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Which method to use for a fast assessment of body fat percentage?

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Institute of Physics and Engineering in Medicine Physiol. Meas. 36 (2015) 1453–1468

Physiological Measurement doi:10.1088/0967-3334/36/7/1453

Which method to use for a fast assessment of body fat percentage? Katja Zdešar Kotnik, Tatjana Robič and Petra Golja Department of Biology, Biotechnical Faculty, University of Ljubljana, Vecna pot 111, SI-1000 Ljubljana, Slovenia E-mail: [email protected], [email protected] and [email protected] Received 28 January 2015, revised 25 March 2015 Accepted for publication 14 April 2015 Published 28 May 2015 Abstract

Body position affects body water distribution and in turn the accuracy of bioelectrical impedance analysis (BIA), which may consequently distort conclusions about an individual’s body composition. We compared body fat percentage (BFP) obtained with leg-to-leg-BIA (LL) and hand-to-leg-BIA (HL) with the reference values. The BFPs of 97 individuals were determined with an LL- (Tanita TBF 215GS, Japan) and HL- (Akern, STA/BIA, Italy) BIA-analyser and with reference skinfold thickness (SF) measurements. Each subject was measured upright with the LL-analyser, and upright and supine with the HL-analyser, both before and after 20 min of supine rest. The one-way ANOVA for repeated measures (HL-BIA), Student’s t-test (LL-BIA), intraclass correlation coefficients, and Bland–Altman’s plots were used for statistical analysis. BFPs determined with HL/LL BIA in upright/supine positions differ significantly. Compared to the SF method, HL-BIA mostly overestimates, while LL-BIA mostly underestimates BFP. Agreement between anthropometrically determined BFP and HL/LL-BIA determined BFP is better with HL for both sexes, and generally better in females than males. HL-BIA-determined estimates of BFP are more similar to reference values than LL-BIA. However, for both BIA methods, BIA-determined estimates of BFP are significantly affected by body position. Consequently, different BIA methods will classify approximately one fifth of subjects into the erroneous body-fat-content category, which calls for urgent standardization. Keywords: bioelectrical impedance analysis, anthropometry, skinfold thickness, agreement (Some figures may appear in colour only in the online journal) 0967-3334/15/071453+16$33.00  © 2015 Institute of Physics and Engineering in Medicine  Printed in the UK

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Introduction Excessive accumulation of body fat increases the risk of several chronic diseases (Kopelman 2000, Haslam and James 2005), consequently, accurate estimation of body fatness is of vital importance when assessing a person’s health and/or nutritional status. Bioelectrical impedance analysis (BIA) is an attractive field method for body fat percentage (BFP) assessment due to its simplicity, speed and low cost, and therefore has been widely used in epidemiological and clinical studies since the 1980s. Validation studies with more sophisticated laboratory techniques (densitometry, dual energy x-ray absorptiometry, and magnetic resonance imaging) revealed that the BIA method is acceptably accurate for body composition assessment, and thus a substitute for anthropometry (Lukaski et al 1986, Fuller and Ellia 1989, Houtkooper et al 1996, Wattanapenpaiboon et al 1998), as it does not require high degrees of technical skills and is not uncomfortable compared to the anthropometric skinfold thickness method (Gray et al 1990). The working principle of BIA is based on differences in the electrical properties of various human tissues, which respond distinguishably to a constant weak alternating electrical current that is injected into the human body, often at different frequencies (0 to 500 kHz). BIA analyzers then measure the electrical impedance of the tissues (Z; ohm (Ω)), which is a complex quantity composed of resistance (R; Ω) and reactance (Xc; Ω) (Kushner et al 1992, Baumgartner et al 1998), that varies with tissues structure and composition, the anatomy of the measured segments, as well as the frequency of the applied signal (Kyle et al 2004, Bera 2014). With adoption of several assumptions, BIA most directly assesses the amount of total body water (extra- and/or intracellular water), from which other compartments of the body (fat-free mass and fat mass) can be calculated. There are a few different designs of BIA measurements, which are based either on measurements with different frequencies (single-frequency BIA, multy-frequency BIA, and bioelectrical impedance spectroscopy), or on different segments of the body (whole-body BIA and segmental BIA, which provide separate measurements for legs, trunk, and arms) and are all well described elsewhere (Organ et al 1994, Kyle et al 2004, Bera 2014). As mentioned above, BIA has been demonstrated to estimate body fat accurately in controlled clinical conditions, but its performance in the field has been reported as inconsistent. Various individual and environmental factors have been shown to affect the accuracy of BIA (Kushner et al 1996, Dehghan and Merchant 2008), which may consequently provide rather incorrect information about an individual’s body composition. Individual factors include different medical conditions (Piccoli et al 1996), ethnicity (Stolarczyk et al 1997), degree of adiposity (Deurenberg 1996, Baumgartner et al 1998), period of menstrual cycle (Deurenberg et al 1988), hydration level (O’Brien et al 2002), recent physical activity (Deurenberg et al 1988), food and beverage intake (Deurenberg et al 1988) and skin temperature (Caton et al 1988, Gudivaka et al 1996), while environmental factors include environmental temperature, abduction of limbs (Gonzalez et al 2000), position of the electrodes (van Marken Lichtenbelt et al 1994), and position of the body during the measurement (Roos et al 1992, Shirreffs and Maughan 1994, Kushner et al 1996). Kyle et al (2004) concluded that BIA allows determination of fat-free mass and total body water in subjects without significant fluid and electrolyte abnormalities, when using a validated equation  that is appropriate with regard to sex, age, and race and established procedures. However, despite a large number of studies on BIA standardisation, BIA still suffers from a lack of a completely standardized method and quality control procedures (Kyle et al 2004). The position of the body during BIA measurement needs to be taken into account due to the inter-compartmental body fluid shifts it induces. Namely, when subjects assume a supine 1454

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position, which is a preferred position for BIA measurement, intravascular pressure in the lower extremities decreases. As a consequence of reduced capillary filtration pressure, fluid is shifted from the extravascular to the intravascular compartment (Maw et al 1995) and extracellular fluid is shifted from the lower (i.e. legs) to the upper (i.e. trunk and arms) parts of the body. Extracellular fluid redistribution to the upper part of the body and a reduced tissue hydration in the legs can thus cause an impedance increase in the legs and its decrease in the trunk. As the trunk contributes only 9% of the whole body impedance (Zhu et al 1998), the total measured body impedance will consequently increase, as well as the calculated values of BFP. In an upright position, this effect is reversed. It is thus expected that these changes in the redistribution of body water can rather significantly influence BIA measurements (Kushner et al 1996) Several studies on healthy normal-weight adults have demonstrated that the position of the body affects the impedance results obtained with a whole-body BIA (Roos et al 1992, Shirreffs and Maughan 1994, Kushner et al 1996) as well as with a segmental BIA method (Scharfetter et al 1997, Zhu et al 1998) at the single- (Roos et al 1992, Shirreffs and Maughan 1994) or multi-frequency (Kushner et al 1996, Scharfetter et al 1997, Zhu et al 1998) BIA techniques. Namely, the results of the studies with the whole-body BIA method have demonstrated a progressive increase in impedance (Z or R) up to 9% in 4 h with the most significant changes in Z over the first hour while supine, and a decrease of R back towards the initial values in 5 min after the subjects assumed an upright position. Similarly, studies with the segmental BIA method demonstrated that 30 min in the supine position caused a significant increase of the measured R and thus of the calculated extracellular volume, compared with the initial upright body position (Scharfetter et al 1997, Zhu et al 1998). It is worthwhile noting, however, that changes in calculated extracellular volume, as determined from the sum of measurements of all segments, were much smaller than the changes in calculated extracellular volume determined with whole-body BIA (Zhu et al 1998). In addition, segmental BIA measurements revealed that legs (45%) and arms (46%) contribute considerably more to overall extracellular impedance than the trunk (9%), which results from differences in the cross-sectional area of different segments (Organ et al 1994, Zhu et al 1998). Although supine rest for at least 10 min duration is a recommended standard protocol before any BIA measurement (Ellis et al 1999), recently more and more commercially available devices for both personal and clinical use are adjusted for measurements in a standing position. As body position and the consequent distribution of water between body compartments affect the accuracy of BIA, such devices may introduce a higher risk of incorrect information about an individual’s body composition. The present study therefore aimed to compare the values of body fat estimates obtained with an upright leg-to-leg (LL) BIA and a supine hand-to-leg (HL) BIA technique, with those obtained with a reference anthropometric method based on the measurement of skinfold thickness (SF). In addition, we aimed to evaluate the effects of body position on BIA-determined BFP for both types of BIA analysers. Subjects and methods Subjects

Healthy young adults aged 18 to 30 years were recruited for voluntary participation in the study. Data were collected during laboratory measurements performed in spring (March) and autumn (October, November) 2012. The protocol of the study was approved by the Slovenian Ethics Committee (no. 104/12/10), and was in accordance with the Declaration of Helsinki. All volunteers provided informed consent before participating in the study. 1455

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Figure 1.  The protocol of BIA measurements. LL: leg-to-leg BIA; HL: hand-to-leg BIA. LL1: upright, before 20 min of supine rest, LL2: upright, after 20 min of supine rest. HL1: upright, before 20 min of supine rest, HL2: supine, immediately after assuming a supine position, HL3: supine, after 20 min of supine rest, HL4: upright, immediately after 20 min of supine rest.

Measurements Bioimpedance analysis (BIA).  All BIA measurements were performed according to the standardized procedure recommended by NIH (NIH 1996). Thus, all subjects were measured in the morning, in the fasting state, after emptying the bladder, and without performing any hard exercise or drinking any alcohol for at least 24 h before the measurement. During all measurements, subjects were dressed in underwear only. All BIA measurements were performed with single frequency BIA devices and with a frequency of 50 kHz. A bipolar leg-to-leg (LL) device (Tanita TBF 215GS, Japan) that was adjusted for an upright position, and a tetrapolar hand-to-leg (HL) device (Akern, STA/BIA, Italy) that was adjusted for a supine position, were used. Bioelectrical impedance (Z; Ω), resistance (R; Ω) and reactance (Xc; Ω) were measured/calculated to the nearest 1 Ω. The measurement protocol is demonstrated in figure 1. Subjects’ body height and body mass, required for the subsequent BFP calculation, were first measured with a LL device (Tanita TBF 215GS, Japan). Body height (cm) was measured barefoot in an upright position from the heel to the top of the head in the Frankfurt horizontal position. Thus, the upper edge of the ear hole (auditory meatus) and the lower edge of the eye aperture (i.e. the edge of bone, approximately 1 cm below the lower lid) were positioned in a horizontal line. The measurement of body height was performed to the nearest 0.5 cm. Body mass (kg) was measured with subjects wearing underwear and barefoot to the nearest 0.1 kg. Also, the subjects were asked to empty their bladder before submitting to BIA measurements. BIA measurements with a LL device, with which BIA measurement can only be performed in an upright position, were performed in an upright position before (LL1) and after (LL2) 20 min of supine rest. Subjects were asked to stand barefoot on two foot-pad electrodes incorporated into the BIA scale. In such setting, each foot-pad electrode is divided in half, so that the anterior and posterior portions form two separate electrodes, which are in contact with the soles and heels of both feet. An electrical current is then applied via the anterior (sole) portion of the foot-pad electrode (i.e. injector electrode) and the voltage drop across the posterior (heel) electrode (i.e. detector electrode) is measured. The BFP was in turn calculated according to an integrated equation provided by the manufacturer. The equation variables included the measured impedance (i.e. the impedance, which included the legs, buttocks and a fraction of the trunk), the subject’s body height and body mass, age, sex, and the level of physical activity (normal or athletic). BIA measurements with a HL device were performed in upright (HL1, HL4) and supine (HL2, HL3) positions, both before (HL1 and HL2) and after (HL3 and HL4) 20 min of supine 1456

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rest. Before electrode placement, the skin was cleaned with alcohol to remove fatty substances and skin residues. Injector electrodes were attached on the dorsal surfaces between the second and third metacarpal of the wrist, and the second and third metatarsal of the ankle. Detector electrodes were attached dorsally on the wrist between the radius and ulna, and on the ankle frontally between the medial and lateral malleolus. Following the manufacturer’s instructions, all electrodes were placed on the right side of the body. The distance between detector and injector electrodes was at least 4 cm. For all four measurements with the HL BIA device, the same four electrodes were used for one subject. The electrodes were not removed from the skin between the consecutive measurements, so as to avoid any inconsistencies due to the altered position of electrodes. When in an upright position, the subjects had their arms and legs abducted 45° from the body axis; while supine, the subjects lay on a flat, non-conducting surface, with arms and legs also abducted 45° from the body axis. The measured values of resistance (R; Ω) and reactance (Xc; Ω) were entered into the Bodygram 1.3 software (Akern Bioresearch, Italy) that converted the measured values (the impedance, which included the arms, trunk and legs) into a BFP obtained by the HL device, while accounting for the age, sex, body mass, and body height of a subject (thus, similar parameters as with the LL device). To enable a direct comparison with the LL device measurements, the impedance values of the HL BIA device (Z; Ω) were also calculated from HL BIA R and Xc according to the following equation (Heyward and Wagner 2004): Z2 = R2 + Xc 2. Skinfold thickness (SF).  A sex-specific anthropometric equation  (Durnin and Womersly

1974) was used to determine body density from four skinfold thicknesses (triceps, biceps, subscapular and suprailiac). For each individual, the equation of Brožek et al (1963) was then used to determine BFP from body density; this value of BFP was adopted as the reference value for all BIA measurements. Skinfolds were measured as recommended by Lohman et al (1988). All four skinfolds were measured with a calibrated skinfold calliper (Harpenden skinfold calliper, Baty International, England, UK) to the nearest 0.2 mm. To ensure the regularity of the results, the measurements of skinfolds were performed in triplicate and the median of the measurements was taken as being representative. The measurements of tricep skinfolds were taken vertically over the tricep muscles halfway between the acromial process of the scapula (top of the shoulder) and the olecranon process of the ulna (elbow). Bicep skinfolds were measured vertically over the bicep muscles at the level of tricep skinfolds. The subscapular skinfold was measured diagonally 2 cm medially from the inferior angle of the right scapula. The suprailiac skinfold was measured immediately above the crest of the right ilium, at a slight angle to the vertical plane, thus, along the normal fold line. Statistical analysis

Subjects with more than 20 and 33% of body fat (as determined with skinfold thickness (SF) measurements) for young adult males and females, respectively (Gallagher et al 2000), as well as self-reported athletes were excluded from further statistical analysis, as the BIA equations for these population groups differ from those for a general population. The Student’s t-test was performed to compare age, body mass, body height and body mass index between females and males. The differences between BFP determined with HL BIA and the BFP determined with the reference anthropometric SF method were statistically evaluated with a 1457

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one-way analysis of variance (ANOVA) for repeated measures. The differences between the BFP determined with LL BIA and the BFP determined with the reference SF method were analyzed with the Student’s t-test for correlated samples. The Chi-square test was performed to assess whether subjects were classified into different body fat content categories (i.e. underweight, normal weight, or overweight; categories set according to Gallagher et al (2000)) when the BFP was determined with either different BIA methods or with the reference SF method. The level of statistical significance was set to α = 0.05. In addition, to compare the anthropometric and BIA methods, the statistical tests recommended by Marrodán Serrano et al (2012) were performed. An intraclass correlation coefficient (ICC) was calculated to assess the level of absolute agreement between BFP determined with BIA measurements and that resulting from anthropometric SF measurements. The ICC was calculated according to the following equation: 2 – (SD 2 /N )) ICC = (SD2A + SD2B – SD2AB)/(SD2A + SD2B – XAB AB

where SDA and SDB are standard deviations of methods A (anthropometry) and B (BIA), respectively, and SDAB is the difference between standard deviations of both methods. XAB stands for the mean of differences between both methods and N is the number of subjects. Values resulting in an ICC above 0.75 were considered as being in close agreement, those with an ICC between 0.40 and 0.75 as being in a fair-to-good agreement, and those with an ICC below 0.40 indicating an absence of agreement (Marrodán Serrano et al 2012). Additionally, the level of agreement between the two methods was graphically illustrated with Bland–Altman’s scatter plots, also called the plots of differences (Bland and Altman 1986). Computational statistical analysis was performed with MedCalc 12.7.1 (MedCalc Software, Ostend, Belgium). Results All results are presented as an average (standard deviation (SD)). All measurements were performed in a laboratory with an ambient temperature of 21.5 (0.7) °C. The measurements were performed on 104 subjects: 20 males and 84 females. As 7 subjects did not comply with the inclusion criteria for the analysis (five females with a BFP greater than 33%, as determined with skinfold thickness (SF) measurements, and two self-reported athletic subjects (one male, one female), they were excluded from the following analysis. The basic physical characteristics of subjects are presented in table 1. On average, males were taller (p  

Which method to use for a fast assessment of body fat percentage?

Body position affects body water distribution and in turn the accuracy of bioelectrical impedance analysis (BIA), which may consequently distort concl...
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