Neurobehavioral Symptoms and Family Functioning in Traumatically Brain-Injured Adults

Archives of Clinical Neuropsychology, Vol. 13, No. 8, pp. 695–711, 1998 Copyright © 1998 National Academy of Neuropsychology Printed in the USA. All rights reserved 0887-6177/98 $19.00 ⫹ .00

PII S0887-6177(98)00005-5

Neurobehavioral Symptoms and Family Functioning in Traumatically Brain-Injured Adults Kevin N. Groom, Terry G. Shaw, Mary E. O’Connor, Nicole I. Howard, and Angela Pickens University of Tulsa

Traumatic brain injury (TBI) often results in a myriad of symptoms across physical, cognitive, and neurobehavioral domains. Despite inherent limitations associated with physical or cognitive impairments, the extant literature suggests that neurobehavioral symptoms tend to be the most distressing symptoms for the family and are more strongly related to poor outcome for the patient. The Neuropsychology Behavior and Affect Profile (NBAP) along with the General Functioning subscale of the Family Assessment Device (FAD-GF) and the Perceived Stress Scale were administered to 153 family members of persons who had sustained a TBI. The results provide new normative data and statistical support for the NBAP as a promising measure of neurobehavioral symptomatology following TBI. The correlation of .54 (p ⬍ .01) between FAD-GF and Full Scale NBAP scores provides powerful support for the hypothesis that family dysfunction is related to the presence of neurobehavioral symptoms in the patient. NBAP domains of Depression, Inappropriateness, Pragnosia, and Indifference appear most strongly related to family functioning and also bear a significant relationship to caregiver stress level and patient unemployment, whereas injury severity had little impact on either family functioning or neurobehavioral symptoms. The findings reinforce the significance of neurobehavioral symptoms and fortify their proposed link to family dysfunction post-TBI. © 1998 National Academy of Neuropsychology. Published by Elsevier Science Ltd

Traumatic brain injury (TBI) is a devastating medical condition because it not only affects the victim but the victim’s family as well by changing the entire family system (Del Orto & Power, 1994). Indeed, nowhere are the effects of TBI felt more strongly than within the context of the family of brain injury survivors. Historically, brain injury rehabilitation has placed greater emphasis on recovery from physical rather than emotional or behavioral disability. Although patients and family members agree that physical disability is an important concern, there is a substantial body of literature indicating that emotional and behavioral disability is a more prolific obstacle to positive psychosocial

We thank each of the participants and their injured relatives for their cooperation in the research project. Several support-group leaders took a special interest in this project and facilitated its completion: Charlotte Bowen, Rod Davidson, Steve Cowden, Gia Scott, Linda Morris, and Barbara Loper. Address correspondence to Kevin N. Groom, 7146 S. Braden, Suite #500, Tulsa, OK 74136.

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outcome and intact family functioning (Grant & Alves, 1987). Kendall and Terry (1996) summarized the predicament as follows: Attempts to account for the variance in psychosocial adjustment among individuals with TBI have relied on neurological variables as explanatory constructs. Although there is evidence that these neurological variables do influence psychosocial outcome, they cannot account completely for the variation in levels of adjustment noted in the TBI literature. The challenge to researchers in this area has, therefore, been the identification of the non-neurological factors that might account for the remaining variance in psychosocial outcome. (pp. 124–125)

As the preeminence of neurobehavioral symptoms in long-term recovery emerges, researchers have demonstrated that family members experience considerable distress following TBI and that a relationship exists between family distress and neurobehavioral symptomatology. However, defining the nature of that relationship has usually been a secondary goal of these research projects, and widely discrepant methodologies have been employed.

THE INFLUENCE OF TBI ON THE FAMILY Cognitive changes are troublesome to families of TBI patients, but “of much greater worry to relatives was the change in personality in the patient which, the relatives felt, overshadowed all other changes” (Brooks, 1984, p. 126). Therefore, just as the neurobehavioral symptoms of TBI exert a disproportionate effect on recovery for the braininjured individual, so too these symptoms exert a disproportionate effect on family adjustment to injury (Brooks, 1984; Cavallo, Kay, & Ezrachi, 1992; Hall et al., 1994; Stambrook, Peters, & Moore, 1989; Thomsen, 1984). This belief has come to be so widely held by researchers that a maxim has developed: Family members find the behavioral and emotional changes associated with TBI most distressing. Unfortunately, family degradation is all too commonplace in this population. For example, Anderson-Parente, DiCesare, and Parente (1990) found that more than two thirds of marriages in which one partner sustained a TBI ended in divorce within 2 years postinjury. Moreover, family disruptions have also been shown to occur at an even higher rate in head injury populations than in other traumatic conditions such as spinal cord injuries (Rosenbaum & Najenson, 1976; Thomsen, 1984). The process of emotional adjustment to TBI for family members is so dramatic that several writers have compared it to the Kubler–Ross model of predictable psychological reaction following the death of a loved one (e.g., Groveman & Brown, 1985; Romano, 1974). One characteristic separating TBI from other medical conditions and from death of a loved one is that important neurobehavioral symptoms may not subside and may even grow more severe over time. For example, Hall et al. (1994) found that caregivers had more severe complaints about their head-injured relative after 2 years postinjury than at 6 months. This can create a confusing inverse relationship whereby physical impairments often stabilize within the first year postinjury, whereas psychosocial impairments may proliferate over the same time period as the patient regains physical stamina and energy. Studies on family member adjustment have revealed depression, anxiety, and other psychological disorders. McKinlay, Brooks, Bond, Martinage, and Marshall (1981) demonstrated that the amount of stress experienced by relatives did not diminish from the 3rd to the 12th month postinjury and was also related to the incidence of mental and behavioral changes in the patient. In like manner, Livingston, Brooks, and Bond (1985) re-

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ported that 30% of caregivers had sufficient emotional problems to warrant clinical intervention and that this proportion increased from the first to the fifth year. Livingston et al. also reported that 30% of relatives have levels of anxiety likely to be of clinical significance and twice the level of psychiatric problems found in the general population. Grant and Alves’s (1987) review of several studies suggests that approximately half of TBI patients will “resume productive lives” (p. 248). Prediction of those individuals most likely to thrive following TBI is not as simple as inspecting traditional measures of injury severity such as length of coma, length of posttraumatic amnesia, or severity of cognitive impairments (Kendall & Terry, 1996). Although isolated neurobehavioral symptoms (e.g., social withdrawal) may be strongly related to injury severity, a host of other neurobehavioral symptoms (e.g., anxiety, tension, depression, hostility, and suspiciousness) have not proven to be strongly related to injury severity (Levin & Grossman, 1978). Levels of psychological distress and psychosocial changes in family members do not bear a simple relationship to injury severity either (Bond, 1975). For example, in the case of caregiver subjective burden, McKinlay et al. (1981) demonstrated a significant positive correlation with injury severity at both 3 and 6 months postinjury. At 1 year postinjury, however, these authors reported that the relationship between injury severity and subjective burden had evaporated. Because it has been established that neurobehavioral symptoms are the most problematic changes for families, several attempts have been made to delineate which neurobehavioral symptoms are most problematic. Indeed identifying the patient symptoms most detrimental to family functioning could prompt the development of practice protocols that place high priority on their mitigation. To this end, Zarski, DePompei, and Zook (1988, p. 40) accurately stated, “Knowing which families are more at-risk than others for catastrophic reactions would be invaluable information and would enable rehabilitation professionals to make important treatment decisions relative to type of intervention.” Using widely varying methodologies, researchers have generated the following list of neurobehavioral symptoms as most troubling to families of patients with TBI: pathological laughter (Thomsen, 1974); verbal expansiveness and confusion (Oddy, Humphrey, & Uttley, 1978); childishness, lability, adynamia, irritability, and aggression (Kreutzer, Marwitz, & Kepler, 1992); egocentricity, dependence, and poor insight (Rosenbaum & Najenson, 1976); and social withdrawal and anger/disinhibition (Hall et al., 1994). A cursory review of this body of literature suggests little agreement across studies. The method of surveying at the symptom level has contributed to the broad variability that currently exists. Instruments that approach neurobehavioral symptoms from a factorial perspective as opposed to a checklist perspective are less likely to produce such disparate findings across samples. Instead, researchers could ask families about the current status of their family and about neurobehavioral symptoms via separate instruments designed for each purpose. To date, no studies have approached the problem in this manner. Researchers who have reported on neurobehavioral symptoms have failed to make family distress their primary area of inquiry. Various aspects of family functioning have been shown to account for a sizable proportion of variance in recovery from several physical disabilities and diseases such as AIDS, multiple sclerosis, cancer, and cystic fibrosis (Patterson, Hamilton, & Warren, 1990; Rait, Ostroff, Smith, & Cella, 1992). In addition, an elegant study by Evans et al. (1987) was conducted with stroke patients and their families considering the relationship between poor family functioning and recidivism to inpatient treatment. Evans et al. found that an unsupportive family may unknowingly interfere with stroke recovery. These data suggest practical reasons for considering family functioning as an important, quantifiable variable in the recovery of patients with central nervous system impairment.

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EMPIRICAL ASSESSMENT OF NEUROBEHAVIORAL SYMPTOMS Neurobehavioral symptoms include psychological, emotional, social, and behavioral problems associated with central nervous system impairment such as somatic concern, anxiety, emotional withdrawal, socially inappropriate comments, aggressive behavior, guilt feelings, agitation, poor insight, depressive mood, irritability, disdain for authority, suspiciousness, unusual thought content, pragmatic communication deficits, and mood lability. Unfortunately, precise classification of neurobehavioral changes has not been accomplished, and they are among the last changes to be quantified (Grant & Alves, 1987). Neuropsychologists currently expend greater energy attempting to assess cognitive disturbances accurately and often ignore emotional, psychosocial, and family disturbances. This inattention is analogous to the historical inattention to cognitive factors of early brain injury rehabilitation programs while paying steadfast attention to physical disability (Alfano & Finlayson, 1987). However, major neuropsychological thinkers such as Ralph M. Reitan have propounded the inclusion of personality, behavior, and emotional status as part of comprehensive neuropsychological assessment (Reitan & Wolfson, 1985). Many neuropsychologists simply rely on clinical observations to provide information in neurobehavioral areas. This method could be justified if one of the following three criteria were met: (a) other rehabilitation professionals routinely carry out thorough assessment of these domains, (b) these domains are relatively less important to the patient’s ultimate recovery than other domains, or (c) no satisfactory instruments exist with which to measure these symptoms. Unfortunately, it would be difficult to make a case that any one of these three criteria is currently met. First, neurobehavioral symptoms are often informally appraised by speech pathologists, physical therapists, occupational therapists, physiatrists, and case managers, but these areas are seldom formally assessed by anyone. Second, these neurobehavioral domains are, to an even greater degree than cognitive symptoms, critical to the patient’s ultimate recovery and are not so refractory to treatment as to be ignored (Grant & Alves, 1987). Third, psychometric instruments have recently been developed that measure these domains. Neuropsychologists have generally opted to use traditional self-rated personality measures and have created only a small number of unpopular instruments designed specifically to measure psychosocial symptoms. In lieu of neurobehavioral measures, “what can be measured (some cognitive capacities, for instance) is inspected for reflections of what cannot be measured (motivation and self-critical concerns, for example)” (Alexander, 1987, p. 192). The most ambitious attempt to quantify crucial neurobehavioral information has come from Linda Nelson and colleagues, who developed the Neuropsychology Behavior and Affect Profile (NBAP), which was published for consumer use in 1994 (Nelson, Satz, & D’Elia, 1994). Because the NBAP is new, critical analyses of its psychometric properties have yet to be published, and representative normative data are lacking. The test was developed specifically with the goal of redressing the inattention paid to neurobehavioral symptoms in the assessment of patients with TBI as well as other syndromes of brain dysfunction such as stroke and dementia (Nelson, Mitrushina, Satz, Sowa, & Cohen, 1993). The NBAP is one of very few instruments that provides information pertaining to the neurobehavioral status of cognitively impaired persons. Aware of the drawbacks inherent in employing self-report or examiner ratings of neurobehavioral symptoms in TBI, Nelson and colleagues made an effort to enlist the perspective of family members in the construction of the NBAP. The NBAP is a 106-item measure of emotional and behavioral functioning in persons

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with brain impairment. Family members are asked to either “agree” or “disagree” in response to statements about the patient such as, “The patient has difficulty making decisions.” The test is made up of five rationally derived scales. Based on a review of relevant literature, the authors suggested that patterns of emotional responding showing some association with focal or lateralized brain dysfunction fall roughly into five major categories: 1. Indifference: An indifference to or denial of an illness or a tendency to minimize a disability or current condition (e.g., “My relative seems unusually unaware of any existing health problems”). 2. Mania: Elevated, expansive, or irritable mood; sustained high energy or activity; or impulsivity (e.g., “My relative is excessively talkative”). 3. Depression: Dysphoric mood, apathy, withdrawal, crying behavior, or loss of interest or pleasure in most usual activities (e.g., “My relative often seems unhappy”). 4. Inappropriateness: Behavior that is bizarre or inappropriate to the context in which it is occurring or to an outside event (e.g., “My relative has habits which seem odd and different”). 5. Pragnosia: A defect in the pragmatics of communicative style (e.g., “My relative often seems to ‘miss the point’ of the discussion”). Test-retest reliability estimates of the five NBAP subscales range from .92 to .97 (Nelson et al., 1989). Normative data are provided separately for small TBI, stroke, and dementia samples for both premorbid (”Before”) and current (”Now”) ratings for each of the five subscales.

PURPOSE OF THE CURRENT STUDY In light of the preceding information, this research project was devised to describe more completely the nature of the relationship between particular neurobehavioral symptoms in TBI patients as measured by the NBAP and the corollary functioning of the patient’s family. Another goal of this project was to provide additional information regarding the psychometric properties of the NBAP. The current study is the first of its kind to employ a neurobehavioral assessment devised specifically for TBI along with a widely used measure of family functioning, the Family Assessment Device (FAD), which has been used previously in TBI samples (Bishop & Miller, 1988). Because of their unique perspective, attempts were made to enlist the participation of family members in the gathering of neurobehavioral information. Additional outcome variables such as individual stress levels of caregivers and employment status of patients were also compared to patients’ neurobehavioral symptoms. Potential moderating influences of demographic, family-related, and injury-related variables help contextualize the larger findings. The NBAP is discussed with respect to a substantially larger TBI population than was previously available.

METHOD Participants One hundred seventy-eight family members volunteered to participate in the study. Seven respondents were not included in the analysis because they left a significant number of questions unanswered (i.e., more than five). Eighteen pairs of individuals re-

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K. N. Groom et al. TABLE 1 Demographic Characteristics of the Sample (N ⫽ 153) Caregivers

Age (years) Education (years)

Employed Female

Patients

M

SD

M

SD

49.2 14.1

13.3 2.5

36.1 13.0

15.3 2.8

n

%

n

%

92 123

63.9 80.3

43 57

28.9 37.2

sponded to the questionnaire in reference to the same patient; most commonly, a mother and father both reported on their son who was injured. In these cases, one of the pair was removed at random so that no patient was rated by more than one family member. After these were excluded, 153 family members (123 women, 30 men) of persons who had sustained a TBI (57 women, 96 men) were included in the analysis. Demographic characteristics of the sample are reported in Table 1. Participants were recruited and informed about the study in two ways. Most participants (86%) were recruited while attending local support-group meetings of the National Brain Injury Association. The remaining participants were recruited while their significant other completed a neuropsychological evaluation. Participants were most commonly mothers, fathers, wives, or husbands of the patient with the TBI. A smaller percentage of participants (13.7%) were siblings, grandparents/ grandchildren, aunts/uncles, nieces/nephews, or close friends of the patient. Participants were 92.8% White, 2.9% Native American, 2.2% African American, and 2.2% Hispanic. Most of the family member participants were employed (63.9%) at the time of the survey, but most patients were unemployed (71.1%). Education level was significantly higher for female TBI patients (M ⫽ 13.8 years, SD ⫽ 2.8) than for their male counterparts (M ⫽ 12.6 years, SD ⫽ 2.8), t(147) ⫽ 2.59, p ⬍ .05. Injury Characteristics Characteristics of the patients’ injuries are shown in Table 2. Median elapsed time postinjury was 4.2 years, ranging from 1 month to 40 years. Median length of coma was 14 days, ranging from no appreciable loss of consciousness (LOC) to 365 days. Alfano, Neilson, Paniak, and Finlayson (1992) defined moderate or severe TBI as LOC of 6 hr or greater. Using this standard, the present sample consisted of 80.4% moderate or severe and 19.6% mild TBI.

TABLE 2 Injury Characteristics of the Sample

Coma duration (days) PTA duration (days) Time postinjury (days)

Median

M

SD

n

14.0 46.0 4.2

38.4 94.8 7.7

62.8 128.5 8.0

138 120 153

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Materials The questionnaire was composed of five sections: informed consent, demographic questions, the FAD-GF, the Perceived Stress Scale (PSS; Cohen, Kamarck, & Mermelstein, 1983), and the NBAP. The current study utilized the version of the NBAP intended for administration to a relative of the patient that is described by test authors as “a more objective measure of change in personality and affect” (Nelson et al., 1994, p. 7). Respondents were asked to answer with respect to their significant others’ current level of postinjury functioning (i.e., Now version). The FAD was designed to provide therapists and researchers with reliable and valid information regarding clinically relevant family dimensions and to identify problem areas in a simple and efficient manner (Epstein, Baldwin, & Bishop, 1983). This approach seems especially suited to head-injured populations and has been previously utilized in this arena (Zarski et al., 1988). The 12-item FAD-GF, which assesses the overall health and pathology of the family, was used. The 14-item PSS measures the overall amount of strains and tension a respondent has felt during the past month. The PSS contains semantically differentiated statements relating to one’s global stress level using values ranging from 1 (never) to 5 (very often). Family member participants were asked to complete this scale with regard to their personal experiences and not in relation to the TBI survivor. Procedure Permission to attend brain injury support group meetings was obtained from presidents of six Midwestern state head injury foundations and respective support group leaders. Surveys were administered subsequent to dividing groups into “family members” and “survivors” to maximize concentration on the questionnaire. As mentioned before, additional data were collected during outpatient neuropsychological evaluations conducted by a board-certified neuropsychologist at three rehabilitation hospitals. For patients who met the inclusion criteria, their accompanying family member was asked to complete the evaluation.

RESULTS The results are presented in two sections: (a) internal analyses of the psychometric properties of the NBAP and (b) external analyses of the interrelationships among NBAP and other pertinent variables. Internal Analyses of the NBAP Descriptive statistics. Nelson et al. (1994) reported normative data on the NBAP for a sample of 42 TBI patients and for 54 controls with no history of TBI. Their clinical sample was recruited from head injury support groups across the United States, and their controls were undergraduate students at a Western university who rated a relative with no history of neurotrauma. All of the patients in Nelson’s clinical sample were more than 6 months postinjury. Applying this same restriction, the present sample was reduced to 145 patients for the internal analyses. Based on the methodology of Nelson and colleagues, mean percentage of items endorsed for each NBAP subscale was calculated (see Table 3). Participation from a new control group of 27 family members (13 women, 14 men;

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K. N. Groom et al. TABLE 3 Mean Percentage (and SD) of NBAP Items Endorsed by the Sample Current Study

Indifference Inappropriateness Pragnosia Depression Mania Full Scale NBAP

TBI (n ⫽ 145)

Student Controls (n ⫽ 27)

33 (27) 48 (29) 35 (25) 44 (30) 33 (21) 39 (20)

12 (10) 15 (24) 8 (09) 19 (19) 26 (22) 16 (11)

Nelson et al. (1994)

t

TBI (n ⫽ 42)

Student Controls (n ⫽ 54)

7.1* 6.4* 10.1* 5.9* 1.9 8.6*

25 32 21 64 19 32

07 18 10 12 17 13

Note. NBAP ⫽ Neuropsychology Behavior and Affect Profile. TBI ⫽ traumatic brain injury. *p ⬍ .01.

mean age ⫽ 34.0 years, SD ⫽ 10.7) of community college students (17 women, 10 men; mean age ⫽ 29.0 years, SD ⫽ 10.0) was enlisted. These participants volunteered for extra credit in two introductory level psychology courses. Their respective family members were asked to complete the NBAP, substituting the student for the patient. The mean percentage of items endorsed on the Full Scale NBAP (mean score of the five subscales) in our control sample was 16 (SD ⫽ 11), which was significantly lower than the clinical sample mean of 39 (SD ⫽ 20; see Table 3). With the notable exception of Mania, each of the NBAP subscales in our study was significantly higher in the clinical group than in the controls (see Table 3). These differences provide further evidence for the discriminant validity of the NBAP in TBI samples. Scores on four of the five scales were higher in our clinical sample (ranging from 33 for Indifference to 48 for Inappropriateness) than Nelson’s previous normative clinical sample (ranging from 19 for Mania to 64 for Depression). Reliability. Internal consistency reliability was calculated for each of the five subscales on the clinical sample. Based on the criteria of Cicchetti (1994) for comparing coefficient alphas, all scales had fair to good coefficient alpha values that ranged from .79 for Inappropriateness to .85 for Depression (see Table 4). Using the same criteria, the alpha value for the entire NBAP was excellent (.92). Mean inter-item correlation of the five subscales ranged from .19 for Mania to very near .30 for each of the other four subscales (see Table 4). TABLE 4 Internal Consistency of NBAP, FAD-GF, and PSS (N ⫽ 145)

NBAP (66 items) Indifference (12 items) Inappropriateness (7 items) Pragnosia (12 items) Depression (11 items) Mania (24 items) FAD-GF (12 items) PSS (14 items)

Alpha

Mean Inter-item Correlation

.92 .81 .79 .80 .85 .85 .92 .82

.15 .27 .34 .25 .34 .19 .50 .35

Note. NBAP ⫽ Neuropsychology Behavior Affect Profile. FAD-GF ⫽ Family Assessment Device-General Functioning subscale. PSS ⫽ Perceived Stress Scale.

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TABLE 5 Correlations of NBAP With FAD-GF and PSS (N ⫽ 153)

Full Scale NBAP Indifference Inappropriateness Pragnosia Depression Mania

FAD-GF

PSS

.54* .40* .44* .40* .44* .29*

.28* .29* .24* .13 .24* .12

Note. NBAP ⫽ Neuropsychology Behavior Affect Profile. FAD-GF ⫽ Family Assessment Device-General Functioning subscale. PSS ⫽ Perceived Stress Scale. *p ⬍ .01.

Factor analysis. Results of a principal components, varimax-rotated factor analysis at the item level provided solid support for the use of the five factors as constructed by test authors. Seventy-four percent or 49 of the 66 items on the NBAP loaded on their respective factor. Together, these five factors accounted for 39.2% of the total variance of the scale. The eigenvalues (with percentage of variance accounted for in parentheses) for the five factors are as follows: Depression ⫽ 12.0 (18.1), Indifference ⫽ 5.6 (8.5), Inappropriateness ⫽ 3.2 (4.8), Mania ⫽ 2.7 (4.1), Pragnosia ⫽ 2.5 (3.7). Rotated factor analysis at the scale level suggests that the two mood subscales, Depression and Mania, are unique enough to constitute their own factors and appear sensitive to mood states. These two factors are smaller than a large, common factor comprised of Pragnosia, Indifference, and Inappropriateness that appears more sensitive to general neurobehavioral symptomatology unrelated to mood fluctuations. External Analyses of the NBAP FAD. The full sample of 153 will be used for the statistics presented in the External Analyses section (except in cases of missing data in which the sample size will be specified). A mean score of 2.06 (SD ⫽ 0.60) on the FAD-GF scale reflected significantly more family disturbance in our sample than Kabacoff, Miller, Bishop, Epstein, and Keitner’s (1990) normative sample of 627 persons whose mean was 1.84 (SD ⫽ 0.43), t(778) ⫽ 4.40, p ⬍ .01. However, our families function significantly better than the Kabacoff et al. psychiatric sample (n ⫽ 1,138), whose mean was 2.27 (SD ⫽ 0.51), t(1289) ⫽ ⫺4.13, p ⬍ .01, and the mean FAD-GF score for our TBI sample is almost identical to the mean of 2.07 for another TBI sample of 60 families that completed the FAD-GF (Kreutzer, Gervasio, & Camplair, 1994b). NBAP subscales each achieved moderately high, statistically significant correlations with the FAD-GF scale, and the hypothesis that neurobehavioral symptomatology is related to family functioning was supported. Indeed, the Pearson product–moment correlation between Full Scale NBAP and FAD-GF scores was .54 (p ⬍ .01). The hypothesis that specific types of neurobehavioral symptoms are more strongly related to family functioning than others was supported as well. The Mania subscale, although significantly positively correlated with FAD-GF scores (r ⫽ .29, p ⬍ .01), may have less clinical or practical utility than Indifference, Inappropriateness, Pragnosia, and Depression inasmuch as each of these scales achieved correlations above .40 (p ⬍ .01) with that measure (see Table 5). Stepwise multiple regression analysis suggested that Depression and Inappropriateness may be the best predictors of family functioning (R2 ⫽ .29, p ⬍ .001), together accounting for over one fourth of the variance in FAD-GF scores (see Table 6). Inclusion

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K. N. Groom et al. TABLE 6 Stepwise Regression Analyses for NBAP Scales Predicting FAD-GF and PSS Predicting FAD-GF

NBAP Scales

Step 1 Inappropriateness Step 2 Inappropriateness Depression

Multiple R

R2

F

SE

B

SE B

␤

.44

.20

37.1a*

.54

.88

.14

.44

.66 .65

.15 .14

.32 .33

.54

.29

30.5b*

.51

Predicting PSS

Step 1 Indifference

.29

.08

13.8a*

8.7

9.7

2.6

.29

Note. NBAP ⫽ Neuropsychology Behavior Affect Profile. FAD-GF ⫽ Family Assessment Device-General Functioning subscale. PSS ⫽ Perceived Stress Scale. SE ⫽ standard error. adf ⫽ 1, 151. bdf ⫽ 2, 150. *p ⬍ .01.

of the three remaining scales into the regression equation does not account for an important increase in proportion of variance in family functioning (R2 ⫽ .32, p ⬍ .001). PSS. Cohen et al. (1983) provided norms for the PSS for the population and for a group of individuals trying to quit smoking. By comparison, individual stress levels of caregivers of TBI patients in this sample (M ⫽ 25.8, SD ⫽ 9.0) were significantly higher than the general population mean provided by Cohen et al. (1983; M ⫽ 23.3, SD ⫽ 7.5), t(597) ⫽ 3.21, p ⬍ .01, but quite comparable to 64 individuals attempting to end smoking habits (M ⫽ 25.0, SD ⫽ 8.0), t(215) ⫽ .66, p ⬎ .05. Additionally, neurobehavioral symptoms were significantly related to individual stress levels in caregivers. The correlation between Full Scale NBAP scores and PSS scores was .28 (p ⬍ .01; see Table 5). Closer inspection reveals that only three of the five NBAP subscales achieved significant positive correlations with PSS scores, Indifference, Inappropriateness, and Depression (see Table 5), which suggests that these symptoms are more strongly related to caregiver stress than are Pragnosia and Mania. Stepwise multiple regression analysis indicated that Indifference was the single best predictor of PSS scores (R2 ⫽ .08, p ⬍ .001), but it accounted for less than 10% of the variance in PSS scores (see Table 6). Adding the four remaining NBAP scales into the regression equation minimally increased the proportion of variance accounted for in PSS scores (R2 ⫽ .13, p ⬍ .001). Injury severity and time postinjury. Data regarding length of coma, as measured in days, was available for 138 patients. Correlations between patients’ length of coma and Full Scale NBAP (r ⫽ .08), FAD-GF scores (r ⫽ .16), and PSS scores (r ⫽ ⫺.07) were all nonsignificant at the .05 level. Because the distribution of patients’ length of coma was heavily positively skewed, patients were subdivided into quartiles. As shown in Table 7, severity of injury rank was not significantly correlated with Full Scale NBAP scores and was positively correlated with only one of the five subscales, Inappropriateness. The table also illustrates that severity of injury rank was not significantly correlated with FADGF or PSS scores. Analyses of variance suggests that the four injury severity groups that were created did not significantly differ from one another on Full Scale NBAP, Indifference, Pragnosia, Depression, Mania, FAD-GF, or PSS but were significantly different on

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TABLE 7 NBAP, FAD-GF, PSS Scores by Severity of Injury Rank Severity of Injury Rank

Full Scale NBAP Indifference Inappropriateness Pragnosia Depression Mania FAD-GF PSS Percentage employed

1 (n ⫽ 38)

2 (n ⫽ 38)

3 (n ⫽ 31)

4 (n ⫽ 32)

F(3, 135)

r

34 28 36 35 48 25 2.00 28.1 21

40 32 47 40 45 37 2.09 24.8 50

37 32 49 29 38 35 1.97 25.8 22

40 33 57 34 42 35 2.14 23.8 16

.79 .24 3.49* 1.10 .58 2.20 .56 1.50 9.29a*

.08 .06 .26* ⫺.06 ⫺.08 .14 .05 ⫺.15

Note. Patients were ranked into four groups based on length of loss of consciousness. NBAP ⫽ Neuropsychology Behavior Affect Profile. FAD-GF ⫽ Family Assessment Device-General Functioning subscale. PSS ⫽ Perceived Stress Scale. aChi-square (df ⫽ 3). *p ⬍ .05.

Inappropriateness and employment status (see Table 7). Much of the statistical difference on employment status is due to a 50% employment rate for the second injury severity group rather than to a linear trend of lower employment in more severe injuries. The correlations between amount of time elapsed since the patient’s injury, as measured in days, and Full Scale NBAP (r ⫽ .05) or FAD-GF scores (r ⫽ .01) were nonsignificant at the .05 level, but a statistically significant negative correlation was observed between time postinjury and perceived individual caregiver stress (r ⫽ ⫺.17, p ⬍ .05). Amount of time elapsed since the patient’s injury also showed a positively skewed distribution. Again, the patients were ranked into quartiles. The five NBAP subscales, the FAD-GF scores, and employment status were not significantly correlated with time postinjury rank. However, a statistically significant negative correlation between time postinjury rank and perceived individual caregiver stress was again observed in the ranked groups (r ⫽ ⫺.22, p ⬍ .01). Employment. The ability of an individual who has sustained a TBI to return to work is emblematic of one’s progress toward independent living and community reintegration. As TABLE 8 Mean Percentage of NBAP Items Endorsed for Employed and Unemployed Patients

Full Scale NBAP Indifference Inappropriateness Pragnosia Depression Mania FAD-GF PSS

Employed (n ⫽ 43)

Unemployed (n ⫽ 106)

t

34 25 44 31 33 35 2.02 23.65

41 36 50 37 49 32 2.08 26.58

⫺1.98* ⫺2.35* ⫺1.01 ⫺1.30 ⫺3.03** .92 ⫺.50 ⫺1.80

Note. NBAP ⫽ Neuropsychology Behavior Affect Profile. FAD-GF ⫽ Family Assessment Device-General Functioning subscale. PSS ⫽ Perceived Stress Scale. *p ⬍ .05. **p ⬍ .01.

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mentioned before, 29% of the patients in this sample were employed. Surprisingly, employment status was not linearly related to severity of injury rank, ␹2 (4, N ⫽ 139) ⫽ 9.29, p ⬍ .05, despite significant fluctuation in employment within and between ranked categories. However, mean Full Scale NBAP scores were significantly higher in the unemployed group (M ⫽ 41, SD ⫽ 19) than in the employed group (M ⫽ 34, SD ⫽ 20), t(147) ⫽ ⫺1.98, p ⬍ .05 (see Table 8). Subscale analysis revealed that mean scores on Indifference and Depression were significantly lower in the employed group than in the unemployed group. Employment status was not significantly related to FAD-GF or PSS scores. Education. Number of years of education for the patient was significantly negatively correlated with Indifference (r ⫽ ⫺.26, p ⬍ .01), Inappropriateness (r ⫽ ⫺.22, p ⬍ .01), and Pragnosia (r ⫽ ⫺.16, p ⬍ .05). Patient education level was also negatively related to PSS scores (r ⫽ ⫺.20, p ⬍ .05) and to FAD-GF scores (r ⫽ ⫺.17, p ⬍ .05). Caregiver education achieved significant negative correlations with Indifference (r ⫽ ⫺.26, p ⬍ .01), FAD-GF scores (r ⫽ ⫺.22, p ⬍ .01), and PSS scores (r ⫽ ⫺.20, p ⬍ .01). The influence of several other variables was examined (e.g., family size, patient and caregiver age, patient and caregiver gender). All of these differences were relatively small and, although some achieved statistical significance, their size argued against any clinically meaningful relationship.

DISCUSSION Family Functioning The results of this study lend credence to the obvious hypothesis that families of TBI patients function less well than other families who have been spared this trauma. This finding is consistent with Kreutzer et al. (1994b). In that sample and in the current sample, families of TBI patients functioned more poorly than nonclinical controls. Given research and anecdotal evidence regarding the plight of families following TBI, the current findings corroborate the upheaval that is common and replicate the finding that it is feasible to measure the level of functioning in such families. The hypothesis that neurobehavioral impairment in the patient is related to family dysfunction was also strongly supported by the current study. Indeed when the five NBAP subscales are combined (Full Scale NBAP), the resultant correlation with FADGF scores is .54 (p ⬍ .01). Although several authors have alluded to this relationship, none have quantified the connection in such a specific way. The NBAP may then be an effective tool for quantification of the types of neurobehavioral symptoms families find most distressing. Specific types of neurobehavioral impairments were more closely related to family dysfunction than others. Inappropriateness, Depression, Indifference, and Pragnosia scores were much more strongly related to impaired family functioning than was Mania. More specifically, Inappropriateness and Depression appear to be more predictive of poor family functioning than do the other subscales. Severity of injury had surprisingly little effect on the relationship between family functioning and NBAP scores. Only one of the five NBAP subscales, Inappropriateness, was positively correlated with injury severity. This suggests that patients with more severe injuries have more disordered social behavior than their mildly injured counterparts. The absence of statistically significant relationships between the remaining four NBAP subscales and injury severity, as well as between family functioning and injury severity, serves to challenge the assumption that more severe injuries necessarily have the greatest adverse

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impact on the patient and his or her family. Kreutzer et al. (1994b) similarly observed no relationship between family functioning as measured by the FAD and injury severity. Neither neurobehavioral symptoms nor family functioning demonstrated clear, identifiable trends in relation to time postinjury. Unlike the recent finding of Kreutzer, Gervasio, and Camplair (1994a) that time postinjury predicted healthy family functioning, no significant relationship between these two variables was evident in the current study. One distinction between the two studies is the range of time postinjury that was between 1 and 5 years in their study and between 1 month and 40 years in the current sample. Caregiver Stress Individual caregivers reported significantly higher levels of perceived stress than published norms for controls; they experienced levels of perceived stress comparable to individuals attempting to end smoking habits. The level of perceived stress in the current sample is almost identical to another study that assessed TBI caregiver stress at 2 years postinjury (Hall et al., 1994). Professionals in contact with caregivers should attempt to be alert to chronic stress as a long-term issue and anticipate treating family members who exhibit anxiety-related problems. Caregiver stress level was significantly related to neurobehavioral functioning, albeit to a lesser degree than was family functioning. In particular, Indifference, Depression, and Inappropriateness were positively correlated with caregiver stress level. Indifference alone does the best job of predicting caregiver stress. Surprisingly, caregivers of patients with more severe injuries were not significantly more likely to experience high levels of individual perceived stress, and there is some indication that this stress may marginally subside over several years. Employment Neurobehavioral symptoms as measured by the NBAP were significantly higher in unemployed patients. Therefore, neurobehavioral symptoms, particularly unawareness of deficits and depressive mood, may play a role in preventing individuals from securing or sustaining employment following TBI. Conversely, it could be the case that unemployment itself increases neurobehavioral symptomatology. In any event, employment status prediction based solely on injury severity was poor. In general, fewer neurobehavioral symptoms, better family functioning, and patient employment were more likely in cases of higher patient and caregiver educational attainment. Performance of the NBAP The NBAP appears to be the only existing behaviorally based test that is specifically designed for individuals with brain dysfunction for which good normative data now exist. This study represents the first large-scale attempt to establish reliability and validity for the NBAP in a TBI population. Overall, the test performed well. Each subscale proved to have adequate internal consistency reliability, even those with few items. In addition, the intercorrelations among the subscales were not so large as to suggest that each subtest is redundantly measuring the same construct. Conversely, intercorrelations among the subscales were of ample size to suggest that each subscale is measuring different aspects of the same construct. The relationships of the NBAP to variables important in brain injury rehabilitation such as employment, family functioning, and caregiver stress provide concurrent and cri-

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terion-related validity for the measure. The observable, behavioral nature of NBAP questions serves to improve reliability and content validity and to bolster the functional importance of the domains. The mean percentage of items endorsed for the Full Scale NBAP in this sample was 39%. Hence, roughly two fifths of the items for a prototypical TBI patient were endorsed to denote neurobehavioral pathology. Conversely, only about one fifth of the items were endorsed in the control group. The relatively higher percentage of items endorsed for Inappropriateness and Depression suggests that inappropriate behavior and depressed mood are two of the most common neurobehavioral TBI sequelae. These results are somewhat dissimilar to Nelson et al.’s (1994) normative sample. Evidence for additional discriminant validity is apparent by examining the t tests in Table 3, which show that NBAP scores, in each scale except Mania, were significantly higher in TBI patients than in student controls. The poor performance of the Mania subscale is a replication of the finding by Nelson et al. (1994) of no difference between TBI patients and samples of both student and sibling controls. This lack of difference between groups is produced not only by a small percentage of items endorsed on the Mania subscale in the TBI sample but also by the fact that student controls scored substantially higher on this subtest than they did on the other four. Factor analysis at the item level provides solid support for the use of the five factors as constructed by the test’s authors. Factor analysis at the scale level suggests that Pragnosia, Indifference, and Inappropriateness each load on a large general neurobehavioral symptomatology factor, whereas the two mood subscales (Depression and Mania) compose their own unique factors. As the test continues to undergo revisions, the results of this study provide information to further the iterative process of test development. Certain problems with the test should be addressed by its authors. Examples of weaknesses include (a) the theoretical basis for the test’s five domains, (b) the decision to exclude other important neurobehavioral symptoms, and (c) the poor performance of the Mania subscale. Nelson et al. (1989) outlined the theoretical basis for the NBAP as a test whose items were rationally derived from a set of behaviors commonly associated with brain dysfunction. Out of a long list of possible domains of behavior, the five domains that were selected were not done so based on either research or treatment utility. Rather, the justification for choosing behavior domains rested on associations with localized areas of cerebral impairment. However, the authors proceed to link four of the five domains to right hemisphere impairment (except Depression) only to admit later that strict structure-function relationships between behavior and localized brain injury cannot be drawn. This is different from the technique of more well-established tests such as the FAD, whose authors selected items based on the ability of each to impact the emotional and physical health of family members. Obviously the NBAP in its present form should be used for purposes other than lesion localization, but a beginning point for researchers could include investigating the subscales’ ability to differentiate between right and left hemisphere injuries. Unfortunately, patients with lateralized injuries did not score as the authors predicted based on their theory of test development in a validation study in stroke patients by Nelson, Cicchetti, et al. (1993). Although according to their model four of the five subscales are associated with right hemisphere injury, stroke patients with left hemisphere injuries scored significantly higher on each subtest as compared to their counterparts with right hemisphere injuries, with the exception of Mania—purported to be a right hemisphere subscale. Making matters worse, only the Depression subscale (a subscale purportedly indicative of left hemisphere damage) was significantly elevated in the right hemisphere group compared to age-matched controls.

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Rather than identifying domains of inquiry based on a loose connection to localized brain pathology, test authors may wish to consider the ability of the NBAP to predict functional tasks and situations such as family functioning or patient employment. As demonstrated by the current study, the test holds promise in these areas independent of theoretical structure. Exciting opportunities for concurrent and predictive validation studies for the NBAP include compliance to treatment, peer relationships, indices of independent living, and the like. Areas such as these are crucial to long-term outcome from TBI and would enable scores on the test to possess greater utility with regard to making treatment decisions. Because NBAP domains represent clusters of like behaviors associated with localized brain dysfunction, other important behavioral domains may have been excluded where no connection to localized brain dysfunction could be identified. Although a number of other domains should be considered, anxiety and aggression are two disturbing neurobehavioral sequelae commonly mentioned in the literature that are not addressed by the NBAP. For example, a study by DiCesare, Parente, and Parente (1990) found that closed-head injury symptom profiles were dominated by depression, hostility, and anxiety. Likewise, Kendall and Terry (1996) also reported a high incidence of anger and anxiety experienced by 69% and 60% of patients, respectively. Similarly, a test that measured aggression would be a helpful contribution. Long-term recovery from TBI is frequently inhibited by problems of aggression and other impulsive behaviors. It is widely recognized that aggression is one of the most burdensome and disturbing changes for family members (Kreutzer et al., 1992). Although manic behavior is a documented phenomenon in patients with TBI, the ability of the NBAP Mania subscale to differentiate persons with brain dysfunction from those without brain dysfunction is poor. The Mania subscale failed to differentiate patients with dementia, stroke, and TBI in Nelson et al.’s previous attempts, and the subscale failed to do so here in a substantially larger TBI sample. Even more disturbing is the finding in the current study, and in Nelson et al. (1994), that family members reporting on controls endorse approximately 20% of the Mania items in the keyed direction themselves as compared to an average of 14% on the other four subscales. The Mania subscale has the lowest mean inter-item correlation of the five subtests. In addition to each of these drawbacks, the Mania subscale has 24 items, making it twice as lengthy as any of the other subscales. Conclusions The primary focus of the study was unique—examination of the relationship between neurobehavioral symptoms and family functioning in TBI patients. Although some associations have been made, little extant research has attempted to explain the symbiotic relationship between family functioning and neurobehavioral outcome following TBI. Use of the NBAP separates this study from those that have employed nonstandardized symptom checklists. Nevertheless, the cross-sectional design of the study prevents definitive statements about whether neurobehavioral symptoms in the patient cause poor family dysfunction or whether family dysfunction prompts the expression of specific patterns of neurobehavioral symptoms. The study was designed to yield information for rehabilitation professionals whose task is to promote recovery of function following TBI. At one level, clinicians should be aware of connections between elevations on Inappropriateness, Depression, Indifference, and Pragnosia subscales and disturbed family functioning, stress in individual caregivers, and patient unemployment. At a broader level, the relevance of scores on these

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subscales to outcome variables is of similar, if not greater, importance than certain neurological variables such as injury severity. Knowledge of emotional changes exhibited in the patient increases the likelihood that one can positively impact the pattern of emotional change (House, Dennis, Molyneux, Warlow, & Hawton, 1989). When the type and severity of emotional changes in TBI patients are addressed, recovery outcomes have been shown to improve (Novack, Haban, Graham, & Satterfield, 1987). Monitoring neurobehavioral symptoms with instruments such as the NBAP could theoretically help prevent family disintegration. Targeting specific neurobehavioral symptoms for treatment could prevent catastrophic reactions and mitigate their adverse impact on the family. Additionally, clinicians can adamantly insist that patients and family members receive appropriate psychological interventions. Lezak (1983) observed that families can more effectively cope with a relative’s brain injury with greater knowledge of emotional change. Professionals can utilize empirical assessment of family functioning, caregiver stress, and neurobehavioral symptoms to promote positive functional outcomes by individualizing treatment of TBI and adjustment to injury symptoms. Continued research investigations of the role of neurobehavioral symptoms in patient and family outcome following TBI will certainly foster more enlightened treatment approaches, and, in so doing, the arduous challenge of recovery from TBI will be advanced. Clinically, the results suggest that rehabilitation professionals may be able to anticipate family dysfunction and proactively improve service to patients and families by measuring, monitoring, and actively treating neurobehavioral symptoms.

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