Association of Ultrasound-Derived Metrics of the Quadriceps Muscle with Protein Energy Wasting in Hemodialysis Patients: A Multicenter Cross-Sectional Study

Sharmela Sahathevan, Ban-Hock Khor, Birinder Kaur Sadu Singh, Alice Sabatino, Enrico Fiaccadori, Zulfitri Azuan Mat Daud, Mohammad Syafiq Ali, Sreelakshmi Sankara Narayanan, Dina Tallman, Karuthan Chinna, Bak-Leong Goh, Abdul Halim Abdul Gafor, Ghazali Ahmad, Zaki Morad, Pramod Khosla, Tilakavati Karupaiah, On Behalf Of The Patch Study Malaysia Investigators, Sharmela Sahathevan, Ban-Hock Khor, Birinder Kaur Sadu Singh, Alice Sabatino, Enrico Fiaccadori, Zulfitri Azuan Mat Daud, Mohammad Syafiq Ali, Sreelakshmi Sankara Narayanan, Dina Tallman, Karuthan Chinna, Bak-Leong Goh, Abdul Halim Abdul Gafor, Ghazali Ahmad, Zaki Morad, Pramod Khosla, Tilakavati Karupaiah, On Behalf Of The Patch Study Malaysia Investigators

Abstract

This study aimed to assess muscle wasting and risk of protein energy wasting (PEW) in hemodialysis (HD) patients using an ultrasound (US) imaging method. PEW was identified using the ISRNM criteria in 351 HD patients. Quadriceps muscle thickness of rectus femoris (RF) and vastus intermedius (VI) muscles and cross-sectional area (CSA) of the RF muscle (RFCSA) were measured using US and compared with other physical measures. Associations of US indices with PEW were determined by logistic regression. Irrespective of gender, PEW vs. non-PEW patients had smaller RF, VI muscles, and RFCSA (all p < 0.001). US muscle sites (all p < 0.001) discriminated PEW from non-PEW patients, but the RFCSA compared to bio-impedance spectroscopy had a greater area under the curve (AUC, 0.686 vs. 0.581), sensitivity (72.8% vs. 65.8%), and specificity (55.6% vs. 53.9%). AUC of the RFCSA was greatest for PEW risk in men (0.74, 95% CI: 0.66-0.82) and women (0.80, 95% CI: 0.70-0.90) (both p < 0.001). Gender-specific RFCSA values (men < 6.00 cm2; women < 4.47 cm2) indicated HD patients with smaller RFCSA were 8 times more likely to have PEW (AOR = 8.63, 95% CI: 4.80-15.50, p < 0.001). The US approach enabled discrimination of muscle wasting in HD patients with PEW. The RFCSA was identified as the best US site with gender-specific RFCSA values to associate with PEW risk, suggesting potential diagnostic criteria for muscle wasting.

Keywords: hemodialysis; muscle wasting; protein energy wasting; quadriceps muscle; ultrasound imaging.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Study flow of patients for recruitment.
Figure 2
Figure 2
Quadriceps muscle thickness (QMT) and cross-sectional area (CSA): (a) QMT of rectus femoris (RF) and vastus intermedius (VI) muscles; (b) RFCSA.
Figure 3
Figure 3
ROC analysis for US measures according to gender. Figure 3 represents the area under curve for risk of PEW according to US muscle sites for (a) men; (b) women. Abbreviations: CSA, cross-sectional area; MID, mid-point; PEW, protein energy wasting; ROC, receiver operating characteristic; RF, rectus femoris; US, ultrasound; VI, vastus intermedius.

References

    1. Fouque D., Kalantar-Zadeh K., Kopple J.D., Cano N., Chauveau P., Cuppari L., A Franch H., Guarnieri G.L., Ikizler T., A Kaysen G., et al. A proposed nomenclature and diagnostic criteria for protein–energy wasting in acute and chronic kidney disease. Kidney Int. 2008;73:391–398. doi: 10.1038/sj.ki.5002585.
    1. Carrero J.J., Thomas F., Nagy K., Arogundade F., Avesani C.M., Chan M., Chmielewski M., Cordeiro A.C., Espinosa-Cuevas A., Fiaccadori E., et al. Global Prevalence of Protein-Energy Wasting in Kidney Disease: A Meta-analysis of Contemporary Observational Studies From the International Society of Renal Nutrition and Metabolism. J. Ren. Nutr. 2018;28:380–392. doi: 10.1053/j.jrn.2018.08.006.
    1. Mourtzakis M., Wischmeyer P. Bedside ultrasound measurement of skeletal muscle. Curr. Opin. Clin. Nutr. Metab. Care. 2014;17:389–395. doi: 10.1097/MCO.0000000000000088.
    1. Workeneh B.T., E Mitch W. Review of muscle wasting associated with chronic kidney disease. Am. J. Clin. Nutr. 2010;91:1128S–1132S. doi: 10.3945/ajcn.2010.28608B.
    1. Carrero 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. Kidney Int. 2016;90:53–66. doi: 10.1016/j.kint.2016.02.025.
    1. Norton K., Eston R. Kinanthropometry and Exercise Physiology. 4th ed. Routledge; New York, NY, USA: 2018.
    1. Khalil S.F., Mohktar M.S., Ibrahim F. The Theory and Fundamentals of Bioimpedance Analysis in Clinical Status Monitoring and Diagnosis of Diseases. Sensors. 2014;14:10895–10928. doi: 10.3390/s140610895.
    1. Chamney P.W., Wabel P., Moissl U.M., Müller M.J., Bosy-Westphal A., Korth O., Fuller N.J. A whole-body model to distinguish excess fluid from the hydration of major body tissues. Am. J. Clin. Nutr. 2007;85:80–89. doi: 10.1093/ajcn/85.1.80.
    1. Sahathevan S., Khor B., Yeong C.H., Tan T.H., Mohaideen A.K.M., Ng H.M., Ong G.R., Narayanan S.S., Gafor A.H.A., Goh B.L., et al. Validity of Ultrasound Imaging in Measuring Quadriceps Muscle Thickness and Cross-Sectional Area in Patients Receiving Maintenance Hemodialysis. J. Parenter. Enter. Nutr. 2020 doi: 10.1002/jpen.1867.
    1. Martín C.A.G., Zepeda E.M., Méndez O.A.L. Bedside Ultrasound Measurement of Rectus Femoris: A Tutorial for the Nutrition Support Clinician. J. Nutr. Metab. 2017;2017:1–5. doi: 10.1155/2017/2767232.
    1. Sabatino A., Regolisti G., Delsante M., Di Motta T., Cantarelli C., Pioli S., Grassi G., Batini V., Gregorini M., Fiaccadori E., et al. Noninvasive evaluation of muscle mass by ultrasonography of quadriceps femoris muscle in End-Stage Renal Disease patients on hemodialysis. Clin. Nutr. 2019;38:1232–1239. doi: 10.1016/j.clnu.2018.05.004.
    1. Scarborough D.M., Krebs D.E., Harris B.A. Quadriceps muscle strength and dynamic stability in elderly persons. Gait Posture. 1999;10:10–20. doi: 10.1016/S0966-6362(99)00018-1.
    1. Gruther W., Benesch T., Zorn C., Paternostro-Sluga T., Quittan M., Fialka-Moser V., Spiss C., Kainberger F., Crevenna R. Muscle wasting in intensive care patients: Ultrasound observation of the M. quadriceps femoris muscle layer. Acta Derm. Venereol. 2008;40:185–189. doi: 10.2340/16501977-0139.
    1. Menon M.K., Houchen L., Harrison S., Singh S.J., Morgan M.D., Steiner M.C. Ultrasound assessment of lower limb muscle mass in response to resistance training in COPD. Respir. Res. 2012;13:119. doi: 10.1186/1465-9921-13-119.
    1. Heymsfield S.B., McManus C., Smith J., Stevens V., Nixon D.W. Anthropometric measurement of muscle mass: Revised equations for calculating bone-free arm muscle area. Am. J. Clin. Nutr. 1982;36:680–690. doi: 10.1093/ajcn/36.4.680.
    1. Ikizler T.A., Burrowes J.D., Byham-Gray L.D., Campbell K.L., Carrero J.-J., Chan W., Fouque D., Friedman A.N., Ghaddar S., Goldstein-Fuchs D.J., et al. KDOQI Clinical Practice Guideline for Nutrition in CKD: 2020 Update. Am. J. Kidney Dis. 2020;76:S1–S107. doi: 10.1053/j.ajkd.2020.05.006.
    1. Kalantar-Zadeh K., Ikizler T., Block G., Avram M.M., Kopple J.D. Malnutrition-inflammation complex syndrome in dialysis patients: Causes and consequences. Am. J. Kidney Dis. 2003;42:864–881. doi: 10.1016/j.ajkd.2003.07.016.
    1. Garagarza C., Flores A.L., Valente A. Influence of Body Composition and Nutrition Parameters in Handgrip Strength: Are There Differences by Sex in Hemodialysis Patients? Nutr. Clin. Pr. 2017;33:247–254. doi: 10.1177/0884533617725512.
    1. Toledo F.R.U., Antunes A.A.U., Vannini F.C.D.U., Silveira L.V.A.U., Martin L.C.U., Barretti P., Caramori J.C.T. Validity of malnutrition scores for predicting mortality in chronic hemodialysis patients. Int. Urol. Nephrol. 2013;45:1747–1752. doi: 10.1007/s11255-013-0482-3.
    1. Isoyama N., Qureshi A.R., Avesani C.M., Lindholm B., Bàràny P., Heimbürger O., Cederholm T., Stenvinkel P., Carrero J.J. Comparative Associations of Muscle Mass and Muscle Strength with Mortality in Dialysis Patients. Clin. J. Am. Soc. Nephrol. 2014;9:1720–1728. doi: 10.2215/CJN.10261013.
    1. Kirchengast S. Gender Differences in Body Composition from Childhood to Old Age: An Evolutionary Point of View. J. Life Sci. 2010;2:1–10. doi: 10.1080/09751270.2010.11885146.
    1. De Souza V.A., Oliveira D., Cupolilo E.N., Miranda C.S., Colugnati F.A.B., Mansur H.N., Fernandes N.M.D.S., Bastos M.G. Rectus femoris muscle mass evaluation by ultrasound: Facilitating sarcopenia diagnosis in pre-dialysis chronic kidney disease stages. Clinics. 2018;73 doi: 10.6061/clinics/2018/e392.
    1. Studenski S.A., Peters K.W., Alley D.E., Cawthon P.M., McLean R.R., Harris T.B., Ferrucci L., Guralnik J.M., Fragala M.S., Kenny A.M., et al. The FNIH Sarcopenia Project: Rationale, Study Description, Conference Recommendations, and Final Estimates. J. Gerontol. Ser. A. Boil. Sci. Med. Sci. 2014;69:547–558. doi: 10.1093/gerona/glu010.
    1. Muscaritoli M., Molfino A., Bollea M.R., Fanelli F.R. Malnutrition and wasting in renal disease. Curr. Opin. Clin. Nutr. Metab. Care. 2009;12:378–383. doi: 10.1097/MCO.0b013e32832c7ae1.
    1. Chen L.-K., Lee W.-J., Peng L.-N., Liu L.-K., Arai H., Akishita M. Recent Advances in Sarcopenia Research in Asia: 2016 Update From the Asian Working Group for Sarcopenia. J. Am. Med. Dir. Assoc. 2016;17:767.e1–767.e7. doi: 10.1016/j.jamda.2016.05.016.
    1. Wilkinson T.J., Gould D.W., Nixon D.G.D., Watson E.L., Smith A. Quality over quantity? Association of skeletal muscle myosteatosis and myofibrosis on physical function in chronic kidney disease. Nephrol. Dial. Transpl. 2019;34:1344–1353. doi: 10.1093/ndt/gfy139.
    1. Seymour J.M., Ward K., Sidhu P.S., Puthucheary Z., Steier J., Jolley C.J., Rafferty G.F., Polkey M.I., Moxham J. Ultrasound measurement of rectus femoris cross-sectional area and the relationship with quadriceps strength in COPD. Thorax. 2009;64:418–423. doi: 10.1136/thx.2008.103986.
    1. Trappe T.A., Lindquist D.M., Carrithers J.A. Muscle-specific atrophy of the quadriceps femoris with aging. J. Appl. Physiol. 2001;90:2070–2074. doi: 10.1152/jappl.2001.90.6.2070.
    1. Mueller N., Murthy S., Tainter C.R., Lee J., Riddell K., Fintelmann F.J., Grabitz S.D., Timm F.P., Levi B., Kurth T., et al. Can Sarcopenia Quantified by Ultrasound of the Rectus Femoris Muscle Predict Adverse Outcome of Surgical Intensive Care Unit Patients as well as Frailty? A Prospective, Observational Cohort Study. Ann. Surg. 2016;264:1116–1124. doi: 10.1097/SLA.0000000000001546.
    1. Battaglia Y., Ullo I., Massarenti S., Esposito P., Prencipe M.A., Ciancio G., Provenzano M., Fiorini F., Andreucci M., Storari A., et al. Ultrasonography of Quadriceps Femoris Muscle and Subcutaneous Fat Tissue and Body Composition by BIVA in Chronic Dialysis Patients. Nutrients. 2020;12:1388. doi: 10.3390/nu12051388.
    1. Bury C., DeChicco R., Nowak D., Lopez R., He L., Jacob S., Kirby D.F., Rahman N., Cresci G. Use of Bedside Ultrasound to Assess Muscle Changes in the Critically Ill Surgical Patient. J. Parenter. Enter. Nutr. 2020 doi: 10.1002/jpen.1840.
    1. Gould D.W., Watson E.L., Wilkinson T.J., Wormleighton J., Xenophontos S., Viana J.L., Smith A. Ultrasound assessment of muscle mass in response to exercise training in chronic kidney disease: A comparison with MRI. J. Cachexia Sarcopeni. 2019;10:748–755. doi: 10.1002/jcsm.12429.
    1. Yamada M., Kimura Y., Ishiyama D., Nishio N., Otobe Y., Tanaka T., Ohji S., Koyama S., Sato A., Suzuki M., et al. Synergistic effect of bodyweight resistance exercise and protein supplementation on skeletal muscle in sarcopenic or dynapenic older adults. Geriatr. Gerontol. Int. 2019;19:429–437. doi: 10.1111/ggi.13643.
    1. Sabatino A., Regolisti G., Bozzoli L., Fani F., Antoniotti R., Maggiore U., Fiaccadori E. Reliability of bedside ultrasound for measurement of quadriceps muscle thickness in critically ill patients with acute kidney injury. Clin. Nutr. 2017;36:1710–1715. doi: 10.1016/j.clnu.2016.09.029.

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel