Assessment of recovery serious injury

Journal ofNeurology, Neurosurgery, and Psychiatry, 1978, 41, 1036-1042

Assessment of recovery from serious head injuryMORRIS E. ESON, JOHN K. YEN, AND ROBERT S. BOURKE

From the State University of New York at Albany, and Division of Neurosurgery,Albany Medical College, Albany, New York, USA

SUMMARY A procedure for serial assessment of neuropsychological recovery after serioushead injury was designed. The assessment procedure consists of four segments, each appropriatefor different phases of the recovery process. Recovery can be traced from early in the periodof post-traumatic amnesia until it reaches an asymptote. The course of recovery of severalpatients has been observed. The procedure is shown to be practical and appears to be valid.The recovery process is compared to ontogenesis, and is shown to be generally similar thoughdiffering in important particulars.

Improved life support technology and patientmanagement have resulted in the survival of everincreasing numbers of seriously head-injuredpatients (Bond and Brooks, 1976; Jennett et al.,1976). The quality of neuropsychological recoveryin patients is highly variable, and the factorsaccounting for the differences in rate, pattern, andultimate level of recovery are largely unknown.Systematic study of the process of recovery mayprovide a basis for more effective treatmentregimes.The usual neuropsychological assessment pro-

cedures are of limited applicability for the evalu-ation of the recently head-injured patient. Thewidely used battery of tests developed by Halsteadand Reitan (Reitan and Davison, 1974), and itsmodification by Russell et al. (1970), are designedfor administration to alert patients with relativelyfixed focal deficits. The Halstead ImpairmentIndex is useful for gross diagnostic determinationsof locus and extent of brain lesions. Luria's pro-cedure (Christenson, 1975; Luria and Majovski,1977), although broader in its scope, is also aimedat a determination of the behavioural consequencesof a static deficit. These assessment procedures arenot designed to study the evolving improvementof function in the patient with altered levels ofalertness and attention span. Moreover, the admin-istration of these test batteries takes several hours,making them impractical for serial testing to

Address for reprint requests: Dr Morris E. Eson, Department ofPsychology, State University ofNew York at Albany, 1400WashingtonAvenue, Albany, New York 12222, USA.Accepted 27 June71978

evaluate time-related improvement. Most patientswith acceleration/deceleration head injuries sufferfocal, scattered histopathological lesions withgeneralised neurological dysfunction rather thanfocal single anatomical lesions with solitary neuro-logical deficits (Graham and Adams, 1971).

Neuropsychological studies of severely head-injured patients that have employed longitudinalor serial assessments have measured changes inspecific functions, such as memory (Brooks,1974a, b, 1975, 1976; Levin et al., 1976; Hannayet al., 1977) or selective attention and choicereaction time (Gronwall and Sampson, 1974).Studies of the recovery of intellectual function ingeneral are remarkably few. One of these earlierstudies (Ruesch and Moore, 1943) demonstratedthat the duration of coma after injury was pre-dictive of the rate and quality of recovery ofintellectual function. Recently Mandleberg andBrooks (1975) traced the natural course of recoveryof intellectual function after severe head injuryby serial administration of the Wechsler AdultIntelligence Scale. They found that functionstested by the verbal subtests demonstrated lessinitial impairment and faster recovery than thosefunctions tested by the non-verbal subtests. Inaddition, Mandleberg (1975) compared WechslerScale test scores of head-injured patients exhibitingclinical signs of post-traumatic amnesia with thosewho had recovered beyond that point. He con-cluded that the period of post-traumatic amnesiawas a qualitatively distinct phase of recovery inhead injury. Although these kinds of assessmentsdemonstrate a pattern in recovery from severe

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Assessment of recovery from serious head injury

head injury, they do not focus on generalisedassessment of adaptive function.The level of adaptive function varies with the

stages of recovery from serious head injury. In theearly stages, it is manifested in the ability to carryon the activities of daily living, self-care, andrudimentary social interaction. In the middlestages recovery of adaptive function is bestmeasured indirectly by assessment of conceptualand information processing skills that underliemore mature social interaction and ability toinitiate and carry out sustained planned activitiesdirected toward a goal. Complete or nearly com-plete recovery of adaptive function is shown whenthe individual is able to seek and maintain employ-ment, and is able to participate in normal adultsocial and recreational activities without super-vision. This latter level we refer to as basic adaptivefunction. The relationship of the performance ona single intelligence scale such as the Wechslerand the level of adaptive function at various stagesof recovery in the recently head-injured has notbeen established. Furthermore, any particular testof cognitive function, such as the Wechsler AdultScale, is designed for restricted ranges of cognitivefunction in the alert subject and is not suitablefor assessment of levels of function that deviatemarkedly from these ranges, particularly inpatients with altered levels of consciousness andrestricted attention span. In attempting to under-stand the various phases of cognitive and adaptivefunction throughout the course of recovery itwould be desirable to use tests designed specificallyfor the assessment of the patient during each phaseof neuropsychological recovery (Luria andMajovski, 1977). Those studies that have beenconcerned with the recovery of adaptive functionafter serious head injury (Bond, 1975; Bond andBrooks, 1976; Najenson et al., 1973, 1974, 1975)were aimed at the evaluation of patient status interms of social and vocational adjustment sixmonths to five years after injury. The process ofrecovery of adaptive function from shortly afterinjury was not investigated.The scale we have designed is modelled on a

developmental scale, with test instruments appro-priate for each level of the recovery process. Thefirst segment of the scale assesses the recovery

during the period of post-traumatic amnesia, a

period for which no assessment procedures are

currently available. The four segments of the scaleare linked to each other as measures of the re-covery of adaptive function paralleling that ofontogenesis. Recovery since time of injury isplotted against months equivalent in developmentfrom zero to 200 months. The scale has general

applicability as long as the premorbid socialhistory reveals at least functional literacy, deter-mined by educational and occupational data. Sincethe assessment procedure concerns itself with therecovery of basic adaptive functions, it becomesunnecessary to ascertain the extent to which theparticular patient's premorbid function may havesurpassed this basic level.

Methods

The scale is designed to be used from the timethe patient recovers from the coma and sequen-tially to the time at which full recovery isdemonstrated (basic adaptive function present inpremorbid state) or until the patient's functionfails to show improvement over a period of two tothree months. The items are arranged accordingto a developmental sequence such that the demon-stration of the presence of a more advanced func-tion can be taken as evidence for the presence ofa less advanced one. The early segments of thisscale allow for the use of the impressions of thenursing staff looking after the patient. The scaleis constructed in such a way that observation ortest items are seldom repeated as long as thepatient shows improvement, thus avoiding practiceeffects, and allowing for the completion of eachevaluation session in 40 minutes or less (with theexception of the last segment which takes aboutone hour).The scale, covering the equivalent of the onto-

genetic span of 16 years-8 months, consists of foursegments each designed to test for the developmentof adaptive function during each of four sequentialperiods of four years. In ontogenesis the earlierdevelopmental achievements are generally con-sidered more fundamental for future adaptation,and are given more weight than later ones. In casesof adult patients the recovery process seems todepend equally on the reacquisition of the funda-mental adaptive functions of each period, con-sequently the chronological equivalents in thegrowth of adaptive function are weighted equallythrough all parts of the scale. The scale emphasisescognitive or intellectual function but takes intoaccount social and motivational components ofdevelopment as well.

SEGMENT 1: 0-4 YEARSThis segment consists of 97 items adapted fromvarious infant scales, such as the Bayley (1969)Scales of Infant Development, the Boyd (1974)Developmental Progress Scale, and the VinelandSocial Maturity Scale (Doll, 1953). About 1500items from various infant scales were placed on

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cards. Two neurosurgeons and a psychologistrated these items as appropriate or inappropriatein assessing recovery. The 97 items that wererated as appropriate by all three raters wereselected for the scale. These items were arrangedin the order in which they appear chronologicallyin the infant scales. They appear to represent anadequate sample of the adaptive functions acquiredin the first four years of life and to represent re-covery through the end of the period of post-traumatic amnesia.The examiner starts the examination with an

item that appears to be within the patient's ca-pacity, then continues with the easier items untilthe patient shows four successive passes. Theexamination proceeds with the more advanceditems until there are four successive failures. Itcan be assumed that the items below the foursuccesses and above four failures would all bepassed or failed respectively.

SEGMENT 2: 4-8 YEARSThis segment consists of 20 items selected fromthe Stanford-Binet Intelligence Scale (Terman andMerrill, 1973) from age levels 4-9 years inclusive.The Binet test, even as originally conceived, wasdesigned to determine readiness for school learn-ing. Our selection of the Stanford-Binet items fromthis age period was guided by the widely acceptedassumption that they represent the basic con-ceptual requirements for achieving the more com-plex adaptive skills. The emphasis in these itemsis on cognitive skills basic to adaptive function.The items test for the following abilities: makingdistinctions (noting differences); abstracting (notingsimilarities); following instructions; organisingsimple perceptual arrays.We have chosen items from the Stanford-Binet

rather than from other intelligence scales because,as Lezak (1976) points out, "individual Binet sub-tests fit well into larger test batteries constructedfor specific research purposes and for the indi-vidual patient." Furthermore, we considered itappropriate to assess these particular cognitivefunctions in studying the recovery of patients withclosed head injuries since they represent the kindsof functions not directly associated with localisedcortical sites but those that seem sensitive togeneralised brain injury (Yacorzinski, 1965).

SEGMENT 3: 8-12 YEARSThe three separate tests for this segment wereselected because they show developmental improve-ment in basic information processing skills, andbecause they provided the opportunity to testwhether or not the recovery process is differenti-ated with respect to type of injury.

Trail Making TestThe first part of the test requires the patient todraw lines in sequence from numbers 1 to 25arranged randomly over an 81 by 11 inch page.The second part of the test requires the patient todraw lines in alternating series consisting of 13numbers and 12 letters. Score is the time to com-plete each part.

This test is taken from the Manual for the USArmy Individual Test and has been used byReitan (1958) as a test for the determination andlocalisation of brain damage. When used as adiagnostic measure in this way it produces toomany false negative and false positive identifi-cations (14 and 17% respectively). However, whenwe analyse what is involved in the performance ofthis task and adopt a developmental view, theTrail Making Test can provide some interestingand useful information about the patient'srecovery.

In performing any task requiring the serialorganisation of behaviour, each of the patient'sresponses has to be determined by the use of in-formation derived from the previous responses.Warrington (1970) cites a study by Stevensonwhich showed that patients with unilateral frontallobe lesions performed significantly more poorlyon sequentially ordered tasks than those withlesions in other regions of the cortex. Right andleft frontal lobe patients were similarly impaired.We have developed age norms for the Trail

Making Test on a sample of 174 subjects rangingin age from 7 to 17 years. These norms are avail-able on request. The test can thus be used to makea developmental assessment of recovery. Also bycomparing the recovery on this task with that ofthe other two tests used in this segment it becomespossible to determine whether recovery is generalor global or whether it is differentiated as to specificaspects of function.

Road Map Test of Direction SenseThe ability to differentiate right and left progressesthrough a developmental sequence (Swanson andBenton, 1955). First appears the ability to makethe right-left (R-L) discrimination of one's ownbody (complete by about age 7 years). The R-Ldiscrimination on a person facing the subject doesnot develop until about age 12 years. The Stan-dardised Road Map Test of Direction Sense(Money, 1965) evaluates the more complex skillin R-L orientation-namely, "that of orientingoneself toward right and left simultaneously withcoming and going in space and then projectingthis orientation onto a flat surface, as in followinga route on a map"(p. 16). The test requires the

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subject to identify the direction of 32 R-L turns ona street map.Benton (1959) asserts that the ability of right-left

orientation is dependent on language processes.The development of this orientation skill seemsto be related to the process of cerebral hemisphericlateralisation.We have included the Standardised Road Map

Test of Direction Sense in our test battery becauseit seems to be a reflection of the gradual develop-ment of hemispheric specialisation. By using theage norms provided in the manual, one is able toobtain a measure of the recovery of the abstractreferencing function of language symbols.

Stroop Color-Word TestAlthough there are many forms of this test measur-ing the effects of perceptual interference, we haveadopted the form proposed by Comalli et al. (1962)because they have provided age norms. We havesupplemented their norms by testing a sample of174 subjects ranging in age from 7 to 17 years.Our results are remarkably close to those obtainedby Comalli et al. Age norms for this form of theColor-Word test are available on request.The test consists of three cards (24X24 cm).

Card 1 consists of 100 colour words (red, blue, andgreen) which the subject reads. Card 2 has 100small colour rectangles (red, blue, and green)which the subject names. Card 3 consists of 100colour words but these words are printed in ink,the actual colour of which conflicts with thatdesignated by the printed word. Thus, the wordred is printed in blue or green ink but not in redink. The subject must name the colour of theink and ignore the printed colour word. Score isthe amount of time for each card.

In order to perform well on card 3 the subjectis required to inhibit word reading and to keep itsubordinate to the more deliberate process ofcolour naming. This task represents the kind ofcomplex adjustment necessary in paying selectiveattention to the environment and in maintainingan inhibitory state with respect to one responsetendency-namely, reading-while at the sametime proceeding actively in making a contradictoryresponse-namely, colour naming. Development-ally, this skill, which involves selective inhibitionand activation, seems to depend on the generalstate of superordination of higher cortical centresover the subcortical centres. The test thus seemsappropriate to measure the reacquisition of thissuperordination in the recovery from serious headinjury.The three tests in this segment, Trail Making,

Direction Sense, and Stroop Color-Word Test,

can be used to determine whether the pattern ofrecovery is generalised or whether different typesof injury lead to differentiated patterns of recoveryfor different functions.

SEGMENT 4: FINAL STAGES OF MATURE ADAPTIVEFUNCTIONFor this segment we have selected a test that usesvarious concepts, skills, and information process-ing in a co-ordinated way to carry out everydayactivities. This test is the REAL (Reading/Every-day Activities in Life) developed by Lichtman(1972). The test consists of nine subparts, such asidentifying road signs by their function, reading atelevision programme matrix, reading the want-adsection of a newspaper, and so on. The test pro-vides norms that differentiate the functionallyilliterate, marginal, and functionally literate. In-structions are given on a cassette tape, and afterinitial instruction the test is self-administered andself-paced.

Further details on the several tests of the batteryused for the Developmental Assessment of Re-covery from Serious Head Injury (DARSHI), andinstructions for administering and scoring, areavailable on request.

Application of assessment procedure

A number of patients with closed head injuryhave been evaluated sequentially using the varioussegments of our assessment procedure. We havefound that the procedure is practical and appearsto be valid. A few patients have been examinedseven or eight times during the first 60 to 90 daysof recovery and once or twice several months afterdischarge. A summary of one such patient'srecovery is presented.A 20 year old man (MP) sustained a head injury

in a car accident. On admission, neurologicalexamination showed that there was no response toverbal command but there was appropriate with-drawal of all extremities to painful stimuli. Inaddition, there was a mild but definite left hemi-paresis including the face. The right pupil waslarger than the left but both responded to light.Oculocephalic reflexes were intact; these was atendency for adversive gaze to the right. Afteradmission to hospital he underwent elevation anddebridement of his skull fracture. At the time ofsurgery cerebral contusion was noted. The dayafter admission, mild left sided decerebrate postur-ing was noted, and the patient underwent a repeatCAT scan which showed diffuse swelling with noevidence of haematoma. Six days after injury hemoved his right extremities appropriately to verbal

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command, but a marked left hemiparesis, armgreater than leg, persisted. Eight days after injuryhe was following command but marked left hemi-paresis persisted. Ten days after injury he wasresponding well to command, and improvement ofhis left hemiparesis was seen. Seventeen days afterinjury the patient was able to say single words,and was noted to be more alert. In addition, slowbut definite improvement of his left hemiparesiswas noted. Thirty-seven days after injury therewas steady improvement in his level of conscious-ness, speech, and left hemiparesis. The patient wasdischarged 67 days after injury. He was noted tobe mildly ataxic but he was able to walk withoutassistance.On the first neuropsychological assessment, 17

days after injury, the patient's level of functionwas at the 12 month equivalent. Ten days laterhis performance improved to the 4 year level. Onday 27 after injury he was started on programmesof physical, occupational, and speech therapy, andat day 39 his performance on the Binet segmentof the test battery placed him at an age equivalentof 94 months. One day later he was tested on twoof the three tests of the third segment of thebattery. On the Trail Making test his score wasequivalent to the 8 year level, and on the test ofdirectional sense his performance was at the 13

ISO`| 180

S 160

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8 80

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RECOVERY CURVE

0 20 40 60 80DAYS SINCE INJURY

Figure Level of recovery in relation to days sinceinjury in patient MP.

year level. He was assigned a combined score of10 years. His Color-Word scores at 50 and 52days were at the 7 and 9 year levels respectively,while his score on the Directional Sense Test re-mained at age 13 years. At 60 days, a few daysbefore discharge, his scores on all three tests hadregressed somewhat, 7 years on Trail Making andthe Color-Word test, and 8 years on the test ofDirectional Sense. On this last test he seemed tohave become confused half way through andcould not reorient himself.The patient was seen 11 months after his injury,

and was tested on the three tests of segmentthree. His scores ranged from 9 years on theStroop interference card to 15 years on the test ofDirectional Sense. His overall performance was atthe 13 year level. In addition, he showed someimmature personality characteristics such as un-controlled sporadic giggling. Although his pre-morbid functioning was judged to be marginal, weestimated it to be equivalent to the level we havetermed basic adaptive function. Thus his recoverywas still considerably short of that level. Thecourse of this patient's recovery from 17 days to11 months after injury is shown in the Figure.

Discussion

The changes in function as revealed by the se-quential assessment by our procedure suggest that

- the course of recovery generally parallels ontogeny.The early stages are marked by rapid improve-ment. This is followed by a period of deceleratingrate of improvement until the asymptote isreached. Newcombe et al. (1975) described asimilar course of recovery in several dyslexicpatients, and Knill-Jones (1975) suggests that theidealised recovery curve should follow this samepattern. However, ontogeny and recovery differin two particular respects. First, patients seem torecover context-free responses before they becomeable to apply these in context-dependent situations.Thus, patients can recite the days of the week insequence and tell what day comes before or aftera specified day before they demonstrate a firmorientation to the current flow of time; they canidentify right and left before they can consistentlyput their shoes on corresponding feet. Second, thefunctions necessary for performance on the latterhalf of segment 2 (items from the Stanford-Binet,testing for 7 to 8 year equivalence) seem to appearearlier than those necessary for performance atthe same age level on the three tests in segment 3-namely, Trail Making, Direction Sense, andColor-Word. Patients could complete all the itemsin segment 2 successfully, achieving an age

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equivalent of 8 years, while at the same timethey could not perform at the 7 year level on thethree tests of segment 3. This finding is consistentwith that reported by Gronwall and Sampson(1974) on a group of concussed patients. Theyfound that concussion after head injury wasassociated with lowered performance in informa-tion processing tasks. It is also consistent withthe findings of Mandleberg and Brooks (1975) thatthere is marked discrepancy between the verbaland performance subtests of the Wechsler AdultIntelligence Scale (19 IQ points in favourof the verbal). Our Binet items resemble theWechsler verbal subtests, and our information pro-cessing tests resemble the performance subtests.Some minor adjustments in the ordering of items

within segments and in the co-ordination of seg-ments 2 and 3 may be desirable ultimately in orderto make the scale conform more precisely to therecovery process observed. However, our findingsthus far indicate that the developmental parallel isgenerally valid in describing the neuropsychologicalrecovery process.The performance of the patients on the three

tests of segment 3 shows that the pattern of re-covery is differentiated. Improvement in per-formance on the three tests was as follows: theability to perform on Direction Sense recoversmost rapidly, the ability to perform on the TrailMaking test is slowest in recovery. This suggeststhat tasks requiring sequential ordering and visualscanning are most impaired in closed headinjury while the abstract referencing function oflanguage symbols and hemispheric specialisationis least impaired. Functions related to hemisphericspecialisation are earlier ontogenetically than thosedemanding serial organisation. This suggests thatthe recovery pattern follows the ontogeneticsequence.The recovery of the patients we have examined

by means of the developmental assessment showmarked individual differences both as to rate andfinal outcome. The findings indicate, however, thatin general the course of recovery of adaptivefunction is relatively rapid at its onset, after re-gaining consciousness, and then appears to slowdown markedly to reach an asymptote. Our find-ings suggest that the assertion of Jennett et al.(1976) that most of the recovery occurs in the firstsix months needs to be qualified. The study of theindividual course of recovery by means of develop-mental assessment suggests that in some casesmaximum recovery is achieved before six months,and in other cases recovery of adaptive functioncontinues beyond that point.The developmental approach to the assessment

of recovery of adaptive function after serious headinjury presented above permits objective assess-ment of recovery in early stages of post-traumaticamnesia, and unifies assessment during the earlystages of recovery with assessments made duringsubsequent periods of recovery. This approachpermits the analysis of neuropsychological re-covery as a continual process. This analysis ofrecovery provides more precise indices for pre-dicting eventual outcome. Developmental assess-ment makes it possible to correlate neurologicaland systemic clinical factors with neuropsycho-logical measures during the course of recovery. Adevelopmental approach to the study of recoveryprovides a more exact description of eventual out-comes than has been possible previously. Forexample, the Glasgow Coma Scale as developedby Jennett et al. (1976) classifies functional out-come into five broad categories: death, persistentvegetative state, severe disability, moderate dis-ability, and good recovery. These categories do notpermit immediate grasp of the qualitative func-tional level of survivors within each designation.A developmental test battery, such as presentedhere, permits a more precise description of out-come on a continuum, and allows for the deter-mination of the relationship between patterns ofrecovery and the duration of improvement inadaptive function. Developmental descriptions canbe useful in research investigations making com-parative evaluations of different courses of treat-ment and rehabilitation both in short-term andlong-term effects. Such developmental assessmentsmay also have practical value in legal determin-ations of damage and in vocational planning.

This project was supported by Grant No NS 13042from the National Institute of Neurological Com-municative Diseases and Stroke, National Institutesof Health. We express our gratitude to the follow-ing individuals who contributed to the investi-gation: Dr R. Ghiulamila, Dr A. J. Popp, P.Donahue, A. Van Deusen, D. Van Deusen, M.Booth, and Professor R. Pruzek.

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Assessment of recovery serious injury