Objective

This study aimed to explore the effects of fluid hydration status on ultrasound muscle measurement in hemodialysis (HD) patients.

Methods

Ultrasound muscle examination of the right rectus femoris and bioelectrical impedance analysis measurement of the right lower limb were performed in HD patients at the periods of predialysis and postdialysis. The correlations between the changes in the corresponding ultrasound and bioelectrical impedance analysis variables were analyzed.

Results

A total of 50 patients on maintenance HD were included, with mean age of 52.6 ± 13.5 years. Patients were 40% female (n = 20), and average dialysis duration was 2.62 ± 2.42 years. Compared to predialysis, the measurements of cross-sectional area, muscle thickness, echo intensity (EI), and their percentage changes all decreased significantly after the HD procedure (P < .05). The change in EI and its percentage change were significantly correlated with changes in total body water, intracellular water, and extracellular water (P < .05).

Conclusions

The HD session may have significant effects on ultrasound muscle measurement. Both the indicators of muscle quantity (cross-sectional area and muscle thickness) and quality (EI) significantly decreased after HD, which may contribute to the change in fluid hydration status and the change in fluid composition.

KeywordsIntroductionPatients on hemodialysis (HD) often suffer from protein energy wasting, muscle wasting, and muscle weakness. Skeletal muscle mass and muscle function are negatively affected by a variety of conditions inherent to chronic kidney disease (CKD) and to dialysis treatment,1Carrero J.J. Johansen K.L. Lindholm B. Stenvinkel P. Cuppari L. Avesani C.M. Screening for muscle wasting and dysfunction in patients with chronic kidney disease. and many studies in the past decades have also linked muscle loss in CKD patients with worse quality of life, depression, protein-energy wasting (PEW), fracture risk, cardiovascular complications, graft failure, and postoperative complications in transplant recipients, as well as with increased hospitalization and mortality.2Sabatino A. Cuppari L. Stenvinkel P. Lindholm B. Avesani C.M. Sarcopenia in chronic kidney disease: what have we learned so far?. The evaluation of muscle mass and function may help formulate intervention measures and improve the prognosis for patients on HD.Traditionally, skeleton muscle mass can be assessed by imaging methods such as dual X-ray absorptiometry (DXA), computed tomography, and magnetic resonance imaging, but these techniques are not commonly used in normal clinical practice due to radiation exposure, special operation room, and high cost.3Sousa-Santos A.R. Barros D. Montanha T.L. Carvalho J. Amaral T.F. Which is the best alternative to estimate muscle mass for sarcopenia diagnosis when DXA is unavailable?.Instead, ultrasound offers essential advantages, including bedside operation, convenience, noninvasiveness, and lack of radiation use.4Sabatino A. Regolisti G. Delsante M. et al.Noninvasive evaluation of muscle mass by ultrasonography of quadriceps femoris muscle in end-stage renal disease patients on hemodialysis. It has recently been widely adopted as a tool in assessing skeleton muscle in patients of different profiles, with right internal and external consistency.5Sabatino A. Regolisti G. Bozzoli L. et al.Reliability of bedside ultrasound for measurement of quadriceps muscle thickness in critically ill patients with acute kidney injury. The sizes of muscle thickness (MT) and cross-sectional area (CSA) measured are usually used to indicate muscle quantity, while muscle echo intensity (EI) is used as an important indicator of muscle quality.6Parry S.M. El-Ansary D. Cartwright M.S. et al.Ultrasonography in the intensive care setting can be used to detect changes in the quality and quantity of muscle and is related to muscle strength and function. The ultrasound parameters MT, CSA, and EI have all been applied in both dialysis-dependent and non–dialysis-dependent CKD patients.7Sabatino A. Broers N.J.H. van der Sande F.M. Hemmelder M.H. Fiaccadori E. Kooman J.P. Estimation of muscle mass in the integrated assessment of patients on hemodialysis.,8Wilkinson T.J. Gould D.W. Nixon D.G.D. Watson E.L. Smith A.C. Quality over quantity? Association of skeletal muscle myosteatosis and myofibrosis on physical function in chronic kidney disease.In particular, when it comes to muscle measurement in HD patients, we must pay attention that a tremendous change in fluid hydration status of muscle occurs before and after the HD procedure. This kind of change may have a great influence on muscle measurements.9Slee A. McKeaveney C. Adamson G. et al.Estimating the prevalence of muscle wasting, weakness, and sarcopenia in hemodialysis patients.,10Cruz-Jentoft A.J. Bahat G. Bauer J. et al.Sarcopenia: revised European consensus on definition and diagnosis. As far as we know, no data are currently available on whether rapid fluid shifts occurring during the HD procedure might influence US measurements of muscle mass and EI.

Therefore, we try to explore the effects of fluid hydration status on ultrasound muscle measurement in HD patients by measuring CSA, MT, and EI of the rectus femoris by ultrasound and comparing these values before and after the HD procedure.

MethodsPatient Selection

This study included patients who had undergone more than 3 months of HD, and those who could not walk or be completely blind were excluded. A total of 50 subjects were eventually analyzed. This study was approved by the ethics committee of the hospital. All subjects signed the written informed consent.

Study ProtocolBaseline characteristics, including age, sex, weight, height, disease history, and duration of HD were collected for all participants before HD. The whole-body bioelectrical impedance analysis (BIA) measurement of the right lower limb and ultrasound examination of the rectus femoris were performed before and after HD. Body mass index was calculated as dry weight (kg)/height2 (m2). Ultrafiltration volume was collected and the dialysis dose was evaluated by calculating Kt/V.11Second generation logarithmic estimates of single-pool variable volume Kt/V: an analysis of error.Bioelectrical Impedance Analysis Measurement

The patient was positioned supine. Water parameters of the right lower limb, including total body water (TBW), intracellular water (ICW), and extracellular water (ECW), were obtained before and after the HD procedure by a multifrequency BIA (InBody S10; InBody Co., Ltd., Seoul, South Korea). The values of phase angles were also recorded by the device at a frequency of 50 kHz. The differences between the values before and after HD were calculated.

Ultrasound Measurement

A 50-mm width linear transducer (5-14 MHz, S II; SonoSite Inc., Bothell, Washington) was used to measure the right rectus femoris muscle before and after HD. All ultrasound images were standardized by the default machine settings (depth, gain, and focus).

The patient was positioned in the supine position at a 45° angle. The ultrasound transducer was placed at the midpoint between the anterior superior iliac spine and the superior patellar border of the right leg. Two 2-dimensional images of the rectus femoris images were obtained at each time. Ultrasound images were transferred to the computer for measurements using ImageJ software (National Institute of Health). The whole rectus femoris muscle within its epimysium was circled as the region of interest, and the software returned measures of CSA, MT, and mean EI values.12Ticinesi A. Narici M.V. Lauretani F. et al.Assessing sarcopenia with vastus lateralis muscle ultrasound: an operative protocol. The average values of the 2 images at the same time were obtained for statistical analysis.Statistical Analysis

Continuous data are presented as mean ± standard deviation, and categorical data are presented as a percentage. Changes and percentage changes in CSA, MT, and EI obtained before and after the HD procedure are compared by a paired Wilcoxon test or signed rank-sum test. Spearman correlation coefficients were performed to determine the correlation between the change in CSA, MT, or EI from predialysis to postdialysis and changes in TBW, ICW, or ECW of the right lower limb. All statistical analyses were performed by SPSS software (Version 22.0; IBM). P < .05 was considered statistically significant.

ResultsPatient characteristics, Kt/V, and ultrafiltration volume are presented in Table 1.

Table 1Main Demographic and Clinical Characteristics of Patients on Hemodialysis (n = 50)

The values of ultrasound CSA, EI, and MT of the rectus femoris before (predialysis) and after HD (postdialysis) are presented in Table 1. The CSA, MT, and EI and their percentage changes all decreased significantly after the HD procedure for the entire group (Table 2). When grouped by gender, the CSA and EI and their percentage changes decreased significantly in the female group; the CSA and EI and their percentage changes decreased significantly in the male group (Table 2). The percentage change in CSA was more significant (−6.6%) than in MT (−2.8%). Representative ultrasound images of one patient’s rectus femoris obtained before and after the HD session are illustrated in Figure 1. Compared to predialysis, the rectus femoris muscle looked smaller in CSA, thinner in MT, and darker in EI after the HD procedure.

Table 2Changes in Cross-Sectional Area, Muscle Thickness, Muscle Echo Intensity and Phase Angle Before and After Dialysis in HD Patients (n = 50)

CSA, cross-sectional area; EI, echo intensity; HD, hemodialysis; MT, muscle thickness; PhA, phase angle.

Figure 1Representative comparison ultrasound images of predialysis and postdialysis obtained from the same rectus femoris location of one of the patients. The patient was 36 years old, male, and with a 7-year dialysis duration. Rectus femoris cross-sectional area is outlined by dotted line. The CSA, MT, and EI values of each image are marked at the lower right corner of the image. CSA, cross-sectional area; EI, echo intensity; MT, muscle thickness; RF, rectus femoris; VI, vastus intermedius.

The TBW, ICW, and ECW of the right leg decreased 0.53 ± 0.28 L, 0.25 ± 0.16 L, and 0.28 ± 0.13 L, respectively. The values of ECW/TBW ratio of the lower limb before and after the HD procedure were 0.40 ± 0.01 and 0.38 ± 0.02 respectively (P Table 2). As shown in Table 3, EI, with its percentage change, is the only value to correlate significantly with changes in TBW, ICW, ECW, Kt/V, and ultrafiltration volume (all P 

Table 3Correlation of Changes in Cross-Sectional Area, Muscle Thickness, and Muscle Echo Intensity With Changes in Total Body Water, Intracellular Water, and Extracellular Water in HD Patients (n = 50)

BMI, body mass index; CSA, cross-sectional area; ECW, extracellular water; EI, echo intensity; HD, hemodialysis; ICW, intracellular water; MT, muscle thickness; TBW, total body water.

Discussion

In the present study, we found that both ultrasound CSA and MT—the 2 indicators of muscle quantity of rectus femoris—decreased after the HD procedure.

At different periods of predialysis and postdialysis, the fluid hydration status will change and may affect the muscle measurements. Barreira et al.13The effects of acute water ingestion on body composition analyses via dual-energy x-Ray absorptiometry. indicated that acute water ingestion before a DXA analysis would significantly influence body composition. However, Sabatino et al.5Sabatino A. Regolisti G. Bozzoli L. et al.Reliability of bedside ultrasound for measurement of quadriceps muscle thickness in critically ill patients with acute kidney injury. compared quadriceps MT values measured by ultrasound before and after renal replacement therapy and found no significant differences. This result was somewhat contrary to ours, and the explanation may be that they use MT, a 1-dimensional single-axis data, as the only indicator of muscle mass, which may not represent the total 3-dimensional volume of muscle. In our study, both the CSA value, a 2-dimensional area data, and the MT value were recorded. Our results showed that the CSA value changed more significantly than the MT value, which changed very little. Besides, we compared the changes in CSA and MT with changes in TBW, ICW, and ECW of the lower limb measured by BIA. The difference in ECW/TBW ratio before and after the HD procedure was very weak, so we did not compare them with ultrasound measures. It turned out that neither the changes in CSA nor MT were correlated significantly with the water parameters. To a certain extent, this result went beyond what we expected. We considered this result for some possible explanations. First, the local rectus femoris muscle actually does not represent the total body muscle or the lower limber. Second, the muscle architecture change is more complicated than BIA change, and will not change proportionally with a water change. Third, after the HD procedure, not only did the area of the rectus femoris decrease but also the rigidity of the rectus femoris muscle improved. Then the muscle’s morphology transformed subtly, which may make the changes in CSA and MT more complicated than the primary change with the hydration status shifting before and after the HD procedure. Eventually, the actual changes in CSA and MT we obtained by ultrasound were not significant enough to correlate with the changes in water parameters. Nevertheless, the evidence of a decrease in CSA and MT provided by the present study is not strong, so further cross-sectional studies with a larger sample are needed to clarify how the change in fluid hydration status affects ultrasound measurement of muscle quantity.Importantly, we also found that ultrasound EI of rectus femoris, the indicator of muscle quantity, decreased after the HD procedure significantly in the current study. An increase in skeleton muscle EI generally indicates various structural changes in the muscle, such as fatty infiltration, fibrosis, or edema.14Mul K. Horlings C.G.C. Vincenten S.C.C. Voermans N.C. van Engelen B.G.M. van Alfen N. Quantitative muscle MRI and ultrasound for facioscapulohumeral muscular dystrophy: complementary imaging biomarkers.,15Hernández-Socorro C.R. Saavedra P. López-Fernández J.C. Ruiz-Santana S. Assessment of muscle wasting in long-stay ICU patients using a new ultrasound protocol. Increased muscle ultrasound EI correlated strongly with decreased muscle strength and has been confirmed in different neuromuscular disorders.16Vill K. Schessl J. Teusch V. et al.Muscle ultrasound in classic infantile and adult Pompe disease: a useful screening tool in adults but not in infants. Our study results showed that, as the fluid was cleared and the edema status was improved in the muscle tissue in the cases of HD patients, the ultrasound EI of skeleton muscle decreased. Furthermore, compared to changes in TBW, ICW, and ECW of the lower limb measured by BIA, the change in EI, but not CSA and MT, was correlated significantly with all these water values. Similarly, compared to the values of Kt/V and ultrafiltration volume, the change in EI was the only ultrasound parameter to correlate significantly with all these BIA water values. This finding suggested that the change in EI correlated more strongly with the change in the hydration status of the muscle than those muscle quantity indicators of CSA and MT. We attributed this difference to the following reasons. First, EI is determined by quantifying the intensity of a pixel within an ultrasound image of the transverse plane of the rectus femoris, and it might be less affected by changes in the overall muscle shape. Second, beyond the change in hydration status, the HD session will produce the change in fluid composition, the changes in ultrasound muscle EI, CSA, and MT might be more complicated than the change in BIA. Damas et al.17Damas F. Phillips S.M. Lixandrao M.E. et al.Early resistance training-induced increases in muscle cross-sectional area are concomitant with edema-induced muscle swelling. found that both muscle CSA and EI increased in early resistance training adults, but the degree was not always consistent.

There were several limitations in the present study. First, the sample size is limited, hampering further evaluation regarding differences in the results grouped by gender. Second, we assessed the fluid status by BIA instead of DXA. We did not use computed tomography or magnetic resonance imaging to further confirm the CSA results and the femoris rectus measured by ultrasound might not reflect whole-body muscle quantity and quality. Third, we just tried to illustrate the effects of acute dehydration on muscle measurements. But what we should keep in mind is the effect of the HD session is more than the change in fluid status. As we assumed, the fluid was redistributed in dehydrated muscles in a short time after the HD procedure. Finally, ultrasound EI may be easily influenced by the degree of ultrasound probe tilt with the muscle, and there is still no standardized technique for EI measurement yet. Further studies are urgently needed to make EI measurement standardized to get reproducible evidence.

Conclusion

This study has revealed that the HD session may significantly have effects on ultrasound muscle measurement. Both the indicators of muscle quantity (CSA and MT) and quality (EI) significantly decreased after the HD procedure, but the changes in muscle quantity were not correlated with the changes in TBW, ICW, and ECW of the lower limb. The changes in muscle measurements may contribute to both the change in fluid hydration status and the change in fluid composition.

Practical Application

Ultrasound skeleton muscle measurement is convenient, nonradiative, and it may help us in identifying muscle changes in nutritional disturbances like sarcopenia, protein energy wasting, and frailty. When we evaluate the muscle mass and quality in HD patients, we recommend to assess muscle mass by ultrasound after the session of dialysis.

Credit Authorship Contribution Statement

Dongsheng Cheng: Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft. Haiqing Luo: Data curation, Formal analysis, Investigation. Shunrong Ren: Investigation, Validation, Visualization. Niansong Wang: Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing – review & editing. Junzhen Wu: Conceptualization, Project administration, Resources, Supervision, Writing – original draft, Writing – review & editing.

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Noninvasive evaluation of muscle mass by ultrasonography of quadriceps femoris muscle in end-stage renal disease patients on hemodialysis.

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Reliability of bedside ultrasound for measurement of quadriceps muscle thickness in critically ill patients with acute kidney injury.

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Estimating the prevalence of muscle wasting, weakness, and sarcopenia in hemodialysis patients.

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Eur J Appl Physiol. 116: 49-56Article InfoPublication History

Published online: May 18, 2022

Publication stageIn Press Journal Pre-ProofFootnotes

Support: This work was sponsored by the Shanghai Municipal Health Commission (grant number 20194y0347 ), and the National Natural Science Foundation of China (grant numbers 81670657 , 81870504 , and 81870468 ).

Financial Disclosure: The authors declare that they have no competing financial interests. The results presented in this paper have not been published previously in whole or part, except in abstract format.

Identification

DOI: https://doi.org/10.1053/j.jrn.2022.04.007

Copyright

© 2022 The Authors. Published by Elsevier Inc. on behalf of the National Kidney Foundation, Inc.

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