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Quantitative ultrasound (qus) at the calcaneus and hand phalanges in polish healthy postmenopausal women
Ultrasound in Med. & Biol., Vol. 27, No. 3, pp. 373–377, 2001 Copyright © 2001 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/01/$–see front matter
PII: S0301-5629(00)00340-9
● Original Contribution QUANTITATIVE ULTRASOUND (QUS) AT THE CALCANEUS AND HAND PHALANGES IN POLISH HEALTHY POSTMENOPAUSAL WOMEN WOJCIECH PLUSKIEWICZ and *BOGNA DROZDZOWSKA Department & Clinic of Internal Diseases, Allergology, and Clinical Immunology, *Department of Pathomorphology, Silesian School of Medicine, Katowice, Poland (Received 7 July 2000; in final form 16 October 2000)
Abstract—In a cross-sectional study, 109 postmenopausal, healthy women, mean age 58.8 years, were studied. The aim of the study was to compare quantitative ultrasound (QUS) performed at two measurement sites of the same persons (correlations between parameters studied, age, and years since menopause (YSM)-related changes, influence of body size). Bone status was established using measurements at the calcaneus by Achilles (Lunar, USA), which measures speed of sound (SOS [m/s], CV% ⴝ 0.22%), broadband ultrasound attenuation (BUA [dB/MHz], CV% ⴝ 1.8%), stiffness index (SI [%], CV% ⴝ 1.3%), and by DBM Sonic 1200 (Igea, Italy), which measures amplitude-dependent speed of sound (Ad-SoS [m/s], CV% ⴝ 0.64%) at the hand phalanges. Mean and SD values were: SOS ⴝ 1498 ⴞ 24.8 m/s, BUA ⴝ 104.6 ⴞ 9.4 dB/MHz, SI ⴝ 69.2 ⴞ 12.3%, Ad-SoS ⴝ 1879 ⴞ 90.1 m/s. Age- and YSM-related changes were as follows: age-SOS r ⴝ ⴚ0.37, p < 0.0001, age-BUA r ⴝ ⴚ0.33, p < 0.001, age-SI r ⴝ ⴚ0.36, p < 0.001, age-Ad-SoS r ⴝ ⴚ0.62, p < 0.00001, YSM-SOS r ⴝ ⴚ0.27, p < 0.01, YSM-BUA r ⴝ ⴚ0.32, p < 0.001, YSM-Ad-SoS r ⴝ ⴚ0.44, p < 0.00001, YSM-SI r ⴝ ⴚ0.29, p < 0.01. In stepwise, multiple regression analyses of ultrasound parameters on age, YSM, height, and weight, the following equations were obtained: SOS [m/s] ⴝ 1564.9 ⴚ 1.1 ⴛ age [y], r ⴝ ⴚ0.37, p < 0.0001; BUA [dB/MHz] ⴝ 88.7 ⴙ 0.28 ⴛ weight [kg] ⴚ 0.36 ⴛ YSM [y], r ⴝ ⴚ0.51, p < 0.00001; SI [%]) ⴝ 79.2 ⴚ 0.5 ⴛ age [y] ⴙ 0.28 ⴛ weight [kg], r ⴝ ⴚ0.47, p < 0.00001; Ad-SoS [m/s] ⴝ 2287 to 6.9 ⴛ age [y], r ⴝ ⴚ0.62, p < 0.00001. In conclusion, QUS at the calcaneus and hand phalanges express similar trends in skeletal changes due to aging and the postmenopausal period, although measurements at the phalanges seem to be more sensitive for detecting bone changes, due to faster decrease rate of the Ad-SoS value than calcaneal measurements. (E-mail: [email protected]) © 2001 World Federation for Ultrasound in Medicine & Biology. Key Words: Quantitative ultrasound, Calcaneus, Phalanges, Women, Normal.
a good predictor of bone strength, but there are also other risk factors for osteoporotic fractures. Damaged microarchitecture or loss of elasticity are examples of the importance of qualitative features of bone tissue (Einhorn 1993; Melton and Riggs 1986). In the diagnosis of osteoporosis, necessity of using methods which are able also to detect quality of bone tissue is obvious. Some studies showed that quantitative ultrasound may provide additional information regarding bone quality (Kaufman and Einhorn 1993; Langton and Evans 1994; Langton et al. 1984). This method does not rely on ionizing radiation and is relatively cost-effective. More recently, some newer ultrasound devices that measure other skeletal sites have been developed. One of the most frequently evaluated is measurements of the hand phalanges using Italian device DBM Sonic 1200 (Igea, Carpi). In many studies, this machine proved its ability to express bone
INTRODUCTION Osteoporosis is a major health problem, because of individual and social costs connected with fractures and their late consequences. Any amelioration of the impact of osteoporosis depends on a reduction of its attendant fractures (Johnston et al. 1997). Bone mineral density accounts for 75% to 85% of the variance in the ultimate strength of bone tissue (Melton et al. 1988). Because bone strength is an important determinant of fracture susceptibility, along with the likelihood of sustaining sufficient trauma, it follows that bone mass measurement is also correlated with fracture risk in patients (Ross et al. 1990). Bone density is
Address correspondence to: Wojciech Pluskiewicz, M.D., Silesian School of Medicine, Department & Clinic of Internal Diseases, Allergology, and Clinical Immunology, 41-800 Zabrze, ul.3 Maja 13/15, Poland. E-mail: [email protected] 373
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Table 1. Clinical characteristics of group studied age (years)
Weight (kg)
Height (m)
BMI (kg/m2)
YSM (years)
SOS (m/s)
BUA (dB/MHz)
SI (%)
Ad-SoS (m/s)
58.8 ⫾ 8.1
69.1 ⫾ 13.3
1.57 ⫾ 0.06
28.0 ⫾ 5.2
10.4 ⫾ 7.9
1498 ⫾ 24.8
104.6 ⫾ 9.4
69.2 ⫾ 12.3
1879 ⫾ 90.1
changes during growth (Halaba and Pluskiewicz 1997), due to some therapeutic interventions (Pluskiewicz and Nowakowska 1997; Pluskiewicz and Drozdzowska 1998), age- and postmenopause-related changes (Pluskiewicz and Drozdzowska 1998; Ventura et al. 1996). The aim of the current study was to compare QUS at two various skeletal sites in regard to age- and years since menopause-related changes, to evaluate correlations between parameters studied, and the influence of body size. MATERIALS AND METHODS In the study, 109 healthy postmenopausal women, mean age 58.8 years, age range 35 to 79, were studied. All were recruited from patients referred to Outpatient Osteoporotic Clinic on bone status evaluation in years 1995 to 1999. In all subjects, no medical conditions affecting bone metabolism (chronic diseases or medications) were noted. None of persons studied prior and during measurements was on treatment for osteoporosis, including hormone replacement therapy, bisphosphonates, and calcitonin. No fractures occurred in the group studied. All women had natural menopause. Clinical characteristics are shown in Table 1. Informed consent was obtained from all subjects and the study was approved by the local ethics committee. Bone status was assessed by two quantitative ultrasound methods. Calcaneus was measured by Achilles (Lunar, USA), and distal metaphyses of II to V proximal phalanges of the hand were measured by DBM Sonic 1200 (Igea, Italy). In all individuals, the right (dominant) side was measured. All measurements were done by the same person. The ultrasound system for heel measurement consists of two unfocused transducers, of 2.54-cm diameter, mounted coaxially about 3.5 cm apart. Acoustic readings were accomplished by submerging the transducer pair and the heel into a 35°C water bath containing a skinwetting surfactant. Achilles measures speed of sound (SOS [m/s]) and broadband ultrasound attenuation (BUA [dB/MHz]). A third variable, the stiffness index, (SI [%]) was also determined. It is a combination of SOS and BUA and is calculated as follows: SI ⫽ 0.67 ⫻ BUA ⫹ 0.28 ⫻ SOS-420. Coefficients of variation (CV%) were: 0.22% for SOS, 1.8% for BUA, and 1.3% for SI.
Bone status at the hand was assessed by a device consisting of two probes mounted on an electronic caliper. The emitter probe positioned on the medial surface of the measured phalanx generates a single period at 1.25 MHz every 128 s. The receiver probe is positioned on the lateral side of the phalanx and obtains the ultrasound that has crossed the phalanx. The time interval between emission and reception of the ultrasound signal was measured and expressed in m/s. We determined the speed of sound in the distal metaphyses of the proximal phalanges of the second through fifth digits of the dominant hand. The speed of sound in bone was calculated using the first signal with an amplitude of more than 36 pixels on the screen. Thus, the measured speed of sound was dependent on signal amplitude (amplitude-dependent speed of sound–Ad-SoS [m/s]). Acoustic coupling was achieved using a standard ultrasound gel. CV% was 0.64%. STATISTICS All statistical analyses were performed using Statistica for Windows. Relationships between parameters studied were established using Pearson’s coefficients of correlation. Influence of age, years since menopause (YSM), and body size on ultrasound variables was evaluated using multiple, stepwise regression analysis. RESULTS Mean values of ultrasound parameters are presented in Table 1. Correlation analysis showed significant relationships between measured variables. The strongest coefficient of correlation was noted, as was expected, between BUA and SOS (r ⫽ 0.74, p ⬍ 0.00001). Ad-SoS correlated with SOS (r ⫽ 0.54, p ⬍ 0.00001) and BUA (r ⫽ 0.49, p ⬍ 0.00001) and SI (r ⫽ 0.55, p ⬍ 0.00001). Table 2 presents correlations and regressions of age and YSM with ultrasound parameters. As shown, phalangeal Ad-SoS presents a faster decrease rate than calcaneal parameters both for age- and YSM-related changes, but negative, significant trends are similar for both measurement sites. In Figures 1– 4, these relationships are shown for SOS and Ad-SoS (dotted lines represent 95% confidential of regression). In stepwise, multiple regression analyses of ultrasound parameters on age, YSM, height and weight, the following equations were obtained: SOS
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Table 2. Correlations and regressions of ultrasound values with age and YSM Linear regression equation
r
p
SOS ⫽ 1565.9 ⫺ 1.14 ⫻ age BUA ⫽ 127.2 ⫺ 0.38 ⫻ age SI ⫽ 101.2 ⫺ 0.55 ⫻ age Ad-SoS ⫽ 2287 ⫺ 6.9 ⫻ age
⫺0.37 ⫺0.33 ⫺0.36 ⫺0.62
⬍ 0.0001 ⬍ 0.001 ⬍ 0.001 ⬍ 0.000001
SOS ⫽ 1506.8 ⫺ 0.86 ⫻ YSM BUS ⫽ 108.6 ⫺ 0.38 ⫻ YSM SI ⫽ 74.0 ⫺ 0.46 ⫻ YSM Ad-SoS ⫽ 1932 ⫺ 5.0 ⫻ YSM
⫺0.27 ⫺0.32 ⫺0.29 ⫺0.44
⬍ 0.01 ⬍ 0.001 ⬍ 0.01 ⬍ 0.00001
[m/s] ⫽ 1564.9 ⫺ 1.1 ⫻ age [y], r ⫽ ⫺0.37, p ⬍ 0.0001; BUA [dB/MHz] ⫽ 88.7 ⫹ 0.28 ⫻ weight [kg] ⫺ 0.36 ⫻ YSM [y], r ⫽ ⫺0.51, p ⬍ 0.00001; SI [%] ⫽ 79.2 to 0.5 ⫻ age [y] ⫹ 0.28 ⫻ weight [kg], r ⫽ ⫺0.47, p ⬍ 0.00001; Ad-SoS [m/s] ⫽ 2287 ⫺ 6.9 ⫻ age [y], r ⫽ ⫺0.62, p ⬍ 0.00001. In stepwise, multiple regression analyses, both SOS and Ad-SoS are significantly dependent only on age, while BUA is a function of weight (positively), and YSM (negatively) and SI depends on age (negative influence) and weight (positive influence).
Fig. 2. Simple linear regression between age and Ad-SoS.
In our study, ultrasound measurements were performed in two skeletal sites. The calcaneus is almost purely trabecular bone and weight-bearing. Hand phalanges consist of both trabecular and cortical bone and are not weight-bearing bones. Measurements in such different sites of the skeleton performed in the same person allow comparison of how various ultrasound methods determine bone status. As was mentioned in Introduction section, several studies showed the ability of QUS in both sites to reveal changes of bone tissue due
to growing, aging, postmenopause, or some medications. Calcaneus measurements have recently received a list of excellent reviews (Gregg et al. 1997) and achieved fixed position in the diagnosis of osteoporosis. Phalangeal ultrasound measurements are merely 7 years under investigation. In many studies, an ability of the method to express bone tissue features/changes are proved (Alenfeld et al. 1998; Cardenas et al. 1997; Halaba and Pluskiewicz 1997; Joly et al. 1999; Pluskiewicz and Nowakowska 1997; Pluskiewicz and Drozdzowska 1998; Ventura et al. 1996). Phalangeal ultrasound measurements were also used for evaluation of a child population (Halaba and Pluskiewicz 1997), that was much easier to perform than using calcaneal measurements (Jaworski et al. 1995). Current study showed that, despite partly different skeletal function and trabecular/cortical ratio in measured bones, ultrasound parameters obtained showed similar trends in age- and YSM-related changes. In our cross-sectional studies recently published, we investigated age- and YSM-related
Fig. 1. Simple linear regression between age and SOS.
Fig. 3. Simple linear regression between YSM and SOS.
DISCUSSION
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Ultrasound in Medicine and Biology
Fig. 4. Simple linear regression between YSM and Ad-SoS.
changes in female populations separately for calcaneus (Pluskiewicz 1998) and hand phalanges (Pluskiewicz and Drozdzowska 1998). In 712 healthy postmenopausal women (mean age 59.5 years), SOS and BUA decreased significantly with age (r ⫽ ⫺0.38, r ⫽ ⫺0.36, respectively) and with YSM (r ⫽ ⫺0.35, r ⫽ ⫺0.33, respectively), which is very close to data obtained in the current study. Some others authors also assessed these relationships at the calcaneus, and the following results were obtained: age-SOS– 0.44, age-BUA– 0.45, YSM-SOS– 0. 56, YSM-BUA– 0.52 (Cepollaro et al. 1995), age-SOS– 0.66, age-BUA– 0.56, YSM-SOS– 0.63, YSM-BUA– 0.5 (Schott et al. 1993). General trends of changes in these studies are similar to our results. In our study performed in 398 healthy women (mean age 53.4 years), Ad-SoS decreased significantly with age and YSM (r ⫽ ⫺0.40, r ⫽ ⫺0.44, respectively) (Pluskiewicz and Drozdzowska 1998). The difference in age-related changes in our previously published and current studies may be explained by the difference in mean age and age range of currently studied women. Agerelated changes in Ad-SoS values were also evaluated by other authors. Alenfeld et al. (1998) obtained r ⫽ ⫺0.73. The same value is given by Duboef et al. (1996), while Joly et al. (1999) noted a slightly lower value of r ⫽ ⫺0.59. Coefficient of correlation between age and AdSoS obtained in the current study (r ⫽ ⫺0.62) is close to data given by other authors. Also, our relationship of Ad-SoS-YSM with r ⫽ ⫺0.44 is comparable to other results: r ⫽ ⫺0.31 (Duboef et al. 1996), r ⫽ ⫺0.38 (Joly et al. 1999), and r ⫽ ⫺0.42 (Ventura et al. 1996). Data from others studies confirm a faster rate of Ad-SoS decline with age than calcaneal ultrasound parameters. We hypothesize that some features of bone tissue (microstructure, elasticity, etc.) may play a role in bone loss, and only more sophisticated or invasive techniques may help to explain results obtained with the use of ultra-
Volume 27, Number 3, 2001
sound measurements. It may be suggested that, due to faster rate of decrease in phalangeal ultrasound parameter than for calcaneal ultrasound parameters, Ad-SoS is more sensitive for detecting age-related bone loss. In some other studies, measurements of phalangeal Ad-SoS and calcaneal parameters obtained by Achilles were presented. Coefficient of correlation given by other authors (Alenfeld et al. 1998) between Ad-SoS and SOS was very close to our result (0.5 vis 0.54); however, in that study, no significant correlation between Ad-SoS and BUA was obtained. In other study (Joly et al. 1999), both calcaneal and hand ultrasound measurements were also performed, but the authors did not provide correlations between them. Interesting information was provided by stepwise, multiple regression analysis of ultrasound parameters on age, YSM, and body size. Both SOS and Ad-SoS are related only to age, while BUA and stiffness index are positively influenced by weight. It is difficult to compare current correlations between body size and ultrasound values with data given by other authors, because in our study, stepwise multiple regression analyses were performed, while in other studies, simple linear correlations were assessed. Alenfeld et al. (1998) have found positive, significant dependence between Ad-SoS and weight (r ⫽ 0.4) and height (r ⫽ 0.23). Also, in the study by Ventura et al. (1996), some correlations of Ad-SoS with body size were obtained. Positive influence of weight on BUA and SI (not on SOS) may be explained by the fact that these parameters express features of weight-bearing bone. As expected, Ad-SoS measured in non-weight-bearing bones does not depend on weight. Thus, calcaneal SOS and Ad-SoS express similar relationships with weight. Both parameters are related to elasticity of bone tissue (Njeh et al. 1997). CV percent obtained for ultrasound parameters are in the same range as given by other authors. Precision of Ad-SoS measurements in other studies ranged from 0.52% to 0.91% (Alenfeld et al. 1998; Joly et al. 1999) vs. our precision of 0.64%. Also, precision of calcaneal measurements was comparable to other studies. Limitations of our study were: cross-sectional study design, relatively small group studied, and lack of analysis of individuals having fractures. Despite these limitations, it can be concluded that QUS at the calcaneus and hand phalanges express similar trends in skeletal changes due to aging and postmenopausal period, although measurements at the phalanges seem to be more sensitive for detecting bone changes due to faster decrease rate of Ad-SoS value than calcaneal measurements. The study allowed comparison of data obtained using two different machines measuring two skeletal sites in the same sample. Such comparison pro-
QUS in postmenopausal women ● W. PLUSKIEWICZ and B. DROZDZOWSKA
vides better possibility to analyze relationships between ultrasound parameters and age, YSM, and body size than data obtained separately for each device in a different study group. Further investigations, especially longitudinal studies in greater populations, are necessary. REFERENCES Alenfeld FE, Wuster C, Funck C, et al. Ultrasound measurements at the proximal phalanges in healthy women and patients with hip fracture. Osteopor Int 1998;8:393–398. Cardenas J, Revilla M, Hernandez ER, et al. Comparison of three bone densitometry methods in osteoporotic women. Calcif Tissue Int 1997;61:358 –361. Cepollaro C, Agnusdei D, Gonelli S, et al. Ultrasonic assessment of bone in normal Italian males and females. Br J Radiol 1993; 68:910 –914. Duboef F, Hans D, Schott AM, et al. Ultrasound velocity measured at the proximal phalanges: Precison and age-related changes in normal females. Rev Rhum 1996;63:427– 434. Einhorn TA. Bone strength: The bottom line. Calcif Tissue Int 1992; 51:331–339. Gregg EW, Kriska AM, Salamone LM, et al. The epidemiology of quantitative ultrasound: A review of the relationships with bone mass, osteoporosis and fracture risk. Osteopor Int 1997;7:89 –99. Halaba Z, Pluskiewicz W. The assessment of development of bone mass in children by quantitative ultrasound through the proximal phalanxes of the hand. Ultrasound Med Biol 1997;23:1331–1335. Jaworski M, Lebiedowski M, Lorenc RS, Trempe J, et al. Ultrasound bone measurement in pediatric subjects. Calcif Tissue Int 1995; 56:368 –371. Johnston CC Slemenda CW, Melton LJ. Bone density measurement and the management of osteoporosis. In: Favus MJ, ed. Osteoporosis Fundamentals of clinical practice. Philadelphia: LippincottRaven; 1997:46 –55. Joly J, Westhovens R, Borghs H, et al. Reference curve and diagnostic
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sensitivity for a new ultrasound device for the phalanges, the DBMsonic 1200, in Belgian women. Osteopor Int 1999;9:284 –289. Kaufman,JJ, Einhorn TA. Ultrasound assessment of bone. J Bone Miner Res 1993;8:517–525. Langton CM, Evans GP. Dependence of ultrasonic velocity and attenuation on the material properties of cancellous bone. (Abstr.) Osteopor Int 1994;4:194. Langton CM, Palmer SB, Porter RW. The assessment of broadband ultrasound attenuation in canellous bone. Eng Med 1984;13:89 –91. Melton LJ, Chao SYS, Lane J. Biomechanical aspects of fractures. In: Riggs BL, Melton LJ, eds. Osteoporosis: Etiology, diagnosis and management. New York: Raven Press; 1988:111–131. Melton LJ, Riggs BL. Risk factor for injury after a fall. Clin Geriatr Med 1986;1:525–536. Njeh CF, Boivin CM, Langton CM. The role of ultrasound in the assessment of osteoporosis: A review. Osteopor Int 1997;7:7–22. Pluskiewicz W, Nowakowska, J. Bone status after long-term anticonvulsant therapy in epileptic patients: Evaluation using quantitative ultrasound of calcaneus and phalanges. Ultrasound Med Biol 1997; 23:553–558. Pluskiewicz W, Drozdzowska B. Ultrasound measurements of proximal phalanges in Polish early postmenopausal women. Osteopor Int 1998;8:578 –583. Pluskiewicz W. Bone status assessed by quantitative ultrasound in Polish healthy postmenopausal women: A normative data. Clin Rheumatol 1998;17:40 – 43. Ross PD, Davies JW, Vogel JM, Wasnich RD, et al. A critical review of bone mass and the risk of fractures in osteoporosis. Calcif Tissue Int 1990;46:149 –161. Schott AM, Hans D, Sornay-Rendu E, Delmas PD, Meunier PJ, et al. Ultrasound measurements on os calcis: Precision and age-related changes in a normal female population. Osteopor Int 1993;3:249 – 254. Ventura V, Mauloni M, Mura M, et al. Ultrasound velocity changes at the proximal phalanges of the hand in pre-, peri- and postmenopausal women. Osteopor Int 1996;6:368 –375.
PII: S0301-5629(00)00340-9
● Original Contribution QUANTITATIVE ULTRASOUND (QUS) AT THE CALCANEUS AND HAND PHALANGES IN POLISH HEALTHY POSTMENOPAUSAL WOMEN WOJCIECH PLUSKIEWICZ and *BOGNA DROZDZOWSKA Department & Clinic of Internal Diseases, Allergology, and Clinical Immunology, *Department of Pathomorphology, Silesian School of Medicine, Katowice, Poland (Received 7 July 2000; in final form 16 October 2000)
Abstract—In a cross-sectional study, 109 postmenopausal, healthy women, mean age 58.8 years, were studied. The aim of the study was to compare quantitative ultrasound (QUS) performed at two measurement sites of the same persons (correlations between parameters studied, age, and years since menopause (YSM)-related changes, influence of body size). Bone status was established using measurements at the calcaneus by Achilles (Lunar, USA), which measures speed of sound (SOS [m/s], CV% ⴝ 0.22%), broadband ultrasound attenuation (BUA [dB/MHz], CV% ⴝ 1.8%), stiffness index (SI [%], CV% ⴝ 1.3%), and by DBM Sonic 1200 (Igea, Italy), which measures amplitude-dependent speed of sound (Ad-SoS [m/s], CV% ⴝ 0.64%) at the hand phalanges. Mean and SD values were: SOS ⴝ 1498 ⴞ 24.8 m/s, BUA ⴝ 104.6 ⴞ 9.4 dB/MHz, SI ⴝ 69.2 ⴞ 12.3%, Ad-SoS ⴝ 1879 ⴞ 90.1 m/s. Age- and YSM-related changes were as follows: age-SOS r ⴝ ⴚ0.37, p < 0.0001, age-BUA r ⴝ ⴚ0.33, p < 0.001, age-SI r ⴝ ⴚ0.36, p < 0.001, age-Ad-SoS r ⴝ ⴚ0.62, p < 0.00001, YSM-SOS r ⴝ ⴚ0.27, p < 0.01, YSM-BUA r ⴝ ⴚ0.32, p < 0.001, YSM-Ad-SoS r ⴝ ⴚ0.44, p < 0.00001, YSM-SI r ⴝ ⴚ0.29, p < 0.01. In stepwise, multiple regression analyses of ultrasound parameters on age, YSM, height, and weight, the following equations were obtained: SOS [m/s] ⴝ 1564.9 ⴚ 1.1 ⴛ age [y], r ⴝ ⴚ0.37, p < 0.0001; BUA [dB/MHz] ⴝ 88.7 ⴙ 0.28 ⴛ weight [kg] ⴚ 0.36 ⴛ YSM [y], r ⴝ ⴚ0.51, p < 0.00001; SI [%]) ⴝ 79.2 ⴚ 0.5 ⴛ age [y] ⴙ 0.28 ⴛ weight [kg], r ⴝ ⴚ0.47, p < 0.00001; Ad-SoS [m/s] ⴝ 2287 to 6.9 ⴛ age [y], r ⴝ ⴚ0.62, p < 0.00001. In conclusion, QUS at the calcaneus and hand phalanges express similar trends in skeletal changes due to aging and the postmenopausal period, although measurements at the phalanges seem to be more sensitive for detecting bone changes, due to faster decrease rate of the Ad-SoS value than calcaneal measurements. (E-mail: [email protected]) © 2001 World Federation for Ultrasound in Medicine & Biology. Key Words: Quantitative ultrasound, Calcaneus, Phalanges, Women, Normal.
a good predictor of bone strength, but there are also other risk factors for osteoporotic fractures. Damaged microarchitecture or loss of elasticity are examples of the importance of qualitative features of bone tissue (Einhorn 1993; Melton and Riggs 1986). In the diagnosis of osteoporosis, necessity of using methods which are able also to detect quality of bone tissue is obvious. Some studies showed that quantitative ultrasound may provide additional information regarding bone quality (Kaufman and Einhorn 1993; Langton and Evans 1994; Langton et al. 1984). This method does not rely on ionizing radiation and is relatively cost-effective. More recently, some newer ultrasound devices that measure other skeletal sites have been developed. One of the most frequently evaluated is measurements of the hand phalanges using Italian device DBM Sonic 1200 (Igea, Carpi). In many studies, this machine proved its ability to express bone
INTRODUCTION Osteoporosis is a major health problem, because of individual and social costs connected with fractures and their late consequences. Any amelioration of the impact of osteoporosis depends on a reduction of its attendant fractures (Johnston et al. 1997). Bone mineral density accounts for 75% to 85% of the variance in the ultimate strength of bone tissue (Melton et al. 1988). Because bone strength is an important determinant of fracture susceptibility, along with the likelihood of sustaining sufficient trauma, it follows that bone mass measurement is also correlated with fracture risk in patients (Ross et al. 1990). Bone density is
Address correspondence to: Wojciech Pluskiewicz, M.D., Silesian School of Medicine, Department & Clinic of Internal Diseases, Allergology, and Clinical Immunology, 41-800 Zabrze, ul.3 Maja 13/15, Poland. E-mail: [email protected] 373
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Table 1. Clinical characteristics of group studied age (years)
Weight (kg)
Height (m)
BMI (kg/m2)
YSM (years)
SOS (m/s)
BUA (dB/MHz)
SI (%)
Ad-SoS (m/s)
58.8 ⫾ 8.1
69.1 ⫾ 13.3
1.57 ⫾ 0.06
28.0 ⫾ 5.2
10.4 ⫾ 7.9
1498 ⫾ 24.8
104.6 ⫾ 9.4
69.2 ⫾ 12.3
1879 ⫾ 90.1
changes during growth (Halaba and Pluskiewicz 1997), due to some therapeutic interventions (Pluskiewicz and Nowakowska 1997; Pluskiewicz and Drozdzowska 1998), age- and postmenopause-related changes (Pluskiewicz and Drozdzowska 1998; Ventura et al. 1996). The aim of the current study was to compare QUS at two various skeletal sites in regard to age- and years since menopause-related changes, to evaluate correlations between parameters studied, and the influence of body size. MATERIALS AND METHODS In the study, 109 healthy postmenopausal women, mean age 58.8 years, age range 35 to 79, were studied. All were recruited from patients referred to Outpatient Osteoporotic Clinic on bone status evaluation in years 1995 to 1999. In all subjects, no medical conditions affecting bone metabolism (chronic diseases or medications) were noted. None of persons studied prior and during measurements was on treatment for osteoporosis, including hormone replacement therapy, bisphosphonates, and calcitonin. No fractures occurred in the group studied. All women had natural menopause. Clinical characteristics are shown in Table 1. Informed consent was obtained from all subjects and the study was approved by the local ethics committee. Bone status was assessed by two quantitative ultrasound methods. Calcaneus was measured by Achilles (Lunar, USA), and distal metaphyses of II to V proximal phalanges of the hand were measured by DBM Sonic 1200 (Igea, Italy). In all individuals, the right (dominant) side was measured. All measurements were done by the same person. The ultrasound system for heel measurement consists of two unfocused transducers, of 2.54-cm diameter, mounted coaxially about 3.5 cm apart. Acoustic readings were accomplished by submerging the transducer pair and the heel into a 35°C water bath containing a skinwetting surfactant. Achilles measures speed of sound (SOS [m/s]) and broadband ultrasound attenuation (BUA [dB/MHz]). A third variable, the stiffness index, (SI [%]) was also determined. It is a combination of SOS and BUA and is calculated as follows: SI ⫽ 0.67 ⫻ BUA ⫹ 0.28 ⫻ SOS-420. Coefficients of variation (CV%) were: 0.22% for SOS, 1.8% for BUA, and 1.3% for SI.
Bone status at the hand was assessed by a device consisting of two probes mounted on an electronic caliper. The emitter probe positioned on the medial surface of the measured phalanx generates a single period at 1.25 MHz every 128 s. The receiver probe is positioned on the lateral side of the phalanx and obtains the ultrasound that has crossed the phalanx. The time interval between emission and reception of the ultrasound signal was measured and expressed in m/s. We determined the speed of sound in the distal metaphyses of the proximal phalanges of the second through fifth digits of the dominant hand. The speed of sound in bone was calculated using the first signal with an amplitude of more than 36 pixels on the screen. Thus, the measured speed of sound was dependent on signal amplitude (amplitude-dependent speed of sound–Ad-SoS [m/s]). Acoustic coupling was achieved using a standard ultrasound gel. CV% was 0.64%. STATISTICS All statistical analyses were performed using Statistica for Windows. Relationships between parameters studied were established using Pearson’s coefficients of correlation. Influence of age, years since menopause (YSM), and body size on ultrasound variables was evaluated using multiple, stepwise regression analysis. RESULTS Mean values of ultrasound parameters are presented in Table 1. Correlation analysis showed significant relationships between measured variables. The strongest coefficient of correlation was noted, as was expected, between BUA and SOS (r ⫽ 0.74, p ⬍ 0.00001). Ad-SoS correlated with SOS (r ⫽ 0.54, p ⬍ 0.00001) and BUA (r ⫽ 0.49, p ⬍ 0.00001) and SI (r ⫽ 0.55, p ⬍ 0.00001). Table 2 presents correlations and regressions of age and YSM with ultrasound parameters. As shown, phalangeal Ad-SoS presents a faster decrease rate than calcaneal parameters both for age- and YSM-related changes, but negative, significant trends are similar for both measurement sites. In Figures 1– 4, these relationships are shown for SOS and Ad-SoS (dotted lines represent 95% confidential of regression). In stepwise, multiple regression analyses of ultrasound parameters on age, YSM, height and weight, the following equations were obtained: SOS
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Table 2. Correlations and regressions of ultrasound values with age and YSM Linear regression equation
r
p
SOS ⫽ 1565.9 ⫺ 1.14 ⫻ age BUA ⫽ 127.2 ⫺ 0.38 ⫻ age SI ⫽ 101.2 ⫺ 0.55 ⫻ age Ad-SoS ⫽ 2287 ⫺ 6.9 ⫻ age
⫺0.37 ⫺0.33 ⫺0.36 ⫺0.62
⬍ 0.0001 ⬍ 0.001 ⬍ 0.001 ⬍ 0.000001
SOS ⫽ 1506.8 ⫺ 0.86 ⫻ YSM BUS ⫽ 108.6 ⫺ 0.38 ⫻ YSM SI ⫽ 74.0 ⫺ 0.46 ⫻ YSM Ad-SoS ⫽ 1932 ⫺ 5.0 ⫻ YSM
⫺0.27 ⫺0.32 ⫺0.29 ⫺0.44
⬍ 0.01 ⬍ 0.001 ⬍ 0.01 ⬍ 0.00001
[m/s] ⫽ 1564.9 ⫺ 1.1 ⫻ age [y], r ⫽ ⫺0.37, p ⬍ 0.0001; BUA [dB/MHz] ⫽ 88.7 ⫹ 0.28 ⫻ weight [kg] ⫺ 0.36 ⫻ YSM [y], r ⫽ ⫺0.51, p ⬍ 0.00001; SI [%] ⫽ 79.2 to 0.5 ⫻ age [y] ⫹ 0.28 ⫻ weight [kg], r ⫽ ⫺0.47, p ⬍ 0.00001; Ad-SoS [m/s] ⫽ 2287 ⫺ 6.9 ⫻ age [y], r ⫽ ⫺0.62, p ⬍ 0.00001. In stepwise, multiple regression analyses, both SOS and Ad-SoS are significantly dependent only on age, while BUA is a function of weight (positively), and YSM (negatively) and SI depends on age (negative influence) and weight (positive influence).
Fig. 2. Simple linear regression between age and Ad-SoS.
In our study, ultrasound measurements were performed in two skeletal sites. The calcaneus is almost purely trabecular bone and weight-bearing. Hand phalanges consist of both trabecular and cortical bone and are not weight-bearing bones. Measurements in such different sites of the skeleton performed in the same person allow comparison of how various ultrasound methods determine bone status. As was mentioned in Introduction section, several studies showed the ability of QUS in both sites to reveal changes of bone tissue due
to growing, aging, postmenopause, or some medications. Calcaneus measurements have recently received a list of excellent reviews (Gregg et al. 1997) and achieved fixed position in the diagnosis of osteoporosis. Phalangeal ultrasound measurements are merely 7 years under investigation. In many studies, an ability of the method to express bone tissue features/changes are proved (Alenfeld et al. 1998; Cardenas et al. 1997; Halaba and Pluskiewicz 1997; Joly et al. 1999; Pluskiewicz and Nowakowska 1997; Pluskiewicz and Drozdzowska 1998; Ventura et al. 1996). Phalangeal ultrasound measurements were also used for evaluation of a child population (Halaba and Pluskiewicz 1997), that was much easier to perform than using calcaneal measurements (Jaworski et al. 1995). Current study showed that, despite partly different skeletal function and trabecular/cortical ratio in measured bones, ultrasound parameters obtained showed similar trends in age- and YSM-related changes. In our cross-sectional studies recently published, we investigated age- and YSM-related
Fig. 1. Simple linear regression between age and SOS.
Fig. 3. Simple linear regression between YSM and SOS.
DISCUSSION
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Fig. 4. Simple linear regression between YSM and Ad-SoS.
changes in female populations separately for calcaneus (Pluskiewicz 1998) and hand phalanges (Pluskiewicz and Drozdzowska 1998). In 712 healthy postmenopausal women (mean age 59.5 years), SOS and BUA decreased significantly with age (r ⫽ ⫺0.38, r ⫽ ⫺0.36, respectively) and with YSM (r ⫽ ⫺0.35, r ⫽ ⫺0.33, respectively), which is very close to data obtained in the current study. Some others authors also assessed these relationships at the calcaneus, and the following results were obtained: age-SOS– 0.44, age-BUA– 0.45, YSM-SOS– 0. 56, YSM-BUA– 0.52 (Cepollaro et al. 1995), age-SOS– 0.66, age-BUA– 0.56, YSM-SOS– 0.63, YSM-BUA– 0.5 (Schott et al. 1993). General trends of changes in these studies are similar to our results. In our study performed in 398 healthy women (mean age 53.4 years), Ad-SoS decreased significantly with age and YSM (r ⫽ ⫺0.40, r ⫽ ⫺0.44, respectively) (Pluskiewicz and Drozdzowska 1998). The difference in age-related changes in our previously published and current studies may be explained by the difference in mean age and age range of currently studied women. Agerelated changes in Ad-SoS values were also evaluated by other authors. Alenfeld et al. (1998) obtained r ⫽ ⫺0.73. The same value is given by Duboef et al. (1996), while Joly et al. (1999) noted a slightly lower value of r ⫽ ⫺0.59. Coefficient of correlation between age and AdSoS obtained in the current study (r ⫽ ⫺0.62) is close to data given by other authors. Also, our relationship of Ad-SoS-YSM with r ⫽ ⫺0.44 is comparable to other results: r ⫽ ⫺0.31 (Duboef et al. 1996), r ⫽ ⫺0.38 (Joly et al. 1999), and r ⫽ ⫺0.42 (Ventura et al. 1996). Data from others studies confirm a faster rate of Ad-SoS decline with age than calcaneal ultrasound parameters. We hypothesize that some features of bone tissue (microstructure, elasticity, etc.) may play a role in bone loss, and only more sophisticated or invasive techniques may help to explain results obtained with the use of ultra-
Volume 27, Number 3, 2001
sound measurements. It may be suggested that, due to faster rate of decrease in phalangeal ultrasound parameter than for calcaneal ultrasound parameters, Ad-SoS is more sensitive for detecting age-related bone loss. In some other studies, measurements of phalangeal Ad-SoS and calcaneal parameters obtained by Achilles were presented. Coefficient of correlation given by other authors (Alenfeld et al. 1998) between Ad-SoS and SOS was very close to our result (0.5 vis 0.54); however, in that study, no significant correlation between Ad-SoS and BUA was obtained. In other study (Joly et al. 1999), both calcaneal and hand ultrasound measurements were also performed, but the authors did not provide correlations between them. Interesting information was provided by stepwise, multiple regression analysis of ultrasound parameters on age, YSM, and body size. Both SOS and Ad-SoS are related only to age, while BUA and stiffness index are positively influenced by weight. It is difficult to compare current correlations between body size and ultrasound values with data given by other authors, because in our study, stepwise multiple regression analyses were performed, while in other studies, simple linear correlations were assessed. Alenfeld et al. (1998) have found positive, significant dependence between Ad-SoS and weight (r ⫽ 0.4) and height (r ⫽ 0.23). Also, in the study by Ventura et al. (1996), some correlations of Ad-SoS with body size were obtained. Positive influence of weight on BUA and SI (not on SOS) may be explained by the fact that these parameters express features of weight-bearing bone. As expected, Ad-SoS measured in non-weight-bearing bones does not depend on weight. Thus, calcaneal SOS and Ad-SoS express similar relationships with weight. Both parameters are related to elasticity of bone tissue (Njeh et al. 1997). CV percent obtained for ultrasound parameters are in the same range as given by other authors. Precision of Ad-SoS measurements in other studies ranged from 0.52% to 0.91% (Alenfeld et al. 1998; Joly et al. 1999) vs. our precision of 0.64%. Also, precision of calcaneal measurements was comparable to other studies. Limitations of our study were: cross-sectional study design, relatively small group studied, and lack of analysis of individuals having fractures. Despite these limitations, it can be concluded that QUS at the calcaneus and hand phalanges express similar trends in skeletal changes due to aging and postmenopausal period, although measurements at the phalanges seem to be more sensitive for detecting bone changes due to faster decrease rate of Ad-SoS value than calcaneal measurements. The study allowed comparison of data obtained using two different machines measuring two skeletal sites in the same sample. Such comparison pro-
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