NeuroRehabilitation An InterdiscipiinalY Journal

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NeuroRehabilitation 5 (1995) 293-297

Epidemiology of agitation following brain injury'i' Jennifer Bogner*, John D. Corrigan Department of Physical Medicine and Rehabilitation, The Ohio State University, Columbus, OH, USA

Accepted 20 July 1995

Abstract Agitation, while considered an important factor influencing outcome following traumatic brain injury (TBI), has been a poorly defined construct. As a result, the literature on agitation has been confusing and incomplete in regard to incidence rates, causes and correlates, intervention methods, and long-term outcomes. In this article, we review previous research on incidence rates, concluding that differences in definition have greatly limited current knowledge. We then review how agitation has been operationalized in previous clinical and research efforts, and we recommend a definition that we believe will allow future studies to proceed in a more systematic manner.

Keywords: Brain injury; Agitation; Incidence; Aggression; Lability; Disinhibition ---------- ------

1. Introduction

The published literature on agitation following traumatic brain injury (TBI) presents an incomplete picture regarding incidence, cause(s), correlates, interventions and long-term effects. The paucity of controlled studies of agitation belies the potential importance of the phenomenon. Ag-

.~ Preparation of this manuscript was supported in part by Grant H 235L20001 from the US Department of Education, Rehabilitation Services Administration, to the Ohio Valley Center for Head Injury Prevention and Rehabilitation. * Corresponding author, Dodd Hall, 480 West 9th Avenue, Columbus, OH 43210,

itation during the early stages of recovery from TBI has been associated with such long-term outcomes as poorer recovery and delayed work reentry [1]; persistent anxiety, depression, and thinking disturbance [2]; and difficulties with psychological adjustment and institutionalization for behavioral disturbance [3]. Despite the possible prognostic value of studying agitation, the published literature has been dominated by case reports of pharmacologic intervention. Given that agitation can have such a deleterious effect on a patient's ability to participate in rehabilitation, it is not surprising that attention has focused on methods for controlling and decreasing agitation. However, in most of these studies, agitation has

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been poorly defined and rarely measured shortcomings which have hindered progress in identifying effective methods [4]. In this article, we will first review the few studies that have investigated the incidence of agitation. We conclude that a mandatory step to improving our knowledge base is to agree on a definition of the construct. In the second part of this article, we review how agitation has been operationalized in previous clinical and research efforts, and we recommend a definition that will allow future studies to proceed in a more systematic manner. 2. Incidence of agitation Denny-Brown studied 200 hospital admissions (excluding 'chronic alcohol addicts and vagrants' and those not between the ages of 15 and 55 years) and found that 15% exhibited excited, emotional, or restless behaviors [1]. This sample included the broadest range of severity of TBI, and likely included more mild TBIs than subsequent studies. Additionally, because it took place in the 1940's, emergency medical services would not have kept alive as many people with severe TBIs. To the extent that agitation is more frequent in more severe injuries, both of the above selection factors would reduce the observed incidence rate in this study when compared to subsequent research. There have been several studies suggesting that persons sustaining more severe cerebral injuries have a greater potential for exhibiting agitation [2,5], and that those with frontal and subcortical lesions may be more susceptible [6]. Over 30 years later, Levin and Grossman [2] studied 65 patients admitted to the neurosurgery service of an acute hospital and found that 34% exhibited sufficient agitation that a notation was warranted in the medical record. They excluded individuals over the age of 59 and those who had histories of alcoholism, previous cerebral disease or injury, or psychiatric illness. Levin and Grossman [2] noted that agitated patients, who manifested more severe injuries, were more likely to be aphasic, and were younger than non-agitated patients. While the sample criteria for this study and Denny-Brown's were similar, the differences

in cohorts described above likely accounts for the higher rate of occurrence. Three additional studies have been conducted on samples from the more severe range of injuries. Reyes et al. [3] found that 37% of admissions to an acute rehabilitation unit exhibited 'restlessness', while 14% were 'agitated'. They excluded patients with histories of other medical conditions that affect the central nervous system, psychiatric problems, anoxia, or substance abuse. Brooke et al. [7] studied patients admitted to a trauma center who experienced a loss of consciousness of greater than 1 h, stayed in the hospital for at least 1 week, and who did not have substance abuse or psychiatric problems severe enough for hospitalization. Their incidence rates were very similar to the Reyes et al. study, with 35% found to be restless and 11 % agitated. Combining restlessness and agitation, the above studies would have yielded incidence rates of 51% and 46%, respectively. At Ohio State University, we have recently compiled data from a prospective sample of 100 consecutive admissions to our rehabilitation unit. Subjects had sustained a TBI severe enough to warrant admission to the unit and were at least 13 years of age. No other exclusion criteria were employed. Preliminary analyses indicate that approximately 42% exhibited agitated behavior during at least one shift, as indicated by an ABS score greater than 21. The criterion used for determining agitation was one of several currently being studied using the Agitated Behavior Scale. In all, with the exception of the Denny-Brown study, incidence rates have ranged from approximately one-third to one-half for the samples studied. Differences in methods of measurement as well as sampling differences account for the range in incidence rates. Studies investigating the incidence of agitation have been minimal. More important, until a consensus is reached regarding the definition and measurement of agitation, no amount of studies would allow significant insight into the incidence of this behavior. 3. Definition of the construct One of the first references to behaviors associated with agitation was provided by Denny-Brown

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[1], who noted that those who have experienced brain injury may be excited, emotional, or restless. Levin and Grossman [2] defined agitated behavior as 'combativeness, arm thrashing, truncal rocking, screaming, and signs of sympathetic activation' (p. 725). Malkmus, Booth, and Kodimer [8], in their description of eight stages of cognitive recovery, ascribed various behaviors to agitation, including attempts to remove tubes and restraints, resistance to treatment, aggressiveness, and confabulation. In all of these descriptions, observational methods were used to determine the presence or absence of the behaviors; no measurement instruments were utilized. Two studies distinguished between agitation and restlessness. In the study by Reyes et al. [3], both terms referred to constant movement, however, 'restlessness' was used to describe behavior which could be b,riefly inhibited. A five-point scale was used to categorize patients as 'in coma', 'sluggish,' 'appropriately active,' 'restless,' or 'agitated.' Brooke, Questad, Patterson and Bashak [7] also made a distinction between agitation and restlessness, but the terms were defined somewhat differently. Restlessness was used to describe behavior which interferes with care, therapy or safety, but was not as severe as agitation, or was continuous. Agitation was used to describe episodic motor or verbal behavior severe enough to be rated on the Overt Aggression Scale [9], require physicalor chemical restraints, or disrupt patient care. As with the previous studies, there was no attempt to define the degree or severity of the behaviors, just their presence/absence. The Agitated Behavior Scale (ABS) [10] was developed to provide an objective basis for measuring the degree and severity of agitation. The ABS was derived using empirical rather than rational scale development criteria; thus, there was not an a priori definition of agitation. Based on experience in the development and validation of the ABS, as well as findings from studies of TBI and other conditions in which agitation is evident, we have arrived at the following definition: 'Agitation is an excess of one or more behaviors that occurs during an altered state of consciousness.' This definition emphasizes that behavioral excess, rather than manifestation of a specific behavior, is the key concept underlying agitation.

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For purposes of measurement, 'excessiveness' in the ABS has been operationalized by combining criteria proposed by Reyes et al. [3] and Brooke et al. [7], i.e. the inability to inhibit and the degree to which the expression of the behavior is dysfunctional. These two dimensions of excessiveness are incorporated in the criteria used to rate each of the 14 items of the ABS (see Fig. 1): 1 2

3

4

the behavior is not present. the behavior is present to a 'slight' degree, but does not prevent the conduct of other, contextually appropriate behavior. Patients may spontaneously redirect themselves or continuation of the agitated behavior does not disrupt appropriate behavior. the behavior is present to a 'moderate' degree, requiring redirection to a more appropriate behavior, but the patient is able to benefit from such cueing. the behavior is present to an 'extreme' degree when the individual is not able to engage in appropriate behavior due to interference of the agitated behavior, even with redirection or cueing.

Agitation is a single construct characterized by any variety of behaviors. Aggressiveness is one behavior that can occur in excess during an altered state of consciousness, but is not synonymous with agitation. Likewise, restlessness is a degree of agitation, not an independent construct. Component behaviors may vary by diagnostic or other group differences, and may have important implications for intervention. However, any behavior can be excessive. A recent confirmatory factor analysis of the ABS [11] suggested that agitation resulting from TBI may be characterized by specific component behaviors. Four models were tested, with one, two, three, and four factors, respectively. Modell was based on the premise that no latent variables exist and therefore only one factor was proposed. Model 2 was composed of factors labeled 'directed agitation', which involved behaviors directed at self or others and 'undirected agitation', which represented restlessness. This model was derived from an initial validation study of the scale, which yielded similar factors [10]. Model3's

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AGITA TED BEHAVIOR SCALE Patient ___________________ Observ. Environ __________ RaterlDisc. _______________

Period of Observation: a.m. From:_ _ p.m,--'_ _' _ _ a.m. To: _ _ _ p.m._ _' _ _' _ _

At the end of the observation period indicate whether the behavior described in each item was present and, if so, to what degree: slight, moderate or extreme. Use the following numerical values and criteria for your ratings. 1 =absent: the behavior is not present. 2 =present to a slight degree: the behavior is present but does not prevent the conduct of other, contextually appropriate behavior. (The individual may redirect spontaneously, or the continuation of the agitated behavior does not disrupt appropriate behavior. ) 3 = present to a moderate degree: the individual needs to be redirected from an agitated to an appropriate behavior, but benefits from such cueing. 4 =present to an extreme degree: the individual is not able to engage in appropriate behavior due to the interference of the agitated behavior, even when external cueing or redirection is provided.

DO NOT LEAVE BLANKS. 1. Short attention span, easy distractibility, inability to concentrate.

2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.

Impulsive, impatient, low tolerance for pain or frustration. Uncooperative, resistant to care, demanding. Violent and or threatening violence toward people or property. Explosive and/or unpredictable anger. Rocking, rubbing, moaning or other self-stimulating behavior. Pulling at tubes, restraints, etc. Wandering from treatment areas. Restlessness, pacing, excessive movement. Repetitive behaviors, motor and/ or verbal. Rapid, loud or excessive talking. Sudden changes of mood. Easily initiated or excessive crying and/or laughter. Self-abusiveness, physical and/or verbal.

Total Score Fig. 1. The Agitated Behavior Scale.

factors were labeled 'disinhibition', 'aggression', and 'lability'. The first two were based on the original factor analysis and the third was based on clinical observations that some patients present with a unique cluster of behaviors consistent with lability and anxiety. Model 4 included factors from model 3 and a fourth factor representing self-stimulation and repetitive behaviors. Model 3 was found to be the best fitting and most parsi-

monious, with the p-value indicating an acceptable fit. The factors were highly interrelated, suggesting that agitation, as measured by the ABS, is best viewed as a single construct with three facets: disinhibition, aggression and lability. A final assumption of our proposed definition is that the behavioral excess comprising agitation occurs during an altered state of consciousness. In the case of TBI, the altered state of conscious-

J. Bogner, J.D. Corrigan / NeuroRehabilitation 5 (1995) 293-297

ness is the diminished arousal that occurs from the time of injury until resolution of post-traumatic amnesia. Corrigan and Mysiw [12] found systematic relationships between the degree of confusion and disorientation present during post-traumatic amnesia and the extent of agitation. When extreme agitation and confusion coexisted (as in Rancho Level IV), confusion tended to decline before agitation improved. Conversely, before post-traumatic amnesia completely resolved, the last vestiges of agitation dissipated. While the sample size was small and therefore generalization must be limited, the suggestion that an altered state of consciousness was a necessary condition for agitation was clear. Just as an altered state of consciousness can be found in a variety of clinical populations, agitation is not limited to TBI. Agitation has been described in psychiatric populations, particularly certain manifestations of severe depression, as well as some psychoses. It can be a prominent symptom in mental retardation, Alzheimer's disease, and substance intoxication. Cohen-Mansfield, Marx, and Rosenthal [13] utilized the Cohen-Mansfield agitation inventory with geriatric nursing home residents and found a factor structure very similar to that yielded by the ABS. They labeled three underlying dimensions as 'aggressive behavior', 'physically non-aggressive behavior' and 'verbally agitated behavior'. Items comprising these three factors were similar to those for the ABS, with 'physically non-aggressive behavior' being most similar to 'disinhibition' and 'verbally aggressive behavior' being most similar to 'lability.' Given that so little is known about the etiology of agitation in TBI and other diagnoses, and given similarities in its manifestation across populations, the definition of agitation should be inclusive, rather than exclusive, to maximize heuristic opportunities. On this basis, the definition of agitation we are proposing (an excess of one or more behaviors that occurs during an altered state of consciousness) is sufficiently broad to include the various' manifestations of the construct in differ-

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ent populations, while capturing the key concepts common across populations. It is evident from the few studies of the prognostic value of early agitation [1-3] that much could be gained from better research, including interventions that address both short and long-term issues.

References [1] [2] [3]

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Denny-Brown D. Disability arising from closed head injury. JAmMed Assoc 1945;127:429-436. Levin HS, Grossman RG. Behavioral sequelae of closed head injury. Arch NeuroI1978;35:720-727. Reyes RL, Bhattacharyya AK, Heller D. Traumatic head injury: Restlessness and agitation as prognosticators of physical and psychological improvement in patients. Arch Phys Med Rehabil 19tH; 62:20-23. Fugate LP. Agitation following traumatic brain injury: Definition, Measurement and Treatment. Masters Thesis, The Ohio State University, 1994. Fichera S, Zielinski R, Mittenberg W. Neuropsychological correlates of post-traumatic agitation. J Clin Exp Neuropsychol 1993;15:105. Zielinski R, Theroux-Fichera S, Tremont G et al. Normative data for the Agitated Behavior Scale. Poster presented at the 102nd Annual APA Convention, Los Angeles, CA, 1994. Brooke M, Questad K, Patterson, D et al. Agitation and restlessness after closed head injury: A prospective study of 100 consecutive admissions. Arch Phys Med Rehabil 1992;73:320-323. Malkmus D, Booth BJ, Kodimer C. Rehabilitation of the head-injured adult: Comprehensive cognitive management, Downey, CA, Professional Staff Association of Ranchos Los Amigos Hospital, Inc., 1980. Yudofsky SC, Silver JM, Jackson W et al. The Overt Aggression Scale for the objective rating of verbal and physical aggression. Am J Psychiatry 1986;143:35-9. Corrigan JD. Development of a scale for assessment of agitation following traumatic brain injury. J Clin Exp Neuropsychol 1989;11:261-277. Corrigan JD, Bogner JA. Factor structure of the Agitated Behavior Scale. J Clin Exp Neuropsychol 1994; 16:386-392. Corrigan JD, Mysiw WJ. Agitation following traumatic head injury: Equivocal evidence for a discrete stage of cognitive recovery. Arch Phys Med Rehabil 1988;69:487-492. Cohen-Mansfield J, Marx MS, Rosenthal AS. A description of agitation in a nursing home. J Gerontol: Med Sci 1989;44(3):M77-M84.

Epidemiology of agitation following brain injury.

Agitation, while considered an important factor influencing outcome following traumatic brain injury (TBI), has been a poorly defined construct. As a ...
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