Posttraumatic Retrograde and Anterograde Amnesia: Pathophysiology and Implications in Grading and Safe Return to Play

Abstract

Objective:

The presence of posttraumatic amnesia (PTA) and loss of consciousness have been main factors used in a number of concussion guidelines. In this article, the focus is on using PTA (both retrograde and anterograde) as salient indicators of traumatic brain injury severity and the most reliable index of outcome prediction, even in mild cases.

Data Sources:

A MEDLINE search for the years 1990–2000 using the key words posttraumatic retrograde and anterograde amnesia, concussion and mild traumatic brain injury was done.

Data Synthesis:

On-the-field testing of PTA is a salient and integral component of the initial and follow-up neurologic assessments of the head-injured athlete.

Conclusions/Recommendations:

Initial and follow-up assessments of PTA, anterograde and retrograde, are an essential part of the neurologic evaluation of the head-injured athlete. Increasingly, neuropsychological testing, including computer models, is being employed in this assessment. The importance of not just PTA but all postconcussion signs and symptoms being absent at rest and exertion before allowing the athlete to return to play is emphasized.

Concussion is derived from the Latin word concussus, which means to shake violently. Initially, it was thought to produce only a temporary disturbance of brain function due to neuronal, chemical, or neuroelectrical changes without gross structural change. We now know that structural damage with loss of brain cells does occur with some concussions. In the last several years, the neurobiology of cerebral concussion has been advanced predominantly in animal studies but also in studies in man as well. It has become clear that, in the minutes to days after concussive brain injury, brain cells that are not irreversibly destroyed remain alive but in a vulnerable state. These cells are particularly vulnerable to minor changes in cerebral blood flow, increases in intracranial pressure, and especially anoxia. Animal studies have shown that, during this period of vulnerability, which may last as long as a week with a minor head injury such as a concussion, a minor reduction in cerebral blood flow that would normally be well tolerated now produces extensive neuronal cell loss.^1–5 This vulnerability appears to be due to an uncoupling of the demand for glucose, which is increased after injury, with a relative reduction in cerebral blood flow. While the precise mechanisms of this dysfunction are still not fully understood, it is now clear that, although concussion in and of itself may not produce extensive neuronal damage, the surviving cells are in a state of vulnerability characterized by a metabolic dysfunction, which can be thought of as a breakdown between energy demand and production. Precisely how long this period of metabolic dysfunction lasts is not presently fully understood. Unfortunately, there are today no neuroanatomic or physiologic measurements that can be used to precisely determine the extent of injury in concussion or the severity of metabolic dysfunction or precisely when it has cleared. It is this fact that makes return-to-play decisions after a concussion a clinical judgment.

Team physicians, athletic trainers, and other medical personnel responsible for the medical care of athletes face no more challenging problem than the recognition and management of concussion. Indeed, such injuries have captured many headlines in recent years and have spurred studies within both the National Football League and the National Hockey League.

When discussing concussion, we must realize that there is no universal agreement on the definition and grading of concussion.^1,6–8 Tables 1–8 present different attempts at grading concussion, all focusing on loss or nonloss of consciousness and posttraumatic amnesia (PTA) as hallmarks in the grading schemes. Furthermore, they may not give enough attention to the other signs and symptoms of concussion. As we all know, a patient with concussion may display any combination of the following signs and symptoms: a feeling of being stunned or seeing bright lights, brief loss of consciousness, lightheadedness, vertigo, loss of balance, headaches, cognitive and memory dysfunction, tinnitus, blurred vision, difficulty concentrating, lethargy, fatigue, personality changes, inability to perform daily activities, sleep disturbances, and motor or sensory symptoms.

Table 1.

Cantu Grading System for Concussion⁹*

Table 8.

Torg Grading System for Concussion¹³

Table 2.

Colorado Medical Society Grading System for Concussion¹⁰

Table 3.

AAN Practice Parameter (Kelly and Rosenberg) Grading System for Concussion⁶

Table 4.

Jordan Grading System for Concussion¹¹

Table 5.

Ommaya Grading System for Concussion¹²

Table 6.

Nelson Grading System for Concussion⁷

Table 7.

Roberts Grading System for Concussion⁸

Presently, there is no universal agreement that PTA is a better or more sensitive predictor of outcome after traumatic brain injury than depth and duration of unconsciousness,^14–16 but many consider the duration of PTA the best indicator of traumatic brain injury severity^15,17 and the most dependable marker of outcome prediction,^18–25 even in mild cases.^16,26 While variously described by different investigators, PTA includes impaired orientation, that is, retrograde amnesia and anterograde amnesia.^22,27–29 Recently, some investigators^16,30–32 have suggested that PTA might better be called posttraumatic confusional state.

Posttraumatic amnesia may be divided into 2 types. The first type of PTA is retrograde, defined by Cartlidge and Shaw²³ as a “partial or total loss of the ability to recall events that have occurred during the period immediately preceding brain injury.” The duration of retrograde amnesia usually progressively decreases. The second type of PTA is anterograde amnesia, a deficit in forming new memory after the accident, which may lead to decreased attention and inaccurate perception. Anterograde memory is frequently the last function to return after the recovery from loss of consciousness.³³

Memory and new learning are believed to involve the cerebral cortex, subcortical projections, hippocampal formation (gyrus dentatus, hippocampus, and parahippocampal gyri), and the diencephalons, especially the medial portions of the dorsomedial and adjacent midline nuclei of the thalamus.³⁴ In addition, frontal lobe lesions may cause alterations in behavior, including irritability, aggressiveness, and loss of inhibition and judgment. Recently, evidence has been presented that the right frontal lobe plays a prominent role in sustained attention.³⁵

The lack of a universal definition or grading scheme for concussion renders the evaluation of epidemiologic data extremely difficult. As a neurosurgeon and team physician, I have evaluated many football players who suffered a concussion. Most of these injuries were mild, not involving loss of consciousness, and were associated with PTA, which was helpful in making the diagnosis, especially in mild cases.

I developed a practical scheme for grading concussion severity based on the duration of unconsciousness or PTA (or both), which has worked well on the field and sideline (see Table 1). The most mild concussion (grade 1) occurs without loss of consciousness, and the only neurologic deficit is a brief period of posttraumatic confusion or PTA, which, by definition, lasts less than 30 minutes. The moderate (grade 2) concussion is usually associated with a brief period of unconsciousness, by definition, not exceeding 5 minutes. Less commonly, consciousness is not lost; the athlete instead experiences a protracted period of PTA lasting more than 30 minutes but less than 24 hours. A severe (grade 3) concussion occurs with a more protracted period of unconsciousness lasting longer than 5 minutes. Rarely, it may occur without a loss of consciousness or with a shorter period of unconsciousness but with a very protracted period of PTA lasting more than 24 hours. In reality, prospective studies over the last several years have shown that virtually all concussions are grade 3 by this guideline because of PTA lasting longer than 24 hours (D. Erlanger, unpublished data, 2000). A protracted period of unconsciousness lasting more than 5 minutes is almost never seen on athletic fields; most periods of unconsciousness last seconds to a minute. Prospective studies over the last 10 years have demonstrated a correlation between the duration of postconcussive symptoms and PTA and abnormal results on neuropsychological tests. Therefore, I present an evidence-based modification of the original Cantu guidelines⁹ (Table 9).

Table 9.

Evidence-Based Cantu Grading System for Concussion

When checking for orientation and retrograde amnesia on the field, asking the athlete the current quarter, the score, what happened, and the names of the current and last week's opponents is useful. When checking for attention or anterograde amnesia deficits, useful tests are repeating 4 words immediately and 2 minutes later, repeating 5 numbers forward and especially backward, and repeating months of the year backward.

Recently, computer-administered minineuropsychological tests have been proposed as a more feasible way to conduct group baseline assessments,^36,37 as well as a personal digital assistant version that can be connected to the Internet.^38,39

Thus, while not yet the standard of care, neuropsychological tests (with a preseason baseline and serial postconcussion assessments) are assisting clinicians in concussion management, including return-to-play decisions.

Whether an athlete has been unconscious is, of course, important. It is generally believed that the degree of brain injury sustained is indicated by the depth and duration of coma.^40–42 However, the coma referred to by these authors is not the seconds to minutes usually seen on the athletic field but rather hours' or days' duration. Thus, while not diminishing the importance of being rendered unconscious, I find it illogical to grade a concussion that produces postconcussion symptoms lasting months or years without loss of consciousness as less severe than a concussion resulting in brief unconsciousness and resolution of all postconcussion symptoms within a few minutes or hours. Brett Lindros, Al Toon, Jim Miller, Steve Young, and Merrill Hodge are professional athletes whose careers were ended by concussions without loss of consciousness that produced sustained postconcussion symptoms. We know these athletes consider their concussions very severe.

RETURN TO COMPETITION AFTER CONCUSSION

A sobering realization is that the ability to process information may be reduced after a concussion, and the severity and duration of functional impairment may be greater with repeated concussions.^43–45 Studies clearly suggest that the damaging effects of the shearing injury to nerve fibers and neurons are proportional to the degree to which the head is accelerated and that these changes may be cumulative.^46–48 Once a player has incurred an initial cerebral concussion, his or her chances of incurring a second one are 3 to 6 times greater than for an athlete who has never sustained a concussion.^48–51

Table 10 presents guidelines for return to play after a concussion, including termination of a season. Before an athlete returns to play, he or she must not only be free of PTA symptoms but also of all postconcussion symptoms at rest and exertion. All the guidelines agree on this salient point. Table 11 is a postconcussion signs and symptoms checklist I have found useful. Thus, while it is a clinical decision as to when to return an athlete to play after a concussion, to return an athlete with postconcussion symptoms risks not only cumulative brain injury but the second-impact syndrome and would be against the recommendations of all current guidelines.

Table 10.

Guidelines for Return to Play After Concussion*

Table 11.

Postconcussion Signs and Symptoms Checklist

CONCLUSION

There is no universal agreement on concussion grading and return-to-play criteria after a concussion. There is, however, unanimous agreement that an athlete still suffering postconcussion symptoms at rest and exertion should not return to contact or collision sports. In this article, I present the logic for using the duration of posttraumatic amnesia (retrograde and especially anterograde) as a criterion to be employed in the grading of concussion severity.