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Prevalence of nutritional risk and its impact on functional recovery in older inpatients on maintenance hemodialysis: a retrospective single-center cohort study

Prevalence of nutritional risk and its impact on functional recovery in older inpatients on... Background: Poor nutritional status and functional impairment are common in patients with end-stage renal disease (ERSD) on maintenance hemodialysis (MHD). Although nutritional status is associated with functional dependence and rehabilitation outcome in several diseases, this association remains unclear in patients with ESRD. The aim of this study was to investigate nutritional risk and its impact on rehabilitation outcomes in MHD inpatients who required rehabilitation. Methods: A retrospective cohort study was performed in 57 consecutive MHD inpatients aged 65 or older who had undergone rehabilitation. The Geriatric Nutritional Risk Index (GNRI) was used to assess nutritional risk and was calculated from height, dry body weight, and serum albumin level at the start of rehabilitation. Nutritional risk was defined as a GNRI < 91.2. The activities of daily living were used as a measure of rehabilitation outcome and were assessed by the Barthel Index (BI) at the start of rehabilitation and discharge. The Mann-Whitney U test and multiple regression analysis were performed. In the multiple regression analysis, BI gain was the dependent variable and age, sex, and GNRI were the independent variables. Results: The study included 34 men and 23 women. Mean (± SD) GNRI was 79.8 ± 9.9. Of the 57 patients, 50 (87.7%) were identified as having a nutritional risk and 7 were not. The gain in BI was significantly higher in patients without nutritional risk (median 50 vs. 10, p = 0.03). Multiple regression analysis showed GNRI was associated independently with BI gain (R =0.14, β =0.29, p =0.03). Conclusions: The majority of the MHD patients who underwent rehabilitation had a nutritional risk. Nutritional risk was associated independently with functional recovery. Keywords: Hemodialysis, Geriatric Nutritional Risk Index, Activities of daily living, Rehabilitation Background 19–26% of MHD patients have a functional impairment Poor nutritional status and functional impairment are in activities of daily living (ADLs); that is, they cannot common in patients with end-stage renal disease (ESRD) perform one or more tasks in ADLs without assistance on maintenance hemodialysis (MHD). In chronic kidney such as bathing, dressing, toilet use, transfer, feeding, disease, poor nutritional status due to multiple factors is and continence [4, 5]. This is especially apparent in categorized as protein-energy wasting and is associated MHD patients aged 65 years or older, with 52% reported with adverse clinical outcomes especially in ERSD patients to have impaired ADLs [6]. Because ADL impairment is [1]. The reported prevalence of malnutrition in dialysis associated with mortality in MHD patients [4], it is patients ranges between 18 and 75% [2, 3]. In addition, important to prevent and minimize these impairments. Rehabilitation is one method for treating impaired ADLs, and there are some ADL measures that can be * Correspondence: shimizu198966@gmail.com Department of Rehabilitation Medicine, Yokohama City University Medical used to assess rehabilitation outcomes [7, 8]. Although Center, 4-57 Urafune-chou, Minami ward, Yokohama City 232-0024, Japan © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 2 of 6 rehabilitation is very important, there have only been a Nutritional status was assessed by the Geriatric Nutri- small number of published reports on rehabilitation tional Risk Index (GNRI) [13]. This index has been reported outcomes in MHD patients with impaired ADLs [9]. to be an accurate tool for identifying MHD patients at Although nutritional status is associated with functional nutritional risk [14] and is calculated as GNRI = {14.89 × dependence and rehabilitation outcome in several diseases, serum albumin (g/dl)} + {41.7 × (body weight/ideal body this association remains unclear in patients with ESRD. weight)}. The ideal body weight was defined as the value A meta-analysis of 240 studies showed malnutrition, calculated from height and a body mass index (BMI) of and related risks were associated directly with functional 22 kg/m . In cases with a (body weight/ideal body dependency [10]. It has also been reported that malnutrition weight) > 1, this value was replaced by 1 [13]. For this is associated with poor rehabilitation outcomes in patients study, GNRI was calculated from the serum albumin level with stroke [11], chronic heart failure [12], or chronic ob- and body weight measured at the hemodialysis session structive pulmonary disease [12]. However, we are unaware closest to the start of rehabilitation. Serum albumin level of any previous reports on the association between nutri- (g/dL) was measured by an improved bromocresol purple tional status and rehabilitationoutcomesinMHD patients. (BCP) method before hemodialysis, body weight (kg) after The aim of this study was therefore to assess nutritional hemodialysis, and height (cm) at admission, with the risk and its impact on rehabilitation outcomes in MHD values expressed to one decimal place. In accordance with inpatients who required rehabilitation. a previous study [14], the risk of malnutrition in MHD patients was defined as a GNRI < 91.2. Methods ADLs were evaluated by physical therapists in charge of A retrospective cohort study was performed in 57 inpatients each patient at the start of rehabilitation and at discharge who had been admitted consecutively to the Yokohama City using the Barthel Index (BI). The BI consists of the following University Medical Center and were subsequently referred ten items: feeding, moving from bed to a wheelchair and by attending physicians to the Department of Rehabilitation back, grooming, toilet use, bathing, mobilization (level sur- Medicine between April 2015 and March 2017. face), going up and down stairs, dressing, bowel continence, The study included patients aged 65 or older who had and bladder continence. The BI score ranges from 0 to 100, undergone both maintenance hemodialysis and rehabili- with higher scores indicating greater functional inde- tation during their hospital stay. Patients were excluded pendence of ADLs [8]. Age, sex, C-reactive protein from the study if they had undergone new or temporary (CRP, mg/dL), etiology of chronic kidney disease, causative hemodialysis, had less than two rehabilitation sessions, disease for admission, and number of days from admission or had died during their hospital stay. to the start of rehabilitation and from the start of rehabili- All participants underwent hemodialysis three times a tation to discharge were also recorded. week and physical therapy five times a week. They A previous study demonstrated that the minimal clinically underwent physical therapy of 20 or 40 min per session, important difference of the 20-point BI in stroke patients while some participants received occupational therapy was 1.85 [15], equivalent to 9.25 in the 100-point BI scale. and/or speech therapy if required. Rehabilitation was In patients with chronic kidney disease who were hospital- performed mainly in an exercise room but sometimes ized and underwent physical therapy, the standard deviation was carried out at the bedside when patients could not of the BI was reported to be 13.4 [16]. Assuming the propor- come to the exercise room because of their physical con- tion of patients with or without nutritional risk was equal dition. According to the disease, general condition, and and using the values α = 0.05, β =0.8, δ = 9.25, and σ = 13.4, ADLs of each patient, the doctors made a rehabilitation we calculated that it was necessary to include 34 participants order that included the location, outline of the program, in each group in order to reject the null hypothesis that frequency, and length of each session. The therapist in the gain in BI was equal. We therefore planned to recruit charge of each patient decided the details of the rehabilita- 68 patients in the study. tion program. Each program was designed with the purpose The statistical analyses were performed using JMP ® Pro of improving or maintaining ADL. Each program mainly 12.2 (SAS Institute Inc.; Cary, NC, USA). Fisher’sexact included a range of motion exercises, resistance training, test and the Mann-Whitney U test were used to determine and practice of ADLs. The practice of ADLs regarding whether or not there were differences in the characteris- moving such as sitting, standing up, walking, and going up tics of patients with or without a risk of malnutrition. A and down stairs was performed as physical therapy. The multiple regression analysis was performed to examine practice of other activities such as feeding, grooming, and whether GNRI was associated independently with the gain dressing was performed as occupational therapy and speech in BI from the start of rehabilitation to discharge. In this therapy. If the patient was fully independent for ADLs, analysis, the dependent variable was BI gain, and the inde- resistance training and aerobic exercise were performed to pendent variables were age, sex, and GNRI. Age and sex achieve further improvement in physical function. were selected as the regression factors because according Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 3 of 6 to previous studies [17, 18], they have a strong probability healthcare settings, showed malnutrition, and its risks of affecting rehabilitation outcome. A p value < 0.05 was were associated directly with a setting-related level of considered statistically significant. dependence. The prevalence of malnutrition in rehabili- tation/sub-acute care was also shown to be higher than Results in all other settings including the community, outpatients, A total of 100 patients underwent both hemodialysis and home-care services, hospitals, nursing homes, and long- rehabilitation during the study period. Thirty-seven patients term care [10]. Granger et al. reported that a BI of 60 who underwent new or temporary hemodialysis during their points appeared to be a pivotal score at which stroke hospital stay, 1 patient who underwent rehabilitation less patients moved from functional dependency to assisted than two times, and 5 patients who died were excluded from independence [19]. In the present study, the upper quartile the analysis. The remaining 57 patients (34 men, 23 women) of BI at the start of rehabilitation was 60, and therefore, were included in the study; all underwent physical therapy, the majority of the patients were considered to be func- 14 had occupational therapy, and 13 received speech tionally dependent. It is possible this high rate of patients therapy. with functional dependency was the reason for the high Table 1 shows the results of the comparison of differ- prevalence of nutritional risk observed in our study. ences in clinical indices between patients with or without a We therefore consider that nutritional assessment is risk of malnutrition. Mean GNRI (± SD) at the start of very important in MHD patients who are undergoing rehabilitation was 79.8 ± 9.9. Fifty patients (87.7%) were rehabilitation. identified as being at risk of malnutrition and 7 patients Our data showed nutritional risk in MHD inpatients (12.3%, all males) were not. Median BI at the start of was associated independently with a gain in the BI and rehabilitation was 35 with an interquartile range of 10–60. that patients without nutritional risk achieved greater The gain in BI from the start of rehabilitation to discharge gains in this index. Other studies have reported the impact was significantly greater in patients not at risk of mal- of GNRI score in MHD patients on mortality [20], physical nutrition than in patients at risk of malnutrition. There function [21], and quality of life [21]. Our study is the first was no significant difference between the two groups in to show an influence of GNRI on rehabilitation outcome the number of days from either admission to the start of in MHD patients. This result indicates that the GNRI may rehabilitation or the start of rehabilitation to discharge. be useful for predicting rehabilitation outcomes in MHD Table 2 shows the results of the multiple regression inpatients. We consider a cutoff value of GNRI < 91.2 may analysis of the gain in BI adjusted for age, sex, and be useful for predicting whether or not rehabilitation will GNRI. GNRI was the only factor associated independently be more effective. with BI gain (β = 0.268, 95% confidence intervals 0.080, The high prevalence of nutritional risk and its impact 1.494, p = 0.030). We estimated that CRP may affect serum on rehabilitation outcomes indicate the importance of albumin concentration. However, CRP could not be rehabilitation nutrition. Yoshimura et al. reported that included in the multiple regression analysis because it nutritional intervention added to resistance training during correlated strongly with both serum albumin concentration convalescent rehabilitation improved ADLs in older patients (r = − 0.607, p < 0.001) and GNRI (r = − 0.523, p <0.001). with a decreased muscle mass [22]. There are only a small number of reports on the combination of nutritional inter- Discussion vention and exercise training in adult MHD patients, and This study obtained two main findings regarding the the benefit of this combination therefore remains uncertain prevalence of nutritional risk and its impact on rehabilita- [23, 24]. In addition, there are no reports on this com- tion outcome in older MHD inpatients who had undergone bination in older MHD patients or MHD patients with rehabilitation. Firstly, 87.7% of MHD patients who under- impaired ADLs. Nutritional intervention added to rehabili- went rehabilitation were identified as having a nutritional tation has the potential to improve both nutritional status risk, assessed by GNRI. Secondly, nutritional risk was and rehabilitation outcomes in MHD patients with impaired associated independently with rehabilitation outcome. ADLs. There is also evidence in patients with stroke and The majority of MHD patients in our study who hip fracture that nutritional improvement is associated underwent rehabilitation were identified as having a nutri- with greater gains in ADLs [25–27]. The concept of tional risk. Yamada et al. reported a prevalence of 39.3% rehabilitation nutrition involving rehabilitation and man- for nutritional risk in MHD patients [14], a value lower agement of nutritional care is important in MHD patients than that observed in our study. A possible reason for this with impaired ADLs [28]. difference may be variations in the characteristics of the This study had some limitations. First, the only sub- subjects, as the Yamada et al. study was on outpatients jects in the study were those referred to the Department and also included patients younger than 65 years. Evidence of Rehabilitation Medicine and did not include patients from a meta-analysis of 240 studies, including various admitted consecutively to the target hospital during the Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 4 of 6 Table 1 Characteristics and comparison of clinical indices in patients with or without a nutritional risk Total (n = 57) With a nutritional risk (n = 50) Without a nutritional risk (n =7) P value Age (years), mean ± SD 73.8 ± 6.4 73.8 ± 6.5 70.5 ± 5.8 0.809 Sex, males/females 34/23 27/23 7/0 0.034 Albumin (g/dL), mean ± SD 2.8 ± 0.6 2.7 ± 0.4 3.65 ± 0.2 <.001 BMI (kg/m ), mean ± SD 20.8 ± 3.1 20.6 ± 3.2 22.1 ± 2.4 0.016 GNRI, mean ± SD 79.8 ± 9.9 77.6 ± 8.3 96.0 ± 1.9 <.001 CRP (mg/dL), median (IQR) 3.365 (0.98–7.742) 3.797 (1.621–9.847) 0.441 (0.235–1.863) 0.014 BI at baseline, median (IQR) 35 (10–60) 35 (11.25–60) 30 (7.5–45) 0.750 BI at discharge, median (IQR) 70 (30–90) 65 (25–90) 85 (77.5–92.5) 0.121 BI gain, median (IQR) 15 (0–30) 10 (0–30) 50 (25–85) 0.027 Length of stay (days), median (IQR) 37 (22–52) 38.5 (23.25–51.25) 29 (19.5–44) 0.436 Days from A to R (days), median (IQR) 8 (5–14) 9 (6–14) 7 (3–8.5) 0.065 Duration of rehabilitation (days), median (IQR) 27 (15–36) 27 (15–36) 25 (15–35.5) 0.855 Duration of hemodialysis (years), median (IQR) 7 (6–12) 7 (3–13) 6 (1–7) 0.200 Causative disease for admission (n) Ischemic heart disease 10 9 1 Aortic disease 4 4 Valvular disease of the heart 4 4 Congestive heart failure 3 3 Cerebral infarction 7 3 4 Parkinson’s disease 1 1 Lumbar disease 6 6 Fracture 3 3 Osteoarthritis 3 3 Psychiatric disease 3 2 1 Perforation of the digestive tract 2 2 Pneumonia 2 2 Shunt complication 2 2 Other 7 7 Etiology of chronic kidney disease (n) Diabetic nephropathy 30 27 3 Nephrosclerosis 9 6 3 Chronic glomerulonephritis; 6 6 Multiple renal cysts 3 2 1 Rapidly progressive glomerulonephritis 1 1 SLE nephritis 1 1 Nephronophthisis 1 1 Chronic pyelonephritis 1 1 Drug-induced kidney injury 1 1 Renal infarction 1 1 Unknown 3 3 BMI body mass index, GNRI Geriatric Nutritional Risk Index, BI Barthel Index, Days from A to R days from admission to start of rehabilitation, IQR interquartile range, SLE systemic lupus erythematosus Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 5 of 6 Table 2 Results of the multiple regression analysis with gain in Availability of data and materials All data generated or analyzed during this study are included in this article. the Barthel Index as the dependent variable B β 95% confidence interval of B P value Authors’ contributions YS conceived the study and drafted the manuscript. YS, TF, and HW Age − 0.997 − 0.234 − 2.098, 0.1046 0.075 interpreted the data and revised the manuscript. All authors read and Sex 2.686 0.098 − 4.421, 9.794 0.452 approved the final manuscript. GNRI 0.787 0.268 0.080, 1.494 0.030 Ethics approval and consent to participate R = 0.139 This study was approved by the ethics committee of the Yokohama City GNRI Geriatric Nutritional Risk Index University Medical Center. The approved number is B171100008. The study protocol and contact address/telephone number were available on the study period. The results of this study can therefore not website of the Yokohama City University Medical Center, so all participants had the opportunity to decline to participate in the study. be applied to the general population of hospitalized MHD patients. Second, the nutritional risk was assessed Consent for publication using only the GNRI and did not include other more Not applicable. reliable and detailed measures. Third, the requisite sample Competing interests size was not reached. Fourth, we used serum albumin level The authors declare that they have no competing interests. measured by an improved BCP method that has been used widely over the past decade, replacing the bromocresol Publisher’sNote green (BCG) method. It has been reported that the percent- Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. age of malnourished patients assessed by controlling nutri- tional status (CONNUT) differs depending on whether the Received: 21 July 2018 Accepted: 8 November 2018 BCP or BCG method is used to measure albumen level [29]. The Japanese Society of Laboratory Medicine recommends References that if the serum albumin level measured by the BCP 1. Fouque D, Kalantar-Zadeh K, Kopple J, Cano N, Chauveau P, Cuppari L, et al. method is ≤ 3.5 g/L, the cutoff value should be modified A proposed nomenclature and diagnostic criteria for protein-energy wasting in acute and chronic kidney disease. Kidney Int. 2008;73(3):391–8. from the value developed for the BCG method [30]. Because 2. Kopple JD. McCollum Award Lecture, 1996: protein-energy malnutrition in the BCG method was the main test used in the past, the maintenance dialysis patients. Am J Clin Nutr. 1997;65(5):1544–57. GNRI would have been developed using the serum albumin 3. Kalantar-Zadeh K, Ikizler TA, Block G, Avram MM, Kopple JD. Malnutrition- inflammation complex syndrome in dialysis patients: causes and level measured by that method. Therefore, it is possible that consequences. Am J Kidney Dis. 2003;42(5):864–81. the serum albumin level needs to be modified in our study. 4. Bossola M, Di Stasio E, Antocicco M, Pepe G, Tazza L, Zuccalà G, et al. Furthermore, we were not able to consider factors in the Functional impairment is associated with an increased risk of mortality in patients on chronic hemodialysis. BMC Nephrol. 2016;17(1):72. https://doi. multiple regression analysis that were likely to affect the gain org/10.1186/s12882-016-0302-y. in BI, such as causative disease for admission because of the 5. Jassal SV, Karaboyas A, Comment LA, Bieber BA, Morgenstern H, Sen A, et al. small number of the participants, and CRP because of Functional dependence and mortality in the international dialysis outcomes and practice patterns study (DOPPS). Am J Kidney Dis. 2016;67(2):283–92. its multicollinearity with the GNRI. Further studies 6. Cook WL, Jassal SV. Functional dependencies among the elderly on investigating the association between nutritional status hemodialysis. Kidney Int. 2008;73(11):1289–95. and rehabilitation outcome in MHD patients should 7. Katz S, Ford Ford AB, Moskowitz RW, Jackson BA, Jaffe MW. Studies of illness in the aged. The index of ADL: a standardized measure of biological and perform a more detailed nutritional assessment in order psychosocial function. JAMA. 1963;185:914–9. to diagnose malnutrition and protein-energy wasting. 8. Mahoney FI, Barthel DW. Functional evaluation: the Barthel Index. Md State Med J. 1965;14:61–5. 9. Endo M, Nakamura Y, Murakami T, Tsukahara H, Watanabe Y, et al. Conclusion Rehabilitation improves prognosis and activities of daily living in The majority of the MHD patients who underwent rehabili- hemodialysis patients with low activities of daily living. Phys Ther Res. 2017; tation had a nutritional risk. Nutritional risk was associated 20(1):9–15. 10. Cereda E, Pedrolli C, Klersy C, Bonardi C, Quarleri L, Cappello S, et al. independently with rehabilitation outcome. The GNRI has Nutritional status in older persons according to healthcare setting: a potential as a predictor of rehabilitation outcome in MHD systematic review and meta-analysis of prevalence data using MNA. Clin patients. Nutr. 2016;35(6):1282–90. 11. Davis JP, Wong AA, Schluter PJ, Henderson RD, O’Sullivan JD, Read SJ. Abbreviations Impact of premorbid undernutrition on outcome in stroke patients. Stroke. ADLs: Activities of daily living; BI: Barthel Index; BMI: Body mass index; 2004;35(8):1930–4. ERSD: End-stage renal disease; GNRI: Geriatric Nutritional Risk Index; 12. Anker SD, John M, Pedersen PU, Raguso C, Cicoira M, Dardai E, et al. ESPEN MHD: Maintenance hemodialysis guidelines on enteral nutrition: cardiology and pulmonology. Clin Nutr. 2006;25(2):311–8. Acknowledgements 13. Bouillanne O, Morineau G, Dupont C, Coulombel I, Vincent JP, Nicolis I, et al. We are grateful to all the staff in the Department of Rehabilitation Medicine, Geriatric nutritional risk index: a new index for evaluating at-risk elderly Yokohama University Medical Center. medical patients. Am J Clin Nutr. 2005;82(4):777–83. 14. Yamada K, Furuya R, Takita T, Maruyama Y, Yamaguchi Y, Ohkawa S, et al. Funding Simplified nutritional screening tools for patients on maintenance We have no financial support. hemodialysis. Am J Clin Nutr. 2008;87(1):106–13. Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 6 of 6 15. Hsieh YW, Wang CH, Wu SC, Chen PC, Sheu CF, Hsieh CL. Establishing the minimal clinically important difference of the Barthel Index in stroke patients. Neurorehabil Neural Repair. 2007;21(3):233–8. 16. Sarmento LA, Pinto JS, da Silva AP, Cabral CM, Chiavegato LD. Effect of conventional physical therapy and Pilates in functionality, respiratory muscle strength and ability to exercise in hospitalized chronic renal patients: a randomized controlled trial. Clin Rehabil. 2017;31(4):508–20. 17. Inouye M, Kishi K, Ikeda Y, Takada M, Katoh J, Iwahashi M, et al. Prediction of functional outcome after stroke rehabilitation. Am J Phys Med Rehabil. 2000; 79(6):513–8. 18. Reeves MJ, Bushnell CD, Howard G, Gargano JW, Duncan PW, Lynch G, et al. Sex differences in stroke: epidemiology, clinical presentation, medical care, and outcomes. Lancet Neurol. 2008;7(10):915–26. 19. Granger CV, Dewis LS, Peters NC, Sherwood CC, Barrett JE. Stroke rehabilitation: analysis of repeated Barthel index measures. Arch Phys Med Rehabil. 1979;60(1):145–54. 20. Kobayashi I, Ishimura E, Kato Y, Okuno S, Yamamoto T, Yamakawa T, et al. Geriatric Nutritional Risk Index, a simplified nutritional screening index, is a significant predictor of mortality in chronic dialysis patients. Nephrol Dial Transplant. 2010;25(10):3361–5. 21. Beberashvili I, Azar A, Sinuani I, Shapiro G, Feldman L, Sandbank J, et al. Geriatric nutritional risk index, muscle function, quality of life and clinical outcome in hemodialysis patients. Clin Nutr. 2016;35(6):1522–9. 22. Yoshimura Y, Uchida K, Jeong S, Yamaga M. Effects of nutritional supplements on muscle mass and activities of daily living in elderly rehabilitation patients with decreased muscle mass: a randomized controlled trial. J Nutr Health Aging. 2016;20(2):185–91. 23. Dong J, Sundell MB, Pupim LB, Wu P, Shintani A, Ikizler TA. The effect of resistance exercise to augment long-term benefits of intradialytic oral nutritional supplementation in chronic hemodialysis patients. J Ren Nutr. 2011;21(2):149–59. 24. 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Rinsho Byori. 2014;62(1):5–9 (in Japanese). http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Renal Replacement Therapy Springer Journals

Prevalence of nutritional risk and its impact on functional recovery in older inpatients on maintenance hemodialysis: a retrospective single-center cohort study

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Medicine & Public Health; Nephrology
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Abstract

Background: Poor nutritional status and functional impairment are common in patients with end-stage renal disease (ERSD) on maintenance hemodialysis (MHD). Although nutritional status is associated with functional dependence and rehabilitation outcome in several diseases, this association remains unclear in patients with ESRD. The aim of this study was to investigate nutritional risk and its impact on rehabilitation outcomes in MHD inpatients who required rehabilitation. Methods: A retrospective cohort study was performed in 57 consecutive MHD inpatients aged 65 or older who had undergone rehabilitation. The Geriatric Nutritional Risk Index (GNRI) was used to assess nutritional risk and was calculated from height, dry body weight, and serum albumin level at the start of rehabilitation. Nutritional risk was defined as a GNRI < 91.2. The activities of daily living were used as a measure of rehabilitation outcome and were assessed by the Barthel Index (BI) at the start of rehabilitation and discharge. The Mann-Whitney U test and multiple regression analysis were performed. In the multiple regression analysis, BI gain was the dependent variable and age, sex, and GNRI were the independent variables. Results: The study included 34 men and 23 women. Mean (± SD) GNRI was 79.8 ± 9.9. Of the 57 patients, 50 (87.7%) were identified as having a nutritional risk and 7 were not. The gain in BI was significantly higher in patients without nutritional risk (median 50 vs. 10, p = 0.03). Multiple regression analysis showed GNRI was associated independently with BI gain (R =0.14, β =0.29, p =0.03). Conclusions: The majority of the MHD patients who underwent rehabilitation had a nutritional risk. Nutritional risk was associated independently with functional recovery. Keywords: Hemodialysis, Geriatric Nutritional Risk Index, Activities of daily living, Rehabilitation Background 19–26% of MHD patients have a functional impairment Poor nutritional status and functional impairment are in activities of daily living (ADLs); that is, they cannot common in patients with end-stage renal disease (ESRD) perform one or more tasks in ADLs without assistance on maintenance hemodialysis (MHD). In chronic kidney such as bathing, dressing, toilet use, transfer, feeding, disease, poor nutritional status due to multiple factors is and continence [4, 5]. This is especially apparent in categorized as protein-energy wasting and is associated MHD patients aged 65 years or older, with 52% reported with adverse clinical outcomes especially in ERSD patients to have impaired ADLs [6]. Because ADL impairment is [1]. The reported prevalence of malnutrition in dialysis associated with mortality in MHD patients [4], it is patients ranges between 18 and 75% [2, 3]. In addition, important to prevent and minimize these impairments. Rehabilitation is one method for treating impaired ADLs, and there are some ADL measures that can be * Correspondence: shimizu198966@gmail.com Department of Rehabilitation Medicine, Yokohama City University Medical used to assess rehabilitation outcomes [7, 8]. Although Center, 4-57 Urafune-chou, Minami ward, Yokohama City 232-0024, Japan © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 2 of 6 rehabilitation is very important, there have only been a Nutritional status was assessed by the Geriatric Nutri- small number of published reports on rehabilitation tional Risk Index (GNRI) [13]. This index has been reported outcomes in MHD patients with impaired ADLs [9]. to be an accurate tool for identifying MHD patients at Although nutritional status is associated with functional nutritional risk [14] and is calculated as GNRI = {14.89 × dependence and rehabilitation outcome in several diseases, serum albumin (g/dl)} + {41.7 × (body weight/ideal body this association remains unclear in patients with ESRD. weight)}. The ideal body weight was defined as the value A meta-analysis of 240 studies showed malnutrition, calculated from height and a body mass index (BMI) of and related risks were associated directly with functional 22 kg/m . In cases with a (body weight/ideal body dependency [10]. It has also been reported that malnutrition weight) > 1, this value was replaced by 1 [13]. For this is associated with poor rehabilitation outcomes in patients study, GNRI was calculated from the serum albumin level with stroke [11], chronic heart failure [12], or chronic ob- and body weight measured at the hemodialysis session structive pulmonary disease [12]. However, we are unaware closest to the start of rehabilitation. Serum albumin level of any previous reports on the association between nutri- (g/dL) was measured by an improved bromocresol purple tional status and rehabilitationoutcomesinMHD patients. (BCP) method before hemodialysis, body weight (kg) after The aim of this study was therefore to assess nutritional hemodialysis, and height (cm) at admission, with the risk and its impact on rehabilitation outcomes in MHD values expressed to one decimal place. In accordance with inpatients who required rehabilitation. a previous study [14], the risk of malnutrition in MHD patients was defined as a GNRI < 91.2. Methods ADLs were evaluated by physical therapists in charge of A retrospective cohort study was performed in 57 inpatients each patient at the start of rehabilitation and at discharge who had been admitted consecutively to the Yokohama City using the Barthel Index (BI). The BI consists of the following University Medical Center and were subsequently referred ten items: feeding, moving from bed to a wheelchair and by attending physicians to the Department of Rehabilitation back, grooming, toilet use, bathing, mobilization (level sur- Medicine between April 2015 and March 2017. face), going up and down stairs, dressing, bowel continence, The study included patients aged 65 or older who had and bladder continence. The BI score ranges from 0 to 100, undergone both maintenance hemodialysis and rehabili- with higher scores indicating greater functional inde- tation during their hospital stay. Patients were excluded pendence of ADLs [8]. Age, sex, C-reactive protein from the study if they had undergone new or temporary (CRP, mg/dL), etiology of chronic kidney disease, causative hemodialysis, had less than two rehabilitation sessions, disease for admission, and number of days from admission or had died during their hospital stay. to the start of rehabilitation and from the start of rehabili- All participants underwent hemodialysis three times a tation to discharge were also recorded. week and physical therapy five times a week. They A previous study demonstrated that the minimal clinically underwent physical therapy of 20 or 40 min per session, important difference of the 20-point BI in stroke patients while some participants received occupational therapy was 1.85 [15], equivalent to 9.25 in the 100-point BI scale. and/or speech therapy if required. Rehabilitation was In patients with chronic kidney disease who were hospital- performed mainly in an exercise room but sometimes ized and underwent physical therapy, the standard deviation was carried out at the bedside when patients could not of the BI was reported to be 13.4 [16]. Assuming the propor- come to the exercise room because of their physical con- tion of patients with or without nutritional risk was equal dition. According to the disease, general condition, and and using the values α = 0.05, β =0.8, δ = 9.25, and σ = 13.4, ADLs of each patient, the doctors made a rehabilitation we calculated that it was necessary to include 34 participants order that included the location, outline of the program, in each group in order to reject the null hypothesis that frequency, and length of each session. The therapist in the gain in BI was equal. We therefore planned to recruit charge of each patient decided the details of the rehabilita- 68 patients in the study. tion program. Each program was designed with the purpose The statistical analyses were performed using JMP ® Pro of improving or maintaining ADL. Each program mainly 12.2 (SAS Institute Inc.; Cary, NC, USA). Fisher’sexact included a range of motion exercises, resistance training, test and the Mann-Whitney U test were used to determine and practice of ADLs. The practice of ADLs regarding whether or not there were differences in the characteris- moving such as sitting, standing up, walking, and going up tics of patients with or without a risk of malnutrition. A and down stairs was performed as physical therapy. The multiple regression analysis was performed to examine practice of other activities such as feeding, grooming, and whether GNRI was associated independently with the gain dressing was performed as occupational therapy and speech in BI from the start of rehabilitation to discharge. In this therapy. If the patient was fully independent for ADLs, analysis, the dependent variable was BI gain, and the inde- resistance training and aerobic exercise were performed to pendent variables were age, sex, and GNRI. Age and sex achieve further improvement in physical function. were selected as the regression factors because according Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 3 of 6 to previous studies [17, 18], they have a strong probability healthcare settings, showed malnutrition, and its risks of affecting rehabilitation outcome. A p value < 0.05 was were associated directly with a setting-related level of considered statistically significant. dependence. The prevalence of malnutrition in rehabili- tation/sub-acute care was also shown to be higher than Results in all other settings including the community, outpatients, A total of 100 patients underwent both hemodialysis and home-care services, hospitals, nursing homes, and long- rehabilitation during the study period. Thirty-seven patients term care [10]. Granger et al. reported that a BI of 60 who underwent new or temporary hemodialysis during their points appeared to be a pivotal score at which stroke hospital stay, 1 patient who underwent rehabilitation less patients moved from functional dependency to assisted than two times, and 5 patients who died were excluded from independence [19]. In the present study, the upper quartile the analysis. The remaining 57 patients (34 men, 23 women) of BI at the start of rehabilitation was 60, and therefore, were included in the study; all underwent physical therapy, the majority of the patients were considered to be func- 14 had occupational therapy, and 13 received speech tionally dependent. It is possible this high rate of patients therapy. with functional dependency was the reason for the high Table 1 shows the results of the comparison of differ- prevalence of nutritional risk observed in our study. ences in clinical indices between patients with or without a We therefore consider that nutritional assessment is risk of malnutrition. Mean GNRI (± SD) at the start of very important in MHD patients who are undergoing rehabilitation was 79.8 ± 9.9. Fifty patients (87.7%) were rehabilitation. identified as being at risk of malnutrition and 7 patients Our data showed nutritional risk in MHD inpatients (12.3%, all males) were not. Median BI at the start of was associated independently with a gain in the BI and rehabilitation was 35 with an interquartile range of 10–60. that patients without nutritional risk achieved greater The gain in BI from the start of rehabilitation to discharge gains in this index. Other studies have reported the impact was significantly greater in patients not at risk of mal- of GNRI score in MHD patients on mortality [20], physical nutrition than in patients at risk of malnutrition. There function [21], and quality of life [21]. Our study is the first was no significant difference between the two groups in to show an influence of GNRI on rehabilitation outcome the number of days from either admission to the start of in MHD patients. This result indicates that the GNRI may rehabilitation or the start of rehabilitation to discharge. be useful for predicting rehabilitation outcomes in MHD Table 2 shows the results of the multiple regression inpatients. We consider a cutoff value of GNRI < 91.2 may analysis of the gain in BI adjusted for age, sex, and be useful for predicting whether or not rehabilitation will GNRI. GNRI was the only factor associated independently be more effective. with BI gain (β = 0.268, 95% confidence intervals 0.080, The high prevalence of nutritional risk and its impact 1.494, p = 0.030). We estimated that CRP may affect serum on rehabilitation outcomes indicate the importance of albumin concentration. However, CRP could not be rehabilitation nutrition. Yoshimura et al. reported that included in the multiple regression analysis because it nutritional intervention added to resistance training during correlated strongly with both serum albumin concentration convalescent rehabilitation improved ADLs in older patients (r = − 0.607, p < 0.001) and GNRI (r = − 0.523, p <0.001). with a decreased muscle mass [22]. There are only a small number of reports on the combination of nutritional inter- Discussion vention and exercise training in adult MHD patients, and This study obtained two main findings regarding the the benefit of this combination therefore remains uncertain prevalence of nutritional risk and its impact on rehabilita- [23, 24]. In addition, there are no reports on this com- tion outcome in older MHD inpatients who had undergone bination in older MHD patients or MHD patients with rehabilitation. Firstly, 87.7% of MHD patients who under- impaired ADLs. Nutritional intervention added to rehabili- went rehabilitation were identified as having a nutritional tation has the potential to improve both nutritional status risk, assessed by GNRI. Secondly, nutritional risk was and rehabilitation outcomes in MHD patients with impaired associated independently with rehabilitation outcome. ADLs. There is also evidence in patients with stroke and The majority of MHD patients in our study who hip fracture that nutritional improvement is associated underwent rehabilitation were identified as having a nutri- with greater gains in ADLs [25–27]. The concept of tional risk. Yamada et al. reported a prevalence of 39.3% rehabilitation nutrition involving rehabilitation and man- for nutritional risk in MHD patients [14], a value lower agement of nutritional care is important in MHD patients than that observed in our study. A possible reason for this with impaired ADLs [28]. difference may be variations in the characteristics of the This study had some limitations. First, the only sub- subjects, as the Yamada et al. study was on outpatients jects in the study were those referred to the Department and also included patients younger than 65 years. Evidence of Rehabilitation Medicine and did not include patients from a meta-analysis of 240 studies, including various admitted consecutively to the target hospital during the Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 4 of 6 Table 1 Characteristics and comparison of clinical indices in patients with or without a nutritional risk Total (n = 57) With a nutritional risk (n = 50) Without a nutritional risk (n =7) P value Age (years), mean ± SD 73.8 ± 6.4 73.8 ± 6.5 70.5 ± 5.8 0.809 Sex, males/females 34/23 27/23 7/0 0.034 Albumin (g/dL), mean ± SD 2.8 ± 0.6 2.7 ± 0.4 3.65 ± 0.2 <.001 BMI (kg/m ), mean ± SD 20.8 ± 3.1 20.6 ± 3.2 22.1 ± 2.4 0.016 GNRI, mean ± SD 79.8 ± 9.9 77.6 ± 8.3 96.0 ± 1.9 <.001 CRP (mg/dL), median (IQR) 3.365 (0.98–7.742) 3.797 (1.621–9.847) 0.441 (0.235–1.863) 0.014 BI at baseline, median (IQR) 35 (10–60) 35 (11.25–60) 30 (7.5–45) 0.750 BI at discharge, median (IQR) 70 (30–90) 65 (25–90) 85 (77.5–92.5) 0.121 BI gain, median (IQR) 15 (0–30) 10 (0–30) 50 (25–85) 0.027 Length of stay (days), median (IQR) 37 (22–52) 38.5 (23.25–51.25) 29 (19.5–44) 0.436 Days from A to R (days), median (IQR) 8 (5–14) 9 (6–14) 7 (3–8.5) 0.065 Duration of rehabilitation (days), median (IQR) 27 (15–36) 27 (15–36) 25 (15–35.5) 0.855 Duration of hemodialysis (years), median (IQR) 7 (6–12) 7 (3–13) 6 (1–7) 0.200 Causative disease for admission (n) Ischemic heart disease 10 9 1 Aortic disease 4 4 Valvular disease of the heart 4 4 Congestive heart failure 3 3 Cerebral infarction 7 3 4 Parkinson’s disease 1 1 Lumbar disease 6 6 Fracture 3 3 Osteoarthritis 3 3 Psychiatric disease 3 2 1 Perforation of the digestive tract 2 2 Pneumonia 2 2 Shunt complication 2 2 Other 7 7 Etiology of chronic kidney disease (n) Diabetic nephropathy 30 27 3 Nephrosclerosis 9 6 3 Chronic glomerulonephritis; 6 6 Multiple renal cysts 3 2 1 Rapidly progressive glomerulonephritis 1 1 SLE nephritis 1 1 Nephronophthisis 1 1 Chronic pyelonephritis 1 1 Drug-induced kidney injury 1 1 Renal infarction 1 1 Unknown 3 3 BMI body mass index, GNRI Geriatric Nutritional Risk Index, BI Barthel Index, Days from A to R days from admission to start of rehabilitation, IQR interquartile range, SLE systemic lupus erythematosus Shimizu et al. Renal Replacement Therapy (2018) 4:48 Page 5 of 6 Table 2 Results of the multiple regression analysis with gain in Availability of data and materials All data generated or analyzed during this study are included in this article. the Barthel Index as the dependent variable B β 95% confidence interval of B P value Authors’ contributions YS conceived the study and drafted the manuscript. YS, TF, and HW Age − 0.997 − 0.234 − 2.098, 0.1046 0.075 interpreted the data and revised the manuscript. All authors read and Sex 2.686 0.098 − 4.421, 9.794 0.452 approved the final manuscript. GNRI 0.787 0.268 0.080, 1.494 0.030 Ethics approval and consent to participate R = 0.139 This study was approved by the ethics committee of the Yokohama City GNRI Geriatric Nutritional Risk Index University Medical Center. The approved number is B171100008. The study protocol and contact address/telephone number were available on the study period. The results of this study can therefore not website of the Yokohama City University Medical Center, so all participants had the opportunity to decline to participate in the study. be applied to the general population of hospitalized MHD patients. Second, the nutritional risk was assessed Consent for publication using only the GNRI and did not include other more Not applicable. reliable and detailed measures. Third, the requisite sample Competing interests size was not reached. Fourth, we used serum albumin level The authors declare that they have no competing interests. measured by an improved BCP method that has been used widely over the past decade, replacing the bromocresol Publisher’sNote green (BCG) method. It has been reported that the percent- Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. age of malnourished patients assessed by controlling nutri- tional status (CONNUT) differs depending on whether the Received: 21 July 2018 Accepted: 8 November 2018 BCP or BCG method is used to measure albumen level [29]. The Japanese Society of Laboratory Medicine recommends References that if the serum albumin level measured by the BCP 1. Fouque D, Kalantar-Zadeh K, Kopple J, Cano N, Chauveau P, Cuppari L, et al. method is ≤ 3.5 g/L, the cutoff value should be modified A proposed nomenclature and diagnostic criteria for protein-energy wasting in acute and chronic kidney disease. Kidney Int. 2008;73(3):391–8. from the value developed for the BCG method [30]. Because 2. Kopple JD. McCollum Award Lecture, 1996: protein-energy malnutrition in the BCG method was the main test used in the past, the maintenance dialysis patients. 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Published: Nov 19, 2018

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