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Increased Resting Energy Expenditure after Endovascular Coiling for Subarachnoid Hemorrhage
ARTICLE IN PRESS
Increased Resting Energy Expenditure after Endovascular Coiling for Subarachnoid Hemorrhage Ayano Nagano, RN,* Yoshitaka Yamada, MD, PhD,† Hiroji Miyake, MD, Kazuhisa Domen, MD, PhD,‡ and Tetsuo Koyama, MD, PhD‡§
PhD,†
Background: Appropriate nutritional care from the acute stage is essential for improved functional outcomes and reduced mortality in patients with subarachnoid hemorrhage (SAH). Although endovascular coiling is increasingly being used as an alternative to neurosurgical clipping and craniotomy for ruptured aneurysms, the resting energy expenditure (REE) of patients treated with this new technique has not been systemically evaluated. Methods: We measured REE values by indirect calorimetry in 12 SAH patients treated with endovascular coiling. We averaged the REE measurements obtained on days 1 and 7 after endovascular coiling, and then we statistically compared the mean REE values with those in 30 patients with acute cerebral infarction (ACI) by the Wilcoxon rank-sum test (P < .05). Next, we calculated the ratio of measured REE values to the values estimated using the Harris– Benedict equation to adjust for demographic differences in sex, weight, height, and age between the groups. Results: The ratios were significantly higher in SAH patients (median value, 1.12; interquartile range, 1.05-1.23) than in ACI patients (median value, 1.02; interquartile range, .97-1.09). Conclusions: Because endovascular coiling is less invasive than neurosurgical clipping, the observed increase in REE was attributed to metabolic changes after SAH. To provide optimal nutritional care to SAH patients from the acute stage, clinicians should be aware of this change in REE. Key Words: Diet—embolization—metabolism—nutrition—stroke. © 2015 National Stroke Association. Published by Elsevier Inc. All rights reserved.
Introduction Appropriate nutritional care is critically important for stroke patients to achieve better functional outcome and From the *Department of Nursing Care, Nishinomiya Kyoritsu Neurosurgical Hospital, Hyogo, Japan; †Department of Neurosurgery, Nishinomiya Kyoritsu Neurosurgical Hospital, Hyogo, Japan; ‡Department of Rehabilitation Medicine, Hyogo College of Medicine, Hyogo, Japan; and §Department of Rehabilitation Medicine, Nishinomiya Kyoritsu Neurosurgical Hospital, Hyogo, Japan. Received November 9, 2015; accepted December 10, 2015. Grant support: This research was supported in part by a Grantin-Aid for Scientific Research (B) from the Japan Society for the Promotion of Science (KAKENHI [25282168]). Address correspondence to Ayano Nagano, RN, Department of Nursing Care, Nishinomiya Kyoritsu Neurosurgical Hospital, 11-1 Imazu-Yamanaka-cho, Nishinomiya, Hyogo 663-8211, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter © 2015 National Stroke Association. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.12.008
reduced mortality.1,2 Metabolic parameters such as resting energy expenditure (REE) differ depending upon the type of stroke and severity of symptoms.3,4 Subarachnoid hemorrhage (SAH) is one of the most severe types of stroke and often requires surgical and/or endovascular intervention, and is associated with hypermetabolism during the acute stage.5,6 However, previous studies included only patients who had undergone conventional procedures such as neurosurgical clipping and craniotomy, which often lead to hypermetabolism due to their invasiveness. However, treatment for SAH has changed in the last decade. Endovascular coiling, a less invasive procedure than neurosurgical clipping or craniotomy, is increasingly being used as an alternative treatment for ruptured intracranial aneurysms.7 However, to our knowledge, no studies have investigated REE in patients treated with endovascular coiling for SAH due to a ruptured aneurysm. The aim of this study was to evaluate REE in the acute care setting among patients with SAH treated with endovascular coiling.
Journal of Stroke and Cerebrovascular Diseases, Vol. ■■, No. ■■ (■■), 2015: pp ■■–■■
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Materials and Methods Patients The present study included patients who were diagnosed as having SAH and who underwent endovascular coiling for ruptured intracranial aneurysm at Nishinomiya Kyoritsu Neurosurgical Hospital from April 2014 to February 2015. The diagnosis of SAH and the location of the aneurysm were confirmed by computed tomography, magnetic resonance angiography, and computed tomography angiography on admission. The severity of SAH was classified according to the World Federation of Neurological Surgeons (WFNS) Scale8 and the Hunt and Kosnik scale.9 On admission, weight was measured by using a patient lift scale and height was measured in the supine position. To minimize variability arising from differences in endovascular intervention technique, we included only patients who were treated by a single neurosurgeon (Y.Y., the second author of this article). Endovascular coiling was performed within 2 days of SAH onset in all patients. Exclusion criteria were as follows: (1) oxygen therapy or ventilator dependence; (2) conditions associated with altered energy metabolism (e.g., fever >38°C, poorly controlled diabetes mellitus, advanced cancer, sepsis); (3) coma; (4) restlessness; and (5) refusal of indirect calorimetry measurements. A total of 17 SAH patients were recruited. Among them, five were excluded from the analysis based on the exclusion criteria (3 patients were dependent on a ventilator and 2 patients were receiving oxygen therapy).
Controls Thirty patients with acute cerebral infarction (ACI) who were hospitalized during the same period as those with SAH were used as a control group. The details of these 30 patients have been previously reported.10 Briefly, the control group comprised patients who lived independently in their community before stroke onset, and whose severity of stroke symptoms on admission was between 4 and 25 according to the National Institutes of Health Stroke Scale. Patients who subsequently required acute medical services were excluded.
measurements were conducted for 15 minutes, and the first 5 minutes of data were discarded.12 Heart rate, respiratory rate, and blood pressure were monitored during the measurement process. Data collected on days 1 and 7 after endovascular coiling were averaged, and the mean was used in statistical analysis. The measurement procedures were nearly identical for the control subjects, as previously reported.10 REE is dependent on age, sex, weight, height, and other variables.13,14 In the present study, in addition to indirect calorimetry measurements, we also estimated REE values derived from the Harris–Benedict equation. This equation is the most widely used predictive equation for estimating REE in a wide variety of clinical settings, including acute stroke care,15 and it is used to calculate REE (kilocalorie) as follows:
Men: 13.75 × Weight (kg ) + 5 × Height (cm ) − 6.76 × Age (years ) + 66.47
Women: 9.56 × Weight (kg ) + 1.85 × Height (cm ) − 4.86 × Age (years ) + 655.1
The calculated values were then used to adjust REE values for differences in sex, weight, height, and age between the SAH and ACI groups.
Statistical Analysis The aim of the present study was to evaluate REE among patients with SAH in the acute care setting relative to patients with ACI. To accomplish this, we adjusted for the differences in patient characteristics using the Harris–Benedict equation. In this procedure, the ratio of the measured REE value obtained using indirect calorimetry to the estimated value obtained using the Harris– Benedict equation was calculated for each patient to adjust for age, sex, weight, and height. This ratio was then used to compare the SAH and ACI groups using the Wilcoxon rank-sum test. To compare the profiles of the patients in the SAH and ACI (control) groups, we used the Pearson chi-square test for categorical data and the Wilcoxon rank-sum test for interval data. A P value less than .05 was considered statistically significant.
Metabolic Measurement We assessed REE by indirect calorimetry using a portable metabolic analyzer designed to measure oxygen consumption and energy expenditure (FitMate Metabolic System, COSMED, Rome, Italy). Measurements were performed on days 1 and 7 after endovascular coiling, between 6 a.m. and 8 a.m. at least 9 hours after meal consumption.11 The patients rested in the supine position for at least 30 minutes before each measurement and were instructed to breathe normally, but not to talk, move, or sleep during the measurement. The gas analyzer was automatically calibrated before each measurement. All
Ethical Considerations The study protocol was approved by the Institutional Review Board of Hyogo College of Medicine. Written informed consent for inclusion in the study was obtained from all patients or their family members.
Results The profiles of the 12 patients (9 women, 3 men; median age, 54.5 years; age range, 35-84 years; median weight, 54.7 kg; weight range, 43.1-96.1 kg; mean height, 153 cm;
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Table 1. Characteristics of patients with SAH
No.
Age (years)
Sex
Aneurysm
Weight (kg)
Height (cm)
mRS
H&K
WFNS
Indirect calorimetry (kcal)
H-B (kcal)
Indirect calorimetry/H-B
1 2 3 4 5 6 7 8 9 10 11 12
36 42 84 65 75 83 51 70 58 35 39 47
F F F F F F M F F F M M
Lt IC-PC Rt IC-PC BA Lt SCA Rt ACA Rt ICA Lt ICA A-com Rt VA-PICA A-com Rt MCA Rt VA Rt IP-PC
43.1 52.0 46.4 54.1 62.8 55.0 52.0 59.3 75.8 54.3 77.0 96.1
154 155 149 149 152 151 168 158 145 150 174 170
2 2 5 5 5 3 2 5 3 3 5 3
2 1 3 3 4 2 1 4 2 3 5 2
1 1 2 2 4 1 1 4 2 2 5 1
1015 1035 1132 1204 1302 1363 1454 1457 1632 1684 1916 2010
1177 1235 966 1132 1172 1057 1277 1174 1366 1282 1732 1920
.862 .838 1.171 1.063 1.111 1.290 1.139 1.241 1.195 1.314 1.106 1.047
Abbreviations: ACA, anterior cerebellar artery; A-com, anterior communicating artery; BA, basilar artery; F, female; H&K, Hunt and Kosnik scale; H-B, Harris–Benedict equation; ICA, internal carotid artery; IC-PC, internal carotid–posterior cerebral artery; Lt, left; M, male; MCA, middle cerebellar artery; mRS, modified Rankin scale; PICA, posterior inferior cerebellar artery; Rt, right; SAH, subarachnoid hemorrhage; SCA, superior cerebellar artery; VA, vertebral artery; WFNS, World Federation of Neurological Surgeons Scale. Patients were ordered 1-12 in accordance with indirect calorimetry values (lowest to highest).
Table 2. Comparison of patient characteristics between the SAH and ACI groups
M/F Age (years) Weight (kg) Height (cm)
SAH
ACI
P
3/9 Median, 54.5; IQR, 39.8-73.8 Median, 54.7; IQR, 52.0-72.6 Median, 153.0; IQR, 149.3-165.5
12/18 Median, 79.5; IQR, 72.0-87.3 Median, 50.4; IQR, 45.6-59.7 Median, 152.5; IQR. 145.8-163.5
.359 <.001 .164 .531
Abbreviations: ACI, acute cerebral infarct; F, female; IQR, interquartile range; M, male; SAH, subarachnoid aneurysm.
height range, 145-174 cm) are shown in Table 1. Indirect calorimetry values ranged from 1015 to 2010 kcal (median, 1409), modified Rankin scale scores ranged from 2 to 5 (median, 3), Hunt and Kosnik scores ranged from 1 to 5 (median, 2.5), and WFNS scores ranged from 1 to 5 (median 2). The results of statistical comparisons of patients’ profiles between the SAH and ACI groups are shown in Table 2. No significant differences were seen in sex ratio, weight, or height between the groups; however, patients in the SAH group were significantly younger than those in the ACI group. A scatterplot of the REE values measured by indirect calorimetry and the estimated Harris–Benedict values for the SAH and ACI groups is shown in Figure 1. The line with slope of 1 indicates a perfect fit where actual REE values are identical to those estimated using the Harris– Benedict equation. Plots for the control ACI group were distributed evenly around the line. In contrast, most (10 of 12) of the plots for the SAH patients were above the line. It is worth noting that actual REE values (vertical axis) increased proportionally with the estimated values (horizontal axis) in SAH patients. Figure 2 shows the results of direct statistical comparison of the ratio of actual REE values to the estimated values between the SAH and ACI
Figure 1. Scatterplot showing the relationship between actual REE values obtained using indirect calorimetry (vertical axis, kilocalorie) and estimated REE values derived from the Harris–Benedict equation (horizontal axis, kilocalorie). Ellipses indicate the 50% density distribution and the line with slope of 1 indicates a perfect fit where the estimated and actual values are identical. Abbreviations: ACI, acute cerebral infarct; REE, resting energy expenditure; SAH, subarachnoid hemorrhage.
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Figure 2. Comparison of the ratio of actual energy expenditure (REE) values to those estimated using the Harris–Benedict equation. Abbreviations: ACI, acute cerebral infarction; REE, resting energy expenditure; SAH, subarachnoid hemorrhage.
groups. The ratio was significantly higher in the SAH group than in the ACI (control) group.
Discussion In the present study, we compared actual REE values between SAH patients who underwent endovascular coiling and ACI patients. Our results show that REE was significantly higher in the SAH group after endovascular treatment than in the CI group, for which the Harris– Benedict equation accurately predicts REE.10 Therefore, it is highly plausible that even after undergoing endovascular coiling, which is a less invasive procedure than neurosurgical clipping or craniotomy, patients with SAH still had increased resting energy consumption. Based on a comparison of the patients’ profiles, we observed a significant difference in age between the 2 groups (Table 2). Age is a contributing factor for REE16-19 and therefore should be carefully considered in patients with SAH who undergo endovascular coiling. In our preliminary analyses, we applied stratified analysis in an attempt to adjust for age; however, this was problematic because the incidence of SAH is much higher in younger patients, whereas the incidence of ACI is higher in older patients.20,21 Therefore, results obtained from stratified analysis cannot be generalized. For this reason, we decided to use the ratio of actual REE values to predicted values from the Harris–Benedict equation. The predictive accuracy of the Harris–Benedict equation for patients with ACI was confirmed in our previous study.10 Accordingly, in the present study, we employed the ratio of actual REE values to the standard Harris–Benedict values to adjust for the patients’ demographic differences. As shown in Figure 1, the SAH data were plotted above the perfect fit line proportionally to the Harris–Benedict values, suggesting that using the ratio of REE values to those obtained using the Harris–Benedict equation may an effective adjustment method.
It is widely accepted that hospitalized patients have systematic increases in energy expenditure or hypermetabolism in some critical conditions such as burns, sepsis, trauma, head injury, and surgery.22-24 On the other hand, a previous study reported finding no increase in REE after surgical procedures with low invasiveness.25 In regard to stroke, hypermetabolism has been observed in patients with hemorrhagic cerebrovascular diseases during acute care.6,26-28 According to 1 study, REE increased postoperatively to 155.5% of its estimated Harris–Benedict values in SAH patients treated by neurosurgical clipping, while preoperative REE was 140.7% of the estimated values.27 A comparable increase in REE from 140% to 198% was reported in SAH patients after neurosurgical clipping.6 However, in the present study, we found that REE after endovascular coiling did not increase as much (median value, 112%; interquartile range, 105%-123%) as REE after neurosurgical clipping reported in previous studies. Taking differences in therapeutic strategies into account, the differences in the ratio of measured to estimated REE between our study and previous reports (the Touho and the Kasuya studies) may be attributed to the effects of neurosurgical clipping and craniotomy. Although endovascular coiling is less invasive than neurosurgical clipping and craniotomy, SAH patients still exhibit increased REE. This suggests that SAH itself induces hypermetabolism during the acute stage, thereby suggesting a need for special nutritional care in such patients. Electrocardiographic abnormalities, cardiomyopathy, and pulmonary edema in relation to plasma catecholamine release are concurrently observed in SAH patients.29,30 It is also well known that plasma catecholamine is associated with increased REE,31 which may be related to increases in REE after SAH. On the other hand, patients with SAH typically report a loss of appetite. As such, increased energy demand and decreased energy intake readily induce malnutrition, which may be associated with an increased rate of mortality and worse functional outcome.26,32-34 To help prevent malnutrition among patients with SAH, clinicians should be aware of the increased energy demands after SAH, even after less invasive therapeutic techniques such as endovascular coiling. The present study has several limitations. First, we did not measure REE preoperatively, as endovascular coiling is typically performed soon after admission. Even though patients were scheduled for elective surgery the next day, they were normally sedated to diminish the risks of rerupture. This precludes indirect calorimetry measurements because sedated patients are typically excluded from analysis in this type of study.35 Second, in the current study, we considered REE equal to basal energy expenditure (BEE), which is the energy expended in a strictly resting condition such as in a postabsorptive state, resting supine position, in the absence of physical and psychological stress, and with normal body temperature. In addition, REE is
ARTICLE IN PRESS ENERGY EXPENDITURE AFTER ENDOVASCULAR COILING
the sum of BEE and the thermic effect of food and activityrelated energy expenditure. In the present study, indirect calorimetry measurement was conducted under strict monitoring in our special care unit (see the Materials and Methods section), and body temperature and resting condition were carefully monitored. No patients had a markedly high body temperature (>38.0°C). Accordingly, the difference between REE and BEE was likely minimal in the present study. Third, the number of patients included in the study (N = 12) was too small to quantify the increase in REE. To quantitatively determine the increase in REE among SAH patients after endovascular coiling, a future study including more patients is needed. In conclusion, in the present study, we compared actual REE values in SAH patients treated by endovascular coiling with those in ACI patients. The results showed increased REE in SAH patients after endovascular coiling. Considering the low invasiveness of this technique, the observed increase in REE may be attributed to hypermetabolism induced by SAH. To provide optimal nutritional care to patients with SAH from the acute stage, clinicians should be aware of such changes in REE.
References 1. Davalos A, Ricart W, Gonzalez-Huix F, et al. Effect of malnutrition after acute stroke on clinical outcome. Stroke 1996;27:1028-1032. 2. Gariballa SE, Parker SG, Taub N, et al. Influence of nutritional status on clinical outcome after acute stroke. Am J Clin Nutr 1998;68:275-281. 3. Kawakami M, Liu M, Wada A, et al. Resting energy expenditure in patients with stroke during the subacute phases—relationships with stroke types, location, severity of paresis, and activities of daily living. Cerebrovasc Dis 2015;39:170-175. 4. Choi-Kwon S, Yang YH, Kim EK, et al. Nutritional status in acute stroke: undernutrition versus overnutrition in different stroke subtypes. Acta Neurol Scand 1998;98:187192. 5. Touho H, Karasawa J, Shishido H, et al. Hypermetabolism in the acute stage of hemorrhagic cerebrovascular disease. J Neurosurg 1990;72:710-714. 6. Kasuya H, Kawashima A, Namiki K, et al. Metabolic profiles of patients with subarachnoid hemorrhage treated by early surgery. Neurosurgery 1998;42:1268-1274, discussion 1274-1265. 7. Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 2002;360:1267-1274. 8. Teasdale GM, Drake CG, Hunt W, et al. A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry 1988;51:1457. 9. Hunt WE, Kosnik EJ. Timing and perioperative care in intracranial aneurysm surgery. Clin Neurosurg 1974;21:7989. 10. Nagano A, Yamada Y, Miyake H, et al. Comparisons of predictive equations for resting energy expenditure in
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patients with cerebral infarct during acute care. J Stroke Cerebrovasc Dis 2015;24:1879-1885. Nieman DC, Austin MD, Benezra L, et al. Validation of Cosmed’s FitMate in measuring oxygen consumption and estimating resting metabolic rate. Res Sports Med 2006;14:89-96. Compher C, Frankenfield D, Keim N, et al. Best practice methods to apply to measurement of resting metabolic rate in adults: a systematic review. J Am Diet Assoc 2006;106:881-903. da Rocha EE, Alves VG, Silva MH, et al. Can measured resting energy expenditure be estimated by formulae in daily clinical nutrition practice? Curr Opin Clin Nutr Metab Care 2005;8:319-328. Roberts SB, Dallal GE. Effects of age on energy balance. Am J Clin Nutr 1998;68:975s-979s. Chalela JA, Haymore J, Schellinger PD, et al. Acute stroke patients are being underfed: a nitrogen balance study. Neurocrit Care 2004;1:331-334. Siervo M, Oggioni C, Lara J, et al. Age-related changes in resting energy expenditure in normal weight, overweight and obese men and women. Maturitas 2015;80:406-413. Klausen B, Toubro S, Astrup A. Age and sex effects on energy expenditure. Am J Clin Nutr 1997;65:895-907. Roberts SB, Dallal GE. Energy requirements and aging. Public Health Nutr 2005;8:1028-1036. Elia M, Ritz P, Stubbs RJ. Total energy expenditure in the elderly. Eur J Clin Nutr 2000;54(Suppl 3):S92-S103. Inagawa T, Tokuda Y, Ohbayashi N, et al. Study of aneurysmal subarachnoid hemorrhage in Izumo City, Japan. Stroke 1995;26:761-766. Di Carlo A, Launer LJ, Breteler MM, et al. Frequency of stroke in Europe: a collaborative study of populationbased cohorts. ILSA Working Group and the Neurologic Diseases in the Elderly Research Group. Italian Longitudinal Study on Aging. Neurology 2000;54:S28-S33. Quirk J. Malnutrition in critically ill patients in intensive care units. Br J Nurs 2000;9:537-541. Reid CL. Nutritional requirements of surgical and critically-ill patients: do we really know what they need? Proc Nutr Soc 2004;63:467-472. Young B, Ott L, Yingling B, et al. Nutrition and brain injury. J Neurotrauma 1992;9(Suppl 1):S375-S383. Yatabe T, Kitagawa H, Yamashita K, et al. Energy expenditure measured using indirect calorimeter after minimally invasive esophagectomy in ventilated postoperative patients. Asia Pac J Clin Nutr 2014;23:555559. Badjatia N, Monahan A, Carpenter A, et al. Inflammation, negative nitrogen balance, and outcome after aneurysmal subarachnoid hemorrhage. Neurology 2015;84:680-687. Touho H, Karasawa J, Shishido H, et al. Measurement of energy expenditure in acute stage of cerebrovascular diseases. Neurol Med Chir (Tokyo) 1990;30:451-455. Esper DH, Coplin WM, Carhuapoma JR. Energy expenditure in patients with nontraumatic intracranial hemorrhage. JPEN J Parenter Enteral Nutr 2006;30:7175. Masuda T, Sato K, Yamamoto S, et al. Sympathetic nervous activity and myocardial damage immediately after subarachnoid hemorrhage in a unique animal model. Stroke 2002;33:1671-1676. Salem R, Vallee F, Depret F, et al. Subarachnoid hemorrhage induces an early and reversible cardiac injury associated with catecholamine release: one-week follow-up study. Crit Care 2014;18:558.
ARTICLE IN PRESS 6 31. Griffith FR Jr. Fact and theory regarding the calorigenic action of adrenaline. Physiol Rev 1951;31:151-187. 32. Wartenberg KE, Schmidt JM, Claassen J, et al. Impact of medical complications on outcome after subarachnoid hemorrhage. Crit Care Med 2006;34:617-623, quiz 624. 33. Mullen JL, Gertner MH, Buzby GP, et al. Implications of malnutrition in the surgical patient. Arch Surg 1979;114:121-125.
A. NAGANO ET AL. 34. Aptaker RL, Roth EJ, Reichhardt G, et al. Serum albumin level as a predictor of geriatric stroke rehabilitation outcome. Arch Phys Med Rehabil 1994;75: 80-84. 35. Terao Y, Miura K, Saito M, et al. Quantitative analysis of the relationship between sedation and resting energy expenditure in postoperative patients. Crit Care Med 2003;31:830-833.
Increased Resting Energy Expenditure after Endovascular Coiling for Subarachnoid Hemorrhage Ayano Nagano, RN,* Yoshitaka Yamada, MD, PhD,† Hiroji Miyake, MD, Kazuhisa Domen, MD, PhD,‡ and Tetsuo Koyama, MD, PhD‡§
PhD,†
Background: Appropriate nutritional care from the acute stage is essential for improved functional outcomes and reduced mortality in patients with subarachnoid hemorrhage (SAH). Although endovascular coiling is increasingly being used as an alternative to neurosurgical clipping and craniotomy for ruptured aneurysms, the resting energy expenditure (REE) of patients treated with this new technique has not been systemically evaluated. Methods: We measured REE values by indirect calorimetry in 12 SAH patients treated with endovascular coiling. We averaged the REE measurements obtained on days 1 and 7 after endovascular coiling, and then we statistically compared the mean REE values with those in 30 patients with acute cerebral infarction (ACI) by the Wilcoxon rank-sum test (P < .05). Next, we calculated the ratio of measured REE values to the values estimated using the Harris– Benedict equation to adjust for demographic differences in sex, weight, height, and age between the groups. Results: The ratios were significantly higher in SAH patients (median value, 1.12; interquartile range, 1.05-1.23) than in ACI patients (median value, 1.02; interquartile range, .97-1.09). Conclusions: Because endovascular coiling is less invasive than neurosurgical clipping, the observed increase in REE was attributed to metabolic changes after SAH. To provide optimal nutritional care to SAH patients from the acute stage, clinicians should be aware of this change in REE. Key Words: Diet—embolization—metabolism—nutrition—stroke. © 2015 National Stroke Association. Published by Elsevier Inc. All rights reserved.
Introduction Appropriate nutritional care is critically important for stroke patients to achieve better functional outcome and From the *Department of Nursing Care, Nishinomiya Kyoritsu Neurosurgical Hospital, Hyogo, Japan; †Department of Neurosurgery, Nishinomiya Kyoritsu Neurosurgical Hospital, Hyogo, Japan; ‡Department of Rehabilitation Medicine, Hyogo College of Medicine, Hyogo, Japan; and §Department of Rehabilitation Medicine, Nishinomiya Kyoritsu Neurosurgical Hospital, Hyogo, Japan. Received November 9, 2015; accepted December 10, 2015. Grant support: This research was supported in part by a Grantin-Aid for Scientific Research (B) from the Japan Society for the Promotion of Science (KAKENHI [25282168]). Address correspondence to Ayano Nagano, RN, Department of Nursing Care, Nishinomiya Kyoritsu Neurosurgical Hospital, 11-1 Imazu-Yamanaka-cho, Nishinomiya, Hyogo 663-8211, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter © 2015 National Stroke Association. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.12.008
reduced mortality.1,2 Metabolic parameters such as resting energy expenditure (REE) differ depending upon the type of stroke and severity of symptoms.3,4 Subarachnoid hemorrhage (SAH) is one of the most severe types of stroke and often requires surgical and/or endovascular intervention, and is associated with hypermetabolism during the acute stage.5,6 However, previous studies included only patients who had undergone conventional procedures such as neurosurgical clipping and craniotomy, which often lead to hypermetabolism due to their invasiveness. However, treatment for SAH has changed in the last decade. Endovascular coiling, a less invasive procedure than neurosurgical clipping or craniotomy, is increasingly being used as an alternative treatment for ruptured intracranial aneurysms.7 However, to our knowledge, no studies have investigated REE in patients treated with endovascular coiling for SAH due to a ruptured aneurysm. The aim of this study was to evaluate REE in the acute care setting among patients with SAH treated with endovascular coiling.
Journal of Stroke and Cerebrovascular Diseases, Vol. ■■, No. ■■ (■■), 2015: pp ■■–■■
1
ARTICLE IN PRESS A. NAGANO ET AL.
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Materials and Methods Patients The present study included patients who were diagnosed as having SAH and who underwent endovascular coiling for ruptured intracranial aneurysm at Nishinomiya Kyoritsu Neurosurgical Hospital from April 2014 to February 2015. The diagnosis of SAH and the location of the aneurysm were confirmed by computed tomography, magnetic resonance angiography, and computed tomography angiography on admission. The severity of SAH was classified according to the World Federation of Neurological Surgeons (WFNS) Scale8 and the Hunt and Kosnik scale.9 On admission, weight was measured by using a patient lift scale and height was measured in the supine position. To minimize variability arising from differences in endovascular intervention technique, we included only patients who were treated by a single neurosurgeon (Y.Y., the second author of this article). Endovascular coiling was performed within 2 days of SAH onset in all patients. Exclusion criteria were as follows: (1) oxygen therapy or ventilator dependence; (2) conditions associated with altered energy metabolism (e.g., fever >38°C, poorly controlled diabetes mellitus, advanced cancer, sepsis); (3) coma; (4) restlessness; and (5) refusal of indirect calorimetry measurements. A total of 17 SAH patients were recruited. Among them, five were excluded from the analysis based on the exclusion criteria (3 patients were dependent on a ventilator and 2 patients were receiving oxygen therapy).
Controls Thirty patients with acute cerebral infarction (ACI) who were hospitalized during the same period as those with SAH were used as a control group. The details of these 30 patients have been previously reported.10 Briefly, the control group comprised patients who lived independently in their community before stroke onset, and whose severity of stroke symptoms on admission was between 4 and 25 according to the National Institutes of Health Stroke Scale. Patients who subsequently required acute medical services were excluded.
measurements were conducted for 15 minutes, and the first 5 minutes of data were discarded.12 Heart rate, respiratory rate, and blood pressure were monitored during the measurement process. Data collected on days 1 and 7 after endovascular coiling were averaged, and the mean was used in statistical analysis. The measurement procedures were nearly identical for the control subjects, as previously reported.10 REE is dependent on age, sex, weight, height, and other variables.13,14 In the present study, in addition to indirect calorimetry measurements, we also estimated REE values derived from the Harris–Benedict equation. This equation is the most widely used predictive equation for estimating REE in a wide variety of clinical settings, including acute stroke care,15 and it is used to calculate REE (kilocalorie) as follows:
Men: 13.75 × Weight (kg ) + 5 × Height (cm ) − 6.76 × Age (years ) + 66.47
Women: 9.56 × Weight (kg ) + 1.85 × Height (cm ) − 4.86 × Age (years ) + 655.1
The calculated values were then used to adjust REE values for differences in sex, weight, height, and age between the SAH and ACI groups.
Statistical Analysis The aim of the present study was to evaluate REE among patients with SAH in the acute care setting relative to patients with ACI. To accomplish this, we adjusted for the differences in patient characteristics using the Harris–Benedict equation. In this procedure, the ratio of the measured REE value obtained using indirect calorimetry to the estimated value obtained using the Harris– Benedict equation was calculated for each patient to adjust for age, sex, weight, and height. This ratio was then used to compare the SAH and ACI groups using the Wilcoxon rank-sum test. To compare the profiles of the patients in the SAH and ACI (control) groups, we used the Pearson chi-square test for categorical data and the Wilcoxon rank-sum test for interval data. A P value less than .05 was considered statistically significant.
Metabolic Measurement We assessed REE by indirect calorimetry using a portable metabolic analyzer designed to measure oxygen consumption and energy expenditure (FitMate Metabolic System, COSMED, Rome, Italy). Measurements were performed on days 1 and 7 after endovascular coiling, between 6 a.m. and 8 a.m. at least 9 hours after meal consumption.11 The patients rested in the supine position for at least 30 minutes before each measurement and were instructed to breathe normally, but not to talk, move, or sleep during the measurement. The gas analyzer was automatically calibrated before each measurement. All
Ethical Considerations The study protocol was approved by the Institutional Review Board of Hyogo College of Medicine. Written informed consent for inclusion in the study was obtained from all patients or their family members.
Results The profiles of the 12 patients (9 women, 3 men; median age, 54.5 years; age range, 35-84 years; median weight, 54.7 kg; weight range, 43.1-96.1 kg; mean height, 153 cm;
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Table 1. Characteristics of patients with SAH
No.
Age (years)
Sex
Aneurysm
Weight (kg)
Height (cm)
mRS
H&K
WFNS
Indirect calorimetry (kcal)
H-B (kcal)
Indirect calorimetry/H-B
1 2 3 4 5 6 7 8 9 10 11 12
36 42 84 65 75 83 51 70 58 35 39 47
F F F F F F M F F F M M
Lt IC-PC Rt IC-PC BA Lt SCA Rt ACA Rt ICA Lt ICA A-com Rt VA-PICA A-com Rt MCA Rt VA Rt IP-PC
43.1 52.0 46.4 54.1 62.8 55.0 52.0 59.3 75.8 54.3 77.0 96.1
154 155 149 149 152 151 168 158 145 150 174 170
2 2 5 5 5 3 2 5 3 3 5 3
2 1 3 3 4 2 1 4 2 3 5 2
1 1 2 2 4 1 1 4 2 2 5 1
1015 1035 1132 1204 1302 1363 1454 1457 1632 1684 1916 2010
1177 1235 966 1132 1172 1057 1277 1174 1366 1282 1732 1920
.862 .838 1.171 1.063 1.111 1.290 1.139 1.241 1.195 1.314 1.106 1.047
Abbreviations: ACA, anterior cerebellar artery; A-com, anterior communicating artery; BA, basilar artery; F, female; H&K, Hunt and Kosnik scale; H-B, Harris–Benedict equation; ICA, internal carotid artery; IC-PC, internal carotid–posterior cerebral artery; Lt, left; M, male; MCA, middle cerebellar artery; mRS, modified Rankin scale; PICA, posterior inferior cerebellar artery; Rt, right; SAH, subarachnoid hemorrhage; SCA, superior cerebellar artery; VA, vertebral artery; WFNS, World Federation of Neurological Surgeons Scale. Patients were ordered 1-12 in accordance with indirect calorimetry values (lowest to highest).
Table 2. Comparison of patient characteristics between the SAH and ACI groups
M/F Age (years) Weight (kg) Height (cm)
SAH
ACI
P
3/9 Median, 54.5; IQR, 39.8-73.8 Median, 54.7; IQR, 52.0-72.6 Median, 153.0; IQR, 149.3-165.5
12/18 Median, 79.5; IQR, 72.0-87.3 Median, 50.4; IQR, 45.6-59.7 Median, 152.5; IQR. 145.8-163.5
.359 <.001 .164 .531
Abbreviations: ACI, acute cerebral infarct; F, female; IQR, interquartile range; M, male; SAH, subarachnoid aneurysm.
height range, 145-174 cm) are shown in Table 1. Indirect calorimetry values ranged from 1015 to 2010 kcal (median, 1409), modified Rankin scale scores ranged from 2 to 5 (median, 3), Hunt and Kosnik scores ranged from 1 to 5 (median, 2.5), and WFNS scores ranged from 1 to 5 (median 2). The results of statistical comparisons of patients’ profiles between the SAH and ACI groups are shown in Table 2. No significant differences were seen in sex ratio, weight, or height between the groups; however, patients in the SAH group were significantly younger than those in the ACI group. A scatterplot of the REE values measured by indirect calorimetry and the estimated Harris–Benedict values for the SAH and ACI groups is shown in Figure 1. The line with slope of 1 indicates a perfect fit where actual REE values are identical to those estimated using the Harris– Benedict equation. Plots for the control ACI group were distributed evenly around the line. In contrast, most (10 of 12) of the plots for the SAH patients were above the line. It is worth noting that actual REE values (vertical axis) increased proportionally with the estimated values (horizontal axis) in SAH patients. Figure 2 shows the results of direct statistical comparison of the ratio of actual REE values to the estimated values between the SAH and ACI
Figure 1. Scatterplot showing the relationship between actual REE values obtained using indirect calorimetry (vertical axis, kilocalorie) and estimated REE values derived from the Harris–Benedict equation (horizontal axis, kilocalorie). Ellipses indicate the 50% density distribution and the line with slope of 1 indicates a perfect fit where the estimated and actual values are identical. Abbreviations: ACI, acute cerebral infarct; REE, resting energy expenditure; SAH, subarachnoid hemorrhage.
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Figure 2. Comparison of the ratio of actual energy expenditure (REE) values to those estimated using the Harris–Benedict equation. Abbreviations: ACI, acute cerebral infarction; REE, resting energy expenditure; SAH, subarachnoid hemorrhage.
groups. The ratio was significantly higher in the SAH group than in the ACI (control) group.
Discussion In the present study, we compared actual REE values between SAH patients who underwent endovascular coiling and ACI patients. Our results show that REE was significantly higher in the SAH group after endovascular treatment than in the CI group, for which the Harris– Benedict equation accurately predicts REE.10 Therefore, it is highly plausible that even after undergoing endovascular coiling, which is a less invasive procedure than neurosurgical clipping or craniotomy, patients with SAH still had increased resting energy consumption. Based on a comparison of the patients’ profiles, we observed a significant difference in age between the 2 groups (Table 2). Age is a contributing factor for REE16-19 and therefore should be carefully considered in patients with SAH who undergo endovascular coiling. In our preliminary analyses, we applied stratified analysis in an attempt to adjust for age; however, this was problematic because the incidence of SAH is much higher in younger patients, whereas the incidence of ACI is higher in older patients.20,21 Therefore, results obtained from stratified analysis cannot be generalized. For this reason, we decided to use the ratio of actual REE values to predicted values from the Harris–Benedict equation. The predictive accuracy of the Harris–Benedict equation for patients with ACI was confirmed in our previous study.10 Accordingly, in the present study, we employed the ratio of actual REE values to the standard Harris–Benedict values to adjust for the patients’ demographic differences. As shown in Figure 1, the SAH data were plotted above the perfect fit line proportionally to the Harris–Benedict values, suggesting that using the ratio of REE values to those obtained using the Harris–Benedict equation may an effective adjustment method.
It is widely accepted that hospitalized patients have systematic increases in energy expenditure or hypermetabolism in some critical conditions such as burns, sepsis, trauma, head injury, and surgery.22-24 On the other hand, a previous study reported finding no increase in REE after surgical procedures with low invasiveness.25 In regard to stroke, hypermetabolism has been observed in patients with hemorrhagic cerebrovascular diseases during acute care.6,26-28 According to 1 study, REE increased postoperatively to 155.5% of its estimated Harris–Benedict values in SAH patients treated by neurosurgical clipping, while preoperative REE was 140.7% of the estimated values.27 A comparable increase in REE from 140% to 198% was reported in SAH patients after neurosurgical clipping.6 However, in the present study, we found that REE after endovascular coiling did not increase as much (median value, 112%; interquartile range, 105%-123%) as REE after neurosurgical clipping reported in previous studies. Taking differences in therapeutic strategies into account, the differences in the ratio of measured to estimated REE between our study and previous reports (the Touho and the Kasuya studies) may be attributed to the effects of neurosurgical clipping and craniotomy. Although endovascular coiling is less invasive than neurosurgical clipping and craniotomy, SAH patients still exhibit increased REE. This suggests that SAH itself induces hypermetabolism during the acute stage, thereby suggesting a need for special nutritional care in such patients. Electrocardiographic abnormalities, cardiomyopathy, and pulmonary edema in relation to plasma catecholamine release are concurrently observed in SAH patients.29,30 It is also well known that plasma catecholamine is associated with increased REE,31 which may be related to increases in REE after SAH. On the other hand, patients with SAH typically report a loss of appetite. As such, increased energy demand and decreased energy intake readily induce malnutrition, which may be associated with an increased rate of mortality and worse functional outcome.26,32-34 To help prevent malnutrition among patients with SAH, clinicians should be aware of the increased energy demands after SAH, even after less invasive therapeutic techniques such as endovascular coiling. The present study has several limitations. First, we did not measure REE preoperatively, as endovascular coiling is typically performed soon after admission. Even though patients were scheduled for elective surgery the next day, they were normally sedated to diminish the risks of rerupture. This precludes indirect calorimetry measurements because sedated patients are typically excluded from analysis in this type of study.35 Second, in the current study, we considered REE equal to basal energy expenditure (BEE), which is the energy expended in a strictly resting condition such as in a postabsorptive state, resting supine position, in the absence of physical and psychological stress, and with normal body temperature. In addition, REE is
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the sum of BEE and the thermic effect of food and activityrelated energy expenditure. In the present study, indirect calorimetry measurement was conducted under strict monitoring in our special care unit (see the Materials and Methods section), and body temperature and resting condition were carefully monitored. No patients had a markedly high body temperature (>38.0°C). Accordingly, the difference between REE and BEE was likely minimal in the present study. Third, the number of patients included in the study (N = 12) was too small to quantify the increase in REE. To quantitatively determine the increase in REE among SAH patients after endovascular coiling, a future study including more patients is needed. In conclusion, in the present study, we compared actual REE values in SAH patients treated by endovascular coiling with those in ACI patients. The results showed increased REE in SAH patients after endovascular coiling. Considering the low invasiveness of this technique, the observed increase in REE may be attributed to hypermetabolism induced by SAH. To provide optimal nutritional care to patients with SAH from the acute stage, clinicians should be aware of such changes in REE.
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