Key summary points
To investigate the association between albumin and C-reactive protein during acute hospitalization with functional and body composition parameters in patients admitted to geriatric rehabilitation.
AbstractSection FindingsLower average albumin, higher albumin variation and lower minimum albumin were associated with larger declines in physical function during acute hospitalization and with lower functional and body composition parameters at geriatric rehabilitation admission. C-reactive protein, was only partly associated with lower gait speed at geriatric rehabilitation admission.
AbstractSection MessageInflammation during acute hospitalization, especially lower albumin concentrations, relates to declined physical function and low functional and body composition parameters upon geriatric rehabilitation admission.
Abstract
Purpose
Albumin and C-reactive protein (CRP) are non-specific markers of inflammation, which could affect muscle tissue during acute hospitalization. We investigated the association between albumin and CRP during acute hospitalization with functional and body composition parameters in patients admitted to geriatric rehabilitation.
Methods
The REStORing Health of Acutely Unwell AdulTs (RESORT) cohort includes geriatric rehabilitation patients assessed for change in activities of daily living (ADL, using the Katz index) during acute hospitalization, and subsequently for Katz ADL, gait speed (GS), handgrip strength (HGS) and skeletal muscle mass index (SMI) at geriatric rehabilitation admission. Albumin and CRP average (median), variation (interquartile range), and maximum or minimum were collected from serum samples, and were examined for their association with functional and body composition parameters using multivariable linear regression analysis adjusted for age, sex and length of acute hospital stay.
Results
1769 Inpatients were included for analyses (mean age 82.6 years ± 8.1, 56% female). Median length of acute hospitalization was 7 [IQR 4, 13] days and median number of albumin and CRP measurements was 5 [IQR 3, 12] times. ADL declined in 89% of patients (median − 3 points, IQR − 4, − 2). Lower average albumin, higher albumin variation and lower minimum albumin were associated with larger declines in ADL and with lower ADL, GS, HGS and SMI at geriatric rehabilitation admission. Higher average and maximum CRP were associated with lower GS.
Conclusion
Inflammation, especially lower albumin concentrations, during acute hospitalization is associated with lower physical function at geriatric rehabilitation admission.
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Introduction
Acute hospitalization influences muscle homeostasis and physical function negatively [1,2,3]. Over one-third of older patients experience loss in activities of daily living (ADL) during hospitalization [2, 4, 5]. Inflammation is likely an important contributor to muscle wasting following acute hospitalization, and a possible target in the prevention of disability [6]. Acute systemic inflammation, characterized by low albumin and high C-reactive protein (CRP) serum levels, is often observed in acutely ill hospitalized patients and can contribute to high levels of muscle wasting [7]. This inflammation can lead to a catabolic state [8], which in turn can cause muscle degeneration through myonuclear apoptosis, alterations in muscle protein turnover and impaired satellite cell function [7, 9, 10].
Albumin and CRP are proteins synthesized in the liver and respond to pro-inflammatory cytokines [11,12,13,14]. Albumin has been suggested as a marker for the nutritional state, but this has been questioned [15]. More recent, albumin has been used as a marker for overall severity of disease; however, the ability to maintain normal levels of albumin may also indicate a level of protection against physiological stress caused by inflammation [12]. Albumin could, therefore, be used as a marker of inflammation: albumin regulates plasma oncotic pressure, and is an antioxidant that moderates the inflammatory response by binding pro-inflammatory molecules [16, 17]. In sepsis and acute illness, the albumin transcapillary escape rate is increased, and the synthesis rate in the liver is increased to a lesser extent, resulting in an altered distribution over fluid compartments and decreased serum albumin [17]. As such, low levels of albumin may increase the risk of catabolism in an individual. Lower albumin concentrations have shown a strong relation with sarcopenia in older adults [18, 19], and have shown to synergistically contribute to increased disability [20]. Lower levels of albumin and higher levels of CRP are associated with a decline in ADL, gait speed (GS), handgrip strength (HGS) and skeletal muscle mass index (SMI) after 5–10 years of follow-up in community-dwelling older adults [21,22,23,24,25,26].
There is limited knowledge about how inflammation experienced during acute hospitalization influences functional and body composition parameters in patients admitted to geriatric rehabilitation. We investigated the associations of albumin and CRP during acute hospitalization with functional and body composition parameters (ADL, GS, HGS, SMI) in patients admitted to geriatric rehabilitation.
Methods
Study design
REStORing health of acutely unwell adulTs (RESORT) is an observational, prospective and longitudinal inception cohort study that commenced recruitment in October 2017 at the Royal Melbourne Hospital (Melbourne, Victoria, Australia). A description of the protocol is accessible elsewhere [27]. The cohort included 1890 patients admitted to geriatric rehabilitation wards from October 16th 2017 and discharged by March 18th 2020. The study was approved by the Melbourne Health Human Research Ethics Committee (no. HREC/17/MH/103). Written informed consent was obtained from the patients or a nominated proxy. Patients were excluded (n = 446, 16.6%) if they were transferred to another healthcare service before consent was obtained, were unable to give informed consent (e.g., severe dementia, delirium) and did not have a nominated proxy, or were receiving palliative care. A total of 356 patients (13.2%) refused to participate in the study. Patients were assessed within 48 h of admission to geriatric rehabilitation and within 48 h of discharge. A Comprehensive Geriatric Assessment (CGA) [28] was performed in every patient as part of usual care by trained medical, nursing and allied health professionals and included physical, cognitive, functional and social domains.
Data collection
Patient characteristics
Demographic data were collected through a self-reported survey at admission to geriatric rehabilitation and included age, sex, living status, use of a walking aid, cognitive impairment and experiencing a fall in the preceding year. Multimorbidity was assessed using the Charlson Comorbidity Index (CCI) [29], risk of malnutrition using the Malnutrition Screening Tool (MST) [30], Global Leadership Initiative on Malnutrition (GLIM) malnutrition prevalence [31], and frailty status using the Rockwood Clinical Frailty Scale (CFS) [32]. Height was measured upright if patients were able to stand, otherwise height was estimated from the knee height using the Longitudinal Aging Study Amsterdam (LASA) formula (male = 74.48 + [2.03 × knee height] − [0.15 × age], female = 68.74 + [2.07 × knee height] − [0.16 × age]) [33]. Weight was measured using a weighing scale or weighing chair. Body mass index was calculated from height and weight. Acute admission diagnosis, number of medication, length of stay (LOS) for acute hospitalization and geriatric rehabilitation were collected from medical records.
Functional and body composition parameters
ADL was scored by trained occupational therapists using the self-reported Katz index [34] 2 weeks before acute hospitalization and at admission to geriatric rehabilitation. The score on the Katz ADL index ranges from 0 to 6 points, with 0 points indicating full dependency and 6 points indication full independency. Change in ADL was calculated subtracting the score at geriatric rehabilitation admission with the score 2 weeks before acute hospitalization.
GS, HGS and SMI were measured at geriatric rehabilitation admission: GS (m/s) was measured using the 4-m walk test at usual pace from a standing start, following the protocol of the Short Physical Performance Battery [35]. The fastest trial out of two attempts was used for analysis. HGS (kg) was measured using a hydraulic handheld dynamometer (Jamar, Sammons Preston, Inc. Bolingbrook, IL, USA) sitting upright in a chair, with elbows unsupported at an angle of 90° [36]. Where patients were confined to bed, HGS was measured in supine position with elbows unsupported in an angle of 30°. Repeated measurements were performed in the same position with three attempts per hand, alternating between hands [37]. The maximum score out of six attempts was used for analysis. SMI (kg/m2) was measured using direct segmental multi-frequency bioelectrical impedance analysis (DSM-BIA, InBody S10, Biospace Co., Ltd, Seoul) [38].Contraindications for DSM-BIA measurement included pacemaker or any electronic internal medical device, plasters or bandages that could not be removed from the positioning place of the electrodes, amputated arm and/or leg or contact isolation.
Inflammatory markers
Albumin and CRP obtained during routine clinical care were used in the present analysis and retrieved from medical records. Albumin (g/L) was measured in serum samples by Albumin BCP assay on the Architect cSystems. High-sensitivity CRP (mg/L) was measured in serum samples by Multigent CRP Vario assay for quantitative immunoturbidimetric determination using the Architect cSystems.
Albumin was expressed as: (1) the median value (average albumin); (2) the interquartile range (albumin variation); and (3) the minimum albumin calculated over all measurements taken during acute hospitalization. CRP was expressed as: (1) the median value (average CRP); (2) the interquartile range (CRP variation); and (3) the maximum CRP. Clusters were formed combining high versus low levels of minimum albumin and albumin variation with high versus low levels of average CRP. Median values were used to categorize high versus low, as predefined cutoff values for high versus low average, variation and minimum are not available.
Statistical analysis
The analysis included 1769 out of 1890 patients (Fig. 1). Figure 2 visualizes the timeline of data collection. Data was presented as number (%), mean (SD) or median [IQR] as appropriate and unadjusted residuals of all models were checked for normality. Potential selection bias of patients with zero, one, or ≥ two measurements of albumin and CRP was investigated using one-way ANOVA (normal distribution), Mann–Whitney U test (skewed distribution) or Chi-square test (categorical variables).
Overview of albumin, C-reactive protein and functional and body composition parameters during acute hospitalization and at geriatric rehabilitation admission. ADL activities of daily living, GS gait speed, HGS handgrip strength, SMI skeletal muscle mass index. Dashed lines indicate the average of albumin and C-reactive protein concentrations. Dashed arrows indicate the variation of albumin and C-reactive protein concentrations
A multivariable linear regression analysis was used to determine the association between the average, variation and minimum albumin and maximum CRP levels with change in ADL, ADL, GS, HGS and SMI. These models were adjusted for age, sex and length of acute hospital stay. The model with change in ADL was additionally adjusted for baseline ADL 2 weeks before acute hospitalization.
Minimum albumin and average CRP were combined into clusters. Clusters consisted of low versus high minimum albumin and high versus low average CRP, with the most favorable cluster including high minimum albumin and low average CRP, and the least favorable cluster including low minimum albumin and high average CRP based on previous literature [21,22,23,24,25,26]. Clusters consisting of high versus low albumin variation and high versus low average CRP were included as Online Resource 1. The associations between the clusters with change in ADL, ADL, GS, HGS and SMI were analyzed using multivariable linear regression models with dummy variables of the clusters, using the same adjustments as described above. Results of the clusters were visualized as bar charts with unstandardized predicted medians using GraphPad Prism for Windows (version 8.0. GraphPad Software Inc.). Associations were considered statistically significant if p < 0.05. The Statistical Package for the Social Sciences was used for all analyses (IBM SPSS Statistics for Windows, Version 23.0. Armonk, NY, IBM Corp).
Results
Characteristics of the RESORT patients are shown in Table 1. Mean age was 82.6 years (SD 8.1), 984 patients (55.6%) were female, 71.8% used a walking aid and 65.8% had experienced a fall in the preceding year. From 2 weeks before acute hospitalization to geriatric rehabilitation admission, 89% of patients experienced a decline in ADL with a median of − 3 points [IQR − 4, − 2]. Online Resource 2 shows the characteristics of patients stratified by zero, one or ≥ two number of albumin and CRP measurements (albumin median 4 [IQR 2, 8] number of measurements during acute hospitalization, CRP median 2 [IQR 1, 5] number of measurements). Compared to patients with zero or one measurement of albumin or CRP, patients with ≥ two measurements were more likely to be male, malnourished, more frail, use more medication, have multimorbidity, a longer acute and geriatric rehabilitation LOS, a lower average and minimum albumin, a higher average and maximum CRP, and a lower ADL and HGS.
Table 2 shows the associations between albumin and CRP with functional and body composition parameters. Lower average albumin was associated with lower change in ADL, ADL, GS, HGS and SMI. For every one g/L lower average albumin, patients had 0.034 points larger decline in ΔADL, 0.030 points lower ADL, 0.009 m/s lower GS, 0.119 kg lower HGS, and 0.018 kg/m2 lower SMI. Higher albumin variation was associated with lower change in ADL, ADL and GS. For every one g/L higher variation albumin, patients had 0.095 points larger decline in ΔADL, 0.064 points lower ADL, and 0.012 m/s lower GS. Lower minimum albumin was associated with lower change in ADL, ADL, GS, HGS and SMI. For every one g/L lower minimum albumin, patients had 0.034 points larger decline in ΔADL, 0.028 points lower ADL, 0.007 m/s lower GS, 0.101 kg lower HGS and 0.022 kg/m2 lower SMI. Higher average and maximum CRP were associated with lower GS. For every one mg/L higher average and maximum CRP, patients had 0.001 and 0.000 m/s lower GS, respectively. No statistically significant associations were observed for CRP and change in ADL, ADL, HGS and SMI.
Figure 3 visualizes clusters of minimum albumin and average CRP. Compared to the most favorable cluster (high minimum albumin, low average CRP), the lower favorable clusters with low minimum albumin or high average CRP showed a larger decline in ADL, a lower ADL and GS. No statistically significant associations were observed for HGS and SMI. The clusters of albumin variation and average CRP are visualized in Online Resource 1. Compared to the most favorable cluster (low albumin variation and low average CRP), the least favorable cluster with high albumin variation and high average CRP showed a larger decline in ADL and a lower GS.
Clusters of minimum albumin and average CRP during acute hospitalization associated with change in ADL, ADL, GS, HGS and SMI at geriatric rehabilitation admission. ADL activities of daily living, CRP C-reactive protein, GS gait speed, HGS handgrip strength, SMI skeletal muscle mass index. Bars: unstandardized predicted medians adjusted for age, sex and length of acute hospital stay. Change in ADL additionally adjusted for baseline ADL 2 weeks before acute hospitalization. Error bars: upper interquartile range. Low minimum albumin < 29 g/L, high average CRP ≥ 32.4 mg/L
Discussion
This is the first study to investigate the association of acute inflammation during acute hospitalization with changes in ADL, GS, HGS and SMI in patients admitted to geriatric rehabilitation. Albumin exerts a more robust association with functional and body composition parameters compared to CRP.
Previous findings showed that geriatric inpatients with albumin < 35 g/L at admission were more likely to have a decline in ADL from 2 weeks prior to hospitalization to discharge, and they were more likely to stay ADL dependent after 1 year of follow-up [39]. Albumin < 30 g/L at admission to the hospital was associated with a higher risk of new onset ADL disability at discharge in geriatric hospitalized patients [40]. Change in albumin from admission to discharge was positively associated with change in ADL in geriatric patients, as opposed to change in CRP which was not associated with change in ADL [41]. These results from previous studies further support our finding that albumin concentrations have a stronger association with physical function compared to CRP.
CRP was not associated with most functional and body composition parameters, contradicting previous findings from the EMPOWER study in geriatric inpatients [42] that identified a maximum CRP > 10 mg/L was associated with lower HGS at discharge, but not with lower skeletal muscle mass. However, a second study in geriatric inpatients identified patients with CRP > 10 mg/L at admission and every 7th day thereafter had significantly lower HGS at admission compared to patients with low CRP, but HGS was not significantly different at discharge [43]. CRP and HGS assessed at admission were not associated in 33 geriatric inpatients admitted with acute infection-induced inflammation [44]. These findings suggest that CRP concentrations during acute hospitalization are unlikely to act as a reliable marker for predicting declines in physical function during acute hospitalization.
In previous research, clusters of albumin (cutoff point: 3.5 g/dL) and CRP (cutoff point: 5 mg/dL) in geriatric inpatients were associated with higher risk of in-hospital mortality [45]. In patients with sepsis aged 18 years and older, albumin/CRP ratios at admission and discharge were better predictors of 90-day and 180-day mortality after hospitalization compared to albumin or CRP alone [46, 47]. We explored combining albumin and CRP into clusters, and observed an association with functional and body composition parameters. The benefit of combining albumin and CRP predicting relevant clinical outcome needs further research.
The impact of acute hospitalization on geriatric rehabilitation is a highly understudied field, while geriatric rehabilitation patients are at high risk of poor muscle status [48], which is related to worse recovery [49, 50]. In geriatric patients after acute hospitalization, albumin and CRP have been associated with negative rehabilitation outcome and mortality [51, 52]. Albumin and CRP are nonspecific markers of inflammation, but may also have a direct effect on muscle health: the size of myotubes in vitro may decrease after exposure to CRP with a decreased rate of protein synthesis through a decrease in regulators of mechanistic target of rapamycin complex 1 and an increase in phosphorylated AMP-activated protein kinase [53]. Albumin binds pro-inflammatory cytokines and reactive oxygen species, indirectly moderating the effect of systemic inflammation on deterioration [17]. Albumin further activates the phosphatidyl–inositol 3-kinase/AKT pathway [54], potentially leading to muscle hypertrophy [55]. Optimal treatment for geriatric inpatients with inflammation comprises pharmacological, resistance training and nutritional intervention [56,57,58], but guidelines for personalised training protocols have still to be established.
Some limitations of this study should be considered. Albumin and CRP are not specific markers of inflammation as they also respond to other biological influences. Ideally inflammation should be assessed using pro-inflammatory cytokines, such as IL-6, however; these measurements are not part of routine patient care and as such other markers of inflammation were not accessible for this study. Patients with a higher number of albumin and CRP measurements were more frail, which could have led to selection bias. Not all variables that might influence the association between CRP, albumin and functional and body composition parameters, such as diagnosis, comorbidities and medication use, were investigated. This needs to be further investigated in future research. We did not have data available on use of specific anti-inflammatory medication. Finally, because of the inclusion of patients at admission to geriatric rehabilitation, we were unable to analyze GS, HGS and SMI before acute hospitalization.
In conclusion, in patients admitted to geriatric rehabilitation, higher inflammation, as measured by lower albumin and higher CRP, during acute hospitalization was related to lower functional and body composition parameters at the start of rehabilitation. Particularly, lower average, higher variation and lower minimum albumin were associated with a larger decline in physical function during acute hospitalization.
Data availability
The data sets during and/or analyzed during the current study available from the corresponding author on reasonable request.
References
Alley DE, Koster A, Mackey D et al (2010) Hospitalization and change in body composition and strength in a population-based cohort of older persons. J Am Geriatr Soc 58:2085–2091. https://doi.org/10.1111/j.1532-5415.2010.03144.x
Zisberg A, Shadmi E, Gur-Yaish N, Tonkikh O, Sinoff G (2015) Hospital-associated functional decline: the role of hospitalization processes beyond individual risk factors. J Am Geriatr Soc 63:55–62. https://doi.org/10.1111/jgs.13193
Van Ancum JM, Scheerman K, Jonkman NH et al (2017) Change in muscle strength and muscle mass in older hospitalized patients: a systematic review and meta-analysis. Exp Gerontol 92:34–41. https://doi.org/10.1016/j.exger.2017.03.006
Covinsky KE, Pierluissi E, Johnston CB (2011) Hospitalization-associated disability: “She was probably able to ambulate, but I’m not sure.” JAMA 306:1782–1793. https://doi.org/10.1001/jama.2011.1556
Brown CJ, Friedkin RJ, Inouye SK (2004) Prevalence and outcomes of low mobility in hospitalized older patients. J Am Geriatr Soc 52:1263–1270. https://doi.org/10.1111/j.1532-5415.2004.52354.x
Alturki M, Beyer I, Mets T, Bautmans I (2018) Impact of drugs with anti-inflammatory effects on skeletal muscle and inflammation: a systematic literature review. Exp Gerontol 114:33–49. https://doi.org/10.1016/j.exger.2018.10.011
Puthucheary ZA, Rawal J, McPhail M et al (2013) Acute skeletal muscle wasting in critical illness. JAMA 310:1591–1600. https://doi.org/10.1001/jama.2013.278481
Evans WJ, Paolisso G, Abbatecola AM et al (2010) Frailty and muscle metabolism dysregulation in the elderly. Biogerontology 11:527–536. https://doi.org/10.1007/s10522-010-9297-0
Buford TW, Anton SD, Judge AR et al (2010) Models of accelerated sarcopenia: critical pieces for solving the puzzle of age-related muscle atrophy. Ageing Res Rev 9:369–383. https://doi.org/10.1016/j.arr.2010.04.004
Argiles JM, Campos N, Lopez-Pedrosa JM, Rueda R, Rodriguez-Manas L (2016) Skeletal muscle regulates metabolism via Interorgan Crosstalk: roles in health and disease. J Am Med Dir Assoc 17:789–796. https://doi.org/10.1016/j.jamda.2016.04.019
Ticinesi A, Lauretani F, Nouvenne A et al (2017) C-reactive protein (CRP) measurement in geriatric patients hospitalized for acute infection. Eur J Intern Med 37:7–12. https://doi.org/10.1016/j.ejim.2016.08.026
Soeters PB, Wolfe RR, Shenkin A (2019) Hypoalbuminemia: pathogenesis and clinical significance. J Parenter Enteral Nutr 43:181–193. https://doi.org/10.1002/jpen.1451
Sheldon J, Riches P, Gooding R, Soni N, Hobbs JR (1993) C-reactive protein and its cytokine mediators in intensive-care patients. Clin Chem 39:147–150. https://doi.org/10.1093/clinchem/39.1.147
De Feo P, Lucidi P (2002) Liver protein synthesis in physiology and in disease states. Curr Opin Clin Nutr Metab Care 5:47–50. https://doi.org/10.1097/00075197-200201000-00009
Eckart A, Struja T, Kutz A et al (2020) Relationship of nutritional status, inflammation, and serum albumin levels during acute illness: a prospective study. Am J Med 133:713-722.e7. https://doi.org/10.1016/j.amjmed.2019.10.031
Ha CE, Bhagavan NV (2013) Novel insights into the pleiotropic effects of human serum albumin in health and disease. Biochim Biophys Acta 1830:5486–5493. https://doi.org/10.1016/j.bbagen.2013.04.012
Artigas A, Wernerman J, Arroyo V, Vincent JL, Levy M (2016) Role of albumin in diseases associated with severe systemic inflammation: pathophysiologic and clinical evidence in sepsis and in decompensated cirrhosis. J Crit Care 33:62–70. https://doi.org/10.1016/j.jcrc.2015.12.019
Silva-Fhon JR, Rojas-Huayta VM, Aparco-Balboa JP, Céspedes-Panduro B, Partezani-Rodrigues RA (2021) Sarcopenia and blood albumin: a systematic review with meta-analysis. Biomedica 41:590–603. https://doi.org/10.7705/biomedica.5765
van Atteveld VA, Van Ancum JM, Reijnierse EM, Trappenburg MC, Meskers CGM, Maier AB (2019) Erythrocyte sedimentation rate and albumin as markers of inflammation are associated with measures of sarcopenia: a cross-sectional study. BMC Geriatr 19:233. https://doi.org/10.1186/s12877-019-1253-5
Uemura K, Doi T, Lee S, Shimada H (2019) Sarcopenia and low serum albumin level synergistically increase the risk of incident disability in older adults. J Am Med Dir Assoc 20:90–93. https://doi.org/10.1016/j.jamda.2018.06.011
Schaap LA, Pluijm SMF, Deeg DJH et al (2009) Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci 64a:1183–1189. https://doi.org/10.1093/gerona/glp097
Westbury LD, Fuggle NR, Syddall HE et al (2018) Relationships between markers of inflammation and muscle mass, strength and function: findings from the Hertfordshire cohort study. Calcif Tissue Int 102:287–295. https://doi.org/10.1007/s00223-017-0354-4
Lassale C, Batty GD, Steptoe A et al (2018) Association of 10-year C-reactive protein trajectories with markers of healthy aging: findings from the English Longitudinal Study of Ageing. J Gerontol A Biol Sci Med Sci. https://doi.org/10.1093/gerona/gly028
Visser M, Kritchevsky SB, Newman AB et al (2005) Lower serum albumin concentration and change in muscle mass: the health, aging and body composition study. Am J Clin Nutr 82:531–537. https://doi.org/10.1093/ajcn/82.3.531
Schalk BW, Deeg DJ, Penninx BW, Bouter LM, Visser M (2005) Serum albumin and muscle strength: a longitudinal study in older men and women. J Am Geriatr Soc 53:1331–1338. https://doi.org/10.1111/j.1532-5415.2005.53417.x
Tuttle CSL, Thang LAN, Maier AB (2020) Markers of inflammation and their association with muscle strength and mass: a systematic review and meta-analysis. Ageing Res Rev 64:101185. https://doi.org/10.1016/j.arr.2020.101185
Clark AB, Reijnierse EM, Lim WK, Maier AB (2020) Prevalence of malnutrition comparing the GLIM criteria, ESPEN definition and MST malnutrition risk in geriatric rehabilitation patients: RESORT. Clin Nutr 39:3504–3511. https://doi.org/10.1016/j.clnu.2020.03.015
Ellis G, Gardner M, Tsiachristas A et al (2017) Comprehensive geriatric assessment for older adults admitted to hospital. Cochrane Database Syst Rev 9:Cd006211. https://doi.org/10.1002/14651858.CD006211.pub3
Hudon C, Fortin M, Vanasse A (2005) Cumulative Illness Rating Scale was a reliable and valid index in a family practice context. J Clin Epidemiol 58:603–608. https://doi.org/10.1016/j.jclinepi.2004.10.017
Ferguson M, Capra S, Bauer J, Banks M (1999) Development of a valid and reliable malnutrition screening tool for adult acute hospital patients. Nutrition 15:458–464. https://doi.org/10.1016/S0899-9007(99)00084-2
Cederholm T, Jensen GL, Correia MITD et al (2019) GLIM criteria for the diagnosis of malnutrition—a consensus report from the global clinical nutrition community. J Cachexia Sarcopenia Muscle 10:207–217. https://doi.org/10.1002/jcsm.12383
Rockwood K, Song X, MacKnight C et al (2005) A global clinical measure of fitness and frailty in elderly people. CMAJ 173:489–495. https://doi.org/10.1503/cmaj.050051
Chumlea WC, Roche AF, Steinbaugh ML (1985) Estimating stature from knee height for persons 60 to 90 years of age. J Am Geriatr Soc 33:116–120. https://doi.org/10.1111/j.1532-5415.1985.tb02276.x
Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW (1963) Studies of illness in the aged. The index of ADL: a standardized measure of biological and psychosocial function. JAMA 185:914–919. https://doi.org/10.1001/jama.1963.03060120024016
Guralnik JM, Simonsick EM, Ferrucci L et al (1994) A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol 49:M85-94. https://doi.org/10.1093/geronj/49.2.M85
Govoni B, Mantovani G, Maietti E et al (2019) Hand grip strength assessment in older people: is the supine position valid and reliable? Eur Geriatr Med 10:741–745. https://doi.org/10.1007/s41999-019-00226-9
Reijnierse EM, de Jong N, Trappenburg MC et al (2017) Assessment of maximal handgrip strength: how many attempts are needed? J Cachexia Sarcopenia Muscle 8:466–474. https://doi.org/10.1002/jcsm.12181
Ling CHY, de Craen AJM, Slagboom PE et al (2011) Accuracy of direct segmental multi-frequency bioimpedance analysis in the assessment of total body and segmental body composition in middle-aged adult population. Clin Nutr 30:610–615. https://doi.org/10.1016/j.clnu.2011.04.001
Boyd CM, Landefeld CS, Counsell SR et al (2008) Recovery of activities of daily living in older adults after hospitalization for acute medical illness. J Am Geriatr Soc 56:2171–2179. https://doi.org/10.1111/j.1532-5415.2008.02023.x
Mehta KM, Pierluissi E, Boscardin WJ et al (2011) A clinical index to stratify hospitalized older adults according to risk for new-onset disability. J Am Geriatr Soc 59:1206–1216. https://doi.org/10.1111/j.1532-5415.2011.03409.x
Dennis RA, Johnson LE, Roberson PK et al (2012) Changes in activities of daily living, nutrient intake, and systemic inflammation in elderly adults receiving recuperative care. J Am Geriatr Soc 60:2246–2253. https://doi.org/10.1111/jgs.12007
Liu JYJ, Reijnierse EM, van Ancum JM, Verlaan S, Meskers CGM, Maier AB (2019) Acute inflammation is associated with lower muscle strength, muscle mass and functional dependency in male hospitalised older patients. PLoS ONE 14:e0215097. https://doi.org/10.1371/journal.pone.0215097
Bautmans I, Njemini R, Lambert M, Demanet C, Mets T (2005) Circulating acute phase mediators and skeletal muscle performance in hospitalized geriatric patients. J Gerontol A Biol Sci Med Sci 60:361–367. https://doi.org/10.1093/gerona/60.3.361
Beyer I, Njemini R, Bautmans I, Demanet C, Bergmann P, Mets T (2012) Inflammation-related muscle weakness and fatigue in geriatric patients. Exp Gerontol 47:52–59. https://doi.org/10.1016/j.exger.2011.10.005
Iwata M, Kuzuya M, Kitagawa Y, Iguchi A (2006) Prognostic value of serum albumin combined with serum C-reactive protein levels in older hospitalized patients: continuing importance of serum albumin. Aging Clin Exp Res 18:307–311. https://doi.org/10.1007/BF03324664
Kim MH, Ahn JY, Song JE et al (2015) The C-reactive protein/albumin ratio as an independent predictor of mortality in patients with severe sepsis or septic shock treated with early goal-directed therapy. PLoS ONE 10:e0132109. https://doi.org/10.1371/journal.pone.0132109
Ranzani OT, Zampieri FG, Forte DN, Azevedo LC, Park M (2013) C-reactive protein/albumin ratio predicts 90-day mortality of septic patients. PLoS ONE 8:e59321. https://doi.org/10.1371/journal.pone.0059321
Churilov I, Churilov L, MacIsaac RJ, Ekinci EI (2018) Systematic review and meta-analysis of prevalence of sarcopenia in post acute inpatient rehabilitation. Osteoporos Int 29:805–812. https://doi.org/10.1007/s00198-018-4381-4
Landi F, Calvani R, Ortolani E et al (2017) The association between sarcopenia and functional outcomes among older patients with hip fracture undergoing in-hospital rehabilitation. Osteoporos Int 28:1569–1576. https://doi.org/10.1007/s00198-017-3929-z
Sanchez-Rodriguez D, Marco E, Miralles R et al (2014) Sarcopenia, physical rehabilitation and functional outcomes of patients in a subacute geriatric care unit. Arch Gerontol Geriatr 59:39–43. https://doi.org/10.1016/j.archger.2014.02.009
Aquilani R, Zuccarelli GC, Maestri R et al (2021) Inflammation, pressure ulcers and poor functional status predict negative rehabilitation outcomes in postacute geriatric patients. Aging Clin Exp Res 33:463–467. https://doi.org/10.1007/s40520-020-01526-y
Guan L, Tuttle CSL, Reijnierse EM, Lim WK, Maier AB (2021) Unresolved inflammation during hospitalization is associated with post-discharge institutionalization and mortality in geriatric rehabilitation inpatients: the RESORT cohort. Exp Gerontol 156:111597. https://doi.org/10.1016/j.exger.2021.111597
Wåhlin-Larsson B, Wilkinson DJ, Strandberg E, Hosford-Donovan A, Atherton PJ, Kadi F (2017) Mechanistic links underlying the impact of C-reactive protein on muscle mass in elderly. Cell Physiol Biochem 44:267–278. https://doi.org/10.1159/000484679
Jones DT, Ganeshaguru K, Anderson RJ et al (2003) Albumin activates the AKT signaling pathway and protects B-chronic lymphocytic leukemia cells from chlorambucil- and radiation-induced apoptosis. Blood 101:3174–3180. https://doi.org/10.1182/blood-2002-07-2143
Lai KM, Gonzalez M, Poueymirou WT et al (2004) Conditional activation of AKT in adult skeletal muscle induces rapid hypertrophy. Mol Cell Biol 24:9295–9304. https://doi.org/10.1128/MCB.24.21.9295-9304.2004
Allen SC (2017) Systemic inflammation in the genesis of frailty and sarcopenia: an overview of the preventative and therapeutic role of exercise and the potential for drug treatments. Geriatrics (Basel). https://doi.org/10.3390/geriatrics2010006
Calle MC, Fernandez ML (2010) Effects of resistance training on the inflammatory response. Nutr Res Pract 4:259–269. https://doi.org/10.4162/nrp.2010.4.4.259
Deer RR, Volpi E (2018) Protein requirements in critically ill older adults. Nutrients 10:378. https://doi.org/10.3390/nu10030378
Acknowledgements
The authors would like to thank all investigators associated with RESORT.
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This work was supported by the Medical Research Future Fund, RART.
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Study concept and design: JMA, CSLT, RK, MP, CGMM, SKP, WKL, EMR, GSL and ABM. Acquisition of data: JMA, CSLT, WKL, EMR and ABM. Analysis and interpretation of data: JMA, CSLT, RK, MP, CGMM, SKP, EMR, GSL and ABM. Drafting of the manuscript: JMA, CSLT, RK, MP, CGMM, EMR, GSL and ABM. Critical revision of the manuscript for important intellectual content: JMA, CSLT, RK, MP, CGMM, SKP, WKL, EMR, GSL and ABM. Study supervision: ABM.
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This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Melbourne Health Human Research Ethics Committee (no. HREC/17/MH/103).
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Van Ancum, J.M., Tuttle, C.S.L., Koopman, R. et al. Albumin and C-reactive protein relate to functional and body composition parameters in patients admitted to geriatric rehabilitation after acute hospitalization: findings from the RESORT cohort. Eur Geriatr Med 13, 623–632 (2022). https://doi.org/10.1007/s41999-022-00625-5
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DOI: https://doi.org/10.1007/s41999-022-00625-5