Sarcopenic Obesity and Activities of Daily Living in Stroke Rehabilitation Patients: A Cross-Sectional Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Participants
2.2. Data Collection
2.3. Main Outcomes
2.4. Definition of Sarcopenic Obesity
2.5. Sample Size Calculation
2.6. Statistical Analysis
2.7. Ethical Consideration
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Doehner, W.; Schenkel, J.; Anker, S.D.; Springer, J.; Audebert, H.J. Overweight and obesity are associated with improved survival, functional outcome, and stroke recurrence after acute stroke or transient ischemic attack: Observations from the TEMPiS trial. Eur. Heart J. 2013, 34, 268–277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aparicio, H.J.; Himali, J.J.; Beiser, A.S.; Davis-Plourde, K.L.; Vasan, R.S.; Kase, C.S.; Wolf, P.A.; Seshadri, S. Overweight, obesity, and survival after stroke in the Framingham Heart Study. J. Am. Heart Assoc. 2017, 6, e004721. [Google Scholar] [CrossRef] [PubMed]
- Park, J.H.; Lee, J.; Ovbiagele, B. Association of optimal combination drug treatment with obesity status among recent ischemic stroke patients: Results of the Vitamin Intervention for Stroke Prevention (VISP) trial. J. Stroke 2017, 19, 213–221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Strazzullo, P.; D’Elia, L.; Cairella, G.; Garbagnati, F.; Cappuccio, F.P.; Scalfi, L. Excess body weight and incidence of stroke: Meta–analysis of prospective studies with 2 million participants. Stroke 2010, 41, 418–426. [Google Scholar] [CrossRef] [Green Version]
- Scherbakov, N.; Sandek, A.; Doehner, W. Stroke-related sarcopenia: Specific characteristics. J. Am. Med. Dir. Assoc. 2015, 16, 272–276. [Google Scholar] [CrossRef]
- English, C.; McLennan, H.; Thoirs, K.; Coates, A.; Bernhardt, J. Loss of skeletal muscle mass after stroke: A systematic review. Int. J. Stroke 2010, 5, 395–402. [Google Scholar] [CrossRef] [PubMed]
- English, C.; Thoirs, K.; Coates, A.; Ryan, A.; Bernhardt, J. Changes in fat mass in stroke survivors: A systematic review. Int. J. Stroke 2012, 7, 491–498. [Google Scholar] [CrossRef] [Green Version]
- Ryan, A.S.; Buscemi, A.; Forrester, L.; Hafer-Macko, C.E.; Ivey, F.M. Atrophy and intramuscular fat in specific muscles of the thigh: Associated weakness and hyperinsulinemia in stroke survivors. Neurorehabilit. Neural Repair 2011, 25, 865–872. [Google Scholar] [CrossRef]
- Lazoura, O.; Papadaki, P.J.; Antoniadou, E.; Groumas, N.; Papadimitriou, A.; Thriskos, P.; Fezoulidis, I.V.; Vlychou, M. Skeletal and body composition changes in hemiplegic patients. J. Clin. Densitom. 2010, 13, 175–180. [Google Scholar] [CrossRef]
- Schaap, L.A.; Koster, A.; Visser, M. Adiposity, muscle mass, and muscle strength in relation to functional decline in older persons. Epidemiol. Rev. 2013, 35, 51–65. [Google Scholar] [CrossRef] [Green Version]
- Wohlfahrt, P.; Lopez–Jimenez, F.; Krajcoviechova, A.; Jozifova, M.; Mayer, O.; Vanek, J.; Filipovsky, J.; Llano, E.M.; Cifkova, R. The obesity paradox and survivors of ischemic stroke. J. Stroke Cerebrovasc. Dis. 2015, 24, 1443–1450. [Google Scholar] [CrossRef] [PubMed]
- Persaud, S.R.; Lieber, A.C.; Donath, E.; Stingone, J.A.; Dangayach, N.S.; Zhang, X.; Mocco, J.; Kellner, C.P. Obesity paradox in intracerebral hemorrhage. Stroke 2019, 50, 999–1002. [Google Scholar] [CrossRef] [PubMed]
- Nishioka, S.; Wakabayashi, H.; Yoshida, T.; Mori, N.; Watanabe, R.; Nishioka, E. Obese Japanese patients with stroke have higher functional recovery in convalescent rehabilitation wards: A retrospective cohort study. J. Stroke Cerebrovasc. Dis. 2016, 25, 26–33. [Google Scholar] [CrossRef] [PubMed]
- Batsis, J.A.; Mackenzie, T.A.; Barre, L.K.; Lopez-Jimenez, F.; Bartels, S.J. Sarcopenia, sarcopenic obesity and mortality in older adults: Results from the National Health and Nutrition Examination Survey III. Eur. J. Clin. Nutr. 2014, 68, 1001–1007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alexandre, T.D.S.; Scholes, S.; Ferreira Santos, J.L.; Duarte, Y.A.O.; de Oliveira, C. The combination of dynapenia and abdominal obesity as a risk factor for worse trajectories of IADL disability among older adults. Clin. Nutr. 2018, 37, 2045–2053. [Google Scholar] [CrossRef] [Green Version]
- Sakuma, K.; Yamaguchi, A. Sarcopenic obesity and endocrinal adaptation with age. Int. J. Endocrinol. 2013, 2013, 204164. [Google Scholar] [CrossRef] [Green Version]
- Marcus, R.L.; Addison, O.; Dibble, L.E.; Foreman, K.B.; Morrell, G.; Lastayo, P. Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J. Aging Res. 2012, 2012, 629637. [Google Scholar] [CrossRef]
- Matsushita, T.; Nishioka, S.; Taguchi, S.; Yamanouchi, A. Sarcopenia as a predictor of activities of daily living capability in stroke patients undergoing rehabilitation. Geriatr. Gerontol. Int. 2019, 19, 1124–1128. [Google Scholar] [CrossRef]
- Yoshimura, Y.; Wakabayashi, H.; Bise, T.; Nagano, F.; Shimazu, S.; Shiraishi, A.; Yamaga, M.; Koga, H. Sarcopenia is associated with worse recovery of physical function and dysphagia, and a lower rate of home discharge in Japanese hospitalized adults undergoing convalescent rehabilitation. Nutrition 2018, 61, 111–118. [Google Scholar] [CrossRef]
- Miyai, I.; Sonoda, S.; Nagai, S.; Takayama, Y.; Inoue, Y.; Kakehi, A.; Kurihara, M.; Ishikawa, M. Results of new policies for inpatient rehabilitation coverage in Japan. Neurorehabilit. Neural Repair 2011, 25, 540–547. [Google Scholar] [CrossRef]
- Vellas, B.; Villars, H.; Abellan, G.; Soto, M.E.; Rolland, Y.; Guigoz, Y.; Morley, J.E.; Chumlea, W.; Salva, A.; Rubenstein, L.Z.; et al. Overview of the MNA––Its history and challenges. J. Nutr. Health Aging 2006, 10, 456–463. [Google Scholar] [PubMed]
- Rubenstein, L.Z.; Harker, J.O.; Salvà, A.; Guigoz, Y.; Vellas, B. Screening for undernutrition in geriatric practice: Developing the short–form mini–nutritional assessment (MNA–SF). J. Gerontol. A Biol. Sci. Med. Sci. 2001, 56, 366–372. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marshall, S.; Young, A.; Bauer, J.; Isenring, E. Nutrition screening in geriatric rehabilitation: Criterion (concurrent and predictive) validity of the Malnutrition Screening Tool and the Mini Nutritional Assessment—Short Form. J. Acad. Nutr. Diet. 2016, 116, 795–801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nishioka, S.; Omagari, K.; Nishioka, E.; Mori, N.; Taketani, Y.; Kayashita, J. Concurrent and predictive validity of the Mini Nutritional Assessment Short-Form and the Geriatric Nutritional Risk Index in older stroke rehabilitation patients. J. Hum. Nutr. Diet. 2020, 33, 12–22. [Google Scholar] [CrossRef]
- Brunnstrom, S. Motor testing procedures in hemiplegia: Based on sequential recovery stage. Phys. Ther. 1966, 46, 357–375. [Google Scholar] [CrossRef] [Green Version]
- Watanabe, H.; Tashiro, K. Brunnstrom stage and wallerian degenerations: A study using MRI. Tohoku J. Exp. Med. 1992, 166, 471–473. [Google Scholar] [CrossRef] [Green Version]
- Ottenbacher, K.J.; Hsu, Y.; Granger, C.V.; Fiedler, R.C. The reliability of the functional independence measure: A quantitative review. Arch. Phys. Med. Rehabil. 1996, 77, 1226–1232. [Google Scholar] [CrossRef]
- Donini, L.M.; Busetto, L.; Bauer, J.M.; Bischoff, S.; Boirie, Y.; Cederholm, T.; Cruz-Jentoft, A.J.; Dicker, D.; Frühbeck, G.; Giustina, A.; et al. Critical appraisal of definitions and diagnostic criteria for sarcopenic obesity based on a systematic review. Clin. Nutr. 2020, 39, 2368–2388. [Google Scholar] [CrossRef]
- Chen, L.K.; Woo, J.; Assantachai, P.; Auyeung, T.W.; Chou, M.Y.; Iijima, K.; Jang, H.C.; Kang, L.; Kim, M.; Kim, S.; et al. Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J. Am. Med. Dir. Assoc. 2020, 21, 300–307. [Google Scholar] [CrossRef]
- Kemmler, W.; von Stengel, S.; Engelke, K.; Sieber, C.; Freiberger, E. Prevalence of sarcopenic obesity in Germany using established definitions: Baseline data of the FORMOsA study. Osteoporos. Int. 2016, 27, 275–281. [Google Scholar] [CrossRef]
- Kemmler, W.; Teschler, M.; Weißenfels, A.; Sieber, C.; Freiberger, E.; von Stengel, S. Prevalence of sarcopenia and sarcopenic obesity in older German men using recognized definitions: High accordance but low overlap! Osteoporos. Int. 2017, 28, 1881–1891. [Google Scholar] [CrossRef] [PubMed]
- Kim, T.N.; Yang, S.J.; Yoo, H.J.; Lim, K.I.; Kang, H.J.; Song, W.; Seo, J.A.; Kim, S.G.; Kim, N.H.; Baik, S.H.; et al. Prevalence of sarcopenia and sarcopenic obesity in Korean adults: The Korean sarcopenic obesity study. Int. J. Obes. 2009, 33, 885–892. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Batsis, J.A.; Mackenzie, T.A.; Emeny, R.T.; Lopez-Jimenez, F.; Bartels, S.J. Low lean mass with and without obesity, and mortality: Results from the 1999-2004 National Health and Nutrition Examination Survey. J. Gerontol. A Biol. Sci. Med. Sci. 2017, 72, 1445–1451. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hong, S.H.; Choi, K.M. Sarcopenic obesity, insulin resistance, and their implications in cardiovascular and metabolic consequences. Int. J. Mol. Sci. 2020, 21, 494. [Google Scholar] [CrossRef] [Green Version]
- Barazzoni, R.; Bischoff, S.C.; Boirie, Y.; Busetto, L.; Cederholm, T.; Dicker, D.; Toplak, H.; Van Gossum, A.; Yumuk, V.; Vettor, R. Sarcopenic obesity: Time to meet the challenge. Clin. Nutr. 2018, 37, 1787–1793. [Google Scholar] [CrossRef]
- Tanaka, M.; Masuda, S.; Yamakage, H.; Inoue, T.; Ohue-Kitano, R.; Yokota, S.; Kusakabe, T.; Wada, H.; Sanada, K.; Ishii, K.; et al. Role of serum myostatin in the association between hyperinsulinemia and muscle atrophy in Japanese obese patients. Diabetes Res. Clin. Pract. 2018, 142, 195–202. [Google Scholar] [CrossRef]
- Gannon, J.; Doran, P.; Kirwan, A.; Ohlendieck, K. Drastic increase of myosin light chain MLC-2 in senescent skeletal muscle indicates fast-to-slow fibre transition in sarcopenia of old age. Eur. J. Cell Biol. 2009, 88, 685–700. [Google Scholar] [CrossRef] [Green Version]
- Batsis, J.A.; Villareal, D.T. Sarcopenic obesity in older adults: Aetiology, epidemiology and treatment strategies. Nat. Rev. Endocrinol. 2018, 14, 513–537. [Google Scholar] [CrossRef]
- Levine, M.E.; Crimmins, E.M. Sarcopenic obesity and cognitive functioning: The mediating roles of insulin resistance and inflammation? Curr. Gerontol. Geriatr. Res. 2012, 2012, 826398. [Google Scholar] [CrossRef] [Green Version]
- Tolea, M.I.; Chrisphonte, S.; Galvin, J.E. Sarcopenic obesity and cognitive performance. Clin. Interv. Aging 2018, 13, 1111–1119. [Google Scholar] [CrossRef] [Green Version]
- Low, S.; Goh, K.S.; Ng, T.P.; Ang, S.F.; Moh, A.; Wang, J.; Ang, K.; Subramaniam, T.; Sum, C.F.; Lim, S.C. The prevalence of sarcopenic obesity and its association with cognitive performance in type 2 diabetes in Singapore. Clin. Nutr. 2020, 39, 2274–2281. [Google Scholar] [CrossRef] [PubMed]
- Canon, M.E.; Crimmins, E.M. Sex differences in the association between muscle quality, inflammatory markers, and cognitive decline. J. Nutr. Health Aging 2011, 15, 695–698. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Berr, C.; Balansard, B.; Arnaud, J.; Roussel, A.M.; Alpérovitch, A. Cognitive decline is associated with systemic oxidative stress: The EVA study. Etude du Vieillissement Artériel. J. Am. Geriatr. Soc. 2000, 48, 1285–1291. [Google Scholar] [CrossRef]
- Geroldi, C.; Frisoni, G.B.; Paolisso, G.; Bandinelli, S.; Lamponi, M.; Abbatecola, A.M.; Zanetti, O.; Guralnik, J.M.; Ferrucci, L. Insulin resistance in cognitive impairment: The InCHIANTI study. Arch. Neurol. 2005, 62, 1067–1072. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, M.; Chino, N.; Tuji, T.; Masakado, Y.; Hase, K.; Kimura, A. Psychometric properties of the Stroke Impairment Assessment Set (SIAS). Neurorehabilit. Neural Repair 2002, 16, 339–351. [Google Scholar] [CrossRef] [PubMed]
Variables | Normal n = 83 | Simple Obesity n = 65 | Sarcopenia without Obesity n = 121 | Sarcopenic Obesity n = 107 | p Value |
---|---|---|---|---|---|
Age, y, mean (SD) | 73.5 (7.2) | 74.1 (6.4) | 80.0 (8.1) *,d | 80.0 (7.3) *,d | <0.001 a |
Sex (men), n (%) | 46 (55) | 50 (77) ‡,e | 47 (39) †,e | 67 (63) | <0.001 b |
Stroke subtype, n (%) | 0.17 b | ||||
Cerebral infarction | 65 (78) | 49 (75) | 79 (65) | 79 (74) | |
Intracerebral hemorrhage | 13 (16) | 16 (25) | 35 (29) | 23 (22) | |
Subarachnoid hemorrhage | 5 (6.0) | 0 (0) | 7 (5.8) | 5 (4.7) | |
Days from onset, d, median [IQR] | 22 (17–34) | 23 (19–299) | 26 (20–35) | 23 (18–31) | 0.13 c |
Care needed before stroke onset, n (%) | 7 (8.4) | 5 (7.7) | 29 (24) *,e | 28 (26) *,e | 0.001 b |
Lower limb motor paralysis, n (%) | 0.74 b | ||||
BRS I–IV | 16 (19) | 12 (19) | 31 (26) | 23 (22) | |
BRSV–VI | 50 (60) | 34 (52) | 65 (54) | 59 (55) | |
absence | 17 (21) | 19 (29) | 25 (21) | 25 (23) | |
Handgrip strength, kg, mean (SD) | 24.9 (7.7) | 27.4 (7.5) | 14.9 (6.2) *,d | 16.6 (6.0) *,d | <0.001 a |
Body mass index, kg/m2, mean (SD) | 21.1 (2.0) ‖,d | 24.9 (2.8) ‖,d | 19.1 (2.3) ‖,d | 23.1 (2.7) ‖,d | <0.001 a |
Skeletal muscle mass index, kg/m2, mean (SD) | 6.4 (0.9) | 6.8 (0.9) | 5.1 (0.9) *,d | 5.5 (0.8) *,d | <0.001 a |
Body fat percentage, mean (SD) | 25.5 (6.8) †,d | 34.9 (5.4) | 26.8 (7.0) †,d | 38.1 (6.5) ‖,d | <0.001 a |
MNA®–SF, n (%) | <0.001 b | ||||
0–5 (Malnourished) g | 24 (29) | 9 (14) †,e | 66 (55) ‖,e | 36 (34) §,e | |
6–7 (At risk of malnutrition) g | 21 (25) | 17 (26) | 35 (29) | 33 (31) | |
8–14 (Well-nourished) g | 38 (46) | 39 (60) †,e | 20 (17) ‖,e | 38 (36) §,e | |
8–11 h | 38 (46) | 35 (54) | 20 (17) | 38 (36) | |
12–14 h | 0 (0) | 4 (6) | 0 (0) | 0 (0) | |
FIM on admission, score, median [IQR] | |||||
Total | 89 (71–107) | 92 (74–110.5) | 71 (46.5–88.5) *,f | 71 (46–86) *,f | <0.001 c |
Motor | 60 (46–78) | 69 (48–81) | 47 (27.5–63) *,f | 47 (29–60) *,f | <0.001 c |
Cognitive | 27 (21–32) | 29 (25–33) | 22 (16–28) *,f | 21 (16–28) *,f | <0.001 c |
Variables | B | 95% Confidence Interval | p Value |
---|---|---|---|
(Constant) | 110.311 | 87.408 to 133.214 | <0.001 |
Simple obesity | 1.064 | −4.865 to 6.994 | 0.72 |
Sarcopenia without obesity | −2.821 | −8.265 to 2.623 | 0.31 |
Sarcopenic obesity | −10.755 | −16.157 to −5.353 | <0.001 |
Age | −0.492 | −0.762 to −0.223 | <0.001 |
Women | −0.087 | −3.978 to 3.804 | 0.97 |
Stroke subtype | |||
Cerebral infarction (reference) | - | - | - |
Intracerebral hemorrhage | −7.286 | −11.977 to −2.596 | 0.002 |
Subarachnoid hemorrhage | −3.306 | −12.573 to 5.961 | 0.48 |
Days from onset to admission | −0.122 | −0.297 to 0.052 | 0.17 |
Care needed before stroke onset | −10.646 | −15.575 to −5.717 | <0.001 |
Lower limb motor paralysis | |||
Absence (reference) | - | - | - |
BRS I–IV | −33.240 | −38.854 to −27.626 | <0.001 |
BRS V–VI | −9.876 | −14.393 to −5.359 | <0.001 |
MNA®–SF, points | 4.097 | 3.274 to 4.920 | <0.001 |
Variables | FIM–Motor Domain Score * | FIM–Cognitive Domain Score † | ||
---|---|---|---|---|
B | 95% Confidence Interval | B | 95% Confidence Interval | |
(Constant) | 78.136 ‡ | 60.368 to 95.903 | 32.176 ‡ | 24.270 to 40.081 |
Simple obesity | −0.452 | −5.052 to 4.148 | 1.517 | −0.530 to 3.563 |
Sarcopenia without obesity | −2.052 | −6.275 to 2.171 | −0.769 | −2.648 to 1.110 |
Sarcopenic obesity | −7.876 ‡ | −12.067 to −3.685 | −2.879 ‡ | −4.743 to −1.014 |
Age | −0.370 ‡ | −0.579 to −0.161 | −0.122 ‡ | −0.215 to −0.029 |
Women | −0.802 | −3.820 to 2.217 | 0.715 | −0.628 to 2.058 |
Stroke subtype | ||||
Cerebral infarction (reference) | - | - | - | - |
Intracerebral hemorrhage | −5.686 ‡ | −9.325 to −2.048 | −1.600 | −3.219 to 0.019 |
Subarachnoid hemorrhage | −3.864 | −11.053 to 3.324 | 0.558 | −2.640 to 3.757 |
Days from onset to admission | −0.030 | −0.166 to 0.105 | −0.092 ‡ | −0.152 to −0.032 |
Care needed before stroke onset | −8.020 ‡ | −11.843 to −4.196 | −2.626 ‡ | −4.328 to −0.925 |
Lower limb motor paralysis | ||||
Absence (reference) | - | - | - | - |
BRS I–IV | −29.330 ‡ | −33.685 to −24.975 | −3.910 ‡ | −5.848 to −1.972 |
BRS V–VI | −8.324 ‡ | −11.829 to −4.820 | −1.552 | −3.111 to 0.008 |
MNA®–SF, points | 3.127 ‡ | 2.489 to 3.765 | 0.970 ‡ | 0.686 to 1.254 |
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Matsushita, T.; Nishioka, S.; Taguchi, S.; Yamanouchi, A.; Nakashima, R.; Wakabayashi, H. Sarcopenic Obesity and Activities of Daily Living in Stroke Rehabilitation Patients: A Cross-Sectional Study. Healthcare 2020, 8, 255. https://doi.org/10.3390/healthcare8030255
Matsushita T, Nishioka S, Taguchi S, Yamanouchi A, Nakashima R, Wakabayashi H. Sarcopenic Obesity and Activities of Daily Living in Stroke Rehabilitation Patients: A Cross-Sectional Study. Healthcare. 2020; 8(3):255. https://doi.org/10.3390/healthcare8030255
Chicago/Turabian StyleMatsushita, Tatsuya, Shinta Nishioka, Shiori Taguchi, Anna Yamanouchi, Ryusei Nakashima, and Hidetaka Wakabayashi. 2020. "Sarcopenic Obesity and Activities of Daily Living in Stroke Rehabilitation Patients: A Cross-Sectional Study" Healthcare 8, no. 3: 255. https://doi.org/10.3390/healthcare8030255
APA StyleMatsushita, T., Nishioka, S., Taguchi, S., Yamanouchi, A., Nakashima, R., & Wakabayashi, H. (2020). Sarcopenic Obesity and Activities of Daily Living in Stroke Rehabilitation Patients: A Cross-Sectional Study. Healthcare, 8(3), 255. https://doi.org/10.3390/healthcare8030255