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Bioimpedance Basics and Phase Angle Fundamentals

This document provides a summary of the basic concepts and theoretical background of bioimpedance analysis (BIA) and phase angle measurement. It explains that BIA measures resistance and reactance, which are related to the conductive properties and cell membrane integrity of tissues. Common electrical circuit models are described which represent biological tissues as resistors and capacitors. Measurement of phase angle using bioimpedance spectroscopy may provide additional insights into cellular health compared to single frequency BIA. Understanding the biophysical models and properties of tissues is important for interpreting BIA measurements.

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0% found this document useful (0 votes)
76 views12 pages

Bioimpedance Basics and Phase Angle Fundamentals

This document provides a summary of the basic concepts and theoretical background of bioimpedance analysis (BIA) and phase angle measurement. It explains that BIA measures resistance and reactance, which are related to the conductive properties and cell membrane integrity of tissues. Common electrical circuit models are described which represent biological tissues as resistors and capacitors. Measurement of phase angle using bioimpedance spectroscopy may provide additional insights into cellular health compared to single frequency BIA. Understanding the biophysical models and properties of tissues is important for interpreting BIA measurements.

Uploaded by

people95
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
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Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391

https://doi.org/10.1007/s11154-022-09780-3

Bioimpedance basics and phase angle fundamentals


Leigh C. Ward1   · Steven Brantlov2

Accepted: 19 December 2022 / Published online: 7 February 2023


© The Author(s) 2023, corrected publication 2023

Abstract
Measurement of phase angle using bioimpedance analysis (BIA) has become popular as an index of so-called “cellular
health”. What precisely is meant by this term is not always clear but strong relationships have been found between cel-
lular water status (the relative amounts of extra- and intracellular water), cell membrane integrity and cellular mass.
Much of the current research is empirical observation and frequently pays little regard to the underlying biophysical
models that underpin the BIA technique or attempts to provide mechanistic explanations for the observations. This
brief review seeks to provide a basic understanding of the electrical models frequently used to describe the passive
electrical properties of tissues with particular focus on phase angle. In addition, it draws attention to some practical
concerns in the measurement of phase angle and notes the additional understanding that can be gained when phase
angle are obtained with bioimpedance spectroscopy (BIS) rather than single frequency BIA (SFBIA) along with the
potential for simulation modelling.

Keywords  Bioielectrical impedance · Bioimpedance · Phase angle · Theoretical background · Equivalent circuits ·
Modelling and simulation

1 Introduction ‑ Bioelectrical impedance where R = resistance (ohm), E = voltage (volts) and I = cur-
analysis of body composition rent (amps). For a simple electrically homogeneous conduc-
tive cylinder, R varies proportionally to cylinder length (L)
Bioelectrical impedance analysis (BIA) has become estab- and inversely to cross-sectional area (A)
lished over the past four decades as a popular technique for
L
the assessment of body composition [1]. The method was Volume ∝ (2)
A
originally developed to provide quantitative prediction of
total body water (TBW) [2, 3] and fat-free mass (FFM) or Combining and rearranging Eqs. (1) and (2) and introduc-
lean body mass (LBM) based on a two-compartment model ing a constant (ρ) for the proportionality in Eq. (2) yields
of the human body [4]. The underlying principle of BIA
is based on Ohm’s law that states that the potential differ- L2
Volume = 𝜌 (3)
ence or voltage across a conductor is directly related to the R
opposition (resistance) to current flow according to Eq. (1) where ρ is the resistivity or specific resistance of the conduc-
E tive material. Equation (3) is often invoked the basis for the
R= (1) BIA technique for the assessment of body composition; the
I
conductive volume of the body, i.e. body water, can be esti-
mated from measurement of the electrical resistance (R) of
the body (typically from wrist to ankle) and the conductive
* Leigh C. Ward length (L) usually represented as its proportional surrogate,
[email protected]
standing height or stature. Typically, Eq. (3) is solved by
1
School of Chemistry and Molecular Biosciences, The using an apparent resistivity (ρ) value derived, either directly
University of Queensland, St Lucia, Brisbane 4072, or indirectly by regression, in separate calibration studies in
Australia which volume is measured as TBW using a reference method
2
Department of Procurement and Clinical Engineering, such as deuterium dilution (­ D2O dilution)or as FFM using
Central Denmark Region, Aarhus, Denmark

13
Vol.:(0123456789)

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382 Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391

dual-energy X-ray absorptiometry [5]. Although, the human and dielectric permittivity both of which are frequency
body is not a simple homogenous cylinder with marked dependent. Consequently, measurement of these electrical
geometric variation in body shape undermining the found- parameters can be related to underlying tissue characteris-
ing assumptions of Eq. (3), the BIA technique is generally tics and properties. For a more detailed and comprehensive
considered to provide clinically acceptable predictions of discussion, the reader is referred to the texts by Rigaud et al.
body composition [6]. Nevertheless, there has been grow- [13] and Foster and Schwan [14].
ing recognition that absolute quantitative measurement of
body composition is not always of paramount importance
in clinical practice; what is often of needed are simply indi- 3 Electrical models of tissues
ces of change in body composition or physiology that relate
directly to cellular function and health status; thus change When an alternating electrical current passes through the
in resistance alone without empirical transformation to a body it will travel through both the extracellular and intra-
body composition measure such as FFM may by informa- cellular fluid compartments in a ratio determined by the
tive [7–9]. Resistance, however, is only one of the passive frequency of the current and the electrical characteristics
electrical characteristics of biological tissues.1 of the various tissues. The extracellular pathway is gener-
ally considered to be purely resistive whereas the need for
2 Electrical properties of biological tissues the current to pass across the cell membranes which act as
imperfect electrical capacitors provide a reactive compo-
The interaction of an electromagnetic wave or force with mat- nent. These electrical properties of biological tissues are
ter are described by complex conductivity and permittivity. frequently considered with reference to equivalent electrical
Conductivity is a measure of the amount of current that will circuit models. Many different equivalent circuits have been
flow across tissues due to an imposed electrical field; permit- proposed to describe biological tissues [see 15] although the
tivity is the amount of charge that will be induced at tissue simplest and most commonly used model is shown in Fig. 1.
interfaces (membranes) by the electric field. Resistivity is the This model represents the extracellular pathway of cur-
inverse of conductivity. These parameters can be considered rent by a single resistor (­ Re) in parallel with the resistance
as scalars that are a function of frequency and it is generally of intracellular fluid (­ Ri) and a capacitor (C) representing
assumed that the properties of interacting tissues are linear, the enclosing cell membranes. The impedance (Z) of this
isotropic and time independent. The early studies demon- equivalent circuit at a specific angular frequency (ω) (where
strated the dependence of tissue impedance on frequency and ω = 2πf) is given by
recognised that biological tissues have the capacity for, at the R0 − R∞
microscopic level, energy storage and dissipation. Through Z = R∞ + (4)
1 + (j𝜔𝜏)
the pioneering work of researchers including Maxwell [10]
and Debye [11] and Fricke [12] in the 1920s and 30s under- where ­R0 is resistance at zero frequency (also named ­Re),
standing of the electrical characteristics of tissues improved ­R∞ is resistance at infinite frequency and tau (τ) is the time
along with the appreciation that biological tissues exhibit constant for a capacitive circuit, i.e., a measure of the rate of
characteristics of a dielectric material. An applied electrical accumulation and dissipation of charge. In biological tissues
current to biological tissue influences those components that where C is not constant, τ is distributed around a mean value
carry a net electric charge and/or a dipolar electrical moment. [16] and Eq. (4) becomes
The most important charge carriers are the mobile ions in
R0 − R∞
tissue water while the key dipolar moments (the separation Z = R∞ + (5)
of positive and negative charges) are the charged protein and 1 + (j𝜔𝜏)(1−𝛼)
lipid molecules of cell membranes. The conductive charac-
where alpha (α) has a value between 0 and 1 [17]. If the
teristic (or conversely resistivity) of biological tissue is due to
real and imaginary parts of Eqs. (4) or (5) are separated, the
movement of charge while the polarization of dipoles results
resistive (R) and reactive components (Xc) of impedance (a
in a momentary delay known as a dielectric relaxation. Thus,
vector quantity) can be defined by
simplistically, opposition to current flow through biological
tissue is defined by electrical conductivity (i.e. resistivity) R0 − R∞
R = R∞ + (6)
1 + 𝜔2 𝜏 2
1
 The BIA method measures the passive electrical properties of
cells, tissues or the whole body as a response to an external electrical 𝜔𝜏(R0 − R∞ )
stimulus. In contrast, some biological tissues, e.g., nerve cells, exhibit Xc = − (7)
1 + 𝜔2 𝜏 2
active electrical properties in that they are capable of generating volt-
ages and currents. These are not measured in BIA.

13

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Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391 383

Fig. 1  Simple electrical equiva-


lent circuit for biological tissues

Equations (4) to (7) clearly show that the impedance char- current flows proportionately down both parallel branches.
acteristics of the equivalent circuit and, by extension that of This frequency dependence is primarily due to the capaci-
biological tissues, are frequency dependent. tive nature of cell membranes. A plot of reactance (Xc)
against resistance (R) describes a semi-circle (by conven-
tion the negative X axis from Eq. (7) is usually ignored
4 Frequency dependence of impedance and plotted as though positive) or eponymously as a
Cole–Cole plot (Fig. 2).
The relative magnitudes of alternating current flow As angular frequency (ω) increases and hence with
through the extra- and intracellular branches of the equiv- increasing frequency, the impedance vector traverses anti-
alent circuit of Fig. 1 are frequency dependent and are clockwise; the length of the vector represents the magnitude
defined by the boundary conditions that at zero frequency of the impedance, R and Xc the co-ordinates at the vector
the current must pass exclusively through the extracel- tip and phase is represented by the angle (ϕ) between the
lular resistance (­ Re = measured resistance or R ­ 0) since vector and the resistance (X) axis. For a pure electrical cir-
the impedance of the membrane capacitance will be infi- cuit characterized by Eq. (4), the centre of the semi-circular
nite while at infinite frequency the membranes are acting locus lies on the X axis, for biological tissues where there
as perfect conductors and the circuit resistance is given is a distribution of time constants, Eq. (5) pertains and the
by ­R ∞ = ­R iRe/(R i + ­Re). At any intermediate frequency, centre is depressed below the X axis as in Fig. 2.

Fig. 2  Graphical representation
of the frequency dependence
of resistance and reactance of a
simple circuit analogue of bio-
logical tissue with distributed
time constants

13

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384 Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391

angle is assumed to be that measured at a frequency of


50 kHz but this is not a formal definition; it is incumbent
upon researchers to make clear when referencing phase
angle the frequency of measurement. Secondly, the ratio of
current flowing down each branch of the parallel circuits
in Fig. 1 is independent of capacitance when ω = ωc and
is determined by the ratio of R­ e to ­Ri. While this implies
that this frequency may be more appropriate for prediction
of TBW by Eq. (3) than a fixed frequency of 50 kHz com-
monly used in single frequency BIA [18], it also suggests
that, since reactance is a measure of the dielectric property
of cell membranes [4], reactance at ωc is the most appro-
Fig. 3  Distribution of characteristics frequencies of a healthy control priate frequency for this purpose. It therefore follows, that
population. a Males, b Females if phase angle is to be used as an index of cell mass and
Data drawn from a database of impedance data held by the authors.
Whole-body impedance measurements obtained in lying with an membrane integrity it would equally be more appropriately
ImpediMed SFB7 bioimpedance spectroscopy analyser (ImpediMed measured at the characteristic frequency.
Ltd., Brisbane). Data analyses and plotted using Medcalc (v 20.115 In practice however this may not be necessary. Figure 3
MedCalc Software bvba, Ostend, Belgium) shows the frequency distribution of fc values for healthy
394 adults (195 males, 199 females) [19, 20 and unpub-
5 Phase angle and frequency dependence lished data]. A normal distribution was found with a mean
of impedance fc of 43.8 kHz (40.2 kHz, males; 47.5 females), very close
to 50 kHz the commonly used frequency for phase angle
It is clear from Fig. 2, that, as the impedance vector moves measurements [21]. There was, however, substantial vari-
around the semi-circle, phase angle will initial increase ation in characteristic frequency: an approximately two-
with frequency reach a maximum and then decline back to fold range for females and an approximately three-fold
zero. Maximum phase angle is the point of maximum reac- range for males. The reason for this variation is unclear.
tance and is defined as the characteristic frequency (ωc) Technical errors in determination appear unlikely since at
where ωc = 2πfc. Two important considerations follow from or around maximal Xc, frequency-dependent errors and
the foregoing analysis. Firstly, that in impedance analysis variability in current flow through intra- and extracellular
there is no single phase angle; a phase angle exists at all paths are minimized. Also a similar range in values has
frequencies of measurement. In common practice, phase been observed by others suggesting it represents primarily

Fig. 4  Change in phase angle


with frequency of applied cur-
rent
Data for a single male partici-
pant drawn from a database of
impedance data held by the
authors. Whole-body imped-
ance measurements obtained in
lying with an ImpediMed SFB7
bioimpedance spectroscopy
analyser (ImpediMed Ltd.,
Brisbane)

13

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Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391 385

Fig. 5  Phase difference in angu-


lar waveforms (phasor diagram)
due to AC current lagging
behind voltage

biological variation [22]. Since fc is dependent upon the 6 Measurement of phase angle, some
capacitive nature of cell membranes then variations in practical concerns
membrane composition and structure between individuals
may be influential. It is also possible variations in tissue BIA measurements are obtained using a phase-sensitive
anisotropy between individuals are important [23]. electronic instrument. There are a number of different elec-
Figure 4 shows the change in phase angle with frequency tronic designs that may be used [25] but generally they all
for a typical adult male. Figure 4 inset shows phase angle have some common features. The device applies a constant
over the complete measured frequency range with phase low-level alternating electric current to the body via elec-
angle increasing from zero to a maximum at fc and then trodes that span the whole body or a region, e.g., a limb.
declining asymptotically to zero at infinite frequency. Data A pair of proximally-placed electrodes measure the volt-
for measured frequencies from 3 to 300 kHz only are pre- age drop as the current flows through the conductive water
sented in the main plot. containing tissues. The attenuation of current flow by the
The characteristic frequency for this individual was capacitance of the reactive membranes elicits a delay or lag
at 42.9 kHz with a phase angle of 7.38°. Phase angle at in current flow (Fig. 5).
50 kHz was slightly smaller at 7.36°. Consequently little It is this time delay that is expressed as the phase angle.
improvement is likely to be seen by using phase angle at The precise electronic method by which impedance and
fc and avoids the need to use bioimpedance spectroscopy phase angle are calculated will depend upon the electronic
devices in order to determine fc. This observation concurs design of the impedance device and the quality (precision
with only minor improvements in prediction of TBW when of measurement) of the device componentry. Other than for
using resistance at fc rather than at 50 kHz [24]. It should safety, there are few regulations governing the respective
also be noted that the phase angle observed at 50 kHz is also performance of devices from different manufacturers and
seen at 39 kHz; only at fc is the value of phase angle unique. these may vary with regulatory authority and not all devices

13

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386 Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391

may perform similarly [26]. Consequently, the researcher supine posture using skin-adhesive Ag-AgCl gel electrodes
has little control over this other than to use devices that or for sitting and standing stainless steel contact plates or
are classed as medical devices or have been independently handles. Different measurement configurations will impact
validated. upon the measurements. The separation of the current drive
In addition, protocols for BIA measurement are not stand- and voltage-sense circuits is designed to mitigate the effects
ardized despite its importance being recognized [e.g., 27]. of the electrode-skin interface. However, it requires that
For example, whole-body (hand to foot) impedance measure- electrodes are as identical as practically possible. Nescolarde
ments may performed with the participant in lying, sitting or et al. found large variation in the electrical characteristics

Fig. 6  Box and violin plots of phase angles at 50  kHz in healthy spectroscopy device, b Device type. Measurements obtained with
males and females combined measured in either lying or standing. a either a bioimpedance spectroscopy device (BIS) or single frequency
Position of measurement. Measurements obtained with bioimpedance impedance device (SFBIA)

13

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Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391 387

of commercially available gel electrodes that significantly between devices. Since phase angle is not only dependent
impacted measurement of phase angle [28]. This observa- upon the cell membrane capacitance but also the relative
tion has been supported by others in which electrode type proportion of body water in the extra- and intracellular
significantly impacted both reactance and phase angle [29]. spaces, reflected in ­R0 and ­Ri (Fig. 1) then this is likely
The original BIA devices were lead and gel electrode to have an impact upon phase angle. The dataset for Fig. 3
devices and performed measurements with the participant provided the opportunity to investigate this. Participants
in lying, now stand-on devices are more common where the were measured using a lead and electrode device in both
participant is measured upright. Consequently the effects of lying and standing with the same device. Phase angle was
gravity and consequent fluid shifts around the body differ significantly lower (P < 0.001) when measured in standing

Fig. 7  Box and violin plots


of phase angles at 50 kHz in
healthy males and females com-
bined measured in either lying
by body region

13

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388 Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391

compared to lying position (Fig. 6a). In addition, data were the limbs or whole body [36]. This may be a reflection of
notably more variable measured in standing. Since the same the technical difficulties associated with truncal impedance
device was used, only posture changed, these differences measurements. Potentially, segmental phase angles may be
are not due to instrumental differences that may confound more informative of overall cellular health than the body
comparisons between specific lead and stand-on devices. It averaged value.
has also been suggested that phase angle when measured By definition, phase angle is an angular measurement
directly at 50 kHz using a single frequency BIA (SFBIA) with such that the range of phase angles describes a segment
device may differ from the value determined using a BIS of a circular distribution. Since biological phase angles typi-
device where phase angle may be determined from data fit- cally fall in a single narrow range they represent a unimodal
ting of the complete frequency spectrum [30]. Using the circular distribution, i.e., a single arc of a circle (Fig. 8a).
dataset above phase angle was measured in the participants It can be argued that such data should be analysed using
using both an SFBIA device and a BIS device. Both were circular statistical methods rather than the more commonly
lead-type devices and the measurements were made in lying. used frequentist approaches based on a normal distribution.
A small (2.9%) but significant difference (P < 0.001) was In contrast, circular statistics are based on the von Mises dis-
found (Fig. 6b). This may not however be the case where tribution and provides a circular analog of the linear stand-
measured data are very close to the fitted data (data analy- ard deviation [37]. Figure 8b shows the circular distributions
sis in BIS typically involves fitting the measured data to for phase angles in the male sample of the data presented
the semi-circular plot seen in Fig. 2) or where the device in Fig. 7.
provides both sets of values allowing actual measured data
to be used. Impedance measurements at 50 kHz have also
been reported to be affected by electrical interference from 7 Interpretation of phase angles
cardiorespiratory monitoring equipment used in a clinical
setting [31]. It is widely held that phase angle is reflectively of changes
The increasingly common stand-on impedance devices in cell membranes and/or the relative amounts of extra- and
are not only more convenient for the participant but also intracellular fluid. Consideration of the underlying theory
readily provide impedance measurements of the individual outlines above supports this. Studies using BIS also pro-
body segments not simply the whole body (hand to foot) vide empirical support. Figure 9 illustrates the relationship
measurements. This has provided the opportunity to measure between phase angle and cell membrane capacitance (Cm)
phase angle of the separate body regions [32–35] more eas- and the ratio of extra- to intracellular water represented by
ily than with SFBIA lead devices (Fig. 7) [36]. the ­Re ­(R0) and ­Ri ratio. Although variability is present, there
These more recent studies have shown that the phase are strong correlations for both relationships supporting the
angle of the trunk is consistently lower than that of the view that change in phase angle is acting as a surrogate
other body regions with whole-body phase angle being index of changes in these cellular characteristics. Unfor-
intermediate between that of the arm and leg unlike early tunately, determining phase angle with a single frequency
studies that found trunk phase angle was larger than that of impedance device only does not allow determination of the

Fig. 8  Distribution of character-
istics frequencies of a healthy
control population. a Circular
distribution of phase angle, b
Circular distribution of phase
angles for body regions plot-
ted for angular range 0 to 10
degrees
Data drawn from a database
of impedance data held by the
authors. Whole-body imped-
ance measurements obtained in
lying with an ImpediMed SFB7
bioimpedance spectroscopy
analyser (ImpediMed Ltd., Bris-
bane). Data analyses and plotted
using JASP (v 0.16.4)

13

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Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391 389

Fig. 9  Relationship of phase
angle at 50 kHz with cell
membrane capacitance and
extracellular resistance: intra-
cellular resistance ratio. a Cell
membrane capacitance, b ­R0:
­Ri ratio

relative contributions of either of these cellular parameters of the complex impedance and phase angle of anisotropic
to phase angle since neither Cm nor R ­ e:Ri can be calculated. tissues may prove fruitful [41].
The underlying theory of BIA is now well developed and
the impedance response of the body can be well modelled by
empirical functions such as those of Cole and other research- 8 Concluding remarks
ers [13, 15] although their applicability and accuracy as
representative biophysical models has been criticized [38]. Measurement of phase angle at 50 kHz has proved to be a
Their general acceptance is largely due to their mathemati- useful index of cellular and tissue health in many studies. It
cal simplicity and that for all practical purposes they allow is beyond the scope of this introductory review to discuss
interpretation of electrical phenomena in physiological terms the potential value and utility of phase angle measurement
although interrelation in terms of biophysical mechanism is in health and nutrition research; this is considered elsewhere
considered difficult [6]. Understanding can be advanced by in this special issue and recent reviews are available [e.g.,
the use of impedance simulation techniques. For example, 35] It is important to recognize that many of these findings
using the bioimpedance simulator, BioZSim [39], imped- are based on empirical observation of associative changes
ance profile of lymphedema, a condition characterized in phase angle with particular clinical or nutritional con-
by accumulation of extracellular fluid, is associated with ditions. Few are theoretically or mechanistically based. As
decreases in maximal reactance and increases membrane Foster and Lukaski observed in the early days of bioimped-
capacitance [40]. Although not determined in this study, ance studies, impedance measurements reflect global char-
these data suggest that phase angle would consequentially acteristics of the body; the connection between impedance
change and was replicable by simulation. Such simulations and body composition is indirect [6]. These comments were
have the potential to clarify the relationship between cell made in the context of using impedance measurements for
and tissue structures and impedance measurements, includ- the quantification of body composition but they are equally
ing phase angle. Of particular note is that current models applicable to consideration of the biological, physiological
for the analysis of impedance data including phase angle or clinical correlates of phase angle. What is now required is
take no account of the anisotropy of biological tissues. In to provide a mechanistic explanation for these relationships.
whole body or indeed segmental impedance analysis, the This can be facilitated by biomedical engineers, biophysi-
general assumption is that current flow is homogeneous and cists and biomedical researchers developing better models
is predominantly through muscle tissue where current flow that harness present day computational power that was not
is considered to be parallel to the alignment of muscle fibres. available to Foster and Lukaski [6].
This is unlikely, however, to be totally true and investigation

13

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390 Reviews in Endocrine and Metabolic Disorders (2023) 24:381–391

Declarations  11. Debye P. Polar molecules. New York: The Chemical Catalog
Company; 1929.
Conflict of interest  Author Ward consults to ImpediMed Ltd., manu- 12. Fricke H. XXXIII. The theory of electrolytic polarization.
facturer of impedance devices. ImpediMed Ltd. had no involvement in London, Edinburgh, Dublin Philos Mag J Sci. 1932;14:310–8.
the concept, design or execution of these study nor in the preparation Available from: http://​www.​t andf​online.​com/​doi/​abs/​10.​1080/​
of the manuscript. All other authors have no relevant conflicts of inter- 14786​44320​94620​64.
est to report. 13. Rigaud B, Morucci JP, Chauveau N. Bioelectrical impedance
techniques in medicine. Part I: Bioimpedance measurement.
Funding  Open Access funding enabled and organized by CAUL and Second section: impedance spectrometry. Crit Rev Biomed Eng.
its Member Institutions. 1996;24:257–351. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​
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Open Access  This article is licensed under a Creative Commons Attri- 14. Foster KR, Schwan HP. Dielectric properties of tissues and
bution 4.0 International License, which permits use, sharing, adapta- biological materials: a critical review. Crit Rev Biomed Eng.
tion, distribution and reproduction in any medium or format, as long 1989;17:25–104. Available from: http://​www.​ncbi.​nlm.​nih.​gov/​
as you give appropriate credit to the original author(s) and the source, pubmed/​26510​01.
provide a link to the Creative Commons licence, and indicate if changes 15. Grimnes S, Martinsen Ø. Bioimpedance and bioelectricity basics.
were made. The images or other third party material in this article are Elsevier; 2015 [cited 2016 Aug 10]. Available from: https://
included in the article's Creative Commons licence, unless indicated ​linki​nghub.​elsev​ier.​com/​retri​eve/​pii/​C2012​00695​17.
otherwise in a credit line to the material. If material is not included in 16. Pethig R, Kell DB. The passive electrical properties of biological
the article's Creative Commons licence and your intended use is not systems: Their significance in physiology, biophysics and biotech-
permitted by statutory regulation or exceeds the permitted use, you will nology. Phys Med Biol. 1987;32:933–70. Available from: https://​
need to obtain permission directly from the copyright holder. To view a iopsc​ience.​iop.​org/​artic​le/​10.​1088/​0031-​9155/​32/8/​001.
copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. 17. Cole KS, Cole RH. Dispersion and absorption in dielectrics I.
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