Abstract
Background: Patients with type 2 diabetes mellitus (T2DM) often have an increased or normal bone mineral density (BMD), but fragility fractures represent one of the most significant complications of the condition. This study aimed to evaluate whether the Radiofrequency Echographic Multi-Spectrometry (REMS) technique could enhance the identification of osteoporosis in T2DM patients.
Methods: A cohort of 90 postmenopausal elderly women (mean age 70.5 ± 7.6 years) with T2DM and 90 healthy controls were studied. BMD was measured at the lumbar spine (LS-BMD), femoral neck (FN-BMD), and total hip (TH-BMD) using dual-energy X-ray absorptiometry (DXA). REMS scans were performed at the same axial sites.
Results: DXA measurements were higher in T2DM women compared to non-T2DM women, but REMS measurements were lower in T2DM women. The percentage of T2DM women classified as “osteoporotic” was higher based on REMS (47.0%) compared to DXA (28.0%). Additionally, T2DM women with fragility fractures presented significantly lower BMD values by REMS (p < 0.05).
Conclusions: REMS technology may represent a useful approach to improve osteoporosis diagnosis in T2DM patients, offering a more accurate classification compared to DXA.
Introduction
The prevalence of type 2 diabetes mellitus (T2DM) is increasing globally due to aging populations, sedentary lifestyles, and the obesity epidemic. In addition to well-known complications such as cardiovascular disease and renal failure, T2DM also increases the risk of fragility fractures. Paradoxically, patients with T2DM often have higher or normal bone mineral density (BMD), yet they remain at an elevated risk for fractures.
Despite this, current assessment methods, primarily using DXA, do not always predict fracture risk accurately in T2DM patients. This discrepancy suggests that bone quality, rather than BMD alone, plays a crucial role in bone fragility in T2DM patients.
The Need for Improved Bone Health Assessment: While DXA remains the gold standard for measuring BMD, it does not account for changes in bone quality that may be present in T2DM. Techniques that complement DXA, such as the Trabecular Bone Score (TBS) and quantitative ultrasound (QUS), have been proposed. One such technique, Radiofrequency Echographic Multi-Spectrometry (REMS), uses unfiltered ultrasound signals to assess bone health and may provide a more accurate prediction of fracture risk.
Purpose of the Study: This study evaluates the potential of REMS in identifying osteoporosis in postmenopausal women with T2DM and compares it with DXA.
Methods
Study Population: The study enrolled 90 postmenopausal women with T2DM, aged between 50 and 80 years, and 90 healthy controls of the same age group. Inclusion criteria for the T2DM group included a diagnosis of T2DM for over 10 years, HbA1c levels below 8.5%, and postmenopausal status. Women with conditions that could affect bone metabolism or who were receiving osteoporosis treatments were excluded.
Bone Mineral Density (BMD) Measurements: BMD was measured using both DXA and REMS. DXA scans were performed using a Discovery W system (Hologic, Waltham, MA), and REMS scans were carried out using an EchoStation device (Echolight, Lecce, Italy) equipped with a 3.5 MHz convex transducer. The measurements were taken at the lumbar spine, femoral neck, and total hip.
Statistical Analysis: Data were analyzed using SPSS, with comparisons between the two groups performed using t-tests and Mann-Whitney U tests where appropriate. Partial correlation analyses were used to evaluate the associations between BMD and clinical parameters such as HbA1c and diabetes duration.
Results
Demographic and Clinical Characteristics: Table 1 shows the clinical characteristics of the T2DM and control groups. There were no significant differences between the groups for age, height, calcium intake, or biochemical parameters like 25OHD and parathyroid hormone (PTH). T2DM women had a significantly higher BMI than non-diabetic women.
Bone Mineral Density Measurements: DXA measurements at the lumbar spine (LS-BMD) and total hip (TH-BMD) were significantly higher in T2DM women compared to controls (p < 0.01). However, REMS measurements were lower in T2DM women at all skeletal sites, but the differences did not reach statistical significance.
Table 1 – Demographic andclinical characteristics of the study population
| Demographic and Clinical Characteristics | T2DM Patients (N = 88) | Controls (N = 87) | p-value |
|---|---|---|---|
| Age (years) | 70.5 ± 7.6 | 69.2 ± 7.5 | n.s |
| Weight (kg) | 69.2 ± 13.7 | 66.1 ± 1.3 | n.s |
| Height (cm) | 160.0 ± 6.6 | 160.1 ± 6.8 | n.s |
| BMI (kg/m²) | 27.0 ± 4.9 | 25.6 ± 4.0 | 0.05 |
| Calcium intake (mg/daily) | 872.2 ± 280.3 | 891.2 ± 255.7 | n.s |
| HbA1c (%) | 7.0 ± 1.1 | – | – |
| T2DM duration (years) | 14.3 ± 11.34 | – | – |
| Creatinine (mg/dl) | 0.9 ± 0.3 | 0.9 ± 0.2 | n.s |
| Calcium (mg/dl) | 9.3 ± 0.6 | 9.2 ± 0.5 | n.s |
| Phosphate (mg/dl) | 3.6 ± 0.5 | 3.4 ± 0.5 | n.s |
| 25OHD (ng/ml) | 21.0 ± 9.9 | 24.4 ± 8.9 | n.s |
| PTH (pg/ml) | 36.3 ± 19.7 | 34.8 ± 17.9 | n.s |
| DXA LS-BMD (g/cm²) | 0.984 ± 0.180 | 0.906 ± 0.142 | 0.01 |
| DXA FN-BMD (g/cm²) | 0.735 ± 0.131 | 0.699 ± 0.118 | n.s |
| DXA TH-BMD (g/cm²) | 0.860 ± 0.123 | 0.809 ± 0.112 | 0.01 |
| REMS LS-BMD (g/cm²) | 0.812 ± 0.106 | 0.841 ± 0.090 | n.s |
| REMS FN-BMD (g/cm²) | 0.632 ± 0.120 | 0.636 ± 0.059 | n.s |
| REMS TH-BMD (g/cm²) | 0.758 ± 0.137 | 0.770 ± 0.067 | n.s |
BMD T-Score at Different Skeletal Sites (DXA vs REMS)

A graph comparing BMD T-scores for DXA and REMS at the lumbar spine (LS), femoral neck (FN), and total hip (TH) in T2DM patients. REMS measurements showed lower BMD T-scores compared to DXA, particularly at the lumbar spine.
| Table 2. Age and BMI-adjusted partial correlations of BMD values by DXA and REMS technique with HbA1c serum level and T2DM duration | ||
|---|---|---|
| BMD Measurement | HbA1c (%) | T2DM duration (years) |
| DXA BMD-LS (g/cm²) | -0.22* | -0.09 |
| REMS BMD-LS (g/cm²) | -0.07 | -0.21* |
| DXA BMD-FN (g/cm²) | -0.24* | 0.04 |
| REMS BMD-FN (g/cm²) | -0.04 | -0.24* |
| DXA BMD-TH (g/cm²) | -0.26* | -0.27* |
| REMS BMD-TH (g/cm²) | -0.07 | -0.20 |
* p < 0.05
Osteoporosis Classification: T2DM women were classified as osteoporotic by DXA in 28% of cases, while REMS identified 47% as osteoporotic. The percentage of women classified as osteopenic or normal by DXA was higher compared to REMS.
Percentage of T2DM Women Classified as Osteoporotic, Osteopenic, or Normal (DXA vs REMS)

A bar chart showing the classification of T2DM women as osteoporotic, osteopenic, or normal based on DXA and REMS T-scores. REMS identified a higher percentage of T2DM women as osteoporotic compared to DXA.
Fracture History and BMD Correlation: Twenty-two (25%) T2DM women had a history of low-trauma fractures. T2DM women with fractures had significantly lower BMD at the lumbar spine by REMS (p < 0.05), but not by DXA.
Comparison of BMD at Lumbar Spine by DXA and REMS in T2DM Patients with and Without Fractures

A comparative chart showing BMD values at the lumbar spine by DXA and REMS in T2DM patients with and without prior fragility fractures. T2DM women with fractures exhibited lower BMD readings on REMS.
Discussion
This study is the first to assess the use of REMS in identifying osteoporosis in T2DM women. The findings suggest that REMS provides a more accurate classification of osteoporosis compared to DXA, particularly in identifying osteoporotic individuals. The use of REMS could improve the diagnosis of bone fragility in T2DM patients by detecting changes in bone quality that DXA does not.
Implications for Clinical Practice: With T2DM increasing in prevalence and associated with a higher risk of fractures despite higher or normal BMD, it is crucial to adopt diagnostic tools that can detect bone quality. REMS, with its non-ionizing radiation and ability to assess axial sites, provides a promising alternative to DXA.
The study also indicates that REMS could be better than DXA in assessing fracture risk, as evidenced by lower BMD values in T2DM women with fragility fractures. This may be due to the ability of REMS to detect structural changes in the bone that are not visible with DXA.
Conclusions
REMS technology may offer an improved method for diagnosing osteoporosis and predicting fracture risk in T2DM patients. By providing a more accurate assessment of bone quality, REMS could become an essential tool in managing bone health in diabetic populations. Further studies are needed to confirm these findings and explore additional parameters related to bone strength.