Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Phase angle of bioimpedance at 50 kHz is associated with cardiovascular diseases: systematic review and meta-analysis

Abstract

The phase angle of bioimpedance is an important prognostic tool in clinical practice. The aim of this study was to investigate the association between phase angle and cardiovascular diseases. Electronic searches were carried out on MEDLINE, EMBASE, Cochrane, SCIELO, LILACS, CINAHL, Scopus, and the Web of Science. The PECO was “P” adults over 18 years of age, “E” the presence of cardiovascular disease, “C” absence of cardiovascular disease, and “O” phase angle values. The phase-angle means difference (MD) was analyzed separately by sex. Subgroup metanalysis with age, body mass index, and heart failure disease and meta-regressions were analyzed with random-effects models. Sensitivity analysis was performed considering only studies with high quality. The heterogeneity among studies was assessed using the Q-Cochran test and I² statistics. Four-hundred-thirty-nine articles were identified, and 22 studies were included in this systematic review, totaling 10.010 participants. Eight studies met the criteria for the meta-analysis, involving 2164 participants. The phase angle (PA) was measured at 50 kHz frequency in all studies. Individuals with cardiovascular disease had a smaller PA compared to the control group, for both males (MD −0.70; 95% CI −1.01 to −0.39) and females (MD −0.76; 95% CI −1.39 to −0.13). In the sensitivity analysis, in men, the quality of studies (P < 0.01), and in women, heart failure (P < 0.01) was significantly different between groups.The values of the phase angle were lower in individuals with cardiovascular disease than in control subjects. This result reinforces the importance of this tool in clinical practice, highlighting its potential to assess health status. Registration: The systematic review protocol was registered in the PROSPERO database as CRD42020164178.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Study flow diagram.
Fig. 2
Fig. 3
Fig. 4

Data availability

The datasets generated during the current study are available from the corresponding author on reasonable request

References

  1. Lukaski HC. Evolution of bioimpedance: a circuitous journey from estimation of physiological function to assessment of body composition and a return to clinical research. Eur J Clin Nutr. 2013;67:S2–S9. https://doi.org/10.1038/ejcn.2012.149.

    Article  PubMed  Google Scholar 

  2. Norman K, Stobäus N, Pirlich M, Bosy-Westphal A. Bioelectrical phase angle and impedance vector analysis - Clinical relevance and applicability of impedance parameters. Clin Nutr. 2012;31:854–61. https://doi.org/10.1016/j.clnu.2012.05.008.

    Article  PubMed  Google Scholar 

  3. Garlini LM, Alves FD, Ceretta LB, Perry sIS, Souza GC, Clausell NO Phase angle and mortality: a systematic review. Eur J Clin Nutr. 2018. https://doi.org/10.1038/s41430-018-0159-1.

  4. Matthie JR. Bioimpedance measurements of human body composition: Critical analysis and outlook. Expert Rev Med Devices. 2008;5:239–61. https://doi.org/10.1586/17434440.5.2.239.

    Article  PubMed  Google Scholar 

  5. Campa F, Matias CN, Marini E, Heymsfield SB, Toselli S, Sardinha LB, et al. Identifying athlete body fluid changes during a competitive season with bioelectrical impedance vector analysis. Int J Sports Physiol Perform 2020;15:361–7. https://doi.org/10.1123/ijspp.2019-0285.

    Article  Google Scholar 

  6. Matias CN, Cavaco-Silva J, Reis M, Campa F, Toselli S, Sardinha L, et al. Phase angle as a marker of muscular strength in breast cancer survivors. Int J Environ Res Public Health. 2020;17:1–10. https://doi.org/10.3390/ijerph17124452.

    Article  Google Scholar 

  7. Arab A, Karimi E, Vingrys K, Shirani F. Is phase angle a valuable prognostic tool in cancer patients’ survival? A systematic review and meta-analysis of available literature. Clin Nutr. 2021;40:3182–90. https://doi.org/10.1016/j.clnu.2021.01.027.

    Article  PubMed  Google Scholar 

  8. Tabinor M, Elphick E, Dudson M, Kwok CS, Lambie M, Davies SJ. Bioimpedance-defined overhydration predicts survival in end stage kidney failure (ESKF): Systematic review and subgroup meta-analysis. Sci Rep. 2018;8:1–14. https://doi.org/10.1038/s41598-018-21226-y.

    CAS  Article  Google Scholar 

  9. Antunes AA, Rodrigues APAP, Geraix J, Silveira- LVDA, Pereira PCM, Carvalhaes MABL Nutritional assessment of hospitalized HIV-infected patients by the phase angle z-score measurement. 2012; 27:771−4. https://doi.org/10.3305/nh.2012.27.3.5684.

  10. Maddocks M, Kon SSC, Jones SE, Canavan JL, Nolan CM, Higginson IJ et al. Bioelectrical impedance phase angle relates to function, disease severity and prognosis in stable chronic obstructive pulmonary disease. Clin Nutr. 2015; 6–11. https://doi.org/10.1016/j.clnu.2014.12.020.

  11. Belarmino G, Gonzalez MC, Torrinhas RS, Sala P, Andraus W, D’Albuquerque LA, et al. Phase angle obtained by bioelectrical impedance analysis independently predicts mortality in patients with cirrhosis. World J Hepatol. 2017;9:401–8. https://doi.org/10.4254/wjh.v9.i7.401.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sobieszek G, Mlak R, Dziekanowska AS, Myśliwy AJ, Homa-Mlak I. Electrical changes in polish patients with chronic heart failure: Preliminary observations. Med. 2019;55:1–12. https://doi.org/10.3390/medicina55080484.

    Article  Google Scholar 

  13. Massari F, Iacoviello M, Scicchitano P, Mastropasqua F, Guida P, Riccioni G, et al. Accuracy of bioimpedance vector analysis and brain natriuretic peptide in detection of peripheral edema in acute and chronic heart failure. Hear Lung 2016;45:319–26. https://doi.org/10.1016/j.hrtlng.2016.03.008.

    Article  Google Scholar 

  14. Drozdová D, Danková Z, Čerňanová V, Siváková D. Body composition of Slovak midlife women with cardiovascular complications. Anthropol Rev 2016;79:169–80. https://doi.org/10.1515/anre-2016-0013.

    Article  Google Scholar 

  15. Naghavi M, Abajobir AA, Abbafati C, Abbas KM, Abd-Allah F, Abera SF, et al. Global, regional, and national age-sex specifc mortality for 264 causes of death, 1980-2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet 2017;390:1151–210. https://doi.org/10.1016/S0140-6736(17)32152-9.

    Article  Google Scholar 

  16. Khambhati J, Allard-Ratick M, Dhindsa D, Lee S, Chen J, Sandesara PB, et al. The art of cardiovascular risk assessment. Clin Cardiol. 2018;41:677–84. https://doi.org/10.1002/clc.22930.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. https://doi.org/10.1136/bmj.n71.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Higgins J, Thomas James Cochrane Handbook for Systematic Reviews of Interventions. Version 6.2. Copyright © 2021 The Cochrane Collaboration; https://training.cochrane.org/handbook/current.

  19. National Institution of Health U.S Department of Health and Human Services Quality assessment tool for observational cohort and cross-sectional studies. 2014; https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools.

  20. Alves FD, Souza GC, Clausell N, Biolo A. Prognostic role of phase angle in hospitalized patients with acute decompensated heart failure. Clin Nutr. 2016;35:1530–4. https://doi.org/10.1016/j.clnu.2016.04.007.

    Article  PubMed  Google Scholar 

  21. Antunes ADA, Vannini FD, Silveira LV de A, Barreti P, Martin LC, et al. Associations between bioelectrical impedance parameters and cardiovascular events in chronic dialysis patients. Int Urol Nephrol. 2012; 1397−403. https://doi.org/10.1007/s11255-012-0337-3.

  22. Irisawa H, Mizushima T Correlation of Body Composition and Nutritional Status with Functional Recovery in Stroke Rehabilitation Patients. 2020; 1–9. https://doi.org/10.3390/nu12071923.

  23. Abe T, Yoshimura Y, Imai R, Yoneoka Y, Tsubaki A, Sato Y. Impact of phase angle on physical function in patients with acute stroke. J Stroke Cerebrovasc. 2021;30:105941. https://doi.org/10.1016/j.jstrokecerebrovasdis.

    Article  Google Scholar 

  24. Wang K, Zelnick LR, Chertow GM, Himmelfarb J, Bansal N. Body composition changes following dialysis initiation and cardiovascular and mortality outcomes in CRIC (chronic renal insufficiency cohort): a bioimpedance analysis substudy. Kidney Med. 2021;3:327–334.e1. https://doi.org/10.1016/j.xkme.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Colín-Ramírez E, Castillo-Martínez L, Orea-Tejeda A, Vázquez-Durán M, Rodríguez AE, Keirns-Davis C. Bioelectrical impedance phase angle as a prognostic marker in chronic heart failure. Nutrition. 2012;28:901–5. https://doi.org/10.1016/j.nut.2011.11.033.

    Article  PubMed  Google Scholar 

  26. González-Islas D, Arámbula-Garza E, Orea-Tejeda A, Castillo-Martínez L, Keirns-Davies C, Salgado-Fernández F, et al. Body composition changes assessment by bioelectrical impedance vectorial analysis in right heart failure and left heart failure. Hear Lung. 2019;49:42–47. https://doi.org/10.1016/j.hrtlng.2019.07.003.

    Article  Google Scholar 

  27. Alves FD, Rabelo-silva ER, Clausell SN, Biolo A. Dynamic changes in bioelectrical impedance vector analysis and phase angle in acute decompensated heart failure. Nutrition. 2015;31:84–9. https://doi.org/10.1016/j.nut.2014.05.004.

    Article  PubMed  Google Scholar 

  28. Da Silva TK, Perry IDS, Brauner JS, Wender OCB, Souza GC, Vieira SRR. Performance evaluation of phase angle and handgrip strength in patients undergoing cardiac surgery: Prospective cohort study. Aust Crit Care. 2018;31:284–90. https://doi.org/10.1016/j.aucc.2017.09.002.

    Article  PubMed  Google Scholar 

  29. Bansal N, Zelnick LR, Himmelfarb J, Chertow GM. Bioelectrical impedance analysis measures and clinical outcomes in CKD. Am J Kidney 2018;72:662–72. https://doi.org/10.1053/j.ajkd.2018.03.030.

    Article  Google Scholar 

  30. Shin J HO, Kim CR, Park KH, Hwang JH, Kim SH. Predicting clinical outcomes using phase angle as assessed by bioelectrical impedance analysis in maintenance hemodialysis patients. Nutrition. 2017;41:7–13. https://doi.org/10.1016/j.nut.2017.02.013.

    Article  PubMed  Google Scholar 

  31. Doesch C, Suselbeck T, Leweling H, Fluechter S, Haghi D, Schoenberg SO, et al. Bioimpedance analysis parameters and epicardial adipose tissue assessed by cardiac magnetic resonance imaging in patients with heart failure. Obesity. 2010;18:2326–32. https://doi.org/10.1038/oby.2010.65.

    Article  PubMed  Google Scholar 

  32. Huang R, Wu M, Wu H, Ye H, Peng Y, Mmed CY et al. Lower phase angle measured by bioelectrical impedance analysis is a marker for increased mortality in incident continuous ambulatory peritoneal. J Ren Nutr. 2019.1–7. https://doi.org/10.1053/j.jrn.2019.06.006.

  33. Castillo Martínez L, Colín Ramírez E, Orea Tejeda A, Asensio Lafuente E, Bernal Rosales LP, Rebollar González V, et al. Bioelectrical impedance and strength measurements in patients with heart failure: comparison with functional class. Nutrition. 2007;23:412–8. https://doi.org/10.1016/j.nut.2007.02.005.

    Article  PubMed  Google Scholar 

  34. Gunn SM, Halbert JA, Giles LC, Stepien JM, Miller MD, Crotty M. Bioelectrical phase angle values in a clinical sample of ambulatory rehabilitation patients. Dyn Med. 2008;7:1–9. https://doi.org/10.1186/1476-5918-7-14.

    Article  Google Scholar 

  35. Massari F, Mastropasqua F, Guida P, De Tommasi E, Rizzon B, Pontraldolfo G, et al. Whole-body bioelectrical impedance analysis in patients with chronic heart failure: Reproducibility of the method and effects of body side. Ital Hear J. 2001;2:594–8.

    CAS  Google Scholar 

  36. Hirose S, Nakajima T, Nozawa N, Katayanagi S Phase angle as an indicator of sarcopenia, malnutrition, and cachexia in inpatients with cardiovascular diseases. 2020; 1–16. https://doi.org/10.3390/jcm9082554.

  37. Sobieszek G, Mlak R, Powrózek T, Mazurek M, Skwarek-Dziekanowska A, Terlecki P, et al. Polymorphism of the ITGAM gene (rs7193943) and bioelectric impedance analysis as potential predictors of cachexia in chronic heart failure. Sci Rep. 2021;11:1–8. https://doi.org/10.1038/s41598-021-99719-6.

    CAS  Article  Google Scholar 

  38. Scicchitano P, Ciccone MM, Passantino A, Valle R, De Palo M, Sasanelli P, et al. Congestion and nutrition as determinants of bioelectrical phase angle in heart failure. Hear Lung. 2020;49:724–8. https://doi.org/10.1016/j.hrtlng.2020.07.007.

    Article  Google Scholar 

  39. Portugal MRC, Canella DS, Curioni CC, Bezerra FF, Faerstein E, Neves MF, et al. Bioelectrical impedance analysis–derived phase angle is related to risk scores of a first cardiovascular event in adults. Nutrition. 2020;78:110865. https://doi.org/10.1016/j.nut.2020.110865.

    Article  PubMed  Google Scholar 

  40. Harada H, Ikeda H, Nishiyama Y, Niiyama H, Katoh A, Kai H. Increased arterial velocity pulse index is an independent factor related to skeletal muscle mass reduction and tissue damage in patients with cardiovascular disease. Hypertens Res. 2020;43:534–42. https://doi.org/10.1038/s41440-020-0404-6.

    CAS  Article  PubMed  Google Scholar 

  41. Langer RD, Larsen SC, Ward LC, Heitmann BL. Phase angle measured by bioelectrical impedance analysis and the risk of cardiovascular disease among adult Danes. Nutrition. 2021;89:111280. https://doi.org/10.1016/j.nut.2021.111280.

    Article  PubMed  Google Scholar 

  42. Chiong M, Wang ZV, Pedrozo Z, Cao DJ, Troncoso R, Ibacache M, et al. Cardiomyocyte death: mechanisms and translational implications. Cell Death. 2011;2:e244–11. https://doi.org/10.1038/cddis.2011.130.

    CAS  Article  Google Scholar 

  43. Barrea L, Muscogiuri G, Pugliese G, Laudisio D, de Alteriis G, Graziadio C, et al. Phase angle as an easy diagnostic tool of meta-inflammation for the nutritionist. Nutrients. 2021;13:1446. https://doi.org/10.3390/nu13051446.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Stobäus N, Pirlich M, Valentini L, Schulzke JD, Norman K. Determinants of bioelectrical phase angle in disease. Br J Nutr. 2012;107:1217–20. https://doi.org/10.1017/S0007114511004028.

    CAS  Article  PubMed  Google Scholar 

  45. Tsipis A, Athanassiadou AM, Petrou E, Miliopoulos D, Athanassiadou P, Kavantzas N, et al. From cell to heart: the impact of the cell organelles dysfunction on heart disease. J Cardiovasc Med. 2018;19:131–40. https://doi.org/10.2459/JCM.0000000000000628.

    CAS  Article  Google Scholar 

  46. Chistiakov DA, Shkurat TP, Melnichenko AA, Grechko V, Orekhov AN The role of mitochondrial dysfunction in cardiovascular disease: a brief review. Ann Med. 2017; 0:000. https://doi.org/10.1080/07853890.2017.1417631.

  47. Mattiello R, Amaral MA, Mundstock E, Ziegelmann PK Reference values for the phase angle of the electrical bioimpedance: Systematic review and meta-analysis involving more than 250,000 subjects. Clin Nutr. 2019; 1–7. https://doi.org/10.1016/j.clnu.2019.07.004.

  48. Gonzalez MC, Barbosa-silva TG, Bielemann RM, Gallagher D, Heymsfield SB. Phase angle and its determinants in healthy subjects: influence of body composition. Am J Clin Nutr. 2016;1:1–5. https://doi.org/10.3945/ajcn.115.116772.

    CAS  Article  Google Scholar 

  49. Lukaski HC, Kyle UG, Kondrup J. Assessment of adult malnutrition and prognosis with bioelectrical impedance analysis: phase angle and impedance ratio. Curr Opin Clin Nutr Metab Care. 2017;20:330–9. https://doi.org/10.1097/MCO.0000000000000387.

    Article  PubMed  Google Scholar 

  50. Dittmar M. Reliability and variability of bioimpedance measures in normal adults: effects of age, gender, and body mass. Am J Phys Anthropol. 2003;122:361–70. https://doi.org/10.1002/ajpa.10301.

    Article  PubMed  Google Scholar 

  51. Kyle UG, Bosaeus I, De Lorenzo AD, Deurenberg P, Elia M, Gómez JM, et al. Bioelectrical impedance analysis - Part I: Review of principles and methods. Clin Nutr. 2004;23:1226–43. https://doi.org/10.1016/j.clnu.2004.06.004.

    Article  PubMed  Google Scholar 

  52. Ringaitiene D, Gineityte D, Vicka V, Zvirblis T, Norkiene I, Sipylaite J, et al. Malnutrition assessed by phase angle determines outcomes in low-risk cardiac surgery patients. Clin Nutr. 2016;35:1328–32. https://doi.org/10.1016/j.clnu.2016.02.010.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Rio Grande do Sul Research Support Foundation (FAPERGS), the National Research Council of Brazil (CNPq) and the Coordination for the Improvement of Higher Education Personnel CAPES Financial Code 001.

Author information

Authors and Affiliations

Authors

Contributions

ELB: designed research, conducted research, wrote paper, had primary responsibility for final content, read and approved the final manuscript; JC: designed research, conducted research, wrote paper, had primary responsibility for final content, read and approved the final manuscript. PKZ: analyzed data or performed statistical analysis, had primary responsibility for final content, read and approved the final manuscript; WCM: had primary responsibility for final content, read and approved the final manuscript; LCB: had primary responsibility for final content, read and approved the final manuscript. MRG: had primary responsibility for final content, read and approved the final manuscript and RM: designed research, conducted research, analyzed data or performed statistical analysis, wrote paper, had primary responsibility for final content, read and approved the final manuscript.

Corresponding author

Correspondence to Rita Mattiello.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

de Borba, E.L., Ceolin, J., Ziegelmann, P.K. et al. Phase angle of bioimpedance at 50 kHz is associated with cardiovascular diseases: systematic review and meta-analysis. Eur J Clin Nutr (2022). https://doi.org/10.1038/s41430-022-01131-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41430-022-01131-4

Further reading

Search

Quick links