Archives of Physical Medicine and Rehabilitation

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Archives of Physical Medicine and Rehabilitation 2015;96(8 Suppl 3):S245-55

ORIGINAL RESEARCH

Enteral Nutrition for Patients With Traumatic Brain

Injury in the Rehabilitation Setting: Associations
With Patient Preinjury and Injury Characteristics and
Outcomes
Susan D. Horn, PhD,a Merin Kinikini, RD, FNP, DNP, CNSC,b
Linda W. Moore, MS, RDN, CCRP,c Flora M. Hammond, MD,d,e Murray E. Brandstater, MD,f
Randall J. Smout, MS,a Ryan S. Barrett, MSa
From the aInstitute for Clinical Outcomes Research, International Severity Information Systems, Inc, Salt Lake City, UT; bNeuro Specialty
Rehabilitation Unit, Intermountain Medical Center, Salt Lake City, UT; cHouston Methodist Hospital, Houston, TX; dCarolinas Rehabilitation,
Charlotte, NC; eIndiana University, Indianapolis, IN; and fLoma Linda University Medical Center, Loma Linda, CA.
Current affiliation for Horn, Department of Population Health Sciences, University of Utah School of Medicine, Salt Lake City, UT.

Abstract
Objective: To determine the association of enteral nutrition (EN) with patient preinjury and injury characteristics and outcomes for patients
receiving inpatient rehabilitation after traumatic brain injury (TBI).
Design: Prospective observational study.
Setting: Nine rehabilitation centers.
Participants: Patients (NZ1701) admitted for first full inpatient rehabilitation after TBI.
Interventions: Not applicable.
Main Outcome Measures: FIM at rehabilitation discharge, length of stay, weight loss, and various infections.
Results: There were many significant differences in preinjury and injury characteristics between patients who received EN and patients who did
not. After matching patients with a propensity score of >40% for the likely use of EN, patients receiving EN with either a standard or a high-
protein formula (>20% of calories coming from protein) for >25% of their rehabilitation stay had higher FIM motor and cognitive scores at
rehabilitation discharge and less weight loss than did patients with similar characteristics not receiving EN.
Conclusions: For patients receiving inpatient rehabilitation after TBI and matched on a propensity score of >40% for the likely use of EN,
clinicians should strongly consider, when possible, EN for ≤25% of the rehabilitation stay and especially with a formula that contains at least 20%
protein rather than a standard formula.
Archives of Physical Medicine and Rehabilitation 2015;96(8 Suppl 3):S245-55
ª 2015 by the American Congress of Rehabilitation Medicine

The provision of adequate nutritional support for patients with electrolyte balance, drug administration, and dysphagia. In addi-
moderate-to-severe traumatic brain injury (TBI) has been a clin- tion, it may be difficult to maintain tubes and lines in a confused
ical challenge for decades.1-3 Patients’ primary and secondary or agitated patient, particularly in a rehabilitation setting.
injuries create unique metabolic derangements that pose issues Individuals with TBI have a much higher resting metabolic
such as optimal timing and route of nutrition, appropriate fluid and expenditure (RME) than do patients without TBI.4 In fact, with
severe TBI, RME has been found to range up to 240% of RME in
Supported by the National Institutes ofHealth, National Center for Medical Rehabilitation Research patients without TBI; they are similar in metabolic response to
(grant no. 1R01HD050439-01), the National Institute on Disability and Rehabilitation Research (grant patients with burns over 20% to 40% of their body surface area.4
no. H133A080023), and the Ontario Neurotrauma Foundation (grant no. 2007-ABI-ISIS-525).
Publication of this article was supported by the American Congress of Rehabilitation Medicine. The consequences of hypermetabolism, hypercatabolism, and
Disclosure: none. altered immune function in patients with acute TBI are excessive

0003-9993/15/$36 - see front matter ª 2015 by the American Congress of Rehabilitation Medicine
http://dx.doi.org/10.1016/j.apmr.2014.06.024
S246 S.D. Horn et al

protein breakdown, which can lead to malnutrition.5 However, of EN support, as well as associations of EN with outcomes,
patients with TBI requiring hospitalization often do not, or cannot, controlling for patient differences.
consume enough nutrition to support their increased requirements
for recovery and rehabilitation.5
Enteral nutrition (EN) administered as early as possible has Methods
been established as the preferential route of nutritional support for
this population versus total parenteral nutrition (TPN); some cen- This comparative effectiveness PBE study examined the differ-
ters use a combination of EN and TPN in the early stages of injury if ential effects of a wide array of specific treatments administered in
the patient does not tolerate adequate amounts of EN alone.6 10 acute inpatient rehabilitation facilities serving patients with
Chourdakis et al7 recently reported that early EN may affect hor- TBI in a brain injury specialty unit who were enrolled from
monal response to TBI and suggests that this may reduce catabolic October 2008 to September 2011. The 10 participating centers
and inflammatory processes induced by TBI. There appears to be a constituted a convenience sample of adults with TBI on the basis
consensus on early initiation of EN, but less definitive are recom- of their willingness to participate in the research. The institutional
mendations on advancement timing and formula components (eg, review board at each center approved the study; each patient or
whether to use specialty formulas such as those containing his/her proxy gave informed consent.
immune-enhancing properties).8-12 The Institute of Medicine rec-
ommended inclusion of nutrient additives (eg, n-3 fatty acids, Participants
creatine, choline, and zinc) as potentially beneficial for recovery
after TBI.3,5 Patients with TBI, similar to other trauma patients, Inclusion criteria were as follows21: (1) Sustained a TBI, defined
likely require 2.0 to 2.5g of protein/kg at a minimum, especially as damage to brain tissue caused by external force and evidenced
during the early period after injury.6,13 Evaluation of the duration of by loss of consciousness, posttraumatic amnesia, skull fracture, or
a higher protein requirement has not been reported in the literature, objective neurological findings. Diagnoses included International
but it likely correlates with metabolic status. If increased metabolic Classification of Diseases, 9th Revision, Clinical Modification
rates extend into the rehabilitation setting, then increased protein codes consistent with the Centers for Disease Control and
needs may also be present. Prevention Guidelines for Surveillance of Central Nervous System
Swallowing disorders and decreased behavioral/cognitive skills Injury; (2) received inpatient care in a designated brain injury
are frequently present in patients with severe brain injury and rehabilitation unit of one of the participating rehabilitation facil-
significantly affect oral intake.14 Persons who swallow abnormally ities; and (3) were 14 years or older and treated in an adult
take much longer to start eating and to achieve total oral feeding, rehabilitation unit.
and they require nonoral supplementation 3 to 4 times longer than
those who swallow normally.14 Patients with severe TBI may also Patient variables
have intolerance to EN, which hampers survival and rehabilita- Patient characteristics, including demographic characteristics and
tion.15 Haddad and Arabi16 discuss proactive use of prokinetic injury characteristics, were recorded on the basis of clinicians’
agents, such as erythromycin and metoclopramide, as well as suggestions as well as previous research indicating their impor-
postpyloric feeding as ways to overcome problems of gastric tance in populations with TBI. In addition to patient data available
distention and intolerance experienced by patients with TBI. on admission, we collected information on patients’ status during
Most reports11,13,17,18 regarding nutrition in patients with TBI their rehabilitation stay, including the presence of aphasia and
address the route (TPN vs EN) and/or timing (early vs late) of dysphagia. Table 1 lists the characteristics of study patients.
initiation of nutritional support related to hospital admission and
have addressed outcomes such as mortality or length of stay Functional dependence
(LOS) in the acute care setting. We could not find any published We used admission FIM, an assessment of independent func-
reports that address the role of nutritional support during reha- tioning consisting of 18 items in 2 domains: motor (13 items) and
bilitation of patients with TBI. A practice-based evidence (PBE) cognitive (5 items). Each FIM item was rated on a 7-category
study in stroke rehabilitation found that the use of EN support for scale, ranging from 1 (total assistance required) to 7 (complete
≤ 25% of the rehabilitation stay for patients with severe stroke was independence). To eliminate distortion in quantifying the status of
a significant factor in predicting higher discharge FIM total and patients whose capability is at the extremes of the instrument’s
motor scores, controlling for patient and other treatment differ- range, FIM motor and cognitive scores were recoded separately
ences.19,20 It is not known if these findings are applicable to using tables published by Heinemann et al,22 which were based on
the population with TBI receiving rehabilitation. This article Rasch analysis of FIM data of a large sample with brain injury.
describes nutritional support methods used for patients in a TBI-
PBE study during rehabilitation21 and examines associations of Injury severity and comorbidity
patient preinjury and injury characteristics with use and duration The primary medical severity measure used was the Compre-
hensive Severity Index (CSI), which defines severity as the
physiological and psychosocial complexity presented owing to
List of abbreviations: the extent and interactions of a patient’s disease(s).21 The CSI is
CSI Comprehensive Severity Index age- and disease-specific and is independent of treatments. It
EN enteral nutrition provides an objective, consistent method to operationalize pa-
LOS length of stay tient severity of illness on the basis of >2100 individual signs,
PBE practice-based evidence symptoms, and physical findings and >5600 disease-specific
RME resting metabolic expenditure
criteria sets related to all of a patient’s disease(s). More details
TBI traumatic brain injury
about the CSI appear elsewhere.21 The CSI modification used
TPN total parenteral nutrition
here allowed separating severity of brain injury (called brain

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Nutritional support for patients with TBI S247

Table 1 Characteristics of patients with and without EN

Table 1 (continued )
EN No EN
EN No EN
Characteristic (NZ451) (NZ1250) P
Characteristic (NZ451) (NZ1250) P
Demographic characteristics Depression before or during 32.2 30.4 .513*
Sex: male (%) 72.3 71.6 .807* rehabilitation
Age at rehabilitation 38.5T19.6 47.1T22.0 <.001y Hypertension before or during 39.7 45.0 .053*
admission (y) rehabilitation
Race/ethnicity .012z Paralysis before or during 53.9 30.3 <.001*
Black 12.0 17.0 rehabilitation
White 80.0 72.7 Renal failure before or during 8.6 8.9 .923*
White Hispanic 4.9 7.4
rehabilitation
Other and unknown 3.1 2.9
Brain injury and severity
Highest education achieved .268z
information
Some high school, 24.2 22.6
Cause of injury <.001z
no diploma Fall 21.3 36.8
High school diploma 24.2 26.6 Motor vehicle collision 69.6 50.0
Work toward or completed 18.0 15.6 Sports 1.6 2.0
associate’s degree Violence 5.1 7.3
Work toward or completed 20.8 19.5 Other 2.4 3.9
bachelor’s degree
GCS score immediately after <.001z
Work toward or completed 9.5 9.8
injury or after arrival
master’s/doctoral degree
in acute care (%)
Unknown 3.3 5.8 Mild (13e15) 8.4 18.2
Marital status at injury .114z Moderate (9e12) 5.8 8.2
Single/never married 47.0 41.2 Severe (3e8) 44.6 23.8
Married/common law 34.6 35.8 Intubated/sedated 14.9 11.0
Previously married 15.7 19.8 Unknown 26.4 38.8
Other/unknown 2.7 3.1
Nature of brain injury .277z
Able to drive before injury <.001z
Skull closed, contusion/ 67.6 70.4
No 5.5 12.6
hemorrhage present
Yes 81.4 68.8
Skull closed, no 23.9 23.3
Unknown 13.1 18.6
contusion/hemorrhage
Primary payer <.001z Skull open, contusion/ 8.4 6.3
Medicare 11.5 25.8 hemorrhage present
Medicaid 12.2 17.0 Facial fracture 18.2 12.5 .003*
Private insurance 26.8 25.3 Skull fracture 31.3 24.6 .006*
Worker’s compensation 9.1 6.8 Brain injury location .300z
Self-pay/none 6.9 4.6 Bilateral 65.9 61.8
MCO/HMO 19.5 14.0 Left 17.3 19.0
No-fault auto insurance 8.9 3.4 Right 16.9 19.2
Other/unknown 5.1 3.1
Midline shift (mm) <.001z
Admission body mass index <.001z
>0e5 9.8 13.6
(kg/m2)
>5 13.1 11.2
<16 1.3 1.4
Midline shift, mm not 11.8 10.2
16e≤18.5 12.4 6.3
specified
>18.5e≤25 54.3 47.0 No midline shift 22.6 34.3
>25e≤30 20.4 26.2 Unknown 42.8 30.6
>30e≤35 6.4 9.0 Subdural hematoma 43.0 47.5 .110*
>35e≤40 1.6 2.9 Epidural hematoma 10.0 7.4 .086*
>40 1.3 1.7 Subarachnoid hemorrhage 66.3 53.2 <.001*
Unknown 2.2 5.5 Intraventricular 24.6 14.0 <.001*
Preexisting and coexisting
hemorrhage
conditions
Brain stem involved 6.9 4.7 .086*
History of alcohol abuse 34.8 36.9 .458*
Craniotomy during care 10.2 4.9 <.001*
before injury
episode
History of drug abuse 20.0 22.8 .233*
Craniectomy during care 20.0 18.9 .626*
before injury
episode
Anxiety before or during 22.0 21.1 .736*
Weight-bearing precaution 27.9 26.9 .666*
rehabilitation
during rehabilitation
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S248 S.D. Horn et al

by International Classification of Diseases, 9th Revision, Clinical

Table 1 (continued) Modification codes in the rehabilitation medical record.
EN No EN
Characteristic (NZ451) (NZ1250) P Data analyses
Days from injury to 31.9T24.5 19.8T24.4 <.001y
rehabilitation admission Analyses were performed using SAS version 9.2.a When data were
missing, ≤1 adjustments were made, depending on the variable
PTA clearance before 17.3 47.8 <.001*
rehabilitation admission and its intended use in analyses. Sometimes we categorized values
Admission brain injury 61.8T20.1 36T17.8 <.001y simply as “unknown” (and included an “unknown” category in the
component of the CSI score analysis as a dummy variable representing missingness); at other
Admission nonebrain injury 22.6T16.1 15.2T13.1 <.001y times we excluded patients with missing data from analyses.
component of the CSI Because our sample had patients with a wide range of func-
score tional and cognitive disabilities and also had many patients who
did not require EN, we needed to find a method to examine the
Moderate-to-severe 90.2 35.2 <.001*
dysphagia on admission effect of EN that was not biased by only the sickest patients or the
most severely injured receiving EN. Our first step was to deter-
Moderate-to-severe aphasia 49.9 43.7 .024*
on admission mine a subset of patients whom we predicted would benefit from
Functional status and LOS EN, but may or may not have actually received it. To find this
Admission FIM motor 21.5T11.3 38.6T16.4 <.001y
subset, we used the patient preinjury and injury characteristics
scoredraw
data to develop a propensity score using a logistic regression
Admission FIM motor 19.6T16.2 38.4T13.5 <.001y
model to predict receipt of EN.23 We then matched patients with
the same propensity score, where one received EN and the other
scoredRasch-transformed
Admission FIM cognitive 10.5T5.4 16.7T6.6 <.001y
did not, and compared outcomes.
Descriptive statistics were used to provide frequencies and
scoredraw
percentages for categorical variables describing patients, treat-
Admission FIM cognitive 25.8T18.1 43.2T16.1 <.001y
ments, and outcomes and means, medians, quartiles, and SDs to
scoredRasch-transformed
summarize continuous variables. Bivariate analyses were con-
Length of rehabilitation stay 32.2T15.0 18.3T10.0 <.001y
ducted to examine how patients who received EN differed from
NOTE. Values are mean T SD or as percentages. those who did not. For discrete variables, we used the chi-square
Abbreviations: GCS, Glasgow Coma Scale; MCO/HMO, managed care test or McNemar test to determine the significance of associations.
organization/health maintenance organization; PTA, posttraumatic For continuous variables, we used t tests, paired t tests, analysis of
amnesia. variance, or Friedman rank sum test. A 2-sided P value of <.05
* Fisher exact test.
y was considered statistically significant. Finally, we used ordinary
Two-sample t test.
c test.
z 2 least squares regression analyses to determine associations of EN
with continuous outcome variables after controlling for other
patient preinjury and injury characteristics. For independent var-
iables with pairwise correlations r>.75, only one of the pair was
injury component of the CSI) from severity of illness of all other allowed to enter the model.
injuries, complications, and comorbidities (called nonebrain To help clinicians more easily decide which patients might
injury component of the CSI). The brain injury component of the benefit from EN, we also used recursive partitioning to build a
CSI allowed the detection of differences in the amount of brain classification model using a 2-stage procedure. First the single
damage in patients that might otherwise be hidden in an overall variable that best splits the data into 2 groups is found; the data are
injury severity score. separated at this point, and then the process is repeated individ-
ually on the resultant subgroups until either they reach a minimum
Treatment factors sample size (depending on the sample size of the data) or no
We collected treatment variables related to EN from a chart improvement can be made in explaining an outcome.
review. These included formula type and start and stop dates. EN The original study sample included 2130 patients with TBI.21
was classified as either high protein or standard. High-protein We excluded patients who had TPN at any time during their
formulas were defined by having at least 20% of calories coming rehabilitation stay (nZ127, 6.0%), because we did not collect
from protein (most of these formulas actually had 25%), or details about TPN start and stop times; hence, we could not
standard formulas (usually having 14%e18% protein) with sup- determine for how long they received TPN or any details about the
plemental protein provided to increase the total protein amount to content of TPN. We also excluded patients who had EN docu-
>20%. On the basis of the finding of better outcomes for EN mented but no formula type was recorded or they had only fiber in
support for ≤25% of the rehabilitation stay for patients with se- their EN, which was not considered EN (nZ15, 0.7%). Next,
vere stroke,19 we explored the same level of EN support in this patients receiving EN at the time of rehabilitation discharge and
study of patients with TBI. having a total CSI severity score at admission of >60 (indicating
serious morbidity) were excluded (nZ107, 5.0%). In addition, we
Outcome variables excluded patients with rehabilitation LOS >75 days (highest
Outcome variables examined to assess the association with EN 1.5%; nZ31). The rationale for excluding these patients was that
were discharge FIM motor and cognitive scores, weight loss if they were discharged on EN and were also severely injured or
during rehabilitation, LOS, and various infections (aspiration stayed a long time in rehabilitation, it was unlikely that EN would
pneumonia, pneumonia, urinary tract infections, sepsis) as defined have a significant effect on their outcomes. Patients with similar

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Nutritional support for patients with TBI S249

Table 2 Propensity score models to predict patient’s need for EN

Model 1 Model 2
Parameter Odds Ratio P Parameter Odds Ratio P
Estimate Estimate (Wald c2) Estimate Estimate (Wald c2)
Intercept —1.74 NA 11.27 .001 —0.36 NA 0.60 .437
Admission brain injury component of the CSI score 0.03 1.03 44.31 <.001 NA NA NA NA
Admission nonebrain injury component of the 0.01 1.01 4.71 .030 NA NA NA NA
CSI score
Admission FIM motor scoredRasch-transformed —0.04 0.96 60.62 <.001 NA NA NA NA
Admission FIM cognitive scoredraw NA NA NA NA —0.13 0.88 87.79 <.001
Moderate-to-severe aphasia on admission —0.66 0.52 15.67 <.001 —0.46 0.63 8.83 .003
Moderate-to-severe dysphagia on admission 1.89 6.65 91.26 <.001 2.36 10.60 157.33 <.001
Age on admission —0.02 0.98 18.85 <.001 —0.02 0.98 25.18 <.001
History of alcohol abuse before injury 0.33 1.39 4.37 .037 NA NA NA NA
Skull fracture 0.48 1.62 7.86 .005 NA NA NA NA
Days from injury to rehabilitation admission 0.01 1.01 8.24 .004 0.01 1.01 20.83 <.001
Cause of injury: miscellaneous —0.97 0.38 4.57 .033 —1.02 0.36 6.02 .014
Marital status: single —0.47 0.63 5.17 .023 —0.50 0.61 6.51 .011
Primary payer: Medicaid —0.72 0.49 10.54 .001 —0.64 0.53 9.46 .002
Primary payer: no-fault auto insurance 0.69 1.99 5.34 .021 0.72 2.06 6.08 .014
Paralysis on admission NA NA NA NA 0.57 1.76 15.00 .000
Able to drive before injury NA NA NA NA 0.41 1.51 5.13 .024
Highest education achieved: high school diploma NA NA NA NA —0.37 0.69 5.27 .022
Race: white NA NA NA NA 0.35 1.43 4.12 .042
No. of observations used 1698 (yesZ449; noZ1249) 1698 (yesZ449; noZ1249)
c statistic .903 .883
Abbreviation: NA, not applicable.

characteristics were excluded from the study of EN in the post- mean admission Rasch-transformed FIM motor and cognitive
stroke rehabilitation study.19 The 107 patients discharged on EN scores, and higher admission brain injury and nonebrain injury
were significantly different (sicker) from those with EN during components of CSI scores. Of the 451 patients receiving EN,
rehabilitation (nZ451, 21.2%) in the following ways: (1) older >90% had moderate-to-severe dysphagia and 50% had aphasia.
age (43.4y vs 38.2y; PZ.025); (2) longer time from injury to The propensity score determined the combination of patient
rehabilitation admission (55.2d vs 32.4d; P ≤.001); (3) higher preinjury and injury characteristics that were significantly asso-
brain injury component of the CSI (78.6 vs 66.5; P<.001); (4) ciated with use and duration of EN support. Significant variables
greater percent craniectomy (18.8% vs 9.9%; PZ.015); (5) lower are included in table 2. The strongest predictors of receiving EN
admission Rasch-transformed FIM motor score (11.9 vs 19.5; included higher admission brain injury component of the CSI
P<.001); and (6) lower admission Rasch-transformed FIM score, lower admission Rasch-transformed FIM motor score, and
cognitive score (18.4 vs 25.6; PZ.0002). Finally, we excluded having moderate-to-severe dysphagia (c statisticZ.903). In
patients from 1 site because of their practice of not using EN to table 2, we also present a second propensity score model that can
treat their patients (nZ149, 7.0%). be used if one does not have admission brain injury component of
the CSI score, admission nonebrain injury component of the CSI
score, or Rasch-transformed FIM motor score. The second model
Results is almost as good as the first model that we used for our subse-
quent analyses and can be used to predict a patient’s probability of
The final study sample included 1701 (79.9%) patients (480 receiving EN when CSI and Rasch-transformed FIM measures are
women and 1221 men). Of these patients, 451 received EN for >1 not available. If instead a recursive partitioning analysis was used
day and 1250 received either no EN or EN for only 1 day. Cli- to estimate a patient’s probability of receiving EN, our data found
nicians decided that 1 day of EN was too few to have any effect on that a close approximation of a propensity score of >40% for the
outcomes and assigned these patients to the “no EN” category. likely use of EN is an admission FIM motor score of≤20,
As shown in table 1, patients with TBI who received EN were moderate-to-severe dysphagia, and >8 days from injury to reha-
more likely to be white and less likely to be black, were more bilitation admission.
likely to be underweight or normal weight, have health mainte- For each of the 1701 patients, we computed a propensity score for
nance organization or no-fault auto insurance, were driving before receiving EN. We decided to use a propensity score of >40% for
injury, were paralyzed, received their TBI in a motor vehicle receiving EN to indicate a need for EN. Of the 451 patients with EN,
collision, had a facial or skull fracture, had a subarachnoid hem- 335 (74.3%) had a propensity score of >40%; of the 1250 patients
orrhage, intraventricular hemorrhage, craniectomy, posttraumatic without EN, only 145 (11.6%) had a propensity score of >40%. The
amnesia during rehabilitation, and more days from injury to mean propensity score for the 335 patients with EN was 73.2%,
rehabilitation admission. Patients receiving EN also had lower whereas the mean propensity score for the 145 patients without EN

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S250 S.D. Horn et al

Table 3 Characteristics of propensity scoreematched patients with and without EN

Characteristic EN (NZ145) No EN (NZ145) P
Demographic characteristics
Sex: male (%) 76.6 80.7 .474*
Age at rehabilitation admission (y) 38.5T18.2 39.5T19.4 .646y
Race/ethnicity .111z
Black 13.1 14.5
White 83.4 75.9
White Hispanic 2.1 8.3
Other and unknown 1.4 1.4
Admission body mass index (kg/m2) 23.0T4.5 23.3T4.7 .507y
Admission body mass index (kg/m2) .921z
<16 2.1 2.8
16e≤18.5 12.4 9.0
>18.5e≤25 56.6 55.2
>25e≤30 18.6 21.4
>30e≤35 8.3 8.3
>35e≤40 0.7 1.4
>40 0.0 0.7
Unknown 1.4 1.4
Brain injury cause and severity
Cause of injury .658z
Fall 24.8 26.2
Motor vehicle collision 64.1 66.9
Sports 1.4 1.4
Violence 5.5 4.1
Other 4.1 1.4
Days from injury to rehabilitation admission 31.1T18.0 31.5T34.9 .896y
PTA clearance before rehabilitation admission 15.2 13.8 .868*
Admission brain injury component of the CSI score 61.3T13.5 59.5T12.8 .246y
Maximum brain injury component of the CSI score 64.4T13.6 63.1T13.1 .405y
Admission nonebrain injury component of the CSI score 22.5T16.6 21.6T14.5 .635y
Maximum nonebrain injury component of the CSI score 32.7T22.8 30.5T18.8 .369y
Moderate-to-severe dysphagia on admission 95.2 95.9 1.000*
Functional independence measures
Admission FIM motor scoredraw 20.9T9.1 21.0T10.3 .900y
Admission FIM motor scoredRasch-transformed 21.0T14.3 20.6T14.7 .824y
Admission FIM cognitive scoredraw 9.9T4.4 10.6T4.6 .192y
Admission FIM cognitive scoredRasch-transformed 25.3T15.8 27.5T15.9 .232y
Nutritional information
Admission Braden total score 14.8T2.4 14.9T2.5 .751y
Discharge Braden total score 18.7T2.3 18.4T2.5 .470y
Lowest Braden nutrition .721z
Very poor 2.1 4.8
Probably inadequate 28.3 28.3
Adequate 26.2 25.5
Excellent 0.7 1.4
Unknown 42.8 40.0
Lowest serum albumin during rehabilitation 3.2T0.6 3.2T0.6 .968y
Lowest serum albumin category .646z
Very low (1.0e3.0g/dL) 37.2 36.6
Low (>3.0e3.49g/dL) 21.4 20.0
Normal (≤3.5g/dL) 31.7 29.0
Missing 9.7 14.5
Lowest serum transthyretin during rehabilitation 25.2T6.4 24.4T7.6 .535y
Lowest serum transthyretin category .386z
Elevated (>29.6mg/dL) 10.3 8.3
Normal (>15.5e29.6mg/dL) 32.4 24.8
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Nutritional support for patients with TBI S251

Table 3 (continued )
Characteristic EN (NZ145) No EN (NZ145) P
Mild malnutrition (10e15.5mg/dL) 2.8 4.1
Missing 54.5 62.8

NOTE. Values are mean T SD or as percentages.

Abbreviation: PTA, posttraumatic amnesia.
* Fisher exact test.
y
Two-sample t test.
c test.
z 2

was only 60.5% (P<.001). Hence, we needed to create a matched and Table 5 presents the results of ordinary least squares regression
balanced sample before examining the association of EN with out- analyses to predict discharge FIM motor and cognitive scores,
comes; we selected 1 patient with EN for each of the 145 patients weight change during rehabilitation, and LOS. We found that EN
without EN, matching on propensity scores. This resulted in mean ≤ 25% of the
with either a standard or a high-protein formula for
propensity scores of 61% and 60.5% for the 145 patients with EN and rehabilitation stay was associated with significantly higher
145 patients without EN, respectively. discharge FIM subscale scores. The range of days for which
Table 3 compares the preinjury and injury characteristics of the patients in the propensity scoreematched sample received EN for
145 patients with EN and the 145 patients without EN. None ≤25% of their stay was 3 to 64 days, with a median of 15 days and
of the characteristics were significantly different between the 2 a mean of 19 days. This is the level of EN support that was
groups irrespective of whether using paired or unpaired tests. EN associated with better outcomes. This was not related to the site
duration ranged from 2 to 64 days (6%e100% of the rehabilitation where the patient was treated, because no site variables entered the
stay), with a mean of 16.6T12.6 days and a median of 13 days. models significantly after patient and treatment variables entered.
The mean percentage of the stay with EN was 52.4%T26.9% and Also, EN with a high-protein formula for≤25% of the stay was
a median of 50.0%. Of the 145 patients with EN, 80 (55.0%) had a associated with an almost 2-lb weight gain from admission to
nothing-by-mouth order during the EN episodes that ranged from discharge as compared with an almost 2-lb weight loss in patients
2 to 33 days (5.6%e100.0% of the rehabilitation stay), with a with no EN. However, EN with either formula for ≤25% of the
mean of 5.1T7.4 days and a median of 2 days. The percentage of stay was not significant in predicting LOS or infections.
the stay with a nothing-by-mouth order was 18.7%T24.0% with a
median of 8.3%.
Table 4 shows bivariate associations of each outcome with Discussion
receipt of EN. Patients receiving EN had borderline higher
discharge Rasch-transformed FIM motor and cognitive scores This study of the potential benefit of EN for patients with TBI
(PZ.055 and PZ.050, respectively), borderline longer LOS requiring inpatient rehabilitation found that EN with either a high-
(PZ.062), and less weight change (PZ.075), but no significant protein or a standard formula for≤25% of the rehabilitation stay
differences in urinary tract infections, sepsis, pneumonia, or was associated with better FIM motor and cognitive scores at
aspiration pneumonia. None of these bivariate analyses took into discharge. Patients who received a high-protein formula had less
account how long the patient received EN or the type of formula weight loss and higher discharge FIM motor scores than those who
used in EN. Hence, we conducted multiple regression analyses to received a standard formula.
account for duration and type of EN and additional potentially There are a number of possible explanations for these results.
confounding outcome variables. Other studies1,24 have found that patients with TBI can have an

Table 4 Outcomes: Complications during rehabilitation and discharge FIM motor and cognitive scores
Characteristic EN (NZ145) No EN (NZ145) P
Change in weight during rehabilitation —0.5T9.0 —2.8T12.1 .075*
Discharge FIM motor scoredraw 60.9T13.4 57.1T16.8 .032*
Discharge FIM motor scoredRasch-transformed 53.1T9.2 50.9T10.7 .055*
Discharge FIM cognitive scoredraw 21.0T5.9 19.6T5.5 .047*
Discharge FIM cognitive scoredRasch-transformed 52.5T12.6 49.7T12 .050*
LOS 31.2T14.0 28.4T12.2 .062*
Pneumonitis/aspiration pneumonia during rehabilitation 0.7 1.4 1.000y
Pneumonitis/aspiration pneumonia before or during rehabilitation 5.5 5.5 1.000y
Pneumonia during rehabilitation 24.1 22.1 .781y
Sepsis during rehabilitation 2.1 4.8 .335y
Urinary tract infection during rehabilitation 7.6 8.3 1.000y
NOTE. Values are mean T SD or as percentages.
* Two-sample t test.
y
Fisher exact test.

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 S252
Table 5 Results of ordinary least squares regression analyses predicting discharge FIM motor and cognitive scores and weight loss during stay
Discharge FIM Motor Scored Discharge FIM Cognitive Scored
Rasch-Transformed Rasch-Transformed Discharge Weight LOS
Standardized Standardized Standardized Standardized
Parameter Parameter Parameter Parameter Parameter Parameter Parameter Parameter
Outcome Estimate Estimate P Estimate Estimate P Estimate Estimate P Estimate Estimate P
Intercept 44.9 .00 <.001 47.1 .000 <.001 10.96 .00 <.001 28.22 .00 <.001
Admission FIM motor scored 0.28 .40 <.001 0.10 .04 .012 —0.34 —.38 <.001
Rasch-transformed
Admission FIM cognitive scored 0.27 .350 <.001
Rasch-transformed
Admission brain injury component of the —0.12 —.132 .026 0.13 .13 .016
CSI score
Admission nonebrain injury component 0.10 .122 .020
of the CSI score
Admission body mass index ≤18.5kg/m2 7.78 .20 <.001
Admission body mass index >30kg/m2 5.75 .05 .014
Admission weight 0.90 .93 <.001
EN for ≤25% of the rehabilitation stay 2.59 .12 .028 4.93 .186 .001
High-protein EN for ≤25% of the 5.65 .16 .003 6.37 .150 .005 3.70 .03 .057
rehabilitation stay
No. of observations used 290 290 263 290
R2 .189 .240 .935 .224
Adjusted R2 .181 .227 .934 .216
NOTE. Independent variables allowed to enter in models include admission FIM motor and cognitive scores, admission brain injury and nonebrain injury components of the CSI score, admission body mass
index categories of ≤8.5, 18.5e25, >25e30, and >30kg/m 2
, tube feeding for ≤25% of the rehabilitation stay, and high-protein tube feeding for ≤25% of the rehabilitation stay.
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S.D. Horn et al
Nutritional support for patients with TBI S253

increased metabolic resting rate after their injury. An imaging demonstrated that the strongest association with outcomes was of
study25 focusing on biopathology of TBI reported a brief period high-protein EN. Although this study did not assess nitrogen bal-
of hypermetabolic activity in the brain immediately after TBI, ance, clinical outcomes of improved discharge FIM subscale scores
followed by several days of glucose metabolic depression. The for both motor skills and cognitive function as well as less weight
period of metabolic depression typically lasts only a few days, but loss were greatest in patients receiving high-protein EN. These
patients with TBI may require a higher metabolic expenditure findings suggest that the protein catabolic rate may continue to
both locally in the brain and more systemically. This increased increase during rehabilitation for TBI. Therefore, research assess-
metabolic need may persist for some time after the injury and ing protein requirements in the rehabilitation setting or extended
could be positively affected by nutritional interventions such as recovery period and not just the acute phase of recovery is greatly
EN. This could help to explain why our study found a greater needed. For example, a randomized trial of a dose-ranging study of
improvement in FIM cognitive scores at discharge than in FIM EN protein levels comparing standard protein (15% of calories) to
motor scores, which was associated with EN and especially so high protein (20% of calories), high protein plus essential amino
with a high-protein formula. acids, low protein plus essential amino acids, and possible com-
A challenge in studying the association of EN with outcomes binations with fish oil and other immune-modulating components
after TBI rehabilitation is that patients who may receive EN are within the formula would help to clarify whether higher protein
generally at the more severe end of the spectrum owing to altered would be beneficial in this population. Other aspects to study were
awareness and arousal or severe dysphagia. Hence, when one as follows: metabolic needs during phases of TBI, best manage-
includes an indicator variable for receipt of EN in analyses and does ment practices for meeting nutritional intake goals, and a more
not have EN patients spread throughout the sample (a balanced detailed look at daily caloric and protein intake in those with diets
sample), one finds that EN is associated with poorer outcomes. and/or EN. Clinical studies should follow.
These poorer outcomes are not due to EN but due to the fact that it is As this study points to the possible benefits of EN, it is also
only the more severely impaired patients who receive EN. Therefore, important to note the potential risks of administering EN to a
one needs to examine EN and its association with outcomes in a population with TBI. EN is invasive and generally not desired by
sample of patients with TBI, where patients receiving EN are patients. In addition, the agitation and confusion that often char-
balanced and spread more evenly throughout the sample. There are acterize the behavior of the individual with TBI receiving inpa-
various ways of accomplishing this in observational studies. We used tient rehabilitation may make it difficult to administer or prevent
patient preinjury and injury characteristics to develop a propensity EN. Restraints or a 1:1 sitter observation may be required to
score for receiving EN and then matched patients with similar pro- maintain tubes. The removal of a gastrostomy tube by the patient
pensity scores, wherein one patient received EN and the other did may place the patient at risk for serious infection. Duodenal tubes
not. For our original sample of 1701 patients, we were able to find introduced nasally require an abdominal radiographic examination
only 145 patients without EN who had a propensity score of >40% to confirm the placement. When a patient pulls the tube out or it is
for the likely use of EN, which was the probability that the project removed accidentally, rehabilitation therapies may be interrupted
team felt indicated a minimal need for EN. This may be an indication to allow time for the radiograph. The use of a nasal bridle system
that in our study centers, patients who needed EN usually received it. may be appropriate at times after TBI. The nasal bridal system has
There were only 145 patients with this indication of needing EN who been used in patients with burns with some success, requiring
did not receive it, and it is with this sample and a matched sample fewer tube insertions and without sinusitis or aspiration pneu-
with EN that we were able to assess the potential associations of EN monia.28 The use of restraints and just the presence of a tube
with outcomes for patients with TBI requiring inpatient rehabilita- (gastric or nasal) itself may make patients more agitated, poten-
tion. A close approximation, in our data, of a propensity score of tially prompting the use of additional medications (with risk of
>40% for receiving EN is an admission FIM motor score of ≤20, side effects of medications), and carry important risks that may
moderate-to-severe dysphagia, and >8 days from injury to rehabil- outweigh the benefits of EN.
itation admission. Pneumonia and aspiration pneumonia are often cited as com-
The role that EN, and particularly protein, plays during reha- plications of EN.29,30 However, the present study suggests atten-
bilitation of patients with TBI is rarely mentioned in the literature. uated risks. For example, our study found no differences in rates
In a recent observational study of patients with TBI treated at of aspiration pneumonia or pneumonia between patients with EN
rehabilitation centers in Italy,26 the incidence of dysphagia on and patients with similar characteristics who did not receive EN.
admission to the rehabilitation center was 42.3%, which decreased This finding is in contrast to previous findings in acute care set-
to 13.7% on discharge. Only 45.8% of patients with TBI admitted tings.7,11,29,30 In addition, our study found improved outcomes
to rehabilitation were on oral feeding, which increased to 84.2% when EN was provided for at least 25% of the stay compared to
by discharge; however, no information on nutritional support patients with similar characteristics who did not receive EN,
during rehabilitation was provided.26 Similarly, a multicenter strongly suggesting a benefit that could be described to patients,
report27 on rehabilitation of patients with complicated mild TBI staff, and family to support an EN decision.
provided insight into the effect of admission FIM and Disability
Rating Scale scores on LOS, but nutritional status or support Study limitations
required or used by these patients during rehabilitation was not
mentioned. The present study indicates that EN, and particularly Some information that is relevant to this research was not available
protein, in the rehabilitation setting may play a significant role in for our patient sample, including nutritional supplementation during
recovery of patients with TBI: receiving EN for at least 25% of the acute care hospitalization, reason(s) for administration of EN, and
rehabilitation stay was associated with higher discharge FIM total caloric intake during inpatient rehabilitation. Acute care records
subscale scores for both motor skills and cognitive function. were not fully available, and thus, we do not know if EN was used
Supporting the hypothesis that protein needs continue to be high there, how many days after injury it was started, what EN formula
in patients with TBI during rehabilitation, the present study was used, and duration of EN before rehabilitation admission. We

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S254 S.D. Horn et al
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vation and Research Program Williams Bldg, Rm 1N491, 295 12. Clifton GL, Robertson CS, Grossman RG, Hodge S, Foltz R, Garza C.
Chipeta Way, Salt Lake City, Utah 84108. E-mail address: susan. The metabolic response to severe head injury. J Neurosurg 1984;60:
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We gratefully acknowledge the contributions of clinical and research Phys Med Rehabil 1999;80:365-71.
staff at each of the 10 inpatient rehabilitation facilities to designing, 15. Tan M, Zhu JC, Yin HH. Enteral nutrition in patients with severe
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and Rehabilitation, Ohio State University, Columbus, OH); Nora nutrition in traumatic brain injury: a prospective randomised trial. Nutr
Cullen, MD (Toronto Rehabilitation Institute, Toronto, Ontario, Hosp 2011;26:1120-4.
Canada); Cynthia L. Beaulieu, PhD (Brooks Rehabilitation Hospital, 18. Dickerson RN, Mitchell JN, Morgan LM, et al. Disparate response to
Jacksonville, FL); Flora M. Hammond, MD (Carolinas Rehabilita- metoclopramide therapy for gastric feeding intolerance in trauma
tion, Charlotte, NC [now at Indiana University]); David K. Ryser, MD patients with and without traumatic brain injury. J Parenter Enteral
(Neuro Specialty Rehabilitation Unit, Intermountain Medical Center, Nutr 2009;33:646-55.
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Salt Lake City, UT); Murray E. Brandstater, MD (Loma Linda Uni-
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PhD (Medstar National Rehabilitation Hospital, Washington, DC); Stroke rehabilitation patients, practice, and outcomes: is earlier and
James A. Young, MD (Physical Medicine and Rehabilitation, Rush more aggressive therapy better? Arch Phys Med Rehabil 2005;
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