Clinical Nutrition 30 (2011) 135e142 Contents lists available at ScienceDirect Clinical Nutrition journal homepage: http://www.elsevier.com/locate/clnu Review Hand grip strength: Outcome predictor and marker of nutritional status Kristina Norman a, *, Nicole Stobäus c, M. Cristina Gonzalez b, Jörg-Dieter Schulzke c, Matthias Pirlich a, d a Department of Gastroenterology, Hepatology and Endocrinology, Charité e University Medicine Berlin, Berlin, Germany Post Graduation Program in Health and Behaviour e Catholic University of Pelotas, Pelotas, Brazil c Department of General Medicine, Charité e University Medicine Berlin, Berlin, Germany d Abteilung für Innere Medizin, Evangelische Elisabeth Klinik, Berlin, Germany b a r t i c l e i n f o s u m m a r y Article history: Received 7 July 2010 Accepted 23 September 2010 Background & aims: Among all muscle function tests, measurement of hand grip strength has gained attention as a simple, non-invasive marker of muscle strength of upper extremities, well suitable for clinical use. This review outlines the prognostic relevance of grip strength in various clinical and epidemiologic settings and investigates its suitability as marker of nutritional status in cross-sectional as well as intervention studies. Methods: Studies investigating grip strength as prognostic marker or nutritional parameter in crosssectional or intervention studies were summarized. Results and conclusions: Numerous clinical and epidemiological studies have shown the predictive potential of hand grip strength regarding short and long-term mortality and morbidity. In patients, impaired grip strength is an indicator of increased postoperative complications, increased length of hospitalization, higher rehospitalisation rate and decreased physical status. In elderly in particular, loss of grip strength implies loss of independence. Epidemiological studies have moreover demonstrated that low grip strength in healthy adults predicts increased risk of functional limitations and disability in higher age as well as all-cause mortality. As muscle function reacts early to nutritional deprivation, hand grip strength has also become a popular marker of nutritional status and is increasingly being employed as outcome variable in nutritional intervention studies. Ó 2010 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved. Keywords: Hand grip strength Muscle function Disease-related malnutrition Outcome 1. Introduction Impaired muscle strength is a well-known phenomenon occurring in disease-related malnutrition. Reduced nutritional intake results in a compensatory loss of whole body protein which is preferably lost from muscle mass, the body’s largest protein reserve.3,4 Simultaneously, muscle protein synthesis can also be reduced in disease-related malnutrition. Since muscle function correlates closely with whole body protein,10,11 body cell mass,12 anthropometrically measured arm muscle mass,13 and even with body mass index (BMI),14,15 loss of weight or muscle mass invariably results in decreased muscle strength, i.e. weakness, which is reflected in deteriorating function tests as well as in prominently altered muscle morphology. Reduced muscle strength is in turn associated with loss of physical functionality and with negative impact on recovery of health after illness or surgery, which partly explains the high * Corresponding author. Medizinische Klinik und Poliklinik, Charité e Universitätsmedizin Berlin,10098 Berlin. Tel.: þ49 30 450 514139; fax: þ49 30 450 514901. E-mail address: kristina.norman@charite.de (K. Norman). predictive power of muscle function tests. Various studies have shown a close correlation between muscle strength and outcome in acute and chronic disease.16e19 2. Measurement of hand grip strength as indicator of muscle function Just as measuring body composition offers a qualitative aspect of nutritional status, muscle function represents a dynamic indicator of muscle mass. Measurement of muscle function as indicator of functional as well as nutritional status has therefore gained considerable attention in the past years. There are several methods for the measurement of voluntary and involuntary muscle function. Electrical stimulation at various frequencies but constant isometric length is used for the determination of involuntary muscle contraction.20e22 While it is considered the superior procedure in regard to objectivity, it is not suitable for clinical routine. Among the measurements of voluntary muscle strength (e.g. hand grip, knee extension or hip flexion strength), hand grip strength is a validated and most feasible bed side method, which makes it attractive and the most frequently used tool for clinical purpose. 0261-5614/$ e see front matter Ó 2010 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved. doi:10.1016/j.clnu.2010.09.010 136 K. Norman et al. / Clinical Nutrition 30 (2011) 135e142 M ALN U T R I T I O N Protein Synthesis Proteolysis fibre atrophy Glycolytic Enzyme Activities [5;7-9] muscle glycolysis ↓ reduced muscle mass R ED U CED Creatine [1;2] Mitochondrial Complex Activites [5;6] Intracellular Calcium [7;8] creatinephosphate ↓ oxidative phosphorylation ↓ impaired free energy change from ATP hydrolysis M U SCLE impaired cell energetics & impaired cell membrane potential FU N CT I O N Fig. 1. Hypotheses 1,2,5,6,9 for the pathogenesis of impaired muscle function in malnutrition. Hand grip strength reflects the maximum strength derived from combined contraction of extrinsic and intrinsic hand muscles which lead to the flexion of hand joints.23 Originally developed for hand surgery in order to determine the capacity after trauma or surgery, hand grip strength has quickly become the focus of interest in numerous studies due to its feasibility and prognostic relevance. Although hand grip strength correlates well with other muscle function tests such as knee extension strength or peak expiratory flow, it cannot be used as surrogate for muscle function of lower extremities when evaluating physical performance.24 3. Determinants of hand grip strength In healthy people, age and gender are the strongest influencing factors on hand grip strength.25 In acute or chronic disease, however, various further factors such as disease severity, co-morbidity load, medical treatment, and immobilisation contribute to a certain extent to muscle weakness and therefore to the patients’ decreased well-being. Bed rest and muscle disuse,26 inflammation, infection, endotoxemia, corticosteroids, muscle relaxants, hypoxia, electrolyte imbalances and oxidative stress all have adverse effects on muscle function.27 Moreover, nutritional status which is frequently reduced in disease invariably has a great impact on muscle strength. In benign disease, for instance, disease-related malnutrition results in decreased muscle function. Our group found 25.8% lower absolute hand grip strength values in malnourished when compared to wellnourished hospitalized patients. This difference was also seen when patients were analysed according to their body mass index, implying that loss of weight has more impact on muscle strength than body mass.12 Similarly, Vaz et al. showed that hand grip strength not merely reflected body mass but could also differentiate between undernourished and simply underweight individuals with equal BMI.28 Moreover, our recent study in cancer patients showed that when malnutrition is defined by the Subjective Global Assessment, it can be considered a strong disease-independent predictor for hand grip strength and other muscle function tests.29 4. Muscle function in obese subjects There are several reasons why muscle strength might be affected in obesity. Obese subjects have greater muscle mass which is a major determinant of muscle strength, at least in normal weight subjects. Also, a certain training effect induced by bearing and supporting the higher weight can strengthen the muscles of obese subjects. On the other hand, high body weight is associated with decreased sedentary lifestyle,30 as well as reduced physical activity and mobility. Moreover, higher weight frequently induces pain in e.g. knees and lower back which in turn has negative impact on muscle strength. Obese subjects have been shown to possess fewer type I and more type IIb muscle fibres than lean people, as fat mass correlates inversely with type I fibres and positively with type II fibres.30e32 Absolute hand grip strength is not significantly different between obese and lean subjects, although muscle function of the lower extremities and fat free mass are higher in obese people.30,33 This is probably because the weight induced training effect is seen only in the muscles of lower extremities. Rollands et al. demonstrated that apart from knee extension strength, muscle function is not significantly different between lean and obese subjects when adjusted for age, height, recreational physical activity, pain, depression and appendicular skeletal muscle mass.33 When corrected for fat free mass through allometric scaling, Hulens and coworkers even reported that obese women exhibit lower muscle strength of both upper and lower extremities when compared to lean women, which might be explained by their lower degree of activity.34 5. Changes of muscle morphology and function in malnutrition The alterations in muscle morphology found in malnutrition are well described. Muscle biopsy specimens of untreated anorectics,35e37 of children with malnutrition38 and even of morbidly obese patients after two weeks of starvation7 consistently show myopathic changes with selective type II fibre (anaerobic, glycolytic, fast twitch) atrophy. Also, Z band degeneration is found in malnutrition.7,39 These principal ultra structural changes in muscle have been suggested to reflect loss of contractile elements.37 Changes in muscle function during malnutrition, assessed by either voluntary hand grip strength or electrostimulation, are well documented.28,40e42 Lopes et al. reported both increased muscle fatigability and an altered pattern of muscle contraction and K. Norman et al. / Clinical Nutrition 30 (2011) 135e142 137 Table 1 Cut off values and outcome prediction of hand grip strength in clinical and epidemiological studies. Author N Setting/patients Outcome prediction Clinical studies Klidjian et al.18 225 Major abdominal surgery Webb et al.19 90 General surgery Guo et al.46 127 Oral and maxillofacial cancer surgery 17 205 General surgery Humphreys et al.16 Kerr et al.48 50 120 General surgery and internal medicine Elderly patients (75e101 years) Vecchiarino et al.49 213 Bohannon et al.50 153 Predominantly elderly patients (72.5 16.5 years) with community-acquired pneumonia Elderly with community-acquired pneumonia HGS <85% of standard value (derived from control group) predicted complications in 48 of the 55 patients (87%) who developed them HGS <85% standard for age and sex (derived from control group) predicted 74% of the complications Patients with HGS< 85% of control value (derived from control group) developed significantly more postoperative complications (48 vs. 18%, p < 0.05) Patients with HGS< 85% of standard developed significantly more postoperative complications (26 vs. 7%, p < 0.0001) and total as well as postoperative LOS (p < 0.001) Predictive of decline in functional status (b ¼ 0.448; p < 0.001) Predictive of LOS: 1 kg increase in grip strength was associated with a 3% increase in likelihood of discharge to usual residence (gender-adjusted hazard ratio, HR per kg increase in grip strength: 1.03 (CI 1.001e07) Grip strength 10 kg: OR of discharge to home: 4.670 (CI 2.102e10.375) OR death within 30 days of discharge: 0.370 (CI 0.149e0.992) Predictive of death and/or readmission within one year of discharge. Grip strength correctly classified 75.2% of patients relative to that outcome; OR: 0.969 (CI 0.948 0.987) Hunt et al. Epidemiological studies 6089 Rantanen et al.85 45e68-year-old men healthy at baseline 56 Rantanen et al. 6040 45e68-year-old men healthy at baseline Rantanen et al.51 567 Elderly (75-year-old) independent in ADL at baseline Rantanen et al.54 919 Moderately to severely disabled women aged 65 to 101 Sasaki et al.55 4912 Men and women 35e74 years old healthy at baseline Newman et al.53 2292 Men and women 70e79 years Gale et al.52 800 Men and women 65 years Lowest tertile of HGS: increased risk of functional limitations and disability; OR: 2.87 (CI 1.76e4.67) within 25 years Lowest tertile of HGS: increased long-term mortality within 30 years independent of BMI class: OR: 1.36 (CI 1.14e1.63) for BMI group<20; OR: 1.25 (CI 1.08e1.45 for BMI 20e24.9; OR: 1.27 (CI 1.08e1.49) for BMI25 Lowest tertile of HGS had two to three times higher ADL dependence within 25 years: OR of walking speed of 0.4 m/s or slower:2.87 (CI 1.76e4.67); OR of losing independence: 2.30 (CI 1.04e5.07) Predictive of cause-specific and total mortality within 5 year follow-up: RR of CVD mortality: 3.21 (CI 2.00e5.14) RR of respiratory mortality: 2.38 (CI 1.09e5.20) RR of other mortality: 2.59 (CI 1.59e4.20) Multivariate-adjusted RR of all causes of death except external causes for each 5-kg increment of grip strength: RR: 0.89 (CI 0.86e0.92) for men, RR: 0.87 (CI 0.83e0.92) for women Predictive of mortality within 4.9 year follow-up; unadjusted HR 1.36 (CI 1.13e1.64) in men 1.84 (CI 1.28e2.65) in women Predictive of mortality within 24 years of follow-up only in men RR of all-cause mortality: 0.81 (CI 0.70e0.95), RR of CVD mortality: 0.73 (CI 0.60e0.89), RR of cancer mortality: 0.81 (CI 0.66e0.98) HGS: hand grip strength; ADL: activities of daily living; CVD: cardiovascular disease, LOS: length of stay, CI: 95% confidence interval. relaxation after electrical stimulation of the ulnar nerve in patients with clinically apparent malnutrition. As a consequence of these abnormalities, a decreased force of contraction at higher stimulation frequencies with maintenance of force at lower frequencies was shown.21 These findings have repeatedly been confirmed by others.7,8,22 A variety of studies have described the impact of malnutrition on muscle morphology as well as the impact on muscle function however, the pathogenesis of muscle dysfunction is not yet understood in detail. Although hand grip strength in general correlates with the proportion of protein loss assessed by In-Vivo-Neutron-ActivationAnalysis (IVNAA),10,11 muscle function, interestingly, responds earlier to both nutritional deprivation and nutritional repletion than body composition parameters like muscle or body mass. Loss of muscle mass does not appear to be exclusively responsible for muscle dysfunction in malnutrition. Short term starvation in obese, healthy women e.g., resulted in significantly lower hand grip strength and altered adductor pollicis muscle function, although no measurable change in anthropometric indices occurred simultaneously.20 In one study, refeeding anorectic patients restored maximal relaxation rate and muscle fatigability within four weeks. All other muscle function parameters returned to normal within eight weeks, whereas body nitrogen increased by only 13% and total body potassium by only 32%.43 Also, 45 days of refeeding improved physical performance in anorexia nervosa patients without simultaneous normalization of fat free mass or oxygen consumption.44 Functional changes in calf muscle have also been reported to occur earlier during nutritional repletion in malnourished elderly patients than changes in muscle mass.41 Moreover, Bissonnette et al. showed that muscle weight, size and protein did not correlate with muscle function in fast and slow twitch rat muscle during under e and subsequent refeeding.45 Further factors such as electrolyte status or energy rich compounds appear to be more responsible for the early changes in muscle function during malnutrition and refeeding than changes in muscle mass. See Fig. 1 for current hypotheses on the pathogenesis of muscle dysfunction in malnutrition. 138 K. Norman et al. / Clinical Nutrition 30 (2011) 135e142 Table 2 Hand grip strength as nutritional outcome variable in clinical studies. Author N Setting Intervention Impact of nutritional intervention on grip strength Christie and Hill73 41 Malnourished IBD patients 14 day TPN Paton et al.74 36 Malnourished tuberculosis patients Oral nutritional supplements for 6 weeks Norman et al.75 80 Malnourished patients with benign gastrointestinal disease Oral nutritional supplements for 3 months Beattie et al.76 101 Malnourished surgical patients Oral nutritional supplements for 10 weeks Keele et al.86 86 Malnourished patients undergoing major abdominal surgery Oral nutritional supplements during hospital stay (phase I of the study) Ha et al.77 124 Malnourished stroke patients Individualized, nutritional support for three months Price et al.78 76 Malnourished elderly Oral nutritional supplements for 8 weeks Edington et al.79 82 Malnourished elderly Oral nutritional supplements for 8 weeks HGS increased by 15% within the first week whereas total body protein did not change during therapy but during convalescence (200 days) Greater increase in lean body mass and HGS (2.79 3.11 compared with 0.65 4.48 kg, P ¼ 0.016) in intervention patients than controls Improvement in HGS and QoL only in intervention patients, significantly correlated to Physical Function (r ¼ 0.30, p ¼ 0.009), and Role Physical (r ¼ 0.26, p ¼ 0.023) Postoperative HGS reduction in intervention patients was less marked, with significantly improved values at 10 weeks when compared with controls ( 0.82 v 1.93 kg/m2; p < 0.001) Control patients showed a significant reduction in HGS during their hospital stay (p < 0.01). In the intervention patients, grip strength dropped at study day 3, but returned to preoperative levels by discharge The intervention patients had a significantly higher increase in QoL score (P ¼ 0.009) and in HGS (difference between groups: 2.6 kg (CI 1.0e4.2); p ¼ 0.002 HGS increased more in the intervention patients (13.9%) than in the control group (7.2%) (p ¼ 0.055) HGS improved significantly in the intervention group during supplementation, and was significantly different from control group at week 8, but it decreased thereafter, and at week 24 there was no significant difference in HGS or QoL between groups HGS: hand grip strength; IBD: inflammatory bowel disease; TPN: total parenteral nutrition; QoL: Quality of life; CI: 95% confidence interval. 6. Outcome associated with impaired muscle function The predictive power of muscle function, and hand grip strength in particular, has been demonstrated in numerous clinical as well as epidemiological studies (see Table 1). In disease, reduced muscle function has severe consequences for functional status, recovery from disease and clinical outcome, particularly as several further factors may also interact. Reduced hand grip strength was early shown to be strongly correlated with postoperative complications18,19,46 and has also been reported to be both predictive of length of hospital stay47,48 and loss of functional status16,48 as well as short term survival49 in hospitalized patients. Even death within one year of hospitalization was correlated with hand grip strength in a study of elderly patients admitted for pneumonia. In these patients, hand grip strength was a more powerful predictor than pneumonia severity, age or number of comorbidities.50 Regarding long-term outcome, hand grip strength has been shown to predict onset of dependency in the activities of daily living (ADL) within the subsequent five years in elderly and even old age disability in at baseline healthy middle aged men. This suggests that higher strength might provide greater physiologic and functional reserve that protects against mortality and morbidity.51 Hand grip or quadriceps strength but not muscle mass or parameters of body composition is moreover related to all-cause mortality in middle aged and elderly subjects.50,52e55 In healthy middle aged men, baseline hand grip strength has even shown to be associated with mortality risk in the subsequent 30 years.56 In the elderly in particular, hand grip strength has been demonstrated to be a superior outcome predictor both in healthy and sick individuals. A systematic review from 2008 demonstrated that low grip strength was consistently associated with greater probability of premature mortality, earlier onset of disability, and increased risk of complications or prolonged length of stay after hospitalization or surgery.47 7. Hand grip strength as predictor of bone mass There is a known site specific effect between muscle mass and strength and bone mineral density (BMD) as the torque placed on bone by muscle contraction strengthens the bone.57,58 This is clinically relevant in the case of knee extension strength and total hip BMD e.g. since muscle weakness is a possible contributing risk factor for falls59,60 and low BMD a clinical predictor for increased risk of fracture in falls. Similarly, hand grip strength functions as indicator of hand BMD in adults,61e67 but also to some extent as predictor of BMD at distant skeletal sites in adolescents,68 as well as postmenopausal women in particular.61,69 A large population based study in 1380 women over the age of 50 demonstrated a clear association between low grip strength and impaired spine and hip BMD as well increased risk of vertebral fracture.70 Maintenance of muscle strength is also associated with lower loss of bone mass during the perimenopausal period and is also suggested to maybe even counteract weight loss related postmenopausal bone loss71 as results from 10-year prospective follow-up studies in 971 and 587 women respectively have shown. Hand grip strength even predicts 15-year fracture free survival in perimenopausal women with normal BMD at baseline, while DEXA measurements performed in 5 year intervals did not.72 K. Norman et al. / Clinical Nutrition 30 (2011) 135e142 139 Fig. 2. Reference values generated in healthy populations. A: men (dominant or right hand). B: men (non-dominant or left hand) C: women (dominant or right hand) D: women (non-dominant or left hand) References 1: Schlüssel et al., 2008. 2: Budziareck et al., 2008. 3: Massy-Westropp et al., 2004. 4: Günther et al., 2008. 5: Goldhahn et al., 2008. 6: Crosby et al., 1994. 140 K. Norman et al. / Clinical Nutrition 30 (2011) 135e142 8. Hand grip strength as nutritional outcome variable Since muscle function reacts earlier to nutritional deprivation as well as restoration than muscle mass, as described above, it is obviously very tempting to employ hand grip strength as target variable for detecting and monitoring changes in nutritional status (see Table 2). Christie and coworkers demonstrated rapid improvement of various muscle function tests including voluntary hand grip strength in 41 severely malnourished IBD patients undergoing a 14 day intervention with total parenteral nutrition, while total body protein measured by IVNAA did not improve significantly during the intervention period.73 This distinction is obviously only seen in short term nutritional therapy, while longterm nutritional therapy usually restores both mass and function. Paton et al. e.g. reported significant increase in fat free mass and hand grip strength in malnourished tuberculosis patients after six week intervention with sip feeds.74 Improvement in muscle function is usually accompanied by improved functional status and thus increased quality of life. We studied the effect of three month post hospital intervention with sip feeds on body composition, muscle function and quality of life in malnourished patients with benign gastrointestinal disease. Whereas the effect on body cell mass was comparable between intervention and control group, both hand grip strength and expiratory peak flow improved significantly only in the intervention group and these changes were paralleled by a similar improvement in physical aspect of quality of life.75 Comparable results are also known from intervention with sip feeds in malnourished surgical patients. While progressive postoperative reduction in grip strength occurred in all patients up to four weeks after surgery, the reduction was less marked in the intervention group and significantly improved grip strength values were observed at ten weeks in comparison with the control patients. These changes were again accompanied by similar increases in the physical aspect of quality of life.76 In stroke patients at nutritional risk, individual nutritional support also improved hand grip strength and quality of life scores mobility, self care and usual activities whereas control patients experienced a worsening of hand grip strength.77 In the elderly, findings on changes in hand grip strength during nutritional therapy are not as consistent. Price et al. investigated the impact of two month nutritional therapy on hand grip strength in geriatric patients (>75 years) following hospital stay. The per-protocol analysis revealed a significant increase of hand grip strength in the intervention patients, whereas the intentionto-treat analysis showed no difference between intervention and control group.78 In a comparable trial by Edington et al. in malnourished elderly patients (>65 years), eight week supplementation resulted in significant improvement in hand grip strength which, however, appeared to be linked to the intake of sip feeds. After six months, hand grip strength values of the intervention patients approached the values of the control group.79 We studied the effect of two month protein and energy supplementation on elderly nursing home residents and found no improvement in hand grip strength, Barthel Index or quality of life despite an increase of BMI and mini nutritional assessment score.80 Furthermore, the meta-analysis by Milne et al found no positive effect of nutritional intervention on hand grip strength in a pooled analysis of ten studies. It is therefore tempting to conclude that muscle function is more closely related to general frailty in older age than to nutritional status.81 This is in accordance with the fact that reduced skeletal muscle mass is a common finding in the elderly as shown in the large cross-sectional survey using data form the Third National Health and Nutrition Examination Survey (NHANES III).82 However, there appears to be a gender-related Table 3 Reference values for hand grip strength derived from studies with >200 healthy participants. Author (country) N (m/f) 214 (105/109) Crosby et al.87 (USA) 540 (254/286) Massy-Westropp et al.88 (Australia) Luna-Heredia et al.89 (Spain) 517 (229/267) Age Hand Device 16e63 18e97 l/r l/r 17e97 l/r Schlüssel et al.84 (Brazil) Budziareck et al.25 (Brazil) Günther et al.90 (Germany) 3050 (1122/1928) 20-70þ l/r 300 (150/150) 18e90 l/r 769 (366/403) 20e95 l/r Werle et al.91 (Switzerland) 1023 (516/507) 18e96 l/r Jamar Jamar and Grippit BASELINE and GRIP-D Jamar Jamar BASELINE digital Jamar Abbreviation: l ¼ left; r ¼ right. difference, as a study of a small non-random sample of 67 older men and women (mean age 59.7 years) revealed that whereas men appear to lose more hand grip strength and body cell mass per decade, loss of isokinetic force of lower leg muscle (knee extension) is more prominent in women.83 In younger adults, however, hand grip strength appears to be an attractive easy-to-use instrument for monitoring of nutritional intervention. Short term effects of nutritional therapy as e.g. refeeding of acute malnutrition are seen earlier by muscle function than by changes in body composition. Long-term nutritional therapy should result in both changes of body composition and muscle function, which should be paralleled by improvements of physical status. For the evaluation of single measurements, however, reference values must be consulted. Fig. 2 and Table 3 give an overview over current reference values generated in healthy populations; the largest database with age- and gender-specific percentiles comes from Brazil (3050 healthy adults aged 20 years).84 Whether they can be transferred to European populations, however, and which percentile proves to be clinically relevant, remains to be seen. 9. Limitations and controversies related to hand grip strength Some limitations related to the measurement of hand grip strength must also be addressed. There is still e.g. no consensus on measurement protocols.92 The American Society of Hand therapists93 proposes assessment of grip strength with the elbow flexed at 90 with the subject in the sitting position, with their shoulders adducted, their elbows flexed 90 , and their forearms in neutral, a methodology which is associated with high intra-test and intertest reliability.94 Consistency in measuring hand grip strength is crucial, since posture, arm side or handle position of the dynamometer easily alter maximum grip strength.13,92,94e96 It must also be kept in mind that hand grip strength is an indicator of upper limb strength only and despite its predictive potential cannot replace evaluation of assessment of activities of daily living (ADL), lower extremity strength or walking speed in fragile populations such as the elderly or patients with neuromuscular disease. Mortality prediction of hand grip strength also depends on which further parameters are included in the regression models. As recently shown by our group, hand grip strength predicted 6 month mortality in cancer patients, but lost significance when bioelectrical phase angle was introduced in the model.97 This may apply to other populations as well. Nevertheless, hand grip strength is a simple bed side parameter which provides valuable information in addition to assessment of nutritional and/or functional status. In order to identify patients at risk, reliable cut off values still have to be proposed and validated. K. Norman et al. / Clinical Nutrition 30 (2011) 135e142 Conflict of interest statement The authors have no disclosure of interest regarding this review article. Acknowledgements KN, NS and MP: concept, literature research and writing of the article. KN and MCG: concept of figures. MCG and JDS: critical revision. All authors have actively contributed, read and approved the final manuscript. No writing assistance was needed. References 1. Symreng T, Larsson J, Schildt B, Wetterfors J. Nutritional assessment reflects muscle energy metabolism in gastric carcinoma. Ann Surg 1983;198:146e50. 2. Thompson A, Damaniovich A, Madapallipattam A, Mikalus D, Allard J, Jeejeebhoy KN. P-nuclear magnetic resonce studies of bioenergetic changes in skeletal muscle in malnourished human adults. Am J Clin Nutr 1998;67:39e43. 3. Heymsfield SB, Mcmanus C, Stevens V, Smith J. Muscle mass: reliable indicator of protein-energy malnutrition severity and outcome. Am J Clin Nutr 1982;35: 1192e9. 4. Daniel PM. The metabolic homoeostatic role of muscle and its function as a store of protein. Lancet 1977;2:446e8. 5. Ardawi MS, Majzoub MF, Masoud IM, Newsholme EA. Enzymic and metabolic adaptations in the gastrocnemius, plantaris and soleus muscles of hypocaloric rats. Biochem J 1989;261:219e25. 6. Madapallimattam AG, Law L, Jeejeebhoy KN. Effect of hypoenergetic feeding on muscle oxidative phosphorylation and mitochondrial complex IeIV activities in rats. Am J Clin Nutr 2002;76:1031e9. 7. Russell DM, Walker PM, Leiter LA, Sima AA, Tanner WK, Mickle DA, et al. Metabolic and structural changes in skeletal muscle during hypocaloric dieting. Am J Clin Nutr 1984;39:503e13. 8. Russell DM, Atwood HL, Whittaker JS, Itakura T, Walker PM, Mickle DA, et al. The effect of fasting and hypocaloric diets on the functional and metabolic characteristics of rat gastrocnemius muscle. Clin Sci (Lond) 1984;67:185e94. 9. Church JM, Choong SY, Hill GL. Abnormalities of muscle metabolism and histology in malnourished patients awaiting surgery: effects of a course of intravenous nutrition. Br J Surg 1984;71:563e9. 10. Peng S, Plank LD, McCall JL, Gillanders LK, McIlroy K, Gane EJ. Body composition, muscle function, and energy expenditure in patients with liver cirrhosis: a comprehensive study. Am J Clin Nutr 2007;85:1257e66. 11. Windsor JA, Hill GL. Grip strength: a measure of the proportion of protein loss in surgical patients. Br J Surg 1988;75:880e2. 12. Norman K, Schutz T, Kemps M, Josef LH, Lochs H, Pirlich M. The Subjective Global Assessment reliably identifies malnutrition-related muscle dysfunction. Clin Nutr 2005;24:143e50. 13. Hillman TE, Nunes QM, Hornby ST, Stanga Z, Neal KR, Rowlands BJ, et al. A practical posture for hand grip dynamometry in the clinical setting. Clin Nutr 2005;24(2):224e8. 14. Chilima DM, Ismail SJ. Nutrition and handgrip strength of older adults in rural Malawi. Public Health Nutr 2001;4:11e7. 15. Pieterse S, Manandhar M, Ismail S. The association between nutritional status and handgrip strength in older Rwandan refugees. Eur J Clin Nutr 2002;56: 933e9. 16. Humphreys J, de la MP, Hirsch S, Barrera G, Gattas V, Bunout D. Muscle strength as a predictor of loss of functional status in hospitalized patients. Nutrition 2002;18:616e20. 17. Hunt DR, Rowlands BJ, Johnston D. Hand grip strengthea simple prognostic indicator in surgical patients. JPEN J Parenter Enteral Nutr 1985;9:701e4. 18. Klidjian AM, Foster KJ, Kammerling RM, Cooper A, Karran SJ. Relation of anthropometric and dynamometric variables to serious postoperative complications. Br Med J 1980;281:899e901. 19. Webb AR, Newman LA, Taylor M, Keogh JB. Hand grip dynamometry as a predictor of postoperative complications reappraisal using age standardized grip strengths. JPEN J Parenter Enteral Nutr 1989;13:30e3. 20. Russell DM, Leiter LA, Whitwell J, Marliss EB, Jeejeebhoy KN. Skeletal muscle function during hypocaloric diets and fasting: a comparison with standard nutritional assessment parameters. Am J Clin Nutr 1983;37:133e8. 21. Lopes J, Russell DM, Whitwell J, Jeejeebhoy KN. Skeletal muscle function in malnutrition. Am J Clin Nutr 1982;36:602e10. 22. Lennmarken C, Larsson J. Skeletal muscle function and energy metabolites in malnourished surgical patients. Acta Chir Scand 1986;152:169e73. 23. Mitsionis G, Pakos EE, Stafilas KS, Paschos N, Papakostas T, Beris AE. Normative data on hand grip strength in a Greek adult population. Int Orthop; 2008. 24. Kuh D, Bassey EJ, Butterworth S, Hardy R, Wadsworth ME. Grip strength, postural control, and functional leg power in a representative cohort of British men and women: associations with physical activity, health status, and socioeconomic conditions. J Gerontol A Biol Sci Med Sci 2005;60:224e31. 25. Budziareck MB, Pureza Duarte RR, Barbosa-Silva MC. Reference values and determinants for handgrip strength in healthy subjects. Clin Nutr 2008;27: 357e62. 141 26. Lindboe CF, Platou CS. Disuse atrophy of human skeletal muscle. An enzyme histochemical study. Acta Neuropathol (Berl) 1982;56:241e4. 27. Wagenmakers AJ. Muscle function in critically ill patients. Clin Nutr 2001;20: 451e4. 28. Vaz M, Thangam S, Prabhu A, Shetty PS. Maximal voluntary contraction as a functional indicator of adult chronic undernutrition. Br J Nutr 1996;76:9e15. 29. Norman K, Stobaus N, Smoliner C, Zocher D, Scheufele R, Valentini L, et al. Determinants of hand grip strength, knee extension strength and functional status in cancer patients. Clin Nutr 2010;29(5):586e91. 30. Tanner CJ, Barakat HA, Dohm GL, Pories WJ, MacDonald KG, Cunningham PR, et al. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 2002;282:E1191e6. 31. Kriketos AD, Pan DA, Lillioja S, Cooney GJ, Baur LA, Milner MR, et al. Interrelationships between muscle morphology, insulin action, and adiposity. Am J Physiol 1996;270:R1332e9. 32. Marin P, Andersson B, Krotkiewski M, Bjorntorp P. Muscle fiber composition and capillary density in women and men with NIDDM. Diabetes Care 1994;17: 382e6. 33. Rolland Y, Lauwers-Cances V, Pahor M, Fillaux J, Grandjean H, Vellas B. Muscle strength in obese elderly women: effect of recreational physical activity in a cross-sectional study. Am J Clin Nutr 2004;79:552e7. 34. Hulens M, Vansant G, Lysens R, Claessens AL, Muls E, Brumagne S. Study of differences in peripheral muscle strength of lean versus obese women: an allometric approach. Int J Obes Relat Metab Disord 2001;25:676e81. 35. Essen B, Fohlin L, Thoren C, Saltin B. Skeletal muscle fibre types and sizes in anorexia nervosa patients. Clin Physiol 1981;1:395e403. 36. Lindboe CF, Askevold F, Slettebo M. Changes in skeletal muscles of young women with anorexia nervosa. An enzyme histochemical study. Acta Neuropathol (Berl) 1982;56:299e302. 37. McLoughlin DM, Spargo E, Wassif WS, Newham DJ, Peters TJ, Lantos PL, et al. Structural and functional changes in skeletal muscle in anorexia nervosa. Acta Neuropathol (Berl) 1998;95:632e40. 38. Brooks SE. Ultrastructure of voluntary muscle in childhood malnutrition. West Indian Med J 1995;44:133e9. 39. Oumi M, Miyoshi M, Yamamoto T. Ultrastructural changes and glutathione depletion in the skeletal muscle induced by protein malnutrition. Ultrastruct Pathol 2001;25:431e6. 40. Gupta RK, Mittal RD, Agarwal KN, Agarwal DK. Muscular sufficiency, serum protein, enzymes and bioenergetic studies (31-phosphorus magnetic resonance spectroscopy) in chronic malnutrition. Acta Paediatr 1994;83:327e31. 41. Bourdel-Marchasson I, Joseph PA, Dehail P, Biran M, Faux P, Rainfray M, et al. Functional and metabolic early changes in calf muscle occurring during nutritional repletion in malnourished elderly patients. Am J Clin Nutr 2001;73:832e8. 42. Padmavathi R, Kurpad AV, Vaz M. Skeletal muscle endurance is reduced in chronically energy deficient adults. Indian J Med Res 2000;111:28e34. 43. Russell DM, Prendergast PJ, Darby PL, Garfinkel PE, Whitwell J, Jeejeebhoy KN. A comparison between muscle function and body composition in anorexia nervosa: the effect of refeeding. Am J Clin Nutr 1983;38:229e37. 44. Rigaud D, Moukaddem M, Cohen B, Malon D, Reveillard V, Mignon M. Refeeding improves muscle performance without normalization of muscle mass and oxygen consumption in anorexia nervosa patients. Am J Clin Nutr 1997;65:1845e51. 45. Bissonnette DJ, Madapallimatam A, Jeejeebhoy KN. Effect of hypoenergetic feeding and high-carbohydrate refeeding on muscle tetanic tension, relaxation rate, and fatigue in slow- and fast-twitch muscles in rats. Am J Clin Nutr 1997; 66:293e303. 46. Guo CB, Zhang W, Ma DQ, Zhang KH, Huang JQ. Hand grip strength: an indicator of nutritional state and the mix of postoperative complications in patients with oral and maxillofacial cancers. Br J Oral Maxillofac Surg 1996;34:325e7. 47. Bohannon RW. Hand-grip dynamometry predicts future outcomes in aging adults. J Geriatr Phys Ther 2008;31:3e10. 48. Kerr A, Syddall HE, Cooper C, Turner GF, Briggs RS, Sayer AA. Does admission grip strength predict length of stay in hospitalised older patients? Age Ageing 2006;35:82e4. 49. Vecchiarino P, Bohannon RW, Ferullo J, Maljanian R. Short-term outcomes and their predictors for patients hospitalized with community-acquired pneumonia. Heart Lung 2004;33:301e7. 50. Bohannon RW, Maljanian R, Ferullo J. Mortality and readmission of the elderly one year after hospitalization for pneumonia. Aging Clin Exp Res 2004;16: 22e5. 51. Rantanen T, Avlund K, Suominen H, Schroll M, Frandin K, Pertti E. Muscle strength as a predictor of onset of ADL dependence in people aged 75 years. Aging Clin Exp Res 2002;4:10e5. 52. Gale CR, Martyn CN, Cooper C, Sayer AA. Grip strength, body composition, and mortality. Int J Epidemiol 2007;36:228e35. 53. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, et al. Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci 2006;61:72e7. 54. Rantanen T, Volpato S, Ferrucci L, Heikkinen E, Fried LP, Guralnik JM. Handgrip strength and cause-specific and total mortality in older disabled women: exploring the mechanism. J Am Geriatr Soc 2003;51:636e41. 142 K. Norman et al. / Clinical Nutrition 30 (2011) 135e142 55. Sasaki H, Kasagi F, Yamada M, Fujita S. Grip strength predicts cause-specific mortality in middle-aged and elderly persons. Am J Med 2007;120:337e42. 56. Rantanen T, Harris T, Leveille SG, Visser M, Foley D, Masaki K, et al. Muscle strength and body mass index as long-term predictors of mortality in initially healthy men. J Gerontol A Biol Sci Med Sci 2000;55:M168e73. 57. Blain H, Vuillemin A, Teissier A, Hanesse B, Guillemin F, Jeandel C. Influence of muscle strength and body weight and composition on regional bone mineral density in healthy women aged 60 years and over. Gerontology 2001;47: 207e12. 58. Segal NA, Torner JC, Yang M, Curtis JR, Felson DT, Nevitt MC. Muscle mass is more strongly related to hip bone mineral density than is quadriceps strength or lower activity level in adults over age 50 year. J Clin Densitom 2008;11: 503e10. 59. Sandler R, Robinovitch S. An analysis of the effect of lower extremity strength on impact severity during a backward fall. J Biomech Eng 2001;123:590e8. 60. Whipple RH, Wolfson LI, Amerman PM. The relationship of knee and ankle weakness to falls in nursing home residents: an isokinetic study. J Am Geriatr Soc 1987;35:13e20. 61. Bauer DC, Browner WS, Cauley JA, Orwoll ES, Scott JC, Black DM, et al. Factors associated with appendicular bone mass in older women. The Study of Osteoporotic Fractures Research Group. Ann Intern Med 1993;118:657e65. 62. Beverly MC, Rider TA, Evans MJ, Smith R. Local bone mineral response to brief exercise that stresses the skeleton. BMJ 1989;299:233e5. 63. Bevier WC, Wiswell RA, Pyka G, Kozak KC, Newhall KM, Marcus R. Relationship of body composition, muscle strength, and aerobic capacity to bone mineral density in older men and women. J Bone Miner Res 1989;4:421e32. 64. Kaya A, Ozgocmen S, Ardicoglu O, Kamanli A, Gudul H. Relationship between grip strength and hand bone mineral density in healthy adults. Arch Med Res 2005;36:603e6. 65. Sinaki M, Wahner HW, Offord KP. Relationship between grip strength and related regional bone mineral content. Arch Phys Med Rehabil 1989;70:823e6. 66. Snow-Harter C, Bouxsein M, Lewis B, Charette S, Weinstein P, Marcus R. Muscle strength as a predictor of bone mineral density in young women. J Bone Miner Res 1990;5:589e95. 67. Tsuji S, Tsunoda N, Yata H, Katsukawa F, Onishi S, Yamazaki H. Relation between grip strength and radial bone mineral density in young athletes. Arch Phys Med Rehabil 1995;76:234e8. 68. Chan DC, Lee WT, Lo DH, Leung JC, Kwok AW, Leung PC. Relationship between grip strength and bone mineral density in healthy Hong Kong adolescents. Osteoporos Int 2008;19:1485e95. 69. Osei-Hyiaman D, Ueji M, Toyokawa S, Takahashi H, Kano K. Influence of grip strength on metacarpal bone mineral density in postmenopausal Japanese women: a cross-sectional study. Calcif Tissue Int 1999;64:263e6. 70. Dixon WG, Lunt M, Pye SR, Reeve J, Felsenberg D, Silman AJ, et al. Low grip strength is associated with bone mineral density and vertebral fracture in women. Rheumatology (Oxford) 2005;44:642e6. 71. Sirola J, Rikkonen T, Tuppurainen M, Honkanen R, Jurvelin JS, Kroger H. Maintenance of muscle strength may counteract weight-loss-related postmenopausal bone lossea population-based approach. Osteoporos Int 2006;17: 775e82. 72. Sirola J, Rikkonen T, Tuppurainen M, Jurvelin JS, Alhava E, Kroger H. Grip strength may facilitate fracture prediction in perimenopausal women with normal BMD: a 15-year population-based study. Calcif Tissue Int 2008;83: 93e100. 73. Christie PM, Hill GL. Effect of intravenous nutrition on nutrition and function in acute attacks of inflammatory bowel disease. Gastroenterology 1990;99:730e6. 74. Paton NI, Chua YK, Earnest A, Chee CB. Randomized controlled trial of nutritional supplementation in patients with newly diagnosed tuberculosis and wasting. Am J Clin Nutr 2004;80:460e5. 75. Norman K, Kirchner H, Freudenreich M, Ockenga J, Lochs H, Pirlich M. Three month intervention with protein and energy rich supplements improve muscle function and quality of life in malnourished patients with non- neoplastic gastrointestinal disease e a randomized controlled trial. Clin Nutr 2008;27:48e56. 76. Beattie AH, Prach AT, Baxter JP, Pennington CR. A randomised controlled trial evaluating the use of enteral nutritional supplements postoperatively in malnourished surgical patients. Gut 2000;46:813e8. 77. Ha L, Hauge T, Spenning AB, Iversen PO. Individual, nutritional support prevents undernutrition, increases muscle strength and improves QoL among elderly at nutritional risk hospitalized for acute stroke: a randomized, controlled trial. Clin Nutr; 2010. 78. Price R, Daly F, Pennington CR, McMurdo ME. Nutritional supplementation of very old people at hospital discharge increases muscle strength: a randomised controlled trial. Gerontology 2005;51:179e85. 79. Edington J, Barnes R, Bryan F, Dupree E, Frost G, Hickson M, et al. A prospective randomised controlled trial of nutritional supplementation in malnourished elderly in the community: clinical and health economic outcomes. Clin Nutr 2004;23:195e204. 80. Smoliner C, Norman K, Scheufele R, Hartig W, Pirlich M, Lochs H. Effects of food fortification on nutritional and functional status in frail elderly nursing home residents at risk of malnutrition. Nutrition 2008;24:1139e44. 81. Milne AC, Avenell A, Potter J. Meta-analysis: protein and energy supplementation in older people. Ann Intern Med 2006;144:37e48. 82. Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 2002;50:889e96. 83. Shephard RJ, Montelpare W, Plyley M, McCracken D, Goode RC. Handgrip dynamometry, Cybex measurements and lean mass as markers of the ageing of muscle function. Br J Sports Med 1991;25:204e8. 84. Schlüssel MM, dos Anjos LA, de Vasconcellos MT, Kac G. Reference values of handgrip dynamometry of healthy adults: a population-based study. Clin Nutr 2008;27:601e7. 85. Rantanen T, Guralnik JM, Foley D, Masaki K, Leveille S, Curb JD, et al. Midlife hand grip strength as a predictor of old age disability. JAMA 1999;281:558e60. 86. Keele AM, Bray MJ, Emery PW, Duncan HD, Silk DB. Two phase randomised controlled clinical trial of postoperative oral dietary supplements in surgical patients. Gut 1997;40:393e9. 87. Crosby CA, Wehbe MA, Mawr B. Hand strength: normative values. J Hand Surg Am 1994;19:665e70. 88. Massy-Westropp N, Rankin W, Ahern M, Krishnan J, Hearn TC. Measuring grip strength in normal adults: reference ranges and a comparison of electronic and hydraulic instruments. J Hand Surg Am 2004;29:514e9. 89. Luna-Heredia E, Martin-Pena G, Ruiz-Galiana J. Handgrip dynamometry in healthy adults. Clin Nutr 2005;24:250e8. 90. Gunther CM, Burger A, Rickert M, Crispin A, Schulz CU. Grip strength in healthy caucasian adults: reference values. J Hand Surg Am 2008;33:558e65. 91. Werle S, Goldhahn J, Drerup S, Simmen BR, Sprott H, Herren DB. Age- and gender-specific normative data of grip and pinch strength in a healthy adult Swiss population. J Hand Surg Eur Vol 2009;34:76e84. 92. Leal V, Mafra D, Fouque D, Anjos L. Use of handgrip strength in the assessment of the muscle function of chronic kidney disease patients on dialysis: a systematic review. Nephrol Dial Transplant; 2010 Aug 13 [Epub ahead of print]. 93. Fess EE, Moran C. Clinical assessment recommendations. Indianapolis: American Society of Hand therapists Monograph; 1981. 94. Mathiowetz V, Weber K, Volland G, Kashman N. Reliability and validity of grip and pinch strength evaluations. J Hand Surg Am 1984 Mar;9(2):222e6. 95. Tredgett M, Pimble LJ, Davis TR. The detection of feigned hand weakness using the five position grip strength test. J Hand Surg Br 1999 Aug;24(4):426e8. 96. Bechtol C. Grip test; the use of a dynamometer with adjustable handle spacings. J Bone Jt Surg Am 1954 Jul;36-A(4):820e4. 97. Norman K, Stobäus N, Zocher D, Bosy-Westphal A, Szramek A, Scheufele R, et al. Cutoff percentiles of bioelectrical phase angle predict functionality, quality of life, and mortality in patients with cancer. Am J Clin Nutr; 2010 Jul 14 [Epub ahead of print].
0
You can add this document to your study collection(s)
Sign in Available only to authorized usersYou can add this document to your saved list
Sign in Available only to authorized users(For complaints, use another form )