 (12.8) 14.3 (2.6) 23.9 (3.6) 193.4 (19.1) 2.5 (1.5)
0.17 0.02 0.35 0.54 0.45
.059 .431 .766 .081 .011b .089
Descriptive variables Gender (F/M), n (%) Age, mean (SD), y Years of education, mean (SD) Days from injury to 1 mo questionnaire, mean (SD) Days from injury to 6 mo questionnaire, mean (SD) Injury Severity Score, mean (SD)
Abbreviation: MTBI, mild traumatic brain injury. a Mann-Whitney P value in all but gender difference analysis in which the Fischer P value was used. b P < .05.
Group differences in fatigue and predictive variables at 1 month among patients with MTBI and the controls TABLE 2
Patients with MTBI (n = 67)
Controls (n = 34)
Cohen d
Pa
14.7 (15.1) 8.9 (12.0) − 5.8 (12.0) 5.3 (5.3) 8.2 (2.2) 3.7 (4.5) 138.9 (17.1)
7.2 (6.8) 6.9 (10.1) − 0.2 (10.3) 3.3 (3.5) 8.4 (2.6) 3.4 (4.2) 138.5 (16.1)
0.59 0.18 0.49 0.41 0.07 0.06 0.01
.025b .641 .050b .236 .943 .951 .733
Fatigue (BNI-FS) at 1 mo, mean (SD) Fatigue (BNI-FS) at 6 mo, mean (SD) Change in fatigue (BNI-FS) from 1 to 6 mo Insomnia (ISI) Pain subscale (RNBI) Depressive symptoms (BDI-II) Resilience (RS)
Abbreviations: BDI-II, Beck Depression Inventory–Second Edition; BNI-FS, Barrow Neurological Institute Fatigue Scale; ISI, Insomnia Severity Index; MTBI, mild traumatic brain injury; RNBI, Ruff Neurobehavioral Inventory; RS, Resilience Scale. a Mann-Whitney P value. b P < .05.
in patients with MTBI (see Table 3). At 6 months, fatigue correlated significantly with pain and depressive symptomps in both groups. In the MTBI group, resilience and insomnia were also significantly correlated with fatigue at 6 months. In patients with MTBI, the correlation between resilience and fatigue was even stronger at follow-up. In the controls, no correlation between resilience and fatigue was found.
Multiple regression analysis was done to examine the predictors of the change in fatigue from 1 to 6 months in the MTBI group. The demographic variables (age, gender, and education) and physical injuries (ISS) did not predict change in fatigue (adjusted R2 = −0.055; P = .968). Adding insomnia, pain, and depressive symptoms simultaneously to the model at the next step produced a significant change (P = .033), but the model did
TABLE 3 Correlations between the predictive variables (at 1 month) and fatigue (BNI-FS total scores) at 1 and 6 months Patients with MTBI (n = 67) Variables Insomnia (ISI) Pain (RNBI) Depressive symptoms (BDI-II) Resilience (RS)
Controls (n = 34)
Fatigue at 1 mo (BNI-FS)
Fatigue at 6 mo (BNI-FS)
Fatigue at 1 mo (BNI-FS)
Fatigue at 6 mo (BNI-FS)
0.67a 0.39a 0.39b − 0.26b
0.50a 0.54a 0.39a − 0.45a
0.42b 0.54a 0.42b − 0.26
0.24 0.48a 0.42b − 0.27
Abbreviations: BDI-II = Beck Depression Inventory II–Second Edition; BNI-FS, Barrow Neurological Institute Fatigue Scale; ISI, Insomnia Severity Index; MTBI, mild traumatic brain injury; RNBI, Ruff Neurobehavioral Inventory; RS, Resilience Scale. a P < .01. b P < .05.
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Resilience Is Associated With Fatigue After MTBI not reach statistical significance (adjusted R2 = 0.043; P = .215). After controlling for the aforementioned variables, resilience added significantly (P = .006) to the model. The final step of the regression model (see Table 4) significantly (adjusted R2 = 0.145; P = .026) predicted the change in fatigue from 1 to 6 months after MTBI. In this final model, insomnia was found to be a significant predictor besides resilience. Depressive symptoms had a trend toward significance, but resilience was the strongest predictor. In the regression model, all variance inflation factor values were under 1.8. Figure 1 illustrates the association of resilience and fatigue by presenting the level of fatigue at both
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measurements (1 and 6 months) in patients groups divided by their resilience scores. DISCUSSION The main finding of this study was that even when controlled for the factors known to be associated with fatigue (depression, sleep disorders, and pain), resilience was a significant predictor of the change in fatigue from 1 to 6 months after injury. This finding concurs with previous findings from other medical conditions.12,13 This is the first study to report this phenomenon in patients with MTBI, although in many previous
Results of the final multivariate regression model for the change in fatigue from 1 to 6 months postinjury in patients with MTBI TABLE 4
Block
Gender (males) Age Years of education Injury severity (ISS) Insomnia (ISI) Pain (RNBI) Depressive symptoms (BDI-II) Resilience (RS)
1 Standardized β
P
−.011 −.073 −.030 −.043
.935 .569 .814 .741
2 Standardized β
P
−.080 −.094 −.067 −.011 −.266 −.119 −.072
.531 .447 .606 .933 .071 .427 .625
3 Standardized β
P
− .142 − .134 − .029 .037 − .279 − .117 − .257 − .380
.249 .254 .812 .764 .046a .409 .098 .006
Abbreviations: BDI-II, Beck Depression Inventory–Second Edition; ISI, Insomnia Severity Index; ISS, Injury Severity Index; MTBI, mild traumatic brain injury; RNBI, Ruff Neurobehavioral Inventory; RS, Resilience Scale. a P < .05.
Figure 1. Mean fatigue scores (BNI-FS) of patient groups stratified by different levels of resilience. BNI-FS indicates Barrow Neurological Institute Fatigue Scale; MTBI, mild traumatic brain injury.
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studies, it has been shown that psychological factors such as depression or stress are associated with fatigue. The current study shows that in a healthy population as well, with no previous psychiatric problems, resilience is associated with the recovery from fatigue. This is in line with other preliminary findings on resilience and MTBI, which have suggested resilience to be a significant contributor to the severity of postinjury anxiety and postconcussive symptoms.18 Resilience correlated significantly with fatigue only in patients with MTBI and the correlation strengthened during follow-up. The level of resilience did not differ between the MTBI and control groups. This would be expected if we define resilience as a personality trait that it was originally referred to.41 The term “resilience” has, however, been not only used to refer to a dynamic developmental process42 and considered as an innate characteristic each person possesses to some degree but can also be enhanced or diminished depending on life circumstances.43 We did not have data on the level of resilience before the injuries, and it was not in the scope of this study to examine the factors associated with resilience. Further research about the stability of resilience after MTBI is thus needed. The results of this study also support the established knowledge about fatigue being an eminent symptom after MTBI. The comparison with the control group demonstrated that the course of fatigue was different after MTBI than after an orthopedic injury. The level of fatigue was found to be significantly higher in patients with MTBI than in the controls at 1 month after the injury. However, there was a significant decrease in the level of fatigue in patients with MTBI during follow-up. At 6 months after injury, there was no significant difference between patients with MTBI and controls regarding self-reported fatigue. Depressive symptoms, sleep disorder, and pain were assessed as confounding factors. In relation to these factors, comparisons between the patients with MTBI and controls were conducted. The patients with MTBI reported slightly more insomnia symptoms than the controls, but the difference was not statistically significant. On pain or depressive symptoms, the MTBI and control groups did not significantly differ. The lack of differences between the groups might partly be explained by the symptoms induced by the physical injuries of the controls. In MTBI literature, comparison with trauma controls (eg, orthopedically injured controls) has been called for. The main reason for this is the unspecific nature of post-TBI symptoms. MTBI-like symptoms are also commonly reported by patients with non-TBI.44 Our results support these findings. Furthermore, our findings show that symptom endorsement among this rigorously selected sample of previously healthy patients with MTBI was not
considerably higher than in controls with an orthopedic injury. Despite the fact that the patients with MTBI and controls did not significantly differ on the aforementioned controllable factors, this study provides further support that insomnia, pain, and depressive symptoms correlate with fatigue after MTBI. It was not the intention of this study to examine their individual effects. However, the results emphasize the identification and treatment of sleep disorders, pain, and depressive symptoms in the management of fatigue after MTBI. It has been previously noted that fatigue, secondary to sleep disturbance, would require a diagnostic and treatment approach different from fatigue due to affective disorders or attention problems.28 Also different treatments, such as teaching good sleep habits (sleep hygiene), may be needed to assist in minimizing any associated distress.45 Furthermore, the importance of early identification and intervention of pain has previously been recommended for patients with MTBI.23 This is the first study to report the association of resilience and fatigue after MTBI. It was beyond the scope of this study to examine the mechanisms or possible physiological underpinnings of this association. It can be hypothesized that the association of resilience and fatigue could be driven by the ability of resilient individuals to adjust and moderate the effects of stress. Coping styles have previously been associated with the outcome of MTBI.46,47 In future research, coping styles among other outcome moderators should be studied in relation to resilience and fatigue. In addition, more research about the role of resilience in recovery from MTBI is needed before making firm statements about the clinical implications of this finding. It has previously been reported in patients with cancer that psychological support focusing on providing strategies to improve resilience might be promising when having to undergo stressful treatments12 because fatigue is determined to some extent by the psychological capacity to deal with patterns of stress related to threat and illness. It has also been proposed that prospective follow-up studies should be done to determine temporal relationships between fatigue and stress early after injury. In addition, nonreferred samples could help determine the optimal timing of interventions such as cognitive-behavioral therapies and stress management.8 It has been noted that after MTBI, fatigue and psychological factors require early treatment to prevent symptom exacerbation.2 Our results also refer that previously healthy patients with MTBI might benefit from early postinjury guidance in the management of fatigue. Future research on the possible interventions is needed. There are some limitations to this study that should be considered when drawing clinical conclusions about the results. By applying strict exclusion criteria, we
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Resilience Is Associated With Fatigue After MTBI enrolled only 2.48% of all consecutively screened patients with head computed tomography due to an acute head injury. Excluding patients with preexisting conditions weakens the generalizability of the results into everyday clinical practice. It has been previously noted by our group32 that, for example, older adults and patients with preexisting neurological or psychiatric problems are frequently seen in the ED because of MTBI, but they are often excluded from clinical studies. These limitations with patient selection have been discussed in more detail in a previous publication of our study group.32 In the current study, our aim was to obtain a homogeneous MTBI population in order to avoid possible bias due to a heterogeneous sample. To enhance the validity of our data, we carefully excluded all premorbid conditions (substance abuse, prior psychiatric disorders or neurological problems, previous brain injuries) to rule out the possible influence of premorbid moderator variables. Thus, examining a premorbidly healthy, homogeneous sample can also be seen as strength. The
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second limitation of this study is the overlap of the measured constructs. In this study, we aimed to reduce the overlap effect of BDI-II with BNI-FS and ISI by conducting the analysis with a reduced item set for BDI-II (with 3 potentially confounding items removed). Third, the number of subjects in this study was relatively small and therefore future studies are needed to confirm the results. Despite these limitations, we have been able to overcome many of the challenges of previous studies by using a longitudinal study design with high follow-up rates and minimal confounding factors. The inclusion of an orthopedic control group enrolled with the same exclusion criteria gives further strength to the study. CONCLUSION Our results show that resilience is a significant predictor of self-reported fatigue following MTBI. Resilience seems to be a relevant factor to be considered in the management of fatigue after MTBI.
REFERENCES 1. Stulemeijer M, Van der Werf S, Bleijenberg G, Biert J, Brauer J, Vos PE. Recovery from mild traumatic brain injury, a focus on fatigue. J Neurol. 2006;253:1041–1047. 2. Norrie J, Heitger M, Leathem J, Anderson T, Jones R, Flett R. Mild traumatic brain injury and fatigue: a prospective longitudinal study. Brain Inj. 2010;24:1528–1538. 3. W¨aljas M, Iverson GL, Hartikainen KM, et al. Reliability, validity and clinical usefulness of the BNI fatigue scale in mild traumatic brain injury. Brain Inj. 2012;26:972–978. 4. Borgaro SR, Baker J, Wethe JV, Prigatano GP, Kwasnica C. Subjective reports of fatigue during early recovery from traumatic brain injury. J Head Trauma Rehabil. 2005;20:416–425. 5. Ponsford JL, Ziino C, Parcell DL, et al. Fatigue and sleep disturbance following traumatic brain injury: their nature, causes, and potential treatments. J Head Trauma Rehabil. 2012;23:224–233. 6. Ziino C, Ponsford J. Measurement and prediction of subjective fatigue following traumatic brain injury. J Int Neuropsychol Soc. 2005;11:416–425. 7. Ouellet M-C, Savard J, Morin CM. Insomnia following traumatic brain injury: a review. Neurorehabil Neural Repair. 2004;18:187– 198. 8. Bay E, Xie Y. Psychological and biological correlates of fatigue after mild-to-moderate traumatic brain injury. West J Nurs Res. 2009;31:731–747. 9. Wagnild GM. The Resilience Scale User’s Guide for the US English Version of the Resilience Scale and the 14-Item Resilience Scale (RS-14). Worden, MT: The Resilience Center; 2009. 10. Nishi D, Uehara R, Kondo M, Matsuoka Y. Reliability and validity of the Japanese version of the Resilience Scale and its short version. BMC Res Notes. 2010;3:310–315. 11. Wagnild GM, Young HM. Development and psychometric evaluation of the Resilience Scale. J Nurs Meas. 1993;1:165–178. 12. Strauss B, Brix C, Fischer S, et al. The influence of resilience on fatigue in cancer patients undergoing radiation therapy. J Cancer Res Clin Oncol. 2007;133:511–518. 13. Robottom BJ, Gruber-Baldini AL, Anderson KE, et al. What determines resilience in patients with Parkinson’s disease? Parkinsonism Relat Disord. 2012;18:174–177.
14. Mak WWS, Ng ISW, Wong CCY. Resilience: enhancing wellbeing through the positive cognitive triad. J Couns Psychol. 2011;58:610–617. 15. Heilemann MV, Lee K, Kury FS. Psychometric properties of the Spanish version of the Resilience Scale. J Nurs Meas. 2003;11:61– 71. 16. Humpreys J. Resilience in sheltered battered women. Issues Ment Health Nurs. 2003;24:137–152. 17. Abiola T, Udofia O. Psychometric assessment of the Wagnild and Young’s Resilience Scale in Kano, Nigeria. BMC Res Notes. 2011;4:509–514. 18. McCauley SR, Wilde EA, Miller ER, et al. Preinjury resilience and mood as predictors of early outcome following mild traumatic brain injury. J Neurotrauma. 2013;30:642–652. 19. Clinchot DM, Bogner J, Mysiw WJ, Fugate L, Corrigan J. Defining sleep disturbance after brain injury. Am J Phys Med Rehabil. 1998;77:291–295. 20. Wallace DM, Shafazand S, Ramos AR, et al. Insomnia characteristics and clinical correlates in Operation Freedom/Operation Iraqi Freedom veterans with posttraumatic stress disorder and mild traumatic brain injury: an exploratory study. Sleep Med. 2011;12:850– 859. 21. Rao V, Bergey A, Hill H, Efron D, McCann U. Sleep disturbance after mild traumatic brain injury: indicator of injury? J Neuropsychiatry Clin Neurosci. 2011;23:201–205. 22. Fogerlberg DJ, Hoffman JM, Dikmen S, Temkin NR, Bell KR. Association of sleep and co-occurring psychological conditions as 1 year after traumatic brain injury. Arc Phys Med Rehabil. 2012;93:1313–1318. 23. Uomoto JM, Esselman PC. Traumatic brain injury and chronic pain: differential types and rates by head injury severity. Arch Phys Med Rehabil. 1993;74:61–64. 24. Sherman KB, Goldberg M, Bell KR. Traumatic brain injury and pain. Phys Med Rehabil Clin N Am. 2006;17:473–490. 25. Iverson GL, McCracken LM. “Postconcussive” symptoms in persons with chronic pain. Brain Inj. 1997;11:783–790. 26. St˚alnacke BM. Postconcussion symptoms in patients with injuryrelated chronic pain [published online ahead of print May
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37. Ruff RM, Hibbard KM. Ruff Neurobehavioral Inventory Professional Manual. Lutz, FL: Psychological Assessment Resources; 2003. 38. Beck AT, Steer RA, Brown GK. Manual for the Beck Depression Inventory-II (Finnish version). San Antonio, TX: The Psychological Corporation; 1996. 39. Losoi H, Turunen S, W¨aljas M, et al. Psychometric properties of the Finnish version of the Resilience Scale and its short version. Psychol Community Health. 2013;2:1–10. 40. Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiology. 1990;1:43–46. 41. Earvolino-Ramirez M. Resilience: a concept analysis. Nurs Forum. 2007;42:73–82. 42. Luthar SS, Cicchetti D, Becker B. The construct of resilience: a critical evaluation and guidelines for future work. Child Dev. 2000;71:543–562. 43. Wagnild GM. Resilience and successful aging. Comparison among low and high income older adults. J Gerontol Nurs. 2003;29:42–49. 44. Meares S, Shores EA, Taylor AJ, et al. Mild traumatic brain injury does not predict acute postconcussion syndrome. J Neurol Neurosurg Psychiatry. 2008;79:300–306. 45. Mathias JL, Alvaro PK. Prevalence of sleep disturbances, disorders, and problems following brain injury: a meta-analysis. Sleep Med. 2012;13:898–905. 46. Maestas KL, Sander AM, Clark AN, et al. Preinjury coping, emotional functioning, and quality of life following uncomplicated and complicated brain injury [published online ahead of print March 26, 2013]. J Head Trauma Rehabil. doi:10.1097/HTR.0b013e31828654b4. 47. Snell DL, Siegert RJ, Hay-Smith EJC, Surgenor LJ. Associations between illness perceptions, coping styles and outcome after mild traumatic brain injury: preliminary results from a cohort study. Brain Inj. 2011;11:1126–1138.
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Resilience Is Associated With Fatigue After Mild Traumatic Brain Injury ¨ Heidi Losoi, MA Psych; Minna Waljas, Psych L; Senni Turunen, MA Psych; Antti Brander, MD, PhD; Mika Helminen, MSc; Teemu M. Luoto, MD; ¨ ¨ Eija Rosti-Otajarvi, PhD; Juhani Julkunen, PhD; Juha Ohman, MD, PhD Objective: To examine resilience as a predictor of change in self-reported fatigue after mild traumatic brain injury (MTBI). Participants: A consecutive series of 67 patients with MTBI and 34 orthopedic controls. Design: Prospective longitudinal study. Main Measures: Resilience Scale, Beck Depression Inventory–Second Edition, and Pain subscale from Ruff Neurobehavioral Inventory 1 month after injury and Barrow Neurological Institute Fatigue Scale 1 and 6 months after injury. Results: Insomnia, pain, and depressive symptoms were significantly correlated with fatigue, but even when these variables were controlled for, resilience significantly predicted the change in fatigue from 1 to 6 months after MTBI. In patients with MTBI, the correlation between resilience and fatigue strengthened during follow-up. In controls, significant associations between resilience and fatigue were not found. Conclusion: Resilience is a significant predictor of decrease in self-reported fatigue following MTBI. Resilience seems to be a relevant factor to consider in the management of fatigue after MTBI along with the previously established associated factors (insomnia, pain, and depressive symptoms). Key words: depressive symptoms, fatigue, head injury, insomnia, pain, resilience, traumatic brain injury
F
ATIGUE is one of the most frequently reported symptoms after mild traumatic brain injury (MTBI).1 It is a very common symptom, especially in the beginning of the recovery, but can also remain a persistent problem.2 Fatigue is associated with limitations in daily functioning1 and can have complex, interwoven, and wholly or partially treatable underlying causes.3 It has been suggested that fatigue after MTBI is unrelated to injury severity,1,4 number of days from injury to assessment, or cognitive impairment.4 Fatigue has been linked with psychological factors and associated with depression in numerous studies.2,3,5,6 However, the nature or direction of the causality between depression and fatigue has not been established.3 It is also possible that the sensation of fatigue over an extended period may cause depression and anxiety.5 Author Affiliations: Department of Neurosciences and Rehabilitation ¨ ¨ (Mss Losoi, Waljas, and Turunen and Drs Luoto, Rosti-Otajarvi, and ¨ Ohman), and Medical Imaging Center, Department of Radiology (Dr Brander), Tampere University Hospital, Tampere, Finland; University of Helsinki, Institute of Behavioural Sciences, Helsinki, Finland (Ms Losoi and Dr Julkunen); School of Health Sciences, University of Tampere, Tampere, Finland (Mr Helminen); and Science Center, Pirkanmaa Hospital District, Tampere, Finland (Mr Helminen). The authors thank research assistants Anne Simi and Marika SuopankiErvasti for their contribution in data collection. The authors declare no conflicts of interest. Corresponding Author: Heidi Losoi, MA Psych, Tampere University Hospital, PO Box 2000, FI-33521 Tampere, Finland ([email protected]). DOI: 10.1097/HTR.0000000000000055
Patients with traumatic brain injury (TBI) are also particularly likely to experience psychosocial stressors, such as inability to return to work or financial restraints, which can precipitate insomnia7 and exacerbate fatigue.2 Perceived chronic stress has been found to be a significant explanatory factor of fatigue after mild to moderate TBI. This supports the idea that fatigue may have a psychological component that is different from depression or pain.8 Resilience, which has been defined as an ability to recover from adversity,9 is a psychological construct that has received considerable attention recently.10 Resilience moderates the effects of stress and improves adaptation and thus can be one potential psychological component affecting fatigue after MTBI.11 Results from other health conditions, such as cancer12 and Parkinson disease,13 suggest that fatigue could be associated with resilience. In patients with cancer undergoing radiation therapy, resilience was found to be the best predictor of initial fatigue, but it could not be determined as a predictor of changes in fatigue during treatment.12 This study did not include a measure of depression and thus the possibility that depression could drive the association between resilience and fatigue could not be ruled out. In patients with Parkinson disease, resilience was found to correlate with fatigue and depression, along with less disability and better health-related quality of life. Since this association did not yet imply causality, prospective studies were suggested to clarify the nature of the relationship.13 Resilient individuals are suggested
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Resilience Is Associated With Fatigue After MTBI to have the tendency to manifest adaptive behavior also in the area of somatic health,11 and its association with well-being has been proposed to be mediated by positive view of the self, the world, and the future.14 Previous studies on non-TBI populations have found resilience to have a positive correlation with life satisfaction, selfesteem, self-rated health, self-actualization, stress management, and social support and a negative correlation with depressive symptoms and anxiety.9–11,14–17 Resilience has not been widely studied as a predictor of recovery from MTBI, but preliminary findings in an ongoing study18 found it to be a significant contributor to the severity of postinjury anxiety and postconcussive symptoms. On the basis of these prior findings, it can be hypothesized that resilience could be associated with fatigue in patients with MTBI. This association has not been, to the best of our knowledge, previously studied. Apart from depression, fatigue has also been linked to sleep disorders and pain. Sleep disorders are common after TBI.7 Patients with a milder injury are even more likely to have sleep disturbances than the patients with a severe TBI.19 After MTBI, the prevalence of insomnia complaints has been reported to range widely from 21% to 93%.20 Brain regions and systems regulating alertness, attention, and sleep are known to be vulnerable to the effect of TBI.5 Nevertheless, it has been stated that more research on the potential associations between fatigue and sleep disturbance in relation to specific neuroanatomical lesions is required.5,21 Psychological and environmental factors may also have a role in explaining the high prevalence of sleep disturbances after TBI.7 Many of the precipitating factors of insomnia, such as pain, brain lesions, and psychosocial stressors related to TBI, may be chronic in nature. Despite this, it has been suggested that mainly the individual’s responses (eg, adaptiveness of sleep habits, dysfunctional beliefs, and attitudes) to the initial sleep problem determine whether the sleep disturbance will cease or become chronic.7 The details of the causal relationship between sleep disturbance and fatigue is unclear.22 Pain is also a common symptom after TBI and is being reported even more frequently after MTBI than in more severe injuries.23,24 It has been well acknowledged that postconcussive symptoms, such as disturbed sleep, fatigue, and irritability, are reported frequently by patients with chronic pain.25,26 Because of this overlap in symptoms, pain has been suggested to be taken into account when assessing patients with MTBI.23,25,27 This is especially important when studying fatigue, since pain is strongly associated with sleep problems27 and can affect both the initiation and maintenance of sleep.7 Medication has also been suggested as a possibly controllable factor in fatigue studies. Also, hospital-related variables potentially impacting fatigue have been proposed to be controlled by using a medical control group.4
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According to the previous literature, fatigue, sleep disturbance, pain, and emotional distress are common and strongly intertwined symptoms after TBI. Many of the studies of fatigue after TBI have been cross-sectional in nature, and longitudinal research has been considered necessary to disentangle the causal relationships between the variables associated with fatigue.1 Additional research to better understand the interactions of these conditions and the contributing factors to fatigue has been considered essential in order to develop more systematic approaches to its management and intervention planning.8,22,28,29 The aim of this study was to examine resilience as a predictor of the recovery from fatigue after MTBI. We controlled for the aforementioned confounding variables (depression, sleep disorders, and pain) known to interfere with fatigue symptoms and used a longitudinal study design. To differentiate general illness/injury effects from MTBI-specific fatigue and to compare the rates and course of fatigue, patients with orthopedic trauma were used as controls. METHODS Study frame and ethics This study is a part of the prospective Tampere Traumatic Head and Brain Injury Study that aims to identify factors affecting the long-term outcome of MTBI. The study group includes researchers from the areas of neuropsychology, neurology, neurosurgery, neuroradiology, and emergency department (ED). This particular substudy is one of the studies focusing on the psychological aspects of MTBI outcome. Ethics approval for the study was obtained from the Ethics Committee of Pirkanmaa Hospital District, Finland. Participants Participants were enrolled consecutively from the ED of the Tampere University Hospital, between August 2010 and July 2012. All consecutive patients with head computed tomography due to acute head injury (n = 3023) were screened to obtain a sample of working aged adults without preinjury medical, psychiatric, or neurological problems who sustained an MTBI, who probably could be reached for an outcome visit, and who were without known communication problems. Criteria for treatment in the ED, and indication for acute head computed tomography, were based on the Scandinavian guidelines for initial management of minimal, mild, and moderate head injuries.30 Subjects were included in the study if they (i) met MTBI criteria of the World Health Organization’s Collaborating Centre for Neurotrauma Task Force,31 (ii) were aged between 18 and 60 years, and (iii) were residents of the hospital www.headtraumarehab.com
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district. Subjects were excluded if they had (i) premorbid neurological problems, (ii) prior psychiatric problems, (iii) past TBI, (iv) regular psychoactive medication use, (v) neurosurgery, (vi) problems with vision or hearing, (vii) first language was not Finnish, (viii) the time interval between injury and arrival to the ED was more than 72 hours, and/or (ix) they declined to participate in the study. The major causes of exclusion were (i) age criteria not met (n = 1552; 51.3%), (ii) MTBI criteria not met (n = 942; 31.2%), (iii) psychiatric problems (n = 860; 28.4%), and/or (iv) neurological problems (n = 744; 24.6%). It should however be considered that there was major overlap in the causes of exclusion because some patients had multiple reasons. Patient enrollment details are discussed thoroughly in our previous publication.32 Control subjects were orthopedically injured patients evaluated in the same ED as the patients with MTBI. All consecutive patients (n = 609) with ankle injury (bone fracture or distension) were screened for inclusion. The same study criteria used with the MTBI sample were applied in the enrollment of the controls when applicable. Control subjects were enrolled in an ageand sex-stratified manner, with 5 men and 5 women in the following age groups: (i) 18-30 years, (ii) 31-40 years, (iii) 41-50 years, and (iv) 51-60 years. By applying the aforementioned inclusion and exclusion criteria 75 patients with MTBI and 40 trauma controls were recruited. Sixty-seven patients with MTBI and 35 trauma controls completed both assessments at 1 and 6 months and thus formed the final sample of this study. Because of a possible confounding effect, one control subject was later excluded from the analysis because of untreated severe obstructive sleep apnea. ED assessment and neuroimaging In the ED, a clinical assessment of the patients in the final sample was performed by a physician (T.M.L.). The assessment included a thorough interview of past health, diagnosed medical conditions, medication use, head injury history, alcohol consumption, and drug and narcotics abuse history. None of the patients in this study had regular psychoactive medication use. Injury-related data consisted of time of injury, mechanism of injury, and alcohol intoxication at the time of injury. Presence and duration of possible loss of consciousness and posttraumatic amnesia and also Glasgow Coma Scale scores were recorded. The cranial and spinal nerves, as well as coordination and balance, were examined. The overall severity of physical injuries was also assessed. All patients with MTBI and controls underwent 3-T magnet resonance (MR) imaging of the brain (Siemens Trio; Siemens AG Medical Solutions, Erlangen, Germany). The MR imaging protocol included sagittal T1-weighted 3-dimensional infrared-prepared gradient echo, axial T2
turbo spin echo, conventional axial and high-resolution sagittal FLAIR (fluid-attenuated inversion recovery), axial T2∗ , axial SWI (susceptibility weighted imaging), and DWI (diffusion weighted imaging) series. All MR images were analyzed and systematically coded by a neuroradiologist (A.B.). Participants filled out self-report questionnaires about demographic variables, fatigue, insomnia, pain, and resilience as part of a larger Internet-based questionnaire at 1 month postinjury. Fatigue was also assessed with the same Internet-based questionnaire at 6 months after injury. Depressive symptoms were evaluated at a neuropsychological follow-up visit at 1 month postinjury.
Key measures Barrow Neurological Institute Fatigue Scale The Barrow Neurological Institute Fatigue Scale (BNIFS) is an 11-item self-report questionnaire designed to assess fatigue during the early stages of recovery after TBI.33 Subjects rate the extent to which each of the items has been a problem for them since the injury on a 7-point scale (0-1 = rarely a problem; 2-3 = occasional problem, but not frequent; 4-5 = frequent problem; 6-7 = a problem most of the time). The item 11 is an overall rating of the level of fatigue on a scale from 0 (no problem) to 10 (severe problem). The total BNI-FS score is the sum of the first 10 items (min = 0; max = 70). In this study, we examined the change in fatigue by calculating the difference in the total score from 1 to 6 months after injury. The BNI-FS has been shown to be a reliable and valid measure of fatigue after MTBI.3
Injury Severity Score The Injury Severity Score34 (ISS) is an internationally recognized anatomical scoring system that provides an overall score for patients with multiple injuries. Injuries are allocated to 6 body regions: (i) head, (ii) face, (iii) chest, (iv) abdomen, (v) extremities (including pelvis), (vi) external. The ISS ranges from 0 to 75.
Insomnia Severity Index The Insomnia Severity Index35 (ISI) is a reliable and valid36 7-item self-report questionnaire measuring the patient’s perception of his or her insomnia. It evaluates, on a 5-point Likert scale, the severity of sleep onset, sleep maintenance, early morning awakening problems, sleep dissatisfaction, interference of sleep difficulties with daytime functioning, noticeability of sleep problems by others, and distress caused by the sleep difficulties.36 The total score ranges from 0 to 28.
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Resilience Is Associated With Fatigue After MTBI Ruff Neurobehavioral Inventory Pain was assessed by the Pain subscale of the Ruff Neurobehavioral Inventory,37 which comprises of 6 items on a 4-point scale, the score thus ranging from 6 to 24. Reliability and validity of the Ruff Neurobehavioral Inventory have been reported adequate.37 Beck Depression Inventory The Beck Depression Inventory–Second Edition38 (BDI-II) self-report questionnaire was used to assess depressive symptoms. In the questionnaire, subjects are asked to rate 21 items on a 4-point scale ranging from 0 to 3. The total score of the scale ranges from 0 to 63. To address the overlap effect of BDI-II with the BNI-FS and the ISI, the analysis in this study was conducted with a reduced item set for BDI-II. Three potentially confounding items (15, “loss of energy”; 16, “changes in sleeping patterns”; and 20, “tiredness or fatigue”) were removed from the BDI-II total score. Resilience Scale Resilience was assessed using the Resilience Scale11 (RS). It comprises 25 items, wherein the respondents are asked to state the degree to which they agree or disagree on a 7-point Likert scale from 1 (strongly disagree) to 7 (strongly agree). The possible total scores thus range from 25 to 175, with higher scores reflecting higher resilience. In this study, resilience was analyzed as a categorical variable using the following scoring for the total score presented by the original author9 : 25100 = very low; 101-115 = low; 116-130 = on the low end; 131-145 = moderate; 145-160 = moderately high; and 161-175 = high. The RS has been reported to be a reliable and valid tool to measure resilience.11 The psychometric properties of the Finnish version of the scale have been previously published by our group.39 Data analysis Differences between the MTBI and control groups were analyzed by using the Mann-Whitney U and Fisher exact tests. This was done to describe and examine the characteristics of the MTBI group in reference to controls and to examine whether the groups differed in symptoms and the course of fatigue. Adjustment for multiple comparisons was not considered necessary.40 Cohen d values were used to illustrate clinical significance. The coefficient correlations between the BNI-FS and the predictive variables were then calculated using the Spearman correlation analysis to demonstrate how the variables are associated and to examine whether the associations are different in patients and controls. Finally, multiple linear regression analysis was conducted to determine eventual independent predictors of the
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change in fatigue from 1 to 6 months. Variables with clinical interest and relevance were included in the regression model. This analysis was conducted only for the MTBI group, because the aim of this study was to examine the association of fatigue and resilience following MTBI. In addition, the amount of reported fatigue among controls was practically unchangeable throughout the follow-up period. The 3 demographic variables (age, gender, and education) and physical injuries (ISS) were controlled for by entering them into to the regression analysis first. In a second step, insomnia, pain, and depressive symptoms were simultaneously added to the model. After controlling for these factors, resilience was added to the model in the third step. Residuals of the regression analysis were found to be normally distributed. The statistical significance level was set to .05 for all the analyses. Statistical analyses were conducted using SPSS for Windows (version 20.0; SPSS Inc, Chicago, Illinois) with the supervision and help of a statistician (M.H.). RESULTS There were no statistically significant differences between the MTBI and control groups in age, education, gender, ISS, or the time interval from injury to 1 month questionnaires. The difference in days from injury to 6 months questionnaires between the MTBI (186 days) and control (193 days) groups was statistically significant. The difference in days is, however, subtle (7.7 days in a follow-up period of 6 months), and the finding can be considered clinically irrelevant. The characteristics of patients with MTBI and the control group are presented in Table 1. In the MTBI group, 15 patients (22.4%) had an acute traumatic lesion on the MR image. The MR images of all the controls were interpreted normal. The MTBI group tended to report more symptoms of insomnia than the control group, but the difference between the groups was not statistically significant. The MTBI and control groups did not significantly differ on pain, depressive symptoms, or resilience. The group differences between the MTBI and control groups on the predictive variables (ISI, Ruff Neurobehavioral Inventory, BDI-II, and RS) and fatigue variables (BNI-FS) are presented in Table 2. The patients with MTBI had a significantly higher level of fatigue at 1 month postinjury than the controls. However, there was a decrease in the level of fatigue in the patients with MTBI during follow-up. In the controls, no significant change in fatigue occurred. At 6 months after injury the difference on fatigue between the patients with MTBI and controls was not statistically significant. At 1 month postinjury, fatigue correlated significantly with insomnia, pain, and depressive symptoms in both the MTBI and control groups. However, significant correlation between resilience and fatigue was found only www.headtraumarehab.com
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JOURNAL OF HEAD TRAUMA REHABILITATION/MAY–JUNE 2015
Characteristics of patients with MTBI and orthopedic controls Patients with MTBI (n = 67)
Controls (n = 34)
Cohen d
Pa
25 (37.3)/42 (62.7) 37.0 (12.0) 14.3 (3.1) 25.3 (4.4) 185.7 (11.5) 3.7 (3.1)
19 (44.1)/15 (55.9) 39.1 (12.8) 14.3 (2.6) 23.9 (3.6) 193.4 (19.1) 2.5 (1.5)
0.17 0.02 0.35 0.54 0.45
.059 .431 .766 .081 .011b .089
Descriptive variables Gender (F/M), n (%) Age, mean (SD), y Years of education, mean (SD) Days from injury to 1 mo questionnaire, mean (SD) Days from injury to 6 mo questionnaire, mean (SD) Injury Severity Score, mean (SD)
Abbreviation: MTBI, mild traumatic brain injury. a Mann-Whitney P value in all but gender difference analysis in which the Fischer P value was used. b P < .05.
Group differences in fatigue and predictive variables at 1 month among patients with MTBI and the controls TABLE 2
Patients with MTBI (n = 67)
Controls (n = 34)
Cohen d
Pa
14.7 (15.1) 8.9 (12.0) − 5.8 (12.0) 5.3 (5.3) 8.2 (2.2) 3.7 (4.5) 138.9 (17.1)
7.2 (6.8) 6.9 (10.1) − 0.2 (10.3) 3.3 (3.5) 8.4 (2.6) 3.4 (4.2) 138.5 (16.1)
0.59 0.18 0.49 0.41 0.07 0.06 0.01
.025b .641 .050b .236 .943 .951 .733
Fatigue (BNI-FS) at 1 mo, mean (SD) Fatigue (BNI-FS) at 6 mo, mean (SD) Change in fatigue (BNI-FS) from 1 to 6 mo Insomnia (ISI) Pain subscale (RNBI) Depressive symptoms (BDI-II) Resilience (RS)
Abbreviations: BDI-II, Beck Depression Inventory–Second Edition; BNI-FS, Barrow Neurological Institute Fatigue Scale; ISI, Insomnia Severity Index; MTBI, mild traumatic brain injury; RNBI, Ruff Neurobehavioral Inventory; RS, Resilience Scale. a Mann-Whitney P value. b P < .05.
in patients with MTBI (see Table 3). At 6 months, fatigue correlated significantly with pain and depressive symptomps in both groups. In the MTBI group, resilience and insomnia were also significantly correlated with fatigue at 6 months. In patients with MTBI, the correlation between resilience and fatigue was even stronger at follow-up. In the controls, no correlation between resilience and fatigue was found.
Multiple regression analysis was done to examine the predictors of the change in fatigue from 1 to 6 months in the MTBI group. The demographic variables (age, gender, and education) and physical injuries (ISS) did not predict change in fatigue (adjusted R2 = −0.055; P = .968). Adding insomnia, pain, and depressive symptoms simultaneously to the model at the next step produced a significant change (P = .033), but the model did
TABLE 3 Correlations between the predictive variables (at 1 month) and fatigue (BNI-FS total scores) at 1 and 6 months Patients with MTBI (n = 67) Variables Insomnia (ISI) Pain (RNBI) Depressive symptoms (BDI-II) Resilience (RS)
Controls (n = 34)
Fatigue at 1 mo (BNI-FS)
Fatigue at 6 mo (BNI-FS)
Fatigue at 1 mo (BNI-FS)
Fatigue at 6 mo (BNI-FS)
0.67a 0.39a 0.39b − 0.26b
0.50a 0.54a 0.39a − 0.45a
0.42b 0.54a 0.42b − 0.26
0.24 0.48a 0.42b − 0.27
Abbreviations: BDI-II = Beck Depression Inventory II–Second Edition; BNI-FS, Barrow Neurological Institute Fatigue Scale; ISI, Insomnia Severity Index; MTBI, mild traumatic brain injury; RNBI, Ruff Neurobehavioral Inventory; RS, Resilience Scale. a P < .01. b P < .05.
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Resilience Is Associated With Fatigue After MTBI not reach statistical significance (adjusted R2 = 0.043; P = .215). After controlling for the aforementioned variables, resilience added significantly (P = .006) to the model. The final step of the regression model (see Table 4) significantly (adjusted R2 = 0.145; P = .026) predicted the change in fatigue from 1 to 6 months after MTBI. In this final model, insomnia was found to be a significant predictor besides resilience. Depressive symptoms had a trend toward significance, but resilience was the strongest predictor. In the regression model, all variance inflation factor values were under 1.8. Figure 1 illustrates the association of resilience and fatigue by presenting the level of fatigue at both
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measurements (1 and 6 months) in patients groups divided by their resilience scores. DISCUSSION The main finding of this study was that even when controlled for the factors known to be associated with fatigue (depression, sleep disorders, and pain), resilience was a significant predictor of the change in fatigue from 1 to 6 months after injury. This finding concurs with previous findings from other medical conditions.12,13 This is the first study to report this phenomenon in patients with MTBI, although in many previous
Results of the final multivariate regression model for the change in fatigue from 1 to 6 months postinjury in patients with MTBI TABLE 4
Block
Gender (males) Age Years of education Injury severity (ISS) Insomnia (ISI) Pain (RNBI) Depressive symptoms (BDI-II) Resilience (RS)
1 Standardized β
P
−.011 −.073 −.030 −.043
.935 .569 .814 .741
2 Standardized β
P
−.080 −.094 −.067 −.011 −.266 −.119 −.072
.531 .447 .606 .933 .071 .427 .625
3 Standardized β
P
− .142 − .134 − .029 .037 − .279 − .117 − .257 − .380
.249 .254 .812 .764 .046a .409 .098 .006
Abbreviations: BDI-II, Beck Depression Inventory–Second Edition; ISI, Insomnia Severity Index; ISS, Injury Severity Index; MTBI, mild traumatic brain injury; RNBI, Ruff Neurobehavioral Inventory; RS, Resilience Scale. a P < .05.
Figure 1. Mean fatigue scores (BNI-FS) of patient groups stratified by different levels of resilience. BNI-FS indicates Barrow Neurological Institute Fatigue Scale; MTBI, mild traumatic brain injury.
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studies, it has been shown that psychological factors such as depression or stress are associated with fatigue. The current study shows that in a healthy population as well, with no previous psychiatric problems, resilience is associated with the recovery from fatigue. This is in line with other preliminary findings on resilience and MTBI, which have suggested resilience to be a significant contributor to the severity of postinjury anxiety and postconcussive symptoms.18 Resilience correlated significantly with fatigue only in patients with MTBI and the correlation strengthened during follow-up. The level of resilience did not differ between the MTBI and control groups. This would be expected if we define resilience as a personality trait that it was originally referred to.41 The term “resilience” has, however, been not only used to refer to a dynamic developmental process42 and considered as an innate characteristic each person possesses to some degree but can also be enhanced or diminished depending on life circumstances.43 We did not have data on the level of resilience before the injuries, and it was not in the scope of this study to examine the factors associated with resilience. Further research about the stability of resilience after MTBI is thus needed. The results of this study also support the established knowledge about fatigue being an eminent symptom after MTBI. The comparison with the control group demonstrated that the course of fatigue was different after MTBI than after an orthopedic injury. The level of fatigue was found to be significantly higher in patients with MTBI than in the controls at 1 month after the injury. However, there was a significant decrease in the level of fatigue in patients with MTBI during follow-up. At 6 months after injury, there was no significant difference between patients with MTBI and controls regarding self-reported fatigue. Depressive symptoms, sleep disorder, and pain were assessed as confounding factors. In relation to these factors, comparisons between the patients with MTBI and controls were conducted. The patients with MTBI reported slightly more insomnia symptoms than the controls, but the difference was not statistically significant. On pain or depressive symptoms, the MTBI and control groups did not significantly differ. The lack of differences between the groups might partly be explained by the symptoms induced by the physical injuries of the controls. In MTBI literature, comparison with trauma controls (eg, orthopedically injured controls) has been called for. The main reason for this is the unspecific nature of post-TBI symptoms. MTBI-like symptoms are also commonly reported by patients with non-TBI.44 Our results support these findings. Furthermore, our findings show that symptom endorsement among this rigorously selected sample of previously healthy patients with MTBI was not
considerably higher than in controls with an orthopedic injury. Despite the fact that the patients with MTBI and controls did not significantly differ on the aforementioned controllable factors, this study provides further support that insomnia, pain, and depressive symptoms correlate with fatigue after MTBI. It was not the intention of this study to examine their individual effects. However, the results emphasize the identification and treatment of sleep disorders, pain, and depressive symptoms in the management of fatigue after MTBI. It has been previously noted that fatigue, secondary to sleep disturbance, would require a diagnostic and treatment approach different from fatigue due to affective disorders or attention problems.28 Also different treatments, such as teaching good sleep habits (sleep hygiene), may be needed to assist in minimizing any associated distress.45 Furthermore, the importance of early identification and intervention of pain has previously been recommended for patients with MTBI.23 This is the first study to report the association of resilience and fatigue after MTBI. It was beyond the scope of this study to examine the mechanisms or possible physiological underpinnings of this association. It can be hypothesized that the association of resilience and fatigue could be driven by the ability of resilient individuals to adjust and moderate the effects of stress. Coping styles have previously been associated with the outcome of MTBI.46,47 In future research, coping styles among other outcome moderators should be studied in relation to resilience and fatigue. In addition, more research about the role of resilience in recovery from MTBI is needed before making firm statements about the clinical implications of this finding. It has previously been reported in patients with cancer that psychological support focusing on providing strategies to improve resilience might be promising when having to undergo stressful treatments12 because fatigue is determined to some extent by the psychological capacity to deal with patterns of stress related to threat and illness. It has also been proposed that prospective follow-up studies should be done to determine temporal relationships between fatigue and stress early after injury. In addition, nonreferred samples could help determine the optimal timing of interventions such as cognitive-behavioral therapies and stress management.8 It has been noted that after MTBI, fatigue and psychological factors require early treatment to prevent symptom exacerbation.2 Our results also refer that previously healthy patients with MTBI might benefit from early postinjury guidance in the management of fatigue. Future research on the possible interventions is needed. There are some limitations to this study that should be considered when drawing clinical conclusions about the results. By applying strict exclusion criteria, we
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Resilience Is Associated With Fatigue After MTBI enrolled only 2.48% of all consecutively screened patients with head computed tomography due to an acute head injury. Excluding patients with preexisting conditions weakens the generalizability of the results into everyday clinical practice. It has been previously noted by our group32 that, for example, older adults and patients with preexisting neurological or psychiatric problems are frequently seen in the ED because of MTBI, but they are often excluded from clinical studies. These limitations with patient selection have been discussed in more detail in a previous publication of our study group.32 In the current study, our aim was to obtain a homogeneous MTBI population in order to avoid possible bias due to a heterogeneous sample. To enhance the validity of our data, we carefully excluded all premorbid conditions (substance abuse, prior psychiatric disorders or neurological problems, previous brain injuries) to rule out the possible influence of premorbid moderator variables. Thus, examining a premorbidly healthy, homogeneous sample can also be seen as strength. The
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second limitation of this study is the overlap of the measured constructs. In this study, we aimed to reduce the overlap effect of BDI-II with BNI-FS and ISI by conducting the analysis with a reduced item set for BDI-II (with 3 potentially confounding items removed). Third, the number of subjects in this study was relatively small and therefore future studies are needed to confirm the results. Despite these limitations, we have been able to overcome many of the challenges of previous studies by using a longitudinal study design with high follow-up rates and minimal confounding factors. The inclusion of an orthopedic control group enrolled with the same exclusion criteria gives further strength to the study. CONCLUSION Our results show that resilience is a significant predictor of self-reported fatigue following MTBI. Resilience seems to be a relevant factor to be considered in the management of fatigue after MTBI.
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