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Handgrip strength predicts 1-year functional recovery and mortality in hip fracture patients

      Highlights

      • Low grip strength in elderly patients with hip fracture predicts greater functional disability.
      • At 1 year after hip fracture,lower grip strength predicts a major change in the ability to walk and a higher mortality rate.
      • There was no association between lower grip strength and change in walking ability in patients aged over 90 years.

      Abstract

      Objectives

      Muscle strength is a possible predictor of adverse events. It could have prognostic value in patients with hip fracture (HF). The aim of this study was to determine if handgrip strength is associated with functional impairment, readmissions, and mortality at one year in elderly patients with HF.

      Design

      A prospective observational study was carried out. It included a cohort of patients aged 65 years or older with a diagnosis of fragility HF, consecutively from January 2013 to February 2014 and seen in follow-up at one year. Statistical analysis was performed using SPSS v21 software.

      Main outcome measures

      Five hundred and nine patients with a mean age of 85.4 ± 0.3 years were included, of whom 403 (79.2 %) were women. Clinical and functional outcomes, laboratory parameters and anthropometric measurements were collected.

      Results

      Of the total sample, 339 (66.6 %) had reduced handgrip strength, and these patients were older, more frequently institutionalized, had poorer functional and cognitive status, higher comorbidity, higher surgical risk, lower body mass index and a greater intra-hospital mortality (all p < 0.01). At one year, patients with lower handgrip strength had a major change in their ability to walk (32.7 % vs. 10.9 %, p < 0.001) and a higher mortality rate (30.4 % vs. 8.8 %, p < 0.001). However, in patients over 91 years of age, there was no association between lower handgrip strength and change in ability to walk. There were no differences in the number of readmissions.

      Conclusion

      Low handgrip strength in elderly patients with HF predicts greater functional disability and higher long-term mortality.

      Keywords

      1. Introduction

      Hip fracture (HF) is a common cause of morbidity in the elderly. It is associated with excess mortality compared to the same age population without HF [
      • Meyer H.E.
      • Tverdal A.
      • Falch J.A.
      • Pedersen J.I.
      Factors associated with mortality after hip fracture.
      ]. These patients often suffer prolonged periods of immobilization, which have negative consequences on their health and quality of life, and in many cases results in institutionalization. There were 620,000 new cases per year in the European Union in 2010 and more than 210,000 new cases per year in the United States between 2008 and 2011, so HF due to fragility can be considered a public health problem [
      • Hernlund E.
      • Svedbom A.
      • Ivergård M.
      • Compston J.
      • Cooper C.
      • Stenmark J.
      • et al.
      Osteoporosis in the European Union: medical management, epidemiology and economic burden: a report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA).
      ,
      • Singer A.
      • Exuzides A.
      • Spangler L.
      • O´Malley C.
      • Colby C.
      • Johnston K.
      • et al.
      Burden of illness for osteoporotic fractures compared with other serious diseases among postmenopausal women in the United States.
      ].
      Sarcopenia, defined as the loss of muscle mass and strength associated with age, plays a key role in functional status of the elderly. Decreased muscle strength seems to precede loss of muscle mass, with strength or weakness being a better predictor of adverse events that muscle mass [
      • Menant J.C.
      • Weber F.
      • Lo J.
      • Sturnieks D.L.
      • Close J.C.
      • Sachdev P.S.
      • et al.
      Strength measures are better than muscle measures in predicting health-related outcomes in older people mass: time to abandon the term sarcopenia?.
      ].
      Measuring handgrip strength is a simple and reliable technique that determines the patient’s muscle strength and appears to have predictive value in patients with HF [
      • Roberts H.C.
      • Denison H.J.
      • Martin H.J.
      • Patel H.P.
      • Syddall H.
      • Cooper C.
      • et al.
      A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardized approach.
      ]. An association between decreased handgrip strength and HF was shown by Denk et al. [
      • Denk K.
      • Lennon S.
      • Gordon S.
      • Jaarsma R.L.
      The association between decreased hand grip strength and hip fracture in older people: a systematic review.
      ]. Decreased strength in HF patients was associated with increased postoperative complications [
      • Davies C.W.
      • Jones D.M.
      • Shearer J.R.
      Hand grip - a simple test for morbidity after fracture of the neck of femur.
      ], increased incidence of pressure ulcers [
      • Gumieiro D.
      • Rafacho B.P.
      • Gradella L.M.
      • Azevedo P.S.
      • Gaspardo D.
      • Zornoff L.A.
      • et al.
      Handgrip strength predicts patients with pressure ulcers in hip fractures.
      ], increased surgical delay [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ], poorer functional status [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Di Monaco R.
      Handgrip strength but not appendicular lean mass is an independent predictor of functional outcome in hip fracture women: a prospective study short-term.
      ,
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Tappero R.
      Handgrip strength is an independent predictor of functional outcome in hip fracture women: a prospective study with 6-month follow-up.
      ,
      • Neira Alvarez M.
      • López-Dóriga P.
      • Thuissard I.J.
      • Sanz-Rosa D.
      • Arias Muñana E.
      • Bielza Galindo R.
      • et al.
      Grip strength and functional recovery after hip fracture: an observational study in elderly population.
      ] and cognitive status [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Neira Alvarez M.
      • López-Dóriga P.
      • Thuissard I.J.
      • Sanz-Rosa D.
      • Arias Muñana E.
      • Bielza Galindo R.
      • et al.
      Grip strength and functional recovery after hip fracture: an observational study in elderly population.
      ], living in a nursing home at one year and increased mortality at one year [
      • Steihaug O.M.
      • Gjesdal C.G.
      • Bogen B.
      • Kristoffersen M.H.
      • Lien G.
      • Hufhammer K.O.
      • et al.
      Does sarcopenia predict change in mobility after hip fracture? Observational multicenter Study with a one-year follow-up.
      ] and in the longer term [
      • Meyer H.E.
      • Tverdal A.
      • Falch J.A.
      • Pedersen J.I.
      Factors associated with mortality after hip fracture.
      However, studies published to date have a number of limitations; most include small patient series, some of them only include women [
      • Davies C.W.
      • Jones D.M.
      • Shearer J.R.
      Hand grip - a simple test for morbidity after fracture of the neck of femur.
      ,
      • Gumieiro D.
      • Rafacho B.P.
      • Gradella L.M.
      • Azevedo P.S.
      • Gaspardo D.
      • Zornoff L.A.
      • et al.
      Handgrip strength predicts patients with pressure ulcers in hip fractures.
      ,
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Di Monaco R.
      Handgrip strength but not appendicular lean mass is an independent predictor of functional outcome in hip fracture women: a prospective study short-term.
      ,
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Tappero R.
      Handgrip strength is an independent predictor of functional outcome in hip fracture women: a prospective study with 6-month follow-up.
      ]. Other studies exclude patients with comorbidities such as those with dementia [
      • Meyer H.E.
      • Tverdal A.
      • Falch J.A.
      • Pedersen J.I.
      Factors associated with mortality after hip fracture.
      ,
      • Davies C.W.
      • Jones D.M.
      • Shearer J.R.
      Hand grip - a simple test for morbidity after fracture of the neck of femur.
      ,
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Di Monaco R.
      Handgrip strength but not appendicular lean mass is an independent predictor of functional outcome in hip fracture women: a prospective study short-term.
      ,
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Tappero R.
      Handgrip strength is an independent predictor of functional outcome in hip fracture women: a prospective study with 6-month follow-up.
      ,
      • Steihaug O.M.
      • Gjesdal C.G.
      • Bogen B.
      • Kristoffersen M.H.
      • Lien G.
      • Hufhammer K.O.
      • et al.
      Does sarcopenia predict change in mobility after hip fracture? Observational multicenter Study with a one-year follow-up.
      ,
      • Beloosesky Y.
      • Weiss A.
      • Manasian M.
      • Salai M.
      Handgrip strength of the elderly after hip fracture repair correlates with functional outcome.
      ], those who did not walk before the HF [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Steihaug O.M.
      • Gjesdal C.G.
      • Bogen B.
      • Kristoffersen M.H.
      • Lien G.
      • Hufhammer K.O.
      • et al.
      Does sarcopenia predict change in mobility after hip fracture? Observational multicenter Study with a one-year follow-up.
      ], those who had suffered a previous HF in the same location [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Di Monaco R.
      Handgrip strength but not appendicular lean mass is an independent predictor of functional outcome in hip fracture women: a prospective study short-term.
      ] that was not accepted for surgery [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Neira Alvarez M.
      • López-Dóriga P.
      • Thuissard I.J.
      • Sanz-Rosa D.
      • Arias Muñana E.
      • Bielza Galindo R.
      • et al.
      Grip strength and functional recovery after hip fracture: an observational study in elderly population.
      ], institutionalized patients [
      • Meyer H.E.
      • Tverdal A.
      • Falch J.A.
      • Pedersen J.I.
      Factors associated with mortality after hip fracture.
      ,
      • Steihaug O.M.
      • Gjesdal C.G.
      • Bogen B.
      • Kristoffersen M.H.
      • Lien G.
      • Hufhammer K.O.
      • et al.
      Does sarcopenia predict change in mobility after hip fracture? Observational multicenter Study with a one-year follow-up.
      ], or those with short life expectancy [
      • Neira Alvarez M.
      • López-Dóriga P.
      • Thuissard I.J.
      • Sanz-Rosa D.
      • Arias Muñana E.
      • Bielza Galindo R.
      • et al.
      Grip strength and functional recovery after hip fracture: an observational study in elderly population.
      ,
      • Steihaug O.M.
      • Gjesdal C.G.
      • Bogen B.
      • Kristoffersen M.H.
      • Lien G.
      • Hufhammer K.O.
      • et al.
      Does sarcopenia predict change in mobility after hip fracture? Observational multicenter Study with a one-year follow-up.
      ,
      • Beloosesky Y.
      • Weiss A.
      • Manasian M.
      • Salai M.
      Handgrip strength of the elderly after hip fracture repair correlates with functional outcome.
      ].
      This study was carried out to determine if handgrip strength values are associated with functional impairment, readmissions, and long-term mortality in a cohort of unselected patients with HF.

      2. Methods

      An observational, analytical, longitudinal, prospective study was performed. All patients over the age of 65, hospitalized consecutively with a diagnosis of fragility HF from January 2013 to February 2014 to a 1300-bed university tertiary hospital with a capacity of 1300 beds were included. The hospital covers an area of ​​approximately 520,000 patients. Patients were admitted directly from the emergency department to the orthogeriatric unit. All patients were evaluated within 72 h of admission, always before surgery. Patients admitted to this unit underwent a comprehensive geriatric assessment and a study of their fall. They were treated jointly by the ortogeriatrician, orthopaedic surgeon and orthogeriatric nurse. They were also helped to start sitting on the first day after surgery, and to bear their own weight on the second day after surgery. The physiotherapist performed an evaluation of the patient and initiated both physical therapy and gait training in the same room in which they were hospitalized. The orthogeriatric team plans the discharge and assesses the need for referral to a geriatric rehabilitation unit after discharge. During hospitalization, patients received the usual orthogeriatric care and a standardized protocol called FONDA (Spanish acronym for function, osteoporosis, nutrition, pain and anemia) was applied to the comprehensive treatment of HF [
      • Gonzalez-Montalvo J.I.
      • Alarcón T.
      • Gotor-Pérez P.
      • Martín-Maestre I.
      ¿Es posible mejorar la atención al paciente con fractura de cadera? Aportaciones del programa FONDA.
      ]. The objectives of this standardized protocol are: 1) optimize physical function by prescribing active and passive exercises in bed and chair upon admission and while standing after surgery; 2) promote bone health by early correction of blood vitamin D levels and initiation of osteoporosis treatment after discharge; 3) maintain adequate nutritional status through nutritional supplementation in cases of hypoproteinemia or body mass index <22 kg/m2; 4) adequate pain control by providing analgesia every 4 h; 5) avoiding anaemia with intravenous administration of iron in cases of iron deficiency and red blood cell transfusion if haemoglobin drops below 9 g/dl or below 10 g/dl if there is vital organ involvement.
      Demographic data such as age, sex and institutionalization were collected, as well as clinical data such as the type of HF and surgery and the surgical risk according to the American Society of Anesthesiologists (ASA) scale. A clinical history was performed which included baseline clinical variables such as previous diseases, anticoagulation, Charlson comorbidity index, and functional variables such as the baseline Functional Ambulation Categories (FAC) (Holden et al., 1984) [
      • Holden M.K.
      • Gill K.M.
      • Magliozzi M.R.
      • Nathan J.
      • Piehl-Baker L.
      Clinical gait assessment in the neurologically impaired. Reliability and meaningfulness.
      ], baseline and admission Barthel Index [
      • Cabañero-Martinez M.J.
      • Cabrero-Garcia J.
      • Richart-Martinez M.
      • Muñoz-Mendoza C.L.
      The Spanish versions of the Barthel index (BI) and the Katz index (KI) of activities of daily living (ADL): a structured review.
      ]. The FAC scale assesses walking ability at levels ranging from 0 (disability) to 5 (independence to walk on all types of surfaces). Patients were classified into 3 groups: FAC 0, inability to walk; 1, 2, 3, walking aid and 4, 5, independent for walking inside and outside the home. The Barthel Index assesses autonomy for basic activities of daily living, and its range goes from 0 (total dependence) to 100 (total independence). Cognitive variables were described by the Cruz Roja Mental scale (CRM) (González Montalvo, 1992) [
      • Gonzalez-Montalvo J.I.
      • Rodríguez-Mañas L.
      • Ruipérez-Cantera I.
      Validación del cuestionario Pfeiffer y la escala de incapacidad mental de la Cruz Roja en la detección del deterioro mental en los pacientes externos de un servicio de geriatría.
      ], which includes values ​​from 0 (completely normal) to 5 (advanced dementia), both baseline and at admission. The Pfeiffer questionnaire was applied (Martínez et al., 2011) [
      • Martinez J.
      • Duenas R.
      • Onís M.C.
      • Aguado-Tabernea C.
      • Albert-Colmenerc
      • Luquec L.
      Adaptación y validación al castellano del cuestionario Pfeiffer (SPMSQ) para detectar la existencia de deterioro cognitivo en personas mayores de 65 años.
      ]. Values equal to or greater than 3 errors of a total of 10 questions, were considered as cognitive impairment. Finally, laboratory parameters such as blood count, biochemistry, total protein, albumin, vitamin D and C-reactive protein (CRP) were collected.
      Body mass index (BMI) and handgrip strength were measured in the first 72 h of admission. To calculate BMI, electronic records of weight and height from Primary Care (Horus System) were used. If not available, the last weight recorded by the patient or their relatives was used. Height was calculated using tables that estimate it according to the length of the ulna [
      • Martinez J.
      • Duenas R.
      • Onís M.C.
      • Aguado-Tabernea C.
      • Albert-Colmenerc
      • Luquec L.
      Adaptación y validación al castellano del cuestionario Pfeiffer (SPMSQ) para detectar la existencia de deterioro cognitivo en personas mayores de 65 años.
      ].
      Handgrip strength was measured in the dominant hand using a Jamar® hydraulic dynamometer (Sammons Preston, Bolingbrook, IL, USA), following the modified Southampton protocol [
      • Roberts H.C.
      • Denison H.J.
      • Martin H.J.
      • Patel H.P.
      • Syddall H.
      • Cooper C.
      • et al.
      A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardized approach.
      ]. Cutoff points were obtained from the measurement of handgrip strength in a sample of 1327 older people from the community, representative of the elderly population in the area [
      • Auyeung T.W.
      • Lee J.S.
      • Kwok T.
      • Leung P.C.
      • Woo J.
      Estimation of stature by measuring fibula and ulna bone length in 2443 older adults.
      ]. Within this sample, the median and interquartile range 25–75 were calculated. In this study, the 25th percentile (<23 kg and <13 kg in men and women respectively) was used as the cutoff point to classify patients. The two study groups were: 1) "low strength" if their strength was below this value, and 2) "high strength" if it was higher. Those patients who were unable to use the dynamometer were included in the low strength group.
      Twenty-four hours prior to discharge, variables related to hospital stay and discharge destination were collected. Deaths during hospitalization were also recorded.
      One year after the HF, patients or their relatives were contacted by phone to find out the vital and functional status (FAC) and the number of hospital readmissions.
      To determine the change in functional status, the variable "change in FAC" was created using the formula “baseline FAC minus FAC at 1 year”. According to this formula, patients were classified into the following groups: "major change" if the difference was >1, "moderate change" if the difference was 1 point and "no change" if the difference between baseline FAC and FAC at 1 year was 0 [
      • Castell M.V.
      • Sanchez M.
      • Julian R.
      • Queipo R.
      • Martín S.
      • Otero Á
      Frailty prevalence and slow walking speed in persons age 65 and older: implications for primary care.
      ].
      The Ethics and Clinical Research Committee at the University Hospital approved the completion of this study (HULP Code: PI:3201). Informed consent was obtained from each patient or relatives prior to inclusion.
      The normality of quantitative variables was analyzed using the Kolmogorov-Smirnov test; non-normality was accepted with p < 0.05. Quantitative variables that followed a normal distribution were presented as mean and standard deviation. Otherwise the median and interquartile range were used. For qualitative variable,s absolute and relative frequencies were calculated. All variables were compared between the two groups (high strength and low strength). To compare discrete variables, the chi-squared test (χ2) was used. When the expected value was less than 5 in one of the squares of the contingency table, Fisher's exact test was used. To analyze the association between dichotomous and continuous variables, Student’s t-test was used for Gaussian distributions and the Mann-Whitney U test was used for non-Gaussian distributions. Values ​​of p < 0.05 were considered statistically significant. The software used for statistical analysis was SPSS v21 (SPSS Inc., Chicago IL., USA.).

      3. Results

      During the study period 535 patients were admitted, of whom 26 (4.8 %) were excluded due to loss during follow-up, failure to give consent before inclusion or death. A total of 509 patients were included. Their characteristics are presented in Table 1; the mean age was 85.4 ± 0.3 years. Of these, 403 (79.2 %) were women, 295 (58.0 %) had suffered a pertrochanteric or subtrochanteric fracture, and 214 (42.0 %) a subcapital fracture.
      Table 1Characteristics of patients in the total sample. Data are expressed as mean ± standard deviation, median (interquartile range) or number (%).
      Total sample (n = 509)
      Age (years)85.4 ± 0.3
      Age> 80399 (78.4 %)
      Women403 (79.2 %)
      Fracture type:
      • -
        Per/subtrochanteric
      295 (58.0 %)
      • -
        Subcapital
      214 (42.0 %)
      Patients undergoing surgery491 (96.5 %)
      Type of surgery:
      • -
        Intramedullary nails and other
      307 (62.5 %)
      • -
        Prosthesis
      184 (37.5 %)
      Living in nursing homes116 (22.8 %)
      Functional ambulation category scale (baseline)
      • -
        0
      18 (3.5 %)
      • -
        1, 2, 3
      88 (17.3 %)
      • -
        4, 5
      403 (79.2 %)
      Baseline Barthel Index85 (65−95)
      Cruz Roja Mental scale ≥ 2 (baseline)165 (32.4 %)
      Barthel Index at admission10 (0−20)
      Pfeiffer Questionnaire ≥ 3289 (56.8 %)
      Cruz Roja Mental at admission ≥ 2204 (40.1 %)
      Anticoagulation240 (47.2 %)
      Modified Charlson index ≥ 3185 (36.3 %)
      Congestive heart failure67 (13.2 %)
      Coronary artery disease61 (12 %)
      Heart disease (any)195 (38.3 %)
      Cerebrovascular disease73 (14.3 %)
      Chronic lung disease46 (9 %)
      Renal disease140 (27.5 %)
      Diabetes119 (23.4 %)
      Cancer65 (12.8 %)
      Peripheral vascular disease15 (2.9 %)
      ASA score III, IV358 (70.3 %)
      Handgrip strength12 (6−16)
      Low handgrip strength ͣ339 (66.6 %)
      Body mass index (kg/m) <2299 (20.1 %)
      Haemoglobin (g/dL) <12 women/<13 men182 (35.8 %)
      C-reactive protein (mg/L)> 110160 (33.4 %)
      Total Protein (g/dL) <6.4127 (25.0 %)
      Albumin (g/dL) <3.5405 (80.5 %)
      Vitamin D (ng/mL) ≤21405 (79.6 %)
      Hospital stay (days)
      • -
        Total
      9 (7−12)
      • -
        Preoperative
      3 (2−4)
      Discharge destination
      • -
        Home
      125 (25.8 %)
      • -
        Residence/Nursing home
      131 (27.0 %)
      • -
        Functional recovery unit
      216 (44.5 %)
      • -
        Long-term unit and other
      13 (2.7 %)
      Exitus (intrahospital)24 (4.7 %)
      ASA, American Society of Anesthesiologists; ͣ low handgrip strength:<23 kg and <13 kg in men and women respectively.
      A total of 491 (96.5 %) patients underwent surgery, 202 (39,7 %) presented a subcapital fracture and 289 (56,8 %) presented pertrochanteric or subtrochanteric fracture. 184 (37.5 %) went surgery by placing prosthesis and 307 (62.5 %) by intramedullary nails or other. Eighteen patients (3.5 %) were not operated, 12 (66.7 %) presented subcapital HP and 6 (33,3 %) presented pertrochanteric or subtrochanteric fracture, all patient included in this last group died before surgery. Of the total sample, 116 (22.8 %) patients came from nursing homes.
      Eighteen (3.5 %) did not walk prior to HF (FAC 0), while 403 (79.2 %) did so independently (FAC 4, 5). Baseline cognitive impairment (CRM ≥ 2) was present in 165 (32.4 %) patients. The most frequent comorbidities and pathologies are also shown in Table 1; at the time of the HF, 240 (47.2 %) patients were on anticoagulant treatment, 185 (36.3 %) had a high Charlson comorbidity index and 358 (70.3 %) had a high surgical risk (scale ASA ≥ III).
      Regarding the laboratory variables, 405 (79.6 %) had ​​Vitamin D levels equal to or less than 21 ng/mL and 405 (80.5 %) had an albumin level of less than 3.5 g/dL.
      Median hospital stay was 9 days. At discharge, 125 (25.8 %) patients returned home, 131 (27.0 %) to nursing homes, 216 (44.5 %) to functional recovery units and 13 (2.7 %) to long-stay units or others. A total of 24 (4.7 %) patients died during acute hospitalization.
      Of the total sample, 447 (87.8 %) were able to use the dynamometer and execute the order. The remaining 62 patients were unable to perform the manoeuvre due to lack of understanding, cognitive impairment or an injury to the dominant hand. Three-hundred-thirty-nine (66.6 %) had low handgrip strength and 99 (20.1 %) had a BMI of less than 22 kg/m².
      The results of the bivariate analysis are shown in Table 2; Patients with low strength were older, more frequently institutionalized and had worse functional and cognitive status at both baseline and admission. They had a higher comorbidity index, increased surgical risk and lower body mass index. Furthermore, low strength values ​​were associated with lower haemoglobin and albumin levels. Finally, in-hospital mortality was higher in the group of patients with low strength, (22 (6.5 %) vs 2 (1.2 %) patients) in the high strength group.
      Table 2Patient characteristics presented as low or high strength at baseline and on admission. Data are expressed as medians (interquartile range) or number (%).
      Low grip strength n = 339 (66.6 %)High grip strength n = 170 (33.4 %)P
      Baseline
      Age > 80287 (84.7 %)112 (65.9 %)<0.001
      Women271 (79.9 %)132 (77.6 %)0.548
      Fracture type:
      • -
        Per/subtrochanteric
      198 (58.4 %)97 (57.1 %)0.771
      • -
        Subcapital
      141 (41.6 %)73 (42.9 %)
      Patients operated322 (95.0 %)169 (99.4 %)<0.01
      Type of surgery:
      • -
        Intramedullary nails and other
      200 (62.1 %)107 (63.3 %)0.794
      • -
        Prosthesis
      122 (37.9 %)62 (36.7 %)
      Previously institutionalized96 (28.3 %)20 (11.8 %)<0.001
      Functional ambulation category scale
      • -
        0
      18 (5.3 %)0 (0.0 %)<0.001
      • -
        1, 2, 3
      76 (22.4 %)12 (7.1 %)
      • -
        4,5
      245 (72.3 %)158 (92.9 %)
      Barthel Index80 (55–91.25)95 (85−100)<0.01
      Cruz Roja mental scale ≥2146 (43.1 %)19 (11.2 %)<0.001
      Hospitalization
      Barthel Index5 (0−15)20 (5−30)<0.01
      Pfeiffer Questionnaire ≥3232 (68.4 %)57 (33.5 %)<0.001
      Cruz Roja mental scale ≥2177 (52.2 %)27 (15.9 %)<0.001
      Modified Charlson index ≥3150 (44.2 %)35 (20.6 %)<0.001
      Score ASA III, IV272 (80.2 %)86 (50.6 %)<0.001
      Body mass index (kg/m) <2278 (24.0 %)21 (12.5 %)<0.01
      Hemoglobin (g/dL) <12 women/<13 men136 (40.1 %)46 (27.1 %)<0.01
      C-reactive proteine (mg/L)> 110115 (36.4 %)45 (27.6 %)0,053
      Total Protein (g/dL) <6.492 (27.1 %)35 (20.6 %)0,107
      Albumin (g/dL) <3.5285 (85.3 %)120 (71.0 %)<0.001
      Vitamin D (ng/mL) ≤21269 (79.4 %)136 (80.0 %)0.864
      Hospital stay (days)
      • -
        Total
      9 (8−12)9 (7−12)0.794
      • -
        Preoperative
      3 (2−4)3 (2−4)0.838
      Discharge destination
      • -
        Home
      66 (20.8 %)59 (35.1 %)<0.001
      • -
        Nursing home
      105 (33.1 %)26 (15.5 %)
      • -
        Functional recovery unit
      135 (42.6 %)81 (48.2 %)
      • -
        Long-term unit and other
      11 (3.5 %)2 (1.2 %)
      Exitus (in-hospital)22 (6.5 %)2 (1.2 %)<0.01
      At 1-year follow-up
      Functional ambulation category scale
      • -
        0
      48 (20.7 %)10 (6.7 %)<0.001
      • -
        1, 2, 3
      59 (25.4 %)16 (10.7 %)
      • -
        4, 5
      125 (53.9 %)123 (82.6 %)
      Readmissions65 (26.5 %)30 (20.8 %)0,207
      Exitus103 (30.4 %)15 (8.8 %)<0.001
      ASA, American Society of Anesthesiologists.
      At one year, 58 (15.2 %) patients did not walk, and 248 (65.1 %) did so independently. Ninety-five (24.4 %) patients were readmitted during the follow-up period and 118 (23.2 %) had died. Those with low strength had a poorer functional status and higher mortality 12 months after the HF. There were no differences in the number of readmissions.
      Table 3 shows that patients younger than 90 years who had lower handgrip strength, had a major change in FAC compared with those with high handgrip strength. On the contrary, patients older than 90 did not show a significant association between low handgrip strength and change in FAC at 1 year after a HF. Furthermore, an association between lower handgrip strength and mortality was found in those younger than 90 years, whereas it presented a statistical trend in patients age 91 or over.
      Table 3Age-adjusted Change in FAC at 1 year grouped into 2 categories (no change and mild change vs major change), according to handgrip strength.
      AgeStrengthNo/Mild Change in FAC n (%)Major Change in FAC n (%)pORAliveDeceasedpOR
      < = 80High50 (94 %)3 (6 %)0.015.38 IC (1.32−21.07)54 (93.1 %)4 (6.9 %)0.033.6 IC (1.1−12.2)
      Low31 (75 %)10 (24 %)41 (78.8 %)11 (21.2 %)
      81−90High73 (90 %)8 (10 %)0.0013.63 IC (1.59−8.27)85 (90.4 %)9 (9.6 %)0.004.0 IC (1.9−8.5)
      Low93 (72 %)37 (28 %)132 (70.2 %)56 (29.8 %)
      > = 91High11 (73 %)4 (27 %)0.516 (88.9 %)2 (11.1 %)0044.6 IC (0.9−21)
      Low39 (64 %)22 (36 %)63 (63.6 %)36 (36.4 %)
      FAC, Functional Ambulation Category Scale.
      Fig. 1 summarizes the differences in FAC between the low and high strength groups, both at baseline and at one year.
      Fig. 1
      Fig. 1Differences between baseline FAC (Functional Ambulation Category Scale) and at 1-year follow up. FAC in patients with low and high handgrip strength. Data are expressed in percentages (%).
      Regarding the change in mobility (Fig. 2), a major change was observed in 69 (32.7 %) of patients with low strength versus 15 (10.9 %) of patients with high strength.
      Fig. 2
      Fig. 2Change in the FAC (Functional Ambulation Category Scale) between baseline and the situation at 1-year follow up in patients with low and high handgrip strength. (P < 0.001). Major change: baseline FAC minus 1-year follow up FAC > 1. Mild change: baseline FAC minus 1-year follow up FAC < 1. No change: baseline FAC minutes 1-year follow up FAC = 0.

      4. Discussion

      The aim of this study was to determine if handgrip strength values are predictors of functional status, hospital readmissions and one-year mortality in elderly patients with HF. The results showed that handgrip strength is useful in predicting gait impairment and mortality but does not predict an increase in hospital readmissions.
      Although a high proportion of patients had cognitive impairment, the vast majority (87.8 %) were able to understand the use of the dynamometer used to asses handgrip strength, which supports the applicability of this measurement in hospitalized elderly patients.
      Patients with low handgrip strength had a worse state of health both at baseline and at admission. This result concurs with those from other authors who reported that lower handgrip strength values were ​​associated with being older, baseline functional and cognitive disability, incontinence and other comorbidities [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Neira Alvarez M.
      • López-Dóriga P.
      • Thuissard I.J.
      • Sanz-Rosa D.
      • Arias Muñana E.
      • Bielza Galindo R.
      • et al.
      Grip strength and functional recovery after hip fracture: an observational study in elderly population.
      ,
      • Beloosesky Y.
      • Weiss A.
      • Manasian M.
      • Salai M.
      Handgrip strength of the elderly after hip fracture repair correlates with functional outcome.
      ]. We found no association between handgrip strength and sex, described previously [
      • Neira Alvarez M.
      • López-Dóriga P.
      • Thuissard I.J.
      • Sanz-Rosa D.
      • Arias Muñana E.
      • Bielza Galindo R.
      • et al.
      Grip strength and functional recovery after hip fracture: an observational study in elderly population.
      ,
      • Beloosesky Y.
      • Weiss A.
      • Manasian M.
      • Salai M.
      Handgrip strength of the elderly after hip fracture repair correlates with functional outcome.
      ], nor between handgrip strength and vitamin D levels, as reported by others [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Ríos-Germán P.P.
      • Menéndez-Colino R.
      • Ramírez-Martín R.
      • Alarcon T.
      • Queipo R.
      • Otero Puime A.
      • et al.
      Baseline and 1-year follow-up differences between hip-fracture patients admitted from nursing homes and the community. A cohort study on 509 consecutive patients (FONDA Cohort).
      ].
      An association between lower handgrip strength and greater one-year functional impairment after HF was found. According to published studies, strength predicts functional recovery in elderly patients with HF [
      • Savino E.
      • Martini E.
      • Lauretani F.
      • Pioli G.
      • Zagatti A.M.
      • Frondini C.
      • et al.
      Handgrip strength predicts recovery after persistent walking hip fracture surgery.
      ,
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Di Monaco R.
      Handgrip strength but not appendicular lean mass is an independent predictor of functional outcome in hip fracture women: a prospective study short-term.
      ,
      • Neira Alvarez M.
      • López-Dóriga P.
      • Thuissard I.J.
      • Sanz-Rosa D.
      • Arias Muñana E.
      • Bielza Galindo R.
      • et al.
      Grip strength and functional recovery after hip fracture: an observational study in elderly population.
      ] as well as functional status at discharge and in the medium-term [
      • Di Monaco M.
      • Castiglioni C.
      • De Toma E.
      • Gardin L.
      • Giordano S.
      • Tappero R.
      Handgrip strength is an independent predictor of functional outcome in hip fracture women: a prospective study with 6-month follow-up.
      ,
      • Beloosesky Y.
      • Weiss A.
      • Manasian M.
      • Salai M.
      Handgrip strength of the elderly after hip fracture repair correlates with functional outcome.
      ]. Lower handgrip strength was also associated with a longer hospital stay in patients with hip arthroplasty [
      • Gumieiro D.
      • Murino Rafacho B.P.
      • Buzati Pereira B.L.
      • Cavallari K.A.
      • Tanni S.E.
      • Azevedo P.S.
      • et al.
      Vitamin D serum levels are associated with handgrip strength but not with muscle mass or length of hospital stay after hip fracture.
      ], an association not found in our study.
      Association between lower handgrip strength values ​at ​admission and increased long-term mortality was also found after HF. This factor is scarcely studied in the literature and as far as we know, it has only been described in the studies from Meyer et al. (2000) [
      • Meyer H.E.
      • Tverdal A.
      • Falch J.A.
      • Pedersen J.I.
      Factors associated with mortality after hip fracture.
      ], in which follow-up was maintained for 3.5 years, and Duchowny (2018) [
      • Shyam Kumar A.J.
      • Beresford-Cleary N.
      • Kumar P.
      • Barai A.
      • Vasukutty N.
      • Yasin S.
      • et al.
      Preoperative grip strength measurement and duration of hospital stay in patients undergoing total hip and knee arthroplasty.
      ], which had a median follow-up of 8 years. We found a statistical trend between handgrip strength and mortality in HF patients who were older than 91 years. To the best of our knowledge, these findings have not yet been described.
      An association between low handgrip strength and higher mortality in the general population without HF has been described, as well as mortality due to cardiovascular and other causes [
      • Duchowny K.
      Do nationally representative cutpoints for clinical muscle weakness predict mortality? Results from nine years of follow-up in the health and retirement study.
      ,
      • Rantanen T.
      • Harris T.
      • Leveille S.G.
      • Visser M.
      • Foley D.
      • Masaki K.
      • et al.
      Muscle strength and body mass index as predictors of long-term mortality in men initially healthy.
      ,
      • Rantanen T.
      • Volpato S.
      • Ferrucci L.
      • Heikkinen E.
      • Fried L.P.
      • Guralnik J.M.
      Handgrip strength and cause-specific mortality in older and all disabled women.
      ,
      • Gale C.R.
      • Martyn C.N.
      • Cooper C.
      • Sayer A.A.
      Grip strength, body composition, and mortality.
      [
      • Bohannon R.W.
      Hand-grip dynamometry predicts future outcomes in aging adults.
      ],
      • Leong D.P.
      • Teo K.K.
      • Rangarajan S.
      • Lopez-Jaramillo P.
      • Avezum Jr., A.
      • Orlandini A.
      • et al.
      Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study.
      ,
      • Von Haehling S.
      • Morley J.E.
      • Coats A.J.S.
      • Anker S.D.
      Ethical guidelines for publishing in the Journal of Cachexia, sarcopenia and Muscle: update 2017.
      ].
      Among the strengths of this study, we highlight the high number of cases included; most of the studies published to date included few patients with HF, generally less than 200 patients. We consider that our study included all HFs that occurred during one year in an area of ​​approximately 520,000 inhabitants, as the hospital in which data is collected is the only public hospital in this area that admits patients with HF and they usually do not go to private centres. Furthermore, no exclusion criteria were established, as has been done in other studies. The cutoff point used to categorize low handgrip strength was taken from a population study carried out in 1327 older patients living in the same catchment area as the patients in this study [
      • Castell M.V.
      • Sanchez M.
      • Julian R.
      • Queipo R.
      • Martín S.
      • Otero Á
      Frailty prevalence and slow walking speed in persons age 65 and older: implications for primary care.
      ]. Another strength is the application of a comprehensive assessment of patients in which clinical, functional and laboratory variables were included. In addition, a one-year follow-up was carried out in which functional variables, readmissions and mortality rate were collected. Finally, the loss rate during the follow-up period was very low in this study.
      Among the limitations of this work, we cannot exclude the presence of confounding factors that may affect results. The aim of this work was to study long-term evolution in elderly patients with HF, so no short-medium term data were collected. Functional status measured with the FAC scale, hospital readmission and mortality rates were collected after one year of follow up. No other variables that could also have provided information on the clinical course of these patients were collected.
      In conclusion, the results of this study show that lower handgrip strength in elderly patients with HF predicts a three times increased risk of long-term mortality and greater functional disability. However, these patients, do not require a significant number of hospital readmissions.

      Contributors

      Patricia Pérez-Rodríguez conceived, designed and performed the published work, interpreted the data, and drafted the paper.
      Laura Rabes-Rodríguez conceived, designed and performed the published work, interpreted the data, and drafted the paper.
      Carmen Sáez-Nieto conceived, designed and performed the published work, interpreted the data, and drafted the paper.
      Teresa Alarcón Alarcón conceived, designed and performed the published work, interpreted the data, and drafted the paper.
      Rocío Queipo analyzed and interpreted the data.
      Ángel Otero-Puime analyzed and interpreted the data.
      J. I. Gonzalez Montalvo conceived, designed and performed the published work, interpreted the data, and drafted the paper.

      Conflict of interest

      The authors declare that they have no conflict of interest.

      Funding

      No external funding was received for this study.

      Ethical approval

      The Ethics and Clinical Research Committee at the University Hospital approved the completion of this study (HULP Code: PI:3201). Informed consent was obtained from each patient or relatives prior to inclusion.

      Provenance and peer review

      This article was not commissioned and was externally peer reviewed.

      Research data (data sharing and collaboration)

      There are no linked research data sets for this paper. Data will be made available on request.

      Appendix A. Supplementary data

      The following is Supplementary data to this article:

      References

        • Meyer H.E.
        • Tverdal A.
        • Falch J.A.
        • Pedersen J.I.
        Factors associated with mortality after hip fracture.
        Osteoporos. Int. 2000; 11: 228-232
        • Hernlund E.
        • Svedbom A.
        • Ivergård M.
        • Compston J.
        • Cooper C.
        • Stenmark J.
        • et al.
        Osteoporosis in the European Union: medical management, epidemiology and economic burden: a report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA).
        Arch. Osteoporos. 2013; 8: 136
        • Singer A.
        • Exuzides A.
        • Spangler L.
        • O´Malley C.
        • Colby C.
        • Johnston K.
        • et al.
        Burden of illness for osteoporotic fractures compared with other serious diseases among postmenopausal women in the United States.
        Mayo Clin. Proc. 2015; 90: 53-62
        • Menant J.C.
        • Weber F.
        • Lo J.
        • Sturnieks D.L.
        • Close J.C.
        • Sachdev P.S.
        • et al.
        Strength measures are better than muscle measures in predicting health-related outcomes in older people mass: time to abandon the term sarcopenia?.
        Osteoporos. Int. 2016; 28: 59-70
        • Roberts H.C.
        • Denison H.J.
        • Martin H.J.
        • Patel H.P.
        • Syddall H.
        • Cooper C.
        • et al.
        A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardized approach.
        Age Aging. 2011; 40: 423-429
        • Denk K.
        • Lennon S.
        • Gordon S.
        • Jaarsma R.L.
        The association between decreased hand grip strength and hip fracture in older people: a systematic review.
        Exp. Gerontol. 2018; 1: 1-9
        • Davies C.W.
        • Jones D.M.
        • Shearer J.R.
        Hand grip - a simple test for morbidity after fracture of the neck of femur.
        JR Soc Med. 1984; 77: 833-836
        • Gumieiro D.
        • Rafacho B.P.
        • Gradella L.M.
        • Azevedo P.S.
        • Gaspardo D.
        • Zornoff L.A.
        • et al.
        Handgrip strength predicts patients with pressure ulcers in hip fractures.
        Nutrition. 2012; 28: 874-878
        • Savino E.
        • Martini E.
        • Lauretani F.
        • Pioli G.
        • Zagatti A.M.
        • Frondini C.
        • et al.
        Handgrip strength predicts recovery after persistent walking hip fracture surgery.
        Am. J. Med. 2013; 126: 1068-1075
        • Di Monaco M.
        • Castiglioni C.
        • De Toma E.
        • Gardin L.
        • Giordano S.
        • Di Monaco R.
        Handgrip strength but not appendicular lean mass is an independent predictor of functional outcome in hip fracture women: a prospective study short-term.
        Arch. Phys. Med. Rehabil. 2014; 95: 1719-1724
        • Di Monaco M.
        • Castiglioni C.
        • De Toma E.
        • Gardin L.
        • Giordano S.
        • Tappero R.
        Handgrip strength is an independent predictor of functional outcome in hip fracture women: a prospective study with 6-month follow-up.
        Medicine. 2015; 94: 1-6
        • Neira Alvarez M.
        • López-Dóriga P.
        • Thuissard I.J.
        • Sanz-Rosa D.
        • Arias Muñana E.
        • Bielza Galindo R.
        • et al.
        Grip strength and functional recovery after hip fracture: an observational study in elderly population.
        Eur. Geriatr. Med. 2016; 7: 556-560
        • Steihaug O.M.
        • Gjesdal C.G.
        • Bogen B.
        • Kristoffersen M.H.
        • Lien G.
        • Hufhammer K.O.
        • et al.
        Does sarcopenia predict change in mobility after hip fracture? Observational multicenter Study with a one-year follow-up.
        BMC Geriatr. 2018; 18: 1-10
        • Beloosesky Y.
        • Weiss A.
        • Manasian M.
        • Salai M.
        Handgrip strength of the elderly after hip fracture repair correlates with functional outcome.
        Disabil. Rehabil. 2010; 32: 367-373
        • Gonzalez-Montalvo J.I.
        • Alarcón T.
        • Gotor-Pérez P.
        • Martín-Maestre I.
        ¿Es posible mejorar la atención al paciente con fractura de cadera? Aportaciones del programa FONDA.
        in: Sáez López P. Valverde García J.A. Sánchez Fernández N. Tercera Actualización En Ortogeriatría. 3rd ed. MC Graphics Solutions, Ávila2016: 102-129
        • Holden M.K.
        • Gill K.M.
        • Magliozzi M.R.
        • Nathan J.
        • Piehl-Baker L.
        Clinical gait assessment in the neurologically impaired. Reliability and meaningfulness.
        Phys. Ther. 1984; 64: 35-40
        • Cabañero-Martinez M.J.
        • Cabrero-Garcia J.
        • Richart-Martinez M.
        • Muñoz-Mendoza C.L.
        The Spanish versions of the Barthel index (BI) and the Katz index (KI) of activities of daily living (ADL): a structured review.
        Arch. Gerontol. Geriatr. 2009; 49: e77-e84
        • Gonzalez-Montalvo J.I.
        • Rodríguez-Mañas L.
        • Ruipérez-Cantera I.
        Validación del cuestionario Pfeiffer y la escala de incapacidad mental de la Cruz Roja en la detección del deterioro mental en los pacientes externos de un servicio de geriatría.
        Rev. Esp. Geriatr. Gerontol. 1992; 27: 129-133
        • Martinez J.
        • Duenas R.
        • Onís M.C.
        • Aguado-Tabernea C.
        • Albert-Colmenerc
        • Luquec L.
        Adaptación y validación al castellano del cuestionario Pfeiffer (SPMSQ) para detectar la existencia de deterioro cognitivo en personas mayores de 65 años.
        Clin. Med. 2011; 117: 129-134
        • Auyeung T.W.
        • Lee J.S.
        • Kwok T.
        • Leung P.C.
        • Woo J.
        Estimation of stature by measuring fibula and ulna bone length in 2443 older adults.
        J. Nutr. Health Aging. 2009; 13: 931-936
        • Castell M.V.
        • Sanchez M.
        • Julian R.
        • Queipo R.
        • Martín S.
        • Otero Á
        Frailty prevalence and slow walking speed in persons age 65 and older: implications for primary care.
        BMC Fam. Pract. 2013; 14: 86
        • Ríos-Germán P.P.
        • Menéndez-Colino R.
        • Ramírez-Martín R.
        • Alarcon T.
        • Queipo R.
        • Otero Puime A.
        • et al.
        Baseline and 1-year follow-up differences between hip-fracture patients admitted from nursing homes and the community. A cohort study on 509 consecutive patients (FONDA Cohort).
        Rev. Esp. Geriatr. Gerontol. 2019; 54: 207-213
        • Gumieiro D.
        • Murino Rafacho B.P.
        • Buzati Pereira B.L.
        • Cavallari K.A.
        • Tanni S.E.
        • Azevedo P.S.
        • et al.
        Vitamin D serum levels are associated with handgrip strength but not with muscle mass or length of hospital stay after hip fracture.
        Nutrition. 2015; 31: 931-934
        • Shyam Kumar A.J.
        • Beresford-Cleary N.
        • Kumar P.
        • Barai A.
        • Vasukutty N.
        • Yasin S.
        • et al.
        Preoperative grip strength measurement and duration of hospital stay in patients undergoing total hip and knee arthroplasty.
        Eur. J. Orthop. Surg. Traumatol. 2013; 23: 553-556
        • Duchowny K.
        Do nationally representative cutpoints for clinical muscle weakness predict mortality? Results from nine years of follow-up in the health and retirement study.
        J. Gerontol. A Biol. Sci. 2018; : gly169
        • Rantanen T.
        • Harris T.
        • Leveille S.G.
        • Visser M.
        • Foley D.
        • Masaki K.
        • et al.
        Muscle strength and body mass index as predictors of long-term mortality in men initially healthy.
        J. Gerontol. Med. Sci. 2000; 55: M168-173
        • Rantanen T.
        • Volpato S.
        • Ferrucci L.
        • Heikkinen E.
        • Fried L.P.
        • Guralnik J.M.
        Handgrip strength and cause-specific mortality in older and all disabled women.
        J. Am. Geriatr. Soc. 2003; 51: 636-641
        • Gale C.R.
        • Martyn C.N.
        • Cooper C.
        • Sayer A.A.
        Grip strength, body composition, and mortality.
        Int. J. Epidemiol. 2007; 36: 228-235
        • Bohannon R.W.
        Hand-grip dynamometry predicts future outcomes in aging adults.
        J. Geriatr. Phys. Ther. 2008; 31: 3-10
        • Leong D.P.
        • Teo K.K.
        • Rangarajan S.
        • Lopez-Jaramillo P.
        • Avezum Jr., A.
        • Orlandini A.
        • et al.
        Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study.
        Lancet. 2015; 386: 266-273
        • Von Haehling S.
        • Morley J.E.
        • Coats A.J.S.
        • Anker S.D.
        Ethical guidelines for publishing in the Journal of Cachexia, sarcopenia and Muscle: update 2017.
        J. Cachexia Sarcopenia Muscle. 2017; 8: 1081-1083