Handgrip strength in end stage of renal disease—a narrative review

Handgrip strength in end stage of renal disease—a narrative review Background: Handgrip strength (HS) measures have been associated with nutritional status, morbidity, and mortality in end stage of renal disease (ESRD). Objective: We aimed to present and discuss the HS method in ESRD patients, by reviewing published studies on the subject. Methods: PUBMED, MEDLINE, and LILACS databases were consulted, with no filters regarding the date of publication or age of population. Results: The terms “handgrip strength,”“end stage of renal disease,” and “nutrition status” were used, and 32 articles with publication dates from 1983 to 2017 were included. Handgrip strength is considered a simple and rapid method of assessing muscle function in chronic kidney disease and is an important predictor of nutritional status depletion, development of comorbidities, and early mortality. Conclusion: There is a lack of studies that analyzed associations between HS and clinical and nutritional outcomes in ESRD. The establishment of HS protocols and reference values in ESRD are necessary, to assist preventive measures of unfavorable outcomes in this population. Keywords: Handgrip strength, Nutrition status, End stage of renal disease Background status changes and predict risk of unfavorable clinical Nutritional and metabolic derangements are common in outcomes [4, 5]. end stage of renal disease (ESRD), caused by hypercatabolic Handgrip strength (HS) is considered a simple and status, uremic toxins, malnutrition, and inflammation. rapid method of assessing muscle function. Currently, it These changes in nutritional status are defined as protein has been used as a reliable marker of clinical prognosis energy wasting (PEW) and are strongly associated with in several populations due to its association with nutri- mortality in chronic diseases, including chronic kidney tional status, morbidity, and mortality [3, 6]. disease (CKD) [1, 2]. There are comparisons in the literature of nutritional The most common consequences of PEW are important and functional parameters, such as HS, reinforcing the decrease of serum proteins and progressive loss of skeletal importance of these indicators in clinical practice as a muscle, which contribute to development of frailty, sarco- useful nutritional assessment instrument [7]. penia, and impairment of muscle functioning, particularly Recent studies relate HS measured by a dynamo- in ESRD patients [1, 3]. meter with clinical conditions and adverse outcomes The prevalence of PEW in early stages of CKD is 20 to such as inflammation, malnutrition, overhydration sta- 25% [2] and increases with progression of the disease. tus, and higher mortality in dialytic and non-dialytic Methods assessing nutritional status and body compos- ESRD population. Because of these associations, it has ition should be able to identify important nutritional been suggested that a dynamometer is a valuable tool for assessing nutritional status in clinical practice in CKD [3, 8]. Despite the use of this, measure is increasing through * Correspondence: maricassani@gmail.com Dialysis Unit of Botucatu School of Medicine, Av. Prof. Mário Rubens the years; no major developments have been done in the Guimarães Montenegro, s/n, UNESP, Botucatu, Botucatu, SP 18618687, Brazil © 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. Oliveira et al. Nutrire (2018) 43:14 Page 2 of 8 past 6 years [6] to develop a standardized protocol to overweight and obese, according to the body mass index use HS as a tool to prevent loss of muscle mass and (BMI). Values tend to decrease with advancing age and function in ESRD population. the presence of PEW [11]. According to Schlüssel et al., there is strength variation Objective also between the sides of the body, which can vary be- This paper aimed to review the use of handgrip strength tween 5 and 30% [7]. Higher absolute values were in end stages of chronic kidney disease—stages G4 and obtained by measurements performed with standing indi- G5, pre-dialytic, and in maintenance dialysis therapy viduals [12–14]. Clinical procedure and hand’s dominance individuals, by reviewing published studies in the may influence the measurement, as described in some literature. studies [15–17], and others only observed a significant dif- ference between the right and left sides [18, 19]. Innes af- Methodology firms that shoulder flexed at 180° yields better results This is a narrative review. PUBMED database, which when compared to 90° flexion or standard position 0° [14]. contains over 26 million citations in MEDLINE biome- Verbal encouragement, as described more than 20 years dical literature; LILACS, the most important and com- ago by Johansson et al., results in 8% higher values of prehensive index of scientific literature in Latin America muscle contraction strength, statistically significant differ- and the Caribbean; scientific journals; and online books ence. In this study, a higher voice volume for transmitting has been consulted. Articles were searched by hand, instructions to men between 18 and 30 years was related using the terms “handgrip strength,”“chronic kidney to greater motivation and strength [20]. disease,” and “nutritional status.” There was no restric- Besides the use of average of several HS readings, it is tion on the basis of the language, and no filters were possible to use the measurement of only one reading, applied, as exclusion criteria, to the year of publication the largest between two or three, or the average of the or age of the study population. two largest readings between three readings. According to Innes, no significant differences were observed Results between them, being the evaluator discretion the most There were 42 articles found with the search in databases. appropriate method [14]. Thirty-one articles, published in full version, with publica- This same author suggests that a period of muscular tion between 1983 and 2017, with data about the use of HS contraction of 3 s is enough to record the greatest meas- in ESRD population, were included (Table 1). Through ure of HS. A rest period between measurements is recom- reading the articles, the discussion of this review was di- mended and may vary from 2, 5, or 15 s to 1 min [14]. vided into four subtopics: “handgrip strength”; “sarcopenia, There are differences of measures performed before frailty, and chronic kidney disease”; “handgrip strength in and after hemodialysis session: Pinto et al. showed that end stage of renal disease”;and “baseline values.” there was a significant reduction of HS observed after the session, when compared to the measure performed Discussion in initial minutes. The authors affirm that hemodialysis Handgrip strength procedure affects negatively the HS [15]. A dynamometer is a portable and practical gauging device, Considering the possible interferences exposed, it is which generates a reliable measure of muscular strength. necessary to establish a protocol in each clinic or institu- It has been applied in several populations and clinical tion and maintain the procedure consistency to ensure situations, including CKD. Reduced measures of HS are reliable measurements provided by HS [7, 9, 21] (Fig. 1). commonly found among ESRD patients and have strong Non-dialytic ESRD individuals have several factors that associations with morbidity and mortality [4, 9]. contribute to the decline of muscle strength and function, Nutritional assessment and muscle function evaluation such as anemia, decreased serum albumin and enable the diagnosis of nutritional and functional im- hemoglobin levels, presence and severity of proteinuria, pairments and, consequently, allow early interventions decreased renal function, protein hypercatabolism, ad- to avoid unfavorable outcomes, such as reduced quality vanced age, and inflammation. These factors are more of life, sarcopenia, frailty, and early death [10, 11]. strongly contributors to decline in strength of ESRD indi- Although a dynamometer is an apparatus currently viduals (CKD stages 4 and 5) than when compared to used in several clinical situations, some factors may in- those of individuals in CKD stages 2 and 3 [10]. fluence the measurement, such as age, gender, body mass, dominant hand, and the manipulator position [8]. Handgrip strength in ESRD Studies show that there is a predominance of higher Due to associations with morbidity and mortality, inves- values of muscular strength in males, in individuals aged tigation of nutritional disorders in ESRD population is between 30 and 45 years and in individuals who are extremely important [6, 11]. Reduced values of HS are Oliveira et al. Nutrire (2018) 43:14 Page 3 of 8 Table 1 Original articles used in the narrative review Study Patients Objectives Principal results Conclusions Amparo et al., 190 nondialysis-dependent It was aimed to test whether A strong negative correlation was MIS shares strong links with 2013 [3] chronic kidney MIS is able to predict muscle found between HGS and MIS in objective measures of muscle disease individuals strength in nondialysis- univariate and multivariate analysis. strength in NDD-CKD stages 2–5 dependent chronic kidney patients. disease individuals. Borges et al., 215 patients on It was aimed to evaluate if > 7 points was able to predict MIS is an independent 2017 [5] maintenance MIS is associated with mortality mortality. Using this cutoff on predictor of mortality in hemodialysis in patients on maintenance Kaplan-Meier survival curve, MIS hemodialysis patients. hemodialysis and establish a was associated with all-cause cutoff to predict mortality at mortality at 18 months and 24 different follow-up periods or more months of follow-up. Stenvinkel 206 ESRD patients, It was aimed to search The presence of cardiovascular Sex is an important factor et al., 2002 [8] classified with regard nutritional markers that can disease, diabetes mellitus, and that must be taken into to the presence of predict outcome, regarding inflammation predicted poor account in studies on cardiovascular disease, body composition in men outcome, with significant nutrition and nutritional diabetes mellitus, and and women. differences between sexes. interventions in ESRD inflammation patients. Hasheminejad 83 randomly selected It was aimed to evaluate the Protein energy wasting was Handgrip strength can be et al., 2016 [9] hemodialysis patients handgrip strength and its prevalent; handgrip strength incorporated as a reliable relationship with the was significantly associated with tool for assessing nutrition Malnutrition-Inflammation nutritional assessment markers. status in clinical practice. Score (MIS) among Iranian dialysis patients. Hiraki et al., 120 ambulant It was aimed to clarify physical All indices of physical function Physical function in pre- 2013 [10] pre-dialysis CKD function in pre-dialysis patients decreased, including handgrip dialysis CKD patients stages 2 to 5 according to CKD stage. strength, according to the decreased as the disease progression of CKD. progressed according to stage. Early intervention in CKD patients might delay the loss of physical function. Boadella et al., 56 healthy subjects It was aimed to assess with The self-selected handgrip position Both in sitting and in 2005 [12] voluntarily participated which of the maximal handgrip resulted in the highest mean standing, participants were strength could be delivered, maximal grip strength compared able to self-select the hand while sitting and while standing. with the non-self-selected grip position on the hand handgrip strength. dynamometer with which the maximal handgrip strength could be delivered. Carrero et al. 223 patients undergoing It was aimed to test if appetite Appetite loss was associated with There is a close association 2007 [13] prevalent hemodialysis would be related to worse clinical outcome even after among prevalence, inflammation and outcome in adjustment for age, sex, inflammation, malnutrition, inflammation, hemodialysis patients, and if sex dialysis vintage, and outcome in patients may account for differences in and comorbidity. undergoing prevalent the symptoms associated with hemodialysis poor appetite. Pinto et al., 156 patients on It was aimed to investigate the A significant reduction of HGS Hemodialysis procedure 2015 [15] maintenance impact of the dialysis session on was observed after the HD session, affects negatively the hemodialysis the handgrip strength in patients associated to the decrease in handgrip strength undergoing hemodialysis. blood pressure during dialysis. Crosby et al., 215 healthy subjects It was aimed to study normal 60% of patients had maximum In left-handed subjects, 1994 [16] voluntarily participated hand strength and the strengths. The majority of right- meaning grip was the same difference between dominant handed subjects were 10% stronger for both hands, the nondo and nondominant hands. in grip strength on the dominant minant hand was stronger in side. 50% of left-handed subjects. Incel et al., 128 right and 21 left It was aimed to evaluate the A statistically significant difference We concluded that the 2002 [17] hand-dominant grip and pinch strength was found between the grip and dominant hand is volunteers differences between sides for pinch strengths of dominant and significantly stronger in the right- and left-handed nondominant hands in favor of the right-handed subjects but no population. dominant hand. such significant difference between sides could be documented for left-handed people. Hanten et al., 1182 healthy subjects It was aimed to develop 1999 [18] voluntarily participated normative maximum grip Oliveira et al. Nutrire (2018) 43:14 Page 4 of 8 Table 1 Original articles used in the narrative review (Continued) Study Patients Objectives Principal results Conclusions strength data for men and Significant differences between the The results will help clinicians women aged 20 to 64 years right and left hands and across the with decision making age groups for both genders. regarding grip strength. Johansson 19 healthy volunteer It was aimed to investigate With the volume increase, it was an Through an awareness and et al., 1983 male subjects the hypothesized correlation increase of 8% in muscle contraction use of the effects of voice [19] between volume of a verbal strength. volume on muscular command and magnitude of contraction, the therapist a resulting voluntary isometric may be able to improve the muscular contraction accuracy and consistency of examination methods and increase the efficacy and efficiency of therapeutic procedures. Chang et al., 128 clinically stable It was aimed to study whether Lower handgrip strength was Handgrip strength is an 2011 [20] patients with CKD-ND PEW is associated with poor associated to significantly poor independent predictor of renal outcomes and whether renal outcomes. composite renal outcomes in the indicators of protein energy CKD-ND patients and can be wasting can predict renal incorporated to clinical outcomes in patients with practice. non-dialysis-dependent chronic kidney disease Vogt et al., 256 patients on It was aimed to verify if handgrip When adjusted for demographic, Handgrip strength was 2016 [21] maintenance hemodialysis strength is associated with all- clinical and nutritional variables, associated with mortality and peritoneal dialysis cause mortality in patients in handgrip strength remained a independent of dialysis maintenance hemodialysis and significant predictor of mortality, modality. peritoneal dialysis independent of dialysis modality Cigarrán et al., 267 men with CKD It was aimed to test if reduced Testosterone significantly and The reduction in testosterone 2013 [22] stages 2–4 endogenous testosterone independently contributed to levels that accompanies CKD associates with features of explain the variances of handgrip may further contribute to the muscle wasting in men strength and fat-free mass procatabolic environment with CKD. leading to muscle wasting. Isoyama et al., 330 incident dialysis It was aimed to address Old age, comorbidities, protein- Low muscle strength was 2014 [23] patients phenotype and mortality energy wasting, physical inactivity, more strongly associated associations of muscle strength low albumin, and inflammation with aging, protein-energy and muscle mass dysfunction associated with low muscle strength, wasting, physical inactivity, entities, alone or in combination but not with low muscle mass. When inflammation, and mortality combined, individuals with low than low muscle mass. muscle mass alone were not at increased risk of mortality. Broers et al., 44 CKD-5 non-dialysis It was aimed to compare Physical activity and handgrip Transition phase from CKD-5 2017 [24] patients, 29 dialysis physical activity and strength were significantly lower in non-dialysis to dialysis is patients, and 20 healthy performance between stage CKD-5 patients as compared to that associated only with a controls 5 chronic kidney disease and in healthy controls. 6 months after modest improvement in healthy individuals and to assess starting dialysis, activity-related activity-related energy alterations during the transition energy expenditure and walking expenditure. from CKD-5 non-dialysis to speed significantly increased. dialysis. Zhou et al., 148 adult patients with It was aimed to investigate the Lean mass, fat mass, appendicular Two important markers of 2018 [26] an estimated GFR relationships between muscle skeletal muscle, and appendicular physical function, balance < 30 mL/min/1.72 m mass and measured glomerular skeletal muscle index were associated and strength, were filtration rate and between with glomerular filtration rate. significantly related to muscle mass and strength and Handgrip strength was associated muscle mass. balance in patients with CKD with arm lean mass. Men had more stages 3–5. sarcopenia than women. Kalantar- 83 outpatients on It was aimed to develop and Malnutrition-Inflammation Score This instrument appears to Zadeh et al., maintenance validate such an instrument to had stronger and pertinent be a comprehensive scoring 2001 [27] hemodialysis therapy predict outcome in maintenance correlation coefficients system with significant for at least 3 months hemodialysis patients. associations with prospective hospitalization and mortality, as well as measures of nutrition, inflammation, and anemia in maintenance hemodialysis patients. Oliveira et al. Nutrire (2018) 43:14 Page 5 of 8 Table 1 Original articles used in the narrative review (Continued) Study Patients Objectives Principal results Conclusions Pereira et al., 287 non-dialysis-dependent It was aimed to investigate Frequency of sarcopenia was Prevalence of sarcopenia in 2015 [28] CKD patients in the prevalence and mortality significantly higher among CKD patients on conservative stages 3–5 predictive power of sarcopenia, non-survivors. Sarcopenia diagnosed therapy varies according to defined by three different by bioelectrical impedance remained the method applied. methods, in non-dialysis- as a predictor of mortality after Sarcopenia defined as dependent CKD patients. multivariate adjustment. reduced handgrip strength and low skeletal muscle mass index estimated by BIA was an independent predictor of mortality in these patients. Heimburguer 15 patients, aged It was aimed to assess the Malnourished patients differed in High prevalence of et al., 2000 younger than 70 years prevalence of malnutrition and several aspects from well-nourished malnutrition in predialysis [30] close to the start of study the relationship between patients. Including handgrip strength patients with chronic renal dialysis therapy various nutritional parameters in measure. failure and suggests that these patients handgrip strength is a reliable, inexpensive, and easy-to-perform nutritional parameter in this population. often found in patients undergoing dialysis therapy and were found. Higher survival in these populations was reflect muscle mass depletion [9]. related to values of HS above the average obtained [6]. A recent systematic review of 18 studies in popula- Vogt et al. established cutoffs of HS to identify all- tions submitted to hemodialysis and peritoneal dialysis cause mortality risk in dialysis patients, most of them on has described associations of reduced HS with dialysis hemodialysis, in different genders. The authors showed and clinical and nutritional parameters. Associations that PEW has been independently associated with poor with reduced levels of serum hemoglobin, presence of outcomes, such as longer hospitalization and mortality. diabetes mellitus, decreased renal function, inflamma- Moreover, HS cutoffs that predicted mortality were tion, carnitine deficiency, and varying degrees of PEW higher for men (22.5 kg) than for women (7.0 kg) [22]. Levels of testosterone in uremia are additional factors that contribute to decline of muscle mass and strength in men with CKD [23]. Low muscle strength is associ- ated with aging, PEW, and physical inactivity, according to Isoyama et al. [24]. End stages of renal disease indi- viduals have, commonly, high levels of physical inactivity that contribute to decrease functional capacity and decreased HS values [25]. The data analyzed suggests that a dynamometer can be considered a useful tool in evaluation of muscle function related to the nutritional status of dialysis patients [6]. There are, to date, few studies that discuss associations of HS measurement and clinical outcomes in patients with non-dialytic ESRD. Five observational, transverse, and longitudinal studies were found in the literature, which described associations between dynamometry and the occurrence, prevalence, and predictive power of sarcopenia mortality, and a litera- ture review that addressed aspects of combating severe mass loss and muscle strength in uremic non-dialytic ESRD individuals [6, 10, 21, 26, 27]. Of the most relevant nephro-protective clinical stra- tegies in ESRD, we highlight the nutritional and body compartment evaluation. Depleted nutritional status and decrease in muscle mass contribute to an accelerated loss of renal function and an increased risk of early Fig. 1 The dynamometer measures characteristics death in pre-dialytic ESRD patients [21]. Oliveira et al. Nutrire (2018) 43:14 Page 6 of 8 A study performed by Amparo et al. observed associa- 31]. Diagnostic methods and interventions can improve tions of HS measurement in CKD stages 2 to 5 patients quality of life, minimize functional disabilities, and reduce with some parameters: lower HS were older, lower renal unfavorable clinical outcomes [31]. function and lower serum albumin, and worse evaluation Although it is not considered a unique method of by the Malnutrition-Inflammation Score [3]. Malnutrition- diagnosis of sarcopenia by International Society of Renal Inflammation Score (MIS) is a nutritional assessment tool Nutrition and Metabolism, researchers have used the HS capable to predict negative clinical outcomes, proposed by in patients submitted to dialysis therapy to aid in their Kalantar-Zadeh et al. in 2001 [28]. diagnosis and treatment [6]. Hiraki et al. investigated physical functionality of non- A recent study estimated the prevalence of 6 to 10% of dialytic patients according to CKD stage. Some parame- sarcopenic stages 3 and 5 CKD patients aged 18 to ters of physical evaluation were used, among them, the 80 years old. Diagnostic criteria used in this study were dynamometer. All parameters showed worse results with HS measurements by the dynamometer (< 30th percent- disease progression, being more significant in period ile of a population-based reference) and other anthropo- before dialysis therapy initiation [10]. metric assessments [29]. Zhou et al. showed that two important markers of In a systematic review, Leal et al. showed that HS is physical functionality, balance, and strength tests were widely used as a method of diagnostic criteria of sarco- significantly related to muscle mass and glomerular penia, and its results are similar to general population: filtration rate decline, demonstrating the development HS values are associated with age and gender, capable to risk of sarcopenia during CKD evolution [26]. predict clinical complications. However, the authors A recent review discusses strategic hypotheses of mass highlighted that it is necessary to standardize the tech- loss attenuation and decreased muscular function related to niques used for HS, the position of measurement, and age and uremic state. Authors affirm that after establishing reference values for this population [6]. strategies to increase muscle mass, such as adequate nutri- tional support, metabolic acidosis correction, and resistance Reference values exercises, other strategies can be considered, such as testos- Although dynamometry is currently used in several clinical terone and growth hormone replacement, stimulation of situations and is capable of assisting clinical interventions, mitochondrial biogenesis, and stem cells [8]. one of the major obstacles to its use is the lack of cutoff points, both in healthy population and in populations with comorbidities, including ESRD [6]. Sarcopenia and frailty in CKD The proposal to define cutoff points or reference The term “sarcopenia” has recently been redefined as a values of HS in different populations is important for syndrome of progressive decline in age-related mass and real and reliable comparisons between obtained and muscle function and associated with an increased risk of normative values [3, 7]. Calibration protocols must be frailty, physical disability, and mortality risk [4, 29]. followed to maintain the measurement consistency. Sarcopenia is associated to functional impairment Few studies have developed cutoff points for HS, but and worsening quality of life, especially in ESRD, in- they have portrayed its importance in classifying muscle fluenced by aging, sedentary lifestyle, low vitamin D mass and function loss degrees, predicting unfavorable levels, high circulating potassium levels, arterial outcomes and designing interventions that may improve hypertension, insulin resistance, deficient macronutri- muscle function [3, 7, 9, 21]. ents, and low socioeconomic level, as demonstrated Pereira et al., in 2015, evaluated sarcopenia prevalence by the NHANES III study [30]. in 287 individuals with stages 3 to 5 CKD, according to Definition of sarcopenia in this population depends on HS measurements and others parameters of muscle the method applied. When defined by reduced values of mass reduction. In this study, in absence of reference HS and skeletal muscle mass, evaluated by electric values for non-dialytic ESRD population, reference bioimpedance test, Pereira et al. found a higher predict- values of a population study were considered [7, 29]. ive power of mortality in this population [29]. The establishment of measurement protocols that en- Frailty is defined as a physiological state of greatest vul- sure the definition of cutoff points for ESRD individuals nerability to stress present in the elderly, characterized by a is necessary to better evaluate muscle function and significant deterioration in cognitive, functional, and health reduce unfavorable clinical event occurrence. status. It was initially described in geriatric population, but currently, there is a high prevalence in young and old CKD individuals, reaching from 26 to 68% in ESRD [31]. Conclusions Sarcopenia and frailty have been associated to increased Handgrip strength is one of the most widely used muscle risk of hospitalizations, falls, and mortality in CKD [11, functional evaluation methods currently available and Oliveira et al. Nutrire (2018) 43:14 Page 7 of 8 has been considered a practical and reliable measure of handgrip strength in nondialysis-dependent CKD patients. J Ren Nutr. 2013;23(N 4):283–7. skeletal muscle function in the general population and 4. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European also in ESRD patients. consensus on definition and diagnosis: report of the European Working The early nutritional and muscle function diagnosis, Group on sarcopenia in older people. Age Ageing. 2010;39:412–23. 5. Borges MCC, Vogt BP, Martin LC, Caramori JCT. Malnutrition Inflammation obtained by the nutritional and muscle strength assess- score CUT-off predicting mortality in maintenance hemodialysis patients. ment, is important to avoid unfavorable consequences Clin Nutr ESPEN. 2017;17:63-67. such as reduced quality of life, PEW, and early death. 6. Leal OV, Mafra D, Fouque D, Anjos LA. Use of handgrip strength in the assessment of the muscle function of chronic kidney disease patients on In this review, we presented studies that dealt with dialysis: a systematic review. Nephrol Dial Transplant. 2011;26:1354–60. occurrence, prevalence, and predictive power of poor clin- 7. Schlüssel MM, Anjos LA, Kac G. A Dinamometria atual e seu uso na ical outcomes, mortality, and aspects to combat the marked avaliação nutricional. Rev Nutr, Campinas. 2008;21(2):223–35. 8. Stenvinkel P, Barany P, Chung SH, et al. A comparative analysis of nutritional loss of muscle mass and strength in uremic individuals. parameters as predictor of outcome in male and female ESRD patients. Thesetopicsare importantand maybasegreater studies. Nephrol Dial Transplant. 2002;17:1266–74. The measure of HS are influenced by age, gender, body 9. Hasheminejad N, Namdari M, Mahmoodi MR, Bahrampour A, Jalal Azmandian J. Association of Handgrip Strength With Malnutrition- mass, presence of sarcopenia and uremia, the stage of Inflammation Score as an Assessment of Nutritional Status in Hemodialysis CKD, hand’s dominance, body position, verbal encour- Patients. Iran J Kidney Dis. 2016;10(1):30-5. agement, and dialysis procedure. It can be considered to 10. Hiraki K, Yasuda T, Hotta C, Izawa KP, Morio Y, Watanabe S, Sakurada T, Shigagaki Y, Kimura K. Decreased physical function in pre-dialysis patients clinical and research practice the average of three HS with chronic kidney disease. Clin Exp Nephrol. 2013;17:225–31. readings, or the average of two higher readings, between 11. Souza VA, Oliveira D, Mansur HN, Fernandes NMS, Bastos MG. Sarcopenia na three readings, or the higher reading, between readings. Doença Renal Crônica. J Bras Nefrol. 2015;37(1):98–105. 12. Boadella JM, Kuijer PP, Sluiter JK, Frings-Dresen MH. Effect of self-selected Further studies are needed to standardize the techniques handgrip position on maximal handgrip strength. Arch Phys Med Rehab. used for HS, establishment protocols, and reference values 2005;86(2):328–31. to assist preventive measures of unfavorable outcomes in 13. Carrero JJ, Qureshi AR, Axelsson J, et al. Comparison of nutritional and inflammatory markers in dialysis patients with reduced appetite. Am J Clin ESRD population. Nutr. 2007;85:695–701. 14. Innes E. Handgrip strength testing: a review of literature. Aust Occup Ther J. Abbreviations 1999;46(3):120–40. 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Johansson CA, Kent BE, Shepard KF. Relationship between verbal command interpretation of data, and drafting the article. MNBB and ALB contributed to volume and magnitude of muscle contraction. Phys Ther. 1983;63(8):1260–5. the conception and design of the study, in drafting the article, revising it 20. Chang YT, Wu HL, Guo HR, Cheng YY, Tseng CC, Wang MC, Lin MC, Sung JM. critically for important intellectual content, and final approval of the version. Handgrip strength is an independent predictor of renal outcomes in patients All authors read and approved the final version of the manuscript. with chronic kidney diseases. Nephrol Dial Transplant. 2011;26:3588–95. 21. Vogt BP, Borges MCC, Góes CR, Caramori JCT. Handgrip strenght is an Ethics approval and consent to participate independent predictor of allcause mortality in maintenance dialysis patients. Not applicable. Clin Nutr. 2016;35(6):1429-1433. 22. Cigarrán S, Pousa M, Castro MJ, González B, Martínez A, Barril G, Aguilera A, Competing interests Coronel F, Stenvinkel P, Carrero JJ. Endogenous testosterone, muscle strength, and The authors declare that they have no competing interests. fat-free mass in men with chronic kidney disease. J Ren Nutr. 2013;23(5):e89–95. 23. Isoyama N, Qureshi AR, Avesani CA, Lindholm B, Bàràny P, Heimbürger O, Cederholm T, Peter Stenvinkel P, Juan Jesús Carrero JJ. Comparative Publisher’sNote associations of muscle mass and muscle strength with mortality in dialysis Springer Nature remains neutral with regard to jurisdictional claims in patients. Clin J Am Soc Nephrol. 2014;9:1720–8. published maps and institutional affiliations. 24. Broers NJH, Martens RJH, Cornelis T, van der Sande FM, Diederen NMP, Hermans MMH, et al. Physical activity in end-stage renal disease patients: Received: 9 November 2017 Accepted: 29 April 2018 the effects of starting dialysis in the first 6 months after transition period. 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Handgrip strength in end stage of renal disease—a narrative review

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Abstract

Background: Handgrip strength (HS) measures have been associated with nutritional status, morbidity, and mortality in end stage of renal disease (ESRD). Objective: We aimed to present and discuss the HS method in ESRD patients, by reviewing published studies on the subject. Methods: PUBMED, MEDLINE, and LILACS databases were consulted, with no filters regarding the date of publication or age of population. Results: The terms “handgrip strength,”“end stage of renal disease,” and “nutrition status” were used, and 32 articles with publication dates from 1983 to 2017 were included. Handgrip strength is considered a simple and rapid method of assessing muscle function in chronic kidney disease and is an important predictor of nutritional status depletion, development of comorbidities, and early mortality. Conclusion: There is a lack of studies that analyzed associations between HS and clinical and nutritional outcomes in ESRD. The establishment of HS protocols and reference values in ESRD are necessary, to assist preventive measures of unfavorable outcomes in this population. Keywords: Handgrip strength, Nutrition status, End stage of renal disease Background status changes and predict risk of unfavorable clinical Nutritional and metabolic derangements are common in outcomes [4, 5]. end stage of renal disease (ESRD), caused by hypercatabolic Handgrip strength (HS) is considered a simple and status, uremic toxins, malnutrition, and inflammation. rapid method of assessing muscle function. Currently, it These changes in nutritional status are defined as protein has been used as a reliable marker of clinical prognosis energy wasting (PEW) and are strongly associated with in several populations due to its association with nutri- mortality in chronic diseases, including chronic kidney tional status, morbidity, and mortality [3, 6]. disease (CKD) [1, 2]. There are comparisons in the literature of nutritional The most common consequences of PEW are important and functional parameters, such as HS, reinforcing the decrease of serum proteins and progressive loss of skeletal importance of these indicators in clinical practice as a muscle, which contribute to development of frailty, sarco- useful nutritional assessment instrument [7]. penia, and impairment of muscle functioning, particularly Recent studies relate HS measured by a dynamo- in ESRD patients [1, 3]. meter with clinical conditions and adverse outcomes The prevalence of PEW in early stages of CKD is 20 to such as inflammation, malnutrition, overhydration sta- 25% [2] and increases with progression of the disease. tus, and higher mortality in dialytic and non-dialytic Methods assessing nutritional status and body compos- ESRD population. Because of these associations, it has ition should be able to identify important nutritional been suggested that a dynamometer is a valuable tool for assessing nutritional status in clinical practice in CKD [3, 8]. Despite the use of this, measure is increasing through * Correspondence: maricassani@gmail.com Dialysis Unit of Botucatu School of Medicine, Av. Prof. Mário Rubens the years; no major developments have been done in the Guimarães Montenegro, s/n, UNESP, Botucatu, Botucatu, SP 18618687, Brazil © 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. Oliveira et al. Nutrire (2018) 43:14 Page 2 of 8 past 6 years [6] to develop a standardized protocol to overweight and obese, according to the body mass index use HS as a tool to prevent loss of muscle mass and (BMI). Values tend to decrease with advancing age and function in ESRD population. the presence of PEW [11]. According to Schlüssel et al., there is strength variation Objective also between the sides of the body, which can vary be- This paper aimed to review the use of handgrip strength tween 5 and 30% [7]. Higher absolute values were in end stages of chronic kidney disease—stages G4 and obtained by measurements performed with standing indi- G5, pre-dialytic, and in maintenance dialysis therapy viduals [12–14]. Clinical procedure and hand’s dominance individuals, by reviewing published studies in the may influence the measurement, as described in some literature. studies [15–17], and others only observed a significant dif- ference between the right and left sides [18, 19]. Innes af- Methodology firms that shoulder flexed at 180° yields better results This is a narrative review. PUBMED database, which when compared to 90° flexion or standard position 0° [14]. contains over 26 million citations in MEDLINE biome- Verbal encouragement, as described more than 20 years dical literature; LILACS, the most important and com- ago by Johansson et al., results in 8% higher values of prehensive index of scientific literature in Latin America muscle contraction strength, statistically significant differ- and the Caribbean; scientific journals; and online books ence. In this study, a higher voice volume for transmitting has been consulted. Articles were searched by hand, instructions to men between 18 and 30 years was related using the terms “handgrip strength,”“chronic kidney to greater motivation and strength [20]. disease,” and “nutritional status.” There was no restric- Besides the use of average of several HS readings, it is tion on the basis of the language, and no filters were possible to use the measurement of only one reading, applied, as exclusion criteria, to the year of publication the largest between two or three, or the average of the or age of the study population. two largest readings between three readings. According to Innes, no significant differences were observed Results between them, being the evaluator discretion the most There were 42 articles found with the search in databases. appropriate method [14]. Thirty-one articles, published in full version, with publica- This same author suggests that a period of muscular tion between 1983 and 2017, with data about the use of HS contraction of 3 s is enough to record the greatest meas- in ESRD population, were included (Table 1). Through ure of HS. A rest period between measurements is recom- reading the articles, the discussion of this review was di- mended and may vary from 2, 5, or 15 s to 1 min [14]. vided into four subtopics: “handgrip strength”; “sarcopenia, There are differences of measures performed before frailty, and chronic kidney disease”; “handgrip strength in and after hemodialysis session: Pinto et al. showed that end stage of renal disease”;and “baseline values.” there was a significant reduction of HS observed after the session, when compared to the measure performed Discussion in initial minutes. The authors affirm that hemodialysis Handgrip strength procedure affects negatively the HS [15]. A dynamometer is a portable and practical gauging device, Considering the possible interferences exposed, it is which generates a reliable measure of muscular strength. necessary to establish a protocol in each clinic or institu- It has been applied in several populations and clinical tion and maintain the procedure consistency to ensure situations, including CKD. Reduced measures of HS are reliable measurements provided by HS [7, 9, 21] (Fig. 1). commonly found among ESRD patients and have strong Non-dialytic ESRD individuals have several factors that associations with morbidity and mortality [4, 9]. contribute to the decline of muscle strength and function, Nutritional assessment and muscle function evaluation such as anemia, decreased serum albumin and enable the diagnosis of nutritional and functional im- hemoglobin levels, presence and severity of proteinuria, pairments and, consequently, allow early interventions decreased renal function, protein hypercatabolism, ad- to avoid unfavorable outcomes, such as reduced quality vanced age, and inflammation. These factors are more of life, sarcopenia, frailty, and early death [10, 11]. strongly contributors to decline in strength of ESRD indi- Although a dynamometer is an apparatus currently viduals (CKD stages 4 and 5) than when compared to used in several clinical situations, some factors may in- those of individuals in CKD stages 2 and 3 [10]. fluence the measurement, such as age, gender, body mass, dominant hand, and the manipulator position [8]. Handgrip strength in ESRD Studies show that there is a predominance of higher Due to associations with morbidity and mortality, inves- values of muscular strength in males, in individuals aged tigation of nutritional disorders in ESRD population is between 30 and 45 years and in individuals who are extremely important [6, 11]. Reduced values of HS are Oliveira et al. Nutrire (2018) 43:14 Page 3 of 8 Table 1 Original articles used in the narrative review Study Patients Objectives Principal results Conclusions Amparo et al., 190 nondialysis-dependent It was aimed to test whether A strong negative correlation was MIS shares strong links with 2013 [3] chronic kidney MIS is able to predict muscle found between HGS and MIS in objective measures of muscle disease individuals strength in nondialysis- univariate and multivariate analysis. strength in NDD-CKD stages 2–5 dependent chronic kidney patients. disease individuals. Borges et al., 215 patients on It was aimed to evaluate if > 7 points was able to predict MIS is an independent 2017 [5] maintenance MIS is associated with mortality mortality. Using this cutoff on predictor of mortality in hemodialysis in patients on maintenance Kaplan-Meier survival curve, MIS hemodialysis patients. hemodialysis and establish a was associated with all-cause cutoff to predict mortality at mortality at 18 months and 24 different follow-up periods or more months of follow-up. Stenvinkel 206 ESRD patients, It was aimed to search The presence of cardiovascular Sex is an important factor et al., 2002 [8] classified with regard nutritional markers that can disease, diabetes mellitus, and that must be taken into to the presence of predict outcome, regarding inflammation predicted poor account in studies on cardiovascular disease, body composition in men outcome, with significant nutrition and nutritional diabetes mellitus, and and women. differences between sexes. interventions in ESRD inflammation patients. Hasheminejad 83 randomly selected It was aimed to evaluate the Protein energy wasting was Handgrip strength can be et al., 2016 [9] hemodialysis patients handgrip strength and its prevalent; handgrip strength incorporated as a reliable relationship with the was significantly associated with tool for assessing nutrition Malnutrition-Inflammation nutritional assessment markers. status in clinical practice. Score (MIS) among Iranian dialysis patients. Hiraki et al., 120 ambulant It was aimed to clarify physical All indices of physical function Physical function in pre- 2013 [10] pre-dialysis CKD function in pre-dialysis patients decreased, including handgrip dialysis CKD patients stages 2 to 5 according to CKD stage. strength, according to the decreased as the disease progression of CKD. progressed according to stage. Early intervention in CKD patients might delay the loss of physical function. Boadella et al., 56 healthy subjects It was aimed to assess with The self-selected handgrip position Both in sitting and in 2005 [12] voluntarily participated which of the maximal handgrip resulted in the highest mean standing, participants were strength could be delivered, maximal grip strength compared able to self-select the hand while sitting and while standing. with the non-self-selected grip position on the hand handgrip strength. dynamometer with which the maximal handgrip strength could be delivered. Carrero et al. 223 patients undergoing It was aimed to test if appetite Appetite loss was associated with There is a close association 2007 [13] prevalent hemodialysis would be related to worse clinical outcome even after among prevalence, inflammation and outcome in adjustment for age, sex, inflammation, malnutrition, inflammation, hemodialysis patients, and if sex dialysis vintage, and outcome in patients may account for differences in and comorbidity. undergoing prevalent the symptoms associated with hemodialysis poor appetite. Pinto et al., 156 patients on It was aimed to investigate the A significant reduction of HGS Hemodialysis procedure 2015 [15] maintenance impact of the dialysis session on was observed after the HD session, affects negatively the hemodialysis the handgrip strength in patients associated to the decrease in handgrip strength undergoing hemodialysis. blood pressure during dialysis. Crosby et al., 215 healthy subjects It was aimed to study normal 60% of patients had maximum In left-handed subjects, 1994 [16] voluntarily participated hand strength and the strengths. The majority of right- meaning grip was the same difference between dominant handed subjects were 10% stronger for both hands, the nondo and nondominant hands. in grip strength on the dominant minant hand was stronger in side. 50% of left-handed subjects. Incel et al., 128 right and 21 left It was aimed to evaluate the A statistically significant difference We concluded that the 2002 [17] hand-dominant grip and pinch strength was found between the grip and dominant hand is volunteers differences between sides for pinch strengths of dominant and significantly stronger in the right- and left-handed nondominant hands in favor of the right-handed subjects but no population. dominant hand. such significant difference between sides could be documented for left-handed people. Hanten et al., 1182 healthy subjects It was aimed to develop 1999 [18] voluntarily participated normative maximum grip Oliveira et al. Nutrire (2018) 43:14 Page 4 of 8 Table 1 Original articles used in the narrative review (Continued) Study Patients Objectives Principal results Conclusions strength data for men and Significant differences between the The results will help clinicians women aged 20 to 64 years right and left hands and across the with decision making age groups for both genders. regarding grip strength. Johansson 19 healthy volunteer It was aimed to investigate With the volume increase, it was an Through an awareness and et al., 1983 male subjects the hypothesized correlation increase of 8% in muscle contraction use of the effects of voice [19] between volume of a verbal strength. volume on muscular command and magnitude of contraction, the therapist a resulting voluntary isometric may be able to improve the muscular contraction accuracy and consistency of examination methods and increase the efficacy and efficiency of therapeutic procedures. Chang et al., 128 clinically stable It was aimed to study whether Lower handgrip strength was Handgrip strength is an 2011 [20] patients with CKD-ND PEW is associated with poor associated to significantly poor independent predictor of renal outcomes and whether renal outcomes. composite renal outcomes in the indicators of protein energy CKD-ND patients and can be wasting can predict renal incorporated to clinical outcomes in patients with practice. non-dialysis-dependent chronic kidney disease Vogt et al., 256 patients on It was aimed to verify if handgrip When adjusted for demographic, Handgrip strength was 2016 [21] maintenance hemodialysis strength is associated with all- clinical and nutritional variables, associated with mortality and peritoneal dialysis cause mortality in patients in handgrip strength remained a independent of dialysis maintenance hemodialysis and significant predictor of mortality, modality. peritoneal dialysis independent of dialysis modality Cigarrán et al., 267 men with CKD It was aimed to test if reduced Testosterone significantly and The reduction in testosterone 2013 [22] stages 2–4 endogenous testosterone independently contributed to levels that accompanies CKD associates with features of explain the variances of handgrip may further contribute to the muscle wasting in men strength and fat-free mass procatabolic environment with CKD. leading to muscle wasting. Isoyama et al., 330 incident dialysis It was aimed to address Old age, comorbidities, protein- Low muscle strength was 2014 [23] patients phenotype and mortality energy wasting, physical inactivity, more strongly associated associations of muscle strength low albumin, and inflammation with aging, protein-energy and muscle mass dysfunction associated with low muscle strength, wasting, physical inactivity, entities, alone or in combination but not with low muscle mass. When inflammation, and mortality combined, individuals with low than low muscle mass. muscle mass alone were not at increased risk of mortality. Broers et al., 44 CKD-5 non-dialysis It was aimed to compare Physical activity and handgrip Transition phase from CKD-5 2017 [24] patients, 29 dialysis physical activity and strength were significantly lower in non-dialysis to dialysis is patients, and 20 healthy performance between stage CKD-5 patients as compared to that associated only with a controls 5 chronic kidney disease and in healthy controls. 6 months after modest improvement in healthy individuals and to assess starting dialysis, activity-related activity-related energy alterations during the transition energy expenditure and walking expenditure. from CKD-5 non-dialysis to speed significantly increased. dialysis. Zhou et al., 148 adult patients with It was aimed to investigate the Lean mass, fat mass, appendicular Two important markers of 2018 [26] an estimated GFR relationships between muscle skeletal muscle, and appendicular physical function, balance < 30 mL/min/1.72 m mass and measured glomerular skeletal muscle index were associated and strength, were filtration rate and between with glomerular filtration rate. significantly related to muscle mass and strength and Handgrip strength was associated muscle mass. balance in patients with CKD with arm lean mass. Men had more stages 3–5. sarcopenia than women. Kalantar- 83 outpatients on It was aimed to develop and Malnutrition-Inflammation Score This instrument appears to Zadeh et al., maintenance validate such an instrument to had stronger and pertinent be a comprehensive scoring 2001 [27] hemodialysis therapy predict outcome in maintenance correlation coefficients system with significant for at least 3 months hemodialysis patients. associations with prospective hospitalization and mortality, as well as measures of nutrition, inflammation, and anemia in maintenance hemodialysis patients. Oliveira et al. Nutrire (2018) 43:14 Page 5 of 8 Table 1 Original articles used in the narrative review (Continued) Study Patients Objectives Principal results Conclusions Pereira et al., 287 non-dialysis-dependent It was aimed to investigate Frequency of sarcopenia was Prevalence of sarcopenia in 2015 [28] CKD patients in the prevalence and mortality significantly higher among CKD patients on conservative stages 3–5 predictive power of sarcopenia, non-survivors. Sarcopenia diagnosed therapy varies according to defined by three different by bioelectrical impedance remained the method applied. methods, in non-dialysis- as a predictor of mortality after Sarcopenia defined as dependent CKD patients. multivariate adjustment. reduced handgrip strength and low skeletal muscle mass index estimated by BIA was an independent predictor of mortality in these patients. Heimburguer 15 patients, aged It was aimed to assess the Malnourished patients differed in High prevalence of et al., 2000 younger than 70 years prevalence of malnutrition and several aspects from well-nourished malnutrition in predialysis [30] close to the start of study the relationship between patients. Including handgrip strength patients with chronic renal dialysis therapy various nutritional parameters in measure. failure and suggests that these patients handgrip strength is a reliable, inexpensive, and easy-to-perform nutritional parameter in this population. often found in patients undergoing dialysis therapy and were found. Higher survival in these populations was reflect muscle mass depletion [9]. related to values of HS above the average obtained [6]. A recent systematic review of 18 studies in popula- Vogt et al. established cutoffs of HS to identify all- tions submitted to hemodialysis and peritoneal dialysis cause mortality risk in dialysis patients, most of them on has described associations of reduced HS with dialysis hemodialysis, in different genders. The authors showed and clinical and nutritional parameters. Associations that PEW has been independently associated with poor with reduced levels of serum hemoglobin, presence of outcomes, such as longer hospitalization and mortality. diabetes mellitus, decreased renal function, inflamma- Moreover, HS cutoffs that predicted mortality were tion, carnitine deficiency, and varying degrees of PEW higher for men (22.5 kg) than for women (7.0 kg) [22]. Levels of testosterone in uremia are additional factors that contribute to decline of muscle mass and strength in men with CKD [23]. Low muscle strength is associ- ated with aging, PEW, and physical inactivity, according to Isoyama et al. [24]. End stages of renal disease indi- viduals have, commonly, high levels of physical inactivity that contribute to decrease functional capacity and decreased HS values [25]. The data analyzed suggests that a dynamometer can be considered a useful tool in evaluation of muscle function related to the nutritional status of dialysis patients [6]. There are, to date, few studies that discuss associations of HS measurement and clinical outcomes in patients with non-dialytic ESRD. Five observational, transverse, and longitudinal studies were found in the literature, which described associations between dynamometry and the occurrence, prevalence, and predictive power of sarcopenia mortality, and a litera- ture review that addressed aspects of combating severe mass loss and muscle strength in uremic non-dialytic ESRD individuals [6, 10, 21, 26, 27]. Of the most relevant nephro-protective clinical stra- tegies in ESRD, we highlight the nutritional and body compartment evaluation. Depleted nutritional status and decrease in muscle mass contribute to an accelerated loss of renal function and an increased risk of early Fig. 1 The dynamometer measures characteristics death in pre-dialytic ESRD patients [21]. Oliveira et al. Nutrire (2018) 43:14 Page 6 of 8 A study performed by Amparo et al. observed associa- 31]. Diagnostic methods and interventions can improve tions of HS measurement in CKD stages 2 to 5 patients quality of life, minimize functional disabilities, and reduce with some parameters: lower HS were older, lower renal unfavorable clinical outcomes [31]. function and lower serum albumin, and worse evaluation Although it is not considered a unique method of by the Malnutrition-Inflammation Score [3]. Malnutrition- diagnosis of sarcopenia by International Society of Renal Inflammation Score (MIS) is a nutritional assessment tool Nutrition and Metabolism, researchers have used the HS capable to predict negative clinical outcomes, proposed by in patients submitted to dialysis therapy to aid in their Kalantar-Zadeh et al. in 2001 [28]. diagnosis and treatment [6]. Hiraki et al. investigated physical functionality of non- A recent study estimated the prevalence of 6 to 10% of dialytic patients according to CKD stage. Some parame- sarcopenic stages 3 and 5 CKD patients aged 18 to ters of physical evaluation were used, among them, the 80 years old. Diagnostic criteria used in this study were dynamometer. All parameters showed worse results with HS measurements by the dynamometer (< 30th percent- disease progression, being more significant in period ile of a population-based reference) and other anthropo- before dialysis therapy initiation [10]. metric assessments [29]. Zhou et al. showed that two important markers of In a systematic review, Leal et al. showed that HS is physical functionality, balance, and strength tests were widely used as a method of diagnostic criteria of sarco- significantly related to muscle mass and glomerular penia, and its results are similar to general population: filtration rate decline, demonstrating the development HS values are associated with age and gender, capable to risk of sarcopenia during CKD evolution [26]. predict clinical complications. However, the authors A recent review discusses strategic hypotheses of mass highlighted that it is necessary to standardize the tech- loss attenuation and decreased muscular function related to niques used for HS, the position of measurement, and age and uremic state. Authors affirm that after establishing reference values for this population [6]. strategies to increase muscle mass, such as adequate nutri- tional support, metabolic acidosis correction, and resistance Reference values exercises, other strategies can be considered, such as testos- Although dynamometry is currently used in several clinical terone and growth hormone replacement, stimulation of situations and is capable of assisting clinical interventions, mitochondrial biogenesis, and stem cells [8]. one of the major obstacles to its use is the lack of cutoff points, both in healthy population and in populations with comorbidities, including ESRD [6]. Sarcopenia and frailty in CKD The proposal to define cutoff points or reference The term “sarcopenia” has recently been redefined as a values of HS in different populations is important for syndrome of progressive decline in age-related mass and real and reliable comparisons between obtained and muscle function and associated with an increased risk of normative values [3, 7]. Calibration protocols must be frailty, physical disability, and mortality risk [4, 29]. followed to maintain the measurement consistency. Sarcopenia is associated to functional impairment Few studies have developed cutoff points for HS, but and worsening quality of life, especially in ESRD, in- they have portrayed its importance in classifying muscle fluenced by aging, sedentary lifestyle, low vitamin D mass and function loss degrees, predicting unfavorable levels, high circulating potassium levels, arterial outcomes and designing interventions that may improve hypertension, insulin resistance, deficient macronutri- muscle function [3, 7, 9, 21]. ents, and low socioeconomic level, as demonstrated Pereira et al., in 2015, evaluated sarcopenia prevalence by the NHANES III study [30]. in 287 individuals with stages 3 to 5 CKD, according to Definition of sarcopenia in this population depends on HS measurements and others parameters of muscle the method applied. When defined by reduced values of mass reduction. In this study, in absence of reference HS and skeletal muscle mass, evaluated by electric values for non-dialytic ESRD population, reference bioimpedance test, Pereira et al. found a higher predict- values of a population study were considered [7, 29]. ive power of mortality in this population [29]. The establishment of measurement protocols that en- Frailty is defined as a physiological state of greatest vul- sure the definition of cutoff points for ESRD individuals nerability to stress present in the elderly, characterized by a is necessary to better evaluate muscle function and significant deterioration in cognitive, functional, and health reduce unfavorable clinical event occurrence. status. It was initially described in geriatric population, but currently, there is a high prevalence in young and old CKD individuals, reaching from 26 to 68% in ESRD [31]. Conclusions Sarcopenia and frailty have been associated to increased Handgrip strength is one of the most widely used muscle risk of hospitalizations, falls, and mortality in CKD [11, functional evaluation methods currently available and Oliveira et al. Nutrire (2018) 43:14 Page 7 of 8 has been considered a practical and reliable measure of handgrip strength in nondialysis-dependent CKD patients. J Ren Nutr. 2013;23(N 4):283–7. skeletal muscle function in the general population and 4. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European also in ESRD patients. consensus on definition and diagnosis: report of the European Working The early nutritional and muscle function diagnosis, Group on sarcopenia in older people. Age Ageing. 2010;39:412–23. 5. Borges MCC, Vogt BP, Martin LC, Caramori JCT. Malnutrition Inflammation obtained by the nutritional and muscle strength assess- score CUT-off predicting mortality in maintenance hemodialysis patients. ment, is important to avoid unfavorable consequences Clin Nutr ESPEN. 2017;17:63-67. such as reduced quality of life, PEW, and early death. 6. Leal OV, Mafra D, Fouque D, Anjos LA. Use of handgrip strength in the assessment of the muscle function of chronic kidney disease patients on In this review, we presented studies that dealt with dialysis: a systematic review. Nephrol Dial Transplant. 2011;26:1354–60. occurrence, prevalence, and predictive power of poor clin- 7. Schlüssel MM, Anjos LA, Kac G. A Dinamometria atual e seu uso na ical outcomes, mortality, and aspects to combat the marked avaliação nutricional. Rev Nutr, Campinas. 2008;21(2):223–35. 8. Stenvinkel P, Barany P, Chung SH, et al. A comparative analysis of nutritional loss of muscle mass and strength in uremic individuals. parameters as predictor of outcome in male and female ESRD patients. Thesetopicsare importantand maybasegreater studies. Nephrol Dial Transplant. 2002;17:1266–74. The measure of HS are influenced by age, gender, body 9. Hasheminejad N, Namdari M, Mahmoodi MR, Bahrampour A, Jalal Azmandian J. Association of Handgrip Strength With Malnutrition- mass, presence of sarcopenia and uremia, the stage of Inflammation Score as an Assessment of Nutritional Status in Hemodialysis CKD, hand’s dominance, body position, verbal encour- Patients. Iran J Kidney Dis. 2016;10(1):30-5. agement, and dialysis procedure. It can be considered to 10. Hiraki K, Yasuda T, Hotta C, Izawa KP, Morio Y, Watanabe S, Sakurada T, Shigagaki Y, Kimura K. Decreased physical function in pre-dialysis patients clinical and research practice the average of three HS with chronic kidney disease. Clin Exp Nephrol. 2013;17:225–31. readings, or the average of two higher readings, between 11. Souza VA, Oliveira D, Mansur HN, Fernandes NMS, Bastos MG. Sarcopenia na three readings, or the higher reading, between readings. Doença Renal Crônica. J Bras Nefrol. 2015;37(1):98–105. 12. Boadella JM, Kuijer PP, Sluiter JK, Frings-Dresen MH. Effect of self-selected Further studies are needed to standardize the techniques handgrip position on maximal handgrip strength. Arch Phys Med Rehab. used for HS, establishment protocols, and reference values 2005;86(2):328–31. to assist preventive measures of unfavorable outcomes in 13. Carrero JJ, Qureshi AR, Axelsson J, et al. Comparison of nutritional and inflammatory markers in dialysis patients with reduced appetite. Am J Clin ESRD population. Nutr. 2007;85:695–701. 14. Innes E. Handgrip strength testing: a review of literature. Aust Occup Ther J. Abbreviations 1999;46(3):120–40. BMI: Body mass index; CKD: Chronic kidney disease; ESRD: End stage of renal 15. Pinto AP, Ramos CI, Meireles MS, Kamimura MA, Cuppari L. Impacto da sessão disease; HS: Handgrip strength; MIS: Malnutrition-Inflammation Score; de hemodiálise na força de preensão manual. J Bras Nefrol. 2015;37(4):00. PEW: Protein energy wasting 16. Crosby CA, Wehbé MA, Mawr B. Hand strength: normative values. J Hand Surg. 1994;19(4):665–70. Availability of data and materials 17. Incel NA, Ceceli E, Durukan PB, Erdem HR, Yorgancioglu ZR. Grip strength: The datasets used and/or analyzed during the current study are available effect of hand dominance. Singap Med J. 2002;43(5):234–7. from the corresponding author on reasonable request. 18. Hanten WP, Chen WY, Austin AA, Brooks RE, Carter HC, Law CA, et al. Maximum grip strength in normal subjects from 24 to 64 years of age. J Authors’ contributions Hand Ther. 1999;12:193–200. MCO contributed to the conception and design of the study, acquisition and 19. Johansson CA, Kent BE, Shepard KF. Relationship between verbal command interpretation of data, and drafting the article. MNBB and ALB contributed to volume and magnitude of muscle contraction. Phys Ther. 1983;63(8):1260–5. the conception and design of the study, in drafting the article, revising it 20. Chang YT, Wu HL, Guo HR, Cheng YY, Tseng CC, Wang MC, Lin MC, Sung JM. critically for important intellectual content, and final approval of the version. Handgrip strength is an independent predictor of renal outcomes in patients All authors read and approved the final version of the manuscript. with chronic kidney diseases. Nephrol Dial Transplant. 2011;26:3588–95. 21. Vogt BP, Borges MCC, Góes CR, Caramori JCT. Handgrip strenght is an Ethics approval and consent to participate independent predictor of allcause mortality in maintenance dialysis patients. Not applicable. Clin Nutr. 2016;35(6):1429-1433. 22. Cigarrán S, Pousa M, Castro MJ, González B, Martínez A, Barril G, Aguilera A, Competing interests Coronel F, Stenvinkel P, Carrero JJ. Endogenous testosterone, muscle strength, and The authors declare that they have no competing interests. fat-free mass in men with chronic kidney disease. J Ren Nutr. 2013;23(5):e89–95. 23. Isoyama N, Qureshi AR, Avesani CA, Lindholm B, Bàràny P, Heimbürger O, Cederholm T, Peter Stenvinkel P, Juan Jesús Carrero JJ. Comparative Publisher’sNote associations of muscle mass and muscle strength with mortality in dialysis Springer Nature remains neutral with regard to jurisdictional claims in patients. Clin J Am Soc Nephrol. 2014;9:1720–8. published maps and institutional affiliations. 24. Broers NJH, Martens RJH, Cornelis T, van der Sande FM, Diederen NMP, Hermans MMH, et al. Physical activity in end-stage renal disease patients: Received: 9 November 2017 Accepted: 29 April 2018 the effects of starting dialysis in the first 6 months after transition period. Nephron. 2017;137(1):47–56. 25. Stenvinkel P, Carrero JJ, Walden F, Ikizler TA, Nader GA. Muscle wasting in end- stage renal disease promulgates premature death: established, emerging and References potential novel treatment strategies. Nephrol Dial Transplant. 2015;0:1–8. 1. Fouque D, Kalantar-Zadeh K, Kopple J, et al. A proposed nomenclature and diagnostic criteria for protein-energy wasting in acute and chronic kidney 26. Zhou Y, Hellberg M Svensson P, Höglund P, Clyne N. Sarcopenia and disease. Kidney Int. 2008;73:391–8. relationships between muscle mass, measured glomerular filtration rate and 2. Kovesdy CP, Kopple JD, Kalantar-Zadeh K. Management of protein-energy physical function in patients with chronic kidney disease stages 3-5. wasting in nondialysis-dependent chronic kidney disease: reconciling low Nephrol Dial Transplant. 2018;33(2):342–348. protein intake with nutritional therapy. Am J Clin Nutr. 2013;97:1163–77. 27. Kalantar-Zadeh K, Kopple JD, Block G, Humphreys MH. A malnutrition- 3. Amparo FC, Cordeiro AC, Carrero JJ, Cuppari L, Lindholm B, Amondeo C, inflammation score is correlated with morbidity and mortality in Kamimura MA. Malnutrition-Inflammation score is associated with maintenance hemodialysis patients. Am J Kidney Dis. 2001;38:1251–63. Oliveira et al. Nutrire (2018) 43:14 Page 8 of 8 28. Pereira RA, Cordeiro AC, Avesani CM, Carrero JJ, Lindholm B, Amparo FC, Amodeo C, Cuppari L, Kamimura MA. Sarcopenia in chronic kidney disease on conservative therapy: prevalence and association with mortality. Nephrol Dial Transplant. 2015;0:1–7. 29. Foley RN, Wang C, Ishani A, Collins AJ, Murray AM. Kidney function and sarcopenia in the United States general population: NHANES III. Am J Nephrol. 2007;27:279–86. 30. Heimburguer O, Qureshi AR, Blaner WS, et al. Hand-grip muscle strength, lean body mass, and plasma proteins as markers of nutritional status in patients with chronic renal failure close to start of dialysis therapy. 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NutrireSpringer Journals

Published: Jun 5, 2018

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