Professional Documents
Culture Documents
ROBERT L. MCINTOSH
by UNIVERSITY OF MISSOURI on 03/12/13. For personal use only.
VITAS ANDERSON
Australian Centre for Radiofrequency Bioeffects Research
and
Swinburne University of Technology
John St, Hawthorn, VIC, 3122, Australia
vitasanderson@swin.edu.au
Accurate numerical calculation of the thermal profile in humans requires reliable esti-
mates of the following five tissue properties: specific heat capacity (c), thermal conduc-
tivity (k), blood perfusion rates (m), metabolic heat production (A0 ), and density (ρ).
A sixth property, water content (w, as a %), can also be used to estimate c and k. To
date, researchers have used various and inconsistent estimates of these parameters, which
hinders comparison of the corresponding results. In an effort to standardize and improve
the accuracy of these parameters for future studies, we have documented over 150 key
papers and books and developed a database of the six thermal properties listed above
for 43 human tissues. For each tissue and each property the following were obtained:
the average value, the number of source values, the minimum and maximum of source
values, and the reference for each source value. A key premise for the development of
the database was to only use references that provided the original measurements. This
database is offered for use by the biological thermal modeling community to help improve
the accuracy and consistency of thermal modeling results.
1. Introduction
Pennes’ bioheat equation1 is often used by researchers when estimating the thermal
profile, T = T (x, t)(◦ C), in biological tissue:
∂T
ρc = ∇ · (k∇T ) + q + A0 − b(T − Tb ) (1)
∂t
129
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where c is the specific heat capacity (J/(kg · ◦ C)), k is the thermal conductivity
(W/(m · ◦ C)), ρ is the mass density of the tissue (kg/m3 ), q is the volumetric heat
(W/m3 ) from an external source such as ultrasound or radiofrequency heating, A0
is the metabolic heat production (W/m3 ), b is the heat-sink strength from each
tissue volume by blood perfusion (W/(m3 · ◦ C)), with these quantities specified
separately for each tissue, and Tb is the temperature of blood (◦ C). The more
common indicator for blood perfusion heat-sink strength found in the literature is
the blood perfusion rate, m, usually stated in ml/min/100 g. It is related to b, via
b = ρ · ρ blood · m · c blood · (10−5 /60), where the latter numerical term on the right
is present to convert the quantity to SI units.
For applications in bioelectromagnetics, Pennes’ equation can be used to deter-
Biophys. Rev. Lett. 2010.05:129-151. Downloaded from www.worldscientific.com
mine the induced tissue temperature rise from exposure to radiofrequency (RF)
electromagnetic fields. For this application, q = ρ · SAR, where the Specific energy
by UNIVERSITY OF MISSOURI on 03/12/13. For personal use only.
Absorption Rate (SAR) is the rate of energy transferred relative to the tissue mass
(W/kg).2 An example is presented in Bernardi et al.3
Many authors state values for tissue properties by quoting values from other
authors, who in turn quote other authors, and so on. When traced back some of
the original values are questionable in their derivation or measurement or were
approximated. In our review we sought to obtain direct sources of original mea-
surements. If numerous values were available for a given property for a tissue then
the spread of values was used to check data quality.
Other good sources for the comprehensive discussion and listing of the phys-
ical properties of tissues include Bowman,4 Duck,5 Erdmann and Gos,6 ICRP,7
Poppendiek,8 Werner and Buse,9 and Woodward and White.10
and k were estimated in the first instance from proxy formulae using water content
data. Use of references without clear measurement details were only employed in
cases where data was not available. For any remaining missing data values, a tis-
sue thermal datum was assigned from another tissue of a similar histology. Blood
perfusion values were used for deriving A0 . More thorough discussion on all of the
above and details of the surrogate data used is given throughout the paper.
The integrity of the values used was checked by ensuring that there was common
agreement between values for that tissue. Consistency between tissues of a similar
type was also considered. The values were selected under the constraint that they
were for humans or animals at rest and adult humans between 18 to 70 years
of age. The animal data was from baboons, dogs, goats, pigs and rabbits, and
Biophys. Rev. Lett. 2010.05:129-151. Downloaded from www.worldscientific.com
from the bovine family. Such animal data was generally avoided if multiple values
from humans were available. Preference was also given to animals with a similar
by UNIVERSITY OF MISSOURI on 03/12/13. For personal use only.
physiology to that of humans such as baboons and pigs. An aim with this database
was not to list all available animal data but to provide suitable values for human
tissues for modeling purposes. Data from small animals (e.g. rodents) were not
used. The remainder of this paper provides information on the sources of the data
for Table 1.
Table 2. (Continued )
(a) All measurements were made in-vitro except for the Lagendijk17 in-vivo study.
(b) Human tissue unless stated otherwise. Specific locations are given as necessary.
4. Thermal Conductivity, k
The sources of data for k are presented in Table 3.
The conventional method for measuring k, through applying a thermal gradient
across a given volume of tissue and measuring the steady-state temperature at
either end of the sample, was employed in Hatfield and Pugh,26 Hatfield,27 Craig
and Peyton,28 Clattenburg et al.,14 and Biyikli et al.15 Variants of this approach
were developed by Soyenkoff and Okun,29 Spells30 (for liquids), and Poppendiek
et al.8 (who considered the determination of k in non-homogeneous tissues, such as
for red-blood cells in blood).
The self-heated thermistor probe described above was used by Bowman et al.,31
Bowman,4 Valvano et al.,19 van Gemert et al.,20 Valvano and Chitsabesan21 and
Youn et al.25 The probe used by Cooper and Trezek18 is described in the previ-
ous section. A “hot-wire” probe with an attached thermocouple was developed by
Bhattacharya and Mahajan32 (the authors also provide a review of measurement
techniques). Similar technologies seem to have also been employed by Gautherie,33
who used a “fine-needle thermoelectric probe”, and El-Brawany et al.22
Bowman4 noted that for lung tissue, k changes significantly with age from a
value of 0.30 W/(m · ◦ C) for a young male to 0.55 W/(m · ◦ C) for an older, diseased
October 8, 2010 8:38 WSPC/S1793-0480 204-BRL S1793048010001184
lung. Poppendiek et al.8 suggests the low value for lung is partially due to the
presence of captured gases.
Many of the values were derived from information on the tissue’s water content
and this is discussed later in the paper.
Data were not available for some tissues with bile assigned the properties of
water, yellow bone marrow that of fat, and lymph nodes were set the average
properties for thyroid and adrenal glands. Whole teeth were assumed to comprise
70% dentine and 30% enamel (based on images in Williams et al.34 ).
Table 3. (Continued )
0.565 Ref. 18
0.490 Bovine Ref. 8
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0.512 Ref. 19
0.483 water % formula Ref. 35
Lung 0.478 Ref. 4
0.302 Ref. 31
0.280 Ref. 8
0.451 Ref. 19
Muscle — cardiac 0.562 Ref. 31
0.586 Ref. 18
0.497 water % formula Ref. 35
Muscle — skeletal 0.508 Ref. 4
0.459 Pigs Ref. 22
0.530 Bovine Ref. 8
0.481 water % formula Ref. 35
Pancreas 0.466 Ref. 4
0.588 Ref. 31
0.542 Ref. 19
0.472 water % formula Ref. 35
Skin 0.498 Ref. 4
0.376 Ref. 116c
0.413 water % formula Ref. 35
Spleen 0.515 Ref. 4
0.544 Ref. 31
0.544 Ref. 18
0.539 Ref. 19
0.514 water % formula Ref. 35
Stomach 0.527 Ref. 4
0.553 Ref. 31
0.514 water % formula Ref. 35
Testicles 0.515 water % formula Ref. 35
Tooth — dentine 0.575 Ref. 28
0.425 Ref. 29
Tooth — enamel 0.933 Ref. 28
0.650 Ref. 29
Urine 0.560 Ref. 8
Uterus 0.511 water % formula Ref. 35
(a) All measurements were made in-vitro except for the Lagendijk17 in-vivo study.
(b) Human tissue unless stated otherwise. Specific locations are given as necessary.
(c) Referenced in Chato.36
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5. Density, ρ
The sources of data for ρ are presented in Table 4.
Standard mass and volume (through water displacement) measurements were
employed by Erdmann and Gos,6 who examined 48 tissue types from ten human
cadavers, Clauser et al.,37 Cooper and Trezek,18 and Robinson and Elliot38 (which
feeds into the survey presented in Robinson39 ). Boyd et al.40 used a method of
cutting cut teeth into precise volumes and measuring their mass. The method of
flotation was employed in Manly et al.41 and Thewlis42 where the liquid is altered
until the density of the liquid matches that of the item under investigation. Liquids
with a density that varied with height (a “density gradient”) were used in Weidmann
et al.,43 Akerstrom et al.44 and Masugata et al.45 The measurement methods in the
Biophys. Rev. Lett. 2010.05:129-151. Downloaded from www.worldscientific.com
Density values for “lung”, are provided for the entire entity including the cap-
tured gases and not the specific lung tissue itself. Huang and Wu46 and Guenard
et al.47 estimated the lung density in-vivo through interpretation of computed
tomography (CT) scan data. The value of Erdmann and Gos6 is quite different
and as noted above was measured through water displacement.
Woodward and White10 provided the first author’s measurements combined
with a reassessment of ICRP (1975)7 tissue data. This is a comprehensive reference
that includes discussion on tissue composition and tissues that are of a similar
nature (which is useful if there is no data for a given tissue).
Scammon and Hesdorffer48 provide data from a survey of lens mass and volume
measurements, complemented by their own measurements, and use these values to
estimate the density (the value for a forty year old was used).
Data were not available for some tissues with dura (as per Pessoa de Barros
et al.49 ) and cornea assigned the properties of ligaments/tendons, cerebellum that
of grey matter, and pituitary glands and lymph nodes set the average properties
for thyroid and adrenal glands.
Table 4. (Continued )
947 Ref. 6
902 Ref. 46
900 Ref. 50
812 Ref. 8
Gall bladder 1115 Ref. 6
Glands — adrenal 1030 Ref. 10
Glands — thyroid 1050 Ref. 10
Intestine — large 1132 Ref. 6
Intestine — small 1030 Ref. 10
Kidneys 1050 Ref. 18
1147 Ref. 6
1019 Bovine Ref. 8
Ligaments/tendons 1174 Ref. 6
Liver 1050 Ref. 18
1158 Ref. 6
1057 Bovine Ref. 8
Lung 563 Ref. 6
288 Ref. 47
255 Ref. 46
604 Bovine Ref. 8
Muscle — cardiac 1060 Ref. 18
1143 Ref. 6
1059 Ref. 46
1082 Ref. 45
Muscle — skeletal 1178 Ref. 6
1087 Ref. 37
1066 Ref. 46
1080 Bovine Ref. 8
Nerve — spine 1112 Ref. 6
Pancreas 1128 Ref. 6
Skin 1102 Ref. 37
1125 Ref. 6
Spleen 1050 Ref. 18
1163 Ref. 6
Stomach 1126 Ref. 6
Testicles 1120 Ref. 6
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Table 4. (Continued )
(a) All measurements were made in-vitro except Guenard et al.47 and Huang
and Wu46 which were in-vivo.
by UNIVERSITY OF MISSOURI on 03/12/13. For personal use only.
(b) Human tissue unless stated otherwise. Specific locations are given as
necessary.
6. Blood Flow, m
The sources of data for m are presented in Table 5.
Tissue blood flow measurement is generally performed in-vivo, with the excep-
tion of the complex setup used in Linzell et al.51 for the study of perfusion in the
mammary gland of a goat. The two main techniques used for measuring blood flow
rates were the clearance method and microsphere trapping.
The clearance method involves injecting a soluble radioactive tracer into a body
and examining the level of radioactivity after a given time period. The isotope
133
Xe is suitable for local blood flow determination, including for muscles in human
subjects. This approach is described in Sekins et al.52 (where the authors estimate
that the method underestimates the true value by around 25%). Amery et al.53
also give muscle blood flow rates after exercise (around 60 ml/min/100 g). Cerebral
blood flow is measured using 133 Xe as a tracer in Madsen et al.54 with blood sampled
through a catheter. Non-invasive techniques are described in Meyer et al.55 and
Wilkinson et al.56 For adipose tissue, Nielsen and Larsen57 use 133 Xe in solution,
and Lesser and Deutsch58 use 85 Kr, inhaled in a gas.
To determine the blood flow rate in organs, animals are regularly used with
measurements of the radioactivity of the organ performed posthumously. An iso-
tope, such as 42 K or 86 Rb, is used and is injected into the heart. The method is
based upon the assumption that the fraction of the injected radioactive indicator
contained in an organ 30–60 s after the injection is equal to the fraction of the
cardiac output perfusing that organ. 42 K clearance is described in Sapirstein59 and
employed in Delaney and Grim.60
In the microsphere trapping method, small radioactive microspheres may be
injected into the left ventricle of the heart and then after a given time the
October 8, 2010 8:38 WSPC/S1793-0480 204-BRL S1793048010001184
atmospheric pressure and measured the nitrogen saturation levels in bone marrow
after given time intervals. Soto et al.66 used the non-invasive Positron Emission
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Tomography (PET) for assessment of myocardial blood flow using the marker 15 O.
Lassen et al.67 used both the 133 Xe clearance method and venous occlusion plethys-
mography on the human calf muscle. Lassen68 also presents an overview on mea-
surement techniques.
Rayner et al.69 quotes and utilizes the Fick principle which states that the
rate of uptake of a test substance is equal to the rate of inflow of that sub-
stance via the arteries minus the rate of outflow via the veins (that is, sources
and sinks are accounted for in a localized area). In Rayner et al.69 the substance
used is deuterium oxide (D2 O), whilst Kety and Schmidt,70 Scheinberg et al.71
and Rowe et al.72 used nitrous oxide (N2 O). Stow and Schieve73 used the Fick
principle and determine blood flow in the skin through measurement of the skin
temperature.
The blood flow was assumed to be non-existent for bile, cortical bone, and
all tissues of the eyes and teeth. Data was not available for some tissues with
bladder,8 gall bladder,8 blood vessels and uterus assigned the properties of muscle.
Best and Taylor74 and Williams and Leggett75 do not directly discuss measurement
techniques and data was only used where no other data is available.
For discussion on skeletal muscle blood flow and metabolism during exercise,
see Grimby76 (where the authors recorded a peak blood flow of 69 ml/min/100 g)
and Rowell.77,78 Scheinberg et al.71 considers cerebral blood flow (which increased
around 25% during exercise to 61 ml/min/100 g) and metabolism.
Table 5. (Continued )
Table 5. (Continued )
(a) All measurements were made in-vitro. In Linzell et al.,51 the mammary gland was sep-
arated from the body.
(b) Value for supine position adjusted to estimate for standing position using information
provided that such a change causes a 21% decrease.
(c) Referenced by Shinaberger and Bruner.87
(d) Average value over the range from 0.1 for isthmus to 7.l ml/min/100 g for superficialis,
in the canine flexor tendons.
(e) Average of the left (around 145 ml/min/100 g), right (90 ml/min/100 g), and cardiac
(130 ml/min/100 g) ventricles.
7. Water Content, w
The sources of data for w are presented in Table 6.
The determination of water content was made through the comparison of the
dry weight and wet weight throughout all references when stated. The measurement
method was not clearly stated in Forbes et al.,99,100 Mitchell et al.,101 Neufeld,102
Poppendiek et al.,8 and Thornton et al.103 From Ohkuda et al.104 we use the data
provided where blood is still present. Woodward and White10 is discussed above.
The books by Best and Taylor74 and Moses and Hart105 do not directly discuss
measurement techniques and data were only used where no other data are available.
This is similarly the case for Cate106 who gives a value of 4% for combined water
content and protein of teeth enamel, which we have halved.
Data were not available for some tissues with bladder assigned the properties of
muscle,10 and dura that of ligament/tendons.49
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Table 6. (Continued )
Duck5 discusses how many authors have recognized a close linear relationship
between the thermal conductivity and the water content. These authors include
Spells,30 Cooper and Trezek,35 and Poppendiek et al.8 The formula presented in
Cooper and Trezek35 is k = 0.0502 + 0.00577 · w (W/(m · ◦ C)) and is used in
the database for tissues with a water content higher than that of fat. That such a
relationship applies to fat (with relatively low water content) is discussed in Spells.30
This was not found to be the case here where the estimated value of k for fat (0.165
(W/(m · ◦ C))) was 20% lower than the average value presented in Table 1.
A similar discussion is presented on specific heat capacity by Duck5 (who quotes
Cooper and Trezek35 and Riedel110,111 ). The formula presented is c = 1670+25.1·w
and is used here for tissues with a water content higher than that of fat.
Biophys. Rev. Lett. 2010.05:129-151. Downloaded from www.worldscientific.com
These estimated values were also included in Table 1 for some tissues due to
the scarcity of data (see Tables 2 and 3). The values were found to be of good
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consistency with measured values when available. The formulas were not used for
bile, blood, urine, lymph nodes, the lens and vitreous humor of the eye, and the
lung, due to the low water content or different physiological structure of the tissue
compared to the main tissue types.
a blood flow of 34.5 ml/min/100 g and a water content between 75 to 85%. Hales84
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measured the blood flow in nasal mucosa (27 ml/min/100 g) in sheep. Delaney
and Grim60 discuss how the blood flow values for the stomach (54 ml/min/100 g)
are distributed between antrum (30 ml/min/100 g) and corpus (61 ml/min/100 g),
and the corpus is distributed between mucosa (91 ml/min/100 g), submucosa
(42 ml/min/100 g), and muscularis (26 ml/min/100 g).
The blood flow in the prostate gland was measured by Andersson et al.115 using
dogs and indicated it is in the range 31 to 79 ml/min/100 g.
11. Conclusions
A comprehensive database has been developed for the thermal properties (c, k,
m, A0 and ρ), of biological tissues represented in the numerical modeling of heat
transfer in the human body, as well as water content. This resource is offered to the
biological thermal modeling community to help improve the accuracy and consis-
tency of published results. A key objective of the development process has been to
only source original measured values to ensure high integrity of the database. An
estimate for the range of a tissue’s property has been obtained in many cases.
The listing of data in Table 1 and the discussion throughout the paper highlight
the numerous tissues where data are scarce and where further measurements of their
thermal properties would be useful. In order to provide a comprehensive property
dataset for all tissues, we have nominated values for the data gaps using proxy
calculations based on tissue water content or by assigning values based on tissues
with similar histologies.
Acknowledgments
We would very much like to thank Joanne Cohen, our Information Officer, for
sourcing many of the papers, and performing extensive literature searches for us.
The grant sponsor was The Mobile Manufacturers Forum and the GSM Associ-
ation under Work Package 4 of the RF Dosimetry Program. The views expressed in
the paper are those of the authors and may not represent the views of the sponsors.
October 8, 2010 8:38 WSPC/S1793-0480 204-BRL S1793048010001184
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