Comparison of Body Composition Assessed by Multi-Frequency Segmental Bioelectrical Impedance Analysis and Dual Energy X-Ray Absorptiometry in Hemodialysis Patients

Abstract

Background: The assessment of body composition during the course of treatment of hemodialysis patients is crucial for optimal treatment. We intended to assess the diagnostic performance of bioelectrical impedance analysis (BIA), which could be used at the bedside in dialysis wards, and compare it with the results of dual-energy X-ray absorptiometry (DEXA). Methods: In a cross-sectional study, 43 patients with end-stage renal disease (ESRD) after hemodialysis sessions underwent direct segmental multi-frequency BIA. Volume status and body composition indices with eight electrodes connected to four limbs were measured at 1, 5, 50, 250, 500, and 1000 kHz frequencies. Then, the patients were sent to the nuclear ward for the corresponding assessments by DEXA. The results of the two methods were compared by a paired t-test and the correlations were assessed using general linear models and regression analyses. For the assessment of agreements, Bald-Altman plots were used. Results: The whole body values for bone, fat, and lean body mass were different between BIA (3.4, 22, and 44.5 kg, respectively) and DEXA (1.5, 28.5, and 40.4 kg, respectively). However, the results were strongly linearly correlated even after adjustment for age and sex (r = 0.67, P = 0.001 for bone mass; r = 0.93, P = 0.001 for fat mass; and r = 0.96, P = 0.001 for lean body mass). The same strong correlation was found for the segmental values. Conclusions: The results of BIA and DEXA are correlated strongly and are interchangeable. As the BIA is more easily available and less expensive, the routine use of BIA at hemodialysis departments is reasonable.

Full text

Uncorrected Proof
Nephro-Urol Mon. In Press(In Press):e83835.
Published online 2018 October 1.
doi: 10.5812/numonthly.83835.
Research Article
Comparison of Body Composition Assessed by Multi-Frequency
Segmental Bioelectrical Impedance Analysis and Dual Energy X-Ray
Absorptiometry in Hemodialysis Patients
Mohammad Taghi Najafi1, Omid Nasiri 1, *, Azam Alamdari 1, **, Farzanehsadat Minoo 1, Mehrshad
Abbasi 2, Saeed Farzanefar 2and Mohammad Reza Abbasi1
1Nephrology Research Center, TehranUniversity of Medical Sciences, Tehran, Iran
2Department of Nuclear Medicine, Vali-Asr Hospital, Tehran University of Medical Sciences, Tehran,Iran
*Corresponding author: Nephrology Research Center, Tehran University of Medical Sciences, Tehran, Iran. E-mail: o_nasiri@yahoo.com
**Corresponding author: Nephrology Research Center, TehranUniversity of Medical Science, Tehran, Iran. E-mail: a-alamdari@sina.tums.ac.ir
Received 2018 September 02; Revised 2018 September 05; Accepted 2018 September 06.
Abstract
Background: The assessment of body composition during the course of treatment of hemodialysis patients is crucial for optimal
treatment. We intended to assess the diagnostic performance of bioelectrical impedance analysis (BIA), which could be used at the
bedside in dialysis wards, and compare it with the results of dual-energy X-ray absorptiometry (DEXA).
Methods: In a cross-sectional study, 43 patients with end-stage renal disease (ESRD) after hemodialysis sessions underwent direct
segmental multi-frequency BIA. Volume status and body composition indices with eight electrodes connected to four limbs were
measured at 1, 5, 50, 250, 500, and 1000 kHz frequencies. Then, the patients were sent to the nuclear ward for the corresponding
assessments by DEXA. The results of the two methods were compared by a paired t-test and the correlations were assessed using
general linear models and regression analyses. For the assessment of agreements, Bald-Altman plots were used.
Results: The whole body values for bone, fat, and lean body mass were different between BIA (3.4, 22, and 44.5 kg, respectively) and
DEXA (1.5, 28.5, and 40.4 kg, respectively). However, the results were strongly linearly correlated even after adjustment for age and
sex (r = 0.67, P = 0.001 for bone mass; r = 0.93, P = 0.001 for fat mass; and r = 0.96, P = 0.001 for lean body mass). The same strong
correlation was found for the segmental values.
Conclusions: The results of BIA and DEXA are correlated strongly and are interchangeable. As the BIA is more easily available and
less expensive, the routine use of BIA at hemodialysis departments is reasonable.
Keywords: Dual-Energy X-Ray Absorptiometry (DEXA), Bioelectrical Impedance Analysis (BIA), Hemodialysis, Body Composition,
Fat Mass, Bone Mass, Lean Body Mass
1. Background
Chronic kidney disease (CKD) is a common health
problem with a rising prevalence all over the world (1,2).
Unfortunately, in spite of increasing expenditures (3), the
patients have high mortality and morbidity (4), as well as
a low quality of life (5). Despite the recent technological
development, the survival of ESRD patients treated with
hemodialysis remains low, with an expected survival less
than that for patients with a solid tumor (6). An important
factor to control this problem is improving the nutritional
status of these patients (7). Malnutrition has been identi-
fied as a major independent risk factor for survival of pa-
tients undergoing hemodialysis (8). Many patients are old,
malnourished, and have multiple comorbidities. The stan-
dard anthropometric assessment provides a valuable view
of the nutritional status of the patients. Several methods
are employed for muscle mass assessment including an-
thropometrics, creatinine kinetics, bioelectric impedance
analysis, and dual-energy X-ray absorptiometry. Among
these methods, dual-energy X-ray absorptiometry (DEXA)
is the most reliable technique for the estimation of bone
mass, fat mass, and lean body mass. However, in compar-
ison with DEXA, bioelectrical impedance analysis (BIA) is
more convenient, less expensive, and operational at the pa-
tient’s bedside in hemodialysis centers (9). The question
is the accuracy of the measurements by BIA in comparison
with the more acceptable methods. This study assessed the
association of the measurements of multi-frequency BIA
for the estimation of body composition with the results of
Copyright © 2018, Author(s). This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License
(http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly
cited.

Uncorrected Proof
Najafi MT et al.
DEXA in outpatient hemodialysis patients. The core assess-
ment was extended to the segmental analysis of upper and
lower extremities.
2. Methods
The study population included outpatients undergo-
ing hemodialysis for four hours thrice a week. They were
at least 18 years old with a history of hemodialysis at least
for 3 months. Patients with any of the following complica-
tions were excluded from the study: Breastfeeding or preg-
nancy, intra-cardiac defibrillator device, pacemaker, ortho-
pedic joint device, history of myocardial infarction or cere-
brovascular accident, lymphedema, deep vein thrombosis,
and psychiatric disorders/diseases. BIA (InBody S10) was
performed after the second hemodialysis session while the
patients were in the supine position with two electrodes
placed on each extremity. In the next step, by using six
different frequencies (1, 5, 50, 250, 500, and 1000 kHz), 30
segmental resistances were measured in each individual.
The following parameters were assessed by BIA: Intracellu-
lar water (ICW), extracellular water (ECW), total body water
(TBW), proteins, minerals, free fat mass (FFM), skeletal lean
mass, skeletal muscle mass (SMM), body cell mass (BCM),
and bone mineral content (BMC). Finally, the patients were
referred to the department of nuclear medicine for the as-
sessment of body composition by the DEXA method. Table
1presents a summary of the specifications of the BIA and
DEXA methods. Written informed consent was obtained
from all the study subjects. The study conforms to the lo-
cal and international ethical concerns and it was approved
by the Ethics Committee of the University. The difference
between the values of BIA and DEXA methods was tested by
paired t-test, the correlation was studied by the assessment
of Pearson’s coefficient of correlation, and the adjustment
for the interfering co-variables was assessed by the use of
general linear models (i.e. ANCOVA). Bland-Altman’s plots
were depicted for the assessment of agreement between
the results of BIA and DEXA. P value equal to 0.05 was con-
sidered for significant changes and correlations in SPSS V.
18 software (Chicago, IL).
3. Results
A total of 43 patients (26 males; 60.5%) aged 59.9 ±
12.5 years (males: 57.6 ±12.3 years; females: 63.5 ±12.4
years) were recruited to the study. Table 2 represents the
main bone, fat mass, and muscle mass indices derived
from DEXA and BIA. The bone, fat, and muscle indices are
significantly different between the two methods. The dif-
ferences between the bone, fat, and lean body mass indices
of the two methods were 1.9 ±0.5, -6.5 ±4.3, and 4.1 ±3.6,
respectively (all differences significant; P = 0.0001). The
bone, fat, and muscle mass measurements by DEXA and
BIA were correlated significantly with reasonably high co-
efficients of correlation (Figure 1). The lean body mass of
four limbs by the two methods was significantly correlated
(Table 3). The correlation of the bone mineral density de-
rived from DEXA examination and the bone mass by BIA re-
mained significant after adjustment for the effect of age,
sex, and weight (r = 0.67; P = 0.001). The correlations of
the fat mass (r = 0.93; P = 0.001) and the lean body mass
(r = 0.94; P = 0.001) by DEXA and BIA methods were also sig-
nificant independent of the effect of age, sex, and weight.
The two methods had considerable agreements as shown
in Figure 2. The equation for conversion of the values of
BIA (X) into the values of DEXA (Y) is as follows:
(1)Y=aX +b
where a and b are respectively 0.30 and 0.44 for bone
content, 0.75 and 7.0, for lean body mass, and 0.96 and 7.3
for fat mass (all in kg).
4. Discussion
This study reports a strong correlation between the
body composition indices of DEXA and BIA in the whole
body and segmental analyses. The differences between the
results obtained by the two methods were considerable
but the values were easily interchangeable after conver-
sion. The reliable assessment of body composition in rou-
tine practice can help improve the quality of life and re-
duce the morbidity and mortality of patients with ESRD
(10). The results of the measurement by DEXA are accept-
able (11) although DEXA is often unavailable in hemodialy-
sis wards and expose patients to X-ray albeit very low doses
(12). BIA can be used to perform regular assessments of
nutritional condition at the bedside since the instrument
is portable. The cost of the instrument and consequently,
the charge of the procedure are considerably lower for BIA
than for DEXA (13). A close linear correlation between the
results of DEXA and BIA with the possibility of conversion,
when needed, reassures the routine use of BIA.
The results concerning the correlation between the
whole body and segmental values of lean body mass by
the two methods are consistent with the findings of other
studies. Furstenberg and Davenport measured the values
for right lower and left upper limbs demonstrating a high
correlation between the values of the two methods (14).
Ling et al. found a perfect correlation between the whole
body measurements of DEXA and BIA (r = 0.95) (15) while
Anderson et al. replicated the results with certain gender
differences (i.e. r = 0.91 in men and r = 0.88 in women)
2Nephro-Urol Mon. In Press(In Press):e83835.

Uncorrected Proof
Najafi MT et al.
Table1. The Characteristics of Instrumentation and Methods of Assessment of Body Composition
Assessment Method Specification
Bioelectric impedance analysis
instrument
InBody S10 (Tepral,Perafita, Portugal); two electrodes for each extremity (overall 8 electrodes); six different frequencies (1, 5,
50, 250, 500, and 1000 kHz); overall 30 impedance measurements.
Bone densitometer STRATOS (DMS group, Mauguio, France); dual energy X-ray radiation, a scan length of less than 60 min; an overall absorbed
dose of less than three microSiv per examination; measurement of bone mineral density, lean body,and fat mass in the
whole body and segmental analyses.
Table2. Body Composition Indices of Participants Measured by the Two DEXA and BIA Methodsa
Males Females Total
Age, y 57.6 (12.3) 63.5 (12.4) 59.9 (12.5)
Weight, kg 73.2 (16) 66.1 (15.8) 70.4 (16.1)
Bone - based on DEXA, kg 1.6 (0.3) 1.3 (0.2) 1.5 (0.3)b
Fat - based on DEXA, kg 27.4 (11.1) 30.3 (13.1) 28.5 (11.9)
Lean weight - based on DEXA, kg 44.2 (6.9) 34.6 (4.9) 40.4 (7.8)b
Bone - based on BIA, kg 3.7 (0.6) 2.9 (0.4) 3.4 (0.7)b, c
Fat - based on BIA, kg 19.3 (10.2) 26.1 (12.4) 22 (11.5)c
Lean weight - based on BIA, kg 49.4 (8.4) 37.1 (6.4) 44.5 (9.7)b, c
aValues are expressed as means (SD).
bSignificant differences (P < 0.05) between the values of males and females.
cSignificant differences (P < 0.05) between the values of DEXA and BIA.
Table3. Correlation Between the Segmental Lean Body Mass Values Obtained by the TwoMethods
DEXA BIA Mean DifferenceaCoefficient of Correlationa
Right arm 2.68 2.3 -0.4 (< 0.001) 0.88 (< 0.001)
Left arm 2.76 2.3 -0.4 (< 0.001) 0.79 (< 0.001)
Right leg 7.05 5.7 -1.3 (< 0.001) 0.89 (< 0.001)
Left leg 6.91 5.7 -1.2 (< 0.001) 0.87 (< 0.001)
Abbreviations: BIA, bioelectrical impedance analysis; DEXA, dual energy X-ray absorptiometry.
aData are differences and coefficients of correlation (Pearson r) and P values are in parentheses.
2.20
2.00
1.80
1.60
1.40
1.20
1.00
.80
60.00
40.00
20.00
.00
55.00
50.00
45.00
40.00
35.00
30.00
25.00
R2Linear = 0.445 R2Linear = 0.869 R2Linear = 0.886
Bone (kg) Based on DEXA
Bone (kg) Based on BI Fat (kg) Based on BI Lean(kg) Based on BI
Fat (kg) Based on DEXA
Lean Weight (kg)- DEXA
2.000 2.500 3.000 3.500 4.000 4.500 5.000 .000 10.000 20.000 30.00040.000 50.000 60.000 20.00 30.00 40.00 50.00 60.00 70.00
A B C
Figure 1. Correlation between the body composition indices of by DEXA and BIA. A, B, and C depict the data for bone, fat, and lean body mass.
(16). Notably, the extent of the correlation and correspond-
ingly, the validity of the values in the upper limbs mainly
on the left side are weak, probably due to arteriovenous fis-
tula (17). Buckinx et al. found a weak correlation between
these two variables. However, one of the limitations of this
study was that the hydration status of the persons had not
been determined before BIA running and this factor could
influence the results. Table 4 presents a summary of the re-
sults and specifications of previous studies.
Several studies have also presented convincing data,
considering the correlation of the measurements of fat
mass by DEXA and BIA (14-16,18,19). There are similar find-
Nephro-Urol Mon. In Press(In Press):e83835. 3

Uncorrected Proof
Najafi MT et al.
3.00
2.50
2.00
1.50
1.00
.50
3.00
.00
-5.00
-10.00
-15.00
-20.00
15.00
10.00
5.00
.00
-5.00
Difference (Bone Index)
Difference (Fat Mass)
Mean (Bone Index) Mean (Fat Mass) Mean (Lean Body Mass)
Difference (Lean Boy Mass)
1.50 2.00 2.50 3.00 3.50 .00 10.00 20.00 30.00 40.00 50.00 60.00 30.00 40.00 50.00 60.00
A B C
Figure 2. Bland-Altman’s plot for the assessment of agreement between the measurements by BEXA and BIA methods. Bone mineral content, fat mass, and lean body mass by
BIA reasonably correspond to the measurements by DEXA.
Table4. A Summary of the Results of Previous Studiesa
Study Year Sample Size Fat Mass Lean Body Mass Bone Mass Specification
Furstenberg and Davenport (14)2011 53 H 0.93 0.95 0.77 Weaker correlation in the upper limbs
Ling et al. (15)2011 484 0.94 *
Molfina et al. (18)2012 36 (11 H) 0.87 *
Anderson et al. (16)2012 50 (25 H) M = 0.87, F = 0.95 Attention to the gender differences
Kamimura et al. (19)2003 30 0.91 *
Current study 2015 43H 0.93 0.96 0.67 Four limbs segmental and whole body
Abbreviation: H, hemodialysis.
aData are coefficients of correlation (i.e. Pearson’s r).
* Indicates only whole body assessment and not segmental.
ings for bone mass (14); however, as it was speculated by
Furstenberg, we found that multifrequency BIA overesti-
mates bone mass in hemodialysis patients. The reason be-
hind the increase in bone mass is probably the indirect
measurement of bone content by calculations based on
the values of normal population that hindered the possi-
bility to extrapolating the calculation algorithm into pa-
tients with ESRD suffering acid-base and fluid imbalance
(14). Thus, patients are in need of the assessment of bone
mineral density by employing the DEXA method periodi-
cally.
When the patient is volume overloaded, multifre-
quency BIA overestimates lean body mass (20). Therefore,
measurements should be conducted at a constant hydra-
tion status. The advantage of multifrequency BIA is that
it can be readily repeated and is noninvasive and inexpen-
sive. Dry weight and target weight for hemodialysis can
be calculated by BIA, which would be a great advantage for
the quality of hemodialysis and reduction of the compli-
cations. The drawback of the procedure is that multifre-
quency BIA cannot be performed in patients with ICD or
pacemaker (21). Malnutrition in patients with ESRD, pa-
tients prone to osteoporosis and more reliable bone min-
eral assessment density may be yet in need. The camera of
DEXA is not readily available at dialysis centers and is ex-
pensive. The present study supports the use of multifre-
quency BIA (InBody S10) in assessing the body composition
of hemodialysis patients. Nevertheless, more research is
needed for the application of this method in patients with
changed body geometry and those with volume imbalance
(22). The significance of our study is to provide the segmen-
tal measurement of lean body mass in all four limbs by two
methods that is unique to the best of our knowledge.
Footnotes
Conflict of Interests: There is no conflict of interests.
Ethical Considerations: 9311402002.
References
1. Couser WG, Remuzzi G, Mendis S, Tonelli M. The contribution of
chronic kidney disease to the global burden of major noncommuni-
cable diseases. Kidney Int. 2011;80(12):1258–70. doi: 10.1038/ki.2011.368.
[PubMed: 21993585].
4Nephro-Urol Mon. In Press(In Press):e83835.

Uncorrected Proof
Najafi MT et al.
2. Najafi I, Shakeri R, Islami F, Malekzadeh F, Salahi R, Yapan-Gharavi M,
et al. Prevalence of chronic kidney disease and its associated risk fac-
tors: The first report from Iran using both microalbuminuria and
urine sediment. Arch Iran Med. 2012;15(2):70–5. [PubMed: 22292573].
3. Honeycutt AA, Segel JE, Zhuo X, Hoerger TJ, Imai K, Williams D.
Medical costs of CKD in the medicare population. J Am Soc Nephrol.
2013;24(9):1478–83. doi: 10.1681/ASN.2012040392. [PubMed: 23907508].
[PubMed Central: PMC3752941].
4. Collins AJ, Foley RN, Gilbertson DT, Chen SC. The state of chronic
kidney disease, ESRD, and morbidity and mortality in the first
year of dialysis. Clin J Am Soc Nephrol. 2009;4 Suppl 1:S5–11. doi:
10.2215/CJN.05980809. [PubMed: 19996006].
5. Poppe C, Crombez G, Hanoulle I, Vogelaers D, Petrovic M. Improving
quality of life in patients with chronic kidney disease: Influence of
acceptance and personality. Nephrol Dial Transplant. 2013;28(1):116–21.
doi: 10.1093/ndt/gfs151. [PubMed: 22822093].
6. Lowrie EG, Lew NL. Death risk in hemodialysis patients: The predictive
value of commonly measured variables and an evaluation of death
rate differences between facilities. Am J Kidney Dis. 1990;15(5):458–82.
doi: 10.1016/s0272-6386(12)70364-5.
7. Kalantar-Zadeh K, Cano NJ, Budde K, Chazot C, Kovesdy CP, Mak
RH, et al. Diets and enteral supplements for improving outcomes
in chronic kidney disease. Nat Rev Nephrol. 2011;7(7):369–84. doi:
10.1038/nrneph.2011.60. [PubMed: 21629229]. [PubMed Central:
PMC3876473].
8. Qureshi AR, Alvestrand A, Divino-Filho JC, Gutierrez A, Heimburger O,
Lindholm B, et al. Inflammation, malnutrition, and cardiac disease
as predictors of mortality in hemodialysis patients. J Am Soc Nephrol.
2002;13 Suppl 1:S28–36. [PubMed: 11792759].
9. Bross R, Chandramohan G, Kovesdy CP, Oreopoulos A, Noori N,
Golden S, et al. Comparing body composition assessment tests in
long-term hemodialysis patients. Am J Kidney Dis. 2010;55(5):885–96.
doi: 10.1053/j.ajkd.2009.12.031. [PubMed: 20346558]. [PubMed Cen-
tral: PMC3175362].
10. Kalantar-Zadeh K, Ikizler TA, Block G, Avram MM, Kopple JD.
Malnutrition-inflammation complex syndrome in dialysis pa-
tients: Causes and consequences. Am J Kidney Dis. 2003;42(5):864–81.
[PubMed: 14582032].
11. Jensen MD, Kanaley JA, Roust LR, O’Brien PC, Braun JS, Dunn WL, et
al. Assessment of body composition with use of dual-energ y X-ray ab-
sorptiometry: Evaluation and comparison with other methods. Mayo
Clin Proc. 1993;68(9):867–73. [PubMed: 8371605].
12. Damilakis J, Adams JE, Guglielmi G, Link TM. Radiation exposure
in X-ray-based imaging techniques used in osteoporosis. Eur Ra-
diol. 2010;20(11):2707–14. doi: 10.1007/s00330-010-1845-0. [PubMed:
20559834]. [PubMed Central: PMC2948153].
13. Bera TK. Bioelectrical impedance methods for noninvasive
health monitoring: A review. J Med Eng. 2014;2014:381251. doi:
10.1155/2014/381251. [PubMed: 27006932]. [PubMed Central:
PMC4782691].
14. Furstenberg A, Davenport A. Comparison of multifrequency bio-
electrical impedance analysis and dual-energy X-ray absorptiome-
try assessments in outpatient hemodialysis patients. Am J Kidney Dis.
2011;57(1):123–9. doi: 10.1053/j.ajkd.2010.05.022.
15. Ling CH, de Craen AJ, Slagboom PE, Gunn DA, Stokkel MP, Wes-
tendorp RG, et al. Accuracy of direct segmental multi-frequency
bioimpedance analysis in the assessment of total body and segmen-
tal body composition in middle-aged adult population. Clin Nutr.
2011;30(5):610–5. doi: 10.1016/j.clnu.2011.04.001. [PubMed: 21555168].
16. Anderson LJ, Erceg DN, Schroeder ET. Utility of multifrequency
bioelectrical impedance compared with dual-energy X-ray absorp-
tiometry for assessment of total and regional body composition
varies between men and women. Nutr Res. 2012;32(7):479–85. doi:
10.1016/j.nutres.2012.05.009.
17. Kraemer M, Rode C, Wizemann V. Detection limit of methods to assess
fluid status changes in dialysis patients. Kidney Int. 2006;69(9):1609–
20. doi: 10.1038/sj.ki.5000286. [PubMed: 16501488].
18. Molfino A, Don BR, Kaysen GA. Comparison of bioimpedance and
dual-energy X-ray absorptiometry for measurement of fat mass
in hemodialysis patients. Nephron Clin Pract. 2012;122(3-4):127–33.
doi: 10.1159/000350817. [PubMed: 23689544]. [PubMed Central:
PMC4353643].
19. Kamimura MA, Avesani CM, Cendoroglo M, Canziani ME, Draibe
SA, Cuppari L. Comparison of skinfold thicknesses and bioelectrical
impedance analysis with dual-energy X-ray absorptiometry for the as-
sessment of body fat in patients on long-term haemodialysis therapy.
Nephrol Dial Transplant. 2003;18(1):101–5. [PubMed: 12480966].
20. Dehghan M, Merchant AT. Is bioelectrical impedance accurate for use
in large epidemiological studies? Nutr J. 2008;7:26. doi: 10.1186/1475-
2891-7-26. [PubMed: 18778488]. [PubMed Central: PMC2543039].
21. Buch E, Bradfield J, Larson T, Horwich T. Effect of bioimpedance
body composition analysis on function of implanted cardiac de-
vices. Pacing Clin Electrophysiol. 2012;35(6):681–4. doi: 10.1111/j.1540-
8159.2012.03377.x. [PubMed: 22452409].
22. Buchholz AC, Bartok C, Schoeller DA. The validity of bioelectri-
cal impedance models in clinical populations. Nutr Clin Pract.
2004;19(5):433–46. doi: 10.1177/0115426504019005433. [PubMed:
16215137].
Nephro-Urol Mon. In Press(In Press):e83835. 5