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(Radiology. 2001;220:400-405.)
© RSNA, 2001

Musculoskeletal Imaging

Quantitative US of the Calcaneus: Cutoff Levels for the Distinction of Healthy and Osteoporotic Individuals1

Stephan Grampp, MD, Christine Henk, MD, Ying Lu, PhD, Christian Krestan, MD, Heinrich Resch, MD, Franz Kainberger, MD, Soraya Youssefzadeh, MD, Friedrich Vorbeck, MD and Herwig Imhof, MD

1 From the Department of Osteology, Universitätsklinik für Radiodiagnostik, Währinger Gürtel 18-20, 1090 Vienna, Austria (S.G., C.H., C.K., F.K., S.Y., F.V., H.I.); Department of Radiology, University of California, San Francisco (S.G., Y.L.); and Department of Internal Medicine, Krankenhaus der Barmherzigen Schwestern, Vienna, Austria (H.R.). From the 1999 RSNA scientific assembly. Received August 15, 2000; revision requested October 11; revision received January 24, 2001; accepted March 7. Supported by the Ludwig-Boltzmann Institut für Klinische und Experimentelle Radiologie and Ludwig-Boltzmann Institut für Fortgeschrittene Altersforschung, Vienna, Austria. Address correspondence to S.G. (e-mail: stephan.grampp@univie.ac.at).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To calculate cutoff levels for quantitative ultrasonography (US) performed to distinguish healthy individuals and those with osteoporosis identified with dual x-ray absorptiometry.

MATERIALS AND METHODS: In 1,357 patients (856 females, aged 55.1 years ± 15.4 [mean ± SD]; 501 males, aged 50.4 years ± 15), bone mineral density measurements of the lumbar spine (posteroanterior, L1 through L4) and femoral neck were obtained, and quantitative US was performed to determine the stiffness of the calcaneus. Individuals with a T score less than -2.5 (osteoporotic) at the spine and femur were identified, and upper T-score cutoff values (3 SDs from the mean) in the groups of male and female patients with osteoporosis were identified.

RESULTS: Females with dual x-ray absorptiometric values that were indicative of osteoporosis of the spine had an upper T-score cutoff value of -1.0 (males, -0.2). Females who had femoral osteoporosis showed an upper quantitative US T-score cutoff value of -0.6 (males, 0).

CONCLUSION: Cutoff values may permit the use of quantitative US to screen for the presence of osteoporosis in the spine and femur. Quantitative US will help to prevent unnecessary dual x-ray absorptiometric and conventional radiographic examinations.

Index terms: Bones, mineralization, 331.1295, 443.1295, 4642.12989 • Bones, US, 331.1298, 43.1298, 4642.1298 • Osteoporosis, 331.56, 443.56, 4642.56


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The most commonly used method to examine the skeletal status is projectional measurement with dual x-ray absorptiometry (DXA), which is typically used in the lumbar spine and proximal femur (ie, femoral neck) (1–3). The only commercially available approach for noninvasive assessment of bone status that does not require radiation is the quantitative ultrasonographic (US) measurement of ultrasound velocity (speed of sound) and broadband ultrasound attenuation at the calcaneus, tibia, and phalanges. Main advantages of a US examination are the complete absence of ionizing radiation and its low cost. Quantitative US of the calcaneus is the only application that has shown valid results in clinical studies (1,4–7).

The diagnosis of osteoporosis, as well as the decision to initiate treatment, is usually made by comparing values in an individual patient to those in a normative database. These reference databases obtained in healthy populations are provided by the manufacturers and implemented into the software for practically all available instruments (DXA, quantitative computed tomography [CT], quantitative US). Results in individual patients are compared with those in the databases obtained in healthy individuals of the same sex and ethnic group.

Usually, the estimated bone density is presented as a T score and a Z score. The T score refers to the peak bone mass in young healthy adults, and it is calculated in a manner similar to that used for the Z score. The Z score shows the patient’s results as the deviation from the mean in age-matched control subjects divided by the SD of this mean, which is an indication of biologic variability (8–11). However, it is known that statistically significant discordance can exist between measurements at different skeletal sites and, especially, between measurements performed with different techniques (2,5). The World Health Organization defined (12) the value for the presence of osteoporosis in Caucasian women without a fracture. With this definition, women are regarded as having osteoporosis if they have a T score of more than 2.5 SDs below the peak bone mass at DXA of the spine.

However, to our knowledge, no specific recommendations for quantitative US results exist. Also, men were not included in these recommendations, and the appropriateness of using a specific T score to indicate the presence of osteoporosis in men has, to our knowledge, not yet been determined. However, as a working hypothesis, the use of a T score of -2.5 as the threshold seemed to be reasonable with DXA in the male population.

The aim of our study was to calculate cutoff levels for quantitative US in the distinction of healthy individuals and those with osteoporosis identified at DXA.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
We examined 1,357 consecutive clinical patients (856 females: aged 55.1 years ± 15.4 [mean ± SD]; range, 15–89 years; 501 males: aged 50.4 years ± 14.6; range, 17–81 years). The patients were referred by various departments and outpatient clinics (orthopedic surgery, internal medicine, obstetrics and gynecology, transplant surgery, pediatrics) for the assessment of bone mineral density. Reasons for referral were postmenopausal osteoporosis; suspected osteoporosis; juvenile osteoporosis; hysterectomy; chronic hemodialysis; rheumatoid arthritis; Crohn disease; corticosteroid treatment; primary and secondary hyperparathyroidism; Wegener disease; pituitary gland insufficiency and pituitary gland adenoma; osteomalacia; hydroxylase deficiency; liver cirrhosis; and kidney, liver, and heart transplantation.

None of the patients had undergone joint replacement in the left lower extremity. All patients were examined according to our standard clinical work-up procedure (13). The data of all examinations were retrospectively gathered from our institutional databases. The posteroanterior lumbar spine at vertebrae L1 through L4 and the proximal femur at the femoral neck were examined in all patients with DXA (Hologic QDR-4500 scanner; Hologic, Waltham, Mass) and the manufacturer-recommended standard procedures. Fractured vertebral bodies, if present, were excluded from the analysis.

A fracture was determined by means of semiquantitative assessment of morphologic changes in the lumbar spine on lateral and anteroposterior conventional radiographs. This assessment was based on the qualitative appearance of each vertebra, with a fracture defined as altered morphology and a decrease in vertebral height of approximately 25% or more (1,2). Conventional radiographs of the lumbar spine were also evaluated for degenerative changes. Cases with obvious calcifications that might have led to an overestimation of bone mineral density were excluded (14,15). Radiographs were evaluated by one of several experienced board-certified radiologists (S.G., F.K., S.Y., F.V.).

The projectional bone mineral density values were determined in grams per square centimeter, and the individual results were expressed as a T score. At the same session, an experienced technologist examined the calcaneus of the patient with a quantitative sonographic device (Achilles; Lunar, Madison, Wis), according to the manufacturer-recommended standard procedures. The system is of the transmission type, with two ultrasound transducers (transmitter and receiver) positioned on each side of the heel. Broadband ultrasound attenuation and speed of sound are given as absolute values of the measurements, but the system provides no normative data for both parameters. Therefore, T scores for broadband ultrasound attenuation and speed of sound could not be calculated.

The sonography-determined stiffness of the calcaneus was automatically determined by using the scanner software according to the following formula (6): stiffness = (0.67 x broadband ultrasound attenuation) + (0.28 x speed of sound) - 420. Stiffness is the default parameter used by the manufacturer for demographic comparison of the patient’s data. The World Health Organization (12) clarified the diagnostic bone-mass threshold for defining osteoporosis in individuals without fracture as a T score less than -2.5 (16). Consequently, osteopenia was defined with T scores of -1 to -2.5. Individuals with T scores less than -2.5 (osteoporotic), -2.5 to -1 (osteopenic), or more than -1 (healthy) at DXA of the spine and femur were identified.

Comparisons of all measured T scores were performed with linear regression analysis for all males and all females by using the Pearson correlation coefficient r. Additionally, P values for testing the significance of correlations were obtained. The mean T scores for all males and females and the percentage of subjects with T scores less than -2.5 were calculated.

For patients with osteopenia and osteoporosis, the mean quantitative US T score and the upper and lower T-score cutoff values (within 97.5% and 99.5% CIs) were identified. The percentage of females and males who did not have osteoporosis at DXA of the spine and femur and who had a quantitative US T score that was more than the determined T score threshold level was consecutively calculated. We further calculated the 95% CI for the number and percentage of subjects in whom DXA could have been avoided if quantitative US T scores above the threshold levels were available. In a final step, we calculated the number of patients who would not have undergone DXA if the proposed threshold levels (97.5% and 99.5% CIs) had been applied.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In females, the correlation coefficient for the comparison of quantitative US T scores with T scores in L1 through L4 was 0.45; for the comparison of quantitative US T scores with neck T scores, r = 0.55. For males, the correlation coefficients were 0.48 and .51, respectively. All P values were less than .001.

A total of 282 (33.0%) females and 152 (30.4%) males had T scores that were indicative of osteoporosis of the spine (Table 1). The percentage of patients with osteoporosis at DXA of the femoral neck was higher, with 42.0% for females and 38.9% for males. However, these values were still lower than measurements obtained with quantitative US of the calcaneus (49.4% and 41.8%, respectively) (Table 1). Females with DXA values indicative of osteoporosis of the spine (97.5% CI) showed a maximum quantitative US T score of -1.0 (males, -0.2) (Figs 1, 2; Table 2. Females with osteoporosis in the femur showed a maximum quantitative US T score of -0.6 (males, 0) (Figs 3, 4; Table 2). Individuals with quantitative US T scores that were greater than these values generally did not show osteoporosis at DXA. These included 143 (16.7%) females (95% CI: 14.2%, 19.2%) and 62 (12.4%) males (95% CI: 9.5%, 15.3%) for the comparison of DXA of the spine and quantitative US and 92 (10.7%) females (95% CI: 8.6% to 12.8%) and 62 (12.4%) males (95% CI: 9.5%, 15.3%) for the comparison of DXA of the femur and quantitative US.


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  		TABLE 1. Mean T Scores and Subjects with T Scores Less than -2.5

 


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  		Figure 1. Scattergram shows the relationship between the DXA T score in L1 through L4 and the quantitative US (QUS) T score in all females (n = 856). DXA T score of -2.5 is marked with a horizontal line. Proposed cutoff level for quantitative US is marked with a vertical line. Values in the right lower quadrant indicate osteoporotic DXA measurements and quantitative US values above the cutoff value.

 


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  		Figure 2. Scattergram shows the relationship between the DXA T score in the femoral neck and the quantitative US (QUS) T score in all females (n = 856). DXA T score of -2.5 is marked with a horizontal line. Proposed cutoff level for quantitative US is marked with a vertical line. Values in the right lower quadrant indicate osteoporotic DXA measurements and quantitative US values above the cutoff value.

 

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  		TABLE 2. Range of T Scores in Subjects with and Subjects without Osteoporosis

 


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  		Figure 3. Scattergram shows the relationship between DXA T score in L1 through L4 and the quantitative US (QUS) T score in all males (n = 501). DXA T score of -2.5 is marked with a horizontal line. Proposed cutoff level for quantitative US is marked with a vertical line. Values in the right lower quadrant indicate osteoporotic DXA measurements and quantitative US values above the cutoff value.

 


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  		Figure 4. Scattergram shows the relationship between the DXA T score in the femoral neck and the quantitative US (QUS) T score in all males (n = 501). DXA T score of -2.5 is marked with a horizontal line. Proposed cutoff level for quantitative US is marked with a vertical line. Values in the right lower quadrant indicate osteoporotic DXA measurements and quantitative US values above the cutoff value.

 
The identical statistical approach was performed with a T-score border of -1 for the detection of osteopenia. Here, the quantitative US cutoff levels were much higher (Table 3); therefore, few patients had individual measurements above these levels.


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  		TABLE 3. Range of T Scores in Subjects with and Subjects without Osteopenia

 
With females and males, we calculated the number of patients with osteoporosis who would not have undergone DXA if the proposed threshold levels of 97.5% and 99.5% CIs were applied. When the 97.5% CI was used in females, four cases (0.5%) in the spine and seven (0.8%) in the hip would have been missed. In males, the numbers were three (0.6%) and four (0.8%) cases, respectively. When the 99.5% CI was used in females, one case (0.1%) in the spine and three (0.4%) in the hip would have been missed. In males, none would have been missed (Figs 1–4).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
A number of investigations (2–4,6–9,17) have shown that all three techniques used in our study (DXA of the spine and femur, quantitative US of the calcaneus) can be used to differentiate healthy pre- and postmenopausal subjects and to reflect age- and menopause-related bone loss. DXA is the most widely used diagnostic modality and generally accepted as a reliable approach for use in the diagnosis of osteoporosis. The value of measurements in the spine (2,18) and hip (2,3) is widely accepted in the diagnosis of local and systemic osteoporotic changes. The tendency of spinal measurements to allow better discrimination of vertebral fractures and, in some cases, of other osteoporotic changes, compared with peripheral measurements has been reported in numerous studies (2,19,20). In contrast, it has also been reported in both cross-sectional and longitudinal studies (4,8,21) that peripheral measurements with x-ray–based techniques or quantitative sonography may be equal to spinal or femoral measurements in the assessment of skeletal status.

In recent years, however, quantitative US measurements have been shown to have an ability on par with that of DXA in the prediction of hip fractures in elderly women (22,23), as well as in the prediction of incidental vertebral deformities (7,24). Glüer et al (4) demonstrated in a large population of about 4,700 females that the odds ratio of the patients having an osteoporotic fracture was predicted in a similarly strong fashion with the use of broadband ultrasound attenuation and bone mineral density in the spine and hip. The use of the quantitative US combination parameter of stiffness has been suggested (25) because it allows improved prediction of fracture risk. Other investigators (20,26–29) have seriously questioned the clinical use of ultrasound-based measurements in the screening and diagnosis of osteoporosis, because the diagnostic sensitivity is low compared with that of DXA and quantitative CT.

When DXA and quantitative US measurements were directly compared, several investigators (20,27,30–33) found modest correlations with axial and peripheral measurement sites. The correlation between x-ray–based methods and ultrasound measurements were only marginally lower than those between x-ray–based methods alone. Different patients were estimated to be at risk with different measurement approaches (2,5).

These levels of diagnostic disagreement may result from a number of factors. All of the techniques have their own specific error sources, as well as fundamentally different methods and units of expression that undermine their respective abilities to define true biologic relationships within or between anatomic sites or between individuals (1,2,5). But beyond technical considerations, it is likely that genetic and environmental influences and pathophysiologic forces may affect the cortical and trabecular bone envelopes or the appendicular and axial skeleton in a different manner (21,34–36); therefore, some of the measured discrepancies reflect true anatomic variations.

In our study, we demonstrated that more than 99% of the males and females who had quantitative US T scores that were more than the proposed cutoff levels could be considered not to have osteoporosis or osteopenia at specific DXA examinations. Regions of interest used in our study are widely used in the literature and clinical practice, but we recognize the fact that the use of different measurement areas at DXA might yield different results (2,3,5,18). Therefore, DXA examination could be avoided if a screening procedure with quantitative US is performed at the beginning of a diagnostic work-up. In our clinical population that had a high probability of osteoporosis, the percentage of female and male patients that could have avoided DXA was about 12%–16%. It is reasonable to assume that this percentage would be substantially higher if screening for osteoporosis is performed in a healthy population that has a smaller number of people with osteoporosis. Individuals with quantitative US values less than the described cutoff levels will still undergo DXA and, in most cases, x-ray examination (14).

A main point of our findings is that the general results and trends for males and females were comparable, and cutoff levels with which few patients would have been missed for further screening were successfully identified for both groups.

One factor influencing our results is, certainly, the use of different normative databases by the equipment manufacturers. This fact has been demonstrated (37) to account for substantial differences in the diagnosis of osteoporosis; however, because of different techniques and a lack of standardization, this factor could not be avoided. Our population has, in general, the advantage that it reflects the real-life situation that a radiologist faces on a daily basis. The patients in our study had various diseases and/or were receiving drug treatment that might have caused different skeletal sites to react to metabolic stimuli in a heterogeneous fashion (8,37,38).

Cutoff values may allow quantitative US to be used as a screening tool for osteoporosis in the spine and femur. The application of quantitative US will help to prevent unnecessary DXA and conventional radiographic examinations. A low-cost and radiation-free screening tool would also be beneficial for the assessment of the skeletal status in much of the population and would, therefore, support the ongoing efforts to detect and treat osteoporosis and related fractures.


   FOOTNOTES
 
Abbreviation: DXA = dual x-ray absorptiometry

Author contributions: Guarantor of integrity of entire study, S.G.; study concepts, S.G., H.R., Y.L.; study design, S.G., C.H.; literature research, C.K.; clinical studies, S.G., S.Y., F.V., F.K.; data acquisition, S.G., C.H.; data analysis/interpretation and statistical analysis, Y.L., S.G.; manuscript preparation and definition of intellectual content, H.I., S.G.; manuscript editing, F.K., H.I., S.G.; manuscript revision/review, C.K., S.G., H.I.; manuscript final version approval, S.G., H.I., F.K.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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