Research ArticleClinical Studies

Predictors for Grip Strength Loss in Patients With Chronic Liver Diseases

HIROKI NISHIKAWA, KAZUNORI YOH, HIRAYUKI ENOMOTO, NAOTO IKEDA, TOMOYUKI TAKASHIMA, NOBUHIRO AIZAWA, TAKASHI NISHIMURA, SHUHEI NISHIGUCHI and HIROKO IIJIMA
In Vivo January 2021, 35 (1) 363-371; DOI: https://doi.org/10.21873/invivo.12267

Abstract

Background/Aim: To elucidate factors associated with secular changes of grip strength (GS) in patients with chronic liver diseases (CLDs) (n=241, 102 males, median age=63 years, 87 liver cirrhosis cases). Materials and Methods: ΔGS (kg/year) was defined as [GS value (second time) – GS value (first time)]/[time interval between the first and second time]. GS loss (GSL) was defined as ΔGS <0 kg/year. Results: The median ΔGS in patients with non-LC, Child-Pugh A (n=70) and Child-Pugh B (n=17) were 0.3, –0.2 and –1.6 kg/year (overall p<0.0001). In the multivariate analysis of factors linked to the GSL for all cases, extracellular water (ECW) to total body water (TBW) ratio was significant (p=0.0007). In the multivariate analysis in male, no significant factor was found, while in female, ECW to TBW ratio was significant (p=0.0024). Conclusion: Liver functional parameters can be closely linked to the GSL especially in female CLD patients.

The liver is the pivotal organ for the metabolism of the human body (1, 2). Advanced chronic liver diseases (CLDs) are frequently associated with disease-related sarcopenia (i.e., secondary sarcopenia) (1-6). Therefore, it is meaningful to consider skeletal muscle as one organ and discuss sarcopenia in relation to organs in the medical treatment and research of liver diseases. CLD patients with sarcopenia can involve both impaired protein synthesis and accelerated muscle proteolysis in skeletal muscles (1, 2). A previous meta-analysis reported the close association between sarcopenia and mortality in CLD patients (4). Many high-quality studies of sarcopenia led to recognition as a disease entity with the awards of an ICD 10 code in 2016 (7). In addition, the recent revisions of diagnostic criteria for sarcopenia in European or Asian guidelines have made sarcopenia research more exciting (8, 9).

Grip strength (GS) does not require difficult movements and can be measured easily and safely in a short time, and thus it is suitable for measuring muscle strength in daily medical care. GS, which is mainly the muscle strength of the upper body, has significant correlations with the muscle strength in the lower limbs and many other parts, and it is used as an index to assess the degree of muscle strength of the whole body (10-13). GS seems to be the main determinant of physical activity (8). Recent numerous studies have also shown that decreased GS is linked to an elevated risk of disease development, disease progression and mortality. However, the impact of skeletal muscle mass rather than GS had mainly been focused in sarcopenia researches for the past several decades (14-30). In our recent study, we emphasized the significance of GS on composite hepatic events in CLD patients (15). Hanai et al. reported that reduced GS rather than skeletal muscle mass and fat mass was significantly linked to an increased risk of mortality in cirrhotic patients (16). However, to our knowledge, data for factors related to the secular changes of GS in CLDs are scarce (31). The aim of this study was to elucidate factors associated with secular changes of GS in patients with CLDs.

Patients and Methods

Patients. Using a retrospective computerized database, a total of 241 CLD individuals who visited our Hospital between January 2013 and April 2020 were analyzed. Diagnosis for liver cirrhosis (LC) was determined according to the current guidelines (32). All analyzed patients received GS measurement twice with an interval of at least 3 months. The most suitable intervention for each underlying liver disease was performed (32-35). The study protocol rigorously conformed to the 1975 Helsinki Declaration, and approval of ethics was obtained from the institutional review board in our hospital. An opt out method was employed.

GS, SMI and ΔGS. A low-GS was defined as <26 kg in males and <18 kg in females based on the Japanese Society of Hepatology (JSH) guidelines (36). Likewise, a low-skeletal muscle index (SMI, SMI indicates appendicular muscle mass divided by height squared [kg/m2]) was defined as <7.0 kg/m2 in males and <5.7 kg/m2 in females using bioelectrical impedance analysis (36). Sarcopenia was defined as both low-GS and low-SMI (36). ΔGS (kg/year) was defined as [GS value (second time) – GS value (first time)] ÷ [time interval between the first time and the second time (year)]. GS loss (GSL) was defined as ΔGS <0 kg/year. We investigated factors associated with the GSL.

Statistical analyses. As for the continuous parameters, Mann-Whitney U-test, Student’s t-test, analysis of variance or Kruskal-Wallis test was employed to adequately assess differences between groups. As for the categorical parameters, Fisher’s exact test or Pearson χ2 test was employed to assess differences between groups. Baseline significant parameters in the univariate analysis were subjected to the multivariate logistic regression analysis to choose candidate parameters. In the multivariate analyses of items associated with the GSL, the median value for each significant item in the univariate analysis was selected to classify the study cohort into the two categorical groups. In the analysis of correlation between parameters, Pearson’s correlation coefficient (r) was employed. A p<0.05 denotes statistical significance by the statistical analysis software (JMP 14 (SAS Institute Inc., Cary, NC)).

Results

Baseline characteristics. The baseline characteristics of the analyzed subjects (n=241, 102 males, median age=63 years) are presented in Table I. There were 178 patients (73.9%) with albumin-bilirubin (ALBI) grade 1, 60 (24.9%) with ALBI grade 2 and 3 (1.2%) with ALBI grade 3. LC was seen in 87 patients (36.1%: Child-Pugh A/B/C in 70/17/0 patients, respectively). Eight male patients (7.8%) had a GS decrease, while 28 female patients (20.1%) had a GS decrease (36). Twenty-seven male patients (26.5%) had an SMI decrease, while 47 female patients (33.8%) had an SMI decrease (36). Collectively, sarcopenia was found in 17 patients (7.1%) [4 male patients (3.9%) and 13 female patients (9.4%)]. The median time interval between the first time GS measurement and the second time GS measurement was 1.41 years. The median [interquartile range (IQR)] ΔGS (kg/year) for all cases was 0 (–1.0, 0.9) kg/year (Figure 1A).

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Table I.

Baseline characteristics (n=241).

Figure 1.
Figure 1.

The distribution of ΔGS (kg/year) [GS value (second time) – GS value (first time)] ÷ [time interval between the first time and the second time (year)] for all cases (n=241) (A), male cases (n=102)) (B) and female cases (n=139) (C).

ΔGS (kg/year) according to gender, age, sarcopenia, body mass index (BMI), ALBI grade, Child-Pugh classification and liver disease etiology. The median (IQR) ΔGS (kg/year) in males (n=102) and females (n=139) were 0.3 (–1.05, 1.1) kg/year and –0.2 (–1.0, 0.7) kg/year, respectively, (p=0.5429) (Figure 1B, C and 2A). The median (IQR) ΔGS (kg/year) in patients aged 65 years or more (n=109) and less than 65 years (n=132) were –0.2 (–1.4, 0.65) kg/year and 0.3 (–0.6, 1.175) kg/year, respectively, (p=0.0672) (Figure 2B). The median (IQR) ΔGS (kg/year) in patients with sarcopenia (n=17) and without sarcopenia (n=224) were 0.1 (–0.35, 1.1) kg/year and 0 (–1.0, 0.9) kg/year, respectively, (p=0.5950) (Figure 2C). The median (IQR) ΔGS (kg/year) in patients with BMI ≥25 kg/m2 (n=72) and <25 kg/m2 (n=169) were –0.1 (–1.3, 0.7) kg/year and 0.1 (–0.7, 0.975) kg/year, respectively, (p=0.4789) (Figure 2D). The median (IQR) ΔGS (kg/year) in patients with ALBI grade 1 (n=178) and ALBI grade 2 or 3 (n=63) were 0.2 (–0.6, 1.0) kg/year and –0.5 (–1.9, 0.5) kg/year, respectively, (p=0.0064) (Figure 2E). The median (IQR) ΔGS (kg/year) in patients with non-LC (n=154), Child-Pugh A (n=70) and Child-Pugh B (n=17) were 0.3 (–0.6, 1.2) kg/year, –0.2 (–1.425, 0.325) kg/year and -1.6 (–4.5, –0.1) kg/year, respectively [p=0.0002 (non-LC vs. Child-Pugh A), p=0.0255 (Child-Pugh A vs. B), p<0.0001 (non-LC vs. Child-Pugh B) and overall p<0.0001] (Figure 3A). The median (IQR) ΔGS (kg/year) in patients with hepatitis B virus (HBV, n=21), hepatitis C virus (HCV, n=154) and others (n=66) were –0.1 (–1.0, 0.95) kg/year, 0 (–0.775, 0.8) kg/year and 0.05 (–1.325, 1.225) kg/year, respectively [p=0.6525 (HBV vs. HCV), p=0.6730 (HCV vs. others), p=0.4810 (HBV vs. others) and overall p=0.7807] (Figure 3B).

Figure 2.
Figure 2.

ΔGS (kg/year) according to gender (A), age (B), sarcopenia (C), body mass index (Figure 2D), albumin-bilirubin grade (E).

Figure 3.
Figure 3.

ΔGS (kg/year) according to Child-Pugh classification (A) and liver disease etiology (B).

Correlation between ΔGS and baseline continuous parameters according to gender. Regarding correlations between ΔGS and baseline continuous parameters, significant associations were found in age (r=–0.24 and p=0.0171) as for male gender, and total bilirubin (r=–0.26 and p=0.0023), serum albumin (r=0.21 and p=0.0148), ALBI score (r=–0.25 and p=0.0027), prothrombin time-INR (PT-INR) (r=0.30 and p=0.0003), platelet count (r=0.31 and p=0.0002) and extracellular water (ECW) to total body water (TBW) ratio (r=–0.42 and p<0.0001) as for female (Table II).

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Table II.

Correlation between ΔGS (kg/year) and baseline continuous parameters according to gender.

Uni- and multivariate analyses of factors linked to the GSL for all cases. For all cases, GSL was found in 113 patients (46.9%). The univariate analysis of factors associated with the GSL identified that 6 had values of p<0.05: age (p=0.0006), presence of LC (p<0.0001), serum albumin (p=0.0015), ALBI score (p=0.0009), PT-INR (p=0.0040) and ECW to TBW ratio (p<0.0001) (Table III). Serum albumin was excluded from the multivariate analysis as ALBI includes serum albumin. In the multivariate analysis of the remaining 5 factors, ECW to TBW ratio was found to be significant (p=0.0007), while presence of LC tended to be significant (p=0.0706). Corresponding odds ratio (OR) and 95% confidence interval (CI) for each variable were demonstrated in Table IV.

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Table III.

Univariate analysis of factors linked to GSL for all cases (n=241).

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Table IV.

Multivariate analysis of factors linked to GSL for all cases.

Uni- and multivariate analyses of factors linked to the GSL for male cases. For male cases, GSL was found in 40 patients (39.2%). The univariate analysis of factors associated with the GSL identified that 4 had values of p<0.05: age (p=0.0044), presence of LC (p=0.0380), estimated glomerular filtration rate (eGFR) (p=0.0273) and ECW to TBW ratio (p=0.0217) (Table V). In the multivariate analysis of the 4 factors, no significant factor was found, while eGFR tended to be significant (p=0.0826). Corresponding OR and 95% CI for each variable were demonstrated in Table VI.

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Table V.

Univariate analysis of factors linked to GSL for male cases (n=102).

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Table VI.

Multivariate analysis of factors linked to GSL for male cases.

Uni- and multivariate analyses of factors linked to the GSL for female cases. For female cases, GSL was found in 73 patients (53.3%). The univariate analysis of factors associated with the GSL identified that 6 had values of p<0.05: presence of LC (p=0.0003), serum albumin (p=0.0239), ALBI score (p=0.0111), PT-INR (p=0.0034), platelet count (p=0.0008) and ECW to TBW ratio (p<0.0001) (Table VII). Serum albumin was excluded for the multivariate analysis as ALBI includes serum albumin. In the multivariate analysis of the remaining 5 factors, ECW to TBW ratio was found to be significant (p=0.0024), while ALBI score tended to be significant (p=0.0895). Corresponding OR and 95% CI for each variable were demonstrated in Table VIII.

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Table VII.

Univariate analysis of factors linked to GSL for female cases (n=139).

View this table:
Table VIII.

Multivariate analysis of factors linked to GSL for female cases.

Discussion

GS is the main determinant of physical activity (8). GS well reflects the degree of muscle strength of the whole body (10-13). GS can be a marker of nutritional status because muscle function responds early to nutritional deficiencies (10). GS measurement is a key part of the JSH assessment criteria for sarcopenia in liver disease (36). However, in the current European guidelines, Asian guidelines or JSH guidelines, description of secular changes in GS is not found anywhere (8, 9, 36). Few data with regard to GSL in CLD patients are currently available (31). Thus, elucidating risk factors for the GSL in patients with CLDs seems to be clinically meaningful.

In our multivariate analysis for all cases, ECW to TBW ratio was found to be an independent factor and presence of LC tended to be a significant factor linked to the GSL. ECW to TBW ratio in CLDs represents edematous status and liver function (37). Management of edematous status in CLDs should be pivotal for avoiding GSL. In our previous investigation, we reported the significant negative correlation between ECW to TBW ratio and walking speed in patients with CLDs, which are similar to the current data (38). As shown in Figure 3, the stepwise decrease of ΔGS was found according to the liver disease severity. While Hiraoka et al. reported the significant correlation between serum albumin level and the GSL, which are in line with our data (31).

In the correlation between ΔGS and baseline continuous parameters according to gender, and in the multivariate analyses of factors linked to the GSL according to gender, large differences between male and female were found. Age significantly correlated with ΔGS in male, while not in female. Total bilirubin, serum albumin, ALBI score, PT-INR, platelet count and ECW to TBW ratio significantly correlated with ΔGS in females, while not in males. ECW to TBW ratio was an independent predictor linked to the GSL in females, while not in males. Hanai et al. reported that GS was independently associated with mortality regardless of gender in LC patients, however, as for secular changes in GS in patients with CLDs, clinicians should be fully aware of gender differences (16). On the other hand, in the multivariate analysis for the GSL in male, eGFR tended to be significant. A previous study reported that in community-dwelling older males (n=789), mild-to-moderate renal impairment at baseline was associated with GS decline, which is in agreement of our results (39).

Sung et al. reported that encephalopathy, higher level of Wisteria floribunda agglutinin-positive Mac-2 binding protein (liver fibrosis marker), advanced age, and sarcopenia were independent adverse predictors for skeletal muscle mass loss in 166 LC patients (40). While contrary to our expectations, sarcopenia and advanced age were not independent factors linked to the GSL in our results. In this study, sarcopenia was found in only 17 patients (7.1%) (4 male patients and 13 female patients), and the small number of sarcopenic patients may be one of possible causes of our results. In addition, the severity of underlying liver disease rather than advanced age may be associated with the GSL.

According to the report of Japan sports agency (JSA), the median values of GS in patients aged 60-64 years were 42.85 kg in male and 26.3 kg in female, while in our data (median age=63 years), the median values of GS were 34.375 kg in males and 20.95 kg in females, which were lower than the JSA data. These may be attributed to the disease-related muscle functional decline. JSA also reported that GS peaks at 35 to 39 years for male and 40 to 44 years for female, and then decreases with aging. In our data, there were 128 patients (53.1%) without GSL. In the analyzed subjects, the most suitable intervention for each underlying liver disease was performed during the follow-up period. These interventions may lead to the maintenance of GS value. However, further examinations are required to confirm whether medical interventions ameliorate GS value in CLD patients.

Several limitations to our study must be acknowledged. First, this single-center study had a retrospective nature. Second, our cohort was heterogeneous including various etiologies for underlying liver diseases and various degrees of liver functional reserve. Third, various interventions for each subject have been done during the follow-up period, making bias for the interpretation of changes of GS values. Fourth, our results were derived from data of only Japanese CLD patients and our study cohort did not include Child-Pugh C patients. Finally, GS value can vary depending on patient conditions. Caution must be, therefore, taken in interpreting the results. Despite the limitations, our study results denote that baseline liver functional parameters are closely linked to the GSL especially in female CLD patients. In conclusion, we would like to emphasize the importance of baseline liver function as a useful predictor for the GSL in patients with CLDs.

Acknowledgements

The Authors would like to thank Yasuko Higuchi in our hospital for the anthropometry measurement. This work was partly supported by Hyogo Innovative Challenge, Hyogo College of Medicine, Japan.

Footnotes

  • Authors’ Contributions

    Data curation, Hiroki Nishikawa, Kazunori Yoh, Hirayuki Enomoto, Naoto Ikeda, Tomoyuki Takashima, Nobuhiro Aizawa and Takashi Nishimura; Formal analysis, Hiroki Nishikawa; Supervision, Shuhei Nishiguchi and Hiroko Iijima; Writing – original draft, Hiroki Nishikawa and Kazunori Yoh; Writing – review & editing, Hirayuki Enomoto.

  • This article is freely accessible online.

  • Conflicts of Interest

    The Authors declare no conflicts of interest.

  • Received September 23, 2020.
  • Revision received October 4, 2020.
  • Accepted October 12, 2020.

References

  1. ↵
    1. Bunchorntavakul C and
    2. Reddy KR
    : Review article: malnutrition/sarcopenia and frailty in patients with cirrhosis. Aliment Pharmacol Ther 51: 64-77, 2020. PMID: 31701570. DOI: 10.1111/apt.15571
    OpenUrlCrossRef
  2. ↵
    1. Aby ES and
    2. Saab S
    : Frailty, sarcopenia, and malnutrition in cirrhotic patients. Clin Liver Dis 23: 589-605, 2019. PMID: 31563213. DOI: 10.1016/j.cld.2019.06.001
    OpenUrlCrossRef
    1. Nishikawa H,
    2. Enomoto H,
    3. Ishii A,
    4. Iwata Y,
    5. Miyamoto Y,
    6. Ishii N,
    7. Yuri Y,
    8. Hasegawa K,
    9. Nakano C,
    10. Nishimura T,
    11. Yoh K,
    12. Aizawa N,
    13. Sakai Y,
    14. Ikeda N,
    15. Takashima T,
    16. Takata R,
    17. Iijima H and
    18. Nishiguchi S
    : Elevated serum myostatin level is associated with worse survival in patients with liver cirrhosis. J Cachexia Sarcopenia Muscle 8: 915-925, 2017. PMID: 28627027. DOI: 10.1002/jcsm.12212
    OpenUrlCrossRefPubMed
  4. ↵
    1. Kim G,
    2. Kang SH,
    3. Kim MY and
    4. Baik SK
    : Prognostic value of sarcopenia in patients with liver cirrhosis: A systematic review and meta-analysis. PLoS One 12: e0186990, 2017. PMID: 29065187. DOI: 10.1371/journal.pone.0186990
    OpenUrlCrossRef
    1. Meyer F and
    2. Valentini L
    : Disease-related malnutrition and sarcopenia as determinants of clinical outcome. Visc Med 35: 282-291, 2019. PMID: 31768391. DOI: 10.1159/000502867
    OpenUrlCrossRef
  6. ↵
    1. Chang KV,
    2. Chen JD,
    3. Wu WT,
    4. Huang KC,
    5. Lin HY and
    6. Han DS
    : Is sarcopenia associated with hepatic encephalopathy in liver cirrhosis? A systematic review and meta-analysis. J Formos Med Assoc 118: 833-842, 2019. PMID: 30279030. DOI: 10.1016/j.jfma.2018.09.011
    OpenUrlCrossRef
  7. ↵
    1. Anker SD,
    2. Morley JE and
    3. von HS
    : Welcome to the ICD-10 code for sarcopenia. J Cachexia Sarcopenia Muscle 7: 512-514, 2016. PMID: 27891296. DOI: 10.1002/jcsm.12147
    OpenUrlCrossRef
  8. ↵
    1. Chen LK,
    2. Woo J,
    3. Assantachai P,
    4. Auyeung TW,
    5. Chou MY,
    6. Iijima K,
    7. Jang HC,
    8. Kang L,
    9. Kim M,
    10. Kim S,
    11. Kojima T,
    12. Kuzuya M,
    13. Lee JSW,
    14. Lee SY,
    15. Lee WJ,
    16. Lee Y,
    17. Liang CK,
    18. Lim JY,
    19. Lim WS,
    20. Peng LN,
    21. Sugimoto K,
    22. Tanaka T,
    23. Won CW,
    24. Yamada M,
    25. Zhang T,
    26. Akishita M, and
    27. Arai H
    : Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. J Am Med Dir Assoc 21: 300-307.e2, 2020. PMID: 32033882. DOI: 10.1016/j.jamda.2019.12.012
    OpenUrlCrossRefPubMed
  9. ↵
    1. Cruz-Jentoft AJ,
    2. Bahat G,
    3. Bauer J,
    4. Boirie Y,
    5. Bruyère O,
    6. Cederholm T,
    7. Cooper C,
    8. Landi F,
    9. Rolland Y,
    10. Sayer AA,
    11. Schneider SM,
    12. Sieber CC,
    13. Topinkova E,
    14. Vandewoude M,
    15. Visser M and
    16. Zamboni M; 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 48: 16-31, 2019. PMID: 30312372. DOI: 10.1093/ageing/afy169
    OpenUrlCrossRefPubMed
  10. ↵
    1. Norman K,
    2. Stobäus N,
    3. Gonzalez MC,
    4. Schulzke JD amd
    5. Pirlich M
    : Hand grip strength: outcome predictor and marker of nutritional status. Clin Nutr. 30: 135-142, 2011. PMID: 21035927. DOI: 10.1016/j.clnu.2010.09.010
    OpenUrlCrossRefPubMed
    1. Bohannon RW
    : Hand-grip dynamometry predicts future outcomes in aging adults. J Geriatr Phys Ther 31: 3-10, 2008. PMID: 18489802. DOI: 10.1519/00139143-200831010-00002
    OpenUrlCrossRefPubMed
    1. Knudsen AW,
    2. Naver A,
    3. Bisgaard K,
    4. Nordgaard-Lassen I,
    5. Becker U,
    6. Krag A and
    7. Slinde F
    : Nutrition impact symptoms, handgrip strength and nutritional risk in hospitalized patients with gastroenterological and liver diseases. Scand J Gastroenterol 50: 1191-1198, 2015. PMID: 25876708. DOI: 10.3109/00365521.2015.1028994
    OpenUrlCrossRef
  13. ↵
    1. Porto JM,
    2. Nakaishi APM,
    3. Cangussu-Oliveira LM,
    4. Freire Júnior RC,
    5. Spilla SB and
    6. Abreu DCC
    : Relationship between grip strength and global muscle strength in community-dwelling older people. Arch Gerontol Geriatr 82: 273-278, 2019. PMID: 30889410. DOI: 10.1016/j.archger.2019.03.005
    OpenUrlCrossRef
  14. ↵
    1. Clark BC and
    2. Manini TM
    : What is dynapenia? Nutrition 28: 495-503, 2012. PMID: 22469110. DOI: 10.1016/j.nut.2011.12.002
    OpenUrlCrossRefPubMed
  15. ↵
    1. Yoh K,
    2. Nishikawa H,
    3. Enomoto H,
    4. Iwata Y,
    5. Ikeda N,
    6. Aizawa N,
    7. Nishimura T,
    8. Iijima H and
    9. Nishiguchi S
    : Grip strength: A useful marker for composite hepatic events in patients with chronic liver diseases. Diagnostics (Basel) 10: 238, 2020. PMID: 32325995. DOI: 10.3390/diagnostics10040238
    OpenUrlCrossRef
  16. ↵
    1. Hanai T,
    2. Shiraki M,
    3. Imai K,
    4. Suetsugu A,
    5. Takai K,
    6. Moriwaki H and
    7. Shimizu M
    : Reduced handgrip strength is predictive of poor survival among patients with liver cirrhosis: A sex-stratified analysis. Hepatol Res 49: 1414-1426, 2019. PMID: 31408558. DOI: 10.1111/hepr.13420
    OpenUrlCrossRef
    1. Leong DP,
    2. Teo KK,
    3. Rangarajan S,
    4. Lopez-Jaramillo P,
    5. Avezum A Jr.,
    6. Orlandini A,
    7. Seron P,
    8. Ahmed SH,
    9. Rosengren A,
    10. Kelishadi R,
    11. Rahman O,
    12. Swaminathan S,
    13. Iqbal R,
    14. Gupta R,
    15. Lear SA,
    16. Oguz A,
    17. Yusoff K,
    18. Zatonska K,
    19. Chifamba J,
    20. Igumbor E,
    21. Mohan V,
    22. Anjana RM,
    23. Gu H,
    24. Li W and
    25. Yusuf S; Prospective Urban Rural Epidemiology (PURE) Study investigators
    : Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet 386: 266-273, 2015. PMID: 25982160. DOI: 10.1016/S0140-6736(14)62000-6
    OpenUrlCrossRefPubMed
    1. García-Hermoso A,
    2. Ramírez-Vélez R,
    3. Peterson MD,
    4. Lobelo F,
    5. Cavero-Redondo I,
    6. Correa-Bautista JE and
    7. Martínez-Vizcaíno V
    : Handgrip and knee extension strength as predictors of cancer mortality: a systematic review and meta-analysis. Scand J Med Sci Sports 28: 1852-1858, 2018. PMID: 29723933. DOI: 10.1111/sms.13206
    OpenUrlCrossRef
    1. Malhotra R,
    2. Tareque MI,
    3. Tan NC and
    4. Ma S
    : Association of baseline hand grip strength and annual change in hand grip strength with mortality among older people. Arch Gerontol Geriatr 86: 103961, 2020. PMID: 31704626. DOI: 10.1016/j.archger.2019.103961
    OpenUrlCrossRef
    1. Wu Y,
    2. Wang W,
    3. Liu T and
    4. Zhang D
    : Association of grip strength with risk of all-cause mortality, cardiovascular diseases, and cancer in community-dwelling populations: A meta-analysis of prospective cohort studies. J Am Med Dir Assoc 18: 551.e17-551.e35, 2017. PMID: 28549705. DOI: 10.1016/j.jamda.2017.03.011
    OpenUrlCrossRefPubMed
    1. Yusuf S,
    2. Joseph P,
    3. Rangarajan S,
    4. Islam S,
    5. Mente A,
    6. Hystad P,
    7. Brauer M,
    8. Kutty, VR,
    9. Gupta R,
    10. Wielgosz A,
    11. AlHabib KF,
    12. Dans A,
    13. Lopez-Jaramillo P,
    14. Avezum A,
    15. Lanas F,
    16. Oguz A,
    17. Kruger IM,
    18. Diaz R,
    19. Yusoff K,
    20. Mony P,
    21. Chifamba J,
    22. Yeates K,
    23. Kelishadi R,
    24. Yusufali A,
    25. Khatib R,
    26. Rahman O,
    27. Zatonska K,
    28. Iqbal R,
    29. Wei L,
    30. Bo H,
    31. Rosengren A,
    32. Kaur M,
    33. Mohan V,
    34. Lear SA,
    35. Teo KK,
    36. Leong D,
    37. O’Donnell M,
    38. McKee M and
    39. Dagenais G
    : Modifiable risk factors, cardiovascular disease, and mortality in 155 722 individuals from 21 high-income, middle-income, and low-income countries (PURE): a prospective cohort study. Lancet 395: 795-808, 2020. PMID: 31492503. DOI: 10.1016/S0140-6736(19)32008-2
    OpenUrlCrossRefPubMed
    1. Celis-Morales CA,
    2. Welsh P,
    3. Lyall DM,
    4. Steell L,
    5. Petermann F,
    6. Anderson J,
    7. Iliodromiti S,
    8. Sillars A,
    9. Graham N,
    10. Mackay DF,
    11. Pell JP,
    12. Gill JMR,
    13. Sattar N and
    14. Gray SR
    : 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 361: k1651, 2018. PMID: 29739772. DOI: 10.1136/bmj.k1651
    OpenUrlAbstract/FREE Full Text
    1. Kim GR,
    2. Sun J,
    3. Han M,
    4. Park S and
    5. Nam CM
    : Impact of handgrip strength on cardiovascular, cancer and all-cause mortality in the Korean longitudinal study of ageing. BMJ Open 9: e027019, 2019. PMID: 31072857. DOI: 10.1136/bmjopen-2018-027019
    OpenUrlAbstract/FREE Full Text
    1. Nishikawa H,
    2. Enomoto H,
    3. Ishii A,
    4. Iwata Y,
    5. Miyamoto Y,
    6. Ishii N,
    7. Yuri Y,
    8. Takata R,
    9. Hasegawa K,
    10. Nakano C,
    11. Nishimura T,
    12. Yoh K,
    13. Aizawa N,
    14. Sakai Y,
    15. Ikeda N,
    16. Takashima T,
    17. Iijima H and
    18. Nishiguchi S
    : Prognostic significance of low skeletal muscle mass compared with protein-energy malnutrition in liver cirrhosis. Hepatol Res 47: 1042-1052, 2017. PMID: 27862791. DOI: 10.1111/hepr.12843
    OpenUrlCrossRef
    1. Kobayashi T,
    2. Kawai H,
    3. Nakano O,
    4. Abe S,
    5. Kamimura H,
    6. Sakamaki A,
    7. Kamimura K,
    8. Tsuchiya A,
    9. Takamura M,
    10. Yamagiwa S and
    11. Terai S
    : Rapidly declining skeletal muscle mass predicts poor prognosis of hepatocellular carcinoma treated with transcatheter intra-arterial therapies. BMC Cancer 18: 756, 2018. PMID: 30041616. DOI: 10.1186/s12885-018-4673-2
    OpenUrlCrossRef
    1. Ebadi M,
    2. Wang CW,
    3. Lai JC,
    4. Dasarathy S,
    5. Kappus MR,
    6. Dunn MA,
    7. Carey EJ and
    8. Montano-Loza AJ; From the Fitness, Life Enhancement, and Exercise in Liver Transplantation (FLEXIT) Consortium
    : Poor performance of psoas muscle index for identification of patients with higher waitlist mortality risk in cirrhosis. J Cachexia Sarcopenia Muscle 9: 1053-1062, 2018. PMID: 30269421. DOI: 10.1002/jcsm.12349
    OpenUrlCrossRefPubMed
    1. Hamaguchi Y,
    2. Kaido T,
    3. Okumura S,
    4. Kobayashi A,
    5. Shirai H,
    6. Yao S,
    7. Yagi S,
    8. Kamo N,
    9. Seo S,
    10. Taura K,
    11. Okajima H and
    12. Uemoto S
    : Preoperative visceral adiposity and muscularity predict poor outcomes after hepatectomy for hepatocellular carcinoma. Liver Cancer 8: 92-109, 2019. PMID: 31019900. DOI: 10.1159/000488779
    OpenUrlCrossRef
    1. Ishizu Y,
    2. Ishigami M,
    3. Kuzuya T,
    4. Honda T,
    5. Hayashi K,
    6. Ishikawa T,
    7. Hirooka Y and
    8. Goto H
    : Low skeletal muscle mass predicts early mortality in cirrhotic patients with acute variceal bleeding. Nutrition. 42: 87-91, 2017. PMID: 28870485. DOI: 10.1016/j.nut.2017.06.004
    OpenUrlCrossRef
    1. Montano-Loza AJ,
    2. Angulo P,
    3. Meza-Junco J,
    4. Prado CM,
    5. Sawyer MB,
    6. Beaumont C,
    7. Esfandiari N,
    8. Ma M and
    9. Baracos VE
    : Sarcopenic obesity and myosteatosis are associated with higher mortality in patients with cirrhosis. J Cachexia Sarcopenia Muscle 7: 126-135, 2016. PMID: 27493866. DOI: 10.1002/jcsm.12039
    OpenUrlCrossRef
  30. ↵
    1. Fujiwara N,
    2. Nakagawa H,
    3. Kudo Y,
    4. Tateishi R,
    5. Taguri M,
    6. Watadani T,
    7. Nakagomi R,
    8. Kondo M,
    9. Nakatsuka T,
    10. Minami T,
    11. Sato M,
    12. Uchino K,
    13. Enooku K,
    14. Kondo Y,
    15. Asaoka Y,
    16. Tanaka Y,
    17. Ohtomo K,
    18. Shiina S and
    19. Koike K
    : Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma. J Hepatol 63: 131-140, 2015. PMID: 25724366. DOI: 10.1016/j.jhep.2015.02.031
    OpenUrlCrossRef
  31. ↵
    1. Hiraoka A,
    2. Michitaka K,
    3. Izumoto H,
    4. Ueki H,
    5. Kitahata S,
    6. Aibiki T,
    7. Okudaira T,
    8. Yamago H,
    9. Miyamoto Y,
    10. Iwasaki R,
    11. Tomida H,
    12. Mori K,
    13. Miyata H,
    14. Tsubouchi E,
    15. Kishida M,
    16. Hirooka M,
    17. Abe M,
    18. Matsuura B,
    19. Ninomiya T and
    20. Hiasa Y
    : Relative changes in handgrip strength and skeletal muscle volume in patients with chronic liver disease over a 2-year observation period. Hepatol Res 48: 502-508, 2018. PMID: 25724366. DOI: 10.1016/j.jhep.2015.02.031
    OpenUrlCrossRef
  32. ↵
    1. Fukui H,
    2. Saito H,
    3. Ueno Y,
    4. Uto H,
    5. Obara K,
    6. Sakaida I,
    7. Shibuya A,
    8. Seike M,
    9. Nagoshi S,
    10. Segawa M,
    11. Tsubouchi H,
    12. Moriwaki H,
    13. Kato A,
    14. Hashimoto E,
    15. Michitaka K,
    16. Murawaki T,
    17. Sugano K,
    18. Watanabe M and
    19. Shimosegawa T
    : Evidence-based clinical practice guidelines for liver cirrhosis 2015. J Gastroenterol 51: 629-650, 2016. PMID: 27246107. DOI: 10.1007/s00535-016-1216-y
    OpenUrlCrossRefPubMed
    1. Kokudo N,
    2. Takemura N,
    3. Hasegawa K,
    4. Takayama T,
    5. Kubo S,
    6. Shimada M,
    7. Nagano H,
    8. Hatano E,
    9. Izumi N,
    10. Kaneko S,
    11. Kudo M,
    12. Iijima H,
    13. Genda T,
    14. Tateishi R,
    15. Torimura T,
    16. Igaki H,
    17. Kobayashi S,
    18. Sakurai H,
    19. Murakami T,
    20. Watadani T and
    21. Matsuyama Y
    : Clinical practice guidelines for hepatocellular carcinoma: The Japan Society of Hepatology 2017 (4th JSH-HCC guidelines) 2019 update. Hepatol Res 49: 1109-1113, 2019. PMID: 31336394. DOI: 10.1111/hepr.13411
    OpenUrlCrossRef
    1. European Association for the Study of the Liver
    : EASL Recommendations on Treatment of Hepatitis C 2018. J Hepatol 69: 461-511, 2018. PMID: 29650333. DOI: 10.1016/j.jhep.2018.03.026
    OpenUrlCrossRefPubMed
  35. ↵
    1. Drafting Committee for Hepatitis Management Guidelines and the Japan Society of Hepatology
    : Japan Society of Hepatology Guidelines for the Management of Hepatitis B Virus Infection: 2019 update. Hepatol Res 50: 892-923, 2020. PMID: 32343469. DOI: 10.1111/hepr.13504
    OpenUrlCrossRef
  36. ↵
    1. Nishikawa H,
    2. Shiraki M,
    3. Hiramatsu A,
    4. Moriya K,
    5. Hino K and
    6. 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 46: 951-963, 2016. PMID: 27481650. DOI: 10.1111/hepr.12774
    OpenUrlCrossRef
  37. ↵
    1. Nishikawa H,
    2. Yoh K,
    3. Enomoto H,
    4. Ishii N,
    5. Iwata Y,
    6. Nakano C,
    7. Takata R,
    8. Nishimura T,
    9. Aizawa N,
    10. Sakai Y,
    11. Ikeda N,
    12. Hasegawa K,
    13. Takashima T,
    14. Iijima H and
    15. Nishiguchi S
    : Extracellular water to total body water ratio in viral liver diseases: A study using bioimpedance analysis. Nutrients 10: 1072, 2018. PMID: 30103528. DOI: 10.3390/nu10081072
    OpenUrlCrossRef
  38. ↵
    1. Nishikawa H,
    2. Enomoto H,
    3. Yoh K,
    4. Iwata Y,
    5. Sakai Y,
    6. Kishino K,
    7. Ikeda N,
    8. Takashima T,
    9. Aizawa N,
    10. Takata R,
    11. Hasegawa K,
    12. Ishii N,
    13. Yuri Y,
    14. Nishimura T,
    15. Iijima H and
    16. Nishiguchi S
    : Walking speed: Japanese data in chronic liver diseases. J Clin Med 9: pii: E166, 2020. PMID: 31936162. DOI: 10.3390/jcm9010166
    OpenUrlCrossRef
  39. ↵
    1. Toyama T,
    2. van den Broek-Best O,
    3. Ohkuma T,
    4. Handelsman D,
    5. Waite LM,
    6. Seibel MJ,
    7. Cumming R,
    8. Naganathan V,
    9. Sherrington C,
    10. Hirani V and
    11. Wang AY
    : Associations of impaired renal function with declines in muscle strength and muscle function in older men: Findings From the CHAMP Study. J Gerontol A Biol Sci Med Sci 74: 1812-1820, 2019. PMID: 31086955. DOI: 10.1093/gerona/glz100
    OpenUrlCrossRef
  40. ↵
    1. Sung JH,
    2. Uojima H,
    3. Hidaka H,
    4. Tanaka Y,
    5. Wada N,
    6. Kubota K,
    7. Nakazawa T,
    8. Shibuya A,
    9. Fujikawa T,
    10. Yamanoue H,
    11. Kako M and
    12. Koizumi W
    : Risk factors for loss of skeletal muscle mass in patients with cirrhosis. Hepatol Res 49: 550-558, 2019. PMID: 30623996. DOI: 10.1111/hepr.13308
    OpenUrlCrossRef
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Predictors for Grip Strength Loss in Patients With Chronic Liver Diseases
HIROKI NISHIKAWA, KAZUNORI YOH, HIRAYUKI ENOMOTO, NAOTO IKEDA, TOMOYUKI TAKASHIMA, NOBUHIRO AIZAWA, TAKASHI NISHIMURA, SHUHEI NISHIGUCHI, HIROKO IIJIMA
In Vivo Jan 2021, 35 (1) 363-371; DOI: 10.21873/invivo.12267
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