© Springer Science+Business Media New York 2015
Charles M. Zaroff and Rik Carl D’Amato (eds.)The Neuropsychology of MenIssues of Diversity in Clinical Neuropsychology10.1007/978-1-4899-7615-4_8Serving Men with Traumatic Brain Injuries
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Department of Educational Psychology, Ball State University, Teachers College, Room 543, Muncie, IN 47306, USA
Keywords
SexGenderMaleNeuropsychologyTraumatic brain injuryTBIPenetrating head injuryClosed head injuryIt is estimated that 1.7 million people suffer a traumatic brain injury (TBI) every year in the United States, and while most are treated and released, 52,000 die as a result (U.S. Department of Health and Human Services, 2010). Traumatic brain injury has a significant impact on children, and about 750 of 100,000 children experience a TBI every year (Anderson, Brown, Newitt, & Hoile, 2011). Although these numbers are concerning, improvements in technology as well as other advances are resulting in decreased mortality, albeit with increased morbidity, which means that neuropsychologists are likely to see more patients with TBI going forward. The Centers for Disease Control and Prevention (CDC; 2011) noted that the decrease in TBI-related deaths could be due to the increased use of seat belts, child safety seats, and motorcycle helmets, as well as changes in driver’s licensing and education programs, and improved pre-hospital triage and hospital care. The prevalence, severity, and functional implications of TBIs vary depending upon factors such as the patient’s age, the type of TBI, the number of previous TBIs, the location of the injury, the duration of coma and Post Traumatic Amnesia (PTA), secondary injuries, the degree of mechanical trauma, environmental risk, ethnicity, and resiliency factors, as well as other considerations (Davis & D’Amato, 2014; Lezak, Howieson, & Loring, 2004). The cognitive deficits that arise following a TBI can have a substantial impact on social, behavioral, and academic and/or vocational functioning, as well as the ability to independently perform activities of daily living. Furthermore, the cognitive and physical limitations associated with TBI may trigger or exacerbate stress within the family. In addition to these considerations, patient gender plays a significant role in the diagnosis and treatment of TBI. For example, males are nearly twice as likely as females to suffer a TBI (Bruns & Hauser, 2003), which also places them at increased risk for subsequent TBIs. Men may also suffer greater deficits following a TBI (Schopp, Shigaki, Johnstone, & Kirkpatrick, 2001), although the research on outcomes related to sex are somewhat mixed (and are reviewed later in this chapter). Other concerns that should be considered when working with men and TBI are related to comorbid psychiatric conditions such as depression or Post-Traumatic Stress Disorder (PTSD) that can impact the sequelae of TBI. For example, Carlson et al. (2011) reviewed the literature regarding TBI and PTSD and noted that in three studies evaluating Iraq and Afghanistan war veterans, the frequency of probable PTSD/mild TBI ranged from 5 to 7 %, although among the war veterans with probable mild TBI the frequency of probable PTSD ranged from 33 to 39 %. These results suggest that the presence of mild TBI is a significant risk factor for comorbid PTSD. This can be troublesome for treatment planning given the overlap between some of the symptoms of PTSD and TBI. Similarly, Vasterling et al. (2012) evaluated 760 soldiers pre- and post-deployment and found that 17.6 % of the soldiers with TBI screened positive for PTSD and 31.3 % had positive depression screens. In summary, the understanding of sex differences in TBI should be an important consideration of neuropsychologists and other members of the treatment team. An understanding of sex differences can result in a more appropriate understanding of the mechanism of injury, and may affect the approach to neuropsychological assessment, as well as facilitate improved care for the patient and their family.
Overview of Traumatic Brain Injury
Traumatic brain injuries can be broadly divided into two categories. The first, Closed Head Injuries (CHI), occur when the traumatic event does not result in significant penetration of the skull by a foreign object, and the brain injury and subsequent effects are related to translational and rotational forces acting on the brain (Greve & Zink, 2009). As such, in closed head injuries, the brain is not directly exposed to an outside object; rather, the mechanical forces inside the skull arising from the traumatic event are what cause brain damage. The other category of TBI, Penetrating Head Injuries (PHI) or Open Head Injuries (OHI) is present when penetration of the skull occurs such as in a gunshot wound. Neurocognitive deficits and outcome resulting from these injuries can be varied; although the type of deficits may be easier to predict based upon the focal site of the injury. In both types of TBI, it is also important for the treatment team to consider secondary effects of the brain injury as well.
Closed Head Injury . Damage from a closed head injury can occur in two stages: the primary injury and the secondary injury (Hannay, Howieson, Loring, Fischer, & Lezak, 2004). The first phase, or the primary injury, is the direct and immediate damage caused by mechanical forces operating on the brain. Contact force occurs as the result of an impact to the skull. This can occur via a static injury where the victim receives a blow to the head while remaining still. Damage initially occurs at the point of impact, with additional injury due to mechanical forces. Inertial forces may result in the brain moving with (translational acceleration), or rotating around (rotational acceleration), its center of gravity. This movement of the brain within the skull can cause the soft tissue of the brain to crash into the hard bony skull.
An additional concern with closed head injuries is cerebral contusions, which are the result of damage to the brain tissue and vascular structure; indeed, disruption of the vascular structure during closed head injuries can represent a substantial immediate threat to the patient’s life. Coup lesions are the result of damage at the point of impact and are associated with functional deficits in the domains associated with this area of the cortex. Contrecoup injuries are lesions opposite the site of the initial blow and are thus associated with neurocognitive deficits associated with the area of cortex opposite of the initial blow. Understanding the nature of the coup-contrecoup relationship is critical to neuropsychologists and the treatment team when working with men with CHI and is facilitated by a thorough understanding of functional neuroanatomy (see Chapter “Imaging and Development: Relevant Findings in Males” in this volume by Semrud-Clikeman & Robillard, in press) as well as how those deficits are expressed by men. Another significant concern with closed head injuries are the rapid acceleration and deceleration forces that act upon the neuronal axons, forces which can result in Diffuse Axonal Injury (DAI; Hannay et al., 2004). That is, the force of the injury may cause axons in the white matter to stretch, tear, or sheer. Patients with diffuse axonal injury may suffer significant deficits, in addition to the cortical impairments associated with the coup-contrecoup concerns, including slowed processing speed (Felmingham, Baguley, & Green, 2004), executive dysfunction (Fork et al., 2005; Scheid, Walther, Guthke, Preul, & von Cramon, 2006), and memory deficits (Chang, Kim, Kim, Bai, & Jang, 2010; Scheid et al., 2006).
The second phase of a closed head injury, the secondary injury, occurs as the result of the trauma the brain incurs following the initial impact and can represent the most immediate danger to the patient following the TBI. Secondary injuries may be the result of elevated intracranial pressure (ICP; Badri et al., 2012), edema (Greve & Zink, 2009), hypoxia (Padayachy et al., 2012), fever (Thompson, Pinto-Martin, & Bullock, 2003), or infection (Kourbeti et al., 2012). Increased ICP can arise from elevated blood volume in the skull and is of great concern to first responders arriving at the site of the trauma (Hannay et al., 2004). Effects of increased ICP on the brainstem can result in disruption of vital functions and cause death. Another significant concern following TBI is cerebral hypo-oxygenation, which is the leading cause of preventable death in patients sustaining a severe TBI (Arellano-Orden et al., 2011).
Penetrating Head Injury . Penetrating head injuries result from a foreign object penetrating the skull. Blood loss from the injury may result in hypotension (low blood pressure; Berry et al., 2012) and hypovolemia (low blood volume; Hannay et al., 2004). Contusions, especially at the site of entry, and hematomas, are also common (Ambrosi, Valenca, & Azevedo-Filho, 2012), as are effects of shockwaves that may be caused by the penetrating object (Hannay et al., 2004). The damage and functional implications resulting from the injury depend on the mass and velocity of the object, the site of the injury, the severity of the damage, as well as secondary effects. As with CHI, sequelae of PHI are also impacted by risk and resiliency factors, including psychiatric symptomatology. The prognosis in PHIs tends to be worse than CHIs in regard to mortality. As the damage resulting from these injuries is likely focal, survivors tend to have more localized cognitive deficits, although diffuse cognitive impairment may also be present; attention difficulties, memory deficits, and slowed processing are common in patients with PHI (Hannay et al., 2004). Seizure disorders may arise following PHI, and the effects of seizures, as well as the effects of anti-seizure medication, may also impact cognitive and behavioral functioning, and are further important treatment considerations.
Severity of Traumatic Brain Injuries
There are multiple ways to assess the severity of a TBI. One widely known measure of TBI severity is the Glasgow Coma Scale (GCS; Teasdale & Jennett, 1974). The GCS measures the level of consciousness on a 15-point scale and is assessed via verbal, nonverbal, and motor responses (Semrud-Clikeman & Bledsoe, 2011). However, given the complex sequelae that may accompany a TBI, the use of a single measure of TBI severity may be misleading, and longitudinal assessment is crucial. Additionally, an important caveat when using the GCS, as well as other measures of TBI severity, is that they can be influenced by other variables, such as alcohol intoxication (Schutte & Hanks, 2010), which may erroneously lead to lower scores at the time of injury. Duration of Loss of Consciousness (LOC) and length of Post-Traumatic Amnesia (PTA), or loss of memory for events following injury, are other measures of severity. Post-traumatic Amnesia, which is measured from the injury to the point where the patient can continuously form new memories, correlates highly with GCS (Hannay et al., 2004) and tends to last about four times as long as LOC (Hannay et al., 2004). Retrograde amnesia (not being able to recall events prior to the injury) may also accompany PTA.
Traumatic brain injuries typically fall into three categories of severity. Mild TBI can be defined in several ways, including PTA of generally less than one hour, or brief periods of LOC. Mild TBIs account for approximately 75 % of all head injuries (U.S. Department of Health and Human Services, 2010). Neuropsychological deficits associated with mild TBI typically include those in attention (Blanchet, Paradis-Giroux, Pepin, & Mckerral, 2009; Kwok, Lee, Leung, & Poon, 2008), memory (Kwok et al., 2008; Rohling et al., 2011; Tsirka et al., 2010), and processing speed (Johansson, Berglund, & Ronnback, 2009; Kwok et al., 2008). Of note, such cognitive deficits may be complicated by other TBI-related symptoms, such as headaches (Chaput, Giguere, Chancy, Denis, & Lavinge, 2009; Finkel, Yerry, Scher, & Choi, 2012), dizziness (Kaufman et al., 2006), sleep difficulties (Chaput et al., 2009; Milroy, Dorris, & McMillan, 2008), fatigue (Norrie et al., 2010), and irritability (Chaput et al., 2009). In most cases, symptoms from a mild TBI usually subside within the first few months and a return to premorbid activities is generally expected (Lange et al., 2012; Rohling et al., 2011), although some symptoms may persist (Fourtassi et al., 2011).
Moderate TBIs are generally characterized by PTA of less than 24 h (Hellawell, Taylor, & Pentland, 1999). Glasgow Coma Scale scores for moderate TBI generally fall between the range of 9 and 12. These injuries account for roughly 8–10 % of all TBIs (Hannay et al., 2004). Quick recovery is less likely in this group, with many still reporting memory disturbance (Colantonio et al., 2004; Horneman & Emanuelson, 2009) and daily functioning deficits (Colantonio et al., 2004) after injury.
Less than 10 % of all brain injuries fall in the severe category (Hannay et al., 2004), which may be classified as PTA of greater than one day. As with other classifications of TBI, cognitive and behavioral deficits vary depending upon the location of the injury, secondary factors, and other variables, although overall impairment tends to be more pervasive and persistent. One of the most common deficits in severe TBI is attention difficulties (Mathias & Mansfield, 2005; Satz et al., 1998; Zgaljardic & Temple, 2010). Processing speed (Colantonio et al., 2004; Horneman & Emanuelson, 2009) and memory deficits (Colantonio et al., 2004; Horneman & Emanuelson, 2009; Mathias & Mansfield, 2005; Satz et al., 1998; Zgaljardic & Temple, 2010) are also common in severe TBI. Many may also suffer executive dysfunction (Beauchamp et al., 2011; Demery, Larson, Dixit, Bauerand, & Perlstein, 2010; Krishnan, Smith, & Donders, 2012; Mathias & Mansfield, 2005; Zgaljardic & Temple, 2010) and word finding difficulties (Hough, 2008). The presence of subarachnoid hemorrhage has also been shown to indicate poorer visual-spatial abilities following severe TBI (Hanlon, Demery, Kuczen, & Kelly, 2005). Motor functioning problems may also persist and are likely to be present 6 months after injury (Satz et al., 1998).
Gender Differences in Prevalence of TBI
From the period of 1997–2007, TBI-related mortality decreased for both males and females, with an 8.5 % decline in males (30.5 per 100,000 to 27.9 per 100,000) and a 9.5 % decline in females (9.6 per 100,000 to 8.7 per 100,000). However, for each of these years the prevalence of TBI-related deaths for males was higher than for females, particularly among males aged 20–24 (Centers for Disease Control, 2011). Similarly, Bruns and Hauser (2003) found males at greater risk for TBI than females, with a male-to-female ratio of 1.5:1 to 1.7:1. They also determined that the pattern of greater prevalence of TBI in men relative to women is observed in other parts of the world, including South Africa (>4:1), Australia (2.7:1), France (2:1), and China (1.3:1). According to Bruns and Hauser, this substantially increased risk is due mostly to interpersonal violence and motor vehicle collisions during adolescence and young adulthood. They determined that in these age ranges, the male to female ratios were the highest, reaching 3 to 4:1. These ratios become smaller, or even inverted, at extreme ages.
Collins et al. (2013) examined 342 children who had experienced a TBI and found that sex differences in TBI were present beginning in infancy and progressed into adolescence. They determined that while falls were the leading cause of TBI in children, boys were less likely than girls to experience a fall resulting in a TBI (51–66 %). Interesting details emerged when the statistics were studied closely. Although boys were less likely than girls to experience a TBI as a result of a fall, boys were more likely to fall from a height: boys were more likely to fall more than 2 m, or 10 steps (29–12 %). Boys were also more likely to be injured on the road (30 % of boys in their sample) or struck by or against an object (17 % of boys in their sample). Boys were less likely to be injured at home compared to girls. Although their study did not show a difference in TBI severity using the GCS, boys were more likely to incur an extradural hematoma and girls were more likely to sustain a subdural hematoma.
There tends to be a reversal in gender rates of TBI in the elderly. In a study of 22,560 adults 65 years of age and older who suffered nonfatal fall-related injuries, 70.5 % were women (Stevens & Sogolow, 2005). Injury rates for the head and neck were highest among both men and women, although the rate for women was 33 % higher than for men. Men’s rate of TBI was exceeded by women above the age of 65, and women over 85 years of age had the highest rate. Stevens and Sogolow argued that the cause of this difference was related to the increased physical activity of men compared to women. The muscle weakness and decreased lower body strength associated with less physical activity in women puts them at higher risk of falls, and thus brain injury. Kraus, Peek-Asa, and McArthur (2000) found that men were significantly younger than women in a sample of moderate to severe TBI patients, with only 19.5 % being over the age of 50, compared to 32.9 % of women. They also found that men were more likely to be injured from assaults and bicycle crashes, while women were more likely to suffer injuries from motor vehicle accidents. There was no sex difference in injuries due to falls or from multiple traumas. Women in the sample presented with significantly higher Glasgow Coma Scale scores, despite having lower survival rates.
More and more media attention is being focused on the short- and long-term effects of traumatic brain injuries/concussions in sports and there appear to be sex differences in this area as well. Colvin et al. (2009) found that soccer players ranging in age from 8 to 24 years with a history of concussion performed significantly worse on cognitive tasks following a concussion, and men performed significantly better than females. Similarly, Covassin, Schatz, and Swanik (2007) found that despite no differences in neurocognitive functioning at baseline, following a concussion, females did more poorly on visual memory testing although men were more likely to report vomiting and sadness following concussion. Another study investigated sex differences in a group of males and females who had experienced concussions across nine different sports. Frommer et al. (2011) discovered that males and females reported about the same number of symptoms, although males reported more memory problems and confusion/disorientation while females reported more drowsiness and sensitivity to noise. Both groups reported headaches as the most prevalent symptom.
Sex Differences in Cognitive Deficits Following Traumatic Brain Injuries
In general, cognitive deficits related to TBI depend on a myriad of factors, including the type of head injury, the location of the injury, secondary factors, demographic variables, comorbid medical and psychiatric conditions, as well as other risk and resiliency factors. As such, despite having a good idea of the location of the injury, it can still be difficult to extrapolate neurocognitive deficits and the sequelae of recovery of those deficits. A common deficit observed in patients with a TBI is attention difficulties, which may be due in part to small lacerations throughout the brain; this damage may also result in slowed processing speed. Persisting attention and processing speed deficits can have the net effect of reduced cognitive efficiency, which in turn may present behaviorally as the patient requiring more effort to complete formerly simple tasks, resulting in fatigue and frustration.
Another potential consequence of TBI is language problems (Russell, Arenth, Scanlon, Kessler, & Ricker, 2012; Vu, Babikian, & Asarnow, 2011). However, the presence and extent of language problems largely depends upon the location of the injury, with obviously more expressive and receptive language deficits occurring in dominant hemisphere lesions. Word finding deficits have been shown to be present for all severities of TBI (Hough, 2008; King, Hough, Walker, Rastatter, & Holbert, 2006). Conversely, visual-spatial deficits are likely to be disproportionately present for non-dominant hemisphere injury.
Memory difficulties can be found in all types of TBI and sex differences in memory post-TBI are common, although the direction of these findings is inconsistent. Moore, Ashman, Cantor, Krinick, and Spielman (2010), in analyzing results of the Cambridge Neuropsychological Test Automated Battery (Morris, Evenden, Sahakian, & Robbins, 1986), found that men with mild traumatic brain injuries performed significantly worse than women on tasks of visual memory (Moore et al., 2010). They found no significant differences in visual memory in the moderate to severe TBI group and neither severity group showed significant gender differences in processing speed and executive functioning. On the other hand, in a study by Raskin, Mateer, and Tweeten (1998), in individuals with mild traumatic brain injury, men performed significantly worse than women on verbal learning tasks on the basis of results of the Wechsler Memory Scales—Revised (Wechsler, 1987) and California Verbal Learning Test (CVLT; Delis, Kramer, Kaplan, & Ober, 1987), but not on visual memory tasks. Further, men had significantly lower scores than women on tasks of attention based on the Symbol Digit Modalities Test (Smith, 1982) and Visual Speed and Accuracy Test (Grimsley, Ruch, & Warren, 1971), and on tasks of executive functioning, according to the Wisconsin Card Sorting Test (Grant & Berg, 1948) and Stroop Color Word Interference (Stroop, 1935). Men also showed deficits in reading speed when compared to women participants. Similar results have been found in children. Donders and Hoffman (2002) evaluated 60 children (30 males and 30 females) who had been diagnosed with a TBI using the California Verbal Learning Test—Children’s Version (CVLT-C; Delis, Kramer, Kaplan, & Ober, 1994). Boys performed significantly worse than girls, although the effect size for this difference was modest.
In considering the results of memory assessment in TBI, not only is the stimulus modality of material to be remembered important, but the memory processes themselves need to be considered. For instance, functional magnetic resonance imaging (fMRI) has shown greater activation during encoding tasks for a group of patients with a TBI compared to a control group, who in turn showed greater activation during recognition tasks (Arenth, Russell, Scanlon, Kessler, & Ricker, 2012). Prospective memory, or remembering to perform a certain task at a later time (Mathias & Mansfield, 2005; Pavawalla, Schmitter-Edgecombe, & Smith, 2012), and verbal declarative memory (Mathias & Mansfield, 2005) have also been shown to be impacted in patients with severe TBI.
Executive dysfunction has also been observed in patients with TBI, including deficits in planning (Krishnan et al., 2012) and cognitive flexibility (Zgaljardic & Temple, 2010), which may contribute to observed personality changes in patients with TBI. Poor response inhibition following TBI has been noted, although it may be attributed to slowed processing speed, fatigue, and under-arousal (Marco, McDonald, Kelly, Tate, & Johnstone, 2011). Working memory deficits may also be present (Vallat-Azouvi, Weber, Legrand, & Azouvi, 2007), although even in the absence of such deficits, neuroimaging can still reveal under-activation in working memory circuits (Chen et al., 2012). Executive dysfunction has been shown to result in greater social dysfunction and has been linked to social competence following TBI (Ganesalingam et al., 2011; McDonald, Saad, & James, 2011), which is not surprising given that many appropriate social interactions require inhibition, planning, and cognitive flexibility. Neuropsychologists working with men with TBI should factor in the age of the patient, their level of support, and their available coping resources when attempting to determine how these executive dysfunctions are likely to interfere with decision making, social interactions, driving, and independent completion of activities of daily living.
Studies examining multiple aspects of cognitive functioning have also found sex differences in performance. Ratcliff et al. (2007) found that men performed significantly worse than women on tests of attention, working memory, and language one year after traumatic brain injury. However, men appeared to perform better with visual analytic skills. Ratcliff et al. determined that the gender differences were not due to premorbid differences by analyzing normative data of the Controlled Oral Word Association Test (COWA; Benton & Hamsher, 1978), Symbol Digit Modalities Test (Smith, 1982), and Block Design test on the Wechsler Adult Intelligence Scale—Third Edition (WAIS-III; Wechsler, 1997).
Interestingly, the severity of overall deficits may vary between men and women. Koponen et al. (2002) found that all 8 of 58 patients with a mean post-injury time of 30 years with severe cognitive impairment according to the Mild Deterioration Battery (Portin et al., 2001) were men. Schopp et al. (2001) found that following traumatic brain injury, men, relative to women, experienced greater cognitive impairments on the Wechsler Adult Intelligence Scale—Revised (WAIS-R; Wechsler, 1981), greater general memory deficits on the Wechsler Memory Scale—Revised (Wechsler, 1987), and greater deficits in cognitive flexibility on the Trail Making Test B (Reitan, 1986). However, an analysis of decline from estimated levels of premorbid functioning revealed a greater decline for women in the areas of overall intelligence and attention, attributed by the authors to a greater rate of depression in women. Conversely, there was a greater decline in cognitive flexibility experienced by men, which was posited to be due to gender differences in the brain’s response to injury.
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