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Article

Grip Strength in Patients with Gastrointestinal Diseases

1
The Second Department of Internal Medicine, Osaka Medical and Pharmaceutical University, Takatsuki 569-8686, Japan
2
The Premier Departmental Research of Medicine, Osaka Medical and Pharmaceutical University, Takatsuki 569-8686, Japan
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
J. Clin. Med. 2022, 11(8), 2079; https://doi.org/10.3390/jcm11082079
Submission received: 10 February 2022 / Revised: 31 March 2022 / Accepted: 5 April 2022 / Published: 7 April 2022
(This article belongs to the Section Gastroenterology & Hepatopancreatobiliary Medicine)

Abstract

:
We sought to elucidate factors contributing to the grip strength (GS) decline in patients with gastrointestinal diseases (Ga-Ds, n = 602, 379 males, median age = 72 years). The GS decline in males and females was defined as <28 kg and <18 kg, respectively, following the current Asian guidelines. The median GS (male) was 28.8 kg, and GS decline (male) was found in 169 patients (44.6%). The median GS (female) was 17.5 kg, and GS decline (female) was found in 122 patients (54.7%). Advanced cancer was identified in 145 patients (24.1%). In terms of the univariate analysis of parameters of the GS decline, age (p < 0.0001), gender (p = 0.0181), body mass index (BMI, p = 0.0002), ECOG-PS (p < 0.0001), SARC-F score (p < 0.0001), hemoglobin value (p < 0.0001), total lymphocyte count (p < 0.0001), serum albumin value (p < 0.0001), C reactive protein (CRP) value (p < 0.0001), and estimated glomerular filtration rate were statistically significant. In terms of the multivariate analysis, age (p < 0.0001), BMI (p = 0.0223), hemoglobin value (p = 0.0186), serum albumin value (p = 0.0284), the SARC-F score (p = 0.0003), and CRP value (p < 0.0001) were independent parameters. In conclusion, the GS decline in patients with Ga-Ds is closely associated with not only the primary factor (i.e., aging) but also secondary factors such as inflammatory factors and nutritional factors.

1. Introduction

Skeletal muscle, besides controlling body movement, functions as a store of protein and has an essential role in glucose uptake and energy metabolism [1,2]. Sarcopenia is characterized by progressive skeletal muscle mass loss and decline in function, linking to physical frailty and survival [1,2,3]. Malnutritional status, inactivity, advanced cancer burden, and persistent inflammatory state often seen in gastrointestinal diseases (Ga-Ds) are common features for sarcopenia [1,2,3,4,5,6,7,8,9,10]. Loss of dietary intakes and worsening of nutritional condition can be also frequently encountered in patients with Ga-Ds [9], and sarcopenia in patients with Ga-Ds is associated with decreased quality of life (QOL) and adverse outcomes [9,11]. Ga-D is a typical disease that causes secondary sarcopenia owing to the disease burden itself [11].
In recent years, a lot of studies have presented that grip strength (GS) is related to the onset of disease and life expectancy [12,13,14,15]. The results of a study in the UK that examined the relationship between GS, disease onset, and mortality were reported [16]. The study included 502,293 people aged 40–69 years, classified into four categories based on the baseline GS, and examined the relationship between GS and overall survival, cardiovascular disease-related survival, respiratory disease-related survival, and cancer-related survival [16]. The results showed that for every 5 kg decrease in GS, overall mortality increased by 20%, cardiovascular disease mortality increased by 19%, respiratory disease mortality increased by 31%, cancer mortality increased by 17%, and this relationship was particularly strong among young people [16]. In addition, the incidence and mortality rates of cardiovascular diseases, respiratory diseases, and cancers were all higher in people with GS of less than 26 kg in men and less than 16 kg in women. In other words, lower GS was as likely an indicator of future disease development and mortality as higher blood pressure and obesity, which are well-accepted prognostic markers [16].
The progression of muscle strength decline is usually accompanied by various metabolic changes [8]. As far as we are aware, however, there have been few reports with regard to factors contributing to the GS decline in patients with Ga-Ds. These problems may deserve to be solved, which urged us to conduct the current cross-sectional analysis.

2. Patients and Methods

2.1. Patients

In our hospital, between October 2020 and October 2021, 602 Japanese Ga-D hospitalized patients with data for GS were identified. In our hospital, GS has been routinely tested in each patient on admission, and sarcopenia risk was assessed according to the SARC-F. SARC-F is recommended for active use as an initial screening method for sarcopenia in the current globally accepted guidelines [17,18]. SARC-F is taken from S for Strength, A for Assistance walking, R for Rising from chair, C for Climbing stairs, and F for Falls, and each is rated on a scale of 0 to 2, with the total score being calculated [19,20,21,22]. In the Asian guidelines for sarcopenia, the recommended reference value of the SARC-F score for the presence of sarcopenia is 4 [17]. As a rule, each inpatient was required to be included in the SARC-F questionnaire on admission. GS was tested according to the guidelines [8]. In brief, the average of the left and right GS was used. The GS decline in male and female was defined as <28 kg and <18 kg, respectively, following the international guidelines [17].

2.2. Study Procedure and Ethics

First, the relevance between the GS decline and baseline characteristics was investigated. Next, univariate and multivariate analyses of the GS decline were carried out. Finally, receiver operating characteristic curve (ROC) analysis of the GS decline was enforced. Advanced cancer was defined as stage III or far advanced cancer. The study was retrospective in design, approved by the relevant institutional ethics committee (approval number, 2021-122), and conducted in accordance with the Declaration of Helsinki. As this study was a retrospective observational study, patients’ consent was waived.

2.3. Statistics

For the comparison between two groups of continuous variables, the most appropriate choice between the Student’s t test and the Mann–Whitney U test was selected after confirmation of distribution. Continuous variables were presented as median (interquartile range, IQR) unless otherwise mentioned. In between-group comparisons of nominal variables, the Pearson χ2 test was utilized. In the univariate analysis, effect size was also presented. Multivariate logistic regression analysis for the GS decline was also conducted to choose independent parameters considering significant parameters in the univariate analysis. ROC analysis for calculating the area under the ROC (AUC) was also done, and the reference value was set up as the point at which the sum of sensitivity and specificity is maximized. A p value less than 0.05 was the significant level in this study according to the JMP ver. 15 (SAS Institute Inc., Cary, NC, USA).

3. Results

3.1. Patient Baseline Features

Table 1 presents baseline features of all study subjects (n = 602, 379 males and 223 females, median (IQR) age = 72 (64–79) years). The median (IQR) GS in males was 28.8 (23.6–34.3) kg, and GS decline in males (i.e., <28 kg) was found in 169 patients (44.6%). The median (IQR) GS in females was 17.5 (13.9–20.5) kg, and GS decline in females (i.e., <18 kg) was found in 122 patients (54.7%). The median (IQR) body mass index (BMI) was 21.9 (19.6–24.4) kg/m2 (missing data, n = 2). The median (IQR) ECOG-PS was 0 (0–1). EOCG-PS 0 was found in 399 patients (66.3%), 1 in 108 (17.9%), 2 in 40 (6.6%), 3 in 38 (6.3%) and 4 in 17 (2.8%). The median (IQR) SARC-F score was 0 (0–2). There were 345 cases (57.3%) with a SARC-F score of 0, 99 (16.4%) with a score of 1, 52 (8.6%) with a score of 2, 33 (5.5%) with a score of 3, and 73 (12.1%) with a score of ≥4. Upper gastrointestinal disease (U-GD) was seen in 149 patients (advanced cancer, 37 cases (24.8%)), lower gastrointestinal disease (L-GD) in 156 (advanced cancer, 28 cases (18.0%)), biliary and pancreatic disease (BP-D) in 209 (advanced cancer, 54 cases (25.8%)), and liver disease (L-D) in 88 (advanced cancer, 26 cases (29.6%)). Overall, advanced cancer was identified in 145 patients (24.1%). Other than advanced cancer, diseases seen in patients included early-stage cancer and benign diseases such as chronic inflammatory disease, benign tumor, and infectious disease.

3.2. GS Decline and ECOG-PS and BMI

In patients with ECOG-PS 0 (n = 399), 1 (n = 108), and ≥2 (n = 95), the percentage of GS decline was 35.3% (141/399), 63.9% (69/108), 85.3% (81/95) (p < 0.0001 in ECOG-PS 0 vs. 1, p < 0.0001 in ECOG-PS 0 vs. ≥2, p = 0.0007 in ECOG-PS 1 vs. ≥2, and overall p < 0.0001) (Figure 1A).
BMI (kg/m2) was classified into three groups (BMI (kg/m2) < 18.5, 18.5 < BMI (kg/m2) < 25, and BMI (kg/m2) > 25) based on the current guidelines in the Japanese Society for the Study of Obesity (JASSO) [23]. In patients with BMI (kg/m2) < 18.5 (n = 96), 18.5 < BMI (kg/m2) < 25 (n = 386), BMI (kg/m2) > 25 (n = 118), the percentage of GS decline was 62.5% (60/96), 48.5% (187/386), 36.4% (43/118) (p = 0.0164 in BMI (kg/m2) < 18.5 vs. 18.5 < BMI (kg/m2) < 25, p = 0.0264 in 18.5 < BMI (kg/m2) < 25 vs. BMI (kg/m2) > 25, p = 0.0002 in BMI (kg/m2) < 18.5 vs. BMI (kg/m2) > 25, and overall p = 0.0007) (Figure 1B).

3.3. GS Decline and the SARC-F Score

The median (IQR) SARC-F score in patients with GS decline (n = 291) and without GS decline (n = 311) was 1 (0–3) and 0 (0–0) (p < 0.0001, Figure 2A). The percentage of patients with a SARC-F score ≥ 4 in patients with and without GS decline was 21.7% (63/291) and 3.2% (10/311) (p < 0.0001, Figure 2B).

3.4. GS Decline According to the Primary Origin of the Disease

The percentage of GS decline in patients with U-GD, L-GD, BP-D, and L-D was 53.7% (80/149) in U-GD, 39.7% (62/156) in L-GD, 49.3% (103/209) in BP-D, and 52.3% (46/88) in L-D (overall p = 0.0737).

3.5. GS Decline and the SARC-F Score in Patients with and without Advanced Cancer

In patients with advanced cancer (n = 145), the median (IQR) SARC-F score in patients with GS decline (n = 74) and without GS decline (n = 71) was 2 (1–4) and 0 (0–1) (p < 0.0001, Figure 3A). The percentage of patients with a SARC-F score ≥ 4 in patients with and without GS decline was 27.0% (20/74) and 8.5% (6/71) (p = 0.0045, Figure 3B).
In patients without advanced cancer (n = 457), the median (IQR) SARC-F score in patients with GS decline (n = 217) and without GS decline (n = 240) was 1 (0–3) and 0 (0–0) (p < 0.0001, Figure 3C). The percentage of patients with a SARC-F score ≥ 4 in patients with and without GS decline was 19.8% (43/217) and 1.7% (4/240) (p < 0.0001, Figure 3D).

3.6. GS Decline According to the Primary Disease Site in Patients with and without Advanced Cancer

Among four categories of primary origin in patients with advanced cancer, no significant difference was seen in the percentage of GS decline (62.2% (23/37) in U-GD, 32.1% (9/28) in L-GD, 53.7% (29/54) in BP-D, 50.0% (13/26) in L-D, overall p = 0.1117).
Among four categories of primary origin in patients without advanced cancer, no significant difference was seen in the percentage of GS decline (50.9% (57/112) in U-GD, 41.4% (53/128) in L-GD, 47.7% (74/155) in BP-D, 53.2% (33/62) in L-D, overall p = 0.3558).

3.7. Uni- and Multivariate Analysis of Variables for the GS Decline

In the univariate analysis of variables for the GS decline, age (p < 0.0001), gender (p = 0.0181), BMI (p = 0.0002), ECOG-PS (p < 0.0001), SARC-F score (p < 0.0001), hemoglobin value (p < 0.0001), total lymphocyte count (p < 0.0001), serum albumin value (p < 0.0001), C reactive protein (CRP) value (p < 0.0001), and estimated glomerular filtration rate were statistically significant (Table 2). In the multivariate analysis, age (p < 0.0001), BMI (p = 0.0223), hemoglobin value (p = 0.0186), serum albumin value (p = 0.0284), the SARC-F score (p = 0.0003), and CRP value (p < 0.0001) were independent parameters of the GS decline (Table 3). Table 3 involves hazard ratio and 95% confidence interval in each factor.

3.8. ROC Analysis of Independent Parameters for the GS Decline

ROC analysis of independent factors in the multivariate analysis for GS decline was performed. AUC, the sensitivity, the specificity, and optimal reference value in each factor are demonstrated in Table 4. Age had the highest AUC for the GS decline (AUC = 0.74), followed by the SARC-F score (AUC = 0.73). The optimal reference value of the SARC-F score was 1, but when the reference value of the SARC-F score was changed to 4 (recommended reference value in the Asian guidelines), the sensitivity and specificity was 21.7% and 96.8%.

4. Discussion

Skeletal muscle mass and strength decrease from middle age to old age. Research related to sarcopenia has been progressing rapidly around the world in recent years. New evidence is also emerging on drug interventions for sarcopenia [24,25]. While in the COVID-19 pandemic, muscle strength decline is a serious concern due to decreased physical activity in daily life [26]. Many studies have shown that GS is related to the overall strength of the whole body, and GS decline is associated with decreased physical activity and adverse prognosis [12,13,14,15,27]. In our previous study, decreased GS was an independent adverse predictor for overall survival in patients with chronic liver disease (n = 1624) [27]. However, to our knowledge, few reports have addressed the contributing factors for GS decline in patients with Ga-Ds. To clarify these issues appears to be clinically meaningful. A large cohort (n = 602) is a major strength in the current analysis.
In our results, older age, lower BMI, lower hemoglobin, lower serum albumin, higher SARC-F score, and higher CRP level were independent factors for the GS decline in our multivariate analysis. These results imply that the GS decline in Ga-Ds is closely associated with not only the primary factor (i.e., aging) but also secondary factors such as inflammatory factor and nutritional factor. SARC-F involves strength (S, “How difficult is it to lift or carry an object weighing around 4.5 kg?”) [19,20], and thus it is not so surprising that the SARC-F score was an independent parameter of the GS decline. Advanced cancer and primary site of disease were not independent factors for the GS decline. The location of the primary lesion and the degree of disease progression do not seem to be directly related to the GS decline.
In our data, the median GS in males and females was 28.8 kg and 17.5 kg, which was considerably lower than that in Japanese people aged >60 years (average GS: male, 38.8 kg; female, 24.2 kg [28]). Multiple factors related to the GS decline in Ga-Ds may account for the current results. On the other hand, out of patients with the GS decline (n = 291), the average SARC-F score in patients with BMI (kg/m2) < 18.5 (n = 60), 18.5 < BMI (kg/m2) < 25 (n = 187), and BMI (kg/m2) > 25 (n = 43) was 1.7, 1.9 and 2.1, respectively. These results indicated that patients with the GS decline and BMI > 25 kg/m2 had the highest possibility for the definite diagnosis of sarcopenia. Sarcopenic obesity may be a serious concern in clinical settings because of its prognostic impact [29,30,31]. For Japanese people, a BMI of 22 kg/m2 is said to be the least likely to cause illness [32]. In our ROC analysis of BMI for the GS decline, the optimal reference value of BMI was 22.6 kg/m2, which is almost identical to the previous reports [32].
CRP value was an independent predictor for the GS decline. A recent meta-analysis reported that independent of disease state, higher CRP values were associated with GS decrease and knee extension strength decrease, which is in line with our data [33]. Proinflammatory cytokines such as TNF-α, IL-1β, IL-6, IFN-γ, and chemokines can cause increment in energy expenditure, appetite loss, and reduced dietary intake, which can be also linked to the current results [27]. Appropriate nutritional interventions may be considered for patients with higher CRP values [34]. Cachexia is common in patients with diseases related to chronic inflammation and skeletal muscle mass loss [35]. Although cachexia is common in patients with Ga-Ds, it is not well recognized by medical experts, and in most cases, the nutritional status deteriorates further without being diagnosed, resulting in skeletal muscle mass loss and decreased physical function [36,37]. In terms of SARC-F, the optimal reference value of the SARC-F score was 1 (the sensitivity/specificity, 64.3/77.5%), but when the reference value of the SARC-F score was changed to 4 (recommended reference value in the Asian guidelines [17]), the sensitivity/specificity was 21.7/96.8%. The relatively low sensitivity of the SARC-F score to the diagnosis of sarcopenia is a concern, which is identical to the current results [38,39,40]. The recommended reference value of the SARC-F score may be re-considered. On the other hand, lower hemoglobin value was independently linked to the GS decline in our data. A Korean study demonstrated a strong association between lower GS and anemia, which is in line with our data [41].
It should be understood that there are several limitations to the present analysis. First, this study is a single-center, cross-sectional study and is retrospective in nature. Second, because data for skeletal muscle mass was not available in the current analysis, the exact number of subjects with a confirmed diagnosis for sarcopenia was unknown. Third, the cohort in this study was highly heterogeneous, including a wide range of Ga-Ds (i.e., U-GD, L-GD, BP-D, and L-D). Fourth, patient daily activities or dietary habits, which can affect GS, were not analyzed in this study, also creating bias. Fifth, effect size was relatively small throughout analyzed parameters. Nevertheless, our study results denoted that GS can be influenced by various factors other than aging in patients with GDs. In conclusion, we would like to emphasize this as an important point when considering the GS decline in patients with Ga-Ds.

Author Contributions

Data curation, K.A., M.M., H.N., M.G., A.A., T.O., T.T., S.N., K.K., T.M., S.F., K.Y. and H.Y.; Formal analysis, H.N., K.U. and H.O.; Supervision, M.G. and K.H.; Writing—original draft, K.A. and H.N.; Writing—review & editing, H.N. and K.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Institutional Review Board of Osaka medical and pharmaceutical university (Approval number, 2021-122: date of approval, 10 January 2022).

Informed Consent Statement

Patient consent was waived due to the retrospective study design.

Data Availability Statement

The data are not publicly available due to personal information of our study cohort.

Acknowledgments

The authors gratefully thank all medical staff in our department for their help with data collection.

Conflicts of Interest

None of the authors has any conflict of interest to declare.

Abbreviations

Ga-D: gastrointestinal disease, QOL; quality of life, GS; grip strength, BMI; body mass index, ROC; receiver operating characteristic curve, IQR; interquartile range, AUC; area under the receiver operating characteristic curve, U-GD; upper gastrointestinal disease, L-GD; lower gastrointestinal disease, BP-D; biliary and pancreatic disease, L-D; liver disease, CRP; C reactive protein.

References

  1. Nishikawa, H.; Fukunishi, S.; Asai, A.; Yokohama, K.; Nishiguchi, S.; Higuchi, K. Pathophysiology and mechanisms of primary sarcopenia. Int. J. Mol. Med. 2021, 48, 156. [Google Scholar] [CrossRef] [PubMed]
  2. Ganapathy, A.; Nieves, J.W. Nutrition and Sarcopenia-What Do We Know? Nutrients 2020, 12, 1755. [Google Scholar] [CrossRef]
  3. Raquel, L.R.; Vicente, R.P.; José, L.G.S.; Anxela, S.R. Prevalence and Factors Associated with Functional Limitations during Aging in a Representative Sample of Spanish Population. Phys. Occup. Ther. Geriatr. 2018, 36, 156–167. [Google Scholar]
  4. Chhetri, J.K.; de Souto Barreto, P.; Fougère, B.; Rolland, Y.; Vellas, B.; Cesari, M. Chronic inflammation and sarcopenia: A regenerative cell therapy perspective. Exp. Gerontol. 2018, 103, 115–123. [Google Scholar] [CrossRef] [PubMed]
  5. Sieber, C.C. Malnutrition and sarcopenia. Aging Clin. Exp. Res. 2019, 31, 793–798. [Google Scholar] [CrossRef]
  6. Shaw, C. Management of diet in gastrointestinal cancer. Proc. Nutr. Soc. 2021, 80, 65–72. [Google Scholar] [CrossRef]
  7. Balestrieri, P.; Ribolsi, M.; Guarino, M.P.L.; Emerenziani, S.; Altomare, A.; Cicala, M. Nutritional Aspects in Inflammatory Bowel Diseases. Nutrients 2020, 12, 372. [Google Scholar] [CrossRef] [Green Version]
  8. Nishikawa, H.; Shiraki, M.; Hiramatsu, A.; Moriya, K.; Hino, K.; Nishiguchi, S. Japan Society of Hepatology guidelines for sarcopenia in liver disease (1st edition): Recommendation from the working group for creation of sarcopenia assessment criteria. Hepatol. Res. 2016, 46, 951–963. [Google Scholar] [CrossRef]
  9. Dunne, R.F.; Loh, K.P.; Williams, G.R.; Jatoi, A.; Mustian, K.M.; Mohile, S.G. Cachexia and Sarcopenia in Older Adults with Cancer: A Comprehensive Review. Cancers 2019, 11, 1861. [Google Scholar] [CrossRef] [Green Version]
  10. Wang, H.; Yang, R.; Xu, J.; Fang, K.; Abdelrahim, M.; Chang, L. Sarcopenia as a predictor of postoperative risk of complications, mortality and length of stay following gastrointestinal oncological surgery. Ann. R. Coll. Surg. Engl. 2021, 103, 630–637. [Google Scholar] [CrossRef]
  11. Meyer, F.; Valentini, L. Disease-Related Malnutrition and Sarcopenia as Determinants of Clinical Outcome. Visc. Med. 2019, 35, 282–291. [Google Scholar] [CrossRef] [PubMed]
  12. Bohannon, R.W. Grip Strength: An Indispensable Biomarker For Older Adults. Clin. Interv. Aging 2019, 14, 1681–1691. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Nakano, J.; Fukushima, T.; Tanaka, T.; Fu, J.B.; Morishita, S. Physical function predicts mortality in patients with cancer: A systematic review and meta-analysis of observational studies. Support Care Cancer 2021, 29, 5623–5634. [Google Scholar] [CrossRef] [PubMed]
  14. Hollingworth, T.W.; Oke, S.M.; Patel, H.; Smith, T.R. Getting to grips with sarcopenia: Recent advances and practical management for the gastroenterologist. Frontline Gastroenterol. 2020, 12, 53–61. [Google Scholar] [CrossRef]
  15. Leong, D.P.; Teo, K.K.; Rangarajan, S.; Lopez-Jaramillo, P.; Avezum, A., Jr.; Orlandini, A.; Seron, P.; Ahmed, S.H.; Rosengren, A.; Kelishadi, R.; et al. Prospective Urban Rural Epidemiology (PURE) Study investigators. Prognostic value of grip strength: Findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet 2015, 386, 266–273. [Google Scholar] [CrossRef]
  16. Celis-Morales, C.A.; Welsh, P.; Lyall, D.M.; Steell, L.; Petermann, F.; Anderson, J.; Iliodromiti, S.; Sillars, A.; Graham, N.; Mackay, D.F.; et al. Associations of grip strength with cardiovascular, respiratory, and cancer outcomes and all-cause mortality: Prospective cohort study of half a million UK Biobank participants. BMJ 2018, 361, k1651. [Google Scholar]
  17. Chen, L.K.; Woo, J.; Assantachai, P.; Auyeung, T.W.; Chou, M.Y.; Iijima, K.; Jang, H.C.; Kang, L.; Kim, M.; Kim, S.; et al. Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. J. Am. Med. Dir. Assoc. 2020, 21, 300–307.e2. [Google Scholar] [CrossRef]
  18. Cruz-Jentoft, A.J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyère, O.; Cederholm, T.; Cooper, C.; Landi, F.; Rolland, Y.; Sayer, A.A.; et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2019, 48, 16–31. [Google Scholar] [CrossRef] [Green Version]
  19. Malmstrom, T.K.; Miller, D.K.; Simonsick, E.M.; Ferrucci, L.; Morley, J.E. SARC-F: A symptom score to predict persons with sarcopenia at risk for poor functional outcomes. J. Cachexia Sarcopenia Muscle 2016, 7, 28–36. [Google Scholar] [CrossRef]
  20. Ida, S.; Kaneko, R.; Murata, K. SARC-F for Screening of Sarcopenia Among Older Adults: A Meta-analysis of Screening Test Accuracy. J. Am. Med. Dir. Assoc. 2018, 19, 685–689. [Google Scholar] [CrossRef]
  21. Kim, S.; Kim, M.; Won, C.W. Validation of the Korean Version of the SARC-F Questionnaire to Assess Sarcopenia: Korean Frailty and Aging Cohort Study. J. Am. Med. Dir. Assoc. 2018, 19, 40–45.e41. [Google Scholar] [CrossRef] [PubMed]
  22. Tanaka, S.; Kamiya, K.; Hamazaki, N.; Matsuzawa, R.; Nozaki, K.; Maekawa, E.; Noda, C.; Yamaoka-Tojo, M.; Matsunaga, A.; Masuda, T.; et al. Utility of SARC-F for Assessing Physical Function in Elderly Patients With Cardiovascular Disease. J. Am. Med. Dir. Assoc. 2017, 18, 176–181. [Google Scholar] [CrossRef] [PubMed]
  23. Japan Society of the Study of Obesity. Available online: http://www.jasso.or.jp/index.html (accessed on 10 January 2022).
  24. Okubo, T.; Atsukawa, M.; Tsubota, A.; Ono, H.; Kawano, T.; Yoshida, Y.; Arai, T.; Hayama, K.; Itokawa, N.; Kondo, C.; et al. Effect of Vitamin D Supplementation on Skeletal Muscle Volume and Strength in Patients with Decompensated Liver Cirrhosis Undergoing Branched Chain Amino Acids Supplementation: A Prospective, Randomized, Controlled Pilot Trial. Nutrients 2021, 13, 1874. [Google Scholar] [CrossRef]
  25. Hanai, T.; Shiraki, M.; Imai, K.; Suetugu, A.; Takai, K.; Shimizu, M. Usefulness of Carnitine Supplementation for the Complications of Liver Cirrhosis. Nutrients 2020, 12, 1915. [Google Scholar] [CrossRef] [PubMed]
  26. Tuzun, S.; Keles, A.; Okutan, D.; Yildiran, T.; Palamar, D. Assessment of musculoskeletal pain, fatigue and grip strength in hospitalized patients with COVID-19. Eur. J. Phys. Rehabil. Med. 2021, 57, 653–662. [Google Scholar] [CrossRef] [PubMed]
  27. Nishikawa, H.; Shiraki, M.; Hiramatsu, A.; Hara, N.; Moriya, K.; Hino, K.; Koike, K. Reduced handgrip strength predicts poorer survival in chronic liver diseases: A large multicenter study in Japan. Hepatol. Res. 2021, 51, 957–967. [Google Scholar] [CrossRef] [PubMed]
  28. Available online: https://www.city.nerima.tokyo.jp/hokenfukushi/hoken/kenkodukuri/kenkoi7/20190305111627975.files/akuryokuheikinti.pdf (accessed on 10 January 2022).
  29. Nishikawa, H.; Asai, A.; Fukunishi, S.; Nishiguchi, S.; Higuchi, K. Metabolic Syndrome and Sarcopenia. Nutrients 2021, 13, 3519. [Google Scholar] [CrossRef]
  30. Colleluori, G.; Villareal, D.T. Aging, obesity, sarcopenia and the effect of diet and exercise intervention. Exp. Gerontol. 2021, 155, 111561. [Google Scholar] [CrossRef]
  31. Hsu, K.J.; Liao, C.D.; Tsai, M.W.; Chen, C.N. Effects of Exercise and Nutritional Intervention on Body Composition, Metabolic Health, and Physical Performance in Adults with Sarcopenic Obesity: A Meta-Analysis. Nutrients 2019, 11, 2163. [Google Scholar] [CrossRef] [Green Version]
  32. Tokunaga, K.; Matsuzawa, Y.; Kotani, K.; Keno, Y.; Kobatake, T.; Fujioka, S.; Tarui, S. ldeal body weight estimated from the body mass index with the lowest morbidity. Int. J. Obes. 1991, 15, 1–5. [Google Scholar]
  33. Tuttle, C.S.L.; Thang, L.A.N.; Maier, A.B. Markers of inflammation and their association with muscle strength and mass: A systematic review and meta-analysis. Ageing Res. Rev. 2020, 64, 101185. [Google Scholar] [CrossRef] [PubMed]
  34. Wakabayashi, H.; Arai, H.; Inui, A. The regulatory approval of anamorelin for treatment of cachexia in patients with non-small cell lung cancer, gastric cancer, pancreatic cancer, and colorectal cancer in Japan: Facts and numbers. J. Cachexia Sarcopenia Muscle 2021, 12, 14–16. [Google Scholar] [CrossRef] [PubMed]
  35. Nishikawa, H.; Goto, M.; Fukunishi, S.; Asai, A.; Nishiguchi, S.; Higuchi, K. Cancer Cachexia: Its Mechanism and Clinical Significance. Int. J. Mol. Sci. 2021, 22, 8491. [Google Scholar] [CrossRef] [PubMed]
  36. Bielecka-Dabrowa, A.; Ebner, N.; Dos Santos, M.R.; Ishida, J.; Hasenfuss, G.; von Haehling, S. Cachexia, muscle wasting, and frailty in cardiovascular disease. Eur. J. Heart Fail. 2020, 22, 2314–2326. [Google Scholar] [CrossRef]
  37. Wyart, E.; Bindels, L.B.; Mina, E.; Menga, A.; Stanga, S.; Porporato, P.E. Cachexia, a Systemic Disease beyond Muscle Atrophy. Int. J. Mol. Sci. 2020, 21, 8592. [Google Scholar] [CrossRef] [PubMed]
  38. Voelker, S.N.; Michalopoulos, N.; Maier, A.B.; Reijnierse, E.M. Reliability and Concurrent Validity of the SARC-F and Its Modified Versions: A Systematic Review and Meta-Analysis. J. Am. Med. Dir. Assoc. 2021, 22, 1864–1876. [Google Scholar] [CrossRef]
  39. Kurita, N.; Wakita, T.; Kamitani, T.; Wada, O.; Mizuno, K. SARC-F Validation and SARC-F+EBM Derivation in Musculoskeletal Disease: The SPSS-OK Study. J. Nutr. Health Aging 2019, 23, 732–738. [Google Scholar] [CrossRef]
  40. Barbosa-Silva, T.G.; Menezes, A.M.; Bielemann, R.M.; Malmstrom, T.K.; Gonzalez, M.C.; Grupo de Estudos em Composição Corporal e Nutrição (COCONUT). Enhancing SARC-F: Improving Sarcopenia Screening in the Clinical Practice. J. Am. Med. Dir. Assoc. 2016, 17, 1136–1141. [Google Scholar] [CrossRef]
  41. Gi, Y.M.; Jung, B.; Kim, K.W.; Cho, J.H.; Ha, I.H. Low handgrip strength is closely associated with anemia among adults: A cross-sectional study using Korea National Health and Nutrition Examination Survey (KNHANES). PLoS ONE 2020, 15, e0218058. [Google Scholar] [CrossRef] [Green Version]
Figure 1. (A) The percentage of GS decline in patients with ECOG-PS 0 (n = 399), ECOG-PS 1 (n = 108), and ECOG-PS 2 (n = 95). (B) The percentage of GS decline in patients with BMI (kg/m2) < 18.5 (n = 96), 18.5 < BMI (kg/m2) < 25 (n = 386), and BMI (kg/m2) > 25 (n = 118).
Figure 1. (A) The percentage of GS decline in patients with ECOG-PS 0 (n = 399), ECOG-PS 1 (n = 108), and ECOG-PS 2 (n = 95). (B) The percentage of GS decline in patients with BMI (kg/m2) < 18.5 (n = 96), 18.5 < BMI (kg/m2) < 25 (n = 386), and BMI (kg/m2) > 25 (n = 118).
Jcm 11 02079 g001
Figure 2. (A) The SARC-F score in patients with the GS non-decline (n = 311) and the GS decline (n = 291). (B) The percentage of the SARC-F score ≥ 4 in patients with the GS non-decline and the GS decline.
Figure 2. (A) The SARC-F score in patients with the GS non-decline (n = 311) and the GS decline (n = 291). (B) The percentage of the SARC-F score ≥ 4 in patients with the GS non-decline and the GS decline.
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Figure 3. (A) The SARC-F score in patients with GS non-decline (n = 71) and GS decline (n = 74) (advanced cancer cases, n = 145). (B) The percentage of the SARC-F score ≥ 4 in patients with GS non-decline and GS decline (advanced cancer cases). (C) The SARC-F score in patients with GS non-decline (n = 240) and GS decline (n = 217) (non-advanced cancer cases, n = 457). (D) The percentage of the SARC-F score ≥ 4 in patients with GS non-decline and GS decline (non-advanced cancer cases).
Figure 3. (A) The SARC-F score in patients with GS non-decline (n = 71) and GS decline (n = 74) (advanced cancer cases, n = 145). (B) The percentage of the SARC-F score ≥ 4 in patients with GS non-decline and GS decline (advanced cancer cases). (C) The SARC-F score in patients with GS non-decline (n = 240) and GS decline (n = 217) (non-advanced cancer cases, n = 457). (D) The percentage of the SARC-F score ≥ 4 in patients with GS non-decline and GS decline (non-advanced cancer cases).
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Table 1. Baseline characteristics (n = 602).
Table 1. Baseline characteristics (n = 602).
VariablesNumber or Median (IQR)
Age (years)72 (64–79)
Gender, male/female379/223
ECOG-PS0 (0–1)
Grip strength (male, kg)28.8 (23.6–34.3)
Grip strength (female, kg)17.5 (13.9–20.5)
The SARC-F score0 (0–2)
Body mass index (kg/m2)21.9 (19.6–24.4)
Advanced cancer, yes/no145/457
Hemoglobin (g/dL)12.5 (11.1–13.8)
Platelet count (×104/μL)21.9 (16.6–27.7)
Total lymphocyte count (/μL)1330 (989–1822)
ALT (IU/L)19 (13–32)
eGFR (mL/min/1.73 m2)67 (55–81)
Serum albumin (g/dL)3.8 (3.4–4.2)
C reactive protein (mg/dL)0.18 (0.05–0.95)
IQR, interquartile range; ALT, alanine aminotransferase; eGFR, estimated glomerular filtration rate.
Table 2. Univariate analysis of factors associated with the grip strength decline.
Table 2. Univariate analysis of factors associated with the grip strength decline.
VariablesGrip Strength Decline
(n = 291)
Grip Strength Non-Decline
(n = 311)
p ValueEffect Size
Age (years)77 (71–82)68 (56–74)<0.00010.15
Gender (male/female)169/122210/1010.01810.10
BMI (kg/m2)21.1 (19.0–23.9)22.7 (20.1–24.9)0.00020.15
ECOG-PS1 (0–2)0 (0–0)<0.00010.36
Advanced cancer, yes/no74/21771/2400.50450.03
Primary origin of disease
U-GD/L-GD/BP-D/L-D
80/62/103/4669/94/106/420.07370.11
SARC-F score1 (0–3)0 (0–0)<0.00010.38
Hemoglobin (g/dL)11.7 (10.6–13.1)13.2 (11.8–14.3)<0.00010.33
Platelet count (×104/μL)21.4 (15.8–28.0)22.4 (17.6–27.5)0.46670.0
Total lymphocyte count (/μL)1251 (900–1728)1480 (1092–1890)<0.00010.16
Serum albumin (g/dL)3.6 (3.1–4.0)4.0 (3.7–4.3)<0.00010.32
CRP (mg/dL)0.30 (0.07–2.32)0.13 (0.05–0.41)<0.00010.19
ALT (IU/L)19 (12–32)19 (13–32)0.71450.01
eGFR (mL/min/1.73 m2)63 (51–79)71 (58–82)0.00030.15
Data are expressed as number or median value (interquartile range). BMI, body mass index; U-GD, upper gastrointestinal disease; L-GD, lower gastrointestinal disease; BP-D, biliary pancreatic disease; L-D, liver disease; CRP, C reactive protein; ALT, alanine aminotransferase; eGFR, estimated glomerular filtration rate.
Table 3. Multivariate analysis of factors for the grip strength decline.
Table 3. Multivariate analysis of factors for the grip strength decline.
VariablesMultivariate Analysis
HR95% CIp Value
Age (per one year)1.0521.033–1.072<0.0001
BMI (per one kg/m2)0.9380.888–0.9920.0223
ECOG-PS (per one)1.2210.857–1.7400.2678
Gender (female)1.2940.852–1.9660.2268
SARC-F score (per one)1.4671.181–1.8230.0003
Hemoglobin (per one g/dL)0.8630.763–0.9760.0186
Serum albumin (per one g/dL)0.6220.405–0.9540.0284
Total lymphocyte count (per one/μL)0.99990.9995–1.00020.4603
eGFR (per one mL/min/1.73 m2)0.9960.985–1.0060.4349
CRP (per one mg/dL)1.0690.998–1.1440.0331
BMI: body mass index; eGFR: estimated glomerular filtration rate; CRP: C reactive protein; HR: hazard ratio; CI: confidence interval.
Table 4. Receiver operating characteristic curve analysis of independent factors in the multivariate analysis for the grip strength decline.
Table 4. Receiver operating characteristic curve analysis of independent factors in the multivariate analysis for the grip strength decline.
VariablesAUCSensitivity (%)Specificity (%)Reference Value
Age (years)0.7472.965.072
BMI (kg/m2)0.6068.351.322.6
SARC-F score0.7364.377.51
Hemoglobin (g/dL)0.7065.666.212.4
Serum albumin (g/dL)0.7080.849.84.0
CRP (mg/dL)0.6044.076.50.46
BMI, body mass index; CRP, C reactive protein; AUC, area under the receiver operating characteristic curve.
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MDPI and ACS Style

Asaishi, K.; Matsui, M.; Nishikawa, H.; Goto, M.; Asai, A.; Ushiro, K.; Ogura, T.; Takeuchi, T.; Nakamura, S.; Kakimoto, K.; et al. Grip Strength in Patients with Gastrointestinal Diseases. J. Clin. Med. 2022, 11, 2079. https://doi.org/10.3390/jcm11082079

AMA Style

Asaishi K, Matsui M, Nishikawa H, Goto M, Asai A, Ushiro K, Ogura T, Takeuchi T, Nakamura S, Kakimoto K, et al. Grip Strength in Patients with Gastrointestinal Diseases. Journal of Clinical Medicine. 2022; 11(8):2079. https://doi.org/10.3390/jcm11082079

Chicago/Turabian Style

Asaishi, Ken, Masahiro Matsui, Hiroki Nishikawa, Masahiro Goto, Akira Asai, Kosuke Ushiro, Takeshi Ogura, Toshihisa Takeuchi, Shiro Nakamura, Kazuki Kakimoto, and et al. 2022. "Grip Strength in Patients with Gastrointestinal Diseases" Journal of Clinical Medicine 11, no. 8: 2079. https://doi.org/10.3390/jcm11082079

APA Style

Asaishi, K., Matsui, M., Nishikawa, H., Goto, M., Asai, A., Ushiro, K., Ogura, T., Takeuchi, T., Nakamura, S., Kakimoto, K., Miyazaki, T., Fukunishi, S., Ohama, H., Yokohama, K., Yasuoka, H., & Higuchi, K. (2022). Grip Strength in Patients with Gastrointestinal Diseases. Journal of Clinical Medicine, 11(8), 2079. https://doi.org/10.3390/jcm11082079

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