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INTRACRANIAL INJURIES RESULTING FROM BOXING
NEUROLOGIC ATHLETIC HEAD AND NECK INJURIES
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INTRACRANIAL INJURIES RESULTING FROM BOXING Allan J. Ryan, MD
The distinction between boxing and prizefighting has not always been clear through the ages. The former is a physical skill and the latter only a general definition of a combat to win a prize usually monetary, that may use a variety of physical means. The sport of boxing as we know it today derives from the ancient Greek religious festivals, which included many sports activities and contests, but particularly from the standards or rules that were established for the Olympic festivals. Boxing did not allow grappling, as did wrestling and pankration, a combination of both. It disappeared following the Roman introduction of gladiatorial combat, but was revived early in the fifteenth century by a Franciscan monk, Bernardine of Siena, who described it as “the parry and exchange of light blows.” He taught it to young men to discourage their use of clubs and knives against each other in the streets. At present, boxing is an international amateur sport governed by its own federation (Association Internationale de Boxe Amateur [AIBA]).The corresponding professional sport is prizefighting, usually abbreviated to ”fighting.” Fighting has been under attack periodically since the nineteenth century because of the public perception, for which there is certainly justification, that the fighter’s chief purpose is to disable his opponent, and that the best way to do this is to attack his brain through punching his head so that he is not able to function effectively, or at all. It is clear from the rules of boxing, as governed by the AIBA, that its chief purpose is to score points by landing punches on circumscribed areas of the body of the opponent but not to attack his consciousness deliberately by ”knocking him out.” There is no premium in the score for such an From the Sports Medicine Enterprise, Minneapolis, Minnesota
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event if it does occur, and the referee declares that the boxer is ”unable to continue.” Women are currently involved to a limited extent in both boxing and fighting. The purpose of this article is to review the available record of experience in boxing and fighting and the medical literature dealing with intracranial injuries in boxing and fighting, which have resulted in fatalities or chronic brain damage. The record of fatalities worldwide resulting from boxing and fighting in organized competition since World War I appears to be reasonably complete. However, determination of the degree of risk is difficult because of the lack of data dealing with the numbers of exposures to injury. Also, owing to lack of adequate follow-up examination and reports, as well as the possibilities that recognized deficiencies could be from other causes, we do not know the rate or ratio of chronic brain injury resulting from boxing and fighting. Six hundred and fifty-nine fatalities have been recorded from January 1918 to January 1, 1997, an average of less than 9 per year (Table l).32, 34 An increase has not been seen in the occurrence of these injuries in more recent years, despite better reporting and an apparent increase in the number of competitive events. In the 39-year period from January 1945 to January 1983, there were 353 fatalities.28There were only 50 deaths reported from the 12-year period from 1970 to 1981. During the period 1979 through 1983 only 28 were identified, and from 1984 to 1997 only 42; thus there appears to be a decreasing trend in the number of fa tali tie^.^^ We do not know the numbers of chronic brain injuries or the survivals in years of those so injured. Of the 70 fatalities that occurred from 1979 to 1997, the fighter’s weight classes were reported for 38. There was 1 heavyweight, 2 light heavyweights, 9 middleweights, 6 welterweights, 7 lightweights, 5 featherweights, 6 bantamweights, and 2 flyweights. All but 11of these deaths occurred in the United States with 3 in England, 3 in South Africa, and 1 each in Brazil, Italy, Japan, the Philippines, and Venezuela. The AIBA, which attempts to control and regulate all organized and amateur boxing, has added stipulations and rules in an attempt to promote safety. Limitations on the number of rounds, increased power of the referee to terminate a match in which one competitor is clearly outmatched, and better medical control over boxers who have had concussions before they can return for another bout have all been important. More thorough precompetition physical examinations and history taking by physicians who are experienced in working with boxers
Table 1. FATALITIES IN BOXING-1918 TO 1997 January 1918-June 6,1983 January 1945-Janualy 1983 January 1970-December 1981 January 1979-December 1983 January 1984-December 1996
645 deaths 353 deaths 50 deaths 28 deaths 42 deaths
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have kept those who are not properly qualified or prepared from undertaking serious risks in the ring. The MR imaging scan that can detect brain damage that cannot be detected or localized in any other way is used frequently not only for the diagnosis of acute brain injury but as a follow-up test to determine prognosis and future eligibility to box competively. There are no federal controls for professional fighting in the United States despite several efforts to establish it. Control depends on each state, and active state commissions are limited almost entirely to states where there is considerable fighting activity. Members of these commissions tend to be more interested in the welfare of fight promoters than the fighters. Some who have been denied licenses because of physical or other reasons in one or more states have been licensed in others. One state commission in recent years licensed a fighter who was legally blind in terms of effective vision. There have been improvements in requirements for ring flooring and the so-called ring ropes, and the thumbless boxing glove is now in general use although mandatory only in New York State. There is a serious deficiency in qualified managers or coaches who know how to teach boxing properly. MECHANISM OF BRAIN INJURY IN BOXING
The mechanism of the production of an injury to the brain and its coverings is complex because of both the effects of direct impact of the gloved fist on the skull and the relative motion of the brain and skull in response to this impact. These factors have been studied experimentally in both humans and animals by scientists interested in preventing brain injury in automobile and other accidents as well as in boxing and other sports, such as race driving and ice hockey. The brain is suspended within the skull by the attachment of its blood vessels and some nerve fibers to its tough elastic covering the dura mater, the outer layer of which is attached in several places to the periosteum of the inner surface of the skull, and by the cerebrospinal fluid that lies between the two inner coverings of the brain, the arachnoid membrane and the pia mater. This suspension allows some movement of the brain within the skull, and because of its relatively great weight, it manifests considerable inertia. When a gloved fist strikes the head, Mawdsley and FergusonZ7 pointed out that there is a transient acceleration of the head and some deformation of the skull, which is itself a living structure. The latter was demonstrated clearly in the studies of Gurdjian and Web~ter.'~ This happens whether or not the person struck is wearing a boxing or even a football helmet. The skull moves faster than the brain because of the inertia of the latter, and as the skull comes to rest the brain continues to move in the direction supplied by the impact. As Denny Brown and Russell1oexplained, the brain impacts one or several of the bony ridges or prominences of the skull's interior surface and the relatively sharp
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edge of the dural attachment. This causes the contusions or lacerations known as contre-coup injuries because they occur on the side of the brain opposite to the point of impact on the skull. At the same time, some of the force of impact is taken up directly by the brain, and small hemorrhages (called petechia) may occur in the cerebral hemispheres and even in the brain stem. These indicate the destruction of nerve cells (neurones) in these areas. These impact forces are said to be responsible for the syndrome of symptoms and findings that we call concussion. Concussion may cause a momentary decrease in consciousness or may result in a complete loss that is usually temporary but may be lasting if associated diffuse axonal injury, the second-impact syndrome, or acute subdural hematoma is also present. At the time of impact of the fist on the skull from the midline or in the vertical plane there are shearing strains on the brain and its coverings, as described by Holbourn,“j and swirling movements in the brain, as described by Pudenz and Sheldon.31These forces can cause damage in the neurones of the brain and degeneration of nerve fibers, as shown by S t r i ~ hEven . ~ ~ more important for the immediate effect, the cerebral veins that empty into the sinuses of the dura and that are thinwalled and do not have valves may be torn, producing the blood pool beneath the dura, which we call subdural hemorrhage. If the increased pressure on the brain from this event is not relieved, it may cause further damage to brain substance and even death. Further than this, according to Govons,” a forceful impact may stimulate the reticular activating center in the brain, which is critical in maintaining the erect posture. This may stimulate a postural righting reflex, which causes a rapid counter rotation of the head causing the concussed individual to fall forcefully to the floor of the ring. This knockout punch may create another impact on the head from its contact with the canvas, ring post, ropes, or even through the ropes onto a scorer’s table, as occurred in one boxer. The boxing helmet is not designed to absorb impacts of that type completely or successfully. The counter rotation can produce further damage to the brain and its blood vessels. ACUTE INJURIES
A study by the New York State Athletic Commission of acute boxing injuries suffered in the professional ring in New York from August 1,1982, through July 1,1984, reported by Jordan and Campbell,19 identified 376 that occurred in 3110 rounds of boxing. Of these, 262 were described as injuries to the head other than lacerations and eye injuries. Four of these fighters required hospitalization and one of them died. Roberts34examined 224 boxers of 250 who had been identified as a 1.5% random sample of 18,781 who had boxed professionally in the United Kingdom between 1929 and 1955. Thirty-seven (17%)had chronic neurologic sequelae of which 13 demonstrated characteristic post-trau-
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matic encephalopathy. Two suffered from frank dementia. Age, number of bouts, and heavy weights were factors associated with an increased frequency of neurologic sequelae. Jedlinski and associates17studied 60 amateur Polish boxers who had more than 100 bouts. Thirty-three (55%) showed positive neurologic signs, although frank encephalopathy was manifested in only 21.7%; severe damage, including dementia, was found in only 8.4%. Those who were heavier and had fought more bouts were more apt to exhibit these signs and symptoms. Thomassen and c o - w ~ r k e r sstudied ~~ 33 former champion amateur Danish boxers and compared them with 53 former First Division soccer players. They found no differences in the frequency and severity of neurologic symptoms and signs between the two groups. The Danish boxers, however, had averaged only half as many fights as the Polish ones. These studies suggest that the occurrence and severity of neurologic signs and symptoms in former boxers are a function of the number and frequency of bouts they have fought, and that boxers in the heavier weight classes are most apt to exhibit these findings. Whether it is due to the gradual accumulation of relatively minor brain injuries or to a greater number of more serious ones is not known. Some of the confusion that surrounds the diagnosis and management of the person who has suffered an acute brain injury or who manifests the chronic effects of repeated acute brain injuries arises from the proper definition of the term cerebral concussion. It is neither a symptom nor a diagnosis; instead the term describes a temporary state of the brain that occurs from several possible causes. Its use as a symptom causes a tendency to overlook the fact that an injury to the brain has occurred. Its use as a diagnosis raises, without answering, the question as to whether any pathologic change has taken place in the brain. Classifying concussion by degrees suggests that lesser or greater injury to the brain has occurred without specifying the location or character of the injury. This has led to the use of such nonspecific terms as serious and not serious. All this makes it difficult to establish whether there may be a cumulative effect of acute brain injuries that do not manifest overt and gross changes, making it difficult to establish guidelines for appropriate management. Rime1 and c011eagues~~ studied 538 nonboxers who had sustained minor head trauma, which was defined as a history of unconsciousness of 20 minutes or less, a Glascow Coma Scale score of 13 to 15, and hospitalization not exceeding 48 hours. Of these patients, 424 were evaluated 3 months after injury. The follow-up evaluation included a history of events since the accident, assessment of subjective complaints and objective measures such as employment status, a neurologic examination, a psychosocial assessment designed to estimate life stress, and a neuropsychologic test battery to measure high cortical function. Of these 424 patients, 79% complained of persistent headaches, and 59% de-
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scribed problems with memory. Of the patients who had been gainfully employed before the accident, 34% were unemployed 3 months later. Comparisons were then made between the employed and the unemployed groups. Three explanations for the high rate of unemployment were examined: (1) evidence of organic brain damage: Although the neurologic examination was completely normal in nearly all patients, neuropsychologic testing demonstrated some problems with attention, concentration, memory, or judgment in most of the 69 patients evaluated; (2) psychological responses to the injury: Emotional stress caused by persistent symptoms seems to be a significant factor in the long-term disability of these patients; and (3) litigation and compensation: These factors usually have a minor role in determining outcome after minor head injury. In conclusion, the most striking observations of these studies are the high rates of morbidity and unemployment in patients 3 months after a seemingly minor to moderate head injury and the evidence that many of these patients have, in fact, suffered organic brain injury. Delayed recovery of intellectual function and the cumulative effects l4 of concussion have been described by Gronwall and Wright~0n.l~. Patients who had suffered concussions were unable, for a period of time, to process information at a normal rate. The time taken to recover was related to the severity of the injury, and after uncomplicated concussion was usually less than 35 days. In those who experience persistent headache and other postconcussion syndromes, it often persisted beyond 35 days. Those who suffered a second concussion took longer to recover these information processing skills. The implications for boxers, who frequently suffer many more concussions, are obvious. CHRONIC INJURIES
There is good evidence to indicate that repeated brain injury, even though each individual injury produces minimal or unobservable immediate effects, causes chronic brain damage with degeneration and atrophy. Damaged central nervous system tissue does not regenerate. The ability of undamaged brain tissue to take over or compensate for the loss of damaged tissue is limited. It is therefore incumbent on those charged with the medical supervision of athletes to identify brain injury when it occurs, even when signs and symptoms may be minimal, and to allow the athlete to recover from that injury as much as possible before resuming sports competition. This may help to prevent a rapid summing up of the effects of acute brain injury. The persistence of signs and symptoms of brain injury may also call for the physician to recommend retirement from a sport, where there is grave danger of reinjury to the brain, before disabling chronic brain injury occurs. The nature of chronic brain injury in boxers and its results in terms of the individual’s behavior and longevity have been the subjects of many studies and publications since 1952. The term punch drunk is a
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long-standing popular one and was used as the title of an article by Martland,26a medical examiner who described a series of autopsies of persons who died with chronic brain injuries. Interestingly, none of these autopsies were boxers. Martland related his findings to the experience of some notable boxers who were said to have been afflicted with symptoms and behavior that might be related to chronic brain injuries. This article has been cited as the beginning of modern studies of chronic brain injuries in boxers. Busse and Silverman4 compared EEGs of boxers who had been knocked out in the ring with some taken on a control group of the same ages. There was a 37% occurrence of abnormal findings among the boxers. No correlation was found between the changes observed in different individuals. Kaplan and Browder,22working with the New York State Boxing Commission between 1950 and 1954, studied 1043 professional fighters including all divisions and types, recording a total of 1400 EEGs. Forty of these EEGs were made within 10 minutes after losing a fight. They observed the styles of the fighters at ringside, estimated the relationship of physical fitness and experience of their performance in the ring, and watched for the apparent effects of blows delivered to the head. Sixteenmillimeter regular speed and slow-motion films of the fights were made for later study. The defeated fighters were also given a gross neurologic examination in the dressing room immediately after the fight. The EEGs were analyzed to divide them into 12 categories. Thirty-four percent of the fighters had EEG patterns that fell within the normal range. When they were divided according to age, number of previous fights, style (slugger or boxer), ring rating, weight, number of bouts lost, and number of knockouts (10-second or technical), there were no significant differences between them based on disorganization of their EEGs. One hundred ninety-seven had from one to six repeat EEGs within the next 4 years, and one-fourth showed some change from their previous pattern. The only conclusion from this study was that those with the lower ring ratings had a higher percentage of disorganized EEGs. Johnson18examined 15 professional boxers about 22 years after their careers had ended and found that 11 showed diffuse pathologic EEG changes. Each boxer had had from 200 to 300 fights. EEG showed chronic brain damage in all but three. The incidence of serious mental and emotional disturbance was high. Kaste and associatesz3found EEG abnormalities in the brains of 6 of 14 Finnish boxers although 12 of the 14 showed no neurologic deficit. Sironi and c o - w ~ r k e r sfound ~ ~ EEG abnormalities in 3 of 10 young (ages 18 to 24) Italian boxers, and they were all in boxers who had been knocked out more than twice. Casson and associates5 studied 10 boxers (ages 20 to 31 years) who had been recently knocked out. Two had abnormal EEGs, although clinical findings were normal, but showed a cavum septi pellucidi on CT scan. Casson and colleagues6 reported studies of 13 former boxers, 2
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active fighters, and 3 active amateur boxers. The 13 who were between ages 25 and 60 years had not retired from boxing for medical, neurologic or psychiatric reasons, and were retired at least 1 year before the study. They had no history of neurologic, psychiatric, or serious medical illness and no known history of drug or alcohol abuse. The other five also met the last two criteria. All 18 were volunteers. They underwent the following tests: (1)a noncontrast computed two graphic CT scans of the brain, (2) an EEG, (3) a formal neurologic examination including mental status, (4) a battery of neuropsychological tests that included the Trail Making Test, the Digit Symbol Test, the Wechsler Memory Test (including both verbal and visual memory) and the Bender Gestalt Test (the standard administration and a 5-s recall administration). Eighty seven percent (13 of 15) of the former and active professional fighters had abnormal results on at least two of the four tests (neurologic examination, EEG, CT scan, and neuropsychologic test battery. The three active amateurs all had normal neurologic examination results, EEG, and CT scan. Eight of the former boxers had abnormal CT scans. One had cerebral cortical atrophy, two had central cerebral atrophy, and five had generalized cerebral atrophy. A cavum septum pellucidum was noted in three of these eight cases. Six of the eight with more than 20 bouts had abnormal CT scans, but only 2 of the 10 with less than 20 professional fights had abnormal CT scans. Four of the five highly ranked or champion professionals had abnormal CT scans, including the three septum pellucidum findings. Of the 13 who had EEGs, 7 had abnormal records and those had an impairment index of greater than 0.50 on the neuropsychological test battery. The investigators considered that the longer a professional fighter’s career lasted, the greater was the possibility of brain damage. A cumulative effect of multiple subconcussive blows appears to be the likely cause. With the availability of MR imaging of the brain, some investigators used it for diagnostic purposes on boxers and fighters. Levin and associa t e performed ~ ~ ~ MR imaging scans on nine young boxers (amateurs and early professionals) and failed to detect any abnormalities. Jordan and ZimmermanZ0performed MR imaging scans on nine amateur boxers who were knocked out or received excessive blows in the New York City Golden Gloves competition and also found no abnormalities. Jordan and ZimmermanZ1compared the results of CT and MR imaging scans in a referred population of 21 boxers ranging in age from 21 to 66 years. Sixteen were active professional fighters, 1 was a retired professional, and 4 were active amateur boxers. Eleven had both normal findings on CT and MR imaging and 7 had abnormal findings on both CT and MR imaging scans. There were no instances where abnormalities demonstrated by CT scanning were not detected by an MR imaging scan, but some abnormalities on MR imaging were not detected on CT scans. MR imaging also showed that three apparent positive findings in CT scans were artifacts. Lampert and hard mar^^^ described in detail the morphologic
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changes in brains of boxers that had been reported by others between 1928 and 1973 including subdural hemorrhages, intracerebral hemorrhages, diffuse axonal injury, cerebral edema, ischemia and herniation, cerebral atrophy, enlarged ventricles and septum cavum, cerebellar changes, loss of nerve cells in the substantia nigra, and neurofiburllary tangles. They did not report any new cases. Ross and c o - w ~ r k e r sexamined ~~ 38 former boxers and 2 current boxers with neurologic examinations (24), EEGs (24), CT scans (38), and a questionnaire concerning performance and medical history. Seven of the 24 EEG results were positive. Of the 11 boxers who had fewer than 50 bouts, 2 (18%)were positive; of 6 with 50 to 100 bouts, 4 (57%)were positive; and of the 7 with more than 100 bouts, 4 (57%)were positive. Beaussart and Beaussart-Boulenge,’ who performed EEGs on 123 amateur boxers before and within 15 minutes after bouts, found no evidence of pathologic changes, even in those who had been knocked out. Also, they failed to find any correlation between EEG changes and the severity of postconcussion syndrome in 3100 cases of the latter. Evaluation of chronic brain damage by other means, including EEG examination, began with Sere1 and J a r o ~ They . ~ ~ studied 1582 boxers from 1957 to 1961 and compared their neurologic findings with those in 100 nonboxers. Signs of chronic encephalopathy occurred in 9% of the boxers compared with 4% of the controls. Isolated reports of former boxers, who had died and whose brains were examined postmortem, have been published. Brandenburg and Hallervorden* found changes characteristic of Alzheimer’s disease in a 51-year-old former middleweight champion who had boxed as an amateur for 10 years and had begun to show clinical signs and symptoms of encephalopathy at age 38 years. Grahmann and Ulelz found brain atrophy and neurofibrillary tangles with large lateral ventricles and a cavum septi pellucidi in a former amateur and professional boxer who died at 48 years old with clinical evidence of chronic encephalopathy. Neuberger and colleaguesz9found cerebral atrophy with considerable gliosis throughout the cerebral cortex in the brains of two former boxers with clinical chronic encephalopathy. Spillane40found septa1 abnormalities in air encephalograms of four of five boxers with symptoms of chronic encephalopathy. Mawdsley and FergusonZ7examined 10 former boxers and obtained a postmortem examination of the brain in 1. Lumbar air encephalography in the other 9 showed abnormal findings in 8-specifically, evidence of enlarged lateral ventricles, cavum septi pellucidi, and evidence of cerebral and cerebellar atrophy. The examined brain showed all of these. Only one had a significantly abnormal EEG, although all had historic or clinical evidence of chronic encephalopathy. Constantinides and Tissot7 examined the brain of a 58-year-old boxer who had been fighting from age 17 to 24 years old and died following a long history of chronic encephalopathy with occasional
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epileptic seizures. They found neurofibrillary damage throughout the brain, cerebral atrophy, and a cavum septi pellucidi. Brennan and O’Conno? reported two deaths and one permanent invalid among amateur boxers who were Air Force personnel between 1963 and 1966. Neuberger and associatesz9found senile plaques and miniature scars in the grey matter in a cerebral biopsy of the frontal lobe of a former boxer who had suffered 30 knockouts in his career. In the brain of another boxer, who had chronic encephalopathy and died at age 53 years, were enlarged ventricles as well as brain atrophy with miniature scars on the grey matter. The report of the Royal College of Physicians (London), Committee on the Medical Aspects of Boxing, was presented by R0berts.3~This was a study of a random sample of 16,781 men who had boxed professionally in the United Kingdom from 1929 to 1955. Of the 224 examined, 37 (17%) demonstrated chronic neurologic symptoms or findings based on neurologic, psychometric, or EEG tests. Of these, 13 demonstrated classic chronic encephalopathy, and 2 had frank dementia. Older age, number of bouts, and heavier weights were all associated positively with these changes. The most complete and elaborate study of the brains of deceased boxers was published by Corsellis and co-workers.* Brains of 15 former boxers (12 professional, 3 amateur) were collected over a 16-year period. Their lives were investigated retrospectively through relatives, friends, hospital records, and boxing journals. Their ring careers extended over the period from 1900 to 1940. Two were world champions at one time and six were national or regional champions. Ages at death ranged from 57 to 91 years. Two of the boxers died after ventricular hemorrhage, and in both, the leaves of the septum were torn and separated, possibly as the result of the hemorrhage, so that they were excluded from further analysis. There was a striking difference between the septa of the 11 boxers and those of 500 controls. All but one of the boxers had a cavum, and in 10 or 12 it was fenestrated. Only 28% of the controls had a cavum, and in only 3% of the 500 was it accompanied by fenestration. The average width of the cavum in the boxers was three times that in the nonboxers. Five of the 15 nonboxers with a cavum and fenestration had firm clinical or other pathologic evidence of past head injury. Examination of the cerebellum showed cortical scarring on the inferior surface of the lateral lobes and significant losses of Purkinje’s cells on the ventral surface. These findings would be consistent with the cerebellum having been forced into the foramen magnum by the shock of impact. These findings are similar to those of Unterharn~cheidt?~ in cats whose brains were damaged experimentally. Degeneration and loss of pigmented cells in the substantia nigra and the presence of many neurofibrillary tangles, both of which are common findings in parkinsonism, were also noted in most of these boxers’ brains. The historic and clinical findings in the boxers in this study appeared to confirm and reinforce the pathology noted in their brains. Four had other single head injuries, none of which appeared serious.
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Many had been alcohol drinkers at one time or another, and 10 were reported to have drunk to excess. Four had cerebrovascular disease resulting in hemiplegia, and one had been treated successfully for tabes dorsalis. None of these conditions could have been responsible for the findings in their brains. Most had memory defects beginning, for the most part, early in life. For all but three, their memory disorders merged imperceptibly into a state of dementia. Some of the men remained addicted to violence long after they had stopped boxing. Cruikshank and colleagues9reported the cases of two young boxers who suffered acute intracranial hemorrhage not identified until 2 weeks later in one case and 2 months later in the other. The first had a hematoma occupying the left lateral ventricle, the head of the caudate nucleus, and the splenium of the corpus callosum. After a surgical evacuation of the hematoma, he made a good recovery. The second had a right parieto-occipital subdural hematoma that was excavated through burr holes with a complete recovery. In noncontrast CT scans of 10 boxers, performed within 1 week of their being knocked out, Casson and co-workers5found 5 normals. The others showed cerebral atrophy, and 1 a cavum septi pellucidi. They ranged in age from 18 to 22 years, and only 1had a minimally abnormal EEG. Four had 20 or more professional bouts. observed abnormal CT scans in 6 of 10 young Sironi and (18- to 24-year-old range) professional boxers. Four showed enlargements of the convexity of the central sulci, and 2 showed widening of the lateral and third ventricles. These were boxers who had been knocked out more than twice. Oleman and reviewed the reports of all personnel of the Army of the United Kingdom admitted to hospitals of the Royal Army Medical Corps during the years 1969 to 1980 and those who died or were medically discharged between 1952 and 1980. There were 437 admissions for boxing injuries, of which 296 (67.7%)were head injuries. Of these, 115 (39%) were for concussions and 69 (23%) for “intracranial injury of other and unspecified nature.” There were two cases (0.68%) of cerebral laceration and contusion, of which one resulted in a medical discharge. There were no deaths during this period. The only estimate of the population at risk is based on a random sample of 3185 Army personnel made in 1962 that found 113 engaged in boxing for an average of 4.9 hours per month each. If these ratios remained constant from 1969 to 1980, there would have been about 5700 men, each spending about 59 hours a year boxing. With an average of 35 injuries a year serious enough for hospital admission, 150 boxers would have been admitted per year, or one serious injury for every 9000 man hours of boxing. Among the 38 former boxers examined by Ross and colleagues36 who had CT scans, 24 also had a complete neurologic examination. Based on evaluation of the CT scans graded on a scale of 0 to 4 for evidence of cerebral atrophy and ventricular enlargement, there was a significant relationship between the numbers of bouts fought and the composite CT score, but this was due more to the presence of ventricular
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enlargement than to evidence of gyral atrophy. This was particularly striking because 25 had fewer than 100 bouts and only 5 had more than 150. The standard neurologic examination was of little value in detecting chronic cerebral damage because only 25% of the boxers showed positive findings. No psychometric tests were administered. It is difficult to evaluate the results of Rodriguez and associates35 who found regional cerebral blood flow to be significantly below normal in seven professional boxers. This finding would have to be correlated with EEG recordings, CT scans, and possibly postmortem brain examinations to determine how it might relate to boxing injury. SUMMARY AND CONCLUSIONS
A review of the available records indicates that there have been a substantial number of fatalities in primarily professional but also amateur boxers due to intracranial injuries sustained in the ring in comparison to the numbers of boxers at risk. The number of such fatalities has decreased steadily in recent years owing to different measures taken by boxing authorities to decrease the physical hazards in the ring and to improve monitoring of boxers during bouts by referees and physicians. The considerable concern about the long-term effects of repeated brain injury as the result of boxing in producing chronic encephalopathy is adequately justified by the many studies of live boxers and pathologic examinations of brains of former boxers made and recorded over the years since 1952. These indicate clearly a significant relationship between the numbers of bouts fought and the presence and severity of chronic encephalopathy. References 1. Beaussart M, Beaussart-Boulenge L Experimental study of cerebral concussions in 123 amateur boxers by clinical examination and EEG, before and immediately after fights. Electroencephalogr Clin Neurophysiol 29:529-530, 1970 2. Brandenburg W, Hallervorden J: Dementia1 Pugilistica mit anatenischem Befund. Virchows Arch Pathol Quatomil Physiol Klin Med 325:680-709, 1954 3. Brennan TN, OConnor PJ: Incidence of boxing injuries in the Royal Air Force in the United Kingdom 1953-66. Br J Ind Med 25:326-329, 1968 4. Busse EW, Silverman AJ: Electroencephalographic changes in professional boxers. JAMA 149:1522-1525, 1952 5. Casson IR, Sham R, Campbell EA, et al: Neurological and CT evaluation of knockedout boxers. J Neurol Neurosurg Psychiatry 453170-174, 1982 6 . Casson IR, Siege1 0, Sham R, et al: Brain damage in modem boxers. JAMA 25126632667, 1984 7. Constantinides J, Tissot R Lesions neurofibrillaires d’Alzheimer generalisees sans plaques seviles. Arch Suisses Neurol Neurochir Psychiatry 100:117-130, 1967 8. Corsellis JAN, Brutan CJ, Freeman-Browne D: The aftermath of boxing. Psycho1 Med 3270-303, 1973 9. Cruikshank JK, Higgens CS, Gray J R Two cases of intracranial hemorrhage in young amateur boxers. Lancet 1:626-627, 1980
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10. Denny Brown D, Russell WR Experimental cerebral concussion. Brain 64:7-163, 1941 11. Govons SR Brain concussion and p o s t u r e t h e knockdown blow of the boxing ring. Confinia Neurologica 30:77-84, 1968 12. Grahmann H, Ule G: Bietrag zur Genntuis der cluarischen cerebralen krankskeit Bilder bei boxem. Psychiatr Neurol 134:261-283, 1957 13. Gronwall D, Wrightson P: Delayed recovery of intellectual function after minor head injury. Lancet 2605-609, 1974 14. Gronwall E, Wrightson P: Cumulative effect of concussion. Lancet 2995, 1975 15. Gurdjian ES, Webster JE: Linear acceleration causing shear in the brain stem in trauma of the central nervous system. Mental Advances in Disease 2498, 1945 16. Holbourn AHS Mechanics of head injuries. Lancet 2438, 1943 17. Jedlinski J, Gatarski J, Szymusik A: Encephalopatha pugilistica (punch drunkedness). Acta Med Pol 12:443, 1971 18. Johnson J: Organic psychosyndromes due to boxing. Br J Psychiatry 115:4553, 1969 19. Jordan BD, Campbell EA: Acute boxing injuries among professional boxers in New York State: A two-year survey. In the 32nd Annual Meeting of the American College of Sports Medicine May 26-29, 1985 20. Jordan BD, Zimmerman RD: Magnetic resonance imaging in amateur boxers. Arch Neurol45:1207-1208, 1988 21. Jordan BD, Zimmerman RD: Computed tomography and magnetic resonance imaging comparisons in boxers. JAMA 263:1670-1674, 1990 22. Kaplan HA, Browder J: Observations on the clinical and brain wave patterns of professional boxers. JAMA 156:1138-1144, 1954 23. Kaste M, Vilkki J, Sainio K, et al: Is chronic brain damage in boxing a hazard of the past? Lancet 21186-1188,1982 24. Lampert PW, Hardman JM: Morphological changes in brains of boxers. JAMA 251:267&2679, 1984 25. Levin HS, Lippold SC, Goldman A, et a1 Neurobehavioral functioning and magnetic resonance imaging findings in young boxers. J Neurosurg 67657-667, 1987 26. Martland HS: Punch drunk. JAMA 91:1103-1107, 1928 27. Mawdsley C, Ferguson FR Neurological disease in boxers. Lancet 2795-801, 1983 28. Moore M: The challenge of boxing: Bringing safety into the ring. The Physician and Sports Medicine 8:lOl-105, 1980 29. Neuberger KT, Sintar DW, Denst J: Cerebral atrophy associated with boxing. Arch Neurol Psychiatry 81:403408, 1959 30. Oleman BJ, Rose CME, Arlow KJ: Boxing injuries in the Army. Journal of the Royal Army Medical Corps 129:22-27, 1983 31. Pudenz RH, Sheldon CH: The lucite calvarium: A method for direct observation of the brain. J Neurosurg 3:487-505, 1946 32. Putnam P: Going-Going-Gone. Sports Illustrated June 6: 23-46, 1983 33. Rime1 RW, Giordani B, Barth JT, et al: Disability caused by minor head injury. Neurosurgery 9221-228, 1981 34. Roberts A H Brain damage in boxers. London, Pitman Medical Science Publications, 1969 35. Rodriguez G, Ferrillo F, Montano V, et a1 Regional cerebral blood flow in boxers. Lancet 2858, 1983 36. Ross RJ, Cole C, Thompson JS, et al: Boxers-computed tomography, EEG, and neurological evaluation. JAMA 249:211-214, 1983 37. Ryan AJ: Personal observations from 50 years of following boxing and collecting factual information from media sources. 38. Sere1 M, Jaros 0 The mechanisms of cerebral concussion in boxing and their consequences. World Neurol3:351-358, 1962 39. Sironi VA, Scotti G, Ravagnati L, et al: CT scan and EEG findings in professional pugilists: Early detection of cerebral atrophy in young boxers. J Neurosurg Sci 26:165168, 1982 40. Spillane JD: Five boxers. BMJ 21205-1210, 1962 41. Strich SJ: Shearing of nerve fibers as a cause of brain damage due to head injury. Lancet 2443448,1961
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42. Thomassen A, Juul-Jensen P, Olivarius B, et al: Neurological electroencephalographic and neuropsychological examination of 53 former amateur boxers. Acta Neurol Scand 60~352-362,1979 43. Unterharnscheidt FJ: Injuries due to boxing and other sports. In Viuken PJ, Bruyra GW (eds): Handbook of Clinical Neurology, vol 23. Amsterdam, North-Holland, 1975, pp 527-593
Address reprint requests to Allan J. Ryan, MD 5800 Jeff Place Edina, MN 55436
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INTRACRANIAL INJURIES RESULTING FROM BOXING Allan J. Ryan, MD
The distinction between boxing and prizefighting has not always been clear through the ages. The former is a physical skill and the latter only a general definition of a combat to win a prize usually monetary, that may use a variety of physical means. The sport of boxing as we know it today derives from the ancient Greek religious festivals, which included many sports activities and contests, but particularly from the standards or rules that were established for the Olympic festivals. Boxing did not allow grappling, as did wrestling and pankration, a combination of both. It disappeared following the Roman introduction of gladiatorial combat, but was revived early in the fifteenth century by a Franciscan monk, Bernardine of Siena, who described it as “the parry and exchange of light blows.” He taught it to young men to discourage their use of clubs and knives against each other in the streets. At present, boxing is an international amateur sport governed by its own federation (Association Internationale de Boxe Amateur [AIBA]).The corresponding professional sport is prizefighting, usually abbreviated to ”fighting.” Fighting has been under attack periodically since the nineteenth century because of the public perception, for which there is certainly justification, that the fighter’s chief purpose is to disable his opponent, and that the best way to do this is to attack his brain through punching his head so that he is not able to function effectively, or at all. It is clear from the rules of boxing, as governed by the AIBA, that its chief purpose is to score points by landing punches on circumscribed areas of the body of the opponent but not to attack his consciousness deliberately by ”knocking him out.” There is no premium in the score for such an From the Sports Medicine Enterprise, Minneapolis, Minnesota
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event if it does occur, and the referee declares that the boxer is ”unable to continue.” Women are currently involved to a limited extent in both boxing and fighting. The purpose of this article is to review the available record of experience in boxing and fighting and the medical literature dealing with intracranial injuries in boxing and fighting, which have resulted in fatalities or chronic brain damage. The record of fatalities worldwide resulting from boxing and fighting in organized competition since World War I appears to be reasonably complete. However, determination of the degree of risk is difficult because of the lack of data dealing with the numbers of exposures to injury. Also, owing to lack of adequate follow-up examination and reports, as well as the possibilities that recognized deficiencies could be from other causes, we do not know the rate or ratio of chronic brain injury resulting from boxing and fighting. Six hundred and fifty-nine fatalities have been recorded from January 1918 to January 1, 1997, an average of less than 9 per year (Table l).32, 34 An increase has not been seen in the occurrence of these injuries in more recent years, despite better reporting and an apparent increase in the number of competitive events. In the 39-year period from January 1945 to January 1983, there were 353 fatalities.28There were only 50 deaths reported from the 12-year period from 1970 to 1981. During the period 1979 through 1983 only 28 were identified, and from 1984 to 1997 only 42; thus there appears to be a decreasing trend in the number of fa tali tie^.^^ We do not know the numbers of chronic brain injuries or the survivals in years of those so injured. Of the 70 fatalities that occurred from 1979 to 1997, the fighter’s weight classes were reported for 38. There was 1 heavyweight, 2 light heavyweights, 9 middleweights, 6 welterweights, 7 lightweights, 5 featherweights, 6 bantamweights, and 2 flyweights. All but 11of these deaths occurred in the United States with 3 in England, 3 in South Africa, and 1 each in Brazil, Italy, Japan, the Philippines, and Venezuela. The AIBA, which attempts to control and regulate all organized and amateur boxing, has added stipulations and rules in an attempt to promote safety. Limitations on the number of rounds, increased power of the referee to terminate a match in which one competitor is clearly outmatched, and better medical control over boxers who have had concussions before they can return for another bout have all been important. More thorough precompetition physical examinations and history taking by physicians who are experienced in working with boxers
Table 1. FATALITIES IN BOXING-1918 TO 1997 January 1918-June 6,1983 January 1945-Janualy 1983 January 1970-December 1981 January 1979-December 1983 January 1984-December 1996
645 deaths 353 deaths 50 deaths 28 deaths 42 deaths
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have kept those who are not properly qualified or prepared from undertaking serious risks in the ring. The MR imaging scan that can detect brain damage that cannot be detected or localized in any other way is used frequently not only for the diagnosis of acute brain injury but as a follow-up test to determine prognosis and future eligibility to box competively. There are no federal controls for professional fighting in the United States despite several efforts to establish it. Control depends on each state, and active state commissions are limited almost entirely to states where there is considerable fighting activity. Members of these commissions tend to be more interested in the welfare of fight promoters than the fighters. Some who have been denied licenses because of physical or other reasons in one or more states have been licensed in others. One state commission in recent years licensed a fighter who was legally blind in terms of effective vision. There have been improvements in requirements for ring flooring and the so-called ring ropes, and the thumbless boxing glove is now in general use although mandatory only in New York State. There is a serious deficiency in qualified managers or coaches who know how to teach boxing properly. MECHANISM OF BRAIN INJURY IN BOXING
The mechanism of the production of an injury to the brain and its coverings is complex because of both the effects of direct impact of the gloved fist on the skull and the relative motion of the brain and skull in response to this impact. These factors have been studied experimentally in both humans and animals by scientists interested in preventing brain injury in automobile and other accidents as well as in boxing and other sports, such as race driving and ice hockey. The brain is suspended within the skull by the attachment of its blood vessels and some nerve fibers to its tough elastic covering the dura mater, the outer layer of which is attached in several places to the periosteum of the inner surface of the skull, and by the cerebrospinal fluid that lies between the two inner coverings of the brain, the arachnoid membrane and the pia mater. This suspension allows some movement of the brain within the skull, and because of its relatively great weight, it manifests considerable inertia. When a gloved fist strikes the head, Mawdsley and FergusonZ7 pointed out that there is a transient acceleration of the head and some deformation of the skull, which is itself a living structure. The latter was demonstrated clearly in the studies of Gurdjian and Web~ter.'~ This happens whether or not the person struck is wearing a boxing or even a football helmet. The skull moves faster than the brain because of the inertia of the latter, and as the skull comes to rest the brain continues to move in the direction supplied by the impact. As Denny Brown and Russell1oexplained, the brain impacts one or several of the bony ridges or prominences of the skull's interior surface and the relatively sharp
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edge of the dural attachment. This causes the contusions or lacerations known as contre-coup injuries because they occur on the side of the brain opposite to the point of impact on the skull. At the same time, some of the force of impact is taken up directly by the brain, and small hemorrhages (called petechia) may occur in the cerebral hemispheres and even in the brain stem. These indicate the destruction of nerve cells (neurones) in these areas. These impact forces are said to be responsible for the syndrome of symptoms and findings that we call concussion. Concussion may cause a momentary decrease in consciousness or may result in a complete loss that is usually temporary but may be lasting if associated diffuse axonal injury, the second-impact syndrome, or acute subdural hematoma is also present. At the time of impact of the fist on the skull from the midline or in the vertical plane there are shearing strains on the brain and its coverings, as described by Holbourn,“j and swirling movements in the brain, as described by Pudenz and Sheldon.31These forces can cause damage in the neurones of the brain and degeneration of nerve fibers, as shown by S t r i ~ hEven . ~ ~ more important for the immediate effect, the cerebral veins that empty into the sinuses of the dura and that are thinwalled and do not have valves may be torn, producing the blood pool beneath the dura, which we call subdural hemorrhage. If the increased pressure on the brain from this event is not relieved, it may cause further damage to brain substance and even death. Further than this, according to Govons,” a forceful impact may stimulate the reticular activating center in the brain, which is critical in maintaining the erect posture. This may stimulate a postural righting reflex, which causes a rapid counter rotation of the head causing the concussed individual to fall forcefully to the floor of the ring. This knockout punch may create another impact on the head from its contact with the canvas, ring post, ropes, or even through the ropes onto a scorer’s table, as occurred in one boxer. The boxing helmet is not designed to absorb impacts of that type completely or successfully. The counter rotation can produce further damage to the brain and its blood vessels. ACUTE INJURIES
A study by the New York State Athletic Commission of acute boxing injuries suffered in the professional ring in New York from August 1,1982, through July 1,1984, reported by Jordan and Campbell,19 identified 376 that occurred in 3110 rounds of boxing. Of these, 262 were described as injuries to the head other than lacerations and eye injuries. Four of these fighters required hospitalization and one of them died. Roberts34examined 224 boxers of 250 who had been identified as a 1.5% random sample of 18,781 who had boxed professionally in the United Kingdom between 1929 and 1955. Thirty-seven (17%)had chronic neurologic sequelae of which 13 demonstrated characteristic post-trau-
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matic encephalopathy. Two suffered from frank dementia. Age, number of bouts, and heavy weights were factors associated with an increased frequency of neurologic sequelae. Jedlinski and associates17studied 60 amateur Polish boxers who had more than 100 bouts. Thirty-three (55%) showed positive neurologic signs, although frank encephalopathy was manifested in only 21.7%; severe damage, including dementia, was found in only 8.4%. Those who were heavier and had fought more bouts were more apt to exhibit these signs and symptoms. Thomassen and c o - w ~ r k e r sstudied ~~ 33 former champion amateur Danish boxers and compared them with 53 former First Division soccer players. They found no differences in the frequency and severity of neurologic symptoms and signs between the two groups. The Danish boxers, however, had averaged only half as many fights as the Polish ones. These studies suggest that the occurrence and severity of neurologic signs and symptoms in former boxers are a function of the number and frequency of bouts they have fought, and that boxers in the heavier weight classes are most apt to exhibit these findings. Whether it is due to the gradual accumulation of relatively minor brain injuries or to a greater number of more serious ones is not known. Some of the confusion that surrounds the diagnosis and management of the person who has suffered an acute brain injury or who manifests the chronic effects of repeated acute brain injuries arises from the proper definition of the term cerebral concussion. It is neither a symptom nor a diagnosis; instead the term describes a temporary state of the brain that occurs from several possible causes. Its use as a symptom causes a tendency to overlook the fact that an injury to the brain has occurred. Its use as a diagnosis raises, without answering, the question as to whether any pathologic change has taken place in the brain. Classifying concussion by degrees suggests that lesser or greater injury to the brain has occurred without specifying the location or character of the injury. This has led to the use of such nonspecific terms as serious and not serious. All this makes it difficult to establish whether there may be a cumulative effect of acute brain injuries that do not manifest overt and gross changes, making it difficult to establish guidelines for appropriate management. Rime1 and c011eagues~~ studied 538 nonboxers who had sustained minor head trauma, which was defined as a history of unconsciousness of 20 minutes or less, a Glascow Coma Scale score of 13 to 15, and hospitalization not exceeding 48 hours. Of these patients, 424 were evaluated 3 months after injury. The follow-up evaluation included a history of events since the accident, assessment of subjective complaints and objective measures such as employment status, a neurologic examination, a psychosocial assessment designed to estimate life stress, and a neuropsychologic test battery to measure high cortical function. Of these 424 patients, 79% complained of persistent headaches, and 59% de-
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scribed problems with memory. Of the patients who had been gainfully employed before the accident, 34% were unemployed 3 months later. Comparisons were then made between the employed and the unemployed groups. Three explanations for the high rate of unemployment were examined: (1) evidence of organic brain damage: Although the neurologic examination was completely normal in nearly all patients, neuropsychologic testing demonstrated some problems with attention, concentration, memory, or judgment in most of the 69 patients evaluated; (2) psychological responses to the injury: Emotional stress caused by persistent symptoms seems to be a significant factor in the long-term disability of these patients; and (3) litigation and compensation: These factors usually have a minor role in determining outcome after minor head injury. In conclusion, the most striking observations of these studies are the high rates of morbidity and unemployment in patients 3 months after a seemingly minor to moderate head injury and the evidence that many of these patients have, in fact, suffered organic brain injury. Delayed recovery of intellectual function and the cumulative effects l4 of concussion have been described by Gronwall and Wright~0n.l~. Patients who had suffered concussions were unable, for a period of time, to process information at a normal rate. The time taken to recover was related to the severity of the injury, and after uncomplicated concussion was usually less than 35 days. In those who experience persistent headache and other postconcussion syndromes, it often persisted beyond 35 days. Those who suffered a second concussion took longer to recover these information processing skills. The implications for boxers, who frequently suffer many more concussions, are obvious. CHRONIC INJURIES
There is good evidence to indicate that repeated brain injury, even though each individual injury produces minimal or unobservable immediate effects, causes chronic brain damage with degeneration and atrophy. Damaged central nervous system tissue does not regenerate. The ability of undamaged brain tissue to take over or compensate for the loss of damaged tissue is limited. It is therefore incumbent on those charged with the medical supervision of athletes to identify brain injury when it occurs, even when signs and symptoms may be minimal, and to allow the athlete to recover from that injury as much as possible before resuming sports competition. This may help to prevent a rapid summing up of the effects of acute brain injury. The persistence of signs and symptoms of brain injury may also call for the physician to recommend retirement from a sport, where there is grave danger of reinjury to the brain, before disabling chronic brain injury occurs. The nature of chronic brain injury in boxers and its results in terms of the individual’s behavior and longevity have been the subjects of many studies and publications since 1952. The term punch drunk is a
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long-standing popular one and was used as the title of an article by Martland,26a medical examiner who described a series of autopsies of persons who died with chronic brain injuries. Interestingly, none of these autopsies were boxers. Martland related his findings to the experience of some notable boxers who were said to have been afflicted with symptoms and behavior that might be related to chronic brain injuries. This article has been cited as the beginning of modern studies of chronic brain injuries in boxers. Busse and Silverman4 compared EEGs of boxers who had been knocked out in the ring with some taken on a control group of the same ages. There was a 37% occurrence of abnormal findings among the boxers. No correlation was found between the changes observed in different individuals. Kaplan and Browder,22working with the New York State Boxing Commission between 1950 and 1954, studied 1043 professional fighters including all divisions and types, recording a total of 1400 EEGs. Forty of these EEGs were made within 10 minutes after losing a fight. They observed the styles of the fighters at ringside, estimated the relationship of physical fitness and experience of their performance in the ring, and watched for the apparent effects of blows delivered to the head. Sixteenmillimeter regular speed and slow-motion films of the fights were made for later study. The defeated fighters were also given a gross neurologic examination in the dressing room immediately after the fight. The EEGs were analyzed to divide them into 12 categories. Thirty-four percent of the fighters had EEG patterns that fell within the normal range. When they were divided according to age, number of previous fights, style (slugger or boxer), ring rating, weight, number of bouts lost, and number of knockouts (10-second or technical), there were no significant differences between them based on disorganization of their EEGs. One hundred ninety-seven had from one to six repeat EEGs within the next 4 years, and one-fourth showed some change from their previous pattern. The only conclusion from this study was that those with the lower ring ratings had a higher percentage of disorganized EEGs. Johnson18examined 15 professional boxers about 22 years after their careers had ended and found that 11 showed diffuse pathologic EEG changes. Each boxer had had from 200 to 300 fights. EEG showed chronic brain damage in all but three. The incidence of serious mental and emotional disturbance was high. Kaste and associatesz3found EEG abnormalities in the brains of 6 of 14 Finnish boxers although 12 of the 14 showed no neurologic deficit. Sironi and c o - w ~ r k e r sfound ~ ~ EEG abnormalities in 3 of 10 young (ages 18 to 24) Italian boxers, and they were all in boxers who had been knocked out more than twice. Casson and associates5 studied 10 boxers (ages 20 to 31 years) who had been recently knocked out. Two had abnormal EEGs, although clinical findings were normal, but showed a cavum septi pellucidi on CT scan. Casson and colleagues6 reported studies of 13 former boxers, 2
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active fighters, and 3 active amateur boxers. The 13 who were between ages 25 and 60 years had not retired from boxing for medical, neurologic or psychiatric reasons, and were retired at least 1 year before the study. They had no history of neurologic, psychiatric, or serious medical illness and no known history of drug or alcohol abuse. The other five also met the last two criteria. All 18 were volunteers. They underwent the following tests: (1)a noncontrast computed two graphic CT scans of the brain, (2) an EEG, (3) a formal neurologic examination including mental status, (4) a battery of neuropsychological tests that included the Trail Making Test, the Digit Symbol Test, the Wechsler Memory Test (including both verbal and visual memory) and the Bender Gestalt Test (the standard administration and a 5-s recall administration). Eighty seven percent (13 of 15) of the former and active professional fighters had abnormal results on at least two of the four tests (neurologic examination, EEG, CT scan, and neuropsychologic test battery. The three active amateurs all had normal neurologic examination results, EEG, and CT scan. Eight of the former boxers had abnormal CT scans. One had cerebral cortical atrophy, two had central cerebral atrophy, and five had generalized cerebral atrophy. A cavum septum pellucidum was noted in three of these eight cases. Six of the eight with more than 20 bouts had abnormal CT scans, but only 2 of the 10 with less than 20 professional fights had abnormal CT scans. Four of the five highly ranked or champion professionals had abnormal CT scans, including the three septum pellucidum findings. Of the 13 who had EEGs, 7 had abnormal records and those had an impairment index of greater than 0.50 on the neuropsychological test battery. The investigators considered that the longer a professional fighter’s career lasted, the greater was the possibility of brain damage. A cumulative effect of multiple subconcussive blows appears to be the likely cause. With the availability of MR imaging of the brain, some investigators used it for diagnostic purposes on boxers and fighters. Levin and associa t e performed ~ ~ ~ MR imaging scans on nine young boxers (amateurs and early professionals) and failed to detect any abnormalities. Jordan and ZimmermanZ0performed MR imaging scans on nine amateur boxers who were knocked out or received excessive blows in the New York City Golden Gloves competition and also found no abnormalities. Jordan and ZimmermanZ1compared the results of CT and MR imaging scans in a referred population of 21 boxers ranging in age from 21 to 66 years. Sixteen were active professional fighters, 1 was a retired professional, and 4 were active amateur boxers. Eleven had both normal findings on CT and MR imaging and 7 had abnormal findings on both CT and MR imaging scans. There were no instances where abnormalities demonstrated by CT scanning were not detected by an MR imaging scan, but some abnormalities on MR imaging were not detected on CT scans. MR imaging also showed that three apparent positive findings in CT scans were artifacts. Lampert and hard mar^^^ described in detail the morphologic
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changes in brains of boxers that had been reported by others between 1928 and 1973 including subdural hemorrhages, intracerebral hemorrhages, diffuse axonal injury, cerebral edema, ischemia and herniation, cerebral atrophy, enlarged ventricles and septum cavum, cerebellar changes, loss of nerve cells in the substantia nigra, and neurofiburllary tangles. They did not report any new cases. Ross and c o - w ~ r k e r sexamined ~~ 38 former boxers and 2 current boxers with neurologic examinations (24), EEGs (24), CT scans (38), and a questionnaire concerning performance and medical history. Seven of the 24 EEG results were positive. Of the 11 boxers who had fewer than 50 bouts, 2 (18%)were positive; of 6 with 50 to 100 bouts, 4 (57%)were positive; and of the 7 with more than 100 bouts, 4 (57%)were positive. Beaussart and Beaussart-Boulenge,’ who performed EEGs on 123 amateur boxers before and within 15 minutes after bouts, found no evidence of pathologic changes, even in those who had been knocked out. Also, they failed to find any correlation between EEG changes and the severity of postconcussion syndrome in 3100 cases of the latter. Evaluation of chronic brain damage by other means, including EEG examination, began with Sere1 and J a r o ~ They . ~ ~ studied 1582 boxers from 1957 to 1961 and compared their neurologic findings with those in 100 nonboxers. Signs of chronic encephalopathy occurred in 9% of the boxers compared with 4% of the controls. Isolated reports of former boxers, who had died and whose brains were examined postmortem, have been published. Brandenburg and Hallervorden* found changes characteristic of Alzheimer’s disease in a 51-year-old former middleweight champion who had boxed as an amateur for 10 years and had begun to show clinical signs and symptoms of encephalopathy at age 38 years. Grahmann and Ulelz found brain atrophy and neurofibrillary tangles with large lateral ventricles and a cavum septi pellucidi in a former amateur and professional boxer who died at 48 years old with clinical evidence of chronic encephalopathy. Neuberger and colleaguesz9found cerebral atrophy with considerable gliosis throughout the cerebral cortex in the brains of two former boxers with clinical chronic encephalopathy. Spillane40found septa1 abnormalities in air encephalograms of four of five boxers with symptoms of chronic encephalopathy. Mawdsley and FergusonZ7examined 10 former boxers and obtained a postmortem examination of the brain in 1. Lumbar air encephalography in the other 9 showed abnormal findings in 8-specifically, evidence of enlarged lateral ventricles, cavum septi pellucidi, and evidence of cerebral and cerebellar atrophy. The examined brain showed all of these. Only one had a significantly abnormal EEG, although all had historic or clinical evidence of chronic encephalopathy. Constantinides and Tissot7 examined the brain of a 58-year-old boxer who had been fighting from age 17 to 24 years old and died following a long history of chronic encephalopathy with occasional
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epileptic seizures. They found neurofibrillary damage throughout the brain, cerebral atrophy, and a cavum septi pellucidi. Brennan and O’Conno? reported two deaths and one permanent invalid among amateur boxers who were Air Force personnel between 1963 and 1966. Neuberger and associatesz9found senile plaques and miniature scars in the grey matter in a cerebral biopsy of the frontal lobe of a former boxer who had suffered 30 knockouts in his career. In the brain of another boxer, who had chronic encephalopathy and died at age 53 years, were enlarged ventricles as well as brain atrophy with miniature scars on the grey matter. The report of the Royal College of Physicians (London), Committee on the Medical Aspects of Boxing, was presented by R0berts.3~This was a study of a random sample of 16,781 men who had boxed professionally in the United Kingdom from 1929 to 1955. Of the 224 examined, 37 (17%) demonstrated chronic neurologic symptoms or findings based on neurologic, psychometric, or EEG tests. Of these, 13 demonstrated classic chronic encephalopathy, and 2 had frank dementia. Older age, number of bouts, and heavier weights were all associated positively with these changes. The most complete and elaborate study of the brains of deceased boxers was published by Corsellis and co-workers.* Brains of 15 former boxers (12 professional, 3 amateur) were collected over a 16-year period. Their lives were investigated retrospectively through relatives, friends, hospital records, and boxing journals. Their ring careers extended over the period from 1900 to 1940. Two were world champions at one time and six were national or regional champions. Ages at death ranged from 57 to 91 years. Two of the boxers died after ventricular hemorrhage, and in both, the leaves of the septum were torn and separated, possibly as the result of the hemorrhage, so that they were excluded from further analysis. There was a striking difference between the septa of the 11 boxers and those of 500 controls. All but one of the boxers had a cavum, and in 10 or 12 it was fenestrated. Only 28% of the controls had a cavum, and in only 3% of the 500 was it accompanied by fenestration. The average width of the cavum in the boxers was three times that in the nonboxers. Five of the 15 nonboxers with a cavum and fenestration had firm clinical or other pathologic evidence of past head injury. Examination of the cerebellum showed cortical scarring on the inferior surface of the lateral lobes and significant losses of Purkinje’s cells on the ventral surface. These findings would be consistent with the cerebellum having been forced into the foramen magnum by the shock of impact. These findings are similar to those of Unterharn~cheidt?~ in cats whose brains were damaged experimentally. Degeneration and loss of pigmented cells in the substantia nigra and the presence of many neurofibrillary tangles, both of which are common findings in parkinsonism, were also noted in most of these boxers’ brains. The historic and clinical findings in the boxers in this study appeared to confirm and reinforce the pathology noted in their brains. Four had other single head injuries, none of which appeared serious.
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Many had been alcohol drinkers at one time or another, and 10 were reported to have drunk to excess. Four had cerebrovascular disease resulting in hemiplegia, and one had been treated successfully for tabes dorsalis. None of these conditions could have been responsible for the findings in their brains. Most had memory defects beginning, for the most part, early in life. For all but three, their memory disorders merged imperceptibly into a state of dementia. Some of the men remained addicted to violence long after they had stopped boxing. Cruikshank and colleagues9reported the cases of two young boxers who suffered acute intracranial hemorrhage not identified until 2 weeks later in one case and 2 months later in the other. The first had a hematoma occupying the left lateral ventricle, the head of the caudate nucleus, and the splenium of the corpus callosum. After a surgical evacuation of the hematoma, he made a good recovery. The second had a right parieto-occipital subdural hematoma that was excavated through burr holes with a complete recovery. In noncontrast CT scans of 10 boxers, performed within 1 week of their being knocked out, Casson and co-workers5found 5 normals. The others showed cerebral atrophy, and 1 a cavum septi pellucidi. They ranged in age from 18 to 22 years, and only 1had a minimally abnormal EEG. Four had 20 or more professional bouts. observed abnormal CT scans in 6 of 10 young Sironi and (18- to 24-year-old range) professional boxers. Four showed enlargements of the convexity of the central sulci, and 2 showed widening of the lateral and third ventricles. These were boxers who had been knocked out more than twice. Oleman and reviewed the reports of all personnel of the Army of the United Kingdom admitted to hospitals of the Royal Army Medical Corps during the years 1969 to 1980 and those who died or were medically discharged between 1952 and 1980. There were 437 admissions for boxing injuries, of which 296 (67.7%)were head injuries. Of these, 115 (39%) were for concussions and 69 (23%) for “intracranial injury of other and unspecified nature.” There were two cases (0.68%) of cerebral laceration and contusion, of which one resulted in a medical discharge. There were no deaths during this period. The only estimate of the population at risk is based on a random sample of 3185 Army personnel made in 1962 that found 113 engaged in boxing for an average of 4.9 hours per month each. If these ratios remained constant from 1969 to 1980, there would have been about 5700 men, each spending about 59 hours a year boxing. With an average of 35 injuries a year serious enough for hospital admission, 150 boxers would have been admitted per year, or one serious injury for every 9000 man hours of boxing. Among the 38 former boxers examined by Ross and colleagues36 who had CT scans, 24 also had a complete neurologic examination. Based on evaluation of the CT scans graded on a scale of 0 to 4 for evidence of cerebral atrophy and ventricular enlargement, there was a significant relationship between the numbers of bouts fought and the composite CT score, but this was due more to the presence of ventricular
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enlargement than to evidence of gyral atrophy. This was particularly striking because 25 had fewer than 100 bouts and only 5 had more than 150. The standard neurologic examination was of little value in detecting chronic cerebral damage because only 25% of the boxers showed positive findings. No psychometric tests were administered. It is difficult to evaluate the results of Rodriguez and associates35 who found regional cerebral blood flow to be significantly below normal in seven professional boxers. This finding would have to be correlated with EEG recordings, CT scans, and possibly postmortem brain examinations to determine how it might relate to boxing injury. SUMMARY AND CONCLUSIONS
A review of the available records indicates that there have been a substantial number of fatalities in primarily professional but also amateur boxers due to intracranial injuries sustained in the ring in comparison to the numbers of boxers at risk. The number of such fatalities has decreased steadily in recent years owing to different measures taken by boxing authorities to decrease the physical hazards in the ring and to improve monitoring of boxers during bouts by referees and physicians. The considerable concern about the long-term effects of repeated brain injury as the result of boxing in producing chronic encephalopathy is adequately justified by the many studies of live boxers and pathologic examinations of brains of former boxers made and recorded over the years since 1952. These indicate clearly a significant relationship between the numbers of bouts fought and the presence and severity of chronic encephalopathy. References 1. Beaussart M, Beaussart-Boulenge L Experimental study of cerebral concussions in 123 amateur boxers by clinical examination and EEG, before and immediately after fights. Electroencephalogr Clin Neurophysiol 29:529-530, 1970 2. Brandenburg W, Hallervorden J: Dementia1 Pugilistica mit anatenischem Befund. Virchows Arch Pathol Quatomil Physiol Klin Med 325:680-709, 1954 3. Brennan TN, OConnor PJ: Incidence of boxing injuries in the Royal Air Force in the United Kingdom 1953-66. Br J Ind Med 25:326-329, 1968 4. Busse EW, Silverman AJ: Electroencephalographic changes in professional boxers. JAMA 149:1522-1525, 1952 5. Casson IR, Sham R, Campbell EA, et al: Neurological and CT evaluation of knockedout boxers. J Neurol Neurosurg Psychiatry 453170-174, 1982 6 . Casson IR, Siege1 0, Sham R, et al: Brain damage in modem boxers. JAMA 25126632667, 1984 7. Constantinides J, Tissot R Lesions neurofibrillaires d’Alzheimer generalisees sans plaques seviles. Arch Suisses Neurol Neurochir Psychiatry 100:117-130, 1967 8. Corsellis JAN, Brutan CJ, Freeman-Browne D: The aftermath of boxing. Psycho1 Med 3270-303, 1973 9. Cruikshank JK, Higgens CS, Gray J R Two cases of intracranial hemorrhage in young amateur boxers. Lancet 1:626-627, 1980
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10. Denny Brown D, Russell WR Experimental cerebral concussion. Brain 64:7-163, 1941 11. Govons SR Brain concussion and p o s t u r e t h e knockdown blow of the boxing ring. Confinia Neurologica 30:77-84, 1968 12. Grahmann H, Ule G: Bietrag zur Genntuis der cluarischen cerebralen krankskeit Bilder bei boxem. Psychiatr Neurol 134:261-283, 1957 13. Gronwall D, Wrightson P: Delayed recovery of intellectual function after minor head injury. Lancet 2605-609, 1974 14. Gronwall E, Wrightson P: Cumulative effect of concussion. Lancet 2995, 1975 15. Gurdjian ES, Webster JE: Linear acceleration causing shear in the brain stem in trauma of the central nervous system. Mental Advances in Disease 2498, 1945 16. Holbourn AHS Mechanics of head injuries. Lancet 2438, 1943 17. Jedlinski J, Gatarski J, Szymusik A: Encephalopatha pugilistica (punch drunkedness). Acta Med Pol 12:443, 1971 18. Johnson J: Organic psychosyndromes due to boxing. Br J Psychiatry 115:4553, 1969 19. Jordan BD, Campbell EA: Acute boxing injuries among professional boxers in New York State: A two-year survey. In the 32nd Annual Meeting of the American College of Sports Medicine May 26-29, 1985 20. Jordan BD, Zimmerman RD: Magnetic resonance imaging in amateur boxers. Arch Neurol45:1207-1208, 1988 21. Jordan BD, Zimmerman RD: Computed tomography and magnetic resonance imaging comparisons in boxers. JAMA 263:1670-1674, 1990 22. Kaplan HA, Browder J: Observations on the clinical and brain wave patterns of professional boxers. JAMA 156:1138-1144, 1954 23. Kaste M, Vilkki J, Sainio K, et al: Is chronic brain damage in boxing a hazard of the past? Lancet 21186-1188,1982 24. Lampert PW, Hardman JM: Morphological changes in brains of boxers. JAMA 251:267&2679, 1984 25. Levin HS, Lippold SC, Goldman A, et a1 Neurobehavioral functioning and magnetic resonance imaging findings in young boxers. J Neurosurg 67657-667, 1987 26. Martland HS: Punch drunk. JAMA 91:1103-1107, 1928 27. Mawdsley C, Ferguson FR Neurological disease in boxers. Lancet 2795-801, 1983 28. Moore M: The challenge of boxing: Bringing safety into the ring. The Physician and Sports Medicine 8:lOl-105, 1980 29. Neuberger KT, Sintar DW, Denst J: Cerebral atrophy associated with boxing. Arch Neurol Psychiatry 81:403408, 1959 30. Oleman BJ, Rose CME, Arlow KJ: Boxing injuries in the Army. Journal of the Royal Army Medical Corps 129:22-27, 1983 31. Pudenz RH, Sheldon CH: The lucite calvarium: A method for direct observation of the brain. J Neurosurg 3:487-505, 1946 32. Putnam P: Going-Going-Gone. Sports Illustrated June 6: 23-46, 1983 33. Rime1 RW, Giordani B, Barth JT, et al: Disability caused by minor head injury. Neurosurgery 9221-228, 1981 34. Roberts A H Brain damage in boxers. London, Pitman Medical Science Publications, 1969 35. Rodriguez G, Ferrillo F, Montano V, et a1 Regional cerebral blood flow in boxers. Lancet 2858, 1983 36. Ross RJ, Cole C, Thompson JS, et al: Boxers-computed tomography, EEG, and neurological evaluation. JAMA 249:211-214, 1983 37. Ryan AJ: Personal observations from 50 years of following boxing and collecting factual information from media sources. 38. Sere1 M, Jaros 0 The mechanisms of cerebral concussion in boxing and their consequences. World Neurol3:351-358, 1962 39. Sironi VA, Scotti G, Ravagnati L, et al: CT scan and EEG findings in professional pugilists: Early detection of cerebral atrophy in young boxers. J Neurosurg Sci 26:165168, 1982 40. Spillane JD: Five boxers. BMJ 21205-1210, 1962 41. Strich SJ: Shearing of nerve fibers as a cause of brain damage due to head injury. Lancet 2443448,1961
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42. Thomassen A, Juul-Jensen P, Olivarius B, et al: Neurological electroencephalographic and neuropsychological examination of 53 former amateur boxers. Acta Neurol Scand 60~352-362,1979 43. Unterharnscheidt FJ: Injuries due to boxing and other sports. In Viuken PJ, Bruyra GW (eds): Handbook of Clinical Neurology, vol 23. Amsterdam, North-Holland, 1975, pp 527-593
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