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Dielectric properties of tissues; variation with age and their relevance in exposure of children to electromagnetic fields; state of knowledge
Progress in Biophysics and Molecular Biology 107 (2011) 434e438
Contents lists available at SciVerse ScienceDirect
Progress in Biophysics and Molecular Biology journal homepage: www.elsevier.com/locate/pbiomolbio
Review
Dielectric properties of tissues; variation with age and their relevance in exposure of children to electromagnetic fields; state of knowledge Azadeh Peyman* Health Protection Agency, Chilton, Didcot, Oxon OX11 0RQ, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 3 September 2011
This paper reviews and summarises the state of knowledge on dielectric properties of tissues; in particular those obtained as a function of age. It also examines the impact of variation in dielectric data on the outcome of recent dosimetric studies assessing the exposure of children to electromagnetic fields. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: Dielectric properties Biological tissues Dosimetry Children
Contents 1. 2.
3. 4. 5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 434 Dielectric properties of tissues, state of knowledge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435 2.1. 1996 database . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435 2.2. MTHR study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435 2.3. Updates on low frequency measurements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436 Variation of dielectric properties with age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436 Impact of variation in dielectric properties on SAR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .437 Summary and concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438
1. Introduction One of the main inputs required in the dosimetry studies assessing the exposure of people to electromagnetic fields (EMF) are dielectric properties of different body tissues which determine the interaction of the fields with the human body. Accurate knowledge of the dielectric properties of tissues is required in order to calculate the energy deposition when they are exposed to EMF. Dielectric properties of tissues are frequency dependent and exhibit systematic changes due to the physiological state of the tissue; for instance the intactness of cellular membrane and the water content of the tissue. The dielectric spectra of tissues consist of three main dispersions predicted by known interaction mechanisms (Fig. 1). The a-dispersion is characterised by the very large
* Tel.: þ44 1235 822679; fax: þ44 1235 822630. E-mail address: [email protected]. 0079-6107/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.pbiomolbio.2011.08.007
permittivity values that are produced by ionic diffusion processes at the site of the cellular membrane at very low frequencies (below a few kHz). At intermediate frequencies (kHz region), the b dispersion occurs due to the polarisation of the cellular membrane. Finally, the g dispersion at microwave frequencies is mainly due to the polarisation of water molecules inside the tissue. The dielectric spectrum of biological tissues can be mathematically modelled by one or more terms of the well-known ColeeCole expression (Cole and Cole, 1941):
^3 ðuÞ ¼
3N
þ
3s
3N
1 þ ðjusÞð1aÞ
þ
si
ju3 0
(1)
Where ^3 is the complex relative permittivity, u the angular frequency and the ColeeCole parameters have their usual significance. Modelling the dielectric properties of tissues using Equation (1) facilitates their incorporation in numerical simulations of human exposure to electromagnetic fields.
A. Peyman / Progress in Biophysics and Molecular Biology 107 (2011) 434e438
Fig. 1. Dielectric spectrum of ovine liver (Gabriel et al. 1996b).
At radiofrequencies, the metric used for assessing people’s exposure is the Specific Energy Absorption Rate (SAR) expressed in watts per kilogram (W kg1). SAR is a function of the electric field induced in the body at any one point and the conductivity of the body tissue at that point:
SAR ¼ s
jE2 j
r
(2)
where s is the conductivity of the tissue in S m1, r is mass density of the tissue in kg m3 and E the root mean square (rms) electric field strength (V m1). Dielectric properties of tissues and their variation with frequency is well studied, reported and reviewed (Schwan and Foster, 1980; Pethig, 1984; Pethig and Kell, 1987; Gabriel et al., 1996a,b,c). While, the earlier studies focused on the interaction mechanisms, later ones aimed to provide a reliable and accurate database of dielectric properties of different body tissues across the frequency spectrum. These data are a necessary input in the electromagnetic dosimetry studies where the exposure of people to external fields are assessed. Until recently, the literature data consisted mostly of dielectric properties of tissues from mature animals (Gabriel et al., 1996 aec), usually used to simulate adult models of the human head/body. Two earlier studies had reported on systematic changes in the dielectric properties of ageing brain tissues (Thurai et al., 1984, 1985). In the last few years, and due to substantial concern about the possible differences between the exposure of children and adults to electromagnetic fields, the focus of many studies has been shifted towards the development of childrens’ head/body models. To provide relevant dielectric data for children’s models, several studies have been carried out on dielectric properties of animal tissues from a range of ages (Peyman et al., 2001, 2007; Schmid and Überbacher, 2005; Peyman and Gabriel, 2010). These studies have triggered discussions on the extent to which the variation of dielectric data as a function of age would affect the results of dosimetry studies, and consequently the possible implications for the exposure of children. This paper summerises the current knowledge of dielectric properties of tissues over a wide frequency range and their variation as a function of age. It also reports the effect of these changes on dosimteric studies at radiofrequencies. 2. Dielectric properties of tissues, state of knowledge 2.1. 1996 database In 1996, Gabriel et al. carried out a systematic review of almost half a century’s literature available at the time in terms of the
435
dielectric properties of tissues over ten frequency decades. They then carried out an extensive experimental study on a large number of biological tissues at body temperature using three different measurement techniques spanning the frequency range of 10 Hze20 GHz (Gabriel et al., 1996b). Their experimental results showed good agreement between data obtained from three experimental setups in the overlapping frequency ranges. The data were also largely in good agreement with the corresponding values in the literature. Finally, Gabriel et al. (1996c) used their experimental data, complemented by the data surveyed from the literature, to develop a parametric model (consisting of four ColeeCole terms plus one ionic conductivity term) to describe the variation of dielectric properties of tissues as a function of frequency. The ColeeCole model parameters later became available on the internet (Gabriel and Gabriel, 1997) and have been used extensively since to reconstruct the dielectric spectrum of each tissue in dosimetry studies. 2.2. MTHR study Although the 1996 database has been used extensively in dosimetric studies, there were still some gaps and limitation associated with it. In particular, since most measurements were carried out on excised tissues, critics argued that data pertaining to live tissue would be more relevant in bioelectromagetic studies. In addition, low frequency dielectric data are associated with larger uncertainties due to practical difficulties such as electrode polarisation and only few values are available for them in the literature. Therefore, the authors of the 1996 database have cautioned the use of the ColeeCole model for lower frequency parts of the spectrum as the best estimate based on the literature data before 1996, until more reliable and accurate data becomes available. Also, a better understanding of the uncertainty associated with dielectric measurements was needed. To fill the above gaps and update the state of knowledge on the subject, a systematic study was carried out as part of the UK’s Mobile Telecommunication Health Research (MTHR) program. The main objective of the study was to review the literature data post 1996 and obtain and analyse extensive and novel experimental data acquired from measurements on “live” animals at microwave frequencies. The study was also aimed to identify different random and systematic sources of errors associated with the dielectric measurements and develop a procedure to assess the total combined uncertainty for the dielectric data. Dielectric data (permittivity 3 0 and conductivity s) were collected from live porcine tissues, which are thought to be a good animal substitute to human tissue and would make a good basis for comparison with the data from the 1996 database that were mostly derived from measurements on excised ovine tissue (Peyman et al., 2005, 2007). For most of the tissues (brain and abdominal tissues) the new data were in good agreement with the 1996 database. However, in the case of skeletal tissues, the large numbers of independent dielectric measurements on both skull and long bone of different pigs show generally higher values than those reported in the Gabriel et al. (1996c) database (Fig. 2). These high values could possibly be due to the differences in the species and the age of the animals used in MTHR study and other studies. As it is apparent from Fig. 2, there is a big difference between data collected from young pigs (50 kg) and those of the older pigs (250 kg mature sows). The 1996 database values are closer to data gathered from older animals. Another important outcome of the MTHR study was that it did not report any systematic difference between dielectric data collected under in-vivo and in-vitro conditions at microwave frequencies
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A. Peyman / Progress in Biophysics and Molecular Biology 107 (2011) 434e438
using an in house developed probe comprising a rectilinear array of four platinum-blacked platinum pin electrodes embedded in PTFE. The authors claimed that this probe produced a coherent set of capacitance and conductance values, down to 1 Hz, when used to measure water and low concentration salt solutions (Gabriel et al., 2009). The effect of electrode polarisation at low frequencies, and some other high-frequency effects were identified as measurement artefacts. Although the authors found ways to subtract electrode polarisation from the lower side of the measured spectrum, highfrequency effects are yet to be fully identified and resolved. 3. Variation of dielectric properties with age
Fig. 2. Reported a: permittivity and b: conductivity of skull tissues.
(Peyman et al., 2005, 2007). This is due to the fact that at microwave frequencies, and the site of g dispersion region, dielectric properties of tissues are associated with the water content of the tissues and if care is taken to avoid drying of excised tissue samples, no systematic difference is anticipated. The situation is different at lower frequencies, in the range of the a and b dispersions in view of the sensitivity of their causal mechanism to the physiological state of the tissue (Kraszewski et al., 1982; Kuang and Nelson, 1998). Finally, systematic statistical and comparative analysis of a large amount of experimental dielectric data showed that for most tissue types the random uncertainty is by far the largest element in the uncertainty budget. This is due to the natural inhomogeneity inherited in biological samples. To determine the uncertainty in the measurement of biological tissue, random variations are obtained from repeat measurements and the instrumental and methodological uncertainties are calculated from measurements on standard liquids with well-known dielectric properties (Gabriel and Peyman, 2006). 2.3. Updates on low frequency measurements Low frequency dielectric data for body tissues are difficult to obtain due to the strong dependency of the dielectric properties on the physiological state of the tissues and changes occurring after death. There are also several practical difficulties in particular electrode polarisation which manifests itself in the low frequency part of the spectrum (<100 Hz). In a recent publication, Gabriel et al. (2009) reported a twopronged approach, review and measurement, to characterise the conductivity of tissues at frequencies below 1 MHz. In their review they covered data published in the last decade (post 1996) for a critical analysis to highlight their usefulness and limitations. They also carried out in-vivo measurements on pig myocardial muscle, liver, skull, fat, lung and in-vitro measurements on pig body fluids
The 1996 database only contains dielectric data obtained from mature animals. A few older studies reported systematic changes in the dielectric properties of ageing brain tissues (Thurai et al., 1984, 1985). Following the publication of the report of the Independent Expert Group on Mobile Phones (IEGMP, 2000), that highlighted the need for rigorous assessment of the exposure of children, a study was carried out by Peyman et al. (2001) on dielectric properties of rodent tissues from new born to fully grown rats at microwave frequencies. This was later extended to intermediate frequencies down to 300 kHz (Peyman and Gabriel, 2003a,b, Gabriel, 2005). The results of these studies showed that some head tissue (brain, skin and skull) exhibit significant variation, mainly decreasing in the measured permittivity and conductivity, as the animal gets older. The authors reported that the corresponding changes for the abdominal tissues are less prominent. To re-examine the above findings and to report data for more tissues, Peyman et al. (2005) carried out dielectric measurements on porcine tissues from 10, 50 and 250 kg pigs to cover developmental stages from piglets to mature animals. Porcine tissues are regarded as a good substitute for human tissues with respect to dielectric properties. To relate their findings to human tissue, Peyman et al. (2005) assumed that dielectric properties of tissues from 10 kg piglets correspond to those of human children of age 1e4 years, the 50 kg pigs to be equivalent to 11e13 years old human and the 250 kg, pigs to be considered equivalent to human adults. Further studies were also carried out on bovine excised tissues as a function of animal age (Schmid and Überbacher, 2005). The results of these studies also generally showed a significant decline in both permittivity and conductivity as a function of age for some tissues such as brain (white matter), long bone, skull, skin, muscle and bone marrow. No variation was observed in the dielectric properties of abdominal tissues. At microwave frequencies, the observed variations in dielectric properties are mainly due to the reduction in water content of tissues as an animal ages. The molecular orientation of tissue water is described in the g dispersion and conditions giving rise to a change in the water content of tissue are reflected in the parameters of this dispersion. At intermediate frequencies (300 kHze300 MHz), the measured dielectric spectrum reflects the site of the b dispersion. Changes in cellular structure and physiological state of the cell membrane are signalled by changes in this dispersion region. In the case of the brain, increased myelination and decreased water content as a function of age is said to be the reason for the drop in permittivity and conductivity values of white matter (No variation was observed in the dielectric data of grey matter) and spinal cord as animals age (Schmid and Überbacher, 2005 and Peyman et al., 2007). Bony tissues have higher variations in the amount of water due to changes in the degree of mineralisation of the calcified bone matrix during growth, resulting in a more “significant” decline in dielectric properties. The largest variation in the dielectric properties as a function of age is observed in bone
A. Peyman / Progress in Biophysics and Molecular Biology 107 (2011) 434e438
marrow tissues (Fig. 3) due to the transformation of high water content red marrow to high fat content yellow marrow as the animal grows (Peyman et al., 2009). The above studies have reported dielectric properties of ageing tissues at selected frequencies. To facilitate the use of experimental data obtained in dosimetry studies, Peyman and Gabriel 2010 provided the ColeeCole parameters for 14 tissue types at three developmental stages using the dielectric spectra of ageing porcine tissues. The 14 tissues identified are those that exhibited a significant decline in dielectric properties as a function of age (Peyman et al., 2005, 2007 and 2009). It is expected that the ColeeCole parameters reported by Gabriel et al. (1996c) continue to be used for the dielectric properties of tissues that did not exhibit age related changes. As the focus of dosimetric studies shifts from children to pregnant women and their foetuses, so does the need for dielectric properties of pregnancy associated tissues. So far, in the absence of such data, substitutes are used to simulate the exposure of pregnant women and their foetus to electromagnetic fields. For example, dielectric properties of muscle and blood are used for placenta and that of cerebrospinal fluid for amniotic fluid. To fill this gap, Peyman et al. (2011) and Peyman (2011) conducted an experimental study to provide dielectric data for human placenta, umbilical cord and amniotic fluid as well as several rat foetuses at different stages of gestation. Their results showed that the dielectric properties of amniotic fluid are significantly different from those of cerebrospinal fluid. They also mapped strong temperature dependency in the dielectric properties of amniotic fluid. Another outcome of this study was that umbilical cord has dielectric properties much higher than that of placenta due to the presence of high water content Wharton’s jelly. The results also showed that the
Fig. 3. Reported a: permittivity and b: conductivity of porcine bone marrow at three different growth stage (Peyman et al., 2005, 2009). Error bars represent 95% confidence intervals.
437
dielectric properties of foetus are generally higher than that of adult muscle and other abdominal tissues. In addition, dielectric properties of the foetus generally decreases as a function of gestation, however the magnitude of decrease in the dielectric data is not very large, and only reflects the fact that the total water content of the foetus as a whole decreases as it gets older. 4. Impact of variation in dielectric properties on SAR To the best of the author’s knowledge, only three studies have used the mentioned experimental dielectric properties of tissues as a function of age to calculate SAR values in models of children’s head/body as a result of exposure to electromagnetic fields. Few other studies have also examined the effect of changes in dielectric properties as a function of age on the calculated SAR by using adult dielectric properties and adjusting them for younger tissues assuming higher water content (Keshvari et al., 2006; Wang et al., 2006; Dimbylow et al., 2010). Each of the following studies have used a different metric in their SAR calculation such as localised SAR values for individual tissues, SAR10 g (SAR averaged over 10 g of tissue) or whole body SAR, therefore a direct comparison can not be drawn. Alfadh et al. (2003) and Gabriel (2005) used age related dielectric properties of rat tissues in a numerical study of exposure of rat models to plane waves at 27, 160, 400, 900, and 2000 MHz. 34 tissue-types have been identified in three rat models (10, 30 and 70 days old), from which only 9 tissues exhibited variation in their dielectric properties as a function of age. The results showed that, although changing the tissue dielectric properties would affect the localised SAR, no clear pattern could be established. The effect on whole body SAR was reported to be small, its extent depending on the variation in properties and the abundance of the tissues in the exposed model. These results can be explained as due to the fact that changes in dielectric properties would affect the coupling with the body and the interaction of tissues with the electromagnetic fields. It is also important to isolate the effect of changing tissue properties from all other factors that would affect the exposure, such as the size of the animal and polarisation and direction of the incident field (Gabriel, 2005). The second study examined the sensitivity of calculated SAR values to variation in dielectric properties when models of children and adults are exposed to EMF from walkie-talkie devices operating at 446 MHz (Peyman et al., 2009). Head models representing adults and 3- and 7-year old children were considered with tissue dielectric properties taken from 10 kg pig (1e4 year old), 50 kg pig (11e13 years old) and 250 kg pigs (adults). The results showed that variations on SAR10gr are less than 10% for the investigated configuration and that the variations of the tissue properties are not really reflected in a variation of SAR10 g. This could be due to the fact that averaging of the SAR dilutes the effect of the change in the SAR10 g. In addition, it is obvious that head tissues do not contribute equally in the averaging volume and not all tissues in the averaging volume have the same variation of the dielectric properties with age (in this case only skin contributed to the variation within the 10 g cube). Finally, Christ et al. (2010) studied the exposure of three anatomical head models (adult, 3 and 7 year old) to a generic dual band mobile phone operating at 900 MHz and 1800 MHz. They incorporated 16 tissue types in the models at 900 MHz and 1800 MHz by assigning dielectric properties of 10 kg, 50 kg and 250 kg pigs. Although the results showed SAR variations due to the age dependent changes to be within 30%, for all the configurations analysed, age dependencies of dielectric tissue properties did not lead to systematic changes of the peak spatial SAR. In other
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A. Peyman / Progress in Biophysics and Molecular Biology 107 (2011) 434e438
words, the hypothesis that variation in the dielectric parameters results in larger exposure of young mobile phone users could not be confirmed. The authors suggested that this may be due to the fact that highest age dependent variations occur in tissues with low water content. To single out the effect of ageing dielectric properties of tissues, Christ et al. (2010) calculated SAR values for single tissues such as bone marrow. They reported that exposure of the bone marrow of children can exceed that of adults by about a factor of ten. This is due to the strong decrease in electric conductivity of this tissue with age (as shown in Fig. 3).
5. Summary and concluding remarks Numerical modelling tools have improved over the last 20 years, from coarse geometrical models to very high resolution models based on real human imaging data. Meanwhile, measurements of dielectric properties of tissues are also becoming more comprehensive, providing in-detail information, expanding the number of tissues defined in the models and taking into consideration the variation of data with age. It is now established that dielectric properties of certain tissues decrease significantly as a function of age. At microwave frequencies this is mainly due to decline in water content of the tissues. It is the matter of reassurance that the dosimetric studies so far have not shown any significant differences in the calculated SAR values due to higher conductivity values for younger tissues. However, in some cases, for instance single tissue exposure such as bone marrow, the differences can not be neglected.
References Alfadh, Y., Chiau, C.C., Wang, Z., Chen, X., Peyman, A., Gabriel, C., 2003. Numerical Dosimetry on 10, 30 and 70 Days Old Rat Models Exposed to a Wide Range of Frequencies and Dielectric Properties ST-9 BEMS 25th Annual Meeting Maui, Hawaii, USA. Christ, A., Gosselin, M.C., Christopoulou, M., Kühn, S., Kuster, N., 2010. Age-dependent tissue-specific exposure of cell phone users. Phys. Med. Biol. 55, 1767. Cole, K.S., Cole, R.H., 1941. Dispersion and absorption in dielectrics: I. Alternating current characteristics. J. Chem. Phys. 9, 341e351. Dimbylow, P., Bolch, W., Lee, C., 2010. SAR calculations from 20 MHz to 6 GHz in the University of Florida newborn voxel phantom and their implications for dosimetry. Phys. Med. Biol. 55, 1519e1530. Gabriel, C., Gabriel, S., 1997. Compilation of the Dielectric Properties of Body Tissues at RF and Microwave Frequencies. http://niremf.ifac.cnr.it/docs/DIELECTRIC/ home.html. Gabriel, C., Peyman, A., 2006. Dielectric measurement error analysis and assessment of uncertainty. Phys. Med.Biol. 51, 6033e6046. Gabriel, C., Gabriel, S., Corthout, E., 1996a. The dielectric properties of biological tissues: I. Literature survey. Phys. Med. Biol. 41, 2231e2249.
Gabriel, S., Lau, R.W., Gabriel, C., 1996b. The dielectric properties of biological tissues: II. Measurements in the frequency range of 10 Hz to 20 GHz. Phys. Med. Biol. 41, 2251e2269. Gabriel, S., Lau, R.W., Gabriel, C., 1996c. The dielectric properties of biological tissues: III. Parametric models for the dielectric spectrum of tissues. Phys. Med. Biol. 41, 2271e2293. Gabriel, C., Peyman, A., Grant, E.H., 2009. Electrical conductivity of tissue at frequencies below 1 MHz. Phys. Med. Biol. 54, 4863e4878. Gabriel, C., 2005. Dielectric properties of biological tissues; variation with age. Bioelectromagnetics (Suppl. 7), S12eS18. IEGMP (Independent Expert Group on Mobile Phones), 2000. Mobile Phones and Health 2000. NRPB, Didcot. Keshvari, J., Keshvari, R., Lang, S., 2006. The effect of increase in dielectric values on specific absorption rate (SAR) in eye and head tissues following 900, 1800 and 2450 MHz radio frequency (RF) exposure. Phys. Med. Biol. 51, 1463. Kraszewski, A., Stuchly, S.S., Stuchly, M.A., Smith, A.M., 1982. In vivo and in vitro dielectric properties of animal tissues at radio frequencies. Bioelectromagnetics 3, 421e432. Kuang, W., Nelson, O., 1998. Low-frequency dielectric properties of biological tissues: a review with some new insights. Trans. Am. Soc. Agric. Eng. 41, 173e184. Pethig, R., Kell, D.B., 1987. The passive electrical properties of biological systems: their significance in physiology, biophysics and biotechnology. Phys. Med. Biol. 32, 933e970. Pethig, R., 1984. Dielectric properties of biological materials: biophysical and medical applications. IEEE Trans. Electr. Insul 19, 453e473. Peyman, A., Gabriel, C., 2003a. Age Related Variation of the Dielectric Properties of Biological Tissues. Final technical report, RRX88. UK Department of Health. Peyman, A., Gabriel, C., 2003b. Dielectric Properties of Aging Rat Tissues at Intermediate Frequencies BEMS annual meeting Maui, Hawaii. Peyman, A., Gabriel, C., 2010. ColeeCole parameters for the dielectric properties of porcine tissues as a function of age at microwave frequencies. Phys. Med. Biol. 55, N413eN419. Peyman, A., Rezazadeh, A.A., Gabriel, C., 2001. Changes in the dielectric properties of rat tissue as a function of age at microwave frequencies. Phys. Med. Biol. 46, 1617e1629. Peyman, A., Holden, S., Gabriel, C., 2005. Dielectric Properties of Tissues at Microwave Frequencies, RUM3 MTHR Final Technical Report. http://www.mthr.org. uk/research_projects/documents/Rum3FinalReport.pdf. Peyman, A., Holden, S.J., Watts, S., Perrott, R., Gabriel, C., 2007. Dielectric properties of porcine cerebrospinal tissues at microwave frequencies: in vivo, in vitro and systematic variation with age. Phys. Med. Biol. 52, 2229e2245. Peyman, A., Gabriel, C., Grant, E.H., Vermeeren, G., Martens, L., 2009. Variation of the dielectric properties of tissues with age: the effect on the values of SAR in children when exposed to walkieetalkie devices. Phys. Med. Biol. 54, 227e241. Peyman, A., Gabriel, C., Benedickter, H.R., Fröhlich, J., 2011. Dielectric properties of human placenta, umbilical cord and amniotic fluid. Phys. Med. Biol. 56, N93eN98. Peyman, A., 2011. Dielectric Properties of Pregnancy-Specific and Foetal Tissues BEMS annual meeting Halifax June 2011. Schmid, G., Überbacher, R., 2005. Age dependence of dielectric properties of bovine brain and ocular tissues in the frequency range of 400 MHz to 18 GHz. Phys. Med. Biol. 50, 4711e4720. Schwan, H.P., Foster, K.R., 1980. RF-field interactions with biological systems: electrical properties and biophysical mechanisms. Proc. IEEE 68, 104e113. Thurai, M., Goodridge, V.D., Sheppard, R.J., Grant, E.H., 1984. Variation with age of the dielectric properties of mouse brain cerebrum. Phys. Med. Biol. 29, 1133e1136. Thurai, M., Steel, M.C., Sheppard, R.J., Grant, E.H., 1985. Dielectric properties of developing rabbit brain at 37 C. Bioelectromagnetics 6, 235e242. Wang, J., Fujiwara, O., Watanabe, S., 2006. Approximation of aging effect on dielectric tissue properties for SAR assessment of mobile telephones. IEEE Trans. Electromagn. Compat. 48 (2), 408e413.
Contents lists available at SciVerse ScienceDirect
Progress in Biophysics and Molecular Biology journal homepage: www.elsevier.com/locate/pbiomolbio
Review
Dielectric properties of tissues; variation with age and their relevance in exposure of children to electromagnetic fields; state of knowledge Azadeh Peyman* Health Protection Agency, Chilton, Didcot, Oxon OX11 0RQ, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 3 September 2011
This paper reviews and summarises the state of knowledge on dielectric properties of tissues; in particular those obtained as a function of age. It also examines the impact of variation in dielectric data on the outcome of recent dosimetric studies assessing the exposure of children to electromagnetic fields. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: Dielectric properties Biological tissues Dosimetry Children
Contents 1. 2.
3. 4. 5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 434 Dielectric properties of tissues, state of knowledge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435 2.1. 1996 database . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435 2.2. MTHR study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435 2.3. Updates on low frequency measurements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436 Variation of dielectric properties with age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436 Impact of variation in dielectric properties on SAR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .437 Summary and concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438
1. Introduction One of the main inputs required in the dosimetry studies assessing the exposure of people to electromagnetic fields (EMF) are dielectric properties of different body tissues which determine the interaction of the fields with the human body. Accurate knowledge of the dielectric properties of tissues is required in order to calculate the energy deposition when they are exposed to EMF. Dielectric properties of tissues are frequency dependent and exhibit systematic changes due to the physiological state of the tissue; for instance the intactness of cellular membrane and the water content of the tissue. The dielectric spectra of tissues consist of three main dispersions predicted by known interaction mechanisms (Fig. 1). The a-dispersion is characterised by the very large
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permittivity values that are produced by ionic diffusion processes at the site of the cellular membrane at very low frequencies (below a few kHz). At intermediate frequencies (kHz region), the b dispersion occurs due to the polarisation of the cellular membrane. Finally, the g dispersion at microwave frequencies is mainly due to the polarisation of water molecules inside the tissue. The dielectric spectrum of biological tissues can be mathematically modelled by one or more terms of the well-known ColeeCole expression (Cole and Cole, 1941):
^3 ðuÞ ¼
3N
þ
3s
3N
1 þ ðjusÞð1aÞ
þ
si
ju3 0
(1)
Where ^3 is the complex relative permittivity, u the angular frequency and the ColeeCole parameters have their usual significance. Modelling the dielectric properties of tissues using Equation (1) facilitates their incorporation in numerical simulations of human exposure to electromagnetic fields.
A. Peyman / Progress in Biophysics and Molecular Biology 107 (2011) 434e438
Fig. 1. Dielectric spectrum of ovine liver (Gabriel et al. 1996b).
At radiofrequencies, the metric used for assessing people’s exposure is the Specific Energy Absorption Rate (SAR) expressed in watts per kilogram (W kg1). SAR is a function of the electric field induced in the body at any one point and the conductivity of the body tissue at that point:
SAR ¼ s
jE2 j
r
(2)
where s is the conductivity of the tissue in S m1, r is mass density of the tissue in kg m3 and E the root mean square (rms) electric field strength (V m1). Dielectric properties of tissues and their variation with frequency is well studied, reported and reviewed (Schwan and Foster, 1980; Pethig, 1984; Pethig and Kell, 1987; Gabriel et al., 1996a,b,c). While, the earlier studies focused on the interaction mechanisms, later ones aimed to provide a reliable and accurate database of dielectric properties of different body tissues across the frequency spectrum. These data are a necessary input in the electromagnetic dosimetry studies where the exposure of people to external fields are assessed. Until recently, the literature data consisted mostly of dielectric properties of tissues from mature animals (Gabriel et al., 1996 aec), usually used to simulate adult models of the human head/body. Two earlier studies had reported on systematic changes in the dielectric properties of ageing brain tissues (Thurai et al., 1984, 1985). In the last few years, and due to substantial concern about the possible differences between the exposure of children and adults to electromagnetic fields, the focus of many studies has been shifted towards the development of childrens’ head/body models. To provide relevant dielectric data for children’s models, several studies have been carried out on dielectric properties of animal tissues from a range of ages (Peyman et al., 2001, 2007; Schmid and Überbacher, 2005; Peyman and Gabriel, 2010). These studies have triggered discussions on the extent to which the variation of dielectric data as a function of age would affect the results of dosimetry studies, and consequently the possible implications for the exposure of children. This paper summerises the current knowledge of dielectric properties of tissues over a wide frequency range and their variation as a function of age. It also reports the effect of these changes on dosimteric studies at radiofrequencies. 2. Dielectric properties of tissues, state of knowledge 2.1. 1996 database In 1996, Gabriel et al. carried out a systematic review of almost half a century’s literature available at the time in terms of the
435
dielectric properties of tissues over ten frequency decades. They then carried out an extensive experimental study on a large number of biological tissues at body temperature using three different measurement techniques spanning the frequency range of 10 Hze20 GHz (Gabriel et al., 1996b). Their experimental results showed good agreement between data obtained from three experimental setups in the overlapping frequency ranges. The data were also largely in good agreement with the corresponding values in the literature. Finally, Gabriel et al. (1996c) used their experimental data, complemented by the data surveyed from the literature, to develop a parametric model (consisting of four ColeeCole terms plus one ionic conductivity term) to describe the variation of dielectric properties of tissues as a function of frequency. The ColeeCole model parameters later became available on the internet (Gabriel and Gabriel, 1997) and have been used extensively since to reconstruct the dielectric spectrum of each tissue in dosimetry studies. 2.2. MTHR study Although the 1996 database has been used extensively in dosimetric studies, there were still some gaps and limitation associated with it. In particular, since most measurements were carried out on excised tissues, critics argued that data pertaining to live tissue would be more relevant in bioelectromagetic studies. In addition, low frequency dielectric data are associated with larger uncertainties due to practical difficulties such as electrode polarisation and only few values are available for them in the literature. Therefore, the authors of the 1996 database have cautioned the use of the ColeeCole model for lower frequency parts of the spectrum as the best estimate based on the literature data before 1996, until more reliable and accurate data becomes available. Also, a better understanding of the uncertainty associated with dielectric measurements was needed. To fill the above gaps and update the state of knowledge on the subject, a systematic study was carried out as part of the UK’s Mobile Telecommunication Health Research (MTHR) program. The main objective of the study was to review the literature data post 1996 and obtain and analyse extensive and novel experimental data acquired from measurements on “live” animals at microwave frequencies. The study was also aimed to identify different random and systematic sources of errors associated with the dielectric measurements and develop a procedure to assess the total combined uncertainty for the dielectric data. Dielectric data (permittivity 3 0 and conductivity s) were collected from live porcine tissues, which are thought to be a good animal substitute to human tissue and would make a good basis for comparison with the data from the 1996 database that were mostly derived from measurements on excised ovine tissue (Peyman et al., 2005, 2007). For most of the tissues (brain and abdominal tissues) the new data were in good agreement with the 1996 database. However, in the case of skeletal tissues, the large numbers of independent dielectric measurements on both skull and long bone of different pigs show generally higher values than those reported in the Gabriel et al. (1996c) database (Fig. 2). These high values could possibly be due to the differences in the species and the age of the animals used in MTHR study and other studies. As it is apparent from Fig. 2, there is a big difference between data collected from young pigs (50 kg) and those of the older pigs (250 kg mature sows). The 1996 database values are closer to data gathered from older animals. Another important outcome of the MTHR study was that it did not report any systematic difference between dielectric data collected under in-vivo and in-vitro conditions at microwave frequencies
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using an in house developed probe comprising a rectilinear array of four platinum-blacked platinum pin electrodes embedded in PTFE. The authors claimed that this probe produced a coherent set of capacitance and conductance values, down to 1 Hz, when used to measure water and low concentration salt solutions (Gabriel et al., 2009). The effect of electrode polarisation at low frequencies, and some other high-frequency effects were identified as measurement artefacts. Although the authors found ways to subtract electrode polarisation from the lower side of the measured spectrum, highfrequency effects are yet to be fully identified and resolved. 3. Variation of dielectric properties with age
Fig. 2. Reported a: permittivity and b: conductivity of skull tissues.
(Peyman et al., 2005, 2007). This is due to the fact that at microwave frequencies, and the site of g dispersion region, dielectric properties of tissues are associated with the water content of the tissues and if care is taken to avoid drying of excised tissue samples, no systematic difference is anticipated. The situation is different at lower frequencies, in the range of the a and b dispersions in view of the sensitivity of their causal mechanism to the physiological state of the tissue (Kraszewski et al., 1982; Kuang and Nelson, 1998). Finally, systematic statistical and comparative analysis of a large amount of experimental dielectric data showed that for most tissue types the random uncertainty is by far the largest element in the uncertainty budget. This is due to the natural inhomogeneity inherited in biological samples. To determine the uncertainty in the measurement of biological tissue, random variations are obtained from repeat measurements and the instrumental and methodological uncertainties are calculated from measurements on standard liquids with well-known dielectric properties (Gabriel and Peyman, 2006). 2.3. Updates on low frequency measurements Low frequency dielectric data for body tissues are difficult to obtain due to the strong dependency of the dielectric properties on the physiological state of the tissues and changes occurring after death. There are also several practical difficulties in particular electrode polarisation which manifests itself in the low frequency part of the spectrum (<100 Hz). In a recent publication, Gabriel et al. (2009) reported a twopronged approach, review and measurement, to characterise the conductivity of tissues at frequencies below 1 MHz. In their review they covered data published in the last decade (post 1996) for a critical analysis to highlight their usefulness and limitations. They also carried out in-vivo measurements on pig myocardial muscle, liver, skull, fat, lung and in-vitro measurements on pig body fluids
The 1996 database only contains dielectric data obtained from mature animals. A few older studies reported systematic changes in the dielectric properties of ageing brain tissues (Thurai et al., 1984, 1985). Following the publication of the report of the Independent Expert Group on Mobile Phones (IEGMP, 2000), that highlighted the need for rigorous assessment of the exposure of children, a study was carried out by Peyman et al. (2001) on dielectric properties of rodent tissues from new born to fully grown rats at microwave frequencies. This was later extended to intermediate frequencies down to 300 kHz (Peyman and Gabriel, 2003a,b, Gabriel, 2005). The results of these studies showed that some head tissue (brain, skin and skull) exhibit significant variation, mainly decreasing in the measured permittivity and conductivity, as the animal gets older. The authors reported that the corresponding changes for the abdominal tissues are less prominent. To re-examine the above findings and to report data for more tissues, Peyman et al. (2005) carried out dielectric measurements on porcine tissues from 10, 50 and 250 kg pigs to cover developmental stages from piglets to mature animals. Porcine tissues are regarded as a good substitute for human tissues with respect to dielectric properties. To relate their findings to human tissue, Peyman et al. (2005) assumed that dielectric properties of tissues from 10 kg piglets correspond to those of human children of age 1e4 years, the 50 kg pigs to be equivalent to 11e13 years old human and the 250 kg, pigs to be considered equivalent to human adults. Further studies were also carried out on bovine excised tissues as a function of animal age (Schmid and Überbacher, 2005). The results of these studies also generally showed a significant decline in both permittivity and conductivity as a function of age for some tissues such as brain (white matter), long bone, skull, skin, muscle and bone marrow. No variation was observed in the dielectric properties of abdominal tissues. At microwave frequencies, the observed variations in dielectric properties are mainly due to the reduction in water content of tissues as an animal ages. The molecular orientation of tissue water is described in the g dispersion and conditions giving rise to a change in the water content of tissue are reflected in the parameters of this dispersion. At intermediate frequencies (300 kHze300 MHz), the measured dielectric spectrum reflects the site of the b dispersion. Changes in cellular structure and physiological state of the cell membrane are signalled by changes in this dispersion region. In the case of the brain, increased myelination and decreased water content as a function of age is said to be the reason for the drop in permittivity and conductivity values of white matter (No variation was observed in the dielectric data of grey matter) and spinal cord as animals age (Schmid and Überbacher, 2005 and Peyman et al., 2007). Bony tissues have higher variations in the amount of water due to changes in the degree of mineralisation of the calcified bone matrix during growth, resulting in a more “significant” decline in dielectric properties. The largest variation in the dielectric properties as a function of age is observed in bone
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marrow tissues (Fig. 3) due to the transformation of high water content red marrow to high fat content yellow marrow as the animal grows (Peyman et al., 2009). The above studies have reported dielectric properties of ageing tissues at selected frequencies. To facilitate the use of experimental data obtained in dosimetry studies, Peyman and Gabriel 2010 provided the ColeeCole parameters for 14 tissue types at three developmental stages using the dielectric spectra of ageing porcine tissues. The 14 tissues identified are those that exhibited a significant decline in dielectric properties as a function of age (Peyman et al., 2005, 2007 and 2009). It is expected that the ColeeCole parameters reported by Gabriel et al. (1996c) continue to be used for the dielectric properties of tissues that did not exhibit age related changes. As the focus of dosimetric studies shifts from children to pregnant women and their foetuses, so does the need for dielectric properties of pregnancy associated tissues. So far, in the absence of such data, substitutes are used to simulate the exposure of pregnant women and their foetus to electromagnetic fields. For example, dielectric properties of muscle and blood are used for placenta and that of cerebrospinal fluid for amniotic fluid. To fill this gap, Peyman et al. (2011) and Peyman (2011) conducted an experimental study to provide dielectric data for human placenta, umbilical cord and amniotic fluid as well as several rat foetuses at different stages of gestation. Their results showed that the dielectric properties of amniotic fluid are significantly different from those of cerebrospinal fluid. They also mapped strong temperature dependency in the dielectric properties of amniotic fluid. Another outcome of this study was that umbilical cord has dielectric properties much higher than that of placenta due to the presence of high water content Wharton’s jelly. The results also showed that the
Fig. 3. Reported a: permittivity and b: conductivity of porcine bone marrow at three different growth stage (Peyman et al., 2005, 2009). Error bars represent 95% confidence intervals.
437
dielectric properties of foetus are generally higher than that of adult muscle and other abdominal tissues. In addition, dielectric properties of the foetus generally decreases as a function of gestation, however the magnitude of decrease in the dielectric data is not very large, and only reflects the fact that the total water content of the foetus as a whole decreases as it gets older. 4. Impact of variation in dielectric properties on SAR To the best of the author’s knowledge, only three studies have used the mentioned experimental dielectric properties of tissues as a function of age to calculate SAR values in models of children’s head/body as a result of exposure to electromagnetic fields. Few other studies have also examined the effect of changes in dielectric properties as a function of age on the calculated SAR by using adult dielectric properties and adjusting them for younger tissues assuming higher water content (Keshvari et al., 2006; Wang et al., 2006; Dimbylow et al., 2010). Each of the following studies have used a different metric in their SAR calculation such as localised SAR values for individual tissues, SAR10 g (SAR averaged over 10 g of tissue) or whole body SAR, therefore a direct comparison can not be drawn. Alfadh et al. (2003) and Gabriel (2005) used age related dielectric properties of rat tissues in a numerical study of exposure of rat models to plane waves at 27, 160, 400, 900, and 2000 MHz. 34 tissue-types have been identified in three rat models (10, 30 and 70 days old), from which only 9 tissues exhibited variation in their dielectric properties as a function of age. The results showed that, although changing the tissue dielectric properties would affect the localised SAR, no clear pattern could be established. The effect on whole body SAR was reported to be small, its extent depending on the variation in properties and the abundance of the tissues in the exposed model. These results can be explained as due to the fact that changes in dielectric properties would affect the coupling with the body and the interaction of tissues with the electromagnetic fields. It is also important to isolate the effect of changing tissue properties from all other factors that would affect the exposure, such as the size of the animal and polarisation and direction of the incident field (Gabriel, 2005). The second study examined the sensitivity of calculated SAR values to variation in dielectric properties when models of children and adults are exposed to EMF from walkie-talkie devices operating at 446 MHz (Peyman et al., 2009). Head models representing adults and 3- and 7-year old children were considered with tissue dielectric properties taken from 10 kg pig (1e4 year old), 50 kg pig (11e13 years old) and 250 kg pigs (adults). The results showed that variations on SAR10gr are less than 10% for the investigated configuration and that the variations of the tissue properties are not really reflected in a variation of SAR10 g. This could be due to the fact that averaging of the SAR dilutes the effect of the change in the SAR10 g. In addition, it is obvious that head tissues do not contribute equally in the averaging volume and not all tissues in the averaging volume have the same variation of the dielectric properties with age (in this case only skin contributed to the variation within the 10 g cube). Finally, Christ et al. (2010) studied the exposure of three anatomical head models (adult, 3 and 7 year old) to a generic dual band mobile phone operating at 900 MHz and 1800 MHz. They incorporated 16 tissue types in the models at 900 MHz and 1800 MHz by assigning dielectric properties of 10 kg, 50 kg and 250 kg pigs. Although the results showed SAR variations due to the age dependent changes to be within 30%, for all the configurations analysed, age dependencies of dielectric tissue properties did not lead to systematic changes of the peak spatial SAR. In other
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words, the hypothesis that variation in the dielectric parameters results in larger exposure of young mobile phone users could not be confirmed. The authors suggested that this may be due to the fact that highest age dependent variations occur in tissues with low water content. To single out the effect of ageing dielectric properties of tissues, Christ et al. (2010) calculated SAR values for single tissues such as bone marrow. They reported that exposure of the bone marrow of children can exceed that of adults by about a factor of ten. This is due to the strong decrease in electric conductivity of this tissue with age (as shown in Fig. 3).
5. Summary and concluding remarks Numerical modelling tools have improved over the last 20 years, from coarse geometrical models to very high resolution models based on real human imaging data. Meanwhile, measurements of dielectric properties of tissues are also becoming more comprehensive, providing in-detail information, expanding the number of tissues defined in the models and taking into consideration the variation of data with age. It is now established that dielectric properties of certain tissues decrease significantly as a function of age. At microwave frequencies this is mainly due to decline in water content of the tissues. It is the matter of reassurance that the dosimetric studies so far have not shown any significant differences in the calculated SAR values due to higher conductivity values for younger tissues. However, in some cases, for instance single tissue exposure such as bone marrow, the differences can not be neglected.
References Alfadh, Y., Chiau, C.C., Wang, Z., Chen, X., Peyman, A., Gabriel, C., 2003. Numerical Dosimetry on 10, 30 and 70 Days Old Rat Models Exposed to a Wide Range of Frequencies and Dielectric Properties ST-9 BEMS 25th Annual Meeting Maui, Hawaii, USA. Christ, A., Gosselin, M.C., Christopoulou, M., Kühn, S., Kuster, N., 2010. Age-dependent tissue-specific exposure of cell phone users. Phys. Med. Biol. 55, 1767. Cole, K.S., Cole, R.H., 1941. Dispersion and absorption in dielectrics: I. Alternating current characteristics. J. Chem. Phys. 9, 341e351. Dimbylow, P., Bolch, W., Lee, C., 2010. SAR calculations from 20 MHz to 6 GHz in the University of Florida newborn voxel phantom and their implications for dosimetry. Phys. Med. Biol. 55, 1519e1530. Gabriel, C., Gabriel, S., 1997. Compilation of the Dielectric Properties of Body Tissues at RF and Microwave Frequencies. http://niremf.ifac.cnr.it/docs/DIELECTRIC/ home.html. Gabriel, C., Peyman, A., 2006. Dielectric measurement error analysis and assessment of uncertainty. Phys. Med.Biol. 51, 6033e6046. Gabriel, C., Gabriel, S., Corthout, E., 1996a. The dielectric properties of biological tissues: I. Literature survey. Phys. Med. Biol. 41, 2231e2249.
Gabriel, S., Lau, R.W., Gabriel, C., 1996b. The dielectric properties of biological tissues: II. Measurements in the frequency range of 10 Hz to 20 GHz. Phys. Med. Biol. 41, 2251e2269. Gabriel, S., Lau, R.W., Gabriel, C., 1996c. The dielectric properties of biological tissues: III. Parametric models for the dielectric spectrum of tissues. Phys. Med. Biol. 41, 2271e2293. Gabriel, C., Peyman, A., Grant, E.H., 2009. Electrical conductivity of tissue at frequencies below 1 MHz. Phys. Med. Biol. 54, 4863e4878. Gabriel, C., 2005. Dielectric properties of biological tissues; variation with age. Bioelectromagnetics (Suppl. 7), S12eS18. IEGMP (Independent Expert Group on Mobile Phones), 2000. Mobile Phones and Health 2000. NRPB, Didcot. Keshvari, J., Keshvari, R., Lang, S., 2006. The effect of increase in dielectric values on specific absorption rate (SAR) in eye and head tissues following 900, 1800 and 2450 MHz radio frequency (RF) exposure. Phys. Med. Biol. 51, 1463. Kraszewski, A., Stuchly, S.S., Stuchly, M.A., Smith, A.M., 1982. In vivo and in vitro dielectric properties of animal tissues at radio frequencies. Bioelectromagnetics 3, 421e432. Kuang, W., Nelson, O., 1998. Low-frequency dielectric properties of biological tissues: a review with some new insights. Trans. Am. Soc. Agric. Eng. 41, 173e184. Pethig, R., Kell, D.B., 1987. The passive electrical properties of biological systems: their significance in physiology, biophysics and biotechnology. Phys. Med. Biol. 32, 933e970. Pethig, R., 1984. Dielectric properties of biological materials: biophysical and medical applications. IEEE Trans. Electr. Insul 19, 453e473. Peyman, A., Gabriel, C., 2003a. Age Related Variation of the Dielectric Properties of Biological Tissues. Final technical report, RRX88. UK Department of Health. Peyman, A., Gabriel, C., 2003b. Dielectric Properties of Aging Rat Tissues at Intermediate Frequencies BEMS annual meeting Maui, Hawaii. Peyman, A., Gabriel, C., 2010. ColeeCole parameters for the dielectric properties of porcine tissues as a function of age at microwave frequencies. Phys. Med. Biol. 55, N413eN419. Peyman, A., Rezazadeh, A.A., Gabriel, C., 2001. Changes in the dielectric properties of rat tissue as a function of age at microwave frequencies. Phys. Med. Biol. 46, 1617e1629. Peyman, A., Holden, S., Gabriel, C., 2005. Dielectric Properties of Tissues at Microwave Frequencies, RUM3 MTHR Final Technical Report. http://www.mthr.org. uk/research_projects/documents/Rum3FinalReport.pdf. Peyman, A., Holden, S.J., Watts, S., Perrott, R., Gabriel, C., 2007. Dielectric properties of porcine cerebrospinal tissues at microwave frequencies: in vivo, in vitro and systematic variation with age. Phys. Med. Biol. 52, 2229e2245. Peyman, A., Gabriel, C., Grant, E.H., Vermeeren, G., Martens, L., 2009. Variation of the dielectric properties of tissues with age: the effect on the values of SAR in children when exposed to walkieetalkie devices. Phys. Med. Biol. 54, 227e241. Peyman, A., Gabriel, C., Benedickter, H.R., Fröhlich, J., 2011. Dielectric properties of human placenta, umbilical cord and amniotic fluid. Phys. Med. Biol. 56, N93eN98. Peyman, A., 2011. Dielectric Properties of Pregnancy-Specific and Foetal Tissues BEMS annual meeting Halifax June 2011. Schmid, G., Überbacher, R., 2005. Age dependence of dielectric properties of bovine brain and ocular tissues in the frequency range of 400 MHz to 18 GHz. Phys. Med. Biol. 50, 4711e4720. Schwan, H.P., Foster, K.R., 1980. RF-field interactions with biological systems: electrical properties and biophysical mechanisms. Proc. IEEE 68, 104e113. Thurai, M., Goodridge, V.D., Sheppard, R.J., Grant, E.H., 1984. Variation with age of the dielectric properties of mouse brain cerebrum. Phys. Med. Biol. 29, 1133e1136. Thurai, M., Steel, M.C., Sheppard, R.J., Grant, E.H., 1985. Dielectric properties of developing rabbit brain at 37 C. Bioelectromagnetics 6, 235e242. Wang, J., Fujiwara, O., Watanabe, S., 2006. Approximation of aging effect on dielectric tissue properties for SAR assessment of mobile telephones. IEEE Trans. Electromagn. Compat. 48 (2), 408e413.