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Nutritional Improvement and Energy Intake Are Associated with Functional Recovery in Patients after Cerebrovascular Disorders
ARTICLE IN PRESS
Nutritional Improvement and Energy Intake Are Associated with Functional Recovery in Patients after Cerebrovascular Disorders Maria Nii, RD,* Keisuke Maeda, MD, PhD,† Hidetaka Wakabayashi, Shinta Nishioka, RD,§ and Atsuko Tanaka, MD, PhD‖
MD,‡
Background: Malnutrition affects the activities of daily living (ADLs) in convalescent patients with cerebrovascular disorders. We investigated the relationship between nutritional improvement, energy intake at admission, and recovery of ADLs. Methods: We evaluated 67 patients with cerebrovascular disorders admitted to our rehabilitation hospital between April 2013 and April 2015. These patients received interventions from the rehabilitation nutritional support team according to the following criteria: weight loss of 2 kg or more and body mass index of 19 kg/m2 or lower. Exclusion criteria included a body mass index of 25 kg/m2 or higher, duration of intervention of less than 14 days, or transfer to an acute care hospital because of clinical deterioration. We assessed nutritional status using the Geriatric Nutritional Risk Index (GNRI) and ADL using the Functional Independence Measure (FIM) score, FIM gain, and FIM efficiency. Results: The mean age of the patients was 78.7 ± 8.0 years. The numbers of patients in each category of cerebrovascular disorder were 39 with cerebral infarction, 16 with intracerebral hemorrhage, 8 with subarachnoid hemorrhage, and 4 others. Compared with the counterpart group, the group with an improvement in GNRI had a greater gain in FIM (median 17 and 20, respectively; P = .036) and a higher FIM efficiency (.14 and .22, respectively; P = .020). Multivariate stepwise regression analysis showed that an improvement in GNRI, increasing energy intake at admission, and intracerebral hemorrhage were associated independently with greater FIM efficiency. Conclusions: This study suggested that nutritional improvement and energy intake at admission are associated with recovery of ADL after cerebrovascular disorders.
From the *Department of Nutrition and Food Service, Sakurakai Medical Corporation, Sakurakai Hospital, Japan; †Department of Nutrition and Dysphagia Rehabilitation, Tamana Regional Health Medical Center, Japan; ‡Department of Rehabilitation Medicine, Yokohama City University Medical Center, Japan; §Department of Clinical Nutrition and Food Service, Nagasaki Rehabilitation Hospital, Japan; and ‖Department of Internal Medicine and Rehabilitation Medicine, Sakurakai Medical Corporation, Sakurakai Hospital, Japan. Received May 30, 2015; revision received July 20, 2015; accepted August 24, 2015. Authors’ contributions: Maria Nii: conception and design of the study, generation, collection, assembly, analysis and interpretation of data, drafting of the manuscript, and approval of the final version of the manuscript. Keisuke Maeda, Hidetaka Wakabayashi, Shinta Nishioka, and Atsuko Tanaka: conception and design of the study, analysis and interpretation of data, revision of the manuscript, and approval of the final version of the manuscript. Grant support: This work was supported by a research Grant-in-Aid for Scientific Research C (no. 25350611) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. The authors declare that they have no conflict of interest. Address correspondence to Keisuke Maeda, MD, PhD, Department of Nutrition and Dysphagia Rehabilitation, Tamana Regional Health Medical Center, 2172 Tamana, Tamana City, Kumamoto 865-0005, 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.2015.08.033
Journal of Stroke and Cerebrovascular Diseases, Vol. ■■, No. ■■ (■■), 2015: pp ■■–■■
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ARTICLE IN PRESS M. NII ET AL.
2 Key Words: Nutritional status—energy intake—activities of daily living—rehabilitation nutrition team—cerebrovascular disorders. © 2015 National Stroke Association. Published by Elsevier Inc. All rights reserved.
Introduction The nutritional status of patients is an important parameter during the subacute and recovery stages following a cerebrovascular disorder. Poor nutritional status is associated with increased severity of the disease, mortality, infectious complications, swallowing difficulty, and less improvement in activities of daily living (ADLs).1-5 The number of patients with protein–energy malnutrition was shown to increase by approximately 60% (16.3%-26.4%) in the first week after a stroke, leading to a higher mortality rate and decline in ADL.6 Nutritional therapy for patients with cerebrovascular disorders in acute settings is known to result in better clinical outcomes, with studies showing that early enteral feeding improves nutritional status7 and early nutritional therapy is associated with lower mortality rates.7 In subacute and rehabilitation settings, an intensive nutritional approach in stroke patients may improve physical function to a greater extent than standard care.8 Nutritional support may therefore be a potential therapeutic strategy for patients with postcerebrovascular disorder. Nutritional care in the rehabilitation setting is considered to be important because patients with cerebrovascular disorders in rehabilitation hospitals are more likely to have poor nutrition than patients in acute hospitals.5,9 Although nutritional support is necessary for patients in this setting, to our knowledge, the association between changes in nutritional parameters and ADL has not been investigated. Recently, Beberashvili et al.10 reported that changes in the Geriatric Nutritional Risk Index (GNRI), a nutritional screening score, correlated with changes in nutritional status evaluated by body composition. Therefore, it is possible to assess the effects of nutritional care in stroke patients in rehabilitation hospitals using the GNRI. This study therefore investigated the relationship between changes in nutritional status assessed by the GNRI, energy intake at admission, and ADL in patients with postcerebrovascular disorder in a rehabilitation setting.
Methods Subjects This cross-sectional, retrospective, single-center study investigated patients aged 65 years or older who were admitted consecutively to the convalescent rehabilitation ward in Sakurakai Hospital between April 2013 and April 2015 to receive rehabilitation for a cerebrovascular disorder. The mean duration of physical rehabilitation in patients in our rehabilitation hospital was 699 minutes
per week. Patients who were treated by our rehabilitation nutrition team (RNT) were included in the study. The criteria for intervention by the RNT were a body mass index (BMI) of 19 kg/m2 or lower, or weight loss of more than 2 kg from onset. Patients who were either overweight (BMI ≥ 25 kg/m2), were transferred to another hospital for treatment of comorbidities, died in our hospital, or with missing data were excluded. The present study was conducted in accordance with the Declaration of Helsinki and was approved by the Ethics Committee of Sakurakai Hospital. Because the study was a retrospective study, written informed consent was not obtained from the patients, and a waiver of consent was obtained from the Ethics Committee.
RNT In our hospital, the RNT identified malnourished patients using the following screening criteria: BMI of 19 kg/m2 or lower, or weight loss of more than 2 kg from onset at admission. These criteria were the same as the inclusion criteria in the present study. The RNT consisted of multidisciplinary staff including a dietician, physical therapist, occupational therapist, and a speech language pathologist who treated all patients with malnutrition during hospitalization. The status and intake of nutrition and amount of rehabilitation for each patient were considered by a member of the RNT. Because protein supplementation and exercise can increase muscle mass and strength,11 the RNT evaluated the amount and load of rehabilitation in patients who needed to be supplied with additional protein supplement. The RNT monitored body weight every 2 weeks and re-evaluated the necessary level of nutritional intake. This intervention was conducted according to the principles of rehabilitation nutrition therapy.12
Parameters The clinical parameters were obtained retrospectively from medical records. The GNRI,13,14 a nutritional risk index, was calculated from the serum albumin concentration and body weight using the following equation: GNRI = [1.489 × albumin concentration (g/dL)] + [41.7 × (actual body weight/ideal body weight)]. The ideal body weight was defined as a BMI of 22.0 kg/m215,16 rather than the Lorentz formula. We divided the patients into 2 groups in accordance with the changes in GNRI from admission to discharge from the hospital. The group with an improvement in GNRI included patients with a higher level of GNRI at discharge than at
ARTICLE IN PRESS NUTRITIONAL AND FUNCTIONAL RECOVERY IN STROKE
admission, because it is known that changes in GNRI reflect nutritional status.10,17 The severity of dysphagia was assessed by the Food Intake Level Scale (FILS).18 The FILS is a 10-point observer rating scale that measures the severity of dysphagia. Levels 1-3 relate to various degrees of nonoral feeding, levels 4-6 to various degrees of oral food intake and alternative nutrition, levels 7-9 to various degrees of oral food intake alone, whereas level 10 indicates normal oral food intake. The reliability and validity of the FILS have been established previously.18 Nutritional intake was estimated by a dietician in the RNT based on the consumption of daily meals and nutritional supplements for 7 days after admission.
Outcome Measures The Functional Independence Measure19 (FIM) efficiency was used as an outcome variable. The FIM score, an 18-item measurement tool with a 7-point ordinal scale, is a validated and reliable score for evaluating disability severity and burden of care in the inpatient rehabilitation setting.20 Admission and discharge FIM motor, cognitive, and total scores were calculated by summing the scores of the items. The FIM efficiency, which is used widely to assess rehabilitation,21 was calculated by dividing the changes in the FIM score between admission and discharge by the length of hospital stay.
Sample Size Calculation In a previous study,22 the standard deviation of the FIM efficiency within each subject group was .17. If the true difference between the means of the group with improved nutrition and the means of the control group is .12, it is necessary to study 66 subjects to be able to reject the null hypothesis that the population means of the groups are equal at a statistical power of .8. The probability of a type I error associated with this test of the null hypothesis is .05. We therefore planned to examine more than 66 patients in the study.
Statistical Analyses The statistical analyses were performed using SPSS software version 21 (IBM Japan, Tokyo, Japan). Parametric data were expressed as the mean ± standard deviation and nonparametric data as the median and interquartile ranges. The chi-square test, t-test, and the Mann–Whitney U-test were used to analyze the differences between the 2 groups. We also conducted a stepwise linear regression analysis to examine whether nutritional improvement was an independent determinant of the degree of functional recovery. Other candidate factors for explanatory parameters were age, gender, category of stroke, albumin concentration, BMI, GNRI, FIM, and energy intake at admission. A P value less than .05 was considered statistically significant.
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Results During the study period, 87 patients with postcerebrovascular disorders requiring rehabilitation were admitted to the convalescent rehabilitation ward in the hospital. Patients who were either overweight (1 case), transferred to another hospital (4 cases), died (1 case), or with missing variables (14 cases in whom the change in GNRI could not be calculated because the serum albumin level was not measured at discharge) were excluded. The remaining 67 poststroke patients (45 males and 22 females; mean age 78.7 ± 8.0 years) were included in the study. The characteristics of the 67 patients at admission are shown in Table 1. The study group included 39 cases of cerebral infarction, 16 of intracerebral hemorrhage, 8 of subarachnoid hemorrhage, and 4 of subdural hematoma. Mean BMI and GNRI at admission showed that many patients in the study were malnourished (BMI = 18.8 ± 2.2 kg/m2; GNRI = 87.3 ± 7.3 points). Mean energy intake at admission was = 33.2 (29.2-39.75) kcal/kg/day. The FIM score showed the patients had impaired physical and cognitive disability at admission (FIM total score = 56 [43-86.5] points, motor score = 35 [27-60] points, and cognition score = 20 [14-27.5] points). The severity of dysphagia, conservative treatment, craniotomy, endovascular surgery, damage to a hemisphere, and use of antidepressants did not differ significantly between the groups with or without an improvement in GNRI. While the group with an improvement in GNRI had lower levels of serum albumin (P = .013) than those in the group without improvement in GNRI, the other parameters recorded at admission were not different between the 2 groups (Table 1). Table 2 summarizes the comparison of changes in nutritional and physical parameters during hospitalization between the groups with and without improvement in GNRI. Total FIM gain and efficiency, and cognition FIM efficiency demonstrated that the patients in the improvement group had a significantly better recovery than those in the nonimprovement group (P = .036, .020, and .047, respectively). A multivariate regression analysis that included age, gender, disease category, albumin level, BMI, GNRI, FIM, energy intake at admission, and improvement of GNRI as variables showed that an improvement in GNRI, amount of energy intake, and type of intracerebral hemorrhage were associated independently with increasing FIM efficiency (Table 3).
Discussion This study addressed 2 issues concerning the association between changes in nutritional status, energy intake, and rehabilitative outcome in patients in a rehabilitation hospital suffering from disabilities caused by
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Table 1. Characteristics of the patients at admission
Characteristic
All (n = 67)
GNRI No improvement (n = 36)
GNRI Improvement (n = 31)
P value
Age (yr) Gender (n) Female Male Category of cerebrovascular disorders (n) Cerebral infarction Intracerebral hemorrhage Subarachnoid hemorrhage Others Medical treatments Conservative treatment Craniotomy Endovascular surgery Damaged hemisphere Right Left Bilateral Antidepressant Use No use Body mass index (kg/m2) GNRI (score) Albumin (g/dL) Nutritional intake (kcal/kg/day) FILS FIM (points) Total Motor Cognition
78.7 ± 8.0
79.8 ± 7.9
77.4 ± 8.0
.235
22 (32.8) 45 (67.2)
11 (30.6) 25 (69.4)
11 (35.5) 20 (64.5)
.795
39 (58.2) 16 (23.9) 8 (11.9) 4 (6.0)
22 (61.1) 8 (22.2) 3 (8.3) 3 (8.3)
17 (54.8) 8 (25.8) 5 (16.1) 1 (3.2)
.634
52 (77.6) 12 (17.9) 3 (4.5)
29 (80.5) 5 (13.9) 2 (5.6)
23 (74.2) 7 (22.6) 1 (3.2)
.639
33 (49.3) 25 (37.3) 9 (13.4)
17 (47.2) 12 (33.3) 7 (19.5)
16 (51.6) 13 (41.9) 2 (6.5)
.288
18 (26.9) 49 (73.1) 18.8 ± 2.2 87.3 ± 7.3 3.48 ± .38 33.2 (29.2-39.75) 8 (7-10)
8 (22.2) 28 (77.8) 18.7 ± 2.3 88.6 ± 7.7 3.58 ± .39 32.3 (29.25-38.02) 8 (7-10)
10 (32.3) 21 (67.7) 18.9 ± 2.0 85.8 ± 6.6 3.35 ± .34 35.5 (29.15-41.0) 8 (7.5-9.5)
.517 .644 .117 .013 .33 .974
56 (43.0-86.5) 35 (27-60) 20 (14.0-27.5)
56.5 (44.75-81.75) 38.5 (28-59.5) 21.5 (15-28)
55 (41-87) 31 (26.5-62.5) 20 (13.0-26.5)
.546 .589 .329
Abbreviations: FILS, Food Intake Level Scale; FIM, Functional Independence Measure; GNRI, Geriatric Nutritional Risk Index.
Table 2. Changes in nutritional and physical parameters during hospitalization
Parameter Length of hospital stay (days) Body mass index (kg/m2) GNRI (score) Albumin (g/dL) Nutritional intake (kcal/kg/day) FIM gain (points) Total Motor Cognition FIM efficiency (points/day) Total Motor Cognition
GNRI No improvement (n = 36)
GNRI Improvement (n = 31)
P value
76.5 [36-98.25] .0 ± 1.1 −4.4 ± 3.7 −.28 ± .26 4.1 [−.5, 8.3]
84 [51.5-110.5] .3 ± 1.4 6.1 ± 5.0 .38 ± .28 3.8 [−.1, 6.3]
.333 .349 <.001 <.001 .975
17 [3.75-23.25] 13.5 [4-22.25] 2 [0-5]
20 [11-37.5] 19 [7-28.5] 3 [1.5-7]
.036 .068 .069
.14 [.03-.20] .12 [.03-.18] .02 [.00-.04]
.22 [.14-.33] .17 [.08-.29] .04 [.01-.06]
.020 .054 .047
Abbreviations: FIM, Functional Independence Measure; GNRI, Geriatric Nutritional Risk Index.
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Table 3. Stepwise linear regression analysis on the efficiency of the Functional Independence Measure Variable
Unadjusted coefficient
95%CI
Adjusted coefficient
P value
GNRI improvement Intracerebral hemorrhage Energy intake at admission (kcal/kg/day) Albumin Constant
.097 .207 .007 .008 −.127
.005-.189 .099-.314 .001-.013 −.120-.136 −.351-.098
.226 .412 .222 .014
.04 <.001 .043 .901 .263
Abbreviation: GNRI, Geriatric Nutritional Risk Index.
cerebrovascular disorders. First, an improvement in nutritional status following admission to discharge from hospital was associated with improved ADL in these patients. Second, the amount of energy intake at admission was associated with the degree of improvement in ADL. Our study demonstrated that an improvement in nutritional status was associated with an improvement in ADL in patients with cerebrovascular disorders during convalescence. Nutritional care could therefore be effective for patients requiring physical rehabilitation.8,23 However, only a few studies have described the relationship between nutritional improvement and physical outcome. Ha et al.23 reported that nutritional care to prevent weight loss in patients with stroke at risk of malnutrition contributed to an increase in hand-grip strength and improved quality of life including significant improvements in mobility, self-care ability, and usual activities. These findings are in accordance with the results of the current study. Finestone et al.24 reported that prolonged malnutrition during hospitalization, diagnosed by anthropometry or blood tests including serum albumin level, was associated with a longer hospital stay. However, they did not analyze the improvement in physical function or ADL in relation to nutritional status. We used the GNRI to evaluate changes in nutritional status. GNRI is calculated using the serum albumin level and BMI. Mizrahi et al.25 reported that improvement in albumin levels was associated with a gain in FIM in patients with hip fractures in a rehabilitation setting. We could not confirm the reason for the difference between the groups on the basis of the results from this study. However, we presume that the minor but continuing difference in dietary intake between the groups during hospitalization, which was estimated at 3.2 kcal/kg/day upon admission, might have contributed to the nutritional difference. Our data showed that the amount of initial energy intake was associated with improved ADL in patients with cerebrovascular disorders during the convalescent stage. The effect of nutritional intake in such patients may differ in the acute and rehabilitation settings. In the acute phase, the large interventional Feed Or Ordinary Diet (FOOD) trial26 concluded that nutritional supplementation in patients with acute stroke did not improve outcome. However, Nip et al.27 showed in an observational study that higher
energy intake in the early stage of stroke was an independent predictor for improvement in ADL, assessed by the Barthel Index at discharge. Evidence from a randomized control trial by Rabadi et al.8 showed that in the rehabilitation phase nutritional supplementation improved physical function during rehabilitation of patients following cerebrovascular disorders. In the present study, the subjects lived in a rehabilitation setting in Japan in which many patients were receiving rehabilitation therapy for more than 15 hours per week following a cerebrovascular disorder.20 We therefore consider that it is necessary to increase energy intake in this setting to a greater extent than in an acute setting. Nutritional care for patients with cerebrovascular disorders has an essential role for both malnutrition and physical rehabilitation.8 This combined strategy is named rehabilitation nutrition.12 Rehabilitation nutrition is a combination of both rehabilitation and nutritional care management that evaluates nutritional status and maximizes functionality in all people with disabilities.12 Because rehabilitation consumes a certain amount of energy, inappropriate nutritional care in malnourished patients with cerebrovascular disorders may worsen both malnutrition and ADL. Nutritional improvement combined with rehabilitation can therefore help more patients with cerebrovascular disorders to recover ADL. Our study had several limitations. First, because the study had a retrospective cross-sectional design, it was not possible to establish a causal relationship between improved nutritional status and ADL. Second, the relatively high number of patients with missing variables excluded from the study (16.1%) may have caused selection bias. Third, the amount and type of rehabilitation and the level of stroke severity were not analyzed. Fourth, all patients received intervention from the RNT. Therefore, we could not evaluate the effectiveness of this intervention. Finally, we could not adjust for all confounding factors because of the relatively low number of patients (i.e., n = 67). Further studies are therefore necessary in patients with cerebrovascular disorders to examine whether or not ADL can be improved to a greater extent by increased nutritional intake, determined by recording the time and intensity of rehabilitation and energy accumulation.
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In conclusion, the present study showed that nutritional improvement at discharge and energy intake at admission were associated with recovery of ADL in patients admitted to a rehabilitation hospital following a cerebrovascular disorder. From a clinical point of view, the current study indicated that intensive nutritional care added to physical rehabilitation led to better clinical outcomes. Further large-scale studies on other conditions are required to examine causality in greater detail. Acknowledgment: The authors wish to thank the rehabilitation nutrition team for their valuable assistance in this project.
References 1. 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. 2. The FOOD Trial Collaboration. Poor nutritional status on admission predicts poor outcomes after stroke: observational data from the FOOD trial. Stroke 2003;34:1450-1456. 3. Davis JP, Wong AA, Schluter PJ, et al. Impact of premorbid undernutrition on outcome in stroke patients. Stroke 2004;35:1930-1934. 4. Yoo SH, Kim JS, Kwon SU, et al. Undernutrition as a predictor of poor clinical outcomes in acute ischemic stroke patients. Arch Neurol 2008;65:39-43. 5. Foley NC, Martin RE, Salter KL, et al. A review of the relationship between dysphagia and malnutrition following stroke. J Rehabil Med 2009;41:707-713. 6. Davalos A, Ricart W, Gonzalez-Huix F, et al. Effect of malnutrition after acute stroke on clinical outcome. Stroke 1996;27:1028-1032. 7. Gariballa SE, Parker SG, Taub N, et al. A randomized, controlled, a single-blind trial of nutritional supplementation after acute stroke. JPEN J Parenter Enteral Nutr 1998;22:315-319. 8. Rabadi MH, Coar PL, Lukin M, et al. Intensive nutritional supplements can improve outcomes in stroke rehabilitation. Neurology 2008;71:1856-1861. 9. Kaiser MJ, Bauer JM, Ramsch C, et al. Frequency of malnutrition in older adults: a multinational perspective using the mini nutritional assessment. J Am Geriatr Soc 2010;58:1734-1738. 10. Beberashvili I, Azar A, Sinuani I, et al. Comparison analysis of nutritional scores for serial monitoring of nutritional status in hemodialysis patients. Clin J Am Soc Nephrol 2013;8:443-451. 11. Cermak NM, Res PT, de Groot LC, et al. Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr 2012;96:1454-1464. 12. Wakabayashi H, Sakuma K. Rehabilitation nutrition for sarcopenia with disability: a combination of both
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
rehabilitation and nutrition care management. J Cachexia Sarcopenia Muscle 2014;5:269-277. Bouillanne O, Morineau G, Dupont C, et al. Geriatric Nutritional Risk Index: a new index for evaluating at-risk elderly medical patients. Am J Clin Nutr 2005;82:777783. Cereda E, Vanotti A. The new Geriatric Nutritional Risk Index is a good predictor of muscle dysfunction in institutionalized older patients. Clin Nutr 2007;26:7883. Shah B, Sucher K, Hollenbeck CB. Comparison of ideal body weight equations and published height-weight tables with body mass index tables for healthy adults in the United States. Nutr Clin Pract 2006;21:312-319. Yamada K, Furuya R, Takita T, et al. Simplified nutritional screening tools for patients on maintenance hemodialysis. Am J Clin Nutr 2008;87:106-113. Kang SH, Cho KH, Park JW, et al. Impact of heavy proteinuria on clinical outcomes in patients on incident peritoneal dialysis. BMC Nephrol 2012;13:171. Kunieda K, Ohno T, Fujishima I, et al. Reliability and validity of a tool to measure the severity of dysphagia: the Food Intake Level Scale. J Pain Symptom Manage 2013;46:201-206. Keith RA, Granger CV, Hamilton BB, et al. The Functional Independence Measure: a new tool for rehabilitation. Adv Clin Rehabil 1987;1:6-18. Dodds TA, Martin DP, Stolov WC, et al. A validation of the functional independence measurement and its performance among rehabilitation inpatients. Arch Phys Med Rehabil 1993;74:531-536. Miyai I, Sonoda S, Nagai S, et al. Results of new policies for inpatient rehabilitation coverage in Japan. Neurorehabil Neural Repair 2011;25:540-547. Sonoda S, Saitoh E, Nagai S, et al. Full-time integrated treatment program, a new system for stroke rehabilitation in Japan: comparison with conventional rehabilitation. Am J Phys Med Rehabil 2004;83:88-93. Ha L, Hauge T, Spenning AB, et al. Individual, nutritional support prevents undernutrition, increases muscle strength and improves QoL among elderly at nutritional risk hospitalized for acute stroke: a randomized, controlled trial. Clin Nutr 2010;29:567-573. Finestone HM, Greene-Finestone LS, Wilson ES, et al. Prolonged length of stay and reduced functional improvement rate in malnourished stroke rehabilitation patients. Arch Phys Med Rehabil 1996;77:340-345. Mizrahi EH, Fleissig Y, Arad M, et al. Rehabilitation outcome of hip fracture patients: the importance of a positive albumin gain. Arch Gerontol Geriatr 2008;47:318326. Dennis MS, Lewis SC, Warlow C, et al. Routine oral nutritional supplementation for stroke patients in hospital (FOOD): a multicentre randomised controlled trial. Lancet 2005;365:755-763. Nip WF, Perry L, McLaren S, et al. Dietary intake, nutritional status and rehabilitation outcomes of stroke patients in hospital. J Hum Nutr Diet 2011;24:460469.
Nutritional Improvement and Energy Intake Are Associated with Functional Recovery in Patients after Cerebrovascular Disorders Maria Nii, RD,* Keisuke Maeda, MD, PhD,† Hidetaka Wakabayashi, Shinta Nishioka, RD,§ and Atsuko Tanaka, MD, PhD‖
MD,‡
Background: Malnutrition affects the activities of daily living (ADLs) in convalescent patients with cerebrovascular disorders. We investigated the relationship between nutritional improvement, energy intake at admission, and recovery of ADLs. Methods: We evaluated 67 patients with cerebrovascular disorders admitted to our rehabilitation hospital between April 2013 and April 2015. These patients received interventions from the rehabilitation nutritional support team according to the following criteria: weight loss of 2 kg or more and body mass index of 19 kg/m2 or lower. Exclusion criteria included a body mass index of 25 kg/m2 or higher, duration of intervention of less than 14 days, or transfer to an acute care hospital because of clinical deterioration. We assessed nutritional status using the Geriatric Nutritional Risk Index (GNRI) and ADL using the Functional Independence Measure (FIM) score, FIM gain, and FIM efficiency. Results: The mean age of the patients was 78.7 ± 8.0 years. The numbers of patients in each category of cerebrovascular disorder were 39 with cerebral infarction, 16 with intracerebral hemorrhage, 8 with subarachnoid hemorrhage, and 4 others. Compared with the counterpart group, the group with an improvement in GNRI had a greater gain in FIM (median 17 and 20, respectively; P = .036) and a higher FIM efficiency (.14 and .22, respectively; P = .020). Multivariate stepwise regression analysis showed that an improvement in GNRI, increasing energy intake at admission, and intracerebral hemorrhage were associated independently with greater FIM efficiency. Conclusions: This study suggested that nutritional improvement and energy intake at admission are associated with recovery of ADL after cerebrovascular disorders.
From the *Department of Nutrition and Food Service, Sakurakai Medical Corporation, Sakurakai Hospital, Japan; †Department of Nutrition and Dysphagia Rehabilitation, Tamana Regional Health Medical Center, Japan; ‡Department of Rehabilitation Medicine, Yokohama City University Medical Center, Japan; §Department of Clinical Nutrition and Food Service, Nagasaki Rehabilitation Hospital, Japan; and ‖Department of Internal Medicine and Rehabilitation Medicine, Sakurakai Medical Corporation, Sakurakai Hospital, Japan. Received May 30, 2015; revision received July 20, 2015; accepted August 24, 2015. Authors’ contributions: Maria Nii: conception and design of the study, generation, collection, assembly, analysis and interpretation of data, drafting of the manuscript, and approval of the final version of the manuscript. Keisuke Maeda, Hidetaka Wakabayashi, Shinta Nishioka, and Atsuko Tanaka: conception and design of the study, analysis and interpretation of data, revision of the manuscript, and approval of the final version of the manuscript. Grant support: This work was supported by a research Grant-in-Aid for Scientific Research C (no. 25350611) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. The authors declare that they have no conflict of interest. Address correspondence to Keisuke Maeda, MD, PhD, Department of Nutrition and Dysphagia Rehabilitation, Tamana Regional Health Medical Center, 2172 Tamana, Tamana City, Kumamoto 865-0005, 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.2015.08.033
Journal of Stroke and Cerebrovascular Diseases, Vol. ■■, No. ■■ (■■), 2015: pp ■■–■■
1
ARTICLE IN PRESS M. NII ET AL.
2 Key Words: Nutritional status—energy intake—activities of daily living—rehabilitation nutrition team—cerebrovascular disorders. © 2015 National Stroke Association. Published by Elsevier Inc. All rights reserved.
Introduction The nutritional status of patients is an important parameter during the subacute and recovery stages following a cerebrovascular disorder. Poor nutritional status is associated with increased severity of the disease, mortality, infectious complications, swallowing difficulty, and less improvement in activities of daily living (ADLs).1-5 The number of patients with protein–energy malnutrition was shown to increase by approximately 60% (16.3%-26.4%) in the first week after a stroke, leading to a higher mortality rate and decline in ADL.6 Nutritional therapy for patients with cerebrovascular disorders in acute settings is known to result in better clinical outcomes, with studies showing that early enteral feeding improves nutritional status7 and early nutritional therapy is associated with lower mortality rates.7 In subacute and rehabilitation settings, an intensive nutritional approach in stroke patients may improve physical function to a greater extent than standard care.8 Nutritional support may therefore be a potential therapeutic strategy for patients with postcerebrovascular disorder. Nutritional care in the rehabilitation setting is considered to be important because patients with cerebrovascular disorders in rehabilitation hospitals are more likely to have poor nutrition than patients in acute hospitals.5,9 Although nutritional support is necessary for patients in this setting, to our knowledge, the association between changes in nutritional parameters and ADL has not been investigated. Recently, Beberashvili et al.10 reported that changes in the Geriatric Nutritional Risk Index (GNRI), a nutritional screening score, correlated with changes in nutritional status evaluated by body composition. Therefore, it is possible to assess the effects of nutritional care in stroke patients in rehabilitation hospitals using the GNRI. This study therefore investigated the relationship between changes in nutritional status assessed by the GNRI, energy intake at admission, and ADL in patients with postcerebrovascular disorder in a rehabilitation setting.
Methods Subjects This cross-sectional, retrospective, single-center study investigated patients aged 65 years or older who were admitted consecutively to the convalescent rehabilitation ward in Sakurakai Hospital between April 2013 and April 2015 to receive rehabilitation for a cerebrovascular disorder. The mean duration of physical rehabilitation in patients in our rehabilitation hospital was 699 minutes
per week. Patients who were treated by our rehabilitation nutrition team (RNT) were included in the study. The criteria for intervention by the RNT were a body mass index (BMI) of 19 kg/m2 or lower, or weight loss of more than 2 kg from onset. Patients who were either overweight (BMI ≥ 25 kg/m2), were transferred to another hospital for treatment of comorbidities, died in our hospital, or with missing data were excluded. The present study was conducted in accordance with the Declaration of Helsinki and was approved by the Ethics Committee of Sakurakai Hospital. Because the study was a retrospective study, written informed consent was not obtained from the patients, and a waiver of consent was obtained from the Ethics Committee.
RNT In our hospital, the RNT identified malnourished patients using the following screening criteria: BMI of 19 kg/m2 or lower, or weight loss of more than 2 kg from onset at admission. These criteria were the same as the inclusion criteria in the present study. The RNT consisted of multidisciplinary staff including a dietician, physical therapist, occupational therapist, and a speech language pathologist who treated all patients with malnutrition during hospitalization. The status and intake of nutrition and amount of rehabilitation for each patient were considered by a member of the RNT. Because protein supplementation and exercise can increase muscle mass and strength,11 the RNT evaluated the amount and load of rehabilitation in patients who needed to be supplied with additional protein supplement. The RNT monitored body weight every 2 weeks and re-evaluated the necessary level of nutritional intake. This intervention was conducted according to the principles of rehabilitation nutrition therapy.12
Parameters The clinical parameters were obtained retrospectively from medical records. The GNRI,13,14 a nutritional risk index, was calculated from the serum albumin concentration and body weight using the following equation: GNRI = [1.489 × albumin concentration (g/dL)] + [41.7 × (actual body weight/ideal body weight)]. The ideal body weight was defined as a BMI of 22.0 kg/m215,16 rather than the Lorentz formula. We divided the patients into 2 groups in accordance with the changes in GNRI from admission to discharge from the hospital. The group with an improvement in GNRI included patients with a higher level of GNRI at discharge than at
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admission, because it is known that changes in GNRI reflect nutritional status.10,17 The severity of dysphagia was assessed by the Food Intake Level Scale (FILS).18 The FILS is a 10-point observer rating scale that measures the severity of dysphagia. Levels 1-3 relate to various degrees of nonoral feeding, levels 4-6 to various degrees of oral food intake and alternative nutrition, levels 7-9 to various degrees of oral food intake alone, whereas level 10 indicates normal oral food intake. The reliability and validity of the FILS have been established previously.18 Nutritional intake was estimated by a dietician in the RNT based on the consumption of daily meals and nutritional supplements for 7 days after admission.
Outcome Measures The Functional Independence Measure19 (FIM) efficiency was used as an outcome variable. The FIM score, an 18-item measurement tool with a 7-point ordinal scale, is a validated and reliable score for evaluating disability severity and burden of care in the inpatient rehabilitation setting.20 Admission and discharge FIM motor, cognitive, and total scores were calculated by summing the scores of the items. The FIM efficiency, which is used widely to assess rehabilitation,21 was calculated by dividing the changes in the FIM score between admission and discharge by the length of hospital stay.
Sample Size Calculation In a previous study,22 the standard deviation of the FIM efficiency within each subject group was .17. If the true difference between the means of the group with improved nutrition and the means of the control group is .12, it is necessary to study 66 subjects to be able to reject the null hypothesis that the population means of the groups are equal at a statistical power of .8. The probability of a type I error associated with this test of the null hypothesis is .05. We therefore planned to examine more than 66 patients in the study.
Statistical Analyses The statistical analyses were performed using SPSS software version 21 (IBM Japan, Tokyo, Japan). Parametric data were expressed as the mean ± standard deviation and nonparametric data as the median and interquartile ranges. The chi-square test, t-test, and the Mann–Whitney U-test were used to analyze the differences between the 2 groups. We also conducted a stepwise linear regression analysis to examine whether nutritional improvement was an independent determinant of the degree of functional recovery. Other candidate factors for explanatory parameters were age, gender, category of stroke, albumin concentration, BMI, GNRI, FIM, and energy intake at admission. A P value less than .05 was considered statistically significant.
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Results During the study period, 87 patients with postcerebrovascular disorders requiring rehabilitation were admitted to the convalescent rehabilitation ward in the hospital. Patients who were either overweight (1 case), transferred to another hospital (4 cases), died (1 case), or with missing variables (14 cases in whom the change in GNRI could not be calculated because the serum albumin level was not measured at discharge) were excluded. The remaining 67 poststroke patients (45 males and 22 females; mean age 78.7 ± 8.0 years) were included in the study. The characteristics of the 67 patients at admission are shown in Table 1. The study group included 39 cases of cerebral infarction, 16 of intracerebral hemorrhage, 8 of subarachnoid hemorrhage, and 4 of subdural hematoma. Mean BMI and GNRI at admission showed that many patients in the study were malnourished (BMI = 18.8 ± 2.2 kg/m2; GNRI = 87.3 ± 7.3 points). Mean energy intake at admission was = 33.2 (29.2-39.75) kcal/kg/day. The FIM score showed the patients had impaired physical and cognitive disability at admission (FIM total score = 56 [43-86.5] points, motor score = 35 [27-60] points, and cognition score = 20 [14-27.5] points). The severity of dysphagia, conservative treatment, craniotomy, endovascular surgery, damage to a hemisphere, and use of antidepressants did not differ significantly between the groups with or without an improvement in GNRI. While the group with an improvement in GNRI had lower levels of serum albumin (P = .013) than those in the group without improvement in GNRI, the other parameters recorded at admission were not different between the 2 groups (Table 1). Table 2 summarizes the comparison of changes in nutritional and physical parameters during hospitalization between the groups with and without improvement in GNRI. Total FIM gain and efficiency, and cognition FIM efficiency demonstrated that the patients in the improvement group had a significantly better recovery than those in the nonimprovement group (P = .036, .020, and .047, respectively). A multivariate regression analysis that included age, gender, disease category, albumin level, BMI, GNRI, FIM, energy intake at admission, and improvement of GNRI as variables showed that an improvement in GNRI, amount of energy intake, and type of intracerebral hemorrhage were associated independently with increasing FIM efficiency (Table 3).
Discussion This study addressed 2 issues concerning the association between changes in nutritional status, energy intake, and rehabilitative outcome in patients in a rehabilitation hospital suffering from disabilities caused by
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Table 1. Characteristics of the patients at admission
Characteristic
All (n = 67)
GNRI No improvement (n = 36)
GNRI Improvement (n = 31)
P value
Age (yr) Gender (n) Female Male Category of cerebrovascular disorders (n) Cerebral infarction Intracerebral hemorrhage Subarachnoid hemorrhage Others Medical treatments Conservative treatment Craniotomy Endovascular surgery Damaged hemisphere Right Left Bilateral Antidepressant Use No use Body mass index (kg/m2) GNRI (score) Albumin (g/dL) Nutritional intake (kcal/kg/day) FILS FIM (points) Total Motor Cognition
78.7 ± 8.0
79.8 ± 7.9
77.4 ± 8.0
.235
22 (32.8) 45 (67.2)
11 (30.6) 25 (69.4)
11 (35.5) 20 (64.5)
.795
39 (58.2) 16 (23.9) 8 (11.9) 4 (6.0)
22 (61.1) 8 (22.2) 3 (8.3) 3 (8.3)
17 (54.8) 8 (25.8) 5 (16.1) 1 (3.2)
.634
52 (77.6) 12 (17.9) 3 (4.5)
29 (80.5) 5 (13.9) 2 (5.6)
23 (74.2) 7 (22.6) 1 (3.2)
.639
33 (49.3) 25 (37.3) 9 (13.4)
17 (47.2) 12 (33.3) 7 (19.5)
16 (51.6) 13 (41.9) 2 (6.5)
.288
18 (26.9) 49 (73.1) 18.8 ± 2.2 87.3 ± 7.3 3.48 ± .38 33.2 (29.2-39.75) 8 (7-10)
8 (22.2) 28 (77.8) 18.7 ± 2.3 88.6 ± 7.7 3.58 ± .39 32.3 (29.25-38.02) 8 (7-10)
10 (32.3) 21 (67.7) 18.9 ± 2.0 85.8 ± 6.6 3.35 ± .34 35.5 (29.15-41.0) 8 (7.5-9.5)
.517 .644 .117 .013 .33 .974
56 (43.0-86.5) 35 (27-60) 20 (14.0-27.5)
56.5 (44.75-81.75) 38.5 (28-59.5) 21.5 (15-28)
55 (41-87) 31 (26.5-62.5) 20 (13.0-26.5)
.546 .589 .329
Abbreviations: FILS, Food Intake Level Scale; FIM, Functional Independence Measure; GNRI, Geriatric Nutritional Risk Index.
Table 2. Changes in nutritional and physical parameters during hospitalization
Parameter Length of hospital stay (days) Body mass index (kg/m2) GNRI (score) Albumin (g/dL) Nutritional intake (kcal/kg/day) FIM gain (points) Total Motor Cognition FIM efficiency (points/day) Total Motor Cognition
GNRI No improvement (n = 36)
GNRI Improvement (n = 31)
P value
76.5 [36-98.25] .0 ± 1.1 −4.4 ± 3.7 −.28 ± .26 4.1 [−.5, 8.3]
84 [51.5-110.5] .3 ± 1.4 6.1 ± 5.0 .38 ± .28 3.8 [−.1, 6.3]
.333 .349 <.001 <.001 .975
17 [3.75-23.25] 13.5 [4-22.25] 2 [0-5]
20 [11-37.5] 19 [7-28.5] 3 [1.5-7]
.036 .068 .069
.14 [.03-.20] .12 [.03-.18] .02 [.00-.04]
.22 [.14-.33] .17 [.08-.29] .04 [.01-.06]
.020 .054 .047
Abbreviations: FIM, Functional Independence Measure; GNRI, Geriatric Nutritional Risk Index.
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Table 3. Stepwise linear regression analysis on the efficiency of the Functional Independence Measure Variable
Unadjusted coefficient
95%CI
Adjusted coefficient
P value
GNRI improvement Intracerebral hemorrhage Energy intake at admission (kcal/kg/day) Albumin Constant
.097 .207 .007 .008 −.127
.005-.189 .099-.314 .001-.013 −.120-.136 −.351-.098
.226 .412 .222 .014
.04 <.001 .043 .901 .263
Abbreviation: GNRI, Geriatric Nutritional Risk Index.
cerebrovascular disorders. First, an improvement in nutritional status following admission to discharge from hospital was associated with improved ADL in these patients. Second, the amount of energy intake at admission was associated with the degree of improvement in ADL. Our study demonstrated that an improvement in nutritional status was associated with an improvement in ADL in patients with cerebrovascular disorders during convalescence. Nutritional care could therefore be effective for patients requiring physical rehabilitation.8,23 However, only a few studies have described the relationship between nutritional improvement and physical outcome. Ha et al.23 reported that nutritional care to prevent weight loss in patients with stroke at risk of malnutrition contributed to an increase in hand-grip strength and improved quality of life including significant improvements in mobility, self-care ability, and usual activities. These findings are in accordance with the results of the current study. Finestone et al.24 reported that prolonged malnutrition during hospitalization, diagnosed by anthropometry or blood tests including serum albumin level, was associated with a longer hospital stay. However, they did not analyze the improvement in physical function or ADL in relation to nutritional status. We used the GNRI to evaluate changes in nutritional status. GNRI is calculated using the serum albumin level and BMI. Mizrahi et al.25 reported that improvement in albumin levels was associated with a gain in FIM in patients with hip fractures in a rehabilitation setting. We could not confirm the reason for the difference between the groups on the basis of the results from this study. However, we presume that the minor but continuing difference in dietary intake between the groups during hospitalization, which was estimated at 3.2 kcal/kg/day upon admission, might have contributed to the nutritional difference. Our data showed that the amount of initial energy intake was associated with improved ADL in patients with cerebrovascular disorders during the convalescent stage. The effect of nutritional intake in such patients may differ in the acute and rehabilitation settings. In the acute phase, the large interventional Feed Or Ordinary Diet (FOOD) trial26 concluded that nutritional supplementation in patients with acute stroke did not improve outcome. However, Nip et al.27 showed in an observational study that higher
energy intake in the early stage of stroke was an independent predictor for improvement in ADL, assessed by the Barthel Index at discharge. Evidence from a randomized control trial by Rabadi et al.8 showed that in the rehabilitation phase nutritional supplementation improved physical function during rehabilitation of patients following cerebrovascular disorders. In the present study, the subjects lived in a rehabilitation setting in Japan in which many patients were receiving rehabilitation therapy for more than 15 hours per week following a cerebrovascular disorder.20 We therefore consider that it is necessary to increase energy intake in this setting to a greater extent than in an acute setting. Nutritional care for patients with cerebrovascular disorders has an essential role for both malnutrition and physical rehabilitation.8 This combined strategy is named rehabilitation nutrition.12 Rehabilitation nutrition is a combination of both rehabilitation and nutritional care management that evaluates nutritional status and maximizes functionality in all people with disabilities.12 Because rehabilitation consumes a certain amount of energy, inappropriate nutritional care in malnourished patients with cerebrovascular disorders may worsen both malnutrition and ADL. Nutritional improvement combined with rehabilitation can therefore help more patients with cerebrovascular disorders to recover ADL. Our study had several limitations. First, because the study had a retrospective cross-sectional design, it was not possible to establish a causal relationship between improved nutritional status and ADL. Second, the relatively high number of patients with missing variables excluded from the study (16.1%) may have caused selection bias. Third, the amount and type of rehabilitation and the level of stroke severity were not analyzed. Fourth, all patients received intervention from the RNT. Therefore, we could not evaluate the effectiveness of this intervention. Finally, we could not adjust for all confounding factors because of the relatively low number of patients (i.e., n = 67). Further studies are therefore necessary in patients with cerebrovascular disorders to examine whether or not ADL can be improved to a greater extent by increased nutritional intake, determined by recording the time and intensity of rehabilitation and energy accumulation.
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In conclusion, the present study showed that nutritional improvement at discharge and energy intake at admission were associated with recovery of ADL in patients admitted to a rehabilitation hospital following a cerebrovascular disorder. From a clinical point of view, the current study indicated that intensive nutritional care added to physical rehabilitation led to better clinical outcomes. Further large-scale studies on other conditions are required to examine causality in greater detail. Acknowledgment: The authors wish to thank the rehabilitation nutrition team for their valuable assistance in this project.
References 1. 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. 2. The FOOD Trial Collaboration. Poor nutritional status on admission predicts poor outcomes after stroke: observational data from the FOOD trial. Stroke 2003;34:1450-1456. 3. Davis JP, Wong AA, Schluter PJ, et al. Impact of premorbid undernutrition on outcome in stroke patients. Stroke 2004;35:1930-1934. 4. Yoo SH, Kim JS, Kwon SU, et al. Undernutrition as a predictor of poor clinical outcomes in acute ischemic stroke patients. Arch Neurol 2008;65:39-43. 5. Foley NC, Martin RE, Salter KL, et al. A review of the relationship between dysphagia and malnutrition following stroke. J Rehabil Med 2009;41:707-713. 6. Davalos A, Ricart W, Gonzalez-Huix F, et al. Effect of malnutrition after acute stroke on clinical outcome. Stroke 1996;27:1028-1032. 7. Gariballa SE, Parker SG, Taub N, et al. A randomized, controlled, a single-blind trial of nutritional supplementation after acute stroke. JPEN J Parenter Enteral Nutr 1998;22:315-319. 8. Rabadi MH, Coar PL, Lukin M, et al. Intensive nutritional supplements can improve outcomes in stroke rehabilitation. Neurology 2008;71:1856-1861. 9. Kaiser MJ, Bauer JM, Ramsch C, et al. Frequency of malnutrition in older adults: a multinational perspective using the mini nutritional assessment. J Am Geriatr Soc 2010;58:1734-1738. 10. Beberashvili I, Azar A, Sinuani I, et al. Comparison analysis of nutritional scores for serial monitoring of nutritional status in hemodialysis patients. Clin J Am Soc Nephrol 2013;8:443-451. 11. Cermak NM, Res PT, de Groot LC, et al. Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr 2012;96:1454-1464. 12. Wakabayashi H, Sakuma K. Rehabilitation nutrition for sarcopenia with disability: a combination of both
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
rehabilitation and nutrition care management. J Cachexia Sarcopenia Muscle 2014;5:269-277. Bouillanne O, Morineau G, Dupont C, et al. Geriatric Nutritional Risk Index: a new index for evaluating at-risk elderly medical patients. Am J Clin Nutr 2005;82:777783. Cereda E, Vanotti A. The new Geriatric Nutritional Risk Index is a good predictor of muscle dysfunction in institutionalized older patients. Clin Nutr 2007;26:7883. Shah B, Sucher K, Hollenbeck CB. Comparison of ideal body weight equations and published height-weight tables with body mass index tables for healthy adults in the United States. Nutr Clin Pract 2006;21:312-319. Yamada K, Furuya R, Takita T, et al. Simplified nutritional screening tools for patients on maintenance hemodialysis. Am J Clin Nutr 2008;87:106-113. Kang SH, Cho KH, Park JW, et al. Impact of heavy proteinuria on clinical outcomes in patients on incident peritoneal dialysis. BMC Nephrol 2012;13:171. Kunieda K, Ohno T, Fujishima I, et al. Reliability and validity of a tool to measure the severity of dysphagia: the Food Intake Level Scale. J Pain Symptom Manage 2013;46:201-206. Keith RA, Granger CV, Hamilton BB, et al. The Functional Independence Measure: a new tool for rehabilitation. Adv Clin Rehabil 1987;1:6-18. Dodds TA, Martin DP, Stolov WC, et al. A validation of the functional independence measurement and its performance among rehabilitation inpatients. Arch Phys Med Rehabil 1993;74:531-536. Miyai I, Sonoda S, Nagai S, et al. Results of new policies for inpatient rehabilitation coverage in Japan. Neurorehabil Neural Repair 2011;25:540-547. Sonoda S, Saitoh E, Nagai S, et al. Full-time integrated treatment program, a new system for stroke rehabilitation in Japan: comparison with conventional rehabilitation. Am J Phys Med Rehabil 2004;83:88-93. Ha L, Hauge T, Spenning AB, et al. Individual, nutritional support prevents undernutrition, increases muscle strength and improves QoL among elderly at nutritional risk hospitalized for acute stroke: a randomized, controlled trial. Clin Nutr 2010;29:567-573. Finestone HM, Greene-Finestone LS, Wilson ES, et al. Prolonged length of stay and reduced functional improvement rate in malnourished stroke rehabilitation patients. Arch Phys Med Rehabil 1996;77:340-345. Mizrahi EH, Fleissig Y, Arad M, et al. Rehabilitation outcome of hip fracture patients: the importance of a positive albumin gain. Arch Gerontol Geriatr 2008;47:318326. Dennis MS, Lewis SC, Warlow C, et al. Routine oral nutritional supplementation for stroke patients in hospital (FOOD): a multicentre randomised controlled trial. Lancet 2005;365:755-763. Nip WF, Perry L, McLaren S, et al. Dietary intake, nutritional status and rehabilitation outcomes of stroke patients in hospital. J Hum Nutr Diet 2011;24:460469.