Epidural Hematoma
Epidural Hematoma
www.elsevier.com/locate/nut
                                                    Applied nutritional investigation
Abstract              Objective: This study explored current nutritional treatment policies and nutritional outcome in
                      patients with severe traumatic brain injury.
                      Methods: We performed a retrospective, structured survey of the medical records of 64 patients up
                      to 6 months after injury or until the patients were independent in nutritional administration.
                      Results: Enteral nutrition was administered to 86% of patients. Fourteen patients (22%) had a
                      gastrostomy; after 6 months four were still in use. At 6 months, 92% of patients received all food
                      orally and 84% had gained nutritional independence. Energy intake was equal to the calculated basal
                      metabolic rate throughout the first month after injury and increased by 21% during the second
                      month. Sixty-eight percent exhibited signs of malnourishment with weight losses of 10 –29%.
                      Conclusion: This study suggests that most patients with severe traumatic brain injury regain their
                      nutritional independence within the first 6 months after injury, but also that most develop signs of
                      malnutrition. © 2007 Elsevier Inc. All rights reserved.
Keywords:             Traumatic brain injury; Parenteral nutrition; Enteral nutrition; Oral feeding; Level of independence; Malnu-
                      trition
0899-9007/07/$ – see front matter © 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.nut.2007.01.010
                                                   K. Krakau et al. / Nutrition 23 (2007) 308 –317                                                309
Fig. 1. Flow chart of inclusion and exclusion procedures of patients. Values are expressed as numbers of patients. G, Gothenburg region; S, Stockholm
region; TBI, traumatic brain injury; U, Uppsala region.
310                                          K. Krakau et al. / Nutrition 23 (2007) 308 –317
were not found by the investigators. Data collection took             Energy intake
place locally in all but nine units, where instead journal
copies were sent for.                                                    The daily delivered intake of energy was recorded on
   The daily recordings made at the units were carefully              separate nutritional protocols mainly during PN and EN
examined for the selected data. The nutritional data sought           periods, but occasionally even when patients were fed
for and, when available, extracted to the preformed protocol          orally. Nutritional deliveries noted in other parts of the
concerned the ways of administering nutritional support, the          medical record were also checked and EI recalculated when
nutritional prescriptions, the predicted energy need, the en-         necessary, i.e., when the intake of PN and EN were listed
ergy expenditure measured by indirect calorimetry, and the            separately and not added together, or when intake was
EI. Moreover, patients’ body height and body weight data              registered in text and volume instead of translated into the
were extracted. When body height was not found in the                 caloric amount. Standardized tables on the energy content of
medical record, the patient, a family member, or nursing              different types of food, drinks, EN, and PN were used to
staff was contacted, the choice of contact depending on the           recalculate these protocols. When patients were on oral
recovery of the patient. Family members were asked to seek            feeding and, e.g., half a portion was registered as eaten, we
for this information in a valid passport of the patient and the       regarded this as half of the energy content of this patient’s
nursing staff was asked to measure it. Another part of the            specific diet even though it was unknown what had been left
protocol concerned factors influencing energy demands, i.e.,          on the plate, the potatoes or the meat. Information on the
other injuries, body temperature, pharmacologic sedation,             specific diets energy content per portion was supplied by the
physical anxiety, wasted residual volumes, vomiting, and              kitchen of the local hospital.
appetite, where any data available concerning this were also
extracted. The protocol also concerned the recovery of pa-            EI and BMR
tients, which is the reason all scoring results from the rating
scales GCS, Functional Independence Measure (FIM), and                    Data on the total energy expenditure according to indi-
Glasgow Outcome Scale were extracted.                                 rect calorimetry [34] were too sporadic to allow any eval-
                                                                      uation of the energy balance. When analyzing the EI of the
                                                                      patients, we related it to the basal metabolic rate (BMR),
Length of stay
                                                                      i.e., what the energy expenditure of these patients would
                                                                      have been before the trauma, while at rest and fasting. We
   The length of stay was defined as the period from the
                                                                      used the Harris-Benedict equation [35], based on admission
injury until discharge to home without any further assis-
                                                                      weight, height, age, and gender to calculate this.
tance needed, adjusted living with assistance given at home,
nursing home, or death.
                                                                      Factors with a possible effect on energy demands
Assisted nutrition and level of nutritional independence                 The length of sedation, i.e., the use of benzodiaz-
                                                                      epines, barbiturates, and propofol, was extracted to pro-
    Assisted nutrition was defined as the state when help was         tocol. Due to difficulties in evaluating the sedative effect
required for administering nutrition parenterally, enterally          retrospectively, the dosage was not specified. Body tem-
or orally. Any verbal or physical guidance needed for ini-            perature data were extracted as days of fever (ⱖ38°C) or
tiation or completion of meals was also considered as as-             hypothermia (⬍36°C).
sisted feeding, i.e., scorings ⱕ5 according to the FIM [33].             No scales to measure physical anxiety of the patients
    The FIM was the most common assessment tool used in               were identified in the records. Therefore data in this respect
scoring the actual level of independence in eating. However,          were extracted from free text in the records, e.g., from notes
FIM was used only in rehabilitation settings; some patients           on the patient being easily stressed, sweating profusely,
were not scored at all and some began eating while cared for          restless, significantly spastic, or agitated.
in other care settings. In these patients we based the re-               Vomiting and wasted residual volumes were recorded
corded level of independence on the daily nutritional notes.          and patients with such problems for ⱖ5 d were defined as
If it was stated in the nutritional notes that “the patient now       having possible upper gastrointestinal intolerance.
eats unattended and with good appetite” and the weight
development from this day did not diverge in any direction,           Malnutrition
the date for this statement was considered the time point for
when assisted feeding ended. If no FIM had been used and                 The term malnutrition is used to describe an imbalance
only scarce nutritional notes were found, we used change in           between intake and depletion that leads to over- or under-
body weight as a proxy measurement. Thus, patients with               feeding. In this study the term is used only in the sense of
considerable weight loss or weight gain were not defined as           energy deficiency, i.e., undernourishment. The anthropo-
independent in eating, although they might have been al-              metric data available to evaluate malnourishment were body
lowed to eat unassisted.                                              mass index (BMI) and weight change over time. According
                                                    K. Krakau et al. / Nutrition 23 (2007) 308 –317                                                   311
feeding after 77 ⫾ 31.3 d. The remaining four patients                        protocols of EI were mainly registered while the patients
remained dependent on gastrostomy 6 mo after injury.                          were on PN and/or EN, but when they started to eat, the
                                                                              recordings were more sparse. From the onset of oral feeding
Course of assisted feeding                                                    the daily total EI was registered in only 25% of the orally
                                                                              fed patients (n ⫽ 15/n ⫽ 59) for 8 ⫾ 8 d. Thus, data for
   From being totally dependent on assisted feeding, pa-                      delivered energy decreased over time and after 2 mo fewer
tients gradually gained more control of their nutritional                     than 10 patients could be evaluated. The analysis covers
intake. The time to the first recorded swallowing test varied                 only the first 2 mo (Fig. 3). BMR could be calculated in 57
but was mostly within 1 mo after injury (median 16 d, IQR                     patients and 2 patients had no EI registrations. This left 56
22). According to measurements of independence (FIM,                          patients to be evaluated. The EI throughout the first month
nutritional notes, or unfavorable changes in body mass), the                  was just below the calculated BMR (EI/BMR ⫽ 0.99 ⫾
period requiring assisted feeding varied a lot, from 9 to                     0.16) and stayed at 21% above BMR (EI/BMR ⫽ 1.21 ⫾
180 d (median 37.5 d, IQR 61). At 6 mo after injury 54                        0.09) during the second month.
patients (84%) had gained total nutritional independence.
This group of patients started to receive all their food orally               Change in body mass
4 to 119 d after injury (median 21 d, IQR 18). Five (8%) of
the remaining dependent patients received all their food                         Weight development was evaluated in 56 patients, but
orally but needed assistance; two (3%) were fed with a                        the frequency of measurements varied between individuals
combination of oral nutrition and EN and two could not                        and between care units, which hampered our evaluation.
swallow any food orally and were given all food enterally.                    Body weight was measured throughout the study period in
The patient who died 1 mo after injury had received PN and                    32 patients. Eleven patients were weighed initially and then
EN throughout this period.                                                    only sporadically and 13 patients were weighed only during
                                                                              the initial intensive care period. Eight patients were with-
EI in relation to BMR                                                         drawn from analysis because they were weighed no more
                                                                              than three times. Adequate data for evaluation of mean
   Energy intake recordings were done in all but two pa-                      values were restricted to the first month because the fre-
tients at an average of 31 ⫾ 38 d (range 1–176 d). Daily                      quency of weight recordings then decreased (Fig. 4).
Fig. 3. Daily mean ratio of EI to BMR during the first 2 mo after injury in 56 patients. Percentages of patients evaluated per day: 100 –50% days 1–18,
50 –25% days 19 –28, 25–14% days 29 – 60. BMR, basal metabolic rate; EI, energy intake.
                                                     K. Krakau et al. / Nutrition 23 (2007) 308 –317                                                    313
Fig. 4. Daily alteration in body mass during the first month after injury in 56 patients. Each mark represents the mean value of ratios between current and
initial body weights in the group. n, number of patients included per day.
   Compared with the first recorded measurement after 3 ⫾                       criterion 3. Fourteen of the patients fulfilled both these
2.9 d, all but four patients had initial weight loss. In eight                  high-risk criteria.
patients (14%), this was ⬍5%; in another eight, it was                              In total, the number of malnourished patients according
5–10%; and in 37 (66%), it was ⬎10%. The weight de-                             to the criteria was 38 (68%). Most patients had their lowest
crease lasted 1–2 mo after injury in most patients and was                      body weight recordings during the second month after in-
followed by a slow return toward the initial weight. Indi-                      jury (Table 2).
vidual measurements are delineated in Figure 5 and dem-
onstrate weight development during the entire study period.
                                                                                Malnourished versus non-malnourished patients
Malnourished patients
                                                                                  The malnourished and non-malnourished patients
   Anthropometric data included body mass, height, and                          were compared regarding factors that might have an
BMI. No data on nutritional status in the patients before
injury was found.
   The change in weight during the study period could be
calculated in 56 patients and the development of BMI was
possible to calculate in 53 patients. Nine patients had a BMI
⬍20 kg/m2 (mean 18.5, range 16.9 –19.9) at the time of
injury. Malnutrition was defined according to the three
high-risk criteria of the Malnutritional Universal Screening
Tool (Table 2).
   Sixteen patients fulfilled one of the low-risk criteria. No
patient had the two low-risk criteria combined, but 7 of
these 16 patients were weighed only during the period early
after injury. Thus, it is uncertain how they developed during
the proceeding hospital period.
   Fifteen patients were malnourished according to high-                        Fig. 5. Each mark represents the ratio between the current weight and
risk criterion 2, and 37 patients were according to high-risk                   initial weight in patients (n ⫽ 56) during the first 6 mo after injury.
314                                                    K. Krakau et al. / Nutrition 23 (2007) 308 –317
Table 2
Malnourishment in patients with severe traumatic brain injury according to risk criteria of the Malnutritional Universal Screening Tool
Risk criteria                            Percentage           Malnourished/total        Patients,         Patients,                   Days after injury,
                                         of patients          patients                  mean ⫾ SD         minimum–maximum             mean ⫾ SD
Low-risk criteria
  BMI 20–18.5 kg/m2                      15%                   8/53                     19.3 ⫾ 0.62       18.5–19.9                   29 ⫾ 20.4
  Weight loss 5–10%                      14%                   8/56                      6.8 ⫾ 1.4           5–8.6                    24 ⫾ 11.8
High-risk criteria
  Both low-risk criteria combined         0%                  0                         0                 0                           0
  BMI ⬍18.5 kg/m2                        28%                  15/53                     16.7 ⫾ 1.4        13.9–18.3                   48 ⫾ 26.1
  Weight loss ⬎10%                       66%                  37/56                     16.2 ⫾ 4.9        10.1–29.2                   49 ⫾ 26.5
Table 3
Proportions and differences between malnourished and non-malnourished patients
Variables                                  Dichotomized variable          Malnourished            Non-malnourished       Pearson chi-square asymptotic
                                                                          patients (n ⫽ 38)       patients (n ⫽ 18)      significance (2-sided)
Age                                        16–30                          19                      10
                                           31–64                          19                       8                     0.698
Gender                                     Women                           6                       4
                                           Men                            32                      14                     0.557
Severity                                   GCS score 3–5                  18                       9
                                           GCS score 6–8                  20                       9                     0.854
Accompanied fractures                      0 fracture                     10                      11
                                           ⱖ1 fracture                    28                       7                     0.012*
Days on sedation                           Median ⱕ12 d                   13                      15
                                           Median ⬎12 d                   24                       3                     0.001*
                                           Missing                         1
Days of hypothermia                        0d                             19                      14
                                           ⱖ1 d                           18                       4                     0.061
                                           Missing                         1
Days of fever                              Median ⱕ9 d                    13                      11
                                           Median ⬎9 d                    24                       7                     0.068
                                           Missing                         1
Days of physical anxiety                   0d                             18                      10
                                           ⱖ1 d                           20                       8                     0.567
Upper gastrointestinal intolerance         ⱕ5 d                           13                      14
                                           ⬎5 d                           25                       4                     0.002*
Length of stay                             Median ⱕ76.5 d                 12                      13
                                           Median ⬎76.5 d                 26                       5                     0.004*
Length of stay in intensive care unit      Median ⱕ17 d                   13                      12
                                           Median ⬎17 d                   25                      16                     0.023*
thus malnutrition was not unexpected [37– 40]. However,              are generally are avoided. Further, any sudden weight loss
the weight development in these patients showed that body            approximately 3 mo after injury might be due to removal of
mass continued to decrease for weeks after the early hyper-          plasters or external fixations, but there was no information
metabolic period. Presumably, the duration of hypermetab-            identified in that respect. Thus the observed weight loss of
olism was not restricted to the early postinjury period but          10 –29% in the malnourished patients is most unlikely ex-
was extended over a longer period or other factors not               plained by the regain in fluid balance or by the removal of
captured in this study mattered, as discussed below.                 external fixations or plasters.
    First, the quality of nutritional care might have been               It may also be pointed out that, to prevent deterioration
threatened by practical conditions. Ways of administering            of nutritional status, the decision to place a gastrostomy
nutrition changed frequently during the first and second             catheter should be considered at an early stage, i.e., when
months after injury and patients were often transferred be-          nutritional intake is expected to be inadequate for 2–3 wk,
tween different care units. It is a demanding task to maintain       taking the clinical situation and ethical issues of the patient
optimal nutritional care and to secure adequate information          in account [43]. In this study, 14 of the 55 enterally fed
when handing over the patients. If routines for nutritional          patients received gastrostomy at 1 mo after injury, when
assessment are missing or inadequate, this most likely en-           weight loss had already advanced. Although 10 of these
dangers the nutritional status of the patients. For instance,        patients needed gastrostomy for only a few months, it is
body height was seldom registered which is why BMI was               possible that this prevented additional weight loss because
often missed as a risk indicator for development of malnu-           repeated removals of nasogastric tubes are common during
trition. Nine patients had a BMI ⬍20 kg/m2 and one of these          stages of anxiety and confusion [44 – 46].
had a BMI ⬍18.5 kg/m2 at the time of injury. Early detec-                Special attention should probably be given to patients in
tion of low BMI is crucial because these patients may be             vegetative state because they frequently develop complica-
more vulnerable to catabolism.                                       tions that affect energy need e.g., epilepsy, dysautonomy
    Second, assessing energy need is not a standardized              (i.e., fever, tachycardia, pronounced sweating, high blood
procedure because no equation has yet been proved valid for          pressure), muscular hypertonus, infections, venous throm-
patients with severe TBI [41,42]. If indirect calorimetry            boembolism, and respiratory and gastrointestinal dysfunc-
measurements are not performed and instead generalized               tions. Energy demands of 40 – 60 kcal · kg⫺1 · d⫺1 and a
equations regarding energy need are used for calculations,           20 – 48% frequency of malnourishment have been reported
there is a risk for over- and underfeeding. In this investiga-       in this subgroup of patients [39].
tion indirect calorimetry was used in only a few patients,               Moreover, pituitary hormone deficiencies have been
sporadically, and only during the intensive care period,             identified in a substantial proportion of patients with TBI
which is the reason energy balances could not be adequately          [47– 49], causing metabolic disruptions that may affect
evaluated. However, overfeeding did not seem to be a prob-           weight development.
lem because EI during the first month covered merely the                 In our study the time needed for assisted feeding varied
BMR and thus obviously not the energy need of the patients.          greatly. This should be interpreted with caution because the
During the second month it was increased by only 21%.                timing for rating the independence at the units may not have
Energy balance was probably negative in most patients, but,          been congruent with the actual time for the patient’s inde-
because not all developed malnutrition, other factors were           pendence, which may have occurred earlier. One conspic-
important. It is also questionable whether the “indepen-             uous finding, however, was that most patients with severe
dence in eating” really tell us that the patient is able to          TBI regained their eating function within the first 6 mo after
control EI in an adequate way. We can not answer this                injury. Only a minority depended on continued assisted
question in the present investigation, but the question needs        feeding. Further, the first recorded swallowing test was done
to be asked.                                                         within 1 mo after injury. The time for the first safe oral
    Third, body mass measurements should be interpreted              feeding has been reported to be a reliable predictor of final
with some caution because various care units used different          outcome in patients with severe TBI [50]. However, be-
scales and it was not always clear whether patients were             cause the time for the first safe oral feeding could not be
weighed under standardized procedures. The recorded weight           stated from our data, its predictive value for the final out-
values were, despite their impreciseness, the ones clinicians        come could not be tested.
had based their interpretations on.
    The first body mass measurement available was per-               Limitations of the study
formed on day 3. Thus patients might then already have
gained weight due to positive fluid balance and fluid reten-            The retrospective design of this study enabled the delin-
tion. Because the first measurement serves as a basic level          eation of current nutritional treatment without interfering
in this study, the proceeding weight loss would then be              with the treatment process and the results are useful for
explained by the regaining of fluid balance. However, fluids         planning prospective studies. The findings in this study
are restricted to keep intracranial pressure down, explaining        must however consider all the weaknesses inherent in a
why extensive positive fluid balances in patients with TBI           retrospective review of medical records. Although the find-
316                                                     K. Krakau et al. / Nutrition 23 (2007) 308 –317
ings are based on a large set of detailed, clinical data,                         [7] Chiolero R, Schutz Y, Lemarchand T, Felber JP, de Tribolet N,
extracted according to a preformed protocol, factors not                              Freeman J, Jequier E. Hormonal and metabolic changes following
                                                                                      severe head injury or noncranial injury. JPEN 1989;13:5–12.
measured in clinical practice and thus not present in this
                                                                                  [8] Haider W, Lackner F, Schlick W, Benzer H, Gerstenbrand F, Irsigler
delineation may have been important for the development of                            K, et al. Metabolic changes in the course of severe acute brain
malnutrition. Moreover, data do not allow any evaluation of                           damage. Eur J Intensive Care Med 1975;1:19 –26.
the possible effect of malnutrition on complication rate or                       [9] Clifton GL, Ziegler MG, Grossman RG. Circulating catecholamines
final outcome.                                                                        and sympathetic activity after head injury. Neurosurgery 1981;8:
                                                                                      10 – 4.
                                                                                 [10] Clifton GL, Robertson CS, Grossman RG, Hodge S, Foltz R, Garza
Future studies                                                                        C. The metabolic response to severe head injury. J Neurosurg 1984;
                                                                                      60:687–96.
   Because evidence-based standards for nutritional assess-                      [11] Fell D, Benner B, Billings A, Siemens R, Harbison B, Newmark SR.
ment and treatment of patients with severe TBI are lacking,                           Metabolic profiles in patients with acute neurosurgical injuries. Crit
further studies are urgently needed. These studies should                             Care Med 1984;12:649 –52.
                                                                                 [12] Young B, Ott L, Norton J, Tibbs P, Rapp R, McClain C, Dempsey R.
define the level of EI in relation to energy expenditure                              Metabolic and nutritional sequelae in the non-steroid treated head
during a relevant period that has the best effect on outcome.                         injury patient. Neurosurgery 1985;17:784 –91.
They should also delineate the duration of catabolism. Eas-                      [13] Robertson CS, Clifton GL, Goodman JC. Steroid administration and
ily manageable assessment tools for clinical practice that                            nitrogen excretion in the head-injured patient. J Neurosurg 1985;63:
captures the diverse nutritional demands of these patients is                         714 – 8.
                                                                                 [14] Moore R, Najarian MP, Konvolinka CW. Measured energy expendi-
also a topical area for research to prevent the development
                                                                                      ture in severe head trauma. J Trauma 1989;29:1633– 6.
of malnutrition.                                                                 [15] Dickerson RN, Guenter PA, Gennarelli TA, Dempsey DT, Mullen JL.
                                                                                      Increased contribution of protein oxidation to energy expenditure in
                                                                                      head-injured patients. J Am Coll Nutr 1990;9:86 – 8.
Conclusion                                                                       [16] Bruder N, Lassegue D, Pelissier D, Graziani N, Francois G. Energy
                                                                                      expenditure and withdrawal of sedation in severe head-injured pa-
                                                                                      tients. Crit Care Med 1994;22:1114 –9.
   This investigation shows that most patients with severe                       [17] Bruder N, Raynal M, Pellissier D, Courtinat C, Francois G. Influence
TBI develop malnutrition, but also that most regain their                             of body temperature, with or without sedation, on energy expenditure
independence in eating within the first 6 months.                                     in severe head-injured patients. Crit Care Med 1998;26:568 –72.
                                                                                 [18] Feldman Z, Contant CF, Pahwa R, Goodman JC, Robertson CS,
                                                                                      Narayan RK, Grossman RG. The relationship between hormonal
                                                                                      mediators and systemic hypermetabolism after severe head injury.
Acknowledgments                                                                       J Trauma 1993;34:806 –16.
                                                                                 [19] Charlin V, Carrasco F, Ferrer L, Brito A, Poblete R. [Protein and
   The authors express their gratitude to the patients and                            energy requirements in patients with severe head injury]. Rev Med
care units that participated in this study. They also thank                           Chil 1993;121:626 –32.
Marianne Omne-Pontén for most valuable comments and                              [20] Fugazza G, Aquilani R, Iadarola P, Dossena M, Catapano M, Boschi
                                                                                      F, et al. The persistence of hypercatabolic state in rehabilitation
Håkan Källmen, Ph.D., for statistical assistance.
                                                                                      patients with complicated head injury. Eur Medicophys 1998;34:
                                                                                      125–9.
                                                                                 [21] Weekes E, Elia M. Observations on the patterns of 24-hour energy
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