Author: megan_hdipub

Jeff Kupfer, Peter R. Killeen, & Randall D. Buzan

“Why is he behaving this way?” is the central question caregivers and family members of patients with Traumatic Brain Injury (TBI) pose, pointing to extreme agitation, antisocial behavior, insensitive interactions, or other manifestations of his condition. Our clinical team gives various answers from the varied perspectives and expertise of members. Accurate though these explanations are, they often don’t hang together, and often don’t satisfy the questioner. What is wrong with our explanations? Was something lost in translation of scientific jargon? Perhaps some features that could provide a complete explanation were omitted. This paper presents a framework for explanations that permits a more integrated and complete picture, and reminds practitioners of aspects that should be included in a thorough understanding of behavior after TBI.

PART ONE:  Explaining a behavioral event: “How did that lamp break?”

Consider the following family situation: a Sunday afternoon family brunch, post-meal conversation around the dining table. Suddenly we hear the laughter of children, footsteps running down the stairs and through the living room. The front door slams, followed by the sound of a lamp crashing to the floor in the foyer. Table 1 organizes the diversity of explanations by the family members for this household accident.

Table 1. Dialogue amongst family members following a behavior event.

Event is Described	Focus	“Cause”
Focus on the behavior
“I’ve told them not to run in the house”	Running describes the form of behavior	Formal
“Joey led the charge out the front door”	Trigger was Joey	Efficient
“They were bored in here with all the adult talk”	State of the system: Arousal ready for displacement	Material
“And they were eager to play with that new hoop set you got for Joey’s birthday.”	Purpose, function,	Final
“Well let’s not forget the sugar high from that excellent dessert”	State of the system: Arousal ready for displacement	Material
Focus on environment
“It’s smithereens now—no way even grandpa could fix it”	Describes current status	Formal
“It’s not completely their fault, Helen. That old lamp was pretty tippy: A strong wind would knock it over”	Many possible ways for it to break	Efficient
“It was Joey who bumped it over”	The particular trigger that tripped it	Efficient
“Helen! It was missing its fourth leg!!”	Lack of structural integrity	Material
“Joseph, I think you loosened it just to make this happen, given how you hated that old lamp!”	The reason the leg was loosened and broken off	Final

We see that an unexceptional event may be examined from various points of view, all which may be correct. Similarly, brain and behavior sciences provide scientific explanations of events from various points of view, but even they typically fall into several classes. These are the classes of explanation identified by Aristotle that are required before we may claim to truly understand a phenomenon (Hocutt, 1974).

Aristotle’s framework for explanations

Aristotle’s name for these classes of explanation was mistranslated as “Causes”, a proper title in modern parlance for only one type (efficient cause). This led to his schema being dismissed as confusing and even teleological. A better class name is reasons for, or becauses (Killeen, 2001). Aristotle’s framework addresses the broad range of possible explanations for any phenomenon, and coordinates these explanations to arrive at a more integrated understanding. We can utilize this model to describe behavior following a brain injury.

Formal causes (names, forms, and models) are the ways we talk about, represent and describe events. They translate the essentials of their relevant aspects into words, numbers or diagrams. Simple descriptions, such as the example above (“running resulted in the lamp breaking”) can get the formal ball rolling, but these can be extended to include models, metaphors, logical phrases, equations, schematics, blueprints, or flowcharts that help us organize, summarize, and communicate phenomena. Behavioral experts use DSM diagnoses as “formal causes” to describe and explain patient behavior, and brain injury professionals use the Glasgow Coma Scale or Ranchos Los Amigos Scale as formal descriptors of a patient’s condition. Physicists and astronomers utilize differential equations as their formal models. Behavior analysts describe behavior with three-and four-term contingencies for simple and conditional discriminations (antecedent, behavior, consequence, A-B-C).

Efficient causes (triggers) refer to the necessary and sufficient conditions to bring about a change in state (factors triggering an event). These are commonly what are meant by “causes” (Joey’s running in the house caused the lamp to fall [when he careened into it]). Efficient causes of reckless behavior identify events or people that trigger action, as well as events that can minimize or prevent its occurrences. Efficient causes are conditions sufficient to trigger the phenomenon being explained that were operative at the critical moment. There may be many possible sufficient conditions, just as there are many possible roads to Rome; functional analyses clarify which ones were operative in a particular case. Necessary causes are usually invoked to explain failures of expected outcomes: Why didn’t the car start? It needed gas (electricity, functional starter, etc.), which are necessary to get the show on the road. Explanations that rely only on efficient causes may become overly mechanistic, thereby distracting investigation from the substrates, underlying mechanisms, and functional aspects.

Material causes (machinery) refer to the substrates, the underlying mechanisms. These causes are of most interest to medical and health professionals who are trained to understand, diagnose, and treat problems with underlying machinery. For instance, high blood glucose may be due to diabetes (formal cause) that may result from insufficient production of insulin (material cause), complicated by eating Twinkies (efficient cause). Parents often turn to material causes to explain challenging behavior in children, particularly when the efficient causes and triggers are inconspicuous and difficult to pin down accurately. “Lacks motivation” is too often the ad hoc explanation by family members; “Lacks character” by neighbors. Explanations that rely exclusively on material causes can become reductionistic, omitting relevant connections to triggers and consequences.

Final causes (functions) are the purposes of an event, what has brought about or sustained a phenomenon or process. Not all phenomena have final causes, or are directly understandable in terms of them. Cerebral edema, for example, is a rescue mechanism of the brain that in extreme can have serious negative consequences. Thus, some outcomes may represent break-down or failure modes of systems, some of which may serve an important function in normal circumstances. Proximate final causes may refer to the immediate consequences of some behaviors or misbehaviors, such as ones that may sometimes occur with the syndrome of TBI: escape and avoidance of difficult situations. Ultimate final causes may involve a learning history that has resulted in current maladaptive behavior.

PART TWO:  Applying Aristotle’s framework to neurobehavioral treatment and the role of Behavior Analysis

When a person becomes aggressive following a brain injury, we quickly try to comprehend the event. We start with a description such as: “He struck the therapist during his therapy session.” This triggers communication with the family, therapists and staff, the physician and other medical professionals, the case managers, insurance adjusters, and so on. The descriptions of the incident set each on their respective paths to explain behavior in order to derive an effective intervention. Agitation has crossed the formal threshold to aggression: physical or verbal behavior directed at another person with the intention to cause harm. We want to know about the specific necessary and sufficient conditions that triggered the aggression (efficient causes), underlying mechanisms (material causes), the function or purpose it served (final causes), and best ways to talk about it, both for treatment, and for communication with family members (formal causes). We may require details about immediate (proximate) variables, as well as enduring variables from the past (personal history, family history) suggesting ultimate reasons for such aggression. In short, we need to communicate much information in a brief period of time for intervention to commence, and we need to continue dialogue throughout treatment to be sure that the stakeholders share our framework.

A Case Study

Sam is a 50-year old male who received a significant brain injury when he was struck by a motor vehicle at the age of 14. Prior to admission to our facility, Sam spent most of his adult life residing at institutional settings where he exhibited physical and verbal aggression, requiring an increased level of staff supervision, and occasional temporary placement in isolated sections of the referring facility.

Upon admission to our program, a functional assessment of problem behaviors (Questions About Behavior Function – QABF) was conducted. The results suggested that physical and verbal aggression were functionally related to attention delivered by caregivers or therapists: When caregivers’ and therapists’ attention to Sam decreased, the probability that he would engage in physical and verbal aggression resulting in attention from others (e.g., redirection, physical intervention or containment) increased. He had the staff on a schedule of negative reinforcement: their lack of attention generated an increase in the frequency of aggression that resulted in a swift staff reaction to escape or delay his aggressive behavior.

On the basis of the functional assessment, differential reinforcement of alternative behavior (DRA) was introduced to treat aggression. Under this procedure all caregivers and therapists: (1) provided little or no attention upon physical and verbal aggression by Sam; and (2) shifted the schedule of reinforcement to deliver attention contingent upon Sam’s use of more cordial, alternative attention-requesting behaviors. During the course of treatment his antipsychotic medications were tapered and discontinued as aggressive behaviors decreased.

Figure 1 summarizes the medication adjustments for Sam during treatment. Data for verbal and physical aggression were recorded according to a 30-min partial interval count for occurrence/non-occurrence of target behaviors.

Vertical dashed lines indicate medication adjustments during the course of treatment, and labels indicate the name of the medication and the adjusted dose. Down-arrows preceding medication labels indicate reductions and discontinuations; up-arrows preceding medication labels indicate increases or initiations. From the slope of the curve we may infer changes in response rates— decreases in the slope of the curve over time (negative acceleration) indicate decreases in the occurrence of aggression. In general, these data show variable but negatively accelerating trends; physical aggression rates (dashed line) were lower than those for verbal aggression (continuous line).

Reductions in trazodone and risperidone often occasioned brief bursts of verbal aggression, which gradually decreased to low or zero rates until the next medication taper. Concurrent with the discontinuation of risperidone, Sam developed bursitis in his elbow from an infection that required medical attention. This brief delivery of attention was correlated with extreme verbal and physical aggression in response to pain in his elbow. After medical treatment was administered, DRA treatment was reinstated for the remainder of the study. However, it was unclear whether this brief delivery of medical attention inadvertently produced and sustained the higher rates of aggression that lasted for approximately five weeks, until risperidone was reinstated, producing a gradual reduction in the frequencies of target behaviors. When these target behaviors approached zero rates, clozapine was introduced and substituted for risperidone, producing brief but decreasing bursts of target behaviors. Subsequently, risperidone was discontinued without any increase in aggression, as was clozapine.

In this example the search for efficient causes (decrease in level of staff attention) and final causes (attention received) resulted in an intervention to change the triggers and consequences. Aggression gradually decreased as a function of shifting the contingencies of reinforcement. This functional relation was confirmed inadvertently when the brief, but intense complaints of pain by Sam produced an unavoidable medical attention to treat bursitis. Additionally, a material explanation (chemistry potentially more responsive to clozapine than to risperidone) produced an intervention based on a review of the current medications and a gradual taper to determine therapeutic effectiveness, and eventual substitution of medications that was either more effective or had fewer agitating side effects. This case history constitutes one more example of attempts at efficient and material explanations, inquiries that expose a range of variables with the potential to contribute to understanding complex behaviors ranging from ADHD (Killeen, Tannock,  & Sagvolden, 2012), to hypnosis (Killeen & Nash, 2003). 

Further benefits from analyses of efficient causes

Closer examination of subtle environmental triggers and contingencies reveals interesting and unexpected efficient causes for behavior that can inform neurobehavior treatment. Recent research, (Mace, McComas, Mauro, Progar, Taylor, Ervin, & Zangrillo, 2010), for example has suggested that DRA procedures may actually prolong extinction effects (causing “extinction bursts”) due to behavioral momentum, thereby prolonging the persistence of target behaviors. Conducting a DRA procedure in a separate context from which learning the target behavior occurred can, however, decrease resistance of the problematic behavior to extinction. Similarly, there are situations in which the extinction component of the DRA procedure cannot be implemented— combative behavior may be too intense to stop or directed toward others in ways that cannot be ignored. In a series of experiments Athens and Vollmer (2010) demonstrated that behavior treatment plans that involve manipulating reinforcer duration, quality, delay, or a combination of these in ways that favors appropriate behavior rather than problem behavior can still produce more appropriate responses, even though problem behavior received occasional (albeit, lower) reinforcement. In both of these cases, the procedures have some risks consequent on implementation (increases in target behavior), but these can be minimized with refinement of the consequences (final causes) thereby averting the need to use medications (material necessary causes) to address the problem.

Behavior analysis techniques can yield benefits in addition to merely addressing problem behaviors as in the above example. An analysis of triggers and consequences can produce more robust effects when teaching adaptive living skills. Decades of research in applied behavior analysis has generated instructional methods for teaching in homes and classrooms, as well as vocational and rehabilitation settings, such as errorless learning (Chandonnet & Kupfer, 2014; Sidman, 2012), fluency and precision teaching (Binder, 1996), and stimulus equivalence training (Sidman, 1994). Research suggests that efficient and final explanations are primarily useful when there is a problem behavior to reduce or eliminate, but other formal explanations (e.g., TBI patients often lack social competence) help clarify potential deficiencies in appropriate responding that may be the result of environmental contingencies that sustain inappropriate behaviors. Thus, if the individual with brain injury could acquire skills in PT, OT, SPL, and so on more quickly and effectively by changing teaching methods, problem behaviors might be less likely to occur. Teaching methods derived from ABA (efficient and final causes) thereby complement those methods used to increase brain, body, and sensory health (material causes).

A thorough bibliography of evidence-based teaching methods for persons with brain injury is located on the Brain Injury Webpage for the Cambridge Center for Behavioral Studies: www.behavior.org.

Pursuing interrelationship between efficient and material causes

            What are the interactions between efficient causes and material causes? In the example of the broken lamp, one family member focused on reckless behavior in the home, but another alluded to the causes involving the environment—a wobbly lamp, an accident waiting to happen. In neurobehavioral treatment, proximate (temporally immediate, relevant and conspicuous) influences over behavior are revealed during initial assessments and ongoing progress reviews, but access to past environmental events or historical influences (medical records, psycho-social histories, interviews, and verbal reports) are relevant as well. Expanding the causal time frame, an examination of family history may reveal generational patterns that implicate ultimate genetic influence. Neurobehavioral approaches do not simply treat a person with a brain injury; they provide treatment within a context of immediate and historical influences.

Figure 2 represents the broader influences of both ultimate variables (across large timeframes) and proximate variables (most recent or conspicuously present) in the Aristotle’s framework to explain the causes of ADHD (Killeen et al, 2012). In this figure, the inner set are proximate (molecular) causes and the outer set ultimate (molar) causes. Triggers of symptoms (states) are proximate efficient causes; triggers of the phenotype (traits) are ultimate efficient causes. Material causes comprise the hardware underlying the behavior (proximate, neurophysiology) and the syndrome it instances (ultimate, structural, or genetic). Recursive arrows show outcomes can modify the system to change the sensitivity to correlated stimuli and responses through shifts in attention, learning, and reframing of the situation.

Isolating interactions between efficient and material causes of behavior is often difficult; however, the topic is of paramount importance in behavior analysis, particularly in relation to interactions between: genes and environment (Suomi, 2002), consequences, genes and brain development (Schneider, 2012), unique conditioning histories and drug effects (Branch, 2006; Terrace, 1963), and behavioral and biological systems (Thompson, 2007). Accordingly, the language of the behavior analysis community continues shifting to accommodate the expansion of efficient and material explanations (Hineline, 1980; Hineline & Groeling, 2011). Skinner (1989) had pointed us in this direction:

“There are two unavoidable gaps in any behavioral account: one between the stimulating action of the environment and the response of the organism, and one between consequences and the resulting change in behavior. Only brain science can fill those gaps. In doing so it completes the account; it does not give a different account of the same thing. Human behavior will eventually be explained (as it can only be explained) by the cooperative action of ethology [which we place as ultimate mechanism, an evolved organism in its niche], brain science [proximate machinery], and behavior analysis [formal, efficient and final causes].” (p.18)

Conclusion

When caregivers and family members seek explanations about behavior changes observed in patients with brain injuries, there is a distinction between “what” is happening, “why” it is happening and “how” it is happening. Addressing the “what” question requires careful analyses to ensure that behavior is not mischaracterized—that it is not, for instance, within the normal range of human responses. If the behavior is categorizable, it is essential that all plausible categories of explanation have been considered. Inferences to material and final causes should be avoided in first-level formal descriptions. These actions all address formal causes. A reference to “why” may lead to consideration of “what was gained by it”, a question about goals and reinforcers. But it may also refer to instigating factors. Thus “why” questions are cues to discuss both the triggers for behavior (efficient causes) and sustaining reinforcers (final causes) It may also reveal a concern over “structure and under lying mechanisms” that govern the behavior (material causes).

Neurobehavioral treatment should attempt to address all of these perspectives. Addressing all four causes (Formal, Efficient, Material, and Final) at relevant levels—molar and molecular—can lead to more comprehensive and inclusive strategies, and a more convincing understanding of behavior for patients, their families, and clinicians.

References

Athens, E.S., Vollmer, T.R. An investigation of differential reinforcement of alternative behavior without extinction. J Appl Beh Analy 2010;43:569-589.

Binder, C. Behavioral fluency: Evolution of a new paradigm. Beh. Analy 1996;19:163-197.

Branch, M. How research in behavioral pharmacology informs behavioral science. J Exp Analy Beh 2006;85:407-423.

Chandonnet, N., Kupfer, J. Errorless learning in therapy. Poster presented at Brain Injury Summit: A Meeting of the Minds, 2015, January, Vail CO.

Hineline, P.H., Groeling, S.M. Behavior-analytic language and interventions for autism. In E.A. Mayville & J.A. Mulick (Eds.), Behavioral foundations of effective autism treatment. NY: Sloan Publishing, 2011.

Hineline, P.H. The language of behavior analysis: Its community, its function, and its limitations. Behaviorism 1980;8:67-87.

Hocutt, M. Aristotle’s four becauses. Philosophy 1974;49:385-399.

Killeen, P.R. The four causes of behavior. Cur Directions in Psych Sci 2001;10:136-140.

Killeen, P.R., Nash, M. The four causes of hypnosis. Int J of Clinic and Exp Hypnosis 2003;51:195-231.

Killeen, P.R., Tannock, R., Sagvolden, T. The four causes of ADHD: A framework. 2012;In S.C. Stanford & R. Tannock (Eds.), Behavioral neuroscience of attention deficit disorder and its treatment. 2012;9:391-425, Berlin, Germany: Springer-Verlag.

Kupfer, J., Eastridge, D., Buzan, R.D., Castro, J. Using cumulative graphs to evaluate the effects of medication adjustments combined with extinction procedures to decrease aggression. Symposium entitled: Welcome Back, MY LOVELY! Cumulative graphs in the analysis of behavior. Presented at the 38^th annual meeting of the Association for Behavior Analysis, 2012, May, Seattle, WA.

Mace, F.C., McComas, J.J., Mauro, B.C., Progar, P.R., Taylor, B., Ervin, R., Zangrillo, A.N. Differential reinforcement of alternative behavior increases resistance to extinction: Clinical demonstration, animal modeling, and clinical test of one solution. J Exp Analy Beh 2010; 93:349-367.

Schneider, S.M. The science of consequences: How they affect genes, change the brain, and impact our world. NY: Prometheus Books, 2012.

Sidman, M. Equivalence relations and behavior: A research story. Boston: Authors Cooperative, Inc., 1994.

Sidman, M. Errorless learning and programmed instruction: The myth of the learning curve. Euro J of Beh Analy.2010;11:167-180.

Skinner, B.F. The origin of cognitive thought, Am Psych 1989;44:13-18.

Suomi, S.J. How gene-environment interactions can shape the development of socioemotional regulation in Rhesus monkeys. In B.S. Zuckerman, A.F. Zuckerman, & N.A. Fox (Eds.), Emotional regulation and developmental health: Infancy and early childhood. NJ: Johnson and Johnson Pediatric Institute, 2002.

Terrace, H. Errorless discrimination learning in the pigeon: Effects of Chlorpromazine and Imipramine. Science.1963;140:318-319.

Thompson, T. Relations among functional systems in behavior analysis. J Exp Analy Beh.2007;87:423-440.

By Mikhaylo Szczupak, MD, and Michael E. Hoffer, MD

Tinnitus is an auditory perception in the absence of any external sound stimulus. Many factors have been associated with tinnitus, such as brain injury, hearing loss and old age. Although the pathophysiology of this disease entity remains unknown, leading theories suggest that the following portions of the auditory pathway may be involved: injured cochlear hair cells repetitively stimulating auditory nerve fibers, spontaneous activity within individual auditory nerve fibers, hyperactivity of auditory brain stem nuclei, or reduction in suppressive activity of the central auditory cortex on peripheral auditory nerve activity (Atik, 2014). The study of tinnitus continues to be a challenge because of the subjective nature of the condition, its likely multifactorial etiology and the many varied tinnitus assessment scales (Hoffer et.al. 2003). Our goal in this review will be to examine several subtypes of post-traumatic tinnitus, in particular acoustic trauma, traumatic brain injury and barotrauma.

Acoustic Trauma
There is a well-known association between history of exposure to noise trauma, high-frequency hearing loss and the presence of high-pitched “whistling tinnitus” (Nicolas-Puel et al., 2006). Hearing loss severity has been demonstrated to predict degree of tinnitus discomfort in symptomatic individuals (Dias et al., 2008) Although pitch matching is not a perfect technique for measuring tinnitus symptoms, the most commonly observed frequency of tinnitus is often the same as the worst frequency for hearing (Axelsson, et al., 2002). Many believe that impulse noise is more damaging to hearing than continuous sound, pure tones are more harmful than composite sounds and high-pitched sounds are likely more harmful than low-pitched sounds (Axelsson, et al., 2002). Clearly there is an association between noise trauma and tinnitus but the exact pathogenesis remains enigmatic.

Acoustic trauma damages the hair cells of the cochlea by exerting vascular, metabolic and chemical changes on normal physiologic processes (Fausti et al., 2009). These changes have been shown to cause decreased hair cell stereocilia stiffness, auditory nerve cell swelling and ultimately cell death/degeneration of auditory nerve fibers (Fausti et al., 2009). The cochlear damage seen following acoustic trauma can be either temporary or permanent and may occur in the absence of elevated hearing thresholds (Schaette et al., 2011) Interestingly, in individuals with normal audiograms, the occurrence of tinnitus is not correlated with current occupational noise level, duration of noise exposure or even cumulative noise exposure (Rubak et al., 2008). Alterations seen following acoustic trauma may be seen centrally in addition to the peripheral changes in the cochlea mentioned above. Current theories suggest that this etiology of tinnitus is related to auditory deprivation secondary to an acoustic insult causing enhanced synchronization of neuronal activity in the auditory cortex (Ortmann el al., 2011). Ortmann et al. were the first to demonstrate these neuroplastic changes in humans, with 13 of 14 amateur rock musicians exhibiting increased gamma activity in the right auditory cortex with transient tinnitus and temporary hearing loss after noise exposure (Ortmann el al., 2011).

Certain vocations, particularly military service members, are at an increased risk of acoustic trauma and as a result, both tinnitus and hearing loss (Mrena et al., 2002). The acoustic environment of a military setting is unique for several reasons: warfighters are often required to remain in noisy environments to complete a mission without the possibility of rotating out. Aircraft/firearm operations take place in reduced areas compared to civilian operations. and individuals may sacrifice hearing protection to more easily communicate with other team members (Yankaskis, 2013). Service weapons may produce noise levels ranging from 150 to 180 dB of sound pressure level (SPL), exceeding the 140 dB SPL threshold where there is a high probability of sustaining marked damage to the auditory system (Ylikoski et al., 1995). There are few studies within the current literature reporting the prevalence of tinnitus within the entire active-duty/veteran United States (U.S.) military population. Helfer et al. demonstrated a 30.8% point estimate for tinnitus prevalence in active U.S. Army soldiers (Helfer et al., 2004). Higher rates of noise-induced tinnitus have been found for military personnel of other nations (Mrena et al., 2009).

Even more common than military service is exposure to music both professionally and recreationally. Hagberg et al. surveyed 407 Swedish music academy students and found that tinnitus was the most prevalent symptom (10.6 individuals per 1000 years of instrumental practice) (Hagberg et al., 2005). Potier et al. investigated tinnitus in disc jockeys, another population of professional musicians (Potier et al., 2009). Nearly three quarters (75.9%) of the 29 included disc jockeys complained of tinnitus, that on pitch matching corresponded with patterns seen on audiogram (Potier et al., 2009). With evolving portable music technology and ever popular electronic dance music festivals, recreational loud music exposure continues to increase. Approximately 75 to 90% of young adults have experienced transient tinnitus after loud music exposure (Quintanilla-Dieck et al., 2009. Gilles et al., 2012). These individuals reported minimal awareness of the long term impact of chronic loud music exposure with only 15% using ear plugs in a concert/nightclub setting (Quintanilla-Dieck et al., 2009). There exists an obvious potential for education of these young adults as well as professional musicians on the proper use of hearing protection to prevent tinnitus and hearing loss.

Traumatic Brain Injury
Traumatic brain injury (TBI) is a broad term used to describe an entity in which there is either a blunt or blast force applied to the head transmitting force to the brain. The incidence of TBI in both the civilian and military populations continues to be a public health issue. Based on the most recent CDC statistics, 2.4 million annual emergency department visits, hospitalizations or deaths were a result of TBI (Coronado et al., 2012). Approximately 75% of these injuries can be classified as mild traumatic brain injury (mTBI) (National CIP, 2003). To warrant diagnosis of mTBI an individual must meet the following criteria: Glasgow Coma Scale (GCS) greater than or equal to 13, loss of consciousness not in excess of 1 hour and post-traumatic amnesia not exceeding 24 hours. Even with decreasing frequencies of operational military engagements, mTBI incidence is expected to remain constant as a result of military training exercises and participation of active duty members in recreational sports (Terrio, et al., 2009).

Tinnitus has been well studied in individuals suffering mTBI, particularly in the military. Since 2007, tinnitus has been the most common service-connected disability of both new (completion of service within the prior 12 months) and existing military veterans (US DOVA, 2015). Based on its prevalence in proportion to all other service-connected disabilities, the cost of tinnitus is estimated to be greater than $3 billion annually in military veterans alone (US DOVA, 2015). Balance disorders, hearing loss, tinnitus, cognitive difficulties and/or sleep disturbances can be seen in more than 95% of all individuals who sustain mTBI (Hoffer et al., 2010). One or more of these symptoms will persist in greater than 80% of individuals treated with the current standard of care (Hoffer et al., 2010).
Oleksiak et al. demonstrated that 76% of Operation Iraqi Freedom/Operation Enduring Freedom veterans diagnosed with mTBI during active duty reported tinnitus upon subsequent audiological evaluation (Oleksiak et al., 2012). In one of the largest epidemiological studies to date, Yurgil et al. prospectively assessed 1647 active-duty Marine and Navy servicemen for tinnitus and TBI (Yurgil et al., 2015). Deployment-related TBI, blast exposure and multiple TBIs each more than doubled the likelihood of post deployment tinnitus (Yurgil et al., 2015). Interestingly, the prevalence of tinnitus in the civilian population recovering from TBI has been found to be slightly lower than the military population. A pilot study of middle aged individuals recovering from blunt TBI by Jury et al. demonstrated that 53% reported symptoms of tinnitus (Jury et al., 2001). The principal theory as to why brain injury leads to auditory dysfunction is thought to be a result of diffuse axonal injury to the central auditory pathway (Nolle et al., 2004). Clearly, tinnitus following mTBI is a partially understood, prevalent condition that is worthwhile to screen for in both military and civilian populations.

The natural history of history of tinnitus secondary to mTBI follows an unexpected course. In data collected from 148 service members who sustained mTBI secondary to blast, over 90% reported “non-concerning ringing” immediately after the injury (Hoffer and Balaban, 2011). One week later only 70% reported tinnitus, and 10 days later less than 33%. Surprisingly, this value then rises to over 60% several months after the initial injury. There are likely multiple factors involved in this trend such as pre-existing tinnitus, “primed” inner ear from previous noise exposure and incompletely understood pathophysiology (Hoffer and Balaban, 2011).
Exclusive to blast mTBI, tympanic membrane rupture is a commonly observed sequelae. Of the 33 victims from the 2005 Thailand terrorist bombings with complete otologic and audiologic follow-up, 22 (66%) exhibited some degree of tympanic membrane perforation (9 bilaterally, 13 unilaterally) (Tungsinmunkong et al., 2007). The tympanic membrane is the most frequently injured anatomical structure from blast and the least resistant to increased atmospheric pressure (DePalma et al, 2005). As a result, some have suggested that if the tympanic membrane is intact, then any primary effects of the blast wave on other air-containing organs are unlikely (DePalma et al., 2005). The majority (75%) of tympanic membrane perforations heal spontaneously within several months without complication while the remainder require surgical intervention (Kronenberg et al., 1993).
There are several specific causes of pulsatile and nonpulsatile tinnitus that occur following TBI. A vascular origin is assumed for pulsatile tinnitus until proven otherwise, several of which are considered life threatening (Kruezer et al., 2014). The three most common causes of post-traumatic pulsatile tinnitus are carotid dissection, arteriovenous fistulas and carotid cavernous fistulas (Chae et al., 2001. Liang et al., 2007. Redekop, 2008). Post-traumatic nonpulsatile tinnitus can occur due to injury at several points along the auditory pathway, such as the cochlea, the auditory nerve or the brain (Kruezer et al., 2014). The most frequent etiologies of nonpulsatile tinnitus are temporal/petrous bone fractures, labyrinthine concussion, ossicular chain disruption and perilymphatic fistula (Fitzgerald, 1995. Chen et al., 2001. Ulug and Ulubil, 2006. Yetiser et al., 2008). The latter two typically surgical intervention and can also be seen following barotrauma.

Barotrauma
Air travel and underwater diving are two common situations when barotrauma to the ear may occur. These injuries are a result of rapid pressure changes from either ascending or descending with inadequate pressure equalization. Damage ensues from a pressure gradient between the middle ear cavity and the external atmosphere across the tympanic membrane (Mirza and Richardson, 2005). For ascent during both air travel and underwater diving, the ambient atmospheric pressure decreases while the gas in the middle ear cavity expands. Subsequently, the eustachian tube opens and vents off positive air pressure beginning at a pressure differential of 15 mmHg (Mizra and Richardson, 2005). Problems rarely occur with passive venting if the eustachian tubes are patent and functioning properly. In contrast, descent during both air travel and underwater diving is an active process. Air does not typically enter the middle ear cavity passively and some form of muscular activity (swallowing, yawning, chewing, etc.) is required. At a pressure differential of 90 mmHg, the soft nasopharyngeal end of the eustachian tube closes at a force greater than that which can be developed by the muscles that open the tube.41 Attempts to equalize pressure once this has occurred are ineffective. The significant density disparity between water and air explains why barotrauma occurs more frequently from underwater diving compared to air travel (Becker and Parell, 2001).

Damage may occur as a result of mucosal edema or blood within the middle ear cavity causing symptoms of tinnitus and/or hearing loss (Becker and Pareell, 2001). More severe injuries include tympanic membrane rupture and ossicular chain disruption (Mizra and Richardson, 2005). Less frequently, injury to the inner ear structures may occur, commonly presenting with the additional symptom of dizziness. Three hypothesized mechanisms of injury are hemorrhage, labyrinthine membrane tear and perilymph fistula via the oval or round windows (Mizra and Richardson, 2005). Damage to the round window occurs more frequently because the oval window membrane is thicker and protected by the both the stapes footplate and surrounding ligaments (Mizra and Richardson, 2005). Treatment of barotrauma injuries is generally conservative aside from ossicular chain disruption, perilymphatic fistula and refractory tympanic membrane perforation, which all require surgery (Duplessis and Hoffer, 2006).

Conclusion
Tinnitus is a common sequelae following brain injury. Severe traumatic events can cause multiple sub-types of post-traumatic tinnitus. For example, following a major blast injury, a soldier may sustain traumatic brain injury as well as acoustic trauma and barotrauma. Additionally, tinnitus is rarely the only complaint after trauma and individuals may present with multiple symptoms which all require evaluation (Kreuzer et al., 2014). A comprehensive diagnostic assessment (complete history and physical, audiological testing, imaging) is crucial to identify the injury and guide treatment which will be covered in subsequent articles within this edition. Ultimately, education and prevention will take a leading role in averting post-traumatic tinnitus as these protective technologies continue to develop.

REFERENCES
Atik A. Pathophysiology and treatment of tinnitus: an elusive disease. Indian J Otolaryngol Head Neck Surg. 66(Suppl 1): 1-5, 1014.

Axelsson A, Prasher D. Tinnitus induced by occupational and leisure noise. Noise Health. 2(8): 47-54, 2000.

Becker GD, Parell GJ. Barotrauma of the ears and sinuses after scuba diving. Eur Arch Otorhinolaryngol 2001.258(4): 159-63, 2005.

Chae SW, Kang HJ, Lee HM, et al. Tinnitus caused by traumatic posterior auricular artery—internal jugular vein fistula. J Laryngol Otol.115(4): 313-5, 2001.

Chen J, Ji C, Yang C, Liu Z. Temporal bone fracture and its complications. Chin J Traumatol.4(2): 106-9, 2001.

Coronado VG, McGuire LC, Sarmiento K, et al. Trends in Traumatic Brain Injury in the U.S> and the public health response: 1995-2009. J Safety Res. 43(4): 299-307, 2012.

DePalma RG, Burris DG, and Champion HR, et al. N Engl J Med 2005.352 (13): 1335-42, 2005.

Dias A, Cordeiro R. Association between hearing loss level and degree of discomfort introduced by tinnitus in workers exposed to noise. Braz J Otorhinolaryngol. 74(6): 876-83, 2008.

Duplessis C, Hoffer M. Tinnitus in an active duty navy diver: A review of inner ear barotrauma, tinnitus and its treatment. Undersear Hyperb Med. 33(4): 223-30, 2006.

Fitzgerald DC. Persistent dizziness following head trauma and perilymphatic fistula. Arch Phys Med Rehabil.76(11): 1017-20, 1995.

Fausti SA, Wilmington DJ, Gallun FJ, et al. Auditory and vestibular dysfunction associated with blast-related traumatic brain injury. J Rehabil Res Dev. 46(6): 797-810, 2009.

Gilles A, De Ridder D, Van Hal G,, et al. Prevalence of leisure noise-induced tinnitus and the attitude toward noise in university students. Otol Neurotol. 33(6): 899-906, 2012.

Hagberg M, Thiringer G, Brandstrom L. Incidence of tinnitus, impaired hearing and musculoskeletal disorders among students enrolled in academic music education—a retrospective cohort study. Int Arch Occup Environ Health. 78(7): 575-83, 2005.

Helfer TM, Jordan NN, Lee RB. Postdeployment hearing loss in U.S. Army soldiers seen at audiology clinics from April 1, 2003, through March 31, 2004. Am J Audiol 2005.14(2): 161-8, 2005.

Hoffer ME, Balaban C. The Impact of Blast on Balance. Presented at the International State-of-the-Science Meeting on Blast-Induced Tinnitus, November 15-16, 2011, Chantilly, VA, USA.

Hoffer ME, Balaban C, Gottshall K, et al. Blast exposure: vestibular consequences and associated characteristics. Otol Neurotol. 31(2): 232-6, 2010.

Hoffer ME, Wester D, Kopke RD, et al. Transtympanic management of tinnitus. Otolaryngol Clin North Am. 36(2): 353-8, 2003.

Jury MA, Flynn MC. Auditory and vestibular sequelae to traumatic brain injury: a pilot study. N Z Med J. 114(1134): 286-8, 2001.

Kronenberg J, Ben-Shoshan J, Wolf M. Perforated tympanic membrane after blast injury. Am J Otol .14(1): 92-4, 1993.

Kreuzer PM, Landgrebe M, Vielsmeier V, et al. Trauma-associated tinnitus. J Head Trauma Rehabil. 29(5): 432-42. 2014.

Liang W, Xiaofeng Y, Weiguo L et al,. Traumatic carotid cavernous fistula accompanying basilar skull fracture: a study on the incidence of traumatic carotid cavernous fistula in the patients with basilar skull fracture and prognostic analysis about traumatic carotid cavernous fistula. J Trauma. 63(5): 1014-20, 2007.

Mirza S, Richardson H. Otic Barotrauma from air travel. J Laryngol Otol. 119(5): 366-70, 2005.

Mrena R, Savolainen S, Kiukaanniemi H, et al. The effect of tightened hearing protection regulations on military noise-induced tinnitus. Int J Audiol. 48(6): 394-400, 2009.

Mrena R, Savolainen S, Kuokkanen JT, et al. Characteristics of tinnitus induced by acute acoustic trauma: a long-term follow-up. Audiol Neurootol.7 (2): 122-30, 2002.

National Center for Injury Prevention. Report to Congress on mild traumatic brain injury in the United States: Steps to prevent a serious public health problem. Atlanta, GA: Centers for Disease Control and Prevention. 2003.

Nicolas-Puel C, Akbaraly T, Lloyd R, et al. Characteristics of tinnitus in a population of 555 patients: specificities of tinnitus induced by noise trauma. Int Tinnitus J. 12(1): 64-70, 2006.

Nolle C, Todt I, Seidl RO, et al. Pathophysiological changes of the central auditory pathway after blunt trauma of the head. J Neurotrauma. 21(3): 251-8, 2004.

Oleksiak M, Smith BM, et al. Audiological issues and hearing loss among Veterans with mild traumatic brain injury. J Rehabil Res Dev. 49(7): 995-1004, 2012.

Ortmann M, Muller N, Schlee W, et al. Rapid increases of gamma power in the auditory cortex following noise trauma in humans. Eur J Neurosci. 33(3): 568-75, 2011.

Potier M, Hoquet C, Lloyd R, et al. The risks of amplified music for disc-jockeys working in nightclubs. Ear Hear. 30(2): 291-3, 2009.

Quintanilla-Dieck Mde L, Artunduaga MA, Eavey RD. Intentional exposure to loud music: the second MTV.com survey reveals an opportunity to educate. J Pediatr. 155(4): 550-5, 2009.

Redekop GJ. Extracranial carotid and vertebral artery dissection: a review. Can J Neurol Sci.35(2):146-52, 2008.

Rubak T, Kock S, Koefoef-Nielsen B, et al. The risk of tinnitus following occupational noise exposure in workers with hearing loss or normal hearing. Int J Audiol. 47(3): 109-14, 2008.

Schaette R, McAlpine D. Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci. 31(38): 13452-7, 2011.

Terrio H, Brenner LA, Ivins BJ, et al. Traumatic brain injury screening: preliminary findings in a US Army Brigade Combat Team. J Head Trauma Rehabil. 24(1): 14-23, 2009.

Tungsinmunkong S, Chongkolwatana C, Piyawongvisal W, et al. Blast injury of the ears: the experience from Yala Hospital, Southern Thailand. J Med Assoc Thai. 90(12): 2662-8, 2007.
Ulug T, Ulubil SA. Contralateral labyrinthine concussion in temporal bone fractures. J Otolaryngol 35(6):380-3, 2006.
US Department of Veteran Affairs. Annual Benefits Report Fiscal Year 2013. Washington, DC: Veterans Benefits Administration, US Department of Veterans Affairs. 2013. http://www.benefits.va.gov/reports/annual_performance_reports.asp. Accessed December 29th, 2015.

Yankaskas K. Prelude: noise-induced tinnitus and hearing loss in the military. Hear Res.295: 3-8. doi: 10.1016, 2013.

Yetiser S, Hidi Y, Birket H, et al. Traumatic ossicular dislocations: etiology and management. Am J Otolaryngol. 29(1): 31-6, 2008.

Ylikoski M, Pekkarinen JO, Starck JP, et al. Physical characteristics of gunfire impulse noise and its attenuation by hearing protectors. Scand Audiol .24(1): 3-11, 1995.

Yurgil KA, Clifford RE, Risbrough, et al. Prospective Associations Between Traumatic Brain Injury and Postdeployment Tinnitus in Active-Duty Marines. J Head Trauma Rehabil 2015.
ABOUT THE AUTHORS
Captain Michael E. Hoffer, MD, received his undergraduate degree from Stanford University and graduated from Medical School at the University of California, San Diego. After his Otolaryngology Residency at the University of Pennsylvania, he completed a neurotology fellowship with Dr. Herb Silverstein in Sarasota, Florida after which he was commissioned as an active duty officer in the United States Navy. Captain Hoffer is board certified in Otolaryngology and Neurotology and serves as specialty leader for Navy Otolaryngology. Dr. Hoffer serves on multiple national level boards including the council of the Triologic Society, the council of the National Institute of Deafness and Communication Disorders, and the NASA Neurologic IPT. He is a member of many national and international societies and considered an expert in inner ear drug delivery and audio-vestibular disorders after blunt and blast head trauma. Captain Hoffer has been deployed twice to Iraq serving with the U.S. Marines and is Fleet Marine Corps Officer Qualified.

Mikhaylo Szczupak, MD, is post-doctoral research fellow in the Department of Otolaryngology at the University of Miami.

To view list of other articles within Brain Injury Professional for this edition, click here.

By Flora M. Hammond, MD and James F. Malec, PhD

To some degree, we always knew that brain injury (BI) was a chronic condition. However, its presentation is often life-threatening and dramatic with the initial medical response so intensive, that it is easy to lose sight of the aftermath. After the initial storm passes — for those who survive the storm—life is often never the same. Individuals with BI and their families and close others often want to believe that once they leave the hospital things will soon return to normal. So early care providers may not belabor the reality that the return to normal may take months if not years — and even then, it is likely to be to a “new normal.”

Masel and DeWitt’s (2010) landmark article brought this reality clearly into focus. They described the medical implications and advantages of reconceptualizing BI as a chronic condition rather than as an “injury” which, like a broken bone, will heal with complete return to normal function. Although mechanisms remain controversial, renewed interest in chronic traumatic encephalopathy (CTE; McKee et al., 2009) reinforced this reality by identifying individuals for whom a traumatic BI appears to initiate a disease process resulting in neurological deterioration.

Survival after BI increased dramatically following the broader availability of emergency response teams in the community in the 1970s. We are only now beginning to witness how BI complicates normal aging as the first cohorts of these early survivors reach more advanced age. In this article, we review the nature of BI as a chronic condition, associated risks and increasing risks with advancing age, and the potential benefits of applying chronic disease management (CDM) strategies over the life time of individuals living with BI.

 

Chronic BI: Associated Risks

A recent Institute of Medicine (IOM) report (Ishibe et al., 2009) on the long term consequences of BI found convincing evidence in the literature that a history of traumatic BI is associated with increased risk for dementia and Parkinsonism, cognitive impairments and decline, seizure and hormonal disorders as well as long term emotional and social problems, and unemployment (Table 1). Many of these risks may be compounded by a normal aging process. Advancing age also increases risk for these same medical conditions as well as for social isolation and depression. The IOM reported suggestive evidence (Table 1) of increased risk for suicide and psychosis and that many of the risks associated with moderate-severe traumatic BI may also be present in cases of milder injury.

Marwitz and colleagues (2001) note that such co-morbid medical conditions may result in re-hospitalization after the initial injury, and that the reason for re-hospitalization varies with time post-injury. Seizures and psychiatric disorders tend to present in the first years after trauma; whereas, other conditions requiring hospitalization are more typical five years post-injury. A single traumatic BI significantly increases the risk of a subsequent traumatic BI with potentially even more severe and cumulative effects (Coronado et al., 2013). The risk for substance abuse may decline in the first few years after injury (Table 1), probably because greater disability and supervision during this early period reduces access. Studies of substance abuse in BI may also be biased by the dependence on the subjective report which requires both honest reporting and successful follow up contact. Hammond et al. (2000) documented a pattern of increasing illicit drug use over the first five years following BI. Upon initial impression it appears there is a flat 8-15% illicit drug use during the first 5 years post-injury. However, 45-76% of those reporting drug use were new reports from individuals who had declined drug use the prior year. While several studies have found shortened life expectancy following traumatic BI, in a tightly controlled study of mortality, Brown and colleagues (in press) found that the risk of death is no greater after traumatic BI than after other injuries when these two groups are equated for the severity of nonhead injuries. However, longevity is reduced for both brain and nonbrain injuries—suggesting that premature death may not be due to the BI itself but associated medical conditions.

Picture any individual with BI familiar to you and then imagine how his or her health and quality of life would be improved if this person had the opportunity simply to receive regular and routine follow-up with a written plan for ongoing care, education in self-management, and more intensive medical and psychosocial interventions as required.

The evidence of increased risk after BI for medical and psychosocial morbidity is clear. Additionally, data from the TBI Model Systems National Database (www.tbindsc.org) reveals that almost a third of individuals demonstrate functional decline over a 15 year period following traumatic BI (Figure 1). On a more positive note almost 40-45% are stable over this period, and about a quarter improve. Factors that contribute to the direction and slope of this functional trajectory are not well understood at this time, and may include the presence or absence of medical co-morbidities, genetic predisposition, and quality and consistency of ongoing care. That functional status remains stable or even improves in the majority of cases offers hope that, with more consistent follow-up and services and with continuing research, the proportion of cases showing decline can be reduced and decline itself can be progressively delayed.

Chronic Disease Management (CDM)

A chronic disease management (CDM) approach has been found to be the optimal way to address other medical conditions, such as, diabetes, asthma, high blood pressure, high cholesterol, that expose affected individuals to additional medical risks.

Primary features of the CDM approach include: (1) integration of care across organizational boundaries that is supported with information and communication technology, e.g., telehealth, smartphone apps, (2) patient self-management, and (3) guideline implementation and systems to promote standardized care (Fitzsimmons et al, 2012). More specifically, CDM is based on the best available evidence relevant to the target disorder and begins with a comprehensive evaluation and screening for commonly associated conditions. On the basis of these initial evaluations, well-defined treatment priorities and goals, including prevention and maintenance, are established and documented in written care plans. These goals and priorities are developed in active collaboration with patient, close others, other members of the medical and psychosocial team, and community partners. As clinical experience and research in chronic care of the target disorder becomes more available, detailed protocols for lifelong management can be disseminated in the field. The condition may be stratified by severity or other features that link to more specific interventions. Such protocols include stepped care plans that prescribe progressively more intensive interventions to more aggressively address the emergence or worsening of medical and psychosocial co-morbidities or functional decline. Most importantly, an active and defined follow-up schedule is established with regular re-evaluations and modification of the care plan as appropriate. These elements are summarized in the World Health Organization’s (WHO) General Principles of Good Chronic Care (WHO, 2004; Table 2).

As mentioned previously, an important component of CDM is engaging patients in active self-management of their conditions with the support of close others as required. It is estimated that individuals with chronically disabling conditions spend an average of only 2 hours out of the 8,760 hours available each year with their physician. Thus, to create change we must look beyond the traditional health professional encounters and empower the person with CBI to be in charge of their care. Self-management approaches activate, empower, and build a sense of self-efficacy through teaching patients and their close others how to monitor and manage their conditions as well as when to seek professional help. Education and implementation in self-management typically uses multiple modalities including individual and group sessions reinforced with written, web-based, and multi-media materials. As with CDM generally, self-management approaches can become more detailed and specific as research and experience in chronic care of a disorder develops to provide a basis for protocol-driven care.

CDM for BI

The increased risk of medical comorbidities as well as psychosocial and functional decline after BI justifies the implementation of a CDM approach to lifelong care following these types of injuries. The WHO principles for good chronic care (Table 2) provide a roadmap for this far-reaching practice change with expected benefits in improved health and quality of life for individuals with BI. Prevention or delay of functional decline is also a reasonable expectation as is an associated increase in the proportion who experience functional improvement over time post-BI. The field is not yet at the point of developing highly detailed, evidence-based protocols for management and self-management in BI CDM. However, such evidence will become available through ongoing research and clinical experience. Appropriate funding for both clinical care and research in BI CDM is critical to successful implementation. While the initial implementation of a CDM approach in BI may initially increase health care costs for this previously neglected group of patients, these costs should be offset over time as the prevalence of costly rehospitalizations, medical and psychosocial co-morbidities, and productivity loss is reduced.

Picture any individual with BI familiar to you and then imagine how his or her health and quality of life would be improved if this person had the opportunity simply to receive regular and routine follow-up with a written plan for ongoing care, education in self-management, and more intensive medical and psychosocial interventions as required.

References

Brown A, Leibson C, Mandrekar J, Ransom J, Malec J. Longterm survival after traumatic brain injury: A population-based analysis. Journal of Head Trauma Rehabilitation in press.

Coronado VG, McGuire LC, Faul M, Sugerman DE, Pearson WS. Traumatic brain injury epdiemiology and public health issues. In: Zasler ND, Katz DI, Zafonte RD (eds), Brain Injury Medicine (2nd ed), New York: DemosMedical, 2013.

Fitzsimons M, Normand C, Varley J, Delanty N. Evidencebased models of care for people with epilepsy. Epilepsy & Behavior 2012;23:1-6.

Hammond F, Donnelly K, Sasser H, Corrigan J, Bogner J, Weintraub A, Berry J, Kreutzer J. Illicit drug use over time following traumatic brain injury. Archives of Physical Medicine and Rehabilitation 2000;81:1260.

Ishibe N, Wlordarczyk RC, Fulco C. Overview of the Institute of Medicine’s committee search strategy and review process for Gulf War and health: Long-term consequences of traumatic brain injury. Journal of Head Trauma Rehabilitation 2009;24:424-9.

Marwitz JH, Cifu DX, Englander J, High WM, Jr. A multicenter analysis of rehospitalizations five years after brain injury. Journal of Head Trauma Rehabilitation 2001;16:307-17.

Masel BE, DeWitt DS. Traumatic brain injury: a disease process, not an event. Journal of Neurotrauma 2010;27:1529-40.

McKee AC, Cantu RC, Nowinski CJ, Hedley-Whyte ET, Gavett BE, Budson AE et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. Journal of Neuropathology & Experimental Neurology 2009;68:709-35. WHO. General Principles of Good Chronic Care 2004. Available from: www.who.int/hiv/pub/imai/generalprinciples082004.pdf.

 

About the authors

Flora M. Hammond, MD is a board certified physiatrist who completed her medical degree at Tulane University School of Medicine, Physical Medicine and Rehabilitation (PM&R) residency at Baylor College of Medicine, and brain injury fellowship at the Rehabilitation Institute of Michigan. Since December 2009, Dr. Hammond has served as the Covalt Professor and Chair of PM&R at the Indiana University School of Medicine (IUSM) and Chief of Medical Affairs at the Rehabilitation Hospital of Indiana (RHI). She also serves as the RHI Brain Injury Program Medical Director and Director of the NIDRR-funded TBI Model System at IUSM/RHI. Dr. Hammond is an experienced researcher who has conducted numerous clinical trials and prospective multicenter studies. She has authored more than 85 peer-reviewed publications. Her excellence in research, teaching, and administration has been acknowledged by receipt of the 2001 Association of Academic Physiatrists Young Academician Award from the Association of Academic Physiatrists and the 2011 Brain Injury Association of America William Caveness Award.

James F. Malec, PhD is Professor and Research Director in PM&R IUSM and RHI, Professor Emeritus of Psychology at the Mayo Clinic, and Board Certified in Clinical Neuropsychology and in Rehabilitation Psychology. Dr. Malec is currently Co-Director of the IUSM/RHI TBI Model System and directed the Mayo TBI Model System from 1999 through 2007. For the past 30 years, he has worked as a clinician and researcher in neuropsychology and brain injury rehabilitation with a particular interest in postacute rehabilitation and outcome measurement. He has over 130 peer-reviewed publications, and has received a number of professional recognitions including: the North American Brain Injury Society Research Award, and the Moody Prize for Distinguished Initiatives in Brain Injury Research and Rehabilita

Alex Nastaskin, MS, ORT/L, Katherine Scheponik, MS, ORT/L, Joe Padova, MS, ORT/L, Mike Tobin, BS

 Brain injury often results in upper extremity impairment, including weakness, spasticity, impaired range of motion, impaired sensation and impaired motor coordination. Muscle, tendon, and joint capsules may stiffen when held in a shortened position for an extended time. Since spastic or flaccid hemiparetic patients often have difficulty moving an arm, functionality declines in the impaired arm due to learned non-use in favor of the intact arm.

Research suggests that task-oriented training focusing on the practice of skilled and meaningful motor performance is a critical link to facilitating neural reorganization and “rewiring” in the central nervous system (Takahashi, et al., 2008). Robotics can provide an opportunity for a person to engage in a task-oriented, structured, multisensory experience.  For example, the patient may be required to move a virtual object on a screen to a virtual shelf. As the machine detects the patient’s physical movements, a visualization of the moved object appears on a screen, illustrating the accuracy and results of the patient’s efforts in real time. The patient can adjust the effort accordingly and perfect the desired motor pattern, supporting neural reorganization that may allow restoration of movement and functionality in the affected arm. These reliable, measurable robotics programs provide repetition, and the customization options make this intervention available to patients with varied motor impairments.

An increasing number of studies indicate that functional motor improvements largely occur through compensatory strategies rather than actual neurological recovery, particularly within the first few weeks following injury (Kwakkel, Kollen and Lindeman, 2004). For example, according to many upper limb robotics studies over the last decade, subjects typically show substantial improvements when performing functional tasks, while demonstrating little change in impairment measures (Hidler, et al., 2005). Thus, rather than demonstrating actual impairment reduction, patients learn to use their impaired systems more effectively. This is an area where motor control and learning principles may provide a basis for developing more effective treatments. Motor control principles dictate repetition of desired movements with kinesthetic and proprioceptive feedback. Robotic neurorehabilitation allows motor learning through practice of a diverse set of repeated tasks with the addition of visual feedback on the individual’s performance.

Following injury onset and during the subacute treatment stage, patients frequently develop maladaptive movement and/or positioning patterns that provide comfort, but impede function as neurological recovery progresses. Robotic neurorehabilitation can promote un-learning of these maladaptive movements, which is particularly important, as sub-optimal positioning may cause soft tissue shortening or stiffening—another obstacle to recovery. If a desired movement can be attained with practice, robotic intervention can provide a platform to help patients replace adverse positioning and non-functional movement with goal-directed movement. One evidence-supported example of this process is constrained-induced movement therapy (CIMT) (Peurala, et al., 2011).  In CIMT, the intact arm is constrained and patient must complete tasks with his or her affected arm. Robotic neurorehabilitation provides a similar approach with the additional application of resistive, assistive and gravity-eliminating forces. This promotes isolated and purposeful movement patterns, customized to the patient’s level of impairment.

A distinct advantage of robotic therapy is the ability to customize task demands, track progress, and make adjustments according to the patient’s improvement. The amount of assistance provided by the robotic orthosis can be modified as patient strength or mobility improves, to facilitate enduring gains. A spring-activated arm exoskeleton orthosis can partially relieve the upper limb’s weight, enabling the patient to initiate goal-directed movement while engaged in a virtual task or doing other tasks designed to incorporate elements of functional arm motion (Gijbels, et al., 2011). For some patients with perceptual deficits, visual scanning may impact how far they can move the affected arm. By enlarging objects and making the work space smaller (or less visually busy), patients with perceptual impairments associated with brain injury may more easily initiate active, goal-directed movement. Working in an environment with minimized distraction, patients can sustain their attention towards a task for longer periods of time, which can lead to more active participation.

A body of evidence demonstrates that following brain injury people retain the ability to generate accurate motor images of actions they cannot perform (Decety and Ingvar, 1990) and that mental practice of motor skills can improve actual performance (Jackson, et al., 2001). Common cerebral motor representations are activated when imaging and planning voluntary movements (Sirigu, et al., 1995). Combining robotic and mental imaging techniques integrates sensorimotor and cognitive stimulation. Thus, robotic orthoses can move a patient’s arm passively and/or provide assistance for active movement, creating an opportunity for kinesthetic and proprioceptive activation. Simultaneously, mental imagery applied during the robotic-assisted motion focuses the patient’s conscious attention on the desired motion. For example, reaching for a cup is an automated – mainly subcortical – activity for people without impairment. Focusing the patient’s conscious attention on the movements involved in reaching and grasping is crucial in order to help reacquire motor representations. 

Case Study 1:
Mrs. P., a 66-year-old female with status post left CVA and right hemiparesis was admitted to outpatient occupational therapy. She presented with a variation of flaccidity and low muscle tone throughout the right upper extremity.  Tactile sensations were intact and there was moderate-intensity pain of the right rotator cuff musculature. During her initial evaluation, Mrs. P. displayed no signs of active motion with her right upper extremity and demonstrated severe difficulty completing upper extremity dressing due to right shoulder pain.  Mrs. P. began twice weekly, 30-minute sessions of robotic arm training using a full-Mrs. P., arm spring-assisted exoskeleton orthosis. After two weeks of robotic training, Mrs. P. began to initiate active isolated motion with right shoulder horizontal abduction, adduction and elbow flexion. This increased active motion allowed Mrs. P. to recruit shoulder stabilizers, position her right arm with less risk of injury and decrease right shoulder pain. Mrs. P. also began actively using her right arm as a gross stabilizer during daily routine tasks.  

Case Study 2:
Mr. R., a 58-year-old male with status post left CVA and right hemiparesis was admitted to outpatient occupational therapy and presented with moderate spasticity and flexion synergy of the right upper extremity.  Mr. R. also demonstrated poor proprioceptive sensation and poor fine and gross motor coordination with minimal, non-functional active movement of the right hand. His therapy plan consisted of robotic intervention twice weekly for at least 30 minutes per session. Robotic training involved the use of a hand exoskeleton that performed continuous passive and active flexion and extension for digits 1 through 5. During robotic training, the therapist asked him to attend to the details of the task, feeling proprioceptive and kinesthetic inputs from the motion, and visualizing the mental actions needed to physically reproduce the movement. After four weeks of combined robotic and mental imagery training, Mr. R. began to display active motion with digits 1-3 and increased grip strength. This gain in active motion and grip strength allowed him to hold grooming articles and use his right hand as an assist to complete self-care routine tasks.

Summary
The use of robotics in upper limb neurorehabilitation is transforming the delivery of therapy for people with both acute and chronic challenges.  It also opens the door to new functional gains, preservation of range of motion and increased motor control. Robots are not equipped or intended to replace therapists but can facilitate therapy delivery and increase patient engagement and motivation. As electronic orthoses evolve, the next phase of robotic neurorehabilitation may feature personal exoskeleton devices that allow daily, self-directed practice at home or possibly other primary settings of productive activity. Autonomous practice may improve recovery through higher intensity and repetition of desired motor patterns and overall facilitate more efficient and effective care.

References
Takahashi, C. D., Der-Yeghiaian, L., Le, V., Motiwala, R. R., & Cramer, S. C. (2008). Robot-based hand motor therapy after stroke. Brain, 131(2), 425-437.
Kwakkel, G., Kollen, B., & Lindeman, E. (2004). Understanding the pattern of functional recovery after stroke: facts and theories. Restorative neurology and neuroscience, 22(3-5), 281-300.
Hidler, J., Nichols, D., Pelliccio, M., & Brady, K. (2015). Advances in the understanding and treatment of stroke impairment using robotic devices.
Peurala, S. H., Kantanen, M. P., Sjögren, T., Paltamaa, J., Karhula, M., & Heinonen, A. (2012). Effectiveness of constraint-induced movement therapy on activity and participation after stroke: a systematic review and meta-analysis of randomized controlled trials. Clinical rehabilitation, 26(3), 209-223.
Gijbels, D., Lamers, I., Kerkhofs, L., Alders, G., Knippenberg, E., & Feys, P. (2011). The Armeo Spring as training tool to improve upper limb functionality in multiple sclerosis: a pilot study. Journal of neuroengineering and rehabilitation, 8(5), 5.
Decety, J., & Ingvar, D. H. (1990). Brain structures participating in mental simulation of motor behavior: a neuropsychological interpretation. Acta Psychologica, 73(1), 13-34.
Jackson, P. L., Lafleur, M. F., Malouin, F., Richards, C., & Doyon, J. (2001). Potential role of mental practice using motor imagery in neurologic rehabilitation. Archives of physical medicine and rehabilitation, 82(8), 1133-1141.
Sirigu, A., Cohen, L., Duhamel, J. R., Pillon, B., Dubois, B., Agid, Y., & Pierrot-Deseilligny, C. (1995). Congruent unilateral impairments for real and imagined hand movements. Neuroreport, 6(7), 997-1001.

About the Authors
Alex Nastaskin, MS OTR/L has over 11 years of experience in both inpatient and outpatient neurological rehabilitation. His specialties include intervention models for right hemisphere stroke population and upper extremity robotic rehabilitation.  He is also certified in Kinesiotaping. 

Katherine Scheponik, MS, OTR/L is an outpatient occupational therapist and has also been a yoga instructor for 10 years with an interest in complementary and alternative therapies for neurological disorders.  

Joe Padova, OTR/L is the long-standing clinical specialist for outpatient neurological rehabilitation at MossRehab regarding upper limb amputee retraining, neurological rehabilitation, kinesiology, orthopedics, splinting, adaptive equipment design in integration of upper extremity robotic trainers for neurologic rehabilitations.

Mike Tobin, BS is an occupational therapy aide with an interest in upper limb robotics and assistive technology.