Enhanced echo intensity of skeletal muscle is associated with poor physical function in hemodialysis patients:a cross-sectional study | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Enhanced echo intensity of skeletal muscle is associated with poor physical function in hemodialysis patients:a cross-sectional study Dongsheng Cheng, Junzhen Wu, Haiqing Luo, Shunrong Ren, Longxiang Shen, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-1325735/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted 10 You are reading this latest preprint version Abstract Background: The objective of this study was to evaluate the relationship between ultrasound echo intensity (EI) of skeletal muscle and physical function of patients on maintenance hemodialysis. Methods: Cross-sectional area (CSA) and mean EI of the right rectus femoris were measured by ultrasound to evaluate the quantity and quality of the muscle, respectively. Physical function was measured by handgrip strength (HGS), gait speed, sit-to-stand 60 s (STS-60) test, and instrumental activities of daily living (IADL) scale. Results: A total of 107 patients on hemodialysis were included, with women accounting for 37.3% (n = 40), and a mean age of 53.53 ± 12.52 years. Among the patients on hemodialysis, EI was moderately and negatively correlated with HGS (r = −0.467, P < 0.001), gait speed (r = −0.285, P = 0.003), and STS-60 (r = −0.313, P = 0.001). Multiple regression analyses adjusted for CSA showed that the enhanced EI of patients on hemodialysis remained associated with worse HGS (β = −0.207, P = 0.047), lower gait speed (β = −0.002, P = 0.001), less STS-60 (β = −0.136, P = 0.049), and a higher likelihood of dependency in IADL (Odds Ratio: 1.070, 95% CI: [1.033–1.111], P = 0.001). Conclusions: In patients on hemodialysis, enhanced EI in the skeletal muscle measured via ultrasound was correlated with poor physical performance. The combined muscle quality and muscle quantity evaluation provides more information for assessing the level of physical function of the patients. Muscle quality Ultrasound Physical performance End-stage renal disease Activities of daily living Figures Figure 1 Figure 2 Introduction Patients on hemodialysis often suffer from reduced muscle strength and exercise capacity, lowering their autonomy and quality of life and shortening survival time [1]. Decreased muscle mass is one of the main causes of reduced muscle strength and exercise capacity [2, 3]. A recent study showed that muscle quality is decreased significantly at the same time as or before the decrease in muscle mass [4]. Studies of the elderly have also reported that the decline of muscle quality is closely related to the decline in physical function and poor prognosis of patients [5, 6]. Therefore, both the quantity and quality of muscle affects muscle function. Joint evaluation may help formulate intervention measures and improve prognosis. Muscle quality is a relative new term that refers to the microscopic and macroscopic changes in muscle structure and composition and the level of muscle function from each muscle mass unit [7]. The existing research methods for evaluating muscle quality are mainly measurements of the amount of fat penetrating into the muscle determined through computed tomography (CT), magnetic resonance imaging (MRI), and muscle radiation attenuation by CT. CT measurement of mid-thigh intermuscular adipose tissue predicts usual gait velocity and 6-min walk distance of patients on hemodialysis [2]. However, only a few studies focused on evaluating the muscle quality of patients on hemodialysis are available. Ultrasound can effectively assess muscle mass and muscle quality with good internal and external consistency [8]. It also has the advantages of bedside operation, convenience, non-invasiveness, and lack of radiation exposure, and is widely studied as a tool in muscle assessment. Echo intensity (EI) is an important indicator for ultrasound assessment of muscle quality. Enhanced EI indicates increased infiltration of fibrotic tissue and/or adipose tissue in the muscle and represents reduced muscle quality [9]. Numerous studies in the elderly have shown that an increase in EI is related to decline of muscle strength and physical function [10-12]. A recent study involving 61 patients with chronic kidney disease (CKD) showed that patients with high EI had low physical function [13]. However, to date, there are no relevant studies evaluating ultrasound derived EI in patients on hemodialysis. Hence, this study clarified the application value of ultrasound EI of skeletal muscle in patients on hemodialysis by evaluating the relationship between ultrasound EI and physical function. Methods Study population This study screened outpatients on maintenance hemodialysis in our county hospital from July 2020 to August 2020. The inclusion criteria of this study included patients who had undergone more than 3 months of hemodialysis. patients on hemodialysis who could not walk or were completely blind were excluded. We screened a total of 110 patients and excluded 3 patients who could not walk. A total of 107 subjects were eventually enrolled. The research was conducted in accordance with the Helsinki Declaration. This study was also approved by the ethics committee of our hospital. All subjects signed the written informed consent, and then their demographic information, past medical history, and duration of dialysis were collected. Various body measurements and assessments of physical function were performed before hemodialysis. A complete ultrasound examination of the right rectus femoris was also performed after hemodialysis. Body measurements and assessments of physical function Measurement of body mass index (BMI) BMI measurement of individual research subjects was calculated based on body dry weight and the following formula: BMI (Kg/m 2 ) = body weight/height 2 . Measurement of handgrip strength (HGS) HGS of individual subjects was measured before hemodialysis. Patients with internal arteriovenous fistula were subjected to HGS measurement on the non-fistula hand twice to obtain the maximum value. Patients using tunneled cuffed catheters were subjected to the HGS measurement on the dominant hand twice to obtain the maximum value. Gait speed Individual subjects were required to walk independently for a 4-meter distance, followed by recording of the completion time and calculation of the gait speed (meter/second) twice to obtain the maximum value. Sit-to-stand 60 s (STS-60) test The number of times an individual patient stood up and sat down on a chair within 60 seconds was calculated. This STS-60 test assessed the strength and endurance of muscles of the lower limbs of the tested subject [14]. The patient was asked to complete the sit down-stand up-sit down movement as many times as possible within 60 seconds by holding his/her hands in front of the chest and starting from the sitting position. The number of STS-60 movements was recorded at the end of the test. Dependence in IADL Physical function was also measured using the instrumental activities of daily living (IADL) scale [15, 16]. The IADL scale included 8 items: ability to shop on the street, do outdoor activities, cook meals, do household activities, wash clothes, use the telephone, take medications, and handle personal finances. The evaluation of the results of each item were divided into 3 levels: completion with no assistance, completion with partial assistance, and completion with full assistance. The IADL scale of individuals with any item which needed assistance (including partial or full assistance) was characterized as impaired IADL, otherwise IADL was characterized as intact. Ultrasound measurement A portable ultrasound machine with a 60-mm width curvilinear transducer (2–5 MHz, S II, SonoSite, USA) was used to gain enough ultrasound window to cover the whole width of the rectus femoris muscle. All ultrasounds were standardized by the default machine settings (depth, gain, and focus). One experienced pain physician who had been practicing musculoskeletal ultrasound more than 10 years obtained all the images. B-mode 2D ultrasonography of the right rectus femoris was taken immediately once hemodialysis was finished. The patient would lie in the supine position at a 45° angle, with the rectus femoris muscle relaxed. A line at the midpoint between the anterior superior iliac spine and the superior patellar border was marked. The ultrasound transducer was placed perpendicular to the longitudinal axis of the thigh, overlying the line. Minimal pressure was applied to avoid muscle distortion. In the transverse ultrasound image, the rectus femoris muscle was confirmed and the muscle epimysium boundary was identified as an oval circle wrapping around the muscle fibers. Two images from the same point for each person were saved. Ultrasound images were transferred to the computer for measurements using Image J software (National Institute of Health, USA). The whole rectus femoris muscle within its epimysium was circled as the region of interest for cross sectional area (CSA) and mean EI measurement (Figure 1). The software returned measures of CSA and the mean EI, which was expressed as a value between 0 (black) and 255 (white) (Figure 1). The average CSA and mean EI values of two images for the same patient were analyzed. Statistical analysis Continuous data are presented as mean ± standard deviation, and categorical data are presented as a percentage. For continuous data, one-way ANOVA was used to compare two groups when normal distribution was fulfilled; otherwise, the non-parametric Wilcoxon rank sum test was performed. For categorical data, the chi-square test was performed. The association of EI with physical function was examined using Pearson’s correlation analysis. Multiple linear regression (continuous outcomes) and logistics regression (dichotomous outcomes) were performed to assess the independent association of EI and CSA with physical function. The two model methods were as follows: Model 1—only adjusted for EI and CSA; Model 2—further adjusted for age, gender,and dialysis duration. All statistical analyses were performed using MedCalc Software (Version 18.2.1 MedCalc Software Ltd, Belgium). P < 0.05 was considered statistically significant. Results Patient characteristics A total of 107 patients on maintenance hemodialysis were enrolled in this study. Patients were 37.3% female (n = 40), mean age was 53.53 ± 12.52 years, average dialysis duration was 2.97 ± 2.32 years, and average BMI was 21.43 ± 3.77 kg/m 2 . In addition, 15.9% of the patients had diabetes (n = 17), 93.5% of the patients had hypertension (n = 100), and 26.2% (n = 28) of the patients had dependency in IADL. As shown in Table 1, no significant differences in age, BMI, prevalence of hypertension, or duration of hemodialysis were found between males and females. However, the prevalence of diabetes in the male group was higher than in the female group (P = 0.018). In terms of physical function, male patients on hemodialysis had significantly stronger HGS than the female patients (P 0.05). In terms of ultrasound parameters of the rectus femoris, the EI value of the male group was significantly lower than in the female group, and the CSA of the male group was significantly higher than the female group (P < 0.001). Relationship between muscle quality and physical function As shown in Figure 2, the EI of the overall patient population on hemodialysis was negatively correlated with HGS (r = −0.467, P < 0.001), gait speed (r = −0.285, P = 0.003), and STS-60 (r = −0.313, P = 0.001). Comparison of physical function with muscle quality (EI) and muscle quantity (CSA) Further multiple linear regression analyses and logistic regression analyses were performed to assess the relationship between EI, CSA, and physical function. As shown in Table 2, Model 1 adjusted for the EI and CSA, and Model 2 further adjusted for age, gender, and dialysis duration. Enhanced EI was associated with worse HGS (β = −0.207, P = 0.047), lower gait speed (β = −0.002, P = 0.001), less STS-60 (β = −0.136, P = 0.049), and a higher likelihood of dependency in IADL in Model 1 (OR: 1.070; 95% CI: [1.030–1.111], P = 0.001), but was only associated with dependency in IALD (P = 0.001) in Model 2. Except for STS-60, increased CSA was a significant predictor of better HGS, higher gait speed, and lower IALD disability in both Model 1 and Model 2 in patients on hemodialysis. Discussion This study was the first to report the relationship between ultrasound derived EI of the skeletal muscle and physical function in patients on hemodialysis. Our results showed that high EI was closely related to low physical function including HGS, gait speed, STS-60, and IADL disability in patients on hemodialysis. The pathophysiological mechanisms of decreased muscle quality include muscle fiber reduction, mitochondrial dysfunction of myocytes, intramuscular fat infiltration, and increased fibrosis [17]. The existing assessment methods of muscle quality mainly include CT, MRI, and ultrasound. Although CT and MRI directly evaluate the degree of intramuscular fat infiltration, they are expensive and require patients go to a specific place or have a certain degree of radiation, which affects patient compliance with the examination. Numerous studies in the elderly have confirmed the close relationship between ultrasound derived EI and physical function. However, in the field of kidney diseases, only one small-scale study of stages 3–5 CKD pre-dialysis patients has reported that EI is moderately and negatively correlated with the STS-60 test, the incremental shuttle walk test (ISWT) (n=61), and peak oxygen consumption (VO 2 peak) results (n = 32), but not with the gait speed and HGS (n = 29); EI was not correlated with any index of physical function when the CSA was corrected [13]. In this study, EI was moderately and negatively correlated with HGS, gait speed, and STS-60 in patients on hemodialysis. Moreover, after adjusting for muscle area, high EI in patients on hemodialysis remained associated with worse HGS, low gait speed, reduced STS-60, and IADL disability. Thus, this is the first report showing the value of ultrasound derived EI in muscle evaluation of patients on hemodialysis. In addition to muscle quality, muscle quantity is also an important indicator for muscle evaluation of patients. A wealth of evidence from multiple studies has shown that muscle size is closely related to the physical function of patients on hemodialysis [2, 3, 18]. When we further corrected for factors such as age, gender, and the duration of dialysis, only CSA was related to the level of physical function of the patients. Thus, in the clinical setting, the combined evaluation of muscle quantity and muscle quality may provide more information for accurately assessing muscle strength and physical function in patients [19]. Interestingly, analysis of the ultrasound parameters of the rectus femoris showed that the CSA of the male group was significantly higher than in the female group, and the EI value of the male group was significantly lower than in the female group. These phenomena are consistent with our expectations. Male muscles are stronger, with larger CSA of the rectus femoris muscle. In addition, the proportion of body fat in the females was generally higher than that of males. Thus, the EI value of the female skeletal muscle was higher. Loss of muscle quantity and quality in patients on hemodialysis may be related to factors such as increased oxidative stress, accumulation of uremic toxins, reduced exercise activities, and malnutrition [20, 21]. Exercise training is an effective way to improve muscle function. In patients with CKD, ultrasound measurement of CSA has been used to effectively assesses muscle mass gain after exercise intervention [22]. Impendence movement reduced the accumulation of fat in the muscles of the elderly [23]. However, there is still a lack of research on the improvement of muscle quality through exercise in patients on hemodialysis. In addition, further research is needed to verify whether EI can be used as an evaluation index of the improvement of muscle quality. Ultrasound-based evaluation of muscle quantity and quality of patients on hemodialysis provided more information for assessing the level of physical function in patients. The ultrasound method has the advantages of simplicity, convenience, non-invasiveness, and without radiation exposure. It has important clinical value and wide application prospects in the muscle evaluation of patients on hemodialysis. This study had some limitations: First, no standardized measurement method for EI is currently available, and the measurement of EI is also affected by different machine parameters. Thus, EI values may differ between different studies and are not comparable. Second, this was a cross-sectional study, and therefore it is impossible to clarify the etiological inference of the decline in muscle quality represented by EI and the decreased physical function of patients on hemodialysis. In addition, this study was carried out in a single dialysis center in China, and the generalization of our conclusions requires international, multi-center studies. Conclusion The present study revealed that enhanced US-derived EI was correlated with poor physical performance in patients on hemodialysis. The combined muscle quality and muscle quantity evaluation provides more information for assessing the level of physical function of the patients. Abbreviations EI: Echo intensity; CSA: Cross-sectional area; HGS: Handgrip strength; STS-60: Gait speed, sit-to-stand 60 s; IADL: Instrumental activities of daily living; CT: computed tomography; MRI: magnetic resonance imaging; CKD: chronic kidney disease; BMI: Body mass index; ISWT: incremental shuttle walk test; SD: Standard deviation; SE: Standard error. Declarations Ethics approval and consent to participate The study protocol complied with the Helsinki Declaration standards and was approved by the Ethics Committee of the People's Hospital of Menghai County (approval number 2020-SNK-001) and Shanghai Jiao Tong University Affiliated Sixth People’s Hospital (approval number 2020-175). All subjects signed the written informed consent. Consent for publication Not Applicable. Availability of data and materials All data generated or analysed during this study are included in this published article. Competing interests The authors declare that they have no competing interests. Funding This work was supported by grants from the Shanghai Municipal Health Commission [grant number 20194y0347], and the National Natural Science Foundation of China [grant numbers 81670657,81870504, 81870468]. Authors' contributions JZW and HQL contributed to the conception of the study, performed statistical analysis and wrote the initial manuscript draft. JZW, SRR and LXS participated in study coordination, performed the recruitment, took the measures and collected the data. DSC and NSW contributed to the conception of the study, supervised the study, helped to interpret the results and corrected the draft. All authors read and approved the final manuscript. Acknowledgements We wish to thank Dr. Jing Chen and Dr Zhenyi Jia for their assistance and thoughtful academic discussions with the current study. References Jassal SV, Karaboyas A, Comment LA, Bieber BA, Morgenstern H, Sen A, et al. Functional Dependence and Mortality in the International Dialysis Outcomes and Practice Patterns Study (DOPPS). Am J Kidney Dis. 2016;67(2):283-92. doi: 10.1053/j.ajkd.2015.09.024. Cheema B, Abas H, Smith B, O'Sullivan AJ, Chan M, Patwardhan A, et al. Investigation of skeletal muscle quantity and quality in end-stage renal disease. Nephrology (Carlton). 2010;15(4):454-63. doi: 10.1111/j.1440-1797.2009.01261.x. McIntyre CW, Selby NM, Sigrist M, Pearce LE, Mercer TH, Naish PF. Patients receiving maintenance dialysis have more severe functionally significant skeletal muscle wasting than patients with dialysis-independent chronic kidney disease. Nephrol Dial Transplant. 2006;21(8):2210-6. doi: 10.1093/ndt/gfl064. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-85. doi: 10.3945/ajcn.2009.28047. Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci. 2005;60(3):324-33. doi: 10.1093/gerona/60.3.324. Correa-de-Araujo R, Harris-Love MO, Miljkovic I, Fragala MS, Anthony BW, Manini TM. The Need for Standardized Assessment of Muscle Quality in Skeletal Muscle Function Deficit and Other Aging-Related Muscle Dysfunctions: A Symposium Report. Front Physiol. 2017;8:87. doi: 10.3389/fphys.2017.00087. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16-31. doi: 10.1093/ageing/afy169. Nijholt W, Scafoglieri A, Jager-Wittenaar H, Hobbelen JSM, van der Schans CP. The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia Sarcopenia Muscle. 2017;8(5):702-12. doi: 10.1002/jcsm.12210. Grimm A, Teschner U, Porzelius C, Ludewig K, Zielske J, Witte OW, et al. Muscle ultrasound for early assessment of critical illness neuromyopathy in severe sepsis. Critical care (London, England). 2013;17(5):R227. doi: 10.1186/cc13050. Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Mori N, et al. Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-aged and elderly persons. Eur J Appl Physiol. 2012;112(4):1519-25. doi: 10.1007/s00421-011-2099-5. Watanabe Y, Yamada Y, Fukumoto Y, Ishihara T, Yokoyama K, Yoshida T, et al. Echo intensity obtained from ultrasonography images reflecting muscle strength in elderly men. Clin Interv Aging. 2013;8:993-8. doi: 10.2147/CIA.S47263. Wilhelm EN, Rech A, Minozzo F, Radaelli R, Botton CE, Pinto RS. Relationship between quadriceps femoris echo intensity, muscle power, and functional capacity of older men. Age (Dordr). 2014;36(3):9625. doi: 10.1007/s11357-014-9625-4. Wilkinson TJ, Gould DW, Nixon DGD, Watson EL, Smith AC. Quality over quantity ? Association of skeletal muscle myosteatosis and myofibrosis on physical function in chronic kidney disease. Nephrol Dial Transplant. 2019;34(8):1344-53. doi: 10.1093/ndt/gfy139. Rikli RE, Jones CJ. Development and validation of criterion-referenced clinically relevant fitness standards for maintaining physical independence in later years. Gerontologist. 2013;53(2):255-67. doi: 10.1093/geront/gns071. Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 1969;9(3):179-86. Cheng XS, Myers J, Han J, Stedman MR, Watford DJ, Lee J, et al. Physical Performance Testing in Kidney Transplant Candidates at the Top of the Waitlist. Am J Kidney Dis. 2020:S0272-6386(20)30728-9. doi: 10.1053/j.ajkd.2020.04.009. Russ DW, Gregg-Cornell K, Conaway MJ, Clark BC. Evolving concepts on the age-related changes in "muscle quality". J Cachexia Sarcopenia Muscle. 2012;3(2):95-109. doi: 10.1007/s13539-011-0054-2. Giglio J, Kamimura MA, Lamarca F, Rodrigues J, Santin F, Avesani CM. Association of Sarcopenia With Nutritional Parameters, Quality of Life, Hospitalization, and Mortality Rates of Elderly Patients on Hemodialysis. J Ren Nutr. 2018;28(3):197-207. doi: 10.1053/j.jrn.2017.12.003. Bourgeois B, Fan B, Johannsen N, Gonzalez MC, Ng BK, Sommer MJ, et al. Improved strength prediction combining clinically available measures of skeletal muscle mass and quality. J Cachexia Sarcopenia Muscle. 2019;10(1):84-94. doi: 10.1002/jcsm.12353. Moorthi RN, Avin KG. Clinical relevance of sarcopenia in chronic kidney disease. Curr Opin Nephrol Hypertens. 2017;26(3):219-28. doi: 10.1097/MNH.0000000000000318. Song YR, Kim JK, Lee HS, Kim SG, Choi EK. Serum levels of protein carbonyl, a marker of oxidative stress, are associated with overhydration, sarcopenia and mortality in hemodialysis patients. BMC Nephrol. 2020;21(1):281. doi: 10.1186/s12882-020-01937-z. Gould DW, Watson EL, Wilkinson TJ, Wormleighton J, Xenophontos S, Viana JL, et al. Ultrasound assessment of muscle mass in response to exercise training in chronic kidney disease: a comparison with MRI. J Cachexia Sarcopenia Muscle. 2019;10(4):748-55. doi: 10.1002/jcsm.12429. Marcus RL, Addison O, Kidde JP, Dibble LE, Lastayo PC. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging. 2010;14(5):362-6. doi: 10.1007/s12603-010-0081-2. Tables Table 1 Patient characteristics, ultrasound measurements and physical performance in both sexes Men (n=67) Women (n=40) P Age (yr) 54.79±13.39 51.42±10.74 0.179 BMI (kg/m 2 ) 21.81±3.73 20.78±3.79 0.172 EI 58.21±16.59 69.26±12.93 < 0.001 CSA (cm 2 ) 6.91±1.55 5.46±1.20 < 0.001 Ethnicity 0.126 Han, n (%) 20 (29.9) 9 (22.5) Dai, n (%) 20 (29.9) 21 (52.5) Hani, n (%) 14 (20.9) 6 (15.0) Other, n (%) 13 (19.4) 4 (10.0) Hypertension, n (%) 63 (94.0) 37 (92.5) 0.758 Diabetes, n (%) 15 (22.4) 2 (5.0) 0.018 Primary disease 0.104 Chronic glomerulonephritis, n (%) 10 (14.9) 11 (27.5) Diabetic nephropathy, n (%) 14 (20.9) 2 (5.0) Hypertensive nephropathy, n (%) 9 (13.4) 5 (12.5) Obstructive nephropathy, n (%) 9 (13.4) 3 (7.5) Other or unknown, n (%) 25 (37.3) 19 (47.5) Dialysis duration (yr) 3.06±2.54 2.82±1.93 0.607 Physical performance measures HGS (kg) 31.27±9.81 21.37±4.36 < 0.001 Gait speed (m/s) 0.97±0.19 0.93±0.14 0.252 STS-60 (repetitions) 30.12±8.44 28.85±7.99 0.445 Dependency in IADL, n (%) 19 (28.4) 9 (22.5) 0.507 BMI, body mass index; EI, echo intensity; CSA, cross-sectional area; HGS, handgrip strength; STS-60, sit-to-stand 60 s; IADL, instrumental activities of daily living. Values are presented as mean (SD) for continuous values, and n (%) for categorical values. Table 2 Comparisons of physical function with muscle quality (EI) and muscle quantity (CSA) in all patients on hemodialysis. Model 1 Model 2 β (SE) P β (SE) P HGS (kg) EI −0.207 (0.047) <0.001 −0.090 (0.047) 0.061 CSA 2.527 (0.479) <0.001 1.393 (0.483) 0.005 Gait speed (m/s) EI −0.002 (0.001) 0.028 −0.002 (0.001) 0.130 CSA 0.030 (0.010) 0.003 0.030 (0.011) 0.009 STS-60 (repetitions) EI −0.136 (0.049) 0.006 −0.081 (0.051) 0.119 CSA 0.892 (0.497) 0.075 0.747 (0.522) 0.156 Odds ratio (95% CI) P Odds ratio (95% CI) P Dependency in IADL EI 1.070 (1.030–1.1112) 0.001 1.086 (1.033–1.141) 0.001 CSA 0.569 (0.376–0.860) 0.008 0.438 (0.255–0.755) 0.003 Multiple linear regression for continuous outcomes and logistic regression for dichotomous outcomes. Model 1: EI + CSA; Model 2: model 1 + sex + age+ dialysis duration. HGS, handgrip strength; EI, echo intensity; CSA, cross-sectional area; STS-60, sit-to-stand 60 s; IADL, instrumental activities of daily living. Additional Declarations No competing interests reported. Cite Share Download PDF Status: Under Review Version 1 posted Editorial decision: Major revision 18 Apr, 2022 Reviews received at journal 06 Apr, 2022 Reviewers agreed at journal 06 Apr, 2022 Reviewers agreed at journal 21 Feb, 2022 Reviewers agreed at journal 21 Feb, 2022 Reviewers invited by journal 21 Feb, 2022 Editor assigned by journal 21 Feb, 2022 Editor invited by journal 07 Feb, 2022 Submission checks completed at journal 07 Feb, 2022 First submitted to journal 03 Feb, 2022 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-1325735","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":81921933,"identity":"c9d8020f-111b-4dfd-bf02-dcc97514d94b","order_by":0,"name":"Dongsheng Cheng","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAy0lEQVRIiWNgGAWjYBACNvbGxgcfeCTq+9kbiNTCx3O42XCGjAXjzJ4DRGqRk0hvk+axqWDccCOBWIdJJDZIzsiRYGa4+XjjDYYam2jCWngeNhh8OCPBxjg7rdiC4VhabgNBLeyJDYkzeyR4mKVzzCQYGw4ToYUhseEw7z8JCTbJM8Rq4UhsbObhkTDgkeAhVgvPwWbGGTwSCRI8QL8kEOMX+fb25z8+8NQl2B8/vPHGhxobwlqQgYFEAinKIVpI1TEKRsEoGAUjAwAAnYQ9BVMObyQAAAAASUVORK5CYII=","orcid":"","institution":"Shanghai Jiao Tong University Affiliated Sixth People's Hospital","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Dongsheng","middleName":"","lastName":"Cheng","suffix":""},{"id":81921929,"identity":"aad72796-3736-4433-840e-2392ecf7d2bc","order_by":1,"name":"Junzhen Wu","email":"","orcid":"","institution":"Shanghai Jiao Tong University Affiliated Sixth People's Hospital","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Junzhen","middleName":"","lastName":"Wu","suffix":""},{"id":81921930,"identity":"e8fdfe58-a282-415d-9a02-ddab1af5eb40","order_by":2,"name":"Haiqing Luo","email":"","orcid":"","institution":"People's Hospital of Menghai County","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Haiqing","middleName":"","lastName":"Luo","suffix":""},{"id":81921931,"identity":"c5fa708f-6cfd-41be-a30a-3e849c07cf3b","order_by":3,"name":"Shunrong Ren","email":"","orcid":"","institution":"People's Hospital of Menghai County","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Shunrong","middleName":"","lastName":"Ren","suffix":""},{"id":81921932,"identity":"099d3e86-3ae4-4612-85ff-6d1c7dc339d3","order_by":4,"name":"Longxiang Shen","email":"","orcid":"","institution":"Shanghai Jiao Tong University Affiliated Sixth People's Hospital","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Longxiang","middleName":"","lastName":"Shen","suffix":""},{"id":81921934,"identity":"c684688b-fad6-4f47-9c9b-2efc8d08e1e3","order_by":5,"name":"Niansong Wang","email":"","orcid":"","institution":"Shanghai Jiao Tong University Affiliated Sixth People's Hospital","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Niansong","middleName":"","lastName":"Wang","suffix":""}],"badges":[],"createdAt":"2022-02-04 02:14:05","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-1325735/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-1325735/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":18454621,"identity":"90fea078-b541-4f14-8ed1-306073b65f76","added_by":"auto","created_at":"2022-02-21 20:45:03","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":326158,"visible":true,"origin":"","legend":"\u003cp\u003eRepresentative ultrasound image of a relaxed rectus femoris. Rectus Femoris cross-sectional area is outlined by the dotted line. The histogram analysis for computerized quantitative grayscale analysis is illustrated at the lower right corner of the image. RF, rectus femoris; VL, vastus lateralis; VI, vastus intermedius\u003c/p\u003e","description":"","filename":"Figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-1325735/v1/8389ab62d3e18c2873b8e9b2.png"},{"id":18454622,"identity":"24e81dc1-2b76-490c-b6f0-1a5b35a1b1c7","added_by":"auto","created_at":"2022-02-21 20:45:03","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":151277,"visible":true,"origin":"","legend":"\u003cp\u003eCorrelation between echo intensity and physical function in all patients. a. HGS; b. Gait speed; c. STS-60. HGS, handgrip strength; STS-60, sit-to-stand 60 s\u003c/p\u003e","description":"","filename":"Figure2.png","url":"https://assets-eu.researchsquare.com/files/rs-1325735/v1/54be61049fcba3b5324dc70c.png"},{"id":18454623,"identity":"6c7510c0-903a-4169-8509-fc4e7f3a53e5","added_by":"auto","created_at":"2022-02-21 20:45:06","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":442724,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-1325735/v1/a06e235c-32f7-467d-8000-1663eefa295d.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Enhanced echo intensity of skeletal muscle is associated with poor physical function in hemodialysis patients:a cross-sectional study","fulltext":[{"header":"Introduction","content":"\u003cp\u003ePatients on hemodialysis often suffer from reduced muscle strength and exercise capacity, lowering their autonomy and quality of life and shortening survival time\u0026nbsp;[1]. Decreased muscle mass is one of the main causes of reduced muscle strength and exercise capacity\u0026nbsp;[2, 3]. A recent study showed that muscle quality is decreased significantly at the same time as or before the decrease in muscle mass\u0026nbsp;[4]. Studies of the elderly have also reported that the decline of muscle quality is closely related to the decline in physical function and poor prognosis of patients\u0026nbsp;[5, 6]. Therefore, both the quantity and quality of muscle affects muscle function. Joint evaluation may help formulate intervention measures and improve prognosis.\u003c/p\u003e\n\u003cp\u003eMuscle quality is a relative new term that refers to the microscopic and macroscopic changes in muscle structure and composition and the level of muscle function from each muscle mass unit\u0026nbsp;[7]. The existing research methods for evaluating muscle quality are mainly measurements of the amount of fat penetrating into the muscle determined through computed tomography (CT), magnetic resonance imaging (MRI), and muscle radiation attenuation by CT. CT measurement of mid-thigh intermuscular adipose tissue predicts usual gait velocity and 6-min walk distance of patients on hemodialysis\u0026nbsp;[2]. However, only a few studies focused on evaluating the muscle quality of patients on hemodialysis are available.\u003c/p\u003e\n\u003cp\u003eUltrasound can effectively assess muscle mass and muscle quality with good internal and external consistency [8]. It also has the advantages of bedside operation, convenience, non-invasiveness, and lack of radiation exposure, and is widely studied as a tool in muscle assessment. Echo intensity (EI) is an important indicator for ultrasound assessment of muscle quality. Enhanced EI indicates increased infiltration of fibrotic tissue and/or adipose tissue in the muscle and represents reduced muscle quality [9]. Numerous studies in the elderly have shown that an increase in EI is related to decline of muscle strength and physical function [10-12]. A recent study involving 61 patients with chronic kidney disease (CKD) showed that patients with high EI had low physical function [13]. However, to date, there are no relevant studies evaluating ultrasound derived EI in patients on hemodialysis. Hence, this study clarified the application value of ultrasound EI of skeletal muscle in patients on hemodialysis by evaluating the relationship between ultrasound EI and physical function.\u003c/p\u003e"},{"header":"Methods","content":"\u003ch2\u003eStudy population\u003c/h2\u003e\n\u003cp\u003eThis study screened outpatients on maintenance hemodialysis in our county hospital from July 2020 to August 2020. The inclusion criteria of this study included patients who had undergone more than 3 months of hemodialysis. patients on hemodialysis who could not walk or were completely blind were excluded. We screened a total of 110 patients and excluded 3 patients who could not walk. A total of 107 subjects were eventually enrolled. The research was conducted in accordance with the Helsinki Declaration. This study was also approved by the ethics committee of our hospital. All subjects signed the written informed consent, and then their\u0026nbsp;demographic information, past medical history, and duration of dialysis were collected. Various body measurements and assessments of physical function were performed before hemodialysis. A complete ultrasound examination of the right rectus femoris was also performed after hemodialysis.\u003c/p\u003e\n\u003ch2\u003eBody measurements and assessments of physical function\u003c/h2\u003e\n\u003ch2\u003e\u003cem\u003eMeasurement of body mass index (BMI)\u003c/em\u003e\u003c/h2\u003e\n\u003cp\u003eBMI measurement of individual research subjects was calculated based on body dry weight and the following formula: BMI (Kg/m\u003csup\u003e2\u003c/sup\u003e) = body weight/height\u003csup\u003e2\u003c/sup\u003e.\u003c/p\u003e\n\u003ch2\u003e\u003cem\u003eMeasurement of handgrip strength (HGS)\u003c/em\u003e\u003c/h2\u003e\n\u003cp\u003eHGS of individual subjects was measured before hemodialysis. Patients with internal arteriovenous fistula were subjected to HGS measurement on the non-fistula hand twice to obtain the maximum value. Patients using tunneled cuffed catheters were subjected to the HGS measurement on the dominant hand twice to obtain the maximum value.\u003c/p\u003e\n\u003ch2\u003e\u003cem\u003eGait speed\u003c/em\u003e\u003c/h2\u003e\n\u003cp\u003eIndividual subjects were required to walk independently for a 4-meter distance, followed by recording of the completion time and calculation of the gait speed (meter/second) twice to obtain the maximum value.\u003c/p\u003e\n\u003ch2\u003e\u003cem\u003eSit-to-stand\u0026nbsp;\u003c/em\u003e\u003cem\u003e60 s\u003c/em\u003e\u003cem\u003e\u0026nbsp;(STS-60) test\u003c/em\u003e\u003c/h2\u003e\n\u003cp\u003eThe number of times an individual patient stood up and sat down on a chair within 60 seconds was calculated. This STS-60 test assessed the strength and endurance of muscles of the lower limbs of the tested subject\u0026nbsp;[14]. The patient was asked to complete the sit down-stand up-sit down movement as many times as possible within 60 seconds by holding his/her hands in front of the chest and starting from the sitting position. The number of STS-60 movements was recorded at the end of the test.\u003c/p\u003e\n\u003ch2\u003e\u003cem\u003eDependence in IADL\u003c/em\u003e\u003c/h2\u003e\n\u003cp\u003ePhysical function was also measured using the instrumental activities of daily living (IADL) scale\u0026nbsp;[15, 16]. The IADL scale included 8 items: ability to shop on the street, do outdoor activities, cook meals, do household activities, wash clothes, use the telephone, take medications, and handle personal finances. The evaluation of the results of each item were divided into 3 levels: completion with no assistance, completion with partial assistance, and completion with full assistance. The IADL scale of individuals with any item which needed assistance (including partial or full assistance) was characterized as impaired IADL, otherwise IADL was characterized as intact.\u003c/p\u003e\n\u003ch2\u003eUltrasound measurement\u003c/h2\u003e\n\u003cp\u003eA portable ultrasound machine with a 60-mm width curvilinear transducer (2\u0026ndash;5 MHz, S II, SonoSite, USA) was used to gain enough ultrasound window to cover the whole width of the rectus femoris muscle. All ultrasounds were standardized by the default machine settings (depth, gain, and focus). One experienced pain physician who had been practicing musculoskeletal ultrasound more than 10 years obtained all the images.\u003c/p\u003e\n\u003cp\u003eB-mode 2D ultrasonography of the right rectus femoris was taken immediately once hemodialysis was finished. The patient would lie in the supine position at a 45\u0026deg; angle, with the rectus femoris muscle relaxed. A line at the midpoint between the anterior superior iliac spine and the superior patellar border was marked. The ultrasound transducer was placed perpendicular to the longitudinal axis of the thigh, overlying the line. Minimal pressure was applied to avoid muscle distortion. In the transverse ultrasound image, the rectus femoris muscle was confirmed and the muscle epimysium boundary was identified as an oval circle wrapping around the muscle fibers. Two images from the same point for each person were saved.\u003c/p\u003e\n\u003cp\u003eUltrasound images were transferred to the computer for measurements using Image J software (National Institute of Health, USA). The whole rectus femoris muscle within its epimysium was circled as the region of interest for cross sectional area (CSA) and mean EI measurement (Figure 1). The software returned measures of CSA and the mean EI, which was expressed as a value between 0 (black) and 255 (white) (Figure 1). The average CSA and mean EI values of two images for the same patient were analyzed.\u003c/p\u003e\n\u003ch2\u003eStatistical analysis\u003c/h2\u003e\n\u003cp\u003eContinuous data are presented as mean \u0026plusmn; standard deviation, and categorical data are presented as a percentage. For continuous data, one-way ANOVA was used to compare two groups when normal distribution was fulfilled; otherwise, the non-parametric Wilcoxon rank sum test was performed. For categorical data, the chi-square test was performed. The association of EI with physical function was examined using Pearson\u0026rsquo;s correlation analysis. Multiple linear regression (continuous outcomes) and logistics regression (dichotomous outcomes) were performed to assess the independent association of EI and CSA with physical function. The two model methods were as follows: Model 1\u0026mdash;only adjusted for EI and CSA; Model 2\u0026mdash;further adjusted for age, gender,and dialysis duration. All statistical analyses were performed using MedCalc Software (Version 18.2.1 MedCalc Software Ltd, Belgium). P \u0026lt; 0.05 was considered statistically significant.\u003c/p\u003e"},{"header":"Results","content":"\u003ch2\u003ePatient characteristics\u003c/h2\u003e\n\u003cp\u003eA total of 107 patients on maintenance hemodialysis were enrolled in this study. Patients were 37.3% female (n = 40), mean age was 53.53 \u0026plusmn; 12.52 years, average\u0026nbsp;dialysis duration was 2.97 \u0026plusmn; 2.32 years, and average BMI was 21.43 \u0026plusmn; 3.77 kg/m\u003csup\u003e2\u003c/sup\u003e. In addition, 15.9% of the patients had diabetes (n = 17), 93.5% of the patients had hypertension (n = 100), and 26.2% (n = 28) of the patients had dependency in IADL.\u003c/p\u003e\n\u003cp\u003eAs shown in Table 1, no significant differences in age, BMI, prevalence of hypertension, or duration of hemodialysis were found between males and females. However, the prevalence of diabetes in the male group was higher than in the female group (P = 0.018). In terms of physical function, male patients on hemodialysis had significantly stronger HGS than the female patients (P \u0026lt; 0.001) while no significant differences in gait speed, STS-60 completion time, or dependency in IADL were found between males and females (P \u0026gt; 0.05). In terms of ultrasound parameters of the rectus femoris, the EI value of the male group was significantly lower than in the female group, and the CSA of the male group was significantly higher than the female group (P \u0026lt; 0.001).\u003c/p\u003e\n\u003ch2\u003eRelationship between muscle quality and physical function\u003c/h2\u003e\n\u003cp\u003eAs shown in Figure 2, the EI of the overall patient population on hemodialysis was negatively correlated with HGS (r = \u0026minus;0.467, P \u0026lt; 0.001), gait speed (r = \u0026minus;0.285, P = 0.003), and STS-60 (r = \u0026minus;0.313, P = 0.001).\u003c/p\u003e\n\u003ch2\u003eComparison of physical function with muscle quality (EI) and muscle quantity (CSA)\u003c/h2\u003e\n\u003cp\u003eFurther multiple linear regression analyses and logistic regression analyses were performed to assess the relationship between EI, CSA, and physical function. As shown in Table 2, Model 1 adjusted for the EI and CSA, and Model 2 further adjusted for age, gender, and dialysis duration. Enhanced EI was associated with worse HGS (\u0026beta; = \u0026minus;0.207, P = 0.047), lower gait speed (\u0026beta; = \u0026minus;0.002, P = 0.001), less STS-60 (\u0026beta; = \u0026minus;0.136, P = 0.049), and a higher likelihood of dependency in IADL in Model 1 (OR: 1.070; 95% CI: [1.030\u0026ndash;1.111], P = 0.001), but was only associated with dependency in IALD (P = 0.001) in Model 2. Except for STS-60, increased CSA was a significant predictor of better HGS, higher gait speed, and lower IALD disability in both Model 1 and Model 2 in patients on hemodialysis.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eThis study was the first to report the relationship between ultrasound derived EI of the skeletal muscle and physical function in patients on hemodialysis. Our results showed that high EI was closely related to low physical function including HGS, gait speed, STS-60, and IADL disability in patients on hemodialysis.\u003c/p\u003e\n\u003cp\u003eThe pathophysiological mechanisms of decreased muscle quality include muscle fiber reduction, mitochondrial dysfunction of myocytes, intramuscular fat infiltration, and increased fibrosis\u0026nbsp;[17]. The existing assessment methods of muscle quality mainly include CT, MRI, and ultrasound. Although CT and MRI directly evaluate the degree of intramuscular fat infiltration, they are expensive and require patients go to a specific place or have a certain degree of radiation, which affects patient compliance with the examination. Numerous studies in the elderly have confirmed the close relationship between ultrasound derived EI and physical function. However, in the field of kidney diseases, only one small-scale study of stages 3\u0026ndash;5 CKD pre-dialysis patients has reported that EI is moderately and negatively correlated with the STS-60 test, the incremental shuttle walk test (ISWT) (n=61), and peak oxygen consumption (VO\u003csub\u003e2\u003c/sub\u003e peak) results (n = 32), but not with the gait speed and HGS (n = 29); EI was not correlated with any index of physical function when the CSA was corrected\u0026nbsp;[13]. In this study, EI was moderately and negatively correlated with HGS, gait speed, and STS-60 in patients on hemodialysis. Moreover, after adjusting for muscle area, high EI in patients on hemodialysis remained associated with worse HGS, low gait speed, reduced STS-60, and IADL disability. Thus, this is the first report showing the value of ultrasound derived EI in muscle evaluation of patients on hemodialysis.\u003c/p\u003e\n\u003cp\u003eIn addition to muscle quality, muscle quantity is also an important indicator for muscle evaluation of patients. A wealth of evidence from multiple studies has shown that muscle size is closely related to the physical function of patients on hemodialysis\u0026nbsp;[2, 3, 18]. When we further corrected for factors such as age, gender, and the duration of dialysis, only CSA was related to the level of physical function of the patients. Thus, in the clinical setting, the combined evaluation of muscle quantity and muscle quality may provide more information for accurately assessing muscle strength and physical function in patients\u0026nbsp;[19].\u003c/p\u003e\n\u003cp\u003eInterestingly, analysis of the ultrasound parameters of the rectus femoris showed that the CSA of the male group was significantly higher than in the female group, and the EI value of the male group was significantly lower than in the female group. These phenomena are consistent with our expectations. Male muscles are stronger, with larger CSA of the rectus femoris muscle. In addition, the proportion of body fat in the females was generally higher than that of males. Thus, the EI value of the female skeletal muscle was higher.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eLoss of muscle quantity and quality in patients on hemodialysis may be related to factors such as increased oxidative stress, accumulation of uremic toxins, reduced exercise activities, and malnutrition\u0026nbsp;[20, 21]. Exercise training is an effective way to improve muscle function. In patients with CKD, ultrasound measurement of CSA has been used to effectively assesses muscle mass gain after exercise intervention\u0026nbsp;[22]. Impendence movement reduced the accumulation of fat in the muscles of the elderly\u0026nbsp;[23]. However, there is still a lack of research on the improvement of muscle quality through exercise in patients on hemodialysis. In addition, further research is needed to verify whether EI can be used as an evaluation index of the improvement of muscle quality.\u003c/p\u003e\n\u003cp\u003eUltrasound-based evaluation of muscle quantity and quality of patients on hemodialysis provided more information for assessing the level of physical function in patients. The ultrasound method has the advantages of simplicity, convenience, non-invasiveness, and without radiation exposure. It has important clinical value and wide application prospects in the muscle evaluation of patients on hemodialysis.\u003c/p\u003e\n\u003cp\u003eThis study had some limitations: First, no standardized measurement method for EI is currently available, and the measurement of EI is also affected by different machine parameters. Thus, EI values may differ between different studies and are not comparable. Second, this was a cross-sectional study, and therefore it is impossible to clarify the etiological inference of the decline in muscle quality represented by EI and the decreased physical function of patients on hemodialysis. In addition, this study was carried out in a single dialysis center in China, and the generalization of our conclusions requires international, multi-center studies.\u0026nbsp;\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eThe present study revealed that enhanced US-derived EI was correlated with poor physical performance in patients on hemodialysis. The combined muscle quality and muscle quantity evaluation provides more information for assessing the level of physical function of the patients.\u0026nbsp;\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cp\u003eEI: Echo intensity; CSA: Cross-sectional area; HGS: Handgrip strength; STS-60: Gait speed, sit-to-stand 60 s; IADL: Instrumental activities of daily living; CT: computed tomography; MRI: magnetic resonance imaging; CKD: chronic kidney disease; BMI: Body mass index; ISWT: incremental shuttle walk test; SD: Standard deviation; SE: Standard error.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eEthics approval and consent to participate\u0026nbsp;\u003c/h2\u003e\n\u003cp\u003eThe study protocol complied with the Helsinki Declaration standards and was approved by the Ethics Committee of the People\u0026apos;s Hospital of Menghai County (approval number 2020-SNK-001) and Shanghai Jiao Tong University Affiliated Sixth People\u0026rsquo;s Hospital (approval number 2020-175). All subjects signed the written informed consent. \u0026nbsp;\u003c/p\u003e\n\u003ch2\u003eConsent for publication\u0026nbsp;\u003c/h2\u003e\n\u003cp\u003eNot Applicable. \u0026nbsp;\u003c/p\u003e\n\u003ch2\u003eAvailability of data and materials\u003c/h2\u003e\n\u003cp\u003eAll data generated or analysed during this study are included in this published article.\u0026nbsp;\u003c/p\u003e\n\u003ch2\u003eCompeting interests\u0026nbsp;\u003c/h2\u003e\n\u003cp\u003eThe authors declare that they have no competing interests.\u0026nbsp;\u003c/p\u003e\n\u003ch2\u003eFunding\u0026nbsp;\u003c/h2\u003e\n\u003cp\u003eThis work was supported by grants from the Shanghai Municipal Health Commission [grant number 20194y0347], and the National Natural Science Foundation of China [grant numbers 81670657,81870504, 81870468].\u0026nbsp;\u003c/p\u003e\n\u003ch2\u003eAuthors\u0026apos; contributions\u0026nbsp;\u003c/h2\u003e\n\u003cp\u003eJZW and HQL contributed to the conception of the study, performed statistical analysis and wrote the initial manuscript draft. JZW, SRR and LXS participated in study coordination, performed the recruitment, took the measures and collected the data. DSC and NSW contributed to the conception of the study, supervised the study, helped to interpret the results and corrected the draft. All authors read and approved the final manuscript. \u0026nbsp;\u003c/p\u003e\n\u003ch2\u003eAcknowledgements\u003c/h2\u003e\n\u003cp\u003eWe wish to thank Dr. Jing Chen and Dr Zhenyi Jia for their assistance and thoughtful academic discussions with the current study. \u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n \u003cli\u003eJassal SV, Karaboyas A, Comment LA, Bieber BA, Morgenstern H, Sen A, et al. Functional Dependence and Mortality in the International Dialysis Outcomes and Practice Patterns Study (DOPPS). Am J Kidney Dis. 2016;67(2):283-92. doi: 10.1053/j.ajkd.2015.09.024.\u003c/li\u003e\n \u003cli\u003eCheema B, Abas H, Smith B, O\u0026apos;Sullivan AJ, Chan M, Patwardhan A, et al. Investigation of skeletal muscle quantity and quality in end-stage renal disease. Nephrology (Carlton). 2010;15(4):454-63. doi: 10.1111/j.1440-1797.2009.01261.x.\u003c/li\u003e\n \u003cli\u003eMcIntyre CW, Selby NM, Sigrist M, Pearce LE, Mercer TH, Naish PF. Patients receiving maintenance dialysis have more severe functionally significant skeletal muscle wasting than patients with dialysis-independent chronic kidney disease. Nephrol Dial Transplant. 2006;21(8):2210-6. doi: 10.1093/ndt/gfl064.\u003c/li\u003e\n \u003cli\u003eDelmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-85. doi: 10.3945/ajcn.2009.28047.\u003c/li\u003e\n \u003cli\u003eVisser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci. 2005;60(3):324-33. doi: 10.1093/gerona/60.3.324.\u003c/li\u003e\n \u003cli\u003eCorrea-de-Araujo R, Harris-Love MO, Miljkovic I, Fragala MS, Anthony BW, Manini TM. The Need for Standardized Assessment of Muscle Quality in Skeletal Muscle Function Deficit and Other Aging-Related Muscle Dysfunctions: A Symposium Report. Front Physiol. 2017;8:87. doi: 10.3389/fphys.2017.00087.\u003c/li\u003e\n \u003cli\u003eCruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16-31. doi: 10.1093/ageing/afy169.\u003c/li\u003e\n \u003cli\u003eNijholt W, Scafoglieri A, Jager-Wittenaar H, Hobbelen JSM, van der Schans CP. The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia Sarcopenia Muscle. 2017;8(5):702-12. doi: 10.1002/jcsm.12210.\u003c/li\u003e\n \u003cli\u003eGrimm A, Teschner U, Porzelius C, Ludewig K, Zielske J, Witte OW, et al. Muscle ultrasound for early assessment of critical illness neuromyopathy in severe sepsis. Critical care (London, England). 2013;17(5):R227. doi: 10.1186/cc13050.\u003c/li\u003e\n \u003cli\u003e Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Mori N, et al. Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-aged and elderly persons. Eur J Appl Physiol. 2012;112(4):1519-25. doi: 10.1007/s00421-011-2099-5.\u003c/li\u003e\n \u003cli\u003e Watanabe Y, Yamada Y, Fukumoto Y, Ishihara T, Yokoyama K, Yoshida T, et al. Echo intensity obtained from ultrasonography images reflecting muscle strength in elderly men. Clin Interv Aging. 2013;8:993-8. doi: 10.2147/CIA.S47263.\u003c/li\u003e\n \u003cli\u003e Wilhelm EN, Rech A, Minozzo F, Radaelli R, Botton CE, Pinto RS. Relationship between quadriceps femoris echo intensity, muscle power, and functional capacity of older men. Age (Dordr). 2014;36(3):9625. doi: 10.1007/s11357-014-9625-4.\u003c/li\u003e\n \u003cli\u003e Wilkinson TJ, Gould DW, Nixon DGD, Watson EL, Smith AC. Quality over quantity ? Association of skeletal muscle myosteatosis and myofibrosis on physical function in chronic kidney disease. Nephrol Dial Transplant. 2019;34(8):1344-53. doi: 10.1093/ndt/gfy139.\u003c/li\u003e\n \u003cli\u003e Rikli RE, Jones CJ. Development and validation of criterion-referenced clinically relevant fitness standards for maintaining physical independence in later years. Gerontologist. 2013;53(2):255-67. doi: 10.1093/geront/gns071.\u003c/li\u003e\n \u003cli\u003e Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 1969;9(3):179-86.\u0026nbsp;\u003c/li\u003e\n \u003cli\u003e Cheng XS, Myers J, Han J, Stedman MR, Watford DJ, Lee J, et al. Physical Performance Testing in Kidney Transplant Candidates at the Top of the Waitlist. Am J Kidney Dis. 2020:S0272-6386(20)30728-9. doi: 10.1053/j.ajkd.2020.04.009.\u003c/li\u003e\n \u003cli\u003e Russ DW, Gregg-Cornell K, Conaway MJ, Clark BC. Evolving concepts on the age-related changes in \u0026quot;muscle quality\u0026quot;. J Cachexia Sarcopenia Muscle. 2012;3(2):95-109. doi: 10.1007/s13539-011-0054-2.\u003c/li\u003e\n \u003cli\u003e Giglio J, Kamimura MA, Lamarca F, Rodrigues J, Santin F, Avesani CM. Association of Sarcopenia With Nutritional Parameters, Quality of Life, Hospitalization, and Mortality Rates of Elderly Patients on Hemodialysis. J Ren Nutr. 2018;28(3):197-207. doi: 10.1053/j.jrn.2017.12.003.\u003c/li\u003e\n \u003cli\u003e Bourgeois B, Fan B, Johannsen N, Gonzalez MC, Ng BK, Sommer MJ, et al. Improved strength prediction combining clinically available measures of skeletal muscle mass and quality. J Cachexia Sarcopenia Muscle. 2019;10(1):84-94. doi: 10.1002/jcsm.12353.\u003c/li\u003e\n \u003cli\u003e Moorthi RN, Avin KG. Clinical relevance of sarcopenia in chronic kidney disease. Curr Opin Nephrol Hypertens. 2017;26(3):219-28. doi: 10.1097/MNH.0000000000000318.\u003c/li\u003e\n \u003cli\u003e Song YR, Kim JK, Lee HS, Kim SG, Choi EK. Serum levels of protein carbonyl, a marker of oxidative stress, are associated with overhydration, sarcopenia and mortality in hemodialysis patients. BMC Nephrol. 2020;21(1):281. doi: 10.1186/s12882-020-01937-z.\u003c/li\u003e\n \u003cli\u003e Gould DW, Watson EL, Wilkinson TJ, Wormleighton J, Xenophontos S, Viana JL, et al. Ultrasound assessment of muscle mass in response to exercise training in chronic kidney disease: a comparison with MRI. J Cachexia Sarcopenia Muscle. 2019;10(4):748-55. doi: 10.1002/jcsm.12429.\u003c/li\u003e\n \u003cli\u003e Marcus RL, Addison O, Kidde JP, Dibble LE, Lastayo PC. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging. 2010;14(5):362-6. doi: 10.1007/s12603-010-0081-2.\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp style=\"text-align: center;\"\u003eTable 1\u0026nbsp;\u003c/p\u003e\n\u003cp style=\"text-align: center;\"\u003ePatient characteristics, ultrasound measurements and physical performance in both sexes\u003c/p\u003e\n\u003cdiv align=\"center\"\u003e\n \u003ctable border=\"0\" cellpadding=\"0\" cellspacing=\"0\" width=\"107%\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003eMen (n=67)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003eWomen (n=40)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003eP\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eAge (yr)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e54.79\u0026plusmn;13.39\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e51.42\u0026plusmn;10.74\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.179\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eBMI (kg/m\u003csup\u003e2\u003c/sup\u003e)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e21.81\u0026plusmn;3.73\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e20.78\u0026plusmn;3.79\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.172\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eEI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e58.21\u0026plusmn;16.59\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e69.26\u0026plusmn;12.93\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026lt; 0.001\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eCSA (cm\u003csup\u003e2\u003c/sup\u003e)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e6.91\u0026plusmn;1.55\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e5.46\u0026plusmn;1.20\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026lt; 0.001\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eEthnicity\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.126\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eHan, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e20 (29.9)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e9 (22.5)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eDai, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e20 (29.9)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e21 (52.5)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eHani, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e14 (20.9)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e6 (15.0)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eOther, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e13 (19.4)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e4 (10.0)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eHypertension, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e63 (94.0)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e37 (92.5)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.758\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eDiabetes, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e15 (22.4)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e2 (5.0)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.018\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003ePrimary disease\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.104\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eChronic glomerulonephritis, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e10 (14.9)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e11 (27.5)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eDiabetic nephropathy, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e14 (20.9)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e2 (5.0)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eHypertensive nephropathy, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e9 (13.4)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e5 (12.5)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eObstructive nephropathy, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e9 (13.4)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e3 (7.5)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eOther or unknown, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e25 (37.3)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e19 (47.5)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eDialysis duration (yr)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e3.06\u0026plusmn;2.54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e2.82\u0026plusmn;1.93\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.607\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003ePhysical performance measures\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eHGS (kg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e31.27\u0026plusmn;9.81\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e21.37\u0026plusmn;4.36\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e\u0026lt; 0.001\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eGait speed (m/s)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e0.97\u0026plusmn;0.19\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e0.93\u0026plusmn;0.14\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.252\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eSTS-60 (repetitions)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e30.12\u0026plusmn;8.44\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e28.85\u0026plusmn;7.99\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.445\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"43.87755102040816%\"\u003e\n \u003cp\u003eDependency in IADL, n (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"19.387755102040817%\"\u003e\n \u003cp\u003e19 (28.4)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"24.489795918367346%\"\u003e\n \u003cp\u003e9 (22.5)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.244897959183673%\"\u003e\n \u003cp\u003e0.507\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003c/table\u003e\n\u003c/div\u003e\n\u003cp\u003eBMI, body mass index; EI, echo intensity; CSA, cross-sectional area; HGS, handgrip strength; STS-60, sit-to-stand 60 s; IADL, instrumental activities of daily living. Values are presented as mean (SD) for continuous values, and n (%) for categorical values.\u003c/p\u003e\n\u003cp id=\"isPasted\" style=\"text-align: center;\"\u003eTable 2\u0026nbsp;\u003c/p\u003e\n\u003cp style=\"text-align: center;\"\u003eComparisons of physical function with muscle quality (EI) and muscle quantity (CSA) in all patients on hemodialysis.\u003c/p\u003e\n\u003cdiv align=\"center\"\u003e\n \u003ctable border=\"0\" cellpadding=\"0\" cellspacing=\"0\" width=\"100%\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd rowspan=\"2\" valign=\"top\" width=\"26.262626262626263%\"\u003e\n \u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd colspan=\"2\" valign=\"top\" width=\"38.38383838383838%\"\u003e\n \u003cp\u003eModel 1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd colspan=\"2\" valign=\"top\" width=\"35.35353535353536%\"\u003e\n \u003cp\u003eModel 2\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"37.5%\"\u003e\n \u003cp\u003e\u0026beta; (SE)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"13.88888888888889%\"\u003e\n \u003cp\u003eP\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"36.111111111111114%\"\u003e\n \u003cp\u003e\u0026beta; (SE)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"12.5%\"\u003e\n \u003cp\u003eP\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eHGS (kg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eEI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e\u0026minus;0.207 (0.047)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e\u0026lt;0.001\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e\u0026minus;0.090 (0.047)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e0.061\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eCSA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e2.527 (0.479)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e\u0026lt;0.001\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e1.393 (0.483)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e0.005\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eGait speed (m/s)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eEI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e\u0026minus;0.002 (0.001)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e0.028\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e\u0026minus;0.002 (0.001)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e0.130\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eCSA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e0.030 (0.010)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e0.003\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e0.030 (0.011)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e0.009\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eSTS-60 (repetitions)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eEI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e\u0026minus;0.136 (0.049)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e0.006\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e\u0026minus;0.081 (0.051)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e0.119\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eCSA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e0.892 (0.497)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e0.075\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e0.747 (0.522)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e0.156\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003eOdds ratio (95% CI)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003eP\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eOdds ratio (95% CI)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003eP\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eDependency in IADL\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eEI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e1.070 (1.030\u0026ndash;1.1112)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e0.001\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e1.086 (1.033\u0026ndash;1.141)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e0.001\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003eCSA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"27.551020408163264%\"\u003e\n \u003cp\u003e0.569 (0.376\u0026ndash;0.860)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"10.204081632653061%\"\u003e\n \u003cp\u003e0.008\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"26.53061224489796%\"\u003e\n \u003cp\u003e0.438 (0.255\u0026ndash;0.755)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" width=\"9.183673469387756%\"\u003e\n \u003cp\u003e0.003\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003c/table\u003e\n\u003c/div\u003e\n\u003cp\u003eMultiple linear regression for continuous outcomes and logistic regression for dichotomous outcomes. Model 1: EI + CSA; Model 2: model 1 + sex + age+ dialysis duration. HGS, handgrip strength; EI, echo intensity; CSA, cross-sectional area; STS-60, sit-to-stand 60 s; IADL, instrumental activities of daily living.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"
[email protected]","identity":"bmc-nephrology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bnep","sideBox":"Learn more about [BMC Nephrology](http://bmcnephrol.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bnep/default.aspx","title":"BMC Nephrology","twitterHandle":"BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Muscle quality, Ultrasound, Physical performance, End-stage renal disease, Activities of daily living","lastPublishedDoi":"10.21203/rs.3.rs-1325735/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-1325735/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003eBackground: \u003c/strong\u003eThe objective of this study was to evaluate the relationship between ultrasound echo intensity (EI) of skeletal muscle and physical function of patients on maintenance hemodialysis.\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eMethods: \u003c/strong\u003eCross-sectional area (CSA) and mean EI of the right rectus femoris were measured by ultrasound to evaluate the quantity and quality of the muscle, respectively. Physical function was measured by handgrip strength (HGS), gait speed, sit-to-stand 60 s (STS-60) test, and instrumental activities of daily living (IADL) scale.\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eResults:\u003c/strong\u003e A total of 107 patients on hemodialysis were included, with women accounting for 37.3% (n = 40), and a mean age of 53.53 ± 12.52 years. Among the patients on hemodialysis, EI was moderately and negatively correlated with HGS (r = −0.467, P \u0026lt; 0.001), gait speed (r = −0.285, P = 0.003), and STS-60 (r = −0.313, P = 0.001). Multiple regression analyses adjusted for CSA showed that the enhanced EI of patients on hemodialysis remained associated with worse HGS (β = −0.207, P = 0.047), lower gait speed (β = −0.002, P = 0.001), less STS-60 (β = −0.136, P = 0.049), and a higher likelihood of dependency in IADL (Odds Ratio: 1.070, 95% CI: [1.033–1.111], P = 0.001).\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eConclusions: \u003c/strong\u003eIn patients on hemodialysis, enhanced EI in the skeletal muscle measured via ultrasound was correlated with poor physical performance. The combined muscle quality and muscle quantity evaluation provides more information for assessing the level of physical function of the patients.\u0026nbsp;\u003c/p\u003e","manuscriptTitle":"Enhanced echo intensity of skeletal muscle is associated with poor physical function in hemodialysis patients:a cross-sectional study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2022-02-21 20:45:01","doi":"10.21203/rs.3.rs-1325735/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Major revision","date":"2022-04-19T03:56:14+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2022-04-06T23:14:06+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"02929b17-0b89-4f55-a737-13920caf158e","date":"2022-04-06T21:16:08+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"fe67d61f-1262-4da7-b2d2-abe97f85d563","date":"2022-02-22T01:51:19+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"20c5361a-6c82-4588-bb33-e34ebe877c05","date":"2022-02-21T23:18:58+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2022-02-21T14:01:54+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2022-02-21T13:58:41+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2022-02-07T06:28:24+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2022-02-07T06:16:36+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Nephrology","date":"2022-02-04T02:10:03+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"
[email protected]","identity":"bmc-nephrology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bnep","sideBox":"Learn more about [BMC Nephrology](http://bmcnephrol.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bnep/default.aspx","title":"BMC Nephrology","twitterHandle":"BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"969e5ea1-b91d-4f5b-8942-4e7f9b483b48","owner":[],"postedDate":"February 21st, 2022","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[],"tags":[],"updatedAt":"2022-05-10T06:44:16+00:00","versionOfRecord":[],"versionCreatedAt":"2022-02-21 20:45:01","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-1325735","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-1325735","identity":"rs-1325735","version":["v1"]},"buildId":"7rjqhiLT3MXkJMwkYKINL","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}
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