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Measurement of body water by multifrequency bioelectrical impedance spectroscopy in a multiethnic pediatric population^1,2,3,4

¹ From the Body Composition Laboratory, US Department of Agriculture, Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, and Texas Children's Hospital, Houston.

² Supported by the US Department of Agriculture, Agricultural Research Service, under cooperative agreement 58-6250-6-001 with Baylor College of Medicine.

³ This work is a publication of the USDA/ARS Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, and Texas Children's Hospital, Houston. The contents of this publication do not necessarily reflect the views or policies of the USDA, nor does mention of trade names, commercial products, or organizations imply endorsement.

⁴ Address reprint requests to KJ Ellis, Body Composition Laboratory, Children's Nutrition Research Center, 1100 Bates Street, Houston, TX 77030. E-mail: kellis{at}bcm.tmc.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Background: Bioelectrical impedance spectroscopy (BIS) may provide a noninvasive, rapid method for the assessment of total body water (TBW), extracellular water (ECW), and intracellular water (ICW). Few studies, however, have examined the accuracy of BIS in pediatric populations.

Objective: Our objective was to evaluate the accuracy of BIS for the measurement of TBW, ECW, and ICW in healthy children.

Design: Dual-energy X-ray absorptiometry (DXA), total body potassium (TBK), and BIS measurements were performed in 347 children (202 males and 145 females aged 4–18 y). The reference values for TBW, ECW, and ICW were defined by using a DXA+TBK model. BIS values were evaluated by using the method of Bland and Altman. A randomly selected calibration group (n = 231) was used to derive new BIS constants that were tested in the remaining group (n = 116).

Results: BIS values were highly correlated with the reference values (r² = 0.94–0.97, P < 0.0001), but differences between the BIS and DXA+TBK models for individuals were significant (P < 0.001). Use of new BIS constants reduced the mean differences between the BIS and DXA+TBK models; the SDs of the mean differences were improved (1.8 L for TBW, 1.4 L for ICW, and 1.0 L for ECW) for the total population.

Conclusions: On a population basis, BIS can be calibrated to replace the DXA+TBK model for the assessment of TBW, ECW, and ICW in healthy children. The accuracy of the BIS measurement in individual children may be refined further by using age- and sex-specific adjustments for the BIS calibration constants.

Key Words: Total body water • extracellular water • intracellular water • bioelectrical impedance analysis • bioelectrical impedance spectroscopy • dual-energy X-ray absorptiometry • total body potassium • children • adolescents • body composition

	INTRODUCTION

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Water is the main component of the body's fat-free mass (FFM) and its fractional content changes during the normal life span (1, 2). Some clinical conditions can produce both acute and chronic changes in the hydration of the FFM (3–5). Thus, accurately monitoring the distribution of water in the body has been a major clinical challenge. Although the classic dilution principle has been used to measure total body water (TBW), this technique has had limited success in most clinical settings (6, 7).

Even when successful, the TBW dilution methods do not provide information about the relative volumes of the intracellular water (ICW) or extracellular water (ECW) compartments. Estimates of ECW volume can be obtained by using the dilution principle; the tracers most commonly used are bromine or sucrose (8, 9). In healthy subjects, it appears that the body's water distribution is normally tightly regulated; therefore, the difference between the TBW and ECW estimates can be used to approximate the ICW volume. In an abnormal state, however, these ratios can be significantly altered, reducing the accuracy of the ICW estimate.

Although the dilution techniques are often cited as the reference methods for body water measurements (6, 10), short-term repeat measurements are difficult, if not impossible, to achieve. Bioelectrical impedance techniques offer the ability to perform frequent, rapid, noninvasive measurements. Single-frequency bioelectrical impedance analysis instruments have been examined extensively (11), but their application in some diseases appears to have serious limitations (11, 12). Bioelectrical impedance spectroscopy (BIS) overcomes at least one of these concerns because a full range of frequencies (1 kHz to 1.35 MHZ) is used in the analysis. Only a few studies, however, have compared the results of BIS measurements with those of other measures of the body water compartments (12–16). Of these studies, only one reported a systematic assessment of BIS for use in children (16).

The objective of the present study was to compare the results of the BIS-derived estimates of TBW, ECW, and ICW with results based on a model combining dual-energy X-ray absorptiometry (DXA) and total body potassium (TBK) measurements. The DXA and TBK measurements were selected as the reference methods because of their excellent precision (typically <1–2%) and relative ease of repeat measurements. We particularly wanted to determine whether BIS could be substituted for the assessment of TBW and its subcompartments in an individual. For BIS to be considered a clinical method of nutritional assessment in individual children, it first must be shown to be accurate for a healthy child in the general population.

	SUBJECTS AND METHODS

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Subjects
A group of 347 children (202 males and 145 females aged 4–18 y) participated in this study. Subjects were from 3 ethnic groups: white (Caucasian or European American), black (African American), and Hispanic (Mexican American). Body weight was measured with an electronic balance to ±0.2 kg; height was measured with a stadiometer to ±0.3 cm. The study was approved by the Institutional Review Board for Human Research at Baylor College of Medicine and written, informed consent was obtained for each subject.

Bioelectrical impedance spectroscopy
A commercial instrument (Xitron 4000B; Xitron Technologies, San Diego) was used to measure whole-body BIS. All measurements were performed in accordance with the manufacturer's instruction manual. For the measurement of a subject, one set of electrodes was attached at the subject's wrist and a second set was placed at the ankle. All measurements were performed on the left side of the body after the subject had been in a supine position for several minutes. All values for the ECW, ICW, and TBW compartments were obtained by using the instrument's software option for water volume analyses.

A detailed description of the electrical circuit model and the mixture theory model was published recently by De Lorenzo et al (15). Resistance values were calculated for the theoretical limits at zero and infinite frequency, from which the resistance values representing the intracellular (R_i) and extracellular (R_e) components were obtained. Repeat measurements over 2 d in 6 subjects indicated a precision of <2–3% for the R_i and R_e estimates for an individual. The equation used to calculate extracellular fluid volume (V_ECF) was as follows (15):

(1)

where Ht is height in cm, Wt is body weight in kg, and R_e is in . The k_ECF term was assumed to be constant (values supplied with the BIS instrument were 0.306 for males and 0.316 for females). The k_ECF term was defined as 10^-3 x (K_B² x _ECF²/D_b)^1/3, where the 3 additional parameters were the body geometry factor (K_B = 4.3), the resistivity of extracellular fluid (_ECF = 214 ^· cm for males and _ECF = 206 ^· cm for females), and total body density (D_b = 1.05 kg/L).

The following equation was reported for the calculation of intracellular fluid volume (V_ICF) (15):

(2)

where R_e and R_i are the extracellular and intracellular resistance values obtained for the Cole-Cole model. The k_P term is the ratio of the resistivity of the intracellular tissues (_ICF) to that of the extracellular tissues (_ECF). Equation 2 can be solved only by an iterative procedure for the value of V_ICF. The values for the k_P terms were 3.82 for males and 3.40 for females. For the BIS measurement, total body water (V_TBW) was defined as V_ECF + V_ICF.

Dual-energy X-ray absorptiometry
Body composition was measured with a Hologic QDR-2000 instrument (Hologic Inc, Waltham, MA). The whole body was scanned in the single beam mode and the data were analyzed with body-composition software version 5.56. The total body scan provided values for total-body bone mineral content, nonbone lean tissue, and total-body fat mass. The nonbone lean tissue and bone mineral content values were combined to give FFM. The precision of the FFM measurements by DXA was <1–2%. For the present studies, the hydration of the FFM was assumed to be constant, such that TBW = 0.732 x FFM(6, 17). This model was independently verified in a subset of children (n = 90) in which the mean ratio of TBW to FFM (TBW:FFM) was 0.74 ± 4% when TBW was obtained by D₂O dilution.

Total body potassium
Total body potassium was measured by using a low-background, multidetector whole-body counter as described previously (18). ⁴⁰K, a radioactive isotope, is an intrinsic trace fraction (0.012%) of body potassium that decays, emitting a gamma-ray that can be detected outside the body. For the weight range examined in this study, the precision for the TBK measurement was 1–2%. For healthy subjects, the intracellular potassium content can be assumed to be constant (150 mmol/L, or 150 mEq/L), such that the ICW volume can be defined as TBK/150 (19). For the same set of subjects used to verify TBW:FFM, the mean ratio of TBK to ICW was 150.5 mmol/L (150.5 mEq/L), for which ICW was defined as TBW - ECW, with ECW obtained by bromine dilution.

Statistical analysis
Data in the tables are reported as means ± SDs. The percentage CV was defined as 100 x (SD/). Analysis of variance (ANOVA) was used to examine effects due to sex and ethnicity, with age, weight, and height as covariates. The paired t test was used to test for differences between the BIS and DXA+TBK results for each sex and ethnic subgroup. Student's t test was used to identify statistical differences between sex groups and among ethnic groups within a sex. Least-squares linear regression analysis was used to test for correlations between the BIS and DXA+TBK methods for each water compartment; the values reported are the correlation coefficient (r), associated probability value (P), and the SEE. Bland-Altman plots (20) were used to assess the degree of interchangeability between the BIS and DXA+TBK methods. The limit of agreement between the 2 methods was defined as ±2 x SD of the mean difference between methods. For the calibration and validation groups, a random number between 0.0000 and 1.0000 was assigned to each subject. Those subjects with a number <0.6667 were placed in the calibration group; those with a number 0.6667 were placed in the validation group. For all statistical analyses, significance was defined as a probability 0.05.

	RESULTS

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Anthropometric characteristics of the study population grouped by sex and ethnicity and divided into 5-y age intervals are shown in Table 1. The results for TBW, ICW, and ECW based on the DXA+TBK model are provided in Table 2. There were significant differences between males and females for TBW (P < 0.004), ICW (P < 0.003), and ECW (P < 0.01); however, ANOVA indicated no significant differences within a sex group by ethnicity.

The results of the Bland-Altman analysis of the total population with use of the newly derived calibration constants are shown in Figure 1. It is evident that the individual difference values were independent of the average values for each water compartment. The results of the Bland-Altman test for the total population are also summarized in Table 4. For each water compartment and for each sex, the mean differences were not significantly different from zero. Compared with the results based on the initial BIS calibration, the main improvements were in the TBW and ICW compartments in the males, for which the SD values were reduced by 0.3 L and 0.7 L, respectively.

View larger version (37K): [in this window] [in a new window]   FIGURE 1. Relation between the difference (BIS value - DXA+TBK value) and the average ([BIS value + (DXA+TBK value)]/2) of the 2 methods for measuring body water in males (•) and females () aged 4–18 y, where BIS is bioelectrical impedance spectroscopy, DXA is dual-energy X-ray absorptiometry, and TBK is total body potassium. The ±2 SD lines define the 95% limits of agreement between methods [Bland-Altman test (20)]. TBW, total body water; ICW, intracellular water; ECW, extracellular water.

	DISCUSSION

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In the present study, the initial BIS estimates for TBW, ICW, and ECW volumes were highly correlated with the corresponding values based on the DXA and TBK measurements. We showed that when the original resistivity values (supplied with the BIS instrument) were used, the results for the BIS method were not interchangeable with those for the DXA+TBK model. To overcome this bias, we used the cross-validation approach to calculate new resistivity values for use with the BIS equations.

We chose the DXA+TBK model as our reference method, in place of the classic dilution techniques, because of the better precision achieved with these 2 methods and because of the relative ease with which the DXA and TBK measurements can be performed. We also chose these methods to eliminate any criticisms attributed to the dilution methods, such as the choice of tracer, which body fluid to assay, the amount of time needed for equilibration, and analytic accuracy (6, 22). For example, the error in the ICW estimate when based on dilution methods is substantially larger than that for the TBK method. For the measurement of TBW, the precision of the DXA and D₂O methods is comparable (23). For our DXA+TBK model, we needed to use 2 conversion factors: 0.732 L/kg to obtain TBW from FFM_DXA and 150 mmol/L (150 mEq/L) to obtain ICW from TBK. However, we did verify these ratios for a separate group of children of the same age range. Thus, there is no physiologic reason to expect that these ratios would be significantly different for healthy children (1, 2, 19).

The k_ECF term in Equation 1 and the k_P^· term in Equation 2 for the BIS estimates were assumed to be constants on the basis of the mixture theory model (15). Only Smye et al (16) reported calculating the value of k_ECF for children. When these investigators compared BIS results with the clearance of ^99mTc-labeled diethylenetriamine pentaacetate in 16 children, the mean value for k_ECF was calculated as 0.335, 3% higher than the mean for our population. We found that the percentage CVs of the newly calculated k_ECF and k_P terms were about ±8%, which is slightly higher than one would want if these values are to be considered true constants for body composition (10, 24). Note also that we found that the BIS values of k_P for individuals were not independent of the resistivity ratio (R₀:R), whereas Equation 2 would not imply this relation.

The k_ECF term in Equation 1 is assumed to be a constant for adults. For the age range examined in the present study, however, this assumption may not be applicable. The numeric value for k_ECF is based on 3 additional body parameters (K_B, D_b, and _ECF). Although any 1 of these 3 parameters could be adjusted separately so that the average bias (ECW difference) would become zero for our population, this adjustment would not appreciably reduce the range of the individual ECW difference values. To reduce the range of the ECW difference values for children, 2 or more of the 3 parameters in the k_ECF term need to be adjusted; hence, the k_ECF term is not truly a constant. We showed already that _ECF must be sex specific. Likewise, it can be expected that K_B may also need to be adjusted for variations in age and sex (25, 26). D_b also changes with age (27), but its effect on the k_ECF value is small (28). For the calculation of intracellular fluid volume, neither the D_b nor the K_B parameter is used. The only assumed constant in Equation 2 is the k_P term, which is defined as the ratio of _ICF to _ECF. Thus, if the _ECF value is adjusted to achieve a correct value for the k_ECF constant, this will also directly affect the calculation of intracellular fluid volume. To date, studies in adults have found that agreement between the BIS and dilution methods can be achieved only when the tissue resistivity values (_ICF and _ECF) are recalculated for each specific population (13, 15, 16, 29–31). Although the BIS instrument was easily recalibrated for the group, this did not necessarily ensure that the BIS estimates were accurate for individuals within the calibration population or for subsequent studies in different populations. In the present study, our cross-validation design showed that the newly derived constants for BIS were equally applicable in both the calibration and retest groups. Further validation studies, however, are still needed in other pediatric populations, especially those with diseases for which an altered body water distribution could be expected.

When we calculated the numeric values needed for the k_ECF and k_P terms for each individual, the percentage CV for the mean k_ECF and k_P values for the total population were 8%, which is just outside the limit usually considered for a constant within the context of body-composition analysis (10, 24). This limitation, however, can be reduced if the 2 BIS constants (k_ECF and k_P) are also adjusted for age. Then the results of the Bland-Altman analyses indicated that the BIS estimates were fairly accurate for individuals. As noted above, adjustments in the k_ECF and k_P terms may be required because of differences in relative body proportions, changes in the resistive properties of tissues, and changes in body density between pre- and postpubertal children. We did observe (data not shown), for example, that the scatter in the difference values for BIS versus DXA+TBK for children taller than 150 cm was considerably higher than that for the younger children. Note that although these effects are limits on the absolute accuracy of the BIS estimates in an individual, these limitations may not preclude the usefulness of the BIS measurement in monitoring relative changes in body water distribution during short-term, nonacute, longitudinal studies in children.

	ACKNOWLEDGMENTS

 
We acknowledge the contributions of JJ Posada and JA Pratt, who performed many of the BIS, DXA, and TBK measurements; J Matthie of Xitron, Inc, for discussions about the BIS theory and for use of the Xitron 4000B instrument; and L Loddeke for editorial assistance in the preparation of the manuscript.

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This Article Abstract Full Text (PDF) An erratum has been published Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ellis, K. J Articles by Wong, W. W Search for Related Content PubMed PubMed Citation Articles by Ellis, K. J Articles by Wong, W. W Agricola Articles by Ellis, K. J Articles by Wong, W. W