J Med Ultrasonics (2018) 45:3–13
https://doi.org/10.1007/s10396-017-0814-5

REVIEW ARTICLE

Attempt at standardization of bone quantitative ultrasoundin Japan
Takahiko Otani1 • Masao Fukunaga2 • Kosei Yho3 • Takami Miki4 •Kaoru Yamazaki5 • Hideaki Kishimoto6 • Mami Matsukawa1 • Nobuyuki Endoh7 •Hiroyuki Hachiya8 • Hiroshi Kanai9 • Saeko Fujiwara10 • Yoshinori Nagai11

Received: 11 May 2017 / Accepted: 3 August 2017 / Published online: 7 September 2017 The Japan Society of Ultrasonics in Medicine 2017

Abstract Dual X-ray absorptiometry (DXA) is used todiagnose osteoporosis. On the other hand, quantitative
ultrasound (QUS) is widely used to assess bone density as
part of medical screening as it is relatively inexpensive andeasy to perform. Current QUS devices do not share precise
ultrasound-related parameters, such as frequency, waveform, beam pattern, transient response, definition of propagation time, definition of degree of attenuation, andprecise measurement site, resulting in different measurements across models. The Japan Osteoporosis Society
established a QUS Standardization Committee in 2007 to& Takahiko Otani
totani@oyoe.jp
1

Faculty of Science and Engineering, Doshisha University,
Kyotanabe, Kyoto 610-0394, Japan

2

Kawasaki Medical School, Okayama, Japan

3

Aino Hospital, Osaka, Japan

4

Izumiotsu Municipal Hospital, Osaka, Japan

5

Department of Orthopedic Surgery, Iwata City Hospital,
Shizuoka, Japan

6

Department of Orthopedic Surgery, Nojima Hospital, Tottori,
Japan

7

Department of Electric, Electronics, and Information
Engineering, Faculty of Engineering, Kanagawa University,
Kanagawa, Japan

8

School of Engineering, Tokyo Institute of Technology,
Tokyo, Japan

9

Graduate Schools of Engineering and Biomedical
Engineering, Tohoku University, Miyagi, Japan

10

Health Management and Promotion Center, Hiroshima
Atomic Bomb Casualty Council, Hiroshima, Japan11

TM Clinical Support Co. Ltd., Tokyo, Japan

investigate standardization of speed of sound (SOS) andbroadband ultrasonic attenuation (BUA) measurements toresolve this issue. The committee came up with a formula
to convert SOS and BUA values yielded by each model
available in Japan. This has made it possible to convert
QUS measurements from different models into standardized values, greatly improving the effectiveness of QUS
measurements.
Keywords Quantitative ultrasound (QUS)  Speed ofsound (SOS)  Broadband ultrasonic attenuation (BUA) 
Standardization of QUS

Introduction
Speed of sound (SOS) (m/s) and broadband ultrasonicattenuation (BUA) (dB/MHz), parameters of quantitative
ultrasound (QUS) used to assess bone density (or bonemass), are highly correlated with bone density (mg/cm3)[or bone mass (mg/cm2)]. Therefore, QUS is widely used in
medical screening in Japan as it is compact, light, inexpensive, and free of exposure to radiation.
Measurement of bone mass (or bone mineral content)(mg/cm2) with dual X-ray absorptiometry (DXA) is currently used to judge increased fracture risk due to osteoporosis and other causes or to diagnose osteoporosis. Thus,
there are few opportunities to use QUS in medical
diagnosis.
Since the ultrasonic waves used in QUS devices areelastic waves, SOS and BUA measurements directly reflect
the elastic properties of bone. Therefore, they are importantparameters for assessing the elastic properties, i.e., themechanical strength, of bone. Given that assessment of
fracture risk, i.e., assessment of the mechanical strength of

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bone, is a critical component of diagnosis of osteoporosis, amethod for evaluating bone using QUS parameters (SOS
and BUA) holds promise. QUS devices are widely used forpreventive medical screening in Japan, but QUS measurements are not used in cross-sectional studies, and they
are not fully utilized in the diagnosis of osteoporosis. The
main reasons for this are the fact that DXA measurements
are considered the de facto diagnostic criteria for osteoporosis, and the fact that QUS devices have become
ubiquitous without a clear definition of QUS parameters(SOS and BUA) and their reference ranges. The calcaneus
is used as the measurement site with current QUS devices,
but the precise measurement site, precise definition of SOS
and BUA, and precise physical characteristics of theultrasonic signals used differ from manufacturer to manufacturer. Thus, the measurements displayed will differ frommanufacturer to manufacturer (or from model to model)
even if the subject is the same. Nevertheless, the correlation coefficients of the measurements across these models
are all high (good), suggesting that all of the models havebeen properly planned and manufactured.
Standardization of measurements of current QUS
devices is an essential step toward establishing thepotential of QUS devices for evaluating bone properties
and expanding the scope of their application. Against thisbackdrop, the Japan Osteoporosis Society established a
QUS Standardization Committee in 2007 to investigate
standardization of QUS parameters (SOS and BUA).
Some of the results of its investigation were reported in
Osteoporosis Japan [1].

Issues associated with evaluation of bone density
using QUS
The propagation speed of ultrasonic waves in a material
and the attenuation coefficient (Np/m) are physical constants that indicate the elastic properties of the material.
Such material physical constants are essential for studies
of materials such as metals, polymers, and ceramics, andfor quality control in the manufacturing process ofindustrial materials. Research on methods for determining
the propagation speeds and attenuation coefficients ofmaterials and the constants for each material beganaround the 1920s with advances in ultrasound technology.
This field of research, which is currently referred to as
ultrasonic material characterization, is an important fieldin condensed matter physics and material science. Many
results were reported for the propagation speeds andattenuation coefficients of biological tissues in the J.
Acoust. Soc. Am and other publications [2–7] from the
1950s to 1980s, and a wide range of research is still being
conducted today.

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Research began in the 1980s on bone characterization
utilizing the fact that there is a strong correlation betweenbone density and the propagation speed and attenuation ofultrasonic waves at sites including cancellous bone [8],resulting in the practical application of an ultrasound-based
method for diagnosing osteoporosis called quantitative
ultrasound. Parameters measured by QUS devices currently
available in Japan are SOS (m/s) and BUA (dB/MHz). SOS
and BUA have been reported by many researchers to correlate well with bone density (or bone mass) [9–19], andSOS and BUA are considered to be widely acceptedparameters for bone characterization. However, the sitewhere QUS parameters are measured, i.e., the propagation
path of the ultrasound beam, is connected to soft tissues,cortical bone, and cancellous bone in a complex configuration, and the ultrasonic beam reflects, refracts, scatters,
and diffracts repeatedly as it is transmitted through themediums. Thus, the SOS and BUA values of ultrasonicwaves transmitted through the body are greatly affected by
the frequency, beam pattern, and pulse waveform of theultrasonic waves. Moreover, the ultrasonic beam is affectedby the transducer material in the ultrasonic transmitter andreceiver, their configuration and size, their mechanicalresonance characteristics and electrical impedance characteristics, and other factors. Despite these issues with
QUS devices that are inherent in in vivo ultrasound measurements, the devices were marketed without clearly
indicating precise measurement sites, definitions of SOS
and BUA, and characteristics of the ultrasonic waves used.
All QUS devices currently on the market show a goodcorrelation with bone density (mg/cm3) or bone mass (mg/cm2) as measured by X-ray methods1, but there are deviations in measurements between models (between manufacturers), making it impossible to compare measurements
between QUS devices at the present time.

Preliminary investigation for QUS standardization
QUS devices that had been approved as medical devices inJapan and were available as of establishment of the QUS
Standardization Committee (October 2007) are shown in
Table 1. The manufacturers (distributers), models, andmeasuring parameters are shown in Table 1. According tothis table, the only QUS parameter that all models have incommon is SOS. In the present study, we first investigated
the standardization of SOS, which was then followed by an
examination of BUA.

1

In the case of X-ray methods, bone density (mg/cm3) is measured
by quantitative computed tomography (QCT), and bone mass (mg/cm2) is determined by dual X-ray absorptiometry (DXA).

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Table 1 QUS devices used instandardization study

5

Manufacturer or (distributor)

DeviceMeasuring parameters

Hitachi-Aloka Medical, Ltd.

AOS-100

SOS, TI, OSI, BUA

Furuno Electric Co., Ltd. (Canon Lifecare Solutions Inc.)

CM-200SOSGE Healthcare Japan, Co.

A-1000

SOS, BUA, StiffnessDMS S.A. (Diagnostic Medical Systems S.A.)UBIS5000

SOS, BUA, STI

Ishikawa Seisakusho, LTD. (NIHON KOHDEN CORPORATION)

Benus

SOS, Bone Area Ratio(NIPPON SIGMAX Co., Ltd.)

Minelyzer

SOS, BUA, BQI

ranging from 1548 to 1587 m/s. This indicated that eachmodel was designed with its own unique standards, but
the coefficient of variation values were all sufficiently
low, suggesting technically very well-made devices that
could be stably operated. However, the coefficient ofvariation is equal to standard deviation/mean value. In
Table 3, mean SOS values for the phantom are shown in
the left column, and mean SOS values for subjects areshown in the right column, in order of highest to lowest
value. Judging from this table, the order of the meanvalues for the phantom and the order of the mean values
for subjects do not agree. Therefore, Table 3 indicatesthat it is not appropriate to convert subject SOS values tostandardized SOS values using phantom SOS values asreference values.

At the 1st meeting (October 13, 2007) of the QUS
Standardization Committee, we took the opportunity tomeasure SOS values using five of the models shown in
Table 1 that we were able to arrange, with 22 committee
members in attendance serving as subjects. An in-house
phantom (equipment number: S/N133) used for calibrating SOS values provided by Furuno Electric Co., Ltd. wasalso measured five times with each model. Figure 1 shows
the SOS values for the 22 subjects in order of subject
number. SOS values differed considerably from model tomodel, but the measurements for all models showed very
similar tendencies, suggesting a high correlation coefficient for SOS values between models. The results ofmeasurement of phantom S/N133 are shown in Table 2.
Each model exhibited its own SOS value, with values

Fig. 1 Preliminary
measurements forstandardization (measurement
results for 22 subjects; October
13, 2007; room temperature:
26 C)

Table 2 Measurement resultsfor phantom (October 31, 2007;
room temperature: 26 C;number of models: 5)

SOS

AOS-100

CM-200A-1000UBIS5000

Benus

Mean (m/s)

1549.41551.41565.01581.01568.2

Maximum (m/s)

1551

1552

1574

1587

1572

Minimum (m/s)

1548

1551

1562

1575

1566

Standard deviation (m/s)

1.517

0.548

5.050

5.339

2.387

CV (%)

0.098

0.035

0.323

0.338

0.152

Phantom: Furuno Electric (S/N 133)
CV coefficient of variation, standard deviation/mean value
CV (%) percent of the CV value

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Table 3 Order of SOS mean values for phantom and subjects

Fig. 2 Age distribution ofsubjects

Causes of differences in SOS values
between models
Normally, the precise method for measuring SOS values
and the procedure for deriving SOS values from transmitted ultrasonic waves (computational procedure and algorithm) are not generally made public for any of the
products. Some possible reasons why SOS values differ
from model to model despite measurement of the samephantom or the same subject are as follows:a.

Differences in the definition of SOS: The definition of
SOS has not been standardized, with the following
three definitions in use:
•
•
•

b.

Calcaneus velocity
Heel velocity including soft tissue
Propagation velocity between transmitting andreceiving transducers

Differences in measurement method of transmit time,i.e., signal processing method of transmitted waves:
When measuring propagation time, the time will differ
and the propagation velocity will change depending onwhether the first apparent deviation from baseline, thefirst zero-crossing, or a fixed threshold is used as thefirst arrival point.

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c.

d.

Differences in measurement site with each model:
Individual differences in the calcaneus contour, size,
and internal structure in each subject result in changes
in the propagation path, which affect the measurement.
Ultrasonic characteristics of each model and differences in waveform processing method: Differences in
the acoustic field characteristics, transient response, or
resonance characteristics of the ultrasonic transmitterand receiver for each model result in differences in
SOS values between devices.

Thus, there are many underlying factors for the ‘‘deviations’’ in SOS values between models, making it impossible to define a standard SOS at the present time.
According to Table 2, however, the correlation coefficient
between each model appears to be quite good; therefore, it
was determined that it would be possible to statisticallyestablish a standardized SOS.
In addition, slight changes (several percent) in QUS
measurements can be seen from measurement to measurement even in cases where the same subject is measured
with the same QUS device, but this is caused by changes in
the propagation path of ultrasonic waves in response to
local changes in the calcaneus contour and its internal
structure, resulting in a QUS value that faithfully reflects
the bone density and trabecular structure of cancellous

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Table 4 Baselinecharacteristics

Male

FemaleMean ± SD

Max.

Min.

Mean ± SD

Max.

Min.

Age (years)

45.9 ± 13.9

85

2350.2 ± 20.6

83

16

Height (cm)170.0 ± 6.5

186

151

155.2 ± 6.3

169

138

Body weight (kg)67.5 ± 9.0

954851.9 ± 7.3

7334

BMI (kg/m2)

23.3 ± 2.7

31.0

17.4

21.6 ± 2.9

30.7

15.7

BMI body mass index
Body weight (kg)BMI ¼
Height (m)2
Table 5 SOS correlation
coefficients between models(p \ 0.0001)

AOS-100

CM-200A-1000

AOS-100

1

CM-2000.82

A-1000

0.87

0.88

1

UBIS5000

0.83

0.85

0.84

UBIS5000

Benus

1
1

Benus

0.73

0.75

0.76

0.68

1

Minelyzer

0.83

0.75

0.86

0.79

0.68

bone at the site of ultrasonic propagation. Changes inmeasurements in the same subject are information related
to the internal structure of the subject’s bone, and it isreasonable to regard the changes as information that serves
as a clue for evaluating bone properties, rather than treatingthem as errors.

QUS standardization
Measurements for QUS standardization
With the cooperation of members participating in the 9th
Annual Meeting of Japan Osteoporosis Society (November
14–16, 2007), QUS measurements were taken in 124 men
and 75 women, and with the cooperation of participants ina public lecture (educational campaign by the Japan
Osteoporosis Society aimed at the general population)(January 17, 2008) in Osaka by the Osteoporosis Network,
QUS measurements were taken in 18 men and 64 women.
For QUS devices, all models approved as medical
devices in Japan (six models in 2007) were arranged withthe cooperation of the manufacturers and distributors. SOS
values for all subjects (volunteers) were measured with allmodels (six models), and BUA measurements were also
taken at the same time for the four models capable ofmeasuring BUA.
The total number of subjects (volunteers) was 281, but
the number of subjects in whom it was possible to measure
SOS with all six models was 232 subjects (122 men, 110

Minelyzer

1

women). The age distribution of the 281 subjects is shownin Fig. 2, and baseline characteristics are shown in Table 4.
Pearson’s correlation coefficient (r) was high in all six
models, i.e., 0.68–0.88 (Table 5). The correlation coefficient between models was high, i.e.,[0.8 (0.82–0.88), forfour of the six models. Based on the investigation by the
QUS Standardization Committee, it was decided to use themean SOS for each subject measured with the four models
with a high correlation coefficient (AOS-100, CM-200,
A-1000, UBIS5000) as the reference value (reference
SOS). The reference SOS for each subject has beenarranged in ascending order from lowest to highest to show
it as a solid black line in Fig. 3, and the SOS values foreach model corresponding to this value are also shown.
There is a difference between the measured SOS values foreach of the models and the reference SOS, but we can see
from Fig. 3 that there is a good correlation (correlation
coefficient) with the reference SOS.
Derivation of standardized SOS
The results of regression analysis of SOS measured witheach model and the reference SOS (mean of four reference models) are shown in Fig. 4. With the reference SOS
on the vertical axis and SOS measured with each modelon the horizontal axis, the regression line and regressionfunction are shown in the figure. It indicates that thecorrelation coefficient, r, is high, i.e., 0.87–0.96. Standard
major axis regression analysis was used for regression
analysis [20]. Measurements yielded by each model can

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Fig. 3 Subject measurement
results for SOS standardization.
The mean SOS for four models
with a high correlation
coefficient has been arranged asa ‘‘reference SOS’’ in ascendingorder from lowest to highest,
and the measured SOS values
for each model are also shown

Fig. 4 Results of regression
analysis of the reference SOS
and the measured SOS values
for each model (p \ 0.0001)(regression analysis: standard
major axis regression analysis)

be converted to a standardized SOS using this regressionfunction. The formulas for converting the SOS measured
by each model (x) to the standardized SOS (y) are summarized in Table 6. The results of regression analysis of
this standardized SOS and reference SOS are shown in
Fig. 5. The regression function satisfies y = x for themost part for all of the models. The results after
employing the same method in Fig. 3 are shown in Fig. 6,
arranging the measured SOS after conversion and reference SOS in ascending order. We can see that good
adjustment has been achieved with the standardization
conversion formula (Table 6).
Summary of standardized SOS
Standardization was attempted for six QUS models currently available in Japan (QUS devices approved as

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Table 6 Conversion formulas between standardized SOS and measured SOS for each QUS device
AOS-100

y = 1.179x - 308.0 (m/s)

CM-200y = 0.863x ? 220.2 (m/s)

A-1000y = 0.789x ? 298.0 (m/s)

UBIS5000

y = 1.031x ? 3.6 (m/s)

Benus

y = 1.395x - 636.7 (m/s)

Minelyzer

y = 2.000 x - 1504.7 (m/s)

y standardized SOS (s-SOS)
x measured SOS

medical devices in Japan, 2007), from which was derived aformula for converting SOS to standardized SOS (s-SOS)(Table 6). The correlation coefficient, r, between s-SOS
yielded by the conversion formula and the reference SOS(mean of four models) is sufficiently high, i.e., 0.87–0.96.

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9Fig. 5 Results of regression
analysis of the reference SOS
and the standardized SOS foreach model (p \ 0.0001)(regression analysis: standard
major axis regression analysis)Fig. 6 Subject measurement
results for standardized SOS.
The mean SOS (reference SOS)
has been arranged in ascendingorder from lowest to highest,
and the standardized SOS foreach model is also shown

This high correlation coefficient indicates that QUS devices are very well-made devices. The method for establishing this s-SOS described in this section is based on themethod used to derive the standardized bone mineraldensity (s-BMD) proposed in the 1990s by the International
Dual-photon X-ray Absorptiometry (DXA) Standardization
Committee [21, 22].
Derivation of standardized BUA
In the case of attenuation of ultrasonic waves transmitted
through the calcaneus, it is known that the degree ofattenuation (dB) increases almost linearly relative to frequency (MHz) in the frequency range of 0.2–0.8 MHz.
This rate of increase in the degree of attenuation relative tothe frequency is referred to as broadband ultrasonic attenuation (BUA) (dB/MHz) and is used to evaluate bonedensity [8, 23, 24]. Like SOS, there is a considerable

difference in BUA measurements from model to model as
the measurement conditions differ for each model, but like
SOS, the correlation coefficient between models is good,i.e., about 0.8.
Of the six QUS models available in Japan, four werecapable of measuring BUA: AOS-100, A-1000, UBIS5000,
and Minelyzer. BUA values of subjects were measured
with each model when the above-mentioned SOS values
were measured. Therefore, the subjects were the same as

Table 7 BUA correlation coefficients between models (p \ 0.0001)
AOS-100

A-1000UBIS5000

AOS-100

1

A-10000.75

1

UBIS5000

0.84

0.79

1

Minelyzer

0.79

0.69

0.78

Minelyzer

1

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Fig. 7 Subject measurement
results for BUA standardization.
The mean BUA for threereference models has beenarranged as a ‘‘reference BUA’’in ascending order from lowest
to highest, and the measured
BUA for each model are also
shown

Fig. 8 Results of regression
analysis of the reference BUA
and the measured BUA values
for each model (p \ 0.0001)(regression analysis: standard
major axis regression analysis)

those who went SOS measurement, with their age distribution shown in Fig. 2 and baseline characteristics inTable 4.
Correlation coefficients for six combinations of two of
the four models calculated using the measured BUA are
shown in Table 7. As shown in the table, correlation
coefficients were distributed within the range of 0.69–0.84.

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Of the four models that were highly correlated in thestandardization of SOS (AOS-100, CM-200, A-1000,
UBIS5000), three models (AOS-100, A-1000, UBIS5000)
were capable of measuring BUA. Since the correlation
between the BUA values measured with these three models
was also relatively good (Table 7), the mean of the BUA
values measured with these three models was used as the

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Table 8 Conversion formulas between standardized BUA and measured BUA for each QUS device
AOS-100

y = 0.6318x ? 38.47 (dB/MHz)

A-1000y = 0.8461x - 13.11 (dB/MHz)UBIS5000

y = 2.1587x - 54.74 (dB/MHz)

Minelyzer

y = 0.7081x ? 28.57 (dB/MHz)y standardized BUA (s-BUA)
x measured BUA

reference value (reference BUA). This reference BUA isillustrated in Fig. 7 arranged from lowest to highest. The
BUA values for each model corresponding to the reference
BUA are also shown in Fig. 7. As was the case with SOS(Fig. 3), we can see that there is a good correlation between
each model’s BUA and the reference BUA. The results ofregression analysis (standard major axis regression analysis) of the reference BUA and BUA measured with eachmodel are shown in Fig. 8 and Table 8. Using the conversion formula shown in Table 8, BUA measured witheach model can be converted to a standardized BUA (sBUA). The results of regression analysis of s-BUA andreference BUA are shown in Fig. 9. The reference BUA
has been arranged in ascending order from lowest to
highest in Fig. 10, and the s-BUA for each model corresponding to this value are also shown. We can see that
good adjustment has been achieved for the most part withthe s-BUA conversion formula.
Summary of standardized BUA
After standardization of SOS, a conversion formula forstandardization of BUA was derived using the same
method as that for SOS standardization. The correlation
coefficient between s-BUA obtained with the BUA standardization conversion formula and the reference BUA(mean BUA of three models) was 0.80–0.95, which was
sufficiently high. We can see that the QUS devices are very
well-made devices.

Fig. 9 Results of regression
analysis of the reference BUA
and the standardized BUA(p \ 0.0001) (regression
analysis: standard major axis
regression analysis)

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Fig. 10 Subject measurement
results for standardized BUA.
The mean BUA (reference
BUA) has been arranged inascending order from lowest to
highest, and the standardized
BUA for each model is also
shown

Conclusion of QUS standardization
Standardization was attempted for six QUS models currently available in Japan (QUS devices approved as medical devices in Japan). This effort yielded a conversion
formula for converting SOS and BUA measured with eachmodel to s-SOS and s-BUA, respectively. In the case of
SOS, the correlation coefficient between s-SOS yielded by
the conversion formula and the reference SOS (mean offour reference models) was sufficiently high, i.e.,
0.87–0.96. In the case of BUA, as well, the correlation
coefficient between s-BUA yielded by the conversion formula and the reference BUA (mean of three reference
models) was sufficiently high, i.e., 0.80–0.95. These s-SOS
and s-BUA conversion formulas appear to yield a relationship that sufficiently stands up to comparison of measurements between models. It should be noted, however,that s-SOS and s-BUA do not indicate SOS and BUA at a
specific site based on a specific definition. Moreover, theconversion formulas are only valid for the models andmeasurement site investigated in this study. Phantoms used
to confirm the operation of the QUS devices cannot be used
for the conversion of indicated values between different
models or for conversion into s-SOS and s-BUA. When
any new QUS device becomes available for clinical measurement, it will be necessary to perform clinical measurements for the new model using the reference models inthis study and calculate a formula for conversion to s-SOS
and s-BUA by means of regression analysis.
Acknowledgements We wish to express our gratitude to Mr. Kaoru
Horii (OYO Electric Co., Ltd.), who helped process an enormous
amount of data in this study of QUS standardization.
Compliance with ethical standards
Ethical statements All procedures followed were in accordance withthe ethical standards of the responsible committee on human123

experimentation (institutional and national) and with the Helsinki
Declaration of 1964 and later versions.
Conflict of interest The authors declare that there is no conflict ofinterest.
Informed consent Informed consent was obtained from all subjects(volunteers) for being included in the study.

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