Nutritional treatment of patients with severe traumatic brain injury during the first six months after injury

Nutritional treatment of patients with severe traumatic brain injury during the first six months after injury

Nutrition 23 (2007) 308 –317 www.elsevier.com/locate/nut Applied nutritional investigation Nutritional treatment of patients with severe traumatic b...

329KB Sizes 0 Downloads 64 Views

Nutrition 23 (2007) 308 –317 www.elsevier.com/locate/nut

Applied nutritional investigation

Nutritional treatment of patients with severe traumatic brain injury during the first six months after injury Karolina Krakau, B.Sc.a,b,*, Annette Hansson, B.Sc.c, Torbjörn Karlsson, M.D., Ph.D.d, Catharina Nygren de Boussard, M.D., Ph.D.b, Christer Tengvar, M.D., Ph.D.e, and Jörgen Borg, M.D., Ph.D.a a

Department of Neuroscience, Rehabilitation Medicine, Uppsala University Hospital, Uppsala, Sweden Department of Rehabilitation Medicine Stockholm, Danderyd University Hospital, Stockholm, Sweden c Department of Neurosurgical Intensive Care, Karolinska University Hospital, Stockholm, Sweden d Department of Surgical Science, Anesthesiology and Intensive Care, Uppsala University Hospital, Uppsala, Sweden e Department of Rehabilitation Medicine, Central Hospital, Västerås, Sweden b

Manuscript received September 28, 2006; accepted January 23, 2007.

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; Malnutrition

Introduction The pathophysiology of a severe traumatic brain injury (TBI) is dependent not only on the primary injury but also on unfavorable secondary events, e.g., epileptic seizures, high intracranial pressure, and fever. Early detection and treatment of such events improve outcome [1– 4]. Less is known about the effect of systemic metabolic disturbances caused by TBI, i.e., hypermetabolism and catabolism. Conclusive data show that patients with moderate and severe TBI have increased energy expenditure during the early This study was supported by the Centre for Clinical Research, Dalarna, the Department of Rehabilitation Medicine, Falu Lasarett, and Fresenius Kabi. * Corresponding author. Tel.: ⫹468-655-5484; fax: ⫹468-655-7754. E-mail address: [email protected] (K. Krakau). 0899-9007/07/$ – see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.nut.2007.01.010

postinjury period [5–22]. The increased energy demand leads to a catabolic state and a net muscle protein breakdown, with possible unfavorable effects on immune function and morbidity [23–26]. To prevent excessive muscle protein breakdown, adequate nutrition balancing the energy expenditure is crucial. There are data indicating that morbidity and mortality are decreased in patients receiving early feeding compared with those given standard nutritional treatment [25–29]. However, evidence is still not strong enough to establish a standard [30 –32], and evidence is lacking for the post–acute rehabilitation period. Moreover, the need of assisted nutrition may continue for a long period. Thus, the care will involve several units with nutritional guidelines that may differ considerably. This urges the contemporary nutritional treatment of all units caring for these patients during the intensive care period and during the early rehabilitation period to be scrutinized, as a

K. Krakau et al. / Nutrition 23 (2007) 308 –317

basis of future prospective studies. We therefore conducted a three-center, retrospective, descriptive study in Sweden to delineate the nutritional treatment of adult patients with severe TBI and to analyze their nutritional outcome during the first 6 mo after injury or until the patients were independent regarding administration of nutrition.

Materials and methods Patients The study took place in the Stockholm, Uppsala, and Gothenburg regions, with a total population of approximately 5.3 million inhabitants. All patients with TBI admitted to one of the three regional neurosurgical intensive care units during a period of 1 y (July 1, 2003 to June 30, 2004) were screened for inclusion into the study. We included patients 16 to 64 y of age with severe TBI, i.e., patients scoring 3– 8 on the Glasgow Coma Scale (GCS). To control for confounding factors such as hypothermia or intoxication, rating scores during the first 24 h were examined. In deteriorating patients, the worst score before medical sedation was recorded, and in patients improving without any interventions, the best score was recorded. Exclusion criteria were other major injuries or diseases with an influence on metabolism or nutritional treatment, as presented in the flow chart in Figure 1. Patients were contacted directly or by an authorized representative. The study was approved by the regional ethical review board of Uppsala University (Uppsala, Sweden).

309

Data collection Data were extracted from patient records covering the period from the injury until the patients became nutritionally independent or, if not, until 6 mo after injury. Data extraction and analysis aimed at answering the following questions. 1. How long was the need for parenteral nutrition (PN) and enteral nutrition (EN)? 2. How many patients received a gastrostomy? When was it placed and for how long was it needed? 3. How long was the need for assisted feeding? 4. What was the relation between energy intake (EI) and calculated basal energy metabolism? 5. How did the patients’ body mass change over time? 6. How many patients fulfilled criteria for malnourishment? 7. What was the frequency and possible effect of “important factors” in malnourished compared with nonmalnourished patients? Documentation systems varied considerably between units having different computerized and manual systems. Data sources were mainly medical and nursing records but, when available, also records kept by occupational therapists, speech-language pathologists, physiotherapists, and dietitians. Data were extracted to a preformed protocol by two of the present investigators. To secure adequate data collection, each care unit provided an experienced employee who introduced the documentation system to the investigators when they were unfamiliar with it. Further contact was made whenever data to the preformed protocol

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 place locally in all but nine units, where instead journal copies were sent for. The daily recordings made at the units were carefully examined for the selected data. The nutritional data sought for and, when available, extracted to the preformed protocol concerned the ways of administering nutritional support, the nutritional prescriptions, the predicted energy need, the energy expenditure measured by indirect calorimetry, and the EI. Moreover, patients’ body height and body weight data were extracted. When body height was not found in the medical record, the patient, a family member, or nursing staff was contacted, the choice of contact depending on the recovery of the patient. Family members were asked to seek for this information in a valid passport of the patient and the nursing staff was asked to measure it. Another part of the protocol concerned factors influencing energy demands, i.e., other injuries, body temperature, pharmacologic sedation, physical anxiety, wasted residual volumes, vomiting, and appetite, where any data available concerning this were also extracted. The protocol also concerned the recovery of patients, which is the reason all scoring results from the rating scales GCS, Functional Independence Measure (FIM), and Glasgow Outcome Scale were extracted. Length of stay The length of stay was defined as the period from the injury until discharge to home without any further assistance needed, adjusted living with assistance given at home, nursing home, or death. Assisted nutrition and level of nutritional independence Assisted nutrition was defined as the state when help was required for administering nutrition parenterally, enterally or orally. Any verbal or physical guidance needed for initiation or completion of meals was also considered as assisted feeding, i.e., scorings ⱕ5 according to the FIM [33]. The FIM was the most common assessment tool used in scoring the actual level of independence in eating. However, FIM was used only in rehabilitation settings; some patients were not scored at all and some began eating while cared for in other care settings. In these patients we based the recorded level of independence on the daily nutritional notes. If it was stated in the nutritional notes that “the patient now eats unattended and with good appetite” and the weight development from this day did not diverge in any direction, the date for this statement was considered the time point for when assisted feeding ended. If no FIM had been used and only scarce nutritional notes were found, we used change in body weight as a proxy measurement. Thus, patients with considerable weight loss or weight gain were not defined as independent in eating, although they might have been allowed to eat unassisted.

Energy intake The daily delivered intake of energy was recorded on separate nutritional protocols mainly during PN and EN periods, but occasionally even when patients were fed orally. Nutritional deliveries noted in other parts of the medical record were also checked and EI recalculated when necessary, i.e., when the intake of PN and EN were listed separately and not added together, or when intake was registered in text and volume instead of translated into the caloric amount. Standardized tables on the energy content of different types of food, drinks, EN, and PN were used to recalculate these protocols. When patients were on oral feeding and, e.g., half a portion was registered as eaten, we regarded this as half of the energy content of this patient’s specific diet even though it was unknown what had been left on the plate, the potatoes or the meat. Information on the specific diets energy content per portion was supplied by the kitchen of the local hospital. EI and BMR Data on the total energy expenditure according to indirect calorimetry [34] were too sporadic to allow any evaluation of the energy balance. When analyzing the EI of the patients, we related it to the basal metabolic rate (BMR), i.e., what the energy expenditure of these patients would have been before the trauma, while at rest and fasting. We used the Harris-Benedict equation [35], based on admission weight, height, age, and gender to calculate this. Factors with a possible effect on energy demands The length of sedation, i.e., the use of benzodiazepines, barbiturates, and propofol, was extracted to protocol. Due to difficulties in evaluating the sedative effect retrospectively, the dosage was not specified. Body temperature data were extracted as days of fever (ⱖ38°C) or hypothermia (⬍36°C). No scales to measure physical anxiety of the patients were identified in the records. Therefore data in this respect were extracted from free text in the records, e.g., from notes on the patient being easily stressed, sweating profusely, restless, significantly spastic, or agitated. Vomiting and wasted residual volumes were recorded and patients with such problems for ⱖ5 d were defined as having possible upper gastrointestinal intolerance. Malnutrition The term malnutrition is used to describe an imbalance between intake and depletion that leads to over- or underfeeding. In this study the term is used only in the sense of energy deficiency, i.e., undernourishment. The anthropometric data available to evaluate malnourishment were body mass index (BMI) and weight change over time. According

K. Krakau et al. / Nutrition 23 (2007) 308 –317

311

to the Malnutritional Universal Screening Tool [36], there is a risk for malnutrition when BMI is 18.5–20 kg/m2 or if there is an involuntary weight loss of 5–10% over 3– 6 mo and the risk for malnutrition is considered high under the following conditions. 1. Both of the previously mentioned risk factors occur at the same time. 2. The BMI is ⬍18.5 kg/m2. 3. Involuntary weight loss exceeds 10%. Patients in this study were considered malnourished when any of these three high-risk criteria was met. Statistical analysis In text, diagrams, and tables, the frequencies and quote data are presented as mean ⫾ SD or, with non-normal distributions, as median and interquartile range (IQR). Clinical factors that might influence body mass were analyzed by comparing malnourished with non-malnourished patients. These variables were tested for association by use of Pearson chi-square test, defining statistically significant differences at P ⬍ 0.05.

Results Demographics, injury data, and levels of care Patient characteristics are summarized in Table 1. Almost 50% (29 of 64) of the patients exhibited GCS scores within the lowest part of the severity range, i.e., 3 to 5. The most common injury mechanisms were traffic accidents

Table 1 Patient and injury characteristics* Age (y) Women Men Body mass (kg) Height (cm) BMI (kg/m2) Isolated EDH or SDH Cerebral contusion and other brain injuries GCS score 3–5 GCS score 6–8 No fractures ⱖ1 fracture Total LOS (d) LOS in ICU (d) LOS in different ward settings (d) LOS in rehabilitation unit (d)

Fig. 2. Number of patients receiving PN or EN or capable of OF during the first 6 mo after injury. EN, enteral nutrition; OF, oral feeding; PN, parenteral nutrition.

(45%) and falls (22%); less common were assaults and sports or other injuries. Total length of hospital stay was 9 to 356 d and number of care units during this period was three to eight. During the first 2 mo, there were 4.7 ⫾ 0.96 transferals between different care units per patient. For most patients (73%), time in the hospital included three periods: an intensive care period followed by a period in different ward settings, mainly surgical or medical wards but also orthopedic care, psychiatric care, and nursing homes, and then in a specialized rehabilitation setting. Six patients went straight from intensive care units to rehabilitation, whereas 11 patients were never transferred to a rehabilitation setting. At discharge from hospital care, 64% of patients (n ⫽ 41) were able to go home without any assistance, whereas 22% (n ⫽ 14) needed further assistance at home. Eight patients (12.5%) were discharged to nursing homes and one patient died during hospital stay 1 mo after injury due to a major stroke. Duration of PN and EN

35 ⫾ 15.7 11 53 75 ⫾ 12.6 178 ⫾ 8.4 24 ⫾ 4.3 12 52 29 35 25 39 76.5 (95) 17 (14) 17 (15) 55 (68)

BMI, body mass index; EDH, epidural hematoma; GCS, Glasgow Coma Scale; ICU, intensive care unit; LOS, length of stay; SDH, subdural hematoma * Values are presented as numbers, mean ⫾ SD, or median (interquartile range).

All patients received PN while in the intensive care unit. The total number of days on PN was 2 to 64 d (19 ⫾ 12.2 d). Most patients (86%) also received EN, whereas 14% never had EN and could start oral feeding immediately after PN. EN started 4 ⫾ 2.9 d after injury and the total days of EN varied between 1 and 178 (median 14 d, IQR 33) during the first 6 mo after injury. As demonstrated in Figure 2, change in the way of administering nutrition was most frequent during the first month. After approximately 3 mo, a final change had been made in most patients (⬎90%), but a few patients continued to make progress in this respect up to 5 mo after injury. Use of gastrostomy Fifty-five patients received EN and 14 of these patients received a gastrostomy approximately 1 mo after injury (31 ⫾ 8.6 d). Ten of these patients could return to total oral

312

K. Krakau et al. / Nutrition 23 (2007) 308 –317

feeding after 77 ⫾ 31.3 d. The remaining four patients remained dependent on gastrostomy 6 mo after injury. Course of assisted feeding From being totally dependent on assisted feeding, patients gradually gained more control of their nutritional intake. The time to the first recorded swallowing test varied but was mostly within 1 mo after injury (median 16 d, IQR 22). According to measurements of independence (FIM, nutritional notes, or unfavorable changes in body mass), the period requiring assisted feeding varied a lot, from 9 to 180 d (median 37.5 d, IQR 61). At 6 mo after injury 54 patients (84%) had gained total nutritional independence. This group of patients started to receive all their food orally 4 to 119 d after injury (median 21 d, IQR 18). Five (8%) of the remaining dependent patients received all their food orally but needed assistance; two (3%) were fed with a combination of oral nutrition and EN and two could not swallow any food orally and were given all food enterally. The patient who died 1 mo after injury had received PN and EN throughout this period. EI in relation to BMR Energy intake recordings were done in all but two patients at an average of 31 ⫾ 38 d (range 1–176 d). Daily

protocols of EI were mainly registered while the patients were on PN and/or EN, but when they started to eat, the recordings were more sparse. From the onset of oral 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 delivered energy decreased over time and after 2 mo fewer than 10 patients could be evaluated. The analysis covers only the first 2 mo (Fig. 3). BMR could be calculated in 57 patients and 2 patients had no EI registrations. This left 56 patients to be evaluated. The EI throughout the first month was just below the calculated BMR (EI/BMR ⫽ 0.99 ⫾ 0.16) and stayed at 21% above BMR (EI/BMR ⫽ 1.21 ⫾ 0.09) during the second month. Change in body mass Weight development was evaluated in 56 patients, but the frequency of measurements varied between individuals and between care units, which hampered our evaluation. Body weight was measured throughout the study period in 32 patients. Eleven patients were weighed initially and then only sporadically and 13 patients were weighed only during the initial intensive care period. Eight patients were withdrawn from analysis because they were weighed no more than three times. Adequate data for evaluation of mean values were restricted to the first month because the frequency 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 ⫾ 2.9 d, all but four patients had initial weight loss. In eight patients (14%), this was ⬍5%; in another eight, it was 5–10%; and in 37 (66%), it was ⬎10%. The weight decrease lasted 1–2 mo after injury in most patients and was followed by a slow return toward the initial weight. Individual measurements are delineated in Figure 5 and demonstrate weight development during the entire study period.

criterion 3. Fourteen of the patients fulfilled both these high-risk criteria. In total, the number of malnourished patients according to the criteria was 38 (68%). Most patients had their lowest body weight recordings during the second month after injury (Table 2). Malnourished versus non-malnourished patients

Malnourished patients Anthropometric data included body mass, height, and 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 highrisk criterion 2, and 37 patients were according to high-risk

The malnourished and non-malnourished patients were compared regarding factors that might have an

Fig. 5. Each mark represents the ratio between the current weight and 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 Low-risk criteria BMI 20–18.5 kg/m2 Weight loss 5–10% High-risk criteria Both low-risk criteria combined BMI ⬍18.5 kg/m2 Weight loss ⬎10%

Percentage of patients

Malnourished/total patients

Patients, mean ⫾ SD

Patients, minimum–maximum

Days after injury, mean ⫾ SD

15% 14%

8/53 8/56

19.3 ⫾ 0.62 6.8 ⫾ 1.4

18.5–19.9 5–8.6

29 ⫾ 20.4 24 ⫾ 11.8

0% 28% 66%

0 15/53 37/56

0 16.7 ⫾ 1.4 16.2 ⫾ 4.9

0 13.9–18.3 10.1–29.2

0 48 ⫾ 26.1 49 ⫾ 26.5

BMI, body mass index

effect. There was no difference in age, gender, severity, days of hypothermia, fever, or days of physical anxiety between malnourished and non-malnourished patients (Table 3). However, associated fractures, days on sedation, upper gastrointestinal intolerance, length of stay, and length of stay in an intensive care unit differed between groups. Energy intake data according to the nutritional protocols could be compared only 18 d after injury because the nutritional protocols in non-malnourished patients ended by then. During this time, the two groups were given the same amount of energy in relation to BMR.

Discussion Findings The two main findings of this detailed, retrospective review of medical records were that 68% of patients with severe TBI exhibited signs of malnutrition extending to the second month after injury and that 84% became nutritionally independent within the first 6 mo after injury. The increased risk associated with hypermetabolism in patients with severe TBI during the first weeks after injury has been extensively described in the literature [5–22] and

Table 3 Proportions and differences between malnourished and non-malnourished patients Variables

Dichotomized variable

Malnourished patients (n ⫽ 38)

Non-malnourished patients (n ⫽ 18)

Age

16–30 31–64 Women Men GCS score 3–5 GCS score 6–8 0 fracture ⱖ1 fracture Median ⱕ12 d Median ⬎12 d Missing 0d ⱖ1 d Missing Median ⱕ9 d Median ⬎9 d Missing 0d ⱖ1 d ⱕ5 d ⬎5 d Median ⱕ76.5 d Median ⬎76.5 d Median ⱕ17 d Median ⬎17 d

19 19 6 32 18 20 10 28 13 24 1 19 18 1 13 24 1 18 20 13 25 12 26 13 25

10 8 4 14 9 9 11 7 15 3

Gender Severity Accompanied fractures Days on sedation

Days of hypothermia

Days of fever

Days of physical anxiety Upper gastrointestinal intolerance Length of stay Length of stay in intensive care unit GCS, Glasgow Coma Scale * P ⬍ 0.05.

Pearson chi-square asymptotic significance (2-sided) 0.698 0.557 0.854 0.012* 0.001*

14 4

0.061

11 7

0.068

10 8 14 4 13 5 12 16

0.567 0.002* 0.004* 0.023*

K. Krakau et al. / Nutrition 23 (2007) 308 –317

thus malnutrition was not unexpected [37– 40]. However, the weight development in these patients showed that body mass continued to decrease for weeks after the early hypermetabolic period. Presumably, the duration of hypermetabolism was not restricted to the early postinjury period but was extended over a longer period or other factors not captured in this study mattered, as discussed below. First, the quality of nutritional care might have been threatened by practical conditions. Ways of administering nutrition changed frequently during the first and second months after injury and patients were often transferred between different care units. It is a demanding task to maintain optimal nutritional care and to secure adequate information when handing over the patients. If routines for nutritional assessment are missing or inadequate, this most likely endangers the nutritional status of the patients. For instance, body height was seldom registered which is why BMI was often missed as a risk indicator for development of malnutrition. Nine patients had a BMI ⬍20 kg/m2 and one of these had a BMI ⬍18.5 kg/m2 at the time of injury. Early detection of low BMI is crucial because these patients may be more vulnerable to catabolism. Second, assessing energy need is not a standardized procedure because no equation has yet been proved valid for patients with severe TBI [41,42]. If indirect calorimetry measurements are not performed and instead generalized equations regarding energy need are used for calculations, there is a risk for over- and underfeeding. In this investigation indirect calorimetry was used in only a few patients, sporadically, and only during the intensive care period, which is the reason energy balances could not be adequately evaluated. However, overfeeding did not seem to be a problem because EI during the first month covered merely the BMR and thus obviously not the energy need of the patients. During the second month it was increased by only 21%. Energy balance was probably negative in most patients, but, because not all developed malnutrition, other factors were important. It is also questionable whether the “independence in eating” really tell us that the patient is able to control EI in an adequate way. We can not answer this question in the present investigation, but the question needs to be asked. Third, body mass measurements should be interpreted with some caution because various care units used different scales and it was not always clear whether patients were weighed under standardized procedures. The recorded weight values were, despite their impreciseness, the ones clinicians had based their interpretations on. The first body mass measurement available was performed on day 3. Thus patients might then already have gained weight due to positive fluid balance and fluid retention. Because the first measurement serves as a basic level in this study, the proceeding weight loss would then be explained by the regaining of fluid balance. However, fluids are restricted to keep intracranial pressure down, explaining why extensive positive fluid balances in patients with TBI

315

are generally are avoided. Further, any sudden weight loss approximately 3 mo after injury might be due to removal of plasters or external fixations, but there was no information identified in that respect. Thus the observed weight loss of 10 –29% in the malnourished patients is most unlikely explained by the regain in fluid balance or by the removal of external fixations or plasters. It may also be pointed out that, to prevent deterioration of nutritional status, the decision to place a gastrostomy catheter should be considered at an early stage, i.e., when nutritional intake is expected to be inadequate for 2–3 wk, taking the clinical situation and ethical issues of the patient in account [43]. In this study, 14 of the 55 enterally fed patients received gastrostomy at 1 mo after injury, when weight loss had already advanced. Although 10 of these patients needed gastrostomy for only a few months, it is possible that this prevented additional weight loss because repeated removals of nasogastric tubes are common during stages of anxiety and confusion [44 – 46]. Special attention should probably be given to patients in vegetative state because they frequently develop complications that affect energy need e.g., epilepsy, dysautonomy (i.e., fever, tachycardia, pronounced sweating, high blood pressure), muscular hypertonus, infections, venous thromboembolism, and respiratory and gastrointestinal dysfunctions. Energy demands of 40 – 60 kcal · kg⫺1 · d⫺1 and a 20 – 48% frequency of malnourishment have been reported in this subgroup of patients [39]. Moreover, pituitary hormone deficiencies have been identified in a substantial proportion of patients with TBI [47– 49], causing metabolic disruptions that may affect weight development. In our study the time needed for assisted feeding varied greatly. This should be interpreted with caution because the timing for rating the independence at the units may not have been congruent with the actual time for the patient’s independence, which may have occurred earlier. One conspicuous finding, however, was that most patients with severe TBI regained their eating function within the first 6 mo after injury. Only a minority depended on continued assisted feeding. Further, the first recorded swallowing test was done within 1 mo after injury. The time for the first safe oral feeding has been reported to be a reliable predictor of final outcome in patients with severe TBI [50]. However, because the time for the first safe oral feeding could not be stated from our data, its predictive value for the final outcome could not be tested. Limitations of the study The retrospective design of this study enabled the delineation of current nutritional treatment without interfering with the treatment process and the results are useful for planning prospective studies. The findings in this study must however consider all the weaknesses inherent in a 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, extracted according to a preformed protocol, factors not measured in clinical practice and thus not present in this delineation may have been important for the development of malnutrition. Moreover, data do not allow any evaluation of the possible effect of malnutrition on complication rate or final outcome. Future studies Because evidence-based standards for nutritional assessment and treatment of patients with severe TBI are lacking, further studies are urgently needed. These studies should define the level of EI in relation to energy expenditure during a relevant period that has the best effect on outcome. They should also delineate the duration of catabolism. Easily manageable assessment tools for clinical practice that captures the diverse nutritional demands of these patients is also a topical area for research to prevent the development of malnutrition.

Conclusion This investigation shows that most patients with severe TBI develop malnutrition, but also that most regain their independence in eating within the first 6 months.

Acknowledgments The authors express their gratitude to the patients and care units that participated in this study. They also thank Marianne Omne-Pontén for most valuable comments and Håkan Källmen, Ph.D., for statistical assistance.

References [1] Elf K, Nilsson P, Enblad P. Outcome after traumatic brain injury improved by an organized secondary insult program and standardized neurointensive care. Crit Care Med 2002;30:2129 –34. [2] Signorini DF, Andrews PJ, Jones PA, Wardlaw JM, Miller JD. Adding insult to injury: the prognostic value of early secondary insults for survival after traumatic brain injury. J Neurol Neurosurg Psychiatry 1999;66:26 –31. [3] Becker DP, Miller JD, Ward JD, Greenberg RP, Young HF, Sakalas R. The outcome from severe head injury with early diagnosis and intensive management. J Neurosurg 1977;47:491–502. [4] Elf K, Nilsson P, Ronne-Engstrom E, Howells T, Enblad P. Cerebral perfusion pressure between 50 and 60 mm Hg may be beneficial in head-injured patients: a computerized secondary insult monitoring study. Neurosurgery 2005;56:962–71. [5] McCall M, Jeejeebhoy K, Pencharz P, Moulton R. Effect of neuromuscular blockade on energy expenditure in patients with severe head injury. JPEN 2003;27:27–35. [6] Bruder N, Dumont JC, Francois G. Evolution of energy expenditure and nitrogen excretion in severe head-injured patients. Crit Care Med 1991;19:43– 8.

[7] Chiolero R, Schutz Y, Lemarchand T, Felber JP, de Tribolet N, Freeman J, Jequier E. Hormonal and metabolic changes following severe head injury or noncranial injury. JPEN 1989;13:5–12. [8] Haider W, Lackner F, Schlick W, Benzer H, Gerstenbrand F, Irsigler K, et al. Metabolic changes in the course of severe acute brain damage. Eur J Intensive Care Med 1975;1:19 –26. [9] Clifton GL, Ziegler MG, Grossman RG. Circulating catecholamines and sympathetic activity after head injury. Neurosurgery 1981;8: 10 – 4. [10] Clifton GL, Robertson CS, Grossman RG, Hodge S, Foltz R, Garza C. The metabolic response to severe head injury. J Neurosurg 1984; 60:687–96. [11] Fell D, Benner B, Billings A, Siemens R, Harbison B, Newmark SR. Metabolic profiles in patients with acute neurosurgical injuries. Crit Care Med 1984;12:649 –52. [12] Young B, Ott L, Norton J, Tibbs P, Rapp R, McClain C, Dempsey R. Metabolic and nutritional sequelae in the non-steroid treated head injury patient. Neurosurgery 1985;17:784 –91. [13] Robertson CS, Clifton GL, Goodman JC. Steroid administration and nitrogen excretion in the head-injured patient. J Neurosurg 1985;63: 714 – 8. [14] Moore R, Najarian MP, Konvolinka CW. Measured energy expenditure in severe head trauma. J Trauma 1989;29:1633– 6. [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. [16] Bruder N, Lassegue D, Pelissier D, Graziani N, Francois G. Energy expenditure and withdrawal of sedation in severe head-injured patients. Crit Care Med 1994;22:1114 –9. [17] Bruder N, Raynal M, Pellissier D, Courtinat C, Francois G. Influence of body temperature, with or without sedation, on energy expenditure 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. J Trauma 1993;34:806 –16. [19] Charlin V, Carrasco F, Ferrer L, Brito A, Poblete R. [Protein and energy requirements in patients with severe head injury]. Rev Med Chil 1993;121:626 –32. [20] Fugazza G, Aquilani R, Iadarola P, Dossena M, Catapano M, Boschi F, et al. The persistence of hypercatabolic state in rehabilitation patients with complicated head injury. Eur Medicophys 1998;34: 125–9. [21] Weekes E, Elia M. Observations on the patterns of 24-hour energy expenditure changes in body composition and gastric emptying in head-injured patients receiving nasogastric tube feeding. JPEN 1996; 20:31–7. [22] Raurich JM, Ibanez J. Metabolic rate in severe head trauma. JPEN 1994;18:521– 4. [23] Quattrocchi KB, Issel BW, Miller CH, Frank EH, Wagner FC Jr. Impairment of helper T-cell function following severe head injury. J Neurotrauma 1992;9:1–9. [24] Wolach B, Sazbon L, Gavrieli R, Broda A, Schlesinger M. Early immunological defects in comatose patients after acute brain injury. J Neurosurg 2001;94:706 –11. [25] Minard G, Kudsk KA, Melton S, Patton JH, Tolley EA. Early versus delayed feeding with an immune-enhancing diet in patients with severe head injuries. JPEN 2000;24:145–9. [26] Sacks GS, Brown RO, Teague D, Dickerson RN, Tolley EA, Kudsk KA. Early nutrition support modifies immune function in patients sustaining severe head injury. JPEN 1995;19:387–92. [27] Young B, Ott L, Haack D, Twyman D, Combs D, Oexmann JB, et al. Effect of total parenteral nutrition upon intracranial pressure in severe head injury. J Neurosurg 1987;67:76 – 80. [28] Taylor SJ, Fettes SB, Jewkes C, Nelson RJ. Prospective, randomized, controlled trial to determine the effect of early enhanced enteral

K. Krakau et al. / Nutrition 23 (2007) 308 –317

[29]

[30]

[31]

[32]

[33]

[34]

[35] [36] [37] [38]

[39]

nutrition on clinical outcome in mechanically ventilated patients suffering head injury. Crit Care Med 1999;27:2525–31. Rapp RP, Young B, Twyman D, Bivins BA, Haack D, Tibbs PA, Bean JR. The favorable effect of early parenteral feeding on survival in head-injured patients. J Neurosurg 1983;58:906 –12. Krakau K, Omne-Ponten M, Karlsson T, Borg J. Metabolism and nutrition in patients with moderate and severe traumatic brain injury: a systematic review. Brain Inj 2006;20:345– 67. Brain Trauma Foundation, American Association of Neurological Surgeons, Joint Section on Neurotrauma and Critical Care. Nutrition. J Neurotrauma 2000;17:539 – 47. Yanagawa T, Bunn F, Roberts I, Wentz R, Pierro A. Nutritional support for head-injured patients. Cochrane Database Syst Rev 2002: CD001530. Kidd D, Stewart G, Baldry J, Johnson J, Rossiter D, Petruckevitch A, Thompson AJ. The Functional Independence Measure: a comparative validity and reliability study. Disabil Rehabil 1995;17:10 – 4. Branson RD. The measurement of energy expenditure: Instrumentation, practical considerations and clinical application. Respir Care 1990;35:640 –59. Harris J, Benedict F. A biometric study of basal metabolism in man. Washington D.C.: Carnegie Institute of Washington, 1919;223–50. Kondrup J, Allison SP, Elia M, Vellas B, Plauth M. ESPEN guidelines for nutrition screening 2002. Clin Nutr 2003;22:415–21. Denes Z. The influence of severe malnutrition on rehabilitation in patients with severe head injury. Disabil Rehabil 2004;26:1163–5. Aquilani R, Viglio S, Iadarola P, Guarnaschelli C, Arrigoni N, Fugazza G, et al. Peripheral plasma amino acid abnormalities in rehabilitation patients with severe brain injury. Arch Phys Med Rehabil 2000;81:176 – 81. Dolce G, Sazbon L. The post-traumatic vegetative state. Stuttgard: Thieme; 2002, p. 22.

317

[40] Thomson MA, Carver AD, Sloan RL. Nutritional status of traumatic and anoxic brain-injured patients on admission to rehabilitation (abstract). Proc Nutr Soc Lond 2000;60:83A. [41] Sunderland PM, Heilbrun MP. Estimating energy expenditure in traumatic brain injury: comparison of indirect calorimetry with predictive formulas. Neurosurgery 1992;31:246 –53. [42] Clifton GL, Robertson CS, Choi SC. Assessment of nutritional requirements of head-injured patients. J Neurosurg 1986;64:895–901. [43] Loser C, Aschl G, Hebuterne X, Mathus-Vliegen EM, Muscaritoli M, Niv Y, et al. ESPEN guidelines on artificial enteral nutrition— percutaneous endoscopic gastrostomy (PEG). Clin Nutr 2005;24: 848 – 61. [44] Stechmiller J, Treloar DM, Derrico D, Yarandi H, Guin P. Interruption of enteral feedings in head injured patients. J Neurosci Nurs 1994;26:224 –9. [45] Ott L, Annis K, Hatton J, McClain M, Young B. Postpyloric enteral feeding costs for patients with severe head injury: blind placement, endoscopy, and PEG/J versus TPN. J Neurotrauma 1999;16:233– 42. [46] Klodell CT, Carroll M, Carrillo EH, Spain DA. Routine intragastric feeding following traumatic brain injury is safe and well tolerated. Am J Surg 2000;179:168 –71. [47] Aimaretti G, Ambrosio MR, Di Somma C, Gasperi M, Cannavo S, Scaroni C, et al. Hypopituitarism induced by traumatic brain injury in the transition phase. J Endocrinol Invest 2005;28:984 –9. [48] Benvenga S, Campenni A, Ruggeri RM, Trimarchi F. Clinical review 113: hypopituitarism secondary to head trauma. J Clin Endocrinol Metab 2000;85:1353– 61. [49] Lieberman SA, Oberoi AL, Gilkison CR, Masel BE, Urban RJ. Prevalence of neuroendocrine dysfunction in patients recovering from traumatic brain injury. J Clin Endocrinol Metab 2001;86:2752– 6. [50] Formisano R, Voogt RD, Buzzi MG, Vinicola V, Penta F, Peppe A, Stanzione P. Time interval of oral feeding recovery as a prognostic factor in severe traumatic brain injury. Brain Inj 2004;18:103–9.