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Safety and Results of Bioelectrical Impedance Analysis in Patients with Cardiac Implantable Electronic Devices

Abstract

Objective:

To analyze the dual interference between cardiac implantable electronic devices (CIEDs) and bioelectrical impedance analysis (BIA).

Methods:

Forty-three individuals admitted for CIEDs implantation were submitted to a tetrapolar BIA with an alternating current at 800 microA and 50 kHz frequency before and after the devices’ implantation. During BIA assessment, continuous telemetry was maintained between the device programmer and the CIEDs in order to look for evidence of possible electric interference in the intracavitary signal of the device.

Results:

BIA in patients with CIEDs was safe and not associated with any device malfunction or electrical interference in the intracardiac electrogram of any electrode. After the implantation of the devices, there were significant reductions in BIA measurements of resistance, reactance, and measurements adjusted for height resistance and reactance, reflecting an increase (+ 1 kg; P<0.05) in results of total body water and extracellular water in liter and, consequently, increases in fat-free mass (FFM) and extracellular mass in kg. Because of changes in the hydration status and FFM values, without changes in weight, fat mass was significantly lower (-1.2 kg; P<0.05).

Conclusion:

BIA assessment in patients with CIEDs was safe and not associated with any device malfunction. The differences in BIA parameters might have occurred because of modifications on the patients’ body composition, associated to their hydration status, and not to the CIEDs.

Keywords:
Electric Impedance. Body Water. Electrophysiologic Techniques; Cardiac. Body Composition. Electricity. Electrodes. Telemetry

Abbreviations, acronyms & symbols BIA = Bioelectrical impedance analysis ICD = Implantable cardioverter defibrillator BCM = Body cell mass ICW = Intracellular water BMI = Body mass index NYHA = New York Heart Association CIEDs = Cardiac implantable electronic devices PA = Phase angle CRT = Cardiac resynchronization therapy PM = Pacemaker CRT-D = Cardiac resynchronization therapy defibrillator R = Resistance DBP = Diastolic blood pressure RVI = Right ventricle impedance DM = Diabetes mellitus RVT = Right ventricle threshold ECM = Extracellular mass SAH = Systemic arterial hypertension ECW = Extracellular water SBP = Systolic blood pressure FFM = Fat-free mass SD = Standard deviation FM = Fat mass SPSS = Statistical Package for the Social Sciences H = Height TBW = Total body water HF = Heart failure Xc = Reactance

INTRODUCTION

The bioelectrical impedance analysis (BIA) has been described since the 1970s as a body composition assessment method based on the opposition of the biological environment to the alternating electric current, determined by the resistance (R) and reactance (Xc) components[11 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(5):1226-43. doi:10.1016/j.clnu.2004.06.004.
https://doi.org/10.1016/j.clnu.2004.06.0...
,22 Sánchez-Iglesias A, Fernández-Lucas M, Teruel JL. The electrical basis of bioimpedance. Nefrologia. 2012;32(2):133-5. doi:10.3265/Nefrologia.pre2012.Jan.11310.
https://doi.org/10.3265/Nefrologia.pre20...
]. It has been used both in healthy individuals and in some clinical situations, such as malnutrition, trauma, pre- and post-surgical period, liver disease, kidney failure, and heart disease[33 Mushnick R, Fein PA, Mittman N, Goel N, Chattopadhyay J, Avram MM. Relationship of bioelectrical impedance parameters to nutrition and survival in peritoneal dialysis patients. Kidney Int Suppl. 2003;64(87):S53-6. doi:10.1046/j.1523-1755.64.s87.22.x.
https://doi.org/10.1046/j.1523-1755.64.s...

4 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(6):1530-4. doi:10.1016/j.clnu.2016.04.007.
https://doi.org/10.1016/j.clnu.2016.04.0...
-55 Llames L, Baldomero V, Iglesias ML, Rodota LP. [Values of the phase angle by bioelectrical impedance; nutritional status and prognostic value]. Nutr Hosp. 2013;28(2):286-95. doi:10.3305/nh.2013.28.2.6306. Spanish.
https://doi.org/10.3305/nh.2013.28.2.630...
]. It stands out by its applicability at bedside due to the practicality of the method, compared to other body composition techniques[66 Mulasi U, Kuchnia AJ, Cole AJ, Earthman CP. Bioimpedance at the bedside: current applications, limitations, and opportunities. Nutr Clin Pract. 2015;30(2):180-93. Erratum in: Nutr Clin Pract. 2015;30(4):589. doi:10.1177/0884533614568155.
https://doi.org/10.1177/0884533614568155...
].

Cardiac implantable electronic devices (CIEDs) have been used in clinical practice for about five decades. Pacemaker (PM) is used to treat clinically significant bradyarrhythmia. Implantable cardioverter defibrillator (ICD) is used in primary and secondary prevention of sudden cardiac death. In patients with heart failure (HF), ICD and cardiac resynchronization therapy (CRT) can be used, individually or combined (CRT defibrillator [CRT-D)][77 Moss AJ, Zareba W, Hall WJ, Klein H, Wilber DJ, Cannom DS, et al. Prophylactic implantation of a defibrillator in patients with myocardial infarction and reduced ejection fraction. N Engl J Med. 2002;346(12):877-83. doi:10.1056/NEJMoa013474.
https://doi.org/10.1056/NEJMoa013474...

8 Bardy GH, Lee KL, Mark DB, Poole JE, Packer DL, Boineau R, et al. Amiodarone or an implantable cardioverter-defibrillator for congestive heart failure. N Engl J Med. 2005;352(20):225-37. Erratum in: N Engl J Med. 2005;352(20):2146. doi:10.1056/NEJMoa043399.
https://doi.org/10.1056/NEJMoa043399...

9 Martinelli Filho M, Zimerman LI, Lorga AM, Vasconcelos JTM, Rassi A Jr. [Guidelines for implantable electronic cardiac devices of the Brazilian society of cardiology]. Arq Bras Cardiol. 2007;89(6):e210-38. Portuguese.
-1010 Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JGF, Coats AJS, et al. 2016 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the task force for the diagnosis and treatment of acute and chronic heart failure of the European society of cardiology (ESC). Developed with the special contribution of the heart failure association (HFA) of the ESC. Eur Heart J. 2016;37(27):2129-200. Erratum in: Eur Heart J. 2016. doi:10.1093/eurheartj/ehw128.
https://doi.org/10.1093/eurheartj/ehw128...
].

The body composition analysis through BIA assessment is not recommended for CIEDs carriers because it can cause an interference on the devices due to the applied electric current[1111 Kyle UG, Bosaeus I, De Lorenzo AD, Deurenberg P, Elia M, Manuel Gómez J, et al. Bioelectrical impedance analysis -part II: utilization in clinical practice. Clin Nutr. 2004;23(6):1430-53. doi:10.1016/j.clnu.2004.09.012.
https://doi.org/10.1016/j.clnu.2004.09.0...
]. However, the small magnitude of the current sent to the body is way inferior to the susceptibility limits of the devices, such as PM and ICD. Still, there is an absence of information on the devices’ manuals about the use of BIA in CIEDs carriers.

In addition, the protocols for BIA assessment demand attention to the presence of metallic objects in order to avoid conduction of the electric current and erroneous results[1111 Kyle UG, Bosaeus I, De Lorenzo AD, Deurenberg P, Elia M, Manuel Gómez J, et al. Bioelectrical impedance analysis -part II: utilization in clinical practice. Clin Nutr. 2004;23(6):1430-53. doi:10.1016/j.clnu.2004.09.012.
https://doi.org/10.1016/j.clnu.2004.09.0...
], which could be relevant to CIEDs carriers. Considering the limited amount of thorough detailed safety analyses, it is recommended to avoid applying body impedance methods in these cases[1212 Foster KR, Lukaski HC. Whole body impedance -- what does it measure? Am J Clin Nutr. 1996;64(3 Suppl):388S-96S. doi:10.1093/ajcn/64.3.388S.
https://doi.org/10.1093/ajcn/64.3.388S...
]. This limitation may influence not only the benefits that BIA could provide for these patients, such as prognosis and body composition, but also the exclusion of this potentially critical population from analyses of body composition and mortality. This study investigated the dual interference between CIEDs and BIA.

METHODS

Study Population

This is a prospective study that included adult patients (age ≥ 18 years old) from the Brazilian Public Health System referred for CIEDs (PM, ICD, and CRT-D) implantation at the Hospital de Clínicas de Porto Alegre, from June 2015 to November 2016. Exclusion criteria were presence of hydroelectrolytic disorders, edema, amputated limbs, extreme body mass index (BMI) (<16 or >36 kg/m²), skin lesions, and women in menstrual period.

The study was approved by the Ethics Committee of the Hospital de Clínicas de Porto Alegre and it was conducted according to ethical principles of Helsinki. A written informed consent was obtained from all participants before taking part in the study.

Study Protocol

Anthropometric Evaluation

The weight values were obtained by a digital scale and the height (H) by a vertical stadiometer attached to a Filizola® scale - Personal Line (São Paulo, Brazil). Then, BMI was calculated by dividing weight (kg) by square H (m) (WHO, 2000)[1313 World Health Organization. Obesity: preventing and managing the global epidemic. Report of a World Health Organization Consultation. Geneva: World Health Organization, 2000. p. 256. WHO Obesity Technical Report Series, n. 284.].

BIA Assessment

BIA was performed with the tetrapolar device Biodynamics 450 (Biodynamics Corp., Seattle, Washington, USA), which has a 50 kHz frequency and 800 microA current, with duration of 10 to 15 seconds. The subjects were instructed to fast for at least four hours, perform no physical activity the day prior to the assessment, and remove all metallic objects in their possession[11 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(5):1226-43. doi:10.1016/j.clnu.2004.06.004.
https://doi.org/10.1016/j.clnu.2004.06.0...
,1414 Mialich MS, Sicchieri JF, Junior AA. Analysis of body composition: a critical review of the use of bioelectrical impedance analysis. Int J Clin Nutr. 2014;2(1):1-10. doi:10.12691/ijcn-2-1-1.
https://doi.org/10.12691/ijcn-2-1-1...
].

The assessments were performed with the patient in supine position, with arms apart from the body and separated legs. Four disposable electrocardiographic electrodes were used in each assessment (Conmed Corporation, Utica, NY). Two distal electrodes were positioned on the dorsal surfaces (in the hand, next to the metacarpus and the phalange joint, and the foot, next to the metatarsus and the phalange joint), and two were placed on the pisiform prominence of the wrist and between the medial lateral malleolus of the ankle[1515 National Institutes of Health Technology Assessment Conference Statement. Bioelectrical impedance analysis in body composition measurement. Am J Clin Nutr. 1996;64(3 Suppl):524S-32S. doi:10.1093/ajcn/64.3.524S.
https://doi.org/10.1093/ajcn/64.3.524S...
]. The collected measurements of BIA were phase angle (PA), fat-free mass (FFM), fat mass (FM), body cell mass (BCM), extracellular mass (ECM), total body water (TBW), intracellular water (ICW), and extracellular water (ECW). Direct measurements of the BIA R and Xc, both also adjusted for H (R/H and Xc/H), were evaluated. BIA was performed in two moments, before and after the implantation of the CIEDs, obtaining an average of eight days (±9.2) between the first and second evaluation.

Evaluation of CIEDs Functioning

The CIEDs assessments were performed by a cardiac electrophysiologist with a specific device programmer designed for interrogation of the device’s parameters. The device programmer head was placed over the patient’s CIED to establish communication. Baseline interrogation was performed, including assessment of electrical impedance, sensing and capturing thresholds of all leads. In patients with ICD, while tachyarrhythmia detection and sensing were programmed on, all therapies (antitachycardia pacing and shock) were temporarily programmed off to avoid the possibility of inappropriate therapies. During the BIA assessment, continuous telemetry was maintained between the device programmer and CIED in order to look for evidence of possible electric interference in the intracavitary signal of the device. After completion of BIA, sensing and pacing parameters were measured again and all tachyarrhythmias therapies were programmed back to their original settings. The possible detection of anomalous electric activity secondary to the passage of the electric current not intrinsic to the heart on the ventricular electrogram was verified through continuous observation of the intracavitary signal on the device setting during the passage of the BIA’s electrical current in the presence of a high programmable sensitivity for that device.

Statistical Analysis

Data are presented in mean and standard deviation (SD) or median and interquartile range. Continuous variables were compared using Student’s t-test for paired samples or the paired Wilcoxon test, in order to obtain the differences of the BIA parameters before and after the implantation of CIEDs, and the values of the CIEDs before and after BIA. According to the BIA’s manufacturer, a 2 to 3% error is expected due to the standardization protocol for conducting the exam.

The normality analysis was assessed by the Shapiro-Wilk test. Categorical variables were described as absolute and relative frequency. The significance level used was 5%. In order to analyze the data, the Statistical Package for the Social Sciences (SPSS) software (SPSS, Chicago) version 23.0 was used.

RESULTS

The sample consisted of 43 individuals, most were male and Caucasian, mean age was 66 ± 10 years, and 39% of them presented HF (Table 1).

Table 1
Characteristics of the study population (n=43).

Twenty-two patients had PM implanted, 15 had an ICD, and six had CRT-D. Implanted CIEDs were manufactured by Medtronic (n=27) and Biotronik (n=16) (Table 2).

Table 2
Characteristics of the devices implanted in the study sample.

Regarding variations in anthropometric and BIA measurements, weight, BMI, PA, BCM, and ICW showed no difference between the first assessment, without the implanted device, and the second, with the implanted device. However, there were significant reductions (before and after CIEDs implantations) in direct BIA measurements (R, R/H, Xc, Xc/H), reflecting an increase (+ 1 kg) in results of TBW (L) and ECW (L) and, consequently, increases in FFM (kg) and ECM (kg). Because of changes in the hydration status and FFM values, without changes in weight, FM was significantly lower (Table 3). All of these variants were approximately 1.36% of the patients' weight, being within the possible margin of error, referring to the protocol to make the examination, especially if they were changes in hydration status.

Table 3
Comparison of the anthropometric variables and the derived variables from BIA before and after CIEDs implantation.

The impact of BIA assessment on CIEDs showed no electrical interference on intracardiac electrogram of any lead (atrial, right ventricular, left ventricular), in any patient. There was no inappropriate sensing or tachycardia detection in any device. Full interrogation of CIEDs after BIA showed no significant differences in lead parameters or device function (Table 4). No patient presented symptoms during BIA.

Table 4
Comparison between the CIEDs parameters before and after the examination using BIA.

DISCUSSION

In our study, BIA with Biodynamics 450 (Biodynamics Corp. Seattle, Washington, USA) in patients with CIEDs was safe and not associated with any device malfunction. We did not find presence of electrical interference on intracardiac electrogram of any lead (atrial, right ventricular, left ventricular) in any patient. With respect to BIA measurements, the significant variations were related to body water and were within the margin of error of the examination.

Since this is a fast, safe, and non-invasive method, with a relatively low cost, the BIA assessment has been used to estimate the body composition and the nutritional status of healthy individuals and patients[11 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(5):1226-43. doi:10.1016/j.clnu.2004.06.004.
https://doi.org/10.1016/j.clnu.2004.06.0...
,1616 Lee SY, Gallagher D. Assessment methods in human body composition. Curr Opin Clin Nutr Metab Care. 2008;11(5):566-72. doi:10.1097/MCO.0b013e32830b5f23.
https://doi.org/10.1097/MCO.0b013e32830b...
]. Nowadays, its prognostic use has been studied through PA, and a possible correlation between low PA values and mortality has been observed in patients with heart disease[44 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(6):1530-4. doi:10.1016/j.clnu.2016.04.007.
https://doi.org/10.1016/j.clnu.2016.04.0...
,1717 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(9):901-5. doi:10.1016/j.nut.2011.11.033.
https://doi.org/10.1016/j.nut.2011.11.03...
].

Concerning the interference of BIA on CIEDs, the same findings were observed by Buch et al.[1818 Buch E, Bradfield J, Larson T, Horwich T. Effect of bioimpedance body composition analysis on function of implanted cardiac devices. Pacing Clin Electrophysiol. 2012;35(6):681-4. doi:10.1111/j.1540-8159.2012.03377.x.
https://doi.org/10.1111/j.1540-8159.2012...
], while performing BIA at the frequencies of 5, 50, and 500 kHz in 20 individuals with HF. No evidence of interference with ICD function was seen in any patient, including no telemetry disruption, no oversensing on any lead, and no patient symptoms. In another larger study (n=63), which also found no electromagnetic interferences in ICDs, the authors conclude on the safety of this procedure and recommend that the current guidelines should be updated[1919 Meyer P, Makhlouf AM, Mondouagne Engkolo LP, Trentaz F, Thibault R, Pichard C, et al. Safety of bioelectrical impedance analysis in patients equipped with implantable cardioverter defibrillators. J Parenter Enteral Nutr. 2017;41(6):981-5. doi:10.1177/0148607116633823.
https://doi.org/10.1177/0148607116633823...
]. Recently, a study of the findings corroborated the results, in an analysis of 200 individuals, indicating that the use of BIA is safe in patients with cardiac devices[2020 Chabin X, Taghli-Lamallem O, Mulliez A, Bordachar P, Jean F, Futier E, et al. Bioimpedance analysis is safe in patients with implanted cardiac electronic devices. Clin Nutr. 2019;38(2):806-11. doi:10.1016/j.clnu.2018.02.029.
https://doi.org/10.1016/j.clnu.2018.02.0...
].

Despite no interferences being observed on the devices in these previous studies[1818 Buch E, Bradfield J, Larson T, Horwich T. Effect of bioimpedance body composition analysis on function of implanted cardiac devices. Pacing Clin Electrophysiol. 2012;35(6):681-4. doi:10.1111/j.1540-8159.2012.03377.x.
https://doi.org/10.1111/j.1540-8159.2012...
,1919 Meyer P, Makhlouf AM, Mondouagne Engkolo LP, Trentaz F, Thibault R, Pichard C, et al. Safety of bioelectrical impedance analysis in patients equipped with implantable cardioverter defibrillators. J Parenter Enteral Nutr. 2017;41(6):981-5. doi:10.1177/0148607116633823.
https://doi.org/10.1177/0148607116633823...
], they did not assess the BIA parameters, which can also suffer interferences, since they are wrapped by a metallic housing. The instructions regarding the use of BIA include the removal of metallic objects, attention so that the patient is not in contact with metallic structures and, if there is presence of any sort of prosthesis, BIA examination must be on the opposite side in order to avoid conduction of the electric current[1111 Kyle UG, Bosaeus I, De Lorenzo AD, Deurenberg P, Elia M, Manuel Gómez J, et al. Bioelectrical impedance analysis -part II: utilization in clinical practice. Clin Nutr. 2004;23(6):1430-53. doi:10.1016/j.clnu.2004.09.012.
https://doi.org/10.1016/j.clnu.2004.09.0...
].

In BIA measurements, an increment in TBW was observed, which may have occurred by an increase in the hydric volume due to the conditions in the hospital stay, such as saline solution administration after the procedure, and other external factors. This increase in TBW value seems to have been due to the increase in ECW (P<0.001) and for this reason there was no change in FFM (which contains large amounts of ICW ~73%). Another measure of BIA affected by hydration was the ECM, that reflects all the metabolically inactive (non-living) parts of the body, including water contained outside living cells. Still, since resistance values (R and R/H) correlate highly with fluid balance, by facilitating the passage of the electric current, the increase of TBW can impact in the reduction of R and R/H[2121 Piccoli A, Rossi B, Pillon L, Bucciante G. A new method for monitoring body fluid variation by bioimpedance analysis: the RXc graph. Kidney Int. 1994;46(2):534-9. doi:10.1038/ki.1994.305.
https://doi.org/10.1038/ki.1994.305...
]. Similar results were found by Pinto et al.[2222 Pinto LW, Gandra SV, Alves MC, Gomes I, Sternick EB. Bioelectrical impedance analysis of body composition: influence of a newly implanted cardiac device. J Electr Bioimp. 2017;8(1):60-5. doi:10.5617/jeb.4760.
https://doi.org/10.5617/jeb.4760...
] in 62 patients with an indication for PM or defibrillator implantation, and they concluded that decrease in resistance and related parameters were associated to hydration status[22 Sánchez-Iglesias A, Fernández-Lucas M, Teruel JL. The electrical basis of bioimpedance. Nefrologia. 2012;32(2):133-5. doi:10.3265/Nefrologia.pre2012.Jan.11310.
https://doi.org/10.3265/Nefrologia.pre20...
]. This limitation may influence not only the benefits that BIA could provide for these patients, such as prognosis and body composition, but also the exclusion of this potentially critical population from analyses of body composition and mortality. This study analyzed the dual interference between CIEDs and BIA[2222 Pinto LW, Gandra SV, Alves MC, Gomes I, Sternick EB. Bioelectrical impedance analysis of body composition: influence of a newly implanted cardiac device. J Electr Bioimp. 2017;8(1):60-5. doi:10.5617/jeb.4760.
https://doi.org/10.5617/jeb.4760...
].

A reduction in reactance values (Xc and Xc/H), reflecting tissue (not water) changes or the absorption of electrical current in tissues, was also demonstrated in our study, and this reflected in the reduction of the calculated measurement in BIA of FM.

Our study has some possible limitations that need to be considered. Our sample was relatively small, and we studied only a single BIA system in patients with CIEDs of two manufacturers. Considering these, our results cannot be applied to all patients with CIEDs or to different BIA systems. Another limitation is the variability of the evaluation time between the first and second BIA. This interval might have influenced the body composition of the individuals, as it was observed in the FM and TBW outcomes, in which case CIEDs might not have influenced this finding.

CONCLUSION

In our study, BIA assessment in patients with CIEDs was safe and not associated with any device malfunction. The differences in BIA measurements might have occurred because of modifications on the patients’ body composition, caused by their hydration status, and not by the CIEDs’ presence. Further larger studies are required to confirm these findings and to determine a change in guidelines and manufacturer’s recommendations.

Author's roles & responsibilities LMG Substantial contributions to the conception of the work, analysis, and interpretation of data for the work; drafting the work and revising it critically for important intellectual content; final approval of the version to be published FDA Substantial contributions to the conception of the work; final approval of the version to be published AK Substantial contributions to the conception of the work, analysis, and interpretation of data for the work; drafting the work and revising it critically for important intellectual content; final approval of the version to be published PZ Drafting the work or revising it critically for important intellectual content; final approval of the version to be published LZ Drafting the work or revising it critically for important intellectual content; final approval of the version to be published MP Substantial contributions to the interpretation of data for the work; drafting the work and revising it critically for important intellectual content; final approval of the version to be published ISP Substantial contributions to the interpretation of data for the work; drafting the work and revising it critically for important intellectual content; final approval of the version to be published GCS Substantial contributions to the interpretation of data for the work; drafting the work and revising it critically for important intellectual content; agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved; final approval of the version to be published NC Drafting the work or revising it critically for important intellectual content; agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved; final approval of the version to be published

ACKNOWLEDGEMENT

We are thankful to the Hospital de Clínicas de Porto Alegre, the Fundo de Incentivo à Pesquisa (FIPE), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financing this research.

  • Financial support: This study was funded by Hospital de Clínicas de Porto Alegre, Fundo de Incentivo à Pesquisa (FIPE) 150145/Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
  • This study was carried out at the Universidade Federal do Rio Grande do Sul - UFRGS, Porto Alegre, RS, Brazil.

REFERENCES

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    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(5):1226-43. doi:10.1016/j.clnu.2004.06.004.
    » https://doi.org/10.1016/j.clnu.2004.06.004
  • 2
    Sánchez-Iglesias A, Fernández-Lucas M, Teruel JL. The electrical basis of bioimpedance. Nefrologia. 2012;32(2):133-5. doi:10.3265/Nefrologia.pre2012.Jan.11310.
    » https://doi.org/10.3265/Nefrologia.pre2012.Jan.11310
  • 3
    Mushnick R, Fein PA, Mittman N, Goel N, Chattopadhyay J, Avram MM. Relationship of bioelectrical impedance parameters to nutrition and survival in peritoneal dialysis patients. Kidney Int Suppl. 2003;64(87):S53-6. doi:10.1046/j.1523-1755.64.s87.22.x.
    » https://doi.org/10.1046/j.1523-1755.64.s87.22.x
  • 4
    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(6):1530-4. doi:10.1016/j.clnu.2016.04.007.
    » https://doi.org/10.1016/j.clnu.2016.04.007
  • 5
    Llames L, Baldomero V, Iglesias ML, Rodota LP. [Values of the phase angle by bioelectrical impedance; nutritional status and prognostic value]. Nutr Hosp. 2013;28(2):286-95. doi:10.3305/nh.2013.28.2.6306. Spanish.
    » https://doi.org/10.3305/nh.2013.28.2.6306
  • 6
    Mulasi U, Kuchnia AJ, Cole AJ, Earthman CP. Bioimpedance at the bedside: current applications, limitations, and opportunities. Nutr Clin Pract. 2015;30(2):180-93. Erratum in: Nutr Clin Pract. 2015;30(4):589. doi:10.1177/0884533614568155.
    » https://doi.org/10.1177/0884533614568155
  • 7
    Moss AJ, Zareba W, Hall WJ, Klein H, Wilber DJ, Cannom DS, et al. Prophylactic implantation of a defibrillator in patients with myocardial infarction and reduced ejection fraction. N Engl J Med. 2002;346(12):877-83. doi:10.1056/NEJMoa013474.
    » https://doi.org/10.1056/NEJMoa013474
  • 8
    Bardy GH, Lee KL, Mark DB, Poole JE, Packer DL, Boineau R, et al. Amiodarone or an implantable cardioverter-defibrillator for congestive heart failure. N Engl J Med. 2005;352(20):225-37. Erratum in: N Engl J Med. 2005;352(20):2146. doi:10.1056/NEJMoa043399.
    » https://doi.org/10.1056/NEJMoa043399
  • 9
    Martinelli Filho M, Zimerman LI, Lorga AM, Vasconcelos JTM, Rassi A Jr. [Guidelines for implantable electronic cardiac devices of the Brazilian society of cardiology]. Arq Bras Cardiol. 2007;89(6):e210-38. Portuguese.
  • 10
    Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JGF, Coats AJS, et al. 2016 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the task force for the diagnosis and treatment of acute and chronic heart failure of the European society of cardiology (ESC). Developed with the special contribution of the heart failure association (HFA) of the ESC. Eur Heart J. 2016;37(27):2129-200. Erratum in: Eur Heart J. 2016. doi:10.1093/eurheartj/ehw128.
    » https://doi.org/10.1093/eurheartj/ehw128
  • 11
    Kyle UG, Bosaeus I, De Lorenzo AD, Deurenberg P, Elia M, Manuel Gómez J, et al. Bioelectrical impedance analysis -part II: utilization in clinical practice. Clin Nutr. 2004;23(6):1430-53. doi:10.1016/j.clnu.2004.09.012.
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Publication Dates

  • Publication in this collection
    07 Nov 2019
  • Date of issue
    Mar-Apr 2020

History

  • Received
    08 Mar 2019
  • Accepted
    24 Apr 2019
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