British Journal of Radiology 75 (2002),59-68 © 2002 The British Institute of Radiology
Influence of region of interest and bone size on calcaneal BMD: implications for the accuracy of quantitative ultrasound assessments at the calcaneus
S Cheng, PhD
1,2
C F Njeh, PhD, CPhys
1
B Fan, MD
1
X Cheng, MD, PhD
1
D Hans, PhD
1
L Wang, MD
1
T Fuerst, PhD
1 and
H K Genant, MD
1
1Osteoporosis and Arthritis Research Group, Department of Radiology, University of California, San Francisco, 350 Parnassus Avenue, San Francisco, CA 94134-1349, USA and 2Department of Health Sciences, University of Jyväskylä, Finland
Correspondence: Christopher F Njeh
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Abstract
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There is considerable technological diversity among quantitative ultrasound (QUS) devices used to assess osteoporosis. Because the distance between the transducer and the footplate remains constant, the location of the calcaneus measured will vary with foot size. This study was designed to quantify the variation in bone mineral density (BMD) between a manufacturer's region of interest (ROI_M), which is fixed relative to the footplate, and an anatomical region of interest (ROI_A), which is defined as 20% of calcaneal length. The effect of foot length and width on QUS variables measured using two Food and Drug Administration cleared QUS devices, the Sahara (Hologic) and the Achilles+ (Lunar) was assessed. 26 healthy subjects (12 male and 14 female), aged 22–54 years (35.6±10 years) and with foot lengths of 21.5 cm to 29.7 cm (25.1±2.3 cm) were recruited. QUS assessments were performed at the right calcaneus. In addition, a Hologic 4500 densitometer was used to measure the BMD of the calcaneus in the ROI_M and ROI_A. The sizes of the ROIs were approximated to the sizes of the transducers of the Sahara and Achilles+ devices. The results showed a significant difference in BMD between the two ROI locations for the Sahara device (BMD 0.642±0.135 g cm-2 vs 0.616±0.114 g cm-2, p=0.014), but no significant difference was found in BMD between the two locations for the Achilles device (BMD 0.661±0.120 g cm-2 vs 0.662±0.123 g cm-2, p=0.818). At the ROI_A, there was a significant difference in BMD between the two QUS devices (p<0.001). The correlation between QUS variables and BMD was slightly higher for the ROI_M (r=0.68–0.79, since this is site-matched) than the ROI_A (r=0.59–0.70) for the Achilles device, while for the Sahara device the correlations were r=0.35–0.40 and r=0.51–0.54, respectively. The smaller ROI of the Sahara device resulted in more than 50% of the subjects having BMD differences of greater than 5% between the ROI_A and the ROI_M, compared with only 20% of the subjects on the Achilles device. ROIs containing cortical bone edge and other soft tissues were found in 58% of cases for the Achilles device and 46% of cases for the Sahara device. The greatest differences occurred in very small and very large feet. Calcaneal length correlated significantly with Sahara speed of sound (SOS), and heel width correlated significantly with Achilles SOS. Heel width also correlated significantly with Sahara broadband ultrasound attenuation (BUA) but not Achilles+ BUA. These results suggest that variation in ROI and bone size might affect the accuracy of QUS measurements, since the calcaneus is heterogeneous both in terms of its external geometry and its internal structure and density.
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Introduction
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Osteoporosis most commonly manifests clinically as fracture of the wrist, spine or hip. As fracture is the principal outcome of osteoporosis, an understanding of the determinants of fracture risk is crucial. Intrinsic bone strength is an important determinant and is influenced by bone mineral density (BMD) as well as bone structure, including bone size and shape as well as the micro-architectural characteristics of the bone. External forces applied to a bone are also important [1, 2].
Quantitative ultrasound (QUS) has been shown to be a valid technique in the non-destructive evaluation of the elastic properties of bone tissue in vitro [3]. Since the work of Langton et al in 1984 [4], there has been increasing interest in QUS assessment of bone status in vivo. QUS isparticularly attractive because it is simple, inexpensive, portable, non-invasive and free of ionizing radiation. As such, QUS has much greater potential for widespread application (including screening for prevention) than traditional X-ray bone densitometry approaches. Studies in vivo have demonstrated the ability of QUS to discriminate patients with osteoporotic fracture from age-matched controls [5–7]. Prospective studies have also demonstrated that QUS predicts risk of future fracture generally as well as bone densitometry [8, 9].
Most of the current QUS devices are non-imaging calcaneal ultrasound devices and have a fixed transducer position with respect to the footplate [10, 11]. The location of the calcaneus measured will vary depending on foot size/length [12]. Thus, the results obtained from different subjects are not directly comparable. In addition, studies have shown that differences in region of interest (ROI) size and location can affect intraindividual and interindividual variability of QUS assessments [13–20]. This technical limitation of QUS devices with fixed transducers has been addressed by some researchers. However, some of these studies were performed with a focused transducer, which is not applicable to most of the current non-imaging QUS devices used in clinical practice [13, 16, 17]. Some of the studies used only the Lunar Achilles device [18, 20]. The aim of this study was to further identify variables that might affect the accuracy of QUS measurements, by: (1) quantifying the variation in BMD between the manufacturer's region of interest (ROI_M), which is fixed relative to the footplate, and an anatomical ROI (ROI_A), which is defined as 20% of calcaneal length; (2) evaluating the effect of foot length and width on QUS variables; and (3) comparing two QUS devices with two different transducer diameters.
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Subjects and methods
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Subjects
26 healthy volunteers (12 male and 14 female), aged 22–54 years (35.6±10 years) with foot lengths varying from 21.5 cm to 29.7 cm (25.1±2.3 cm), were recruited. The subjects did not have oedema or injury at the ankle and foot at the time of the measurements, nor were they taking any medication or suffering from any diseases known to affect bone metabolism. Informed consent was obtained prior to the measurements.
Methods
Two Food and Drug Administration cleared QUS devices, the Sahara (Hologic Inc., Bedford, MA) and the Achilles+ (Lunar/GE, Madison, WI) were used to measure broadband ultrasound attenuation (BUA) (dB MHz-1) and speed of sound (SOS) (m s-1). A derived variable, quantitative ultrasound index (QUI), was reported for the Sahara, and a stiffness index (SI) was reported forthe Achilles+. In addition, a dual energy X-ray absorptiometry (DXA) densitometer (4500; Hologic Inc.) was used to measure BMD (g cm-2) at different (ROIs) at the calcaneus. Two circular ROIs were used for data analysis: ROI_M, whose coordinates are fixed relative to the footplate, and ROI_A, whose coordinates are defined relative to the foot length of the individual. The sizes of these ROIs were determined using the transducer sizes of the QUS devices. Since the two devices have different transducer sizes and fixed locations, this resulted in four different sized ROIs (ROI_A (Sahara), ROI_A(Achilles+), ROI_M (Sahara) and ROI_M(Achilles+)).
Measurement procedure
Foot length (FL), ankle width (AW) and heel width (HW) were measured prior to the QUS assessments. FL was defined as the distance between the furthest posterior point and the furthest anterior point. AW was defined as the widest point between the lateral malleolus of the fibula and the medial malleolus of the tibia. HW was measured with a caliper at the following locations: (1) in the middle of the heel at the centre of the ROI for both Sahara and Achilles+; and (2) at the location adjusted for foot length, i.e. 20% of foot length. When the Achilles+ is used for bone status assessment, the transducers are not in contact with the subject's foot; in the Sahara, the transducers press inwards on the heel bone. Thus, HW was measured two ways. First, heel width was measured without pressing the caliper to the heel. Second, heel width was measured while pressing the caliper to the subject's heel until the subject became uncomfortable and the technologist felt she could not press any more.
A QUS scan was first carried out using the Sahara on the right foot of each subject. At the end of the scan, the position of the transducers on the subject's foot was marked before the foot was removed from the device. Then the subject lay on the DXA table on his/her left side with the right foot positioned lateral side upwards. A metal key ring was placed on the lateral side of the subject's heel where the QUS scan had been taken. The key ring was 19 mm in diameter, the same size as the Sahara transducer (Figures 1a and c
). After the DXA scan was taken, the metal ring was removed. The second image of the calcaneuswas acquired without foot repositioning and without the ring. A forearm version of the Hologic 4500 DXA was used because at the time there was no software available for scanning the calcaneus.
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Figure 1. Examples of the original images from dual energy X-ray absorptiometry scans used for bone mineral density determination, demonstrating the effect of foot size on the region of interest (ROI). The ring indicates the position of the manufacturer's ROI (ROI_M). The upper images (a,b) show a large foot (29 cm) and the lower images (c,d) show a small foot (22.5 cm). (a,c) The ROI_M of the Sahara, with a diameter of 19 mm, which was the same size as the transducer. (b,d) The ROI_M of the Achilles+, with a diameter of 25 mm, the same size as the transducer.
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The same procedure was performed with the Achilles+. At the end of the QUS scan, a paper ring the same size as the Achilles+ transducer was hooked into the transducer hole of the lateral side before the subject removed their foot from the device. The edge of the paper ring was filled with colour and gel. The subject was asked to gently contact the paper ring without moving the heel back and forth. In so doing, the area of Achilles measurement was marked on the heel. For the DXA scan, a metal key ring with the diameter of 25 mm, the same size as the Achilles+ transducer, was placed on the lateral side of the subject's heel where the ROI corresponding to the Achilles+ scan location was marked (Figures 1b and d
). Two DXA scans of the calcaneus were taken, with and without the ring and without foot repositioning.
Bone density analysis
BMD values were analysed in three steps. (1) Total calcaneus BMD (BMD_tot) was analysed from the two images without rings. The coefficient of variation (CV%) was calculated. (2) The ROI_M was determined from the DXA image using the metal key ring. The Sahara and Achilles+ have different transducer sizes, thus the size of the ROI_M and the ROI_A was different for the two devices. The area averaged 230 mm2 for the Sahara and 453 mm2 for the Achilles+, comparable with the transducer areas. BMD values at the ROI_M were analysed and the ROI was then copied. (3) On the same image, the copied ROI_M was moved to the location at 20% of the calcaneus length and defined as the ROI_A (Figure 2a). BMD values were then calculated. It is worth noting that four ROIs were measured (ROI_M Sahara, ROI_M Achilles, ROI_A Sahara and ROI_A Achilles). These ROIs were used only for BMD assessments.
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Figure 2. (a) The location of the manufacturer's region of interest (ROI_M) and the anatomical region of interest ROI_A where bone mineral density was analysed, where R1 represents ROI_M and R2 represents ROI_A. The upper image shows the ROIs determined using the Sahara device and the lower image are the ROIs determined using the Achilles+ device. (b) An example of how the true dimension has been calculated for each subject. True calcaneal length=measured calcaneal length x (true ring diameter/measured diameter).
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Calcaneal length (CL) was measured from the DXA image. Owing to DXA pixel asymmetry, the scaling factor inherent in the DXA image was first determined by measuring the diameter of the ring in each image in the direction parallel to the direction of measurement of CL. Then the true dimension for each of the subjects was calculated (Figure 2b). The CL was measured on the screen by moving the cursor from the furthest posterior point to the furthest anterior point. We also obtained the soft tissue thickness (STT, in mm) from the lowest furthest point to the bone edge.
In addition, we also estimated the volumetric BMD (BMDv, in mg cm-3) by dividing the area BMD (mg cm-2) by heel width.
Statistical analysis
A Student's t-test (paired, two-tailed) was applied to examine the significance of the differences between the means of the ROI_M and the ROI_A. Linear regression analysis was used to examine the relationship between QUS and BMD results. A stepwise regression was applied to evaluate the relationship between QUS variables, BMD, FL, CL and HW. For the Achilles+, the factors included in the regression were BMD at the ROI_M (BMD_M), BMD_tot, total calcaneus area, FL, CL, non-pressing HW and STT. For the Sahara, the predictors included in the regression were BMD_M, BMD_tot, total calcaneus area, FL, CL, pressing HW and STT. The symmetric measures were used to estimate the measure of agreement (kappa value, above mean or below mean) between the Achilles+ and Sahara devices. Statistical analyses were conducted using SPSS-X software.
We have previously reported a short-term standardized measurement precision of 4.3% for BUA and 3.85% for SOS using the Achilles+, and 4.41% for BUA and 3.83% for SOS using the Sahara. The CV% for the ROI area measured with DXA was 1.5 for the Sahara and 0.4 for the Achilles+.
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Results
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The physical characteristics, the BMD values of the total calcaneus and the QUS variable results are given in Table 1. The results showed that there were significant differences in HW at three different locations of the heel (p<0.001), indicating that the thickness of the heel is inhomogeneous. No difference was found between the two scanners for calculating total BMD. The correlation coefficient was 0.999.
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Table 1. The physical characteristics, the bone mineral density (BMD) values of the total calcaneus in different regions of interest and the quantitative ultrasound results with the Sahara and the Achilles+ devices
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The QUS results for individual subjects measured both with the Achilles+ and the Sahara are presented in Figure 3. We divided the QUS values above and below the mean and compared the agreement between the two devices. The results showed that there was a moderate agreement between the Achilles+ and the Sahara for all QUS variables (73% for BUA and SOS, 81% for SI/QUI). The kappa values were 0.47 for BUA, 0.46 for SOS and 0.62 for SI/QUI. The same was true when comparing BMD in ROIs at different locations, and when comparing BMD of ROIs at the same location but with different sizes. The agreement of BMD between the ROI_M and the ROI_A was 81% for the Sahara (kappa score 0.62) and 88% for the Achilles+ (kappa score 0.77). Forthe ROI_M, the agreement of BMD between the Sahara ROI and the Achilles+ ROI was 77% andthe kappa score was 0.54. Similarly, for the ROI_A with different ROI sizes, the agreement of BMD was 92% and the kappa score was 0.85, which is significantly better than for the ROI_M.
There was a significant difference in BMD between the two ROIs for the Sahara (Table 1; p=0.014; Figure 4a), but no significant difference was found in BMD between the two locations for the Achilles (Table 1; p=0.818; Figure 4b). At the ROI_A, there was a significant difference in BMD between the Sahara and the Achilles+ (BMD 0.616 mg cm-2 vs 0.662 mg cm-2, p<0.001). The small area (transducer diameter) of the Sahara ROI resulted in more than 50% of the subjects having more than 5% difference between the ROI_M and the ROI_A, compared with 20% of the subjects on the Achilles. On the other hand, ROIs containing cortical bone edge and other soft tissue were found in 58% of cases for the Achilles+ and 46% of cases for the Sahara. The variation was much larger when comparing the BMD in the ROI_M and the ROI_A between the Achilles+ and the Sahara. The difference in BMD ranged from -0.107 mg cm-2 to 0.157 mg cm-2 (mean 0.019 mg cm-2, SD 0.061) for the ROI_M and from 0.012 mg cm-2 to 0.101 mg cm-2 (mean 0.046 mg cm-2, SD 0.002) for the ROI_A.
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Figure 4. Areal bone mineral density (BMD) between the manufacturer's region of interest (ROI_m) and the anatomical region of interest (ROI_a) for (a) the Sahara and (b) the Achilles+. The dots represent individual values and the lines link measurements on the same person.
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There was a negative correlation between Sahara SOS and CL (r=-0.391, p=0.048), and between Achilles+ SOS and non-pressing HW (r=-0.422, p=0.032). BUA of the Achilles+ was corrected with HW (r=0.417, p=0.038) and AW (r=0.549, p=0.004). There was also a tendency for Achilles+ BUA to correlate with foot length (r=0.365, p=0.067). No significant correlations were found between BUA of Sahara and FL, CL and HW. BMD was found to correlate significantly with FL (r=0.452–0.549), CL (r=0.435–0.550) and HW (r=0.456–0.557). The correlation between QUS variables and BMD was slightly higher for the ROI_M (r=0.68–0.78, since this is site-matched) than the ROI_A (r=0.59–0.70) for the Achilles (Table 2). In contrast, the correlation was r=0.35–0.40 and r=0.51–0.54, respectively, for the Sahara (Table 2).
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Table 2. Correlations (r values) between quantitative ultrasound variables and bone mineral density (BMD) (pvalues in parentheses)
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We further used a stepwise regression model to evaluate the relationship between QUS variables and FL, CL, HW and BMD. We found that BMD_M and HW had a significant effect on the QUS variables measured with the Achilles+, and that BMD_tot, STT and CL had a significant effect on the QUS variables measured with the Sahara (Table 3).
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Table 3. Stepwise regression analysis between quantitative ultrasound (QUS) variables, bone mineral density (BMD) and bone size
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In addition, as an estimate of volumetric BMD, we calculated BMDv (mg cm-3) by dividing area BMD (mg cm-2) by pressed heel width. We found that BMDv differed significantly between the ROI_M and the ROI_A (p<0.001; Figure 5) both for the Sahara and the Achilles+ ROI. The correlation between QUS variables and BMDv was stronger than the correlation between QUS variables and area BMD (Table 2), especially between SOS and BMDv.
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Figure 5. Volumetric BMD between the manufacturer's region of interest (ROI_m) and the anatomical region of interest (ROI_a) for (a) the Sahara and (b) the Achilles+. The dots represent individual values and the lines link values for the same person.
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Discussions
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In this study we found that HW has a significant effect on Achilles+ assessments, and that CL and STT have a substantial effect on Sahara assessments. A QUS device with fixed transducers cannot adjust the location of the ROI for different individuals, leading to poor accuracy of the QUS assessment.
We investigated the effect of fixed ROIs on BMD. Since the transducers were fixed, we could not perform QUS measurements at the two ROIs. However, we could base our analyses on the assumption that QUS is highly dependent on BMD [21], so the observed variation for BMD with the two ROIs (ROI_M and ROI_A) can be expected to be similar for QUS variables. Assuming also that QUS is dependent on structure, then the variation may be more pronounced. Lin et al [22] observed up to 40% variation in structure defined using trabecular separation obtained from MR images. The clinical implications of using a fixed ROI compared with an anatomical ROI are significant. The fact that not all subjects are measured at the same region introduces spread into the data. This spread is likely to affect the calculation of T-scores. Our data show that for the Sahara, the SD of BMD_M was 21% compared with a SD of 18.5% for BMD_A. This indicates that the variation was greater at the ROI_M location than at the ROI_A location for the same person. These findings are in agreement with a study by Damilakis et al [19], who found that the SD of BUA was 12.2% for variable ROIs compared with 14.4% for fixed ROIs. They also observed that measuring ultrasound parameters at variable ROIs compared with measurements at fixed ROIs improved reproducibility and enabled significantly better differentiation of diseased subjects from healthy individuals. In a recent study, Tsuda-Futami et al [23] demonstrated that using different footplates to compensate for a fixed transducer resulted in better reproducibility.
Both QUS devices used in this study have relatively good precision, but their accuracy is unknown. To ensure high accuracy, it is important to know where the QUS values are measured. Our results indicate that there are significant differences between the Achilles+ ROI and the Sahara ROI. About 58% of the cases for the Achilles+ and 46% of the cases for the Sahara included bone edge and other soft tissue. These findings are in accordance with other studies showing similar results in women [18] and in vitro [24]. Since the sound wave pathway is not the same in all subjects, some subjects may be misclassified [25].
It is important to know whether HW (bone and soft tissue) really plays a role in QUS assessments, since the difference in HW could be more than 2 cm. Theoretically, as sound waves propagate they are attenuated exponentially as a function of distance [26, 27]. Previous studies in vitro have shown that there is a linear relationship between BUA and thickness [28] and that the BUA signal is dependent on bone thickness [20, 29]. In an in vivo study using the Achilles+, Töyräs et al [20] did not observe any significant association of BUA with heel thickness but did observe a slightly negative correlation between HW and SOS. In the present study, we found that SOS negatively correlates with non-pressing HW measured with Achilles+ but not with other variables on either device. No correlations were found between pressing HW and QUS variables. The non-pressing HW explained about 18% of the variation in SOS. This is an interesting finding, since the Sahara uses considerable contact force while the Achilles+ uses a water-bath between the heel and the transducer. This indicates that the soft tissue around the heel, but not HW per se, may affect the outcome of QUS assessments.
We found that total CL and STT were associated with QUS variables measured with the Sahara but not with the Achilles+. This is an interesting observation since the effect of CL and STT was only associated with QUS variables measured using the Sahara device. As previously mentioned, the Sahara is a contact QUS device. This observation may imply that, in addition to the effect of soft tissue, back scattering may also affect the outcome of Sahara assessments.
We found that after controlling for foot size (FL, CL and HW), the correlation between QUS and BMD variables became stronger, especially for SOS for both devices. In addition, we found that there was no significant difference for area BMD between ROI_M and ROI_A, but that BMDv differed significantly between ROI_M and ROI_A. These findings also agree with our previous study [14], which showed that when the scanning distance was increased by an average 0.47 cm from the back of the heel upward along the heel's axis, there were no significant change in area BMD, but BMDv increased significantly. This implies the importance of the effect of the HW and CL. We believe that it may be useful toadjust HW and CL for QUS assessments, especially for SOS.
It has been suggested that QUS assessment can be used to estimate BMD [30]. To do this, one has to show high correlations between QUS and BMD. Previous in vivo and in vitro studies have shown an inconsistent relationship between QUS and BMD assessments [31]. The differences were derived in part from the variations of the bone thickness and the amount of soft tissue around the bone, as well as the location of the measurements. One would expect a better correlation between QUS and BMD for ROI_M, since this was a site-matched ROI. This was true for the correlation between QUS variables and BMD_M for the Achilles+ but not for the Sahara. We believe that these discrepancies were mainly due to the differences in ROI location and size. The smaller size of the Sahara ROI led to more variations in different individuals and induced larger variations in BMD at different ROIs, while the large size of the ROI for Achilles+ reduced the variability of the BMD in the population and at different locations.
In addition, the comparison between QUS variables and area BMD or BMDv may partially account for the differences. Based on the correlation coefficient value, it seems that BUA better reflects the amount of bone mass (area BMD), while SOS is associated more with bone density (BMDv). This could support a recent in vitro finding that trabecular bone volume is associated with BUA, and apparent ash density is associated with SOS [21].
As mentioned earlier, QUS instruments from different manufacturers have significant differences in their calibration methods and analysis software as well as in the design of the transducers. Nevertheless, we should expect similar diagnoses for the same subject. In this study, we found that the agreement between these two devices for classifying the subject below or above the mean was relatively poor. This poor agreement is partly due to the different size of the ROIs. The small ROI for the Sahara resulted in larger differences in BMD between ROI_M and ROI_A compared with the Achilles+. On the other hand, the Achilles+ included more bone edge and soft tissue than the Sahara. At the ROI_A, the difference between the Sahara and the Achilles+ was on average 7.6% (SD=3.3%), while for the ROI_M the difference was up to 26% (mean 3.9%, SD 9.6%), although the agreement was relatively good for classifying the subject with different ROI sizes in the ROI_A location. The effect of the ROI size is obvious. Finding an optimal ROI size for all the QUS devices may be a useful approach for standardization of QUS assessment.
QUS has been suggested for studying paediatric bone status. It will be particularly useful to study the effect of foot length and foot size in the paediatric range on QUS variables.
We have to acknowledge some of the limitations of the study. First, the limited sample size may affect the correlations derived in this study. A second important limitation is the lack of direct QUS measurement at the ROI_A. Ideally, this experiment could be carried out using a bench top system whereby the transducers and location could be changed. In that case the true effect of size of the ROI/transducer and the location on QUS variables could be quantified.
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Conclusion
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HW has a significant effect on Achilles+ assessments and CL, and STT has a substantial effect on Sahara assessments. A QUS device withfixed transducers cannot adjust the location of theROI for different individuals, leading to poor accuracy. In addition, different ROI sizes might affect the accuracy of QUS measurements. Our results suggest that using comparable ROI size and assessment locations in different QUS devicesmight help in comparing results measured with different devices and might improve the accuracy—and perhaps precision—of the QUS assessments.
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Acknowledgments
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We are grateful to the willing volunteers from the University of California, San Francisco. We would also like to thank Mr David Breazeale for his editorial assistance.
Received for publication December 18, 2000.
Revision received July 16, 2001.
Accepted for publication August 23, 2001.
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Top
Abstract
Introduction
) and the Achilles+ (
). The broken vertical line (–.–) indicates the mean value obtained with the Sahara and the dotted vertical line (....) indicates the mean value obtained with Achilles+. The horizontal line links the same person measured with both devices. BUA, broadband ultrasound attenuation; SOS, speed of sound; QUI, quantitative ultrasound index; SI, stiffness index.