- Email: [email protected]
Ultrasonic attenuation in fresh human tissues
Ultrasonic
attenuation
in fresh human tissues
Dear Sir, As a preliminary stage of a project’ designed to assess the usefulness of measurements of acoustic propagation properties for identifying pathology in human tissues, a series of measurements was made of the ultrasonic attenuation coefficient, as a function of frequency, of excised normal human tissues. Although some results of this early series of measurements have been presented previously23’ they are not easily available and have never been published in full. A brief discussion of these data, in the light of subsequent experience, may be of value to readers interested in making similar measurements. The measurement technique was basically that described previously by Chivers and HilIp with modifications to facilitate rapid automatic data collection and analysis.’ Reasonably detailed descriptions may also be found elsewhere. 596 Specimens of the organs of interest were obtained direct from autopsy of normal human subjects. Most of the measurements were made at room temperature with specimens immersed in saline and contained in a thin, taut, polythene bag. No special efforts were made to degas these preparations, other than palpation with the fingers to remove any visible signs of bubbles. Using analogue spectral analysis of very short acoustic pulses an average attenuation coefficient for 3 to 6 regions, chosen at random, within each specimen was obtained at 44 or more frequencies in the range 1 to 6 MHz. The average attenuation coefficient, 01,as a function of frequency, f,for each specimen was then fitted, by eye using double logarithmic scales, to the equation (Y= by. Values of the slope, m, and the intercept, b (that is, the value of (Yat 1 MHz), were finally averaged over similar tissue types (Table 1). The results for human spleen agree very welI with the one other data set with which they may be compared,’ and those for brain fall within the range of values found in the literature (see for example that reviewed by Kremkau et als). It is seen that the ratio of the average attenuation coefficient at 1 MHz for mostly white matter against a mixture of grey and white matter is 1.4. This value is comparable with the value of 1.7 obtained for a similar ratio by means of absorption measurements in pure white and pure grey matter,g and happens to be identical to an equivalent ratio for attenuation in human brain obtained by Kremkau et al.’ It has been noted’ that variation of water content provides a reasonably quantitative explanation for the differences between white and grey matter; an explanation that is consistent with results as a function of water content in liver. lo It is also seen that, while the values for spleen and brain are relatively tightly grouped, liver, for reasons unknown at the time, gave extremely variable results. The anomalous nature of ultrasonic properties of liver has since been noticed on a number of occasions,5~11~‘2 and appears now (possibly) to be related to a number of factors.’ These include relatively large spatial variations in the attenuation coefficient and propagation speed, the latter leading to varying degrees of 0041-624X/81/040187-02/$02.00 ULTRASONICS.
JULY 1981
excess attenuation and erratic frequency dependences due to phase cancellation,“13s14 and a tendency for gas bubbles to interfere with the measurement.15s16 Gas is possibly more likely to be present in liver than in specimens of other organs because of its highly vascular structure (gas may have been introduced at times after excision) and its tendency to produce gas during autolytic decay.5y17 Erratic results were also obtained from human stomach fat with regions of negative dependence on frequency often being observed and, since only six specimens were examined, mean values of b and m have not been computed. Phase cancellation at the receiver’33’4 is probably an important mechanism in producing these effects. The speed of sound in fat is variable and may be as much as 6% lower than the speed of sound in saline. Added to this, stomach fat has a very heterogeneous gross structure and the specimens were difficult to cut to a uniform thickness.
Table 1. Results of measurement of ultrasonic attenuation in freshly excised human tissues, expressed in terms of average values for the constants b and m in the equation (Y= bfm. The variations noted refer to the total range of values observed between specimens of the same organ.
Organ
Number of Specimens
Remarks
Spleen
4
None
5
f Brain
3
b[dB cm-‘]
m
Mixed grey and white matter
0.58 +_
+ 1.3_
12% 8%
Mostly white matter
0.8
+ -
5% 10%
Liver*
25
Resultsvariable and erratic
Stomach fat
6
Results extremely erratic (only range values given)
Testis
4
Values forb obtained by extrapolation of 3 - 7 MHz data
3%
+ 20% _ loy 0
+ 200% 1 _ 7oo/0
1.1
+ 110% 1_ 6oo/0
0.6 to 5.2
0.4 to 1.4
+ 47% 0.17 _ 41%
+ 20% 1.7 _ 26%
l More recent results using the same measurement technique but with precautions mentioned in the text yielded values b = 1.1 f 40% dB cm -‘I and m = 0.9 f 30% for specimens of normal human liver. 1 ,20 It is likely, however, that due to the influence of gas bubbles even these values are over estimates at low frequencies and posses an excessive variation from specimen to specimen16*”
0 1981 IPC Business Press 187
The attenuation of ultrasound in human testis was often, at the lower frequencies, too small to be measured with the apparatus employed. Values for b were therefore obtained by extrapolation of results obtained at higher frequencies (3 to 7 MHz). The results for human testis are consistent with the finding” that the absorption coefficient of testes from small mammals is much lower than values for other soft tissues, following the relationship cu, = 0.13 f” (dB cm-’ ). It would appear that low attenuation values in testis might be explained in terms of the extremely high water content and the low structural protein content of this organ.lg The above-noted erratic and variable results for liver and fat led to a series of investigations designed to assess the usefulness of autopsy material for this kind of study, the results of which have since been reported.‘ysy6 Selection of measurement sites for minimum phase cancellation artefact, the use of de-gassing procedures and general improvements in specimen handling techniques (for example, storage, cutting and measurement) have resulted in some reduction in the observed variation of the attenuation coefficient of human liver’F11720 (see caption to Table 1). The presence of gas in the specimens is probably the greatest single problem to be encountered in measurements of this kind. The nature of the effects of gas, and techniques for its removal, are subjects discussed elsewhere.159’6 I should like to acknowledge that many of the measurements reported here were made by M.J. Fry, assistance and advice were provided by F. Dunn and D. Nicholas, and the work was conducted while studying for a Ph.D. under the supervision of C.R. Hill. Yours faithfully J. C. Bamber Physics Division, Block F, institute of Cancer Research, Clifton Avenue, Sutton, Surrey SM2 5PX, UK Received 26 February 1981
3
4 5
6
I
8
9
10 11 12 13
14
15
16 17
18
19 References 1
2
188
Bamber, J.C., Ultrasonic characterization of structure and pathology in human soft tissues, Ph.D. Thesis, London University (1979) Bamber, J.C., Nicholas, D., Fry, M., Dunn, F., in British Biocoustics meeting (report by A.R. Williams), Lntrasound Med. Biol., 2 (1976) 357
20
Bamber, J.C., in Scientific basis of diagnostic ultrasound (meeting report by A. Hall), Hosp. P&s. Ass. Bull., (Dec. 1976) 14-18 Chivers, RC, HiII, C.R, Ultrasonic attenuation in human tissue. Ultrasound Med. Biol.. 2 (1915) 25-29 Ban&r, J.C., Fry, NJ., HiU,‘C’i, Du& F., Ultrasonic attenuation and backscattering by mammalian organs as a function of time after excision, Ultrasound Med. BioZ., 3 (1977) 15-20 Bamber, J.C, HiB, CR, Ultrasonic attenuation and propagation speed in mammalian tissues as a function of temperature, Ultrasound Med. Biol., 5 (1979) 149-157 Nicholas, D., Orientation and frequency dependence of backscattered energy and its clinical application, in Recent advances in ultrasound in biomedicine (Edited by D.N. White) 1 Research Studies Press, Oregon (1977) 29-54 Kremkau, F.W., McGraw, C.P., Barnes, RN., Attenuation and propagation speed in normal human brain, J. Acoust. Sot. Am (submitted for publication) Fry, W.J., Dunn, F., Ultrasound analysis and experimental methods in biological research, in Physical techniques in biological research, Ch. 4 Academic Press, New York (1962) 261-394 Bamber, J.C., HiB, C.R, King, J.A., Acoustic properties of normal and cancerous human liver: II dependence on tissue structure, Ultrasound Med. Biol. 7 (1981) 135-144. FrizzeIL LA.. Ultrasonic heating of tissues. Ph.D. Thesis, University of’Rochester, New York (1975) Gammell, PM, Ix Croissette, D.H., Heyser, RC, Temperature and frequency dependence of ultrasonic attenuation in selected tissues, Ultrasound Med. Biol., 5(1979) 269-277 Miller, J.C, Yuhas, D.E., Mimbs, J.W., Dierker, S.B., Busse, LJ., Laterra, J.J., Weiss, A.N., SobeI, B.E., Ultrasonic tissue characterization: correlation between biochemical and ultrasonic indices of myocardial injury, Ultrasonics Symp. Proc. IEEE Cat. No. 76 CH1120-5SU (1976) 33-43 FrizzeB, L.A., Bamber, J.C., Effect of phase cancellation artefact on frequency dependence of ultrasonic attenuation measurements (to be submitted). FrizzeB, LA., Carstensen, E.L., Davis, J.D., Ultrasonic absorption in liver tissue, J. Acoust, Sot. Am, 65 (1979) 1309-1312. Bamber, J.C., Nassiri, D.K., Effect of gaseous inclusions on the frequency dependence of ultrasonic attenuation in liver, Ultrasonics (submitted for publication) Sandritter, W., Thomas, C., Kirsten, W.H., Colour atlas and textbook of macropathology, Ch. 6, Year book Medical Publishers, Chicago (1976) 139 Goss, S.A., FrizzeII, LA., Dunn, F., Frequency dependence of ultrasonic absorption in mammalian testis, J. Acoust. Sot. Am, 63 (1978) 1226-1229 Johnston, RL, Goss, Sk, Maynard, V., Brady, J.K., FrizzeB, LA., O’Brien, W.D. Jr., Dunn, F., Elements of tissue characterization: part I, ultrasonic propagation properties, in Ultrasonic tissue characterization II (Edited by M. Linzer) NBS Spec. Publ. 525, US Govt. Printing Office, Washington DC (1979) 19-27 Bamber, J.C., HiB, CR, Acoustic properties of normal and cancerous human liver: I, dependence on pathological condition, UltrasoundMed. BioZ. 7, (1981) 121-113
ULTRASONICS.
JULY 1981
attenuation
in fresh human tissues
Dear Sir, As a preliminary stage of a project’ designed to assess the usefulness of measurements of acoustic propagation properties for identifying pathology in human tissues, a series of measurements was made of the ultrasonic attenuation coefficient, as a function of frequency, of excised normal human tissues. Although some results of this early series of measurements have been presented previously23’ they are not easily available and have never been published in full. A brief discussion of these data, in the light of subsequent experience, may be of value to readers interested in making similar measurements. The measurement technique was basically that described previously by Chivers and HilIp with modifications to facilitate rapid automatic data collection and analysis.’ Reasonably detailed descriptions may also be found elsewhere. 596 Specimens of the organs of interest were obtained direct from autopsy of normal human subjects. Most of the measurements were made at room temperature with specimens immersed in saline and contained in a thin, taut, polythene bag. No special efforts were made to degas these preparations, other than palpation with the fingers to remove any visible signs of bubbles. Using analogue spectral analysis of very short acoustic pulses an average attenuation coefficient for 3 to 6 regions, chosen at random, within each specimen was obtained at 44 or more frequencies in the range 1 to 6 MHz. The average attenuation coefficient, 01,as a function of frequency, f,for each specimen was then fitted, by eye using double logarithmic scales, to the equation (Y= by. Values of the slope, m, and the intercept, b (that is, the value of (Yat 1 MHz), were finally averaged over similar tissue types (Table 1). The results for human spleen agree very welI with the one other data set with which they may be compared,’ and those for brain fall within the range of values found in the literature (see for example that reviewed by Kremkau et als). It is seen that the ratio of the average attenuation coefficient at 1 MHz for mostly white matter against a mixture of grey and white matter is 1.4. This value is comparable with the value of 1.7 obtained for a similar ratio by means of absorption measurements in pure white and pure grey matter,g and happens to be identical to an equivalent ratio for attenuation in human brain obtained by Kremkau et al.’ It has been noted’ that variation of water content provides a reasonably quantitative explanation for the differences between white and grey matter; an explanation that is consistent with results as a function of water content in liver. lo It is also seen that, while the values for spleen and brain are relatively tightly grouped, liver, for reasons unknown at the time, gave extremely variable results. The anomalous nature of ultrasonic properties of liver has since been noticed on a number of occasions,5~11~‘2 and appears now (possibly) to be related to a number of factors.’ These include relatively large spatial variations in the attenuation coefficient and propagation speed, the latter leading to varying degrees of 0041-624X/81/040187-02/$02.00 ULTRASONICS.
JULY 1981
excess attenuation and erratic frequency dependences due to phase cancellation,“13s14 and a tendency for gas bubbles to interfere with the measurement.15s16 Gas is possibly more likely to be present in liver than in specimens of other organs because of its highly vascular structure (gas may have been introduced at times after excision) and its tendency to produce gas during autolytic decay.5y17 Erratic results were also obtained from human stomach fat with regions of negative dependence on frequency often being observed and, since only six specimens were examined, mean values of b and m have not been computed. Phase cancellation at the receiver’33’4 is probably an important mechanism in producing these effects. The speed of sound in fat is variable and may be as much as 6% lower than the speed of sound in saline. Added to this, stomach fat has a very heterogeneous gross structure and the specimens were difficult to cut to a uniform thickness.
Table 1. Results of measurement of ultrasonic attenuation in freshly excised human tissues, expressed in terms of average values for the constants b and m in the equation (Y= bfm. The variations noted refer to the total range of values observed between specimens of the same organ.
Organ
Number of Specimens
Remarks
Spleen
4
None
5
f Brain
3
b[dB cm-‘]
m
Mixed grey and white matter
0.58 +_
+ 1.3_
12% 8%
Mostly white matter
0.8
+ -
5% 10%
Liver*
25
Resultsvariable and erratic
Stomach fat
6
Results extremely erratic (only range values given)
Testis
4
Values forb obtained by extrapolation of 3 - 7 MHz data
3%
+ 20% _ loy 0
+ 200% 1 _ 7oo/0
1.1
+ 110% 1_ 6oo/0
0.6 to 5.2
0.4 to 1.4
+ 47% 0.17 _ 41%
+ 20% 1.7 _ 26%
l More recent results using the same measurement technique but with precautions mentioned in the text yielded values b = 1.1 f 40% dB cm -‘I and m = 0.9 f 30% for specimens of normal human liver. 1 ,20 It is likely, however, that due to the influence of gas bubbles even these values are over estimates at low frequencies and posses an excessive variation from specimen to specimen16*”
0 1981 IPC Business Press 187
The attenuation of ultrasound in human testis was often, at the lower frequencies, too small to be measured with the apparatus employed. Values for b were therefore obtained by extrapolation of results obtained at higher frequencies (3 to 7 MHz). The results for human testis are consistent with the finding” that the absorption coefficient of testes from small mammals is much lower than values for other soft tissues, following the relationship cu, = 0.13 f” (dB cm-’ ). It would appear that low attenuation values in testis might be explained in terms of the extremely high water content and the low structural protein content of this organ.lg The above-noted erratic and variable results for liver and fat led to a series of investigations designed to assess the usefulness of autopsy material for this kind of study, the results of which have since been reported.‘ysy6 Selection of measurement sites for minimum phase cancellation artefact, the use of de-gassing procedures and general improvements in specimen handling techniques (for example, storage, cutting and measurement) have resulted in some reduction in the observed variation of the attenuation coefficient of human liver’F11720 (see caption to Table 1). The presence of gas in the specimens is probably the greatest single problem to be encountered in measurements of this kind. The nature of the effects of gas, and techniques for its removal, are subjects discussed elsewhere.159’6 I should like to acknowledge that many of the measurements reported here were made by M.J. Fry, assistance and advice were provided by F. Dunn and D. Nicholas, and the work was conducted while studying for a Ph.D. under the supervision of C.R. Hill. Yours faithfully J. C. Bamber Physics Division, Block F, institute of Cancer Research, Clifton Avenue, Sutton, Surrey SM2 5PX, UK Received 26 February 1981
3
4 5
6
I
8
9
10 11 12 13
14
15
16 17
18
19 References 1
2
188
Bamber, J.C., Ultrasonic characterization of structure and pathology in human soft tissues, Ph.D. Thesis, London University (1979) Bamber, J.C., Nicholas, D., Fry, M., Dunn, F., in British Biocoustics meeting (report by A.R. Williams), Lntrasound Med. Biol., 2 (1976) 357
20
Bamber, J.C., in Scientific basis of diagnostic ultrasound (meeting report by A. Hall), Hosp. P&s. Ass. Bull., (Dec. 1976) 14-18 Chivers, RC, HiII, C.R, Ultrasonic attenuation in human tissue. Ultrasound Med. Biol.. 2 (1915) 25-29 Ban&r, J.C., Fry, NJ., HiU,‘C’i, Du& F., Ultrasonic attenuation and backscattering by mammalian organs as a function of time after excision, Ultrasound Med. BioZ., 3 (1977) 15-20 Bamber, J.C, HiB, CR, Ultrasonic attenuation and propagation speed in mammalian tissues as a function of temperature, Ultrasound Med. Biol., 5 (1979) 149-157 Nicholas, D., Orientation and frequency dependence of backscattered energy and its clinical application, in Recent advances in ultrasound in biomedicine (Edited by D.N. White) 1 Research Studies Press, Oregon (1977) 29-54 Kremkau, F.W., McGraw, C.P., Barnes, RN., Attenuation and propagation speed in normal human brain, J. Acoust. Sot. Am (submitted for publication) Fry, W.J., Dunn, F., Ultrasound analysis and experimental methods in biological research, in Physical techniques in biological research, Ch. 4 Academic Press, New York (1962) 261-394 Bamber, J.C., HiB, C.R, King, J.A., Acoustic properties of normal and cancerous human liver: II dependence on tissue structure, Ultrasound Med. Biol. 7 (1981) 135-144. FrizzeIL LA.. Ultrasonic heating of tissues. Ph.D. Thesis, University of’Rochester, New York (1975) Gammell, PM, Ix Croissette, D.H., Heyser, RC, Temperature and frequency dependence of ultrasonic attenuation in selected tissues, Ultrasound Med. Biol., 5(1979) 269-277 Miller, J.C, Yuhas, D.E., Mimbs, J.W., Dierker, S.B., Busse, LJ., Laterra, J.J., Weiss, A.N., SobeI, B.E., Ultrasonic tissue characterization: correlation between biochemical and ultrasonic indices of myocardial injury, Ultrasonics Symp. Proc. IEEE Cat. No. 76 CH1120-5SU (1976) 33-43 FrizzeB, L.A., Bamber, J.C., Effect of phase cancellation artefact on frequency dependence of ultrasonic attenuation measurements (to be submitted). FrizzeB, LA., Carstensen, E.L., Davis, J.D., Ultrasonic absorption in liver tissue, J. Acoust, Sot. Am, 65 (1979) 1309-1312. Bamber, J.C., Nassiri, D.K., Effect of gaseous inclusions on the frequency dependence of ultrasonic attenuation in liver, Ultrasonics (submitted for publication) Sandritter, W., Thomas, C., Kirsten, W.H., Colour atlas and textbook of macropathology, Ch. 6, Year book Medical Publishers, Chicago (1976) 139 Goss, S.A., FrizzeII, LA., Dunn, F., Frequency dependence of ultrasonic absorption in mammalian testis, J. Acoust. Sot. Am, 63 (1978) 1226-1229 Johnston, RL, Goss, Sk, Maynard, V., Brady, J.K., FrizzeB, LA., O’Brien, W.D. Jr., Dunn, F., Elements of tissue characterization: part I, ultrasonic propagation properties, in Ultrasonic tissue characterization II (Edited by M. Linzer) NBS Spec. Publ. 525, US Govt. Printing Office, Washington DC (1979) 19-27 Bamber, J.C., HiB, CR, Acoustic properties of normal and cancerous human liver: I, dependence on pathological condition, UltrasoundMed. BioZ. 7, (1981) 121-113
ULTRASONICS.
JULY 1981