Abstract
Background
As a person ages, total body water (TBW), intracellular water (ICW), muscle mass and muscle strength tend to decline. The decline in ICW may reflect losses in the number of muscle cells but may also be responsible for less hydrated muscle cells.
Aim
To assess whether TBW and ICW are associated with muscle strength, functional performance and frailty in an aged population, independently of muscle mass.
Methodology: Design
An observational cross-sectional study of community-dwelling individuals aged 75 years and older. TBW, ICW, fat mass, lean mass and muscle mass were assessed by bioelectrical impedance analysis, frailty status was measured according to Fried criteria, handgrip strength was measured using the hand-held JAMAR dynamometer, and functional performance was measured according to the Barthel index and gait speed.
Results
A total of 324 subjects were recruited (mean age 80.1 years, 47.5% women). TBW and ICW were closely correlated with muscle mass in both sexes. ICW was also associated with Barthel score, gait speed and frailty in both sexes and with handgrip in men. Considerable variability in ICW was observed for the same muscle mass. Multivariate analysis showed a positive effect of ICW on handgrip, functional performance and gait speed and a protective effect of ICW on frailty, independently of age, sex, body mass index and number of comorbidities.
Conclusions
In elderly individuals with similar muscle mass, those with higher ICW had a better functional performance and a lower frailty risk, suggesting a protective effect of cell hydration, independently of muscle mass.
Key words: Total body water, intracellular water, ageing, muscle mass, muscle strength, frailty, functional performance
Introduction
Water is the main component of human body and represents approximately 60% of body weight in adult men and 50%- 55% in adult women (1). Water content in lean body mass and in adipose tissue is about 73% and 10%, respectively. Older persons, women and obese individuals have lower total body water (TBW) because of their lower lean body mass. Water is distributed in the body as intracellular water (ICW) and extracellular water (ECW), which mainly includes plasma fluid and interstitial fluid. Fluid exchange between compartments is regulated by osmotic and hydrostatic pressure, with water flowing according to changes in extracellular fluid osmolarity (2). Water has fundamental functions in the body: a) it provides structure for cells and body fluids; b) it acts as a reaction medium and solvent and also as a reactant in body metabolism; c) it transports nutrients in the blood and interstitial fluid and transports waste in the urine; and d) it helps control body temperature through sweat evaporation (3). Water losses mainly occur in urine and sweat, but also through the faeces, skin and respiration. Water inputs mainly come from diet (food and fluids) but small quantities also come from body metabolic activity. Water balance in the body is tightly regulated by the kidneys, which can concentrate or dilute urine depending on metabolic wastes and water intake (2).
The water content of muscle, which represents the major component of body weight, is about 76%, so water losses may affect muscle function. It is known that moderate acute water losses (2%-3% of body weight) can produce fatigue and weakness, and can also alter mental state, inducing memory loss and affecting mental and psychomotor skills (4, 5). However, the effects of small but gradual losses of water observed with age are not well known. Water loss may be the result of a parallel decline in muscle mass, but may also be a contributor to muscle function impairment due to muscle cell dehydration (6). We hypothesize that the slow and gradual water losses that occur with age may be partially responsible for muscular weakness, functional impairment and frailty. The aim of this study was to assess if TBW and ICW are associated with muscle weakness, frailty and impaired functional performance in an aged population, independently of muscle mass, age, sex and body mass index (BMI).
Methodology
Study design and population
An observational cross-sectional study was performed of community-dwelling subjects aged 75 years and older. A sample was randomly selected from the database of 3 primary care centres in the city of Mataró (Barcelona, Spain). Selected subjects were invited to participate if they were not institutionalized, did not have active malignancy, dementia or serious mental illness and had a life expectancy greater than 6 months. Recruitment took place from January to July 2014. Study design details have been reported elsewhere (7). The hospital research ethics committee approved the study protocol (code 64/13) and all participants signed an informed consent form before inclusion.
Study factors and data collection
The main study factors included TBW, ICW, muscle mass, muscle strength and functional performance. TBW (in absolute litres or as % of total body weight), ICW (in absolute litres or as % TBW) and fat mass, lean mass and muscle mass (in absolute kg or as % of total body weight) were assessed by bioelectrical impedance analysis (BIA) (Bioelectrical Impedance Analyser, EFG3Elecrtofluidgraph, Akern SRL). Frailty status (robust, pre-frail or frail) was assessed according to Fried criteria (8), muscle strength was estimated from handgrip strength (assessed in kg by a hand-held JAMAR dynamometer), and functional performance was assessed according to the Barthel index score, the timed up-and-go test (TUG) and gait speed. Other study variables included socio-demographic characteristics, co-morbidities, geriatric syndromes and chronic medication. Information on comorbidities and medications was obtained from patient electronic medical records held by the corresponding centres. All other information was obtained directly from the patient by trained healthcare professionals.
Statistical analysis
The Pearson correlation coefficient (r) was used to assess TBW and ICW correlations with other continuous variables such as muscle mass, Barthel index score and gait speed. Frail and non-frail subjects were compared using the X2 test or Fisher's exact test for categorical variables and the t-test or Mann-Whitney U test for numerical variables. Linear regression analyses were performed and beta coefficients estimated to assess the effect of TBW and ICW on handgrip, Barthel index score and gait speed. The odds ratio (OR), calculated using logistic regression, was used as a measure of TBW and ICW associations with frailty. Regression analyses were used to adjust the effect of TBW and ICW for age, sex, muscle mass, BMI and number of co-morbidities. To assess the effect of ICW on strength, performance and frailty adjusted for muscle mass, a stratified analysis was also conducted of two muscle mass groups categorized according to the 50th percentile (p50) cut-off. To assess interactions according to sex, all analyses were performed on the full sample and separately for men and women. Statistical significance was set to p<0.05.
Results
A total of 324 community-dwelling elderly subjects were recruited with a mean age of 80.1 (SD 3.5) years, 154 (47.5%) of whom were women. TBW represented 56.7% and 48.4% of total body weight in men and women, respectively, and ICW represented 52.2% and 49.9% of TBW in men and women, respectively. TBW (as % of total body weight) was uncorrelated with age (r=-0.059, p=0.290), in both men (r=- 0.138, p=0.075) and women (r=0.054, p=0.508). ICW (as %TBW) was negatively correlated with age in the overall sample (r=-0.260, p<0.001) and in men (r=-0.439, p<0.001), but not in women (r=-0.096, p=0.239). While TBW was negatively correlated with BMI (r=-0.607, p<0.001) in both men (r=-0.531, p<0.001) and women (r=-0.748, p<0.001), ICW was uncorrelated with BMI (r=0.077, p=0.166) in both men (r=0.134, p=0.083) and women (r=0.174, p=0.032).
Table 1 shows TBW and ICW correlations with muscle mass, handgrip, Barthel index score and gait speed, as well as their relationship with frailty for both the overall sample and the sample stratified by sex. Evident is the high correlation of muscle mass with TBW and ICW in both men and women, and a significant ICW association with Barthel index score, gait speed and frailty in both sexes and also with handgrip in men.
Table 1.
Total body water (TBW) and intracellular water (ICW)for the overall sample and by sex: correlationswith muscle mass, muscle strength, Barthel index score and gait speed, and association with frailty
| Muscle mass | Handgrip (kg) | Barthel index | Gait speed (m/s) | Frailty | |||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| r | p | r | p | r | p | r | p | Yes | no | p | |
| All individuals | |||||||||||
| TBW (%) | 0.89 | <0.001 | 0.62 | <0.001 | <0.001 | 0.34 | <0.001 | 0.34 | 49.1% | 53.3% | <0.001 |
| ICW (%) | 0.60 | <0.001 | 0.40 | <0.001 | 0.33 | <0.001 | 0.31 | <0.001 | 48.9% | 51.4% | <0.001 |
| Women | |||||||||||
| TRW (%) | 0.80 | <0.001 | 0.13 | 0.116 | 0.22 | 0.006 | 0.16 | 0.042 | 47.4% | 48.6% | 0.117 |
| ICW (%) | 0.44 | <0.001 | 0.13 | 0.102 | 0.25 | 0.002 | 0.25 | 0.002 | 48.7% | 50.2% | 0.027 |
| Men | |||||||||||
| TBW (%) | 0.71 | <0.001 | 0.02 | 0.766 | 0.16 | 0.034 | 0.21 | <0.001 | 54.5% | 56.9% | 0.110 |
| ICW (%) | 0.60 | <0.001 | 0.20 | 0.010 | 0.24 | 0.002 | 0.26 | 0.001 | 49.4% | 52.4% | 0.018 |
Muscle mass as % of total body weight. r: Pearson correlation coefficient.
Figure 1 plots muscle mass and ICW, showing that, for both men and women with a similar muscle mass, ICW is highly variable. Figure 2 plots muscle strength and ICW by muscle mass and sex groups. Table 2 reports results for the effect of TBW and ICW on handgrip, Barthel index score, gait speed (linear regression analysis) and frailty (logistic regression analysis) adjusted for age, sex, muscle mass or BMI and number of co-morbidities. Evident are the positive effect of ICW on handgrip and functional performance and the protective effect on frailty.
Figure 1.
Relationship between muscle strength (handgrip) and intracellular water (ICW) stratified by muscle mass (above or below p50) and sex
Figure 2.
Relationship between muscle strength (handgrip) and intracellular water (ICW) stratified by muscle mass (above or below p50) and sex
Table 2.
Adjusted effect of total body water (TBW) and intracellular water (ICW) on handgrip, Barthel index score, gait speed and frailty for the overall sample and by sex
| Handgrip (kg) | Barthel index | Gait speed (m/s) | Frailty | |||||
|---|---|---|---|---|---|---|---|---|
| β | p | β | p | β | p | OR | p | |
| All individuals | ||||||||
| TBW (%)a | 0.139 | 0.114 | 0.139 | 0.143 | 0.004 | 0.285 | 0.96 | 0.429 |
| ICW (%)a | 0.197 | 0.021 | 0.299 | 0.001 | 0.013 | <0.001 | 0.84 | 0.005 |
| ICW (%)b | 0.144 | 0.144 | 0.140 | 0.189 | 0.007 | 0.090 | 0.89 | 0.061 |
| Women | ||||||||
| TBW (%)c | 0.174 | 0.098 | 0.299 | 0.094 | 0.002 | 0.740 | 0.96 | 0.581 |
| ICW (%)c | 0.127 | 0.176 | 0.393 | 0.013 | 0.016 | <0.001 | 0.84 | 0.017 |
| ICW (%)d | 0.059 | 0.579 | 0.170 | 0.340 | 0.009 | 0.090 | 0.88 | 0.089 |
| Men | ||||||||
| TBW (%c | 0.115 | 0.409 | -0.002 | 0.985 | 0.005 | 0.292 | 0.93 | 0.496 |
| ICW (%)c | 0.352 | 0.022 | 0.229 | 0.017 | 0.011 | 0.060 | 0.84 | 0.162 |
| ICW (%)d | 0.306 | 0.080 | 0.145 | 0.192 | 0.006 | 0.018 | 0.91 | 0.460 |
TBWas % of total body weight. ICWas % of total body water. β: linear regression coefficient. OR: odds ratio; a. Adjusted for age, sex, BMI and number of comorbidities; b. Adjusted for age, sex, muscle mass and number of comorbidities; c. Adjusted for age, BMI and number of comorbidities;d. Adjusted for age, muscle mass, BMI and number of comorbidities.
Table 3 compares handgrip, Barthel index score, gait speed and frailty status for groups with a similar muscle mass but different ICW. It shows that, in individuals with above-median muscle mass, those with ICW>p50 have a higher Barthel index score and lower TUG test than those with ICW<p50.
Table 3.
Intracellular water (ICW) relationship with strength, functionality, performance and frailty stratified by muscle massfor the overall sample and by sex
| Muscle mass <p50 | Muscle mass ≥ p50 | |||||
|---|---|---|---|---|---|---|
| ICW<p50 | ICW ≥p50 | p | ICW<p50 | ICW ≥p50 | p | |
| All individuals | ||||||
| Handgrip (kg) | 24.1 (9.6) | 23.7 (8.8) | 0.875 | 22.3 (7.9) | 25.4 (8.9) | 0.096 |
| Barthel index | 95.1 (7.0) | 95.8 (7.8) | 0.158 | 96.3 (6.1) | 98.6 (3.3) | 0.016 |
| Gait speed (m/s) | 0.88 (0.2) | 0.88 (0.2) | 0.997 | 0.90 (0.2) | 1.00 (0.2) | 0.085 |
| TUG (seconds) | 9.7 (3.5) | 9.4 (3.3) | 0.613 | 9.2 (2.6) | 8.0 (1.6) | 0.004 |
| Frailty (%) | 21.3% | 16.4% | 0.430 | 14.3% | 4.2% | 0.067 |
| Women | ||||||
| Handgrip (kg) | 15.3 (4.7) | 16.7 (3.6) | 0.164 | 17.7 (4.6) | 17.1 (4.3) | 0.357 |
| Barthel index | 93.0 (7.0) | 93.0 (9.9) | 0.346 | 95.0 (7.0) | 98.0 (4.9) | 0.122 |
| Gait speed (m/s) | 0.78 (0.2) | 0.80 (0.2) | 0.563 | 0.84 (0.2) | 0.95 (0.2) | 0.030 |
| TUG (seconds) | 11.0 (3.0) | 10.4 (4.0) | 0.142 | 9.7 (3.0) | 8.4 (2.0) | 0.017 |
| Frailty (%) | 33.3% | 29.0% | 0.685 | 22.2% | 6.8% | 0.065 |
| Men | ||||||
| Handgrip (kg) | 30.4 (6.8) | 30.9 (6.4) | 0.737 | 30.6 (5.4) | 32.4 (5.0) | 0.244 |
| Barthel index | 96.6 (6.2) | 98.7 (2.6) | 0.151 | 98.3 (4.1) | 99.4 (1.9) | 0.261 |
| Gait speed (m/s) | 0.95 (0.2) | 0.97 (0.2) | 0.858 | 1.03 (0.3) | 1.05 (0.2) | 0.577 |
| TUG (seconds) | 8.9 (3.4) | 8.4 (1.8) | 0.888 | 8.1 (2.3) | 7.7 (1.6) | 0.499 |
| Frailty (%) | 12.7% | 3.3% | 0.150 | 0% | 1.9% | --- |
p50: 50thpercentile. TUG: timed up-and-go test; p50of muscle mass for men =46%. p50of muscle mass for women =37%. p50of ICW for men =52.5%. p50 of ICW for women =50.0%
Discussion
The main results of the present study indicate that, for community-dwelling elderly subjects: a) TBW is closely correlated with muscle mass and is also positively correlated with Barthel index score and gait speed in both men and women; b) ICW is correlated with muscle mass, Barthel index score and gait speed in both men and women and is also correlated with handgrip in men; c) frail compared to nonfrail men and women have lower ICW percentages, indicating that ICW has a protective effect on frailty; d) ICW, when adjusted for age, BMI and co-morbidities, has a positive effect on Barthel index score, gait speed and frailty in women and on handgrip and Barthel index score in men; and e) for a muscle mass above p50, higher ICW is associated with better functional performance. These results point to a relevant role of intracellular water in muscle functioning and suggest that its determination could be a relevant marker of functional capacity and performance in elderly subjects.
Water is an essential nutrient for life, but as a person ages, TBW tends to decline because of a decrease in fat-free mass and muscle mass. Different studies have proposed poor physical activity, malnutrition (7), anabolic hormonal decline (9), insulin resistance (10) and inflammation (11) as the main factors responsible for muscle wasting with age (12). However, other factors may influence TBW in elderly individuals, such as decreased water intake secondary to a reduced thirst sensation (13), age-related dysphagia or dysphagia secondary to stroke or neurodegenerative diseases (14), and increased water excretion due to medication or an impaired kidney capacity to concentrate urine (15). Decreased water intake or excessive water excretion may lead to dehydration. However, age-related dehydration does not seem to affect ECW and ICW compartments equally. Increased ECW relative to ICW with age has been described and proposed as a biomarker of muscle ageing (6). This idea is reinforced by the observation of increased relaxation time for fast-twitch muscle fibres in elderly people attributed to increased extracellular space (16).
The above findings are corroborated by the results of our study. We observed that muscle mass was strongly correlated with TBW and ICW. However, the correlation between ICW and muscle mass, in both men and women, was not very high, indicating variability in % ICW for the same muscle mass (as shown in Figure 1), that is, variability in muscle cell hydration. The observed effect of ICW on strength and performance may be partially attributed to reasons other than muscle mass, such as better quality and better hydrated muscle cells. Our results show an independent effect of ICW on muscle strength, functional performance, gait speed and frailty when adjusted for age, sex, BMI and co-morbidities. However, except for gait speed in men, this effect was not statistically significant when adjusted for muscle mass, probably because of a lack of statistical power. Noteworthy is the fact that, when adjusted for age, sex, muscle mass and co-morbidities, ICW had a protective effect on frailty, with OR=0.89 (p=0.061), suggesting an 11% reduction in frailty risk for each 1% increase in ICW. Yamada et al. (6) reported that thigh ECW/ICW ratio was a significant predictor of knee extension strength and gait speed independently of age, sex, BMI and skeletal muscle mass. These authors conclude that ECW space in skeletal muscle tissue increases with age and that the expanded ECW (or reduced ICW) can partially explain the reduction in muscle quality (muscle strength/skeletal muscle mass) observed with ageing. A study that assessed and compared body water compartments for healthy adults, healthy elderly and elderly patients, reported higher ECW in elderly patients compared to healthy elderly individuals. Another finding was that the proportions of water spaces remained constant from healthy adults to healthy elderly individuals, suggesting that cell hydration is preserved in the latter (17).
Similar results have been reported for young adult athletes. Silva et al.(18) reported that athletes who increase muscle strength by more than 3% over a full sport season showed significantly higher ICW and concluded that ICW is the main predictor of leg strength and jump performance in highly trained athletes. Moreover, athletes who showed a decrease in ICW during training sessions were also found to have reduced power and grip strength (19, 20). Proposed as a physiological explanation for this direct relationship is the so-called cell swelling theory (21, 22), which suggests that cell volume is a metabolic signal that regulates cellular function. The theory is based on in vivo evidence indicating that cellular swelling leads to anabolism, counteracts proteolysis and stimulates glycogen synthesis, whereas cellular shrinkage promotes catabolism and protein degradation. Since cell volume is influenced by extracellular osmolality, extracellular hypo-osmolality leads to cell swelling, whereas extracellular hyper-osmolality leads to cell shrinking. Keller et al.(23), who assessed the effect of acute changes in extracellular osmolality on protein, glucose and lipid metabolism in 10 male subjects, concluded that hypoosmolality promotes lipolysis and counteracts proteolysis and glycogenolysis, while hyper-osmolality induces glycogenolysis. The cell swelling theory is also supported by the idea that water, inbinding to glycogen, ensures good availability of nutrients and optimal energy resource usage and has anabolic effect, whereas ICW depletion impedes nutrient availability and may produce an intracellular catabolic effect.
ICW evaluation may also be of interest for several critical conditions that can be considered in terms of accelerated model of frailty. In critically ill patients, for instance, ECW/ICW ratio trends could help manage sarcopenia subsequent to sepsis and assist with nutritional and functional monitoring (24, 25). In this kind of patient, biochemical or anthropometric evaluation are not useful in monitoring the effect of nutritional support and radiologic evaluation of muscle mass (26) is both static and laborious. BIA has been shown to be useful in assessing and monitoring nutritional status in critically ill patients (27). The ECW/ICW ratio in critically ill patients is increased, and when >1, is associated with proteolysis and poorer evolution of patients with sepsis and trauma (28, 29, 30). All the above mentioned evidence would suggest that ICW plays an important role in cell functioning and that cell dehydration may partially be responsible for poor muscle strength. There are very few published studies reporting the effect of ICW on muscle function and frailty in elderly individuals, which required further large and prospective studies.
Among the limitations of this study is its cross-sectional design, which does not allow causal relationships to be established. Another limitation is the small sample size, which compromises its statistical power, especially for subgroup and multivariate analyses. Finally, although BIA was performed in standard conditions (an apparently well hydrated patient who had rested for 15 minutes before testing, who was tested lying down, with all metallic elements removed), the reliability of this measurement may be compromised because of hours of food and liquid fasting, previous exercise, temperature, sweating or liquid retention.
In summary, the decline in TBW and in ICW in the elderly mainly reflects a decrease in muscle mass and is accompanied by a decrease in muscle strength and impaired functional performance. However, for individuals with a similar muscle mass, the fact that those with higher ICW have a better functional performance and a lower frailty risk would suggest that cell hydration has a protective effect that is independent of muscle mass. These results have two main potential clinical implications; a) ICW could be used as an indicator or a biomarker for frailty and muscular impairment, and b) physicians should keep in mind the importance of good hydration in the elderly, should recommend enough water intake and should assess possible effects of diseases, pharmacological treatments, diets, physical activity or environmental conditions on water balance to ensure good hydration. Further prospective and well-powered observational studies are needed to assess the role played by TBW and the ECW/ICW ratio in the genesis of frailty and disability in elderly individuals.
y
All authors declare that they have no conflict of interest in relation with this study.
Ethical standard
This study comply with the current Spanish laws regarding confidenciality and clinical research.
Funding
This work was supported by a grand from the Spanish Ministry of Health (Instituto de Salud Carlos III, FIS PI 13/00931). (Co-funded by European Regional Development Fund/European Social Fund/»Investing in your future»).
References
- 1.EFSA journal. 2010;8(3) [Google Scholar]
- 2.Roumelioti ME, Glew RH, Khitan ZJ, Rondon–Berrios H, Argyropoulos CP, Malhota D, et al. Fluid balance concepts in medicine:principles and practice. World J Nephrol. 2018;7(1):1–28. doi: 10.5527/wjn.v7.i1.1. 10.5527/wjn.v7.i1.1 PubMed PMID: 29359117, PMCID 5760509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Kleiner S. Water:an essential but overlooked nutrient. J Am Diet Assoc. 1999;99(2):200–206. doi: 10.1016/S0002-8223(99)00048-6. 10.1016/S0002-8223(99)00048-6 PubMed PMID: 9972188. [DOI] [PubMed] [Google Scholar]
- 4.Hooper L, Bunn D, Jimoh FO, Fairweather–Tait SJ. Water–loss dehydration and aging. Mech Ageing Dev. 2014;136–137:50–58. doi: 10.1016/j.mad.2013.11.009. 10.1016/j.mad.2013.11.009 PubMed PMID: 24333321. [DOI] [PubMed] [Google Scholar]
- 5.Miller HJ. Dehydration in the Older Adult. J GerontolNurs. 2015;41(9):8–13. doi: 10.3928/00989134-20150814-02. [DOI] [PubMed] [Google Scholar]
- 6.Yamada Y, Yoshida T, Yocoyama K, Watanabe Y, Miyake M, Yamagata E, et al. The extracellular to intracellular water ratio in upper legs is negatively associated with skeletal muscle strength and gait speed in older people. J GerontolABiol Sci Med Sci. 2017;72:293–298. doi: 10.1093/gerona/glw125. [DOI] [PubMed] [Google Scholar]
- 7.Serra–Prat M, Papiol M, Vico J, Palomera E, Bartolomé M, Burdoy E. Factors associated with poor muscle mass and strength in a community–dwelling elderly population:a cross–sectional study. J GerontolGeriatr Res. 2017;6:2. [Google Scholar]
- 8.Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA. Frailty in older adults:evidence for a phenotype. The Journals of Gerontology series A Biological Sciences and Medical Sciences. 2001;56A:M146–M156. doi: 10.1093/gerona/56.3.m146. 10.1093/gerona/56.3.M146 [DOI] [PubMed] [Google Scholar]
- 9.Morley J, Malmstrom T. Frailty, sarcopenia and hormones. EndocrinolMetabClin N Am. 2013;42:391–405. doi: 10.1016/j.ecl.2013.02.006. 10.1016/j.ecl.2013.02.006 [DOI] [PubMed] [Google Scholar]
- 10.Barzilay JI, Cotsonis GA, Walston J, the Health ABC study Insulin resistance is associated with decreased quadriceps muscle strength in nondiabetic adults aged ≥70 years. Diabetes Care. 2009;32:736–738. doi: 10.2337/dc08-1781. 10.2337/dc08-1781 PubMed PMID: 19171728, PMCID 2660450. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Fougère, B, Boulanger, E, Nourhashémi, F, Guyonnet, S, Cesari, M, Chronic Inflammation:Accelerator of Biological Aging, J GerontolABiol Sci Med Sci., 2016 [DOI] [PubMed]
- 12.Cruz–Jentoft A, Landi F, Topinková E, et al. Understanding sarcopenia as a geriatric syndrome. CurrOpin Clin NutrMetab Care. 2010;13:1–7. doi: 10.1097/MCO.0b013e328333c1c1. 10.1097/MCO.0b013e328333c1c1 [DOI] [PubMed] [Google Scholar]
- 13.Kenney, WL, Chiu, P, Influence of age in thirst and fluid intake, Medicine and Science in sports and exercise, 2001, 33 [DOI] [PubMed]
- 14.Carrión, S, Roca, M, Arreola, V, Ortega, O, Palomera, E, Serra–Prat, M, Cabré, M, Clavé, P, Nutrition status of older patients with oropharyngealdysphagia in a chronic versus an acute clinical situation, Clinical Nutrition, 2016 [DOI] [PubMed]
- 15.Bennett J. Dehydration:Hazards and benefits. Geriatric Nursing. 2000;21:84–88. doi: 10.1067/mgn.2000.107135. 10.1067/mgn.2000.107135 PubMed PMID: 10769332. [DOI] [PubMed] [Google Scholar]
- 16.Hatakenaka M, Ueda M, Ishigami K, Otsuka M, Masuda K. Effects of ageing on muscle T2relaxation time:difference between fast–and slow–twitch muscles. Invest Radiol. 2001;36:692–698. doi: 10.1097/00004424-200112000-00003. 10.1097/00004424-200112000-00003 PubMed PMID: 11753139. [DOI] [PubMed] [Google Scholar]
- 17.Ritz P. Investigators of the Source Study and of the Human Nutrition Research Centre–Auvergne. Chronic cellular dehydration and the aged patient. J GerontolABiol Sci Med Sci. 2001;56:M349–M352. doi: 10.1093/gerona/56.6.m349. 10.1093/gerona/56.6.M349 [DOI] [PubMed] [Google Scholar]
- 18.Silva AM, Matias CN, Santos DA, Rocha PM, Minderico CS, Sardinha LB. Increases in intracellular water explain strength and power improvements over a season. Int J Sports Med. 2014;35(13):1101–1105. doi: 10.1055/s-0034-1371839. 10.1055/s-0034-1371839 PubMed PMID: 25009970. [DOI] [PubMed] [Google Scholar]
- 19.Silva A M, Fields D A, Heymsfield S B, Sardinha L B. Body composition and power changes in elite judo athletes. Int J Sports Med. 2010;31:737–741. doi: 10.1055/s-0030-1255115. 10.1055/s-0030-1255115 PubMed PMID: 20645233. [DOI] [PubMed] [Google Scholar]
- 20.Silva A M, Fields D A, Heymsfield S B, Sardinha L B. Relationship between changes in total–body water and fluid distribution with maximal forearm strength in elite judo athletes. J Strength Cond Res. 2011;25:2488–2495. doi: 10.1519/JSC.0b013e3181fb3dfb. 10.1519/JSC.0b013e3181fb3dfb PubMed PMID: 21869630. [DOI] [PubMed] [Google Scholar]
- 21.Lang F, Busch G L, Ritter M, Volkl H, Waldegger S, Gulbins E, Haussinger D. Functional significance of cell volume regulatory mechanisms. Physiol Rev. 1998;78:247–306. doi: 10.1152/physrev.1998.78.1.247. 10.1152/physrev.1998.78.1.247 PubMed PMID: 9457175. [DOI] [PubMed] [Google Scholar]
- 22.Haussinger D, Roth E, Lang F, Gerok W. Cellular hydration state:an important determinant of protein catabolism in health and disease. Lancet. 1993;341:1330–1332. doi: 10.1016/0140-6736(93)90828-5. 10.1016/0140-6736(93)90828-5 PubMed PMID: 8098459. [DOI] [PubMed] [Google Scholar]
- 23.Keller U, Szinnai G, Bilz S, Berneis K. Effects of changes in hydration onprotein, glucose and lipid metabolism in man: impact on health. Eur J Clin Nutr. 2003;57:s69–s74. doi: 10.1038/sj.ejcn.1601904. 10.1038/sj.ejcn.1601904 PubMed PMID: 14681716. [DOI] [PubMed] [Google Scholar]
- 24.McClave SA, Martindale RG, Vanek VW, McCarthy M, Roberts P, Taylor B, Ochoa JB, Napolitano L, Cresci G. ASPEN Board of Directors; American College of Critical Care Medicine; Society of Critical Care Medicine. Guidelines for the Provision and Assessment of Nutrition Support Therapy in the Adult Critically Ill Patient: Society of Critical Care Medicine (SCCM) and American Society for Parenteral and Enteral Nutrition (ASPEN) JPEN J Parenter Enteral Nutr. 2009;33(3):277–316. doi: 10.1177/0148607109335234. 10.1177/0148607109335234 [DOI] [PubMed] [Google Scholar]
- 25.Singer P, Berger MM, Van den Berghe G, Biolo G, Calder P, Forbes A, Griffiths R, Kreyman G, Leverve X, Pichard C. ESPEN. ESPEN Guidelines on Parenteral Nutrition: intensive care. Clin Nutr. 2009;28(4):387–400. doi: 10.1016/j.clnu.2009.04.024. 10.1016/j.clnu.2009.04.024 PubMed PMID: 19505748. [DOI] [PubMed] [Google Scholar]
- 26.Sheean PM, Peterson SJ, Gomez Perez S, Troy KL, Patel A, Sclamberg JS, Ajanaku FC, Braunschweig CA. The prevalence of sarcopenia in patients with respiratory failure classified as normally nourished using computed tomography and subjective global assessment. JPEN J Parenter Enteral Nutr. 2014;38(7):873–879. doi: 10.1177/0148607113500308. 10.1177/0148607113500308 PubMed PMID: 23980135. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Lee Y, Kwon O, Shin CS, Lee SM. Use of bioelectrical impedance analysis for the assessment of nutritional status in critically ill patients. Clin Nutr Res. 2015;4(1):32–40. doi: 10.7762/cnr.2015.4.1.32. 10.7762/cnr.2015.4.1.32 PubMed PMID: 25713790, PMCID 4337921. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Plank, LD, Hill, GL, Similarity of changes in body composition in intensive care patients following severe sepsis or major blunt injury, Ann N Y Acad Sci, 2000 [DOI] [PubMed]
- 29.Malbrain ML, Huygh J, Dabrowski W, De Waele JJ, Staelens A, Wauters J. The use of bio–electrical impedance analysis (BIA) to guide fluid management, resuscitation and deresuscitation in critically ill patients: a bench–to–bedside review. Anaesthesiol Intensive Ther. 2014;46(5):381–391. doi: 10.5603/AIT.2014.0061. 10.5603/AIT.2014.0061 PubMed PMID: 25432557. [DOI] [PubMed] [Google Scholar]
- 30.Finn PJ, Plank LD, Clark MA, Connolly AB, Hill GL. Progressive cellular dehydration and proteolysis in critically ill patients. Lancet. 1996;347(9002):654–656. doi: 10.1016/s0140-6736(96)91204-0. 10.1016/S0140-6736(96)91204-0 PubMed PMID: 8596380. [DOI] [PubMed] [Google Scholar]