CLINICAL AND RESEARCH REPORTS

Subtle Neurological Signs

Predict the Severity of
Subacute Cognitive and
Functional Impairments
After Traumatic Brain
Injury
Hal S. Wortzel, M.D.
Kimberly L. Frey, M.S.
C. Alan Anderson, M.D.
David B. Arciniegas, M.D.
The presence of paratonia and primitive reflexes
(frontal release signs), such as glabellar, snout,
suck, grasp, and palmomental responses, after
traumatic brain injury predicts performance on
bedside cognitive assessments, level of functional
independence, and duration of acute inpatient
rehabilitation.
(The Journal of Neuropsychiatry and Clinical
Neurosciences 2009; 21:463 466)

raumatic brain injury (TBI) is a common problem in

the United States, with an annual hospitalization
rate approaching 200 per 100,000 people.1 The inpatient
neurological and neurobehavioral evaluation of these
individuals usually includes at least an elementary neurological examination, a general mental status examination, and some type of bedside cognitive assessment.2
Our Behavioral Neurology & Neuropsychiatry consultation service, which serves an acute inpatient brain
injury rehabilitation unit, also routinely includes assessment for subtle neurological signs, including several
primitive reflexes and paratonia. In this context, multiple primitive reflexes and paratonia are elicited commonly, particularly among patients with marked posttraumatic cognitive impairment and functional
disability.
These observations prompted a retrospective study
intended to address the following hypotheses: the number of subtle neurological signs predicts (a) raw and

J Neuropsychiatry Clin Neurosci 21:4, Fall 2009

Z-transformed
Mini-Mental
State
Examination
(MMSE)3 scores; (b) raw and Z-transformed Frontal Assessment Battery (FAB)4 scores; (c) total Functional Independence Measure (FIM)5 score at time of Behavioral
Neurology & Neuropsychiatry consultation; (d) total
FIM score at time of rehabilitation discharge; and (e)
rehabilitation length of stay.

METHODS
This retrospective study was approved by the Colorado
Multiple Institutional Review Board and the HealthONE Institutional Review Board.
Participants
Medical records of 83 patients consecutively admitted
to an acute inpatient neurorehabilitation unit following
traumatic brain injury were reviewed. Inclusion criteria
for this study were: clinical diagnosis of TBI by American Congress of Rehabilitation Medicine definition6;
nonpenetrating TBI; age 20 89 years; English as the
primary language; not aphasic; Behavioral Neurology
& Neuropsychiatry consultation performed, including
neurological and cognitive examinations required to
address the study hypotheses; and medical records containing all relevant assessment and rehabilitation outcome measures. Among participants meeting these inclusion criteria, medical records data extraction
included: subject age, gender and education; mechanism of injury; presence or absence of intracranial abnormality on computed tomography (CT) or MRI of
the brain; whether or not the patient was in the period of posttraumatic amnesia as assessed by the
Received May 30, 2008; revised September 23, 2008; accepted September 30, 2008. Dr. Wortzel, Ms. Frey, and Dr. Arciniegas are affiliated
with Brain Injury Rehabilitation Unit, HealthONE Spalding Rehabilitation Hospital, in Aurora, CO; Drs. Wortzel, Anderson, and Arciniegas are affiliated with VISN-19 MIRECC, Denver Veterans Affairs
Medical Center, in Denver, CO; Dr. Wortzel, Ms. Frey, Dr. Anderson,
and Dr. Arciniegas are affiliated with the Neurobehavioral Disorders
Program, Department of Psychiatry, University of Colorado School of
Medicine, in Denver; Drs. Anderson and Arciniegas are affiliated
with Behavioral Neurology Section, Department of Neurology, University of Colorado School of Medicine, in Denver. Address correspondence to Hal S. Wortzel, M.D., VISN 19 MIRECC, 1055 Clermont
Street, Room 4E130, Denver, CO 80220; Hal.wortzel@ucdenver.edu
(e-mail).
Copyright 2009 American Psychiatric Publishing, Inc.

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COGNITIVE AND FUNCTIONAL IMPAIRMENTS AFTER TBI

Galveston Orientation and Amnesia Test (GOAT)7
upon rehabilitation admission and also upon Behavioral Neurology & Neuropsychiatry consultation;
neurological examination findings; MMSE, and FAB
scores; FIM scores at time of rehabilitation admission,
proximate (3 days) to Behavioral Neurology & Neuropsychiatry consultation, and at rehabilitation hospital discharge; and acute hospital and rehabilitation
hospital lengths of stay.
Subtle Neurological Signs Score
A subtle neurological signs score was constructed based
on the neurological examination data recorded during
the Behavioral Neurology & Neuropsychiatry consultations. The elements contributing to the subtle neurological signs score included paratonia (mitgehen and/or
gegenhalten) and primitive reflexes. Mitgehen and gegenhalten reflect impairments of volitional motor inhibition
during assessment of resistance to passive manipulation (hence the designation of paratonia). Mitgehen
(from German, go along or go with) refers to a
patients inability to inhibit active movement of the
extremity under examination despite instructions to the
patient to remain passive during the examiners movement of that extremity. Gegenhalten (from German,
hold against or go against) describes purposeless
resistance by the patient against movement of the extremity by the examiner (pull-counter-pull phenomenon). The primitive reflexes included in the subtle neurological signs score: glabellar response, snout
response, grasp response (left and right), palmomental
(left and right), suck reflex, and rooting response. The
examination for these findings and interpretation of
primitive reflexes were performed according to the
methods described in Arciniegas and Beresford.8 One
point was allocated for each abnormal finding, and
missing data points were scored as 0. The subtle neurological signs score was equal to [# of primitive reflexes] [mitgehen] [gegenhalten], with a range of 0 10
points.
Cognitive Assessment Measures
The MMSE was administered as described by Folstein
et al.3 and the FAB was administered as described by
Dubois et al.4 To correct for the effects of age and education on MMSE and FAB scores, Z-transformations
were performed using normative data for these measures.9,10

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Functional Independence Measure Assessments

The FIM assessments were performed by physical therapy, occupational therapy, speech language pathology,
and nursing staff assigned to the acute inpatient rehabilitation unit using the method described in the Guide
for Uniform Data Set for Medical Rehabilitation, Version 5.1.5
Statistical Analyses
Statistica 8.0 (StatSoft, Inc., Tulsa, Okla.) was used for
all descriptive data analyses as well as for regression
analyses to test the study hypotheses. Simple regression
modeling was used to investigate the proportion of
variance in MMSE and FAB scores (raw and Z-scores),
FIM scores, and rehabilitation length of stay accounted
for by subtle neurological signs score.

RESULTS
Fifty-one participants (13 women) met study inclusion
criteria; these patients are described in Table 1. Among
these patients, causes of TBI included motor vehicle
accidents (50.9%), falls (31.4%), sports/recreational
(11.8%), and assaults (5.9%). Neuroimaging (CT and/or
MRI) demonstrated intracranial abnormalities consistent with TBI among 47 patients (92.2%). At the time of
rehabilitation admission, 23 patients (45.1%) were in
posttraumatic amnesia, and 14 (27.5%) were still in
posttraumatic amnesia at the time of Behavioral Neurology & Neuropsychiatry consultation (usually 5 6
days after rehabilitation admission).
Paratonia and Primitive Reflexes
Paratonia was present in 30 patients (58.8%); all of these
demonstrated mitgehen, and eight patients (15.7%) also
demonstrated gegenhalten. Fifty patients (98%) demonstrated at least one primitive reflex; two or more primitive reflexes were present in 45 patients (88.2%), and
three or more were present in 34 patients (66.7%). Glabelar response was the most common primitive reflex
(82.4%), followed by snout response (74.5%), palmomental response (left 49% and right 47.1%), grasp response (left 41.2% and right 41.2%), suck reflex (19.6%),
and rooting response (3.9%).
Regression Modeling of Cognitive and Functional Status
Using Subtle Neurological Signs
Subtle neurological signs score predicts raw FAB score
(adjusted R20.28, 0.54, p0.00005), raw MMSE

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WORTZEL et al.
score (adjusted R20.25, 0.51, p0.0002), FAB Zscore (adjusted R20.24, 0.51, p0.0002), and
MMSE Z-score (adjusted R20.15, 0.41, p0.003).
Subtle neurological signs score also predicts total FIM
score at the time of Behavioral Neurology & Neuropsychiatry consultation (adjusted R20.12, 0.37,
p0.01) and rehabilitation discharge (adjusted R20.13,
0.38, p0.006). Finally, subtle neurological signs
score predicts rehabilitation length of stay (adjusted
R20.24, 0.51, p0.0002).

DISCUSSION
Paratonia and primitive reflexes predict cognitive performance, functional independence, and inpatient rehabilitation length of stay in the subacute period following TBI. Assessment for these subtle neurological signs
among inpatients with recent TBI therefore may contribute useful information regarding their need for further neurobehavioral rehabilitative evaluation and
treatments.
After correcting for age and education, subtle neurological signs score accounted for a greater proportion of
the variance in performance on the FAB than on the
MMSE. This observation, that subtle neurological signs
score is more strongly associated with performance on
a measure of executive function (FAB) than one of general cognition (MMSE), is concordant with the common
attribution of paratonia and primitive reflexes to frontal
dysfunction,11 although the anatomic localization of
these findings remains a matter of controversy.11,12
TABLE 1.

Since the presence of paratonia and primitive reflexes

predicts cognitive impairment in this population, eliciting such findings on the elementary neurological examination should prompt the clinician to perform a
more detailed bedside cognitive examination, such as
that included in our Behavioral Neurology & Neuropsychiatry consultations.
Subtle neurological signs also predicted functional
status as assessed by the FIM, similar to the association
between primitive reflexes and functional status in neurodegenerative dementias.13,14 When planning rehabilitation treatment, expectations regarding duration of
inpatient treatment may also be anticipated by the
number of subtle neurological signs given that 24% of
the variance in rehabilitation length of stay was accounted for by subtle neurological signs score.
Describing these findings and their implications with
respect to cognitive performance, functional status, and
rehabilitation outcomes may also be of use in the education of family and other care providers during the
acute rehabilitation period. In our experience, some
families have difficulty accepting as objective the cognitive and functional assessments performed in the
acute rehabilitation setting. Neurological examination
findings are, for many of these families, more easily
accepted as objective and as evidence of injury-related
neurological dysfunction. Complementing discussions
of posttraumatic cognitive, neurobehavioral and functional impairments with the presentation of neurological findings such as paratonia and primitive reflexes
may allow, in such circumstances, families to engage in
these discussions more fully and to appreciate more

Descriptive Participant Data (Continuous Variables, n51)

Age (years)
Education (years)
MMSE (raw)
MMSE (Z-score)
FAB (raw)
FAB (Z-score)
SNS score
Admission FIM, total
Consultation FIM, total
Discharge FIM, total
Acute length of stay (days)
Time to Behavioral Neurology & Neuropsychiatry
consultation post-TBI (days)
Rehabilitation length of stay (days)

Mean SD

Min,
Max

46.917.2
13.72.3
23.05.4
2.72.8
12.34.1
5.74.1
4.32.2
55.719.1
68.623.9
102.518.4
22.920.7
28.321.0

20, 79
9, 20
6, 30
11.5, 0.8
2, 18
15.4, 1.0
0, 9
18, 90
21, 126
34, 126
3, 117
7, 121

20.711.8

4, 52

MMSEMini-Mental State Examination; FABFrontal Assessment Battery; FIMFunctional Independence Measure; SNSsubtle neurological signs; TBItraumatic brain injury

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readily the serious nature of their loved ones clinical
condition.
The principal limitation of the present study is its
retrospective design and predication on data collected
originally for clinical rather than research purposes.
Additionally, the preliminary nature of the subtle neurological signs metric employed in this study is of concern: this metric has not yet been validated, and its
reliability has not been established. While acknowledging these limitations, it is noteworthy that statistically
significant relationships were identified between the
subtle neurological signs score and the cognitive and
functional measures in a data set derived from everyday practice. This observation suggests that the generalizability of these findings may be substantial despite
the retrospective nature of this study. Other limitations
include the lack of a data set of size sufficient to permit
item-level analyses, such as prediction of cognitive or
functional status by individual primitive reflex or paratonia findings, or to establish a cutoff subtle neurological signs score that is predictive of cognitive or functional impairment.
Despite these limitations, the present findings suggest that assessment of persons with recent TBI for
paratonia and primitive reflexes may yield information
with important diagnostic and treatment implications.

Given the need to develop further clinical metrics that

identify persons with recent TBI in need of further diagnostic and functional interventions,15 we recommend
the development of prospective studies of this subject,
including validation of the subtle neurological signs
metric employed here, determination of its reliability,
and further investigation of its clinical usefulness.
This work was presented as a poster at the 19th Annual
Meeting of the American Neuropsychiatric Association, Savannah, Ga., on March 3, 2008. This work was also published
in abstract form as: Wortzel HS, Frey KL, Anderson CA,
Arciniegas DB: Subtle neurological signs predict the severity
of subacute posttraumatic cognitive and functional impairments in traumatic brain injury (Abstract # P2), in Abstracts Presented at the 19th Annual Meeting of the American Neuropsychiatric Association. J Neuropsych Clin
Neurosci 2008; 20:232234 (available online at http://
neuro.psychiatryonline.org/content/vol20/issue2/index.dtl#
ABSTRACTS)
This work was supported by HealthONE Spalding Rehabilitation Hospital (KLF, DBA) and the VISN-19 MIRECC
(HSW, CAA, DBA). The authors are grateful to Kenneth L.
Tyler, M.D., for his assistance during the preparation of this
manuscript.

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