OBJECTIVE—To establish a bedside test with ultrasonography for evaluation of foot muscle atrophy in diabetic patients.

RESEARCH DESIGN AND METHODS—Thickness and cross-sectional area (CSA) of the extensor digitorum brevis muscle (EDB) and of the muscles of the first interstitium (MILs) were determined in 26 diabetic patients and in 26 matched control subjects using ultrasonography. To estimate the validity, findings were related to the total volume of all foot muscles determined at magnetic resonance imaging (MRI-FMvol). Furthermore, the relations of ultrasonographic estimates to nerve conduction, sensory perception thresholds, and clinical condition were established.

RESULTS—In diabetic patients, the ultrasonographic thickness of EDB (U-EDBt) was (means ± SD) 6.4 ± 2.1 vs. 9.0 ± 1.0 mm in control subjects (P < 0.001), the thickness of MIL (U-MILt) was 29.6 ± 8.3 vs. 40.2 ± 3.6 mm in control subjects (P < 0.001), and the CSA of EDB (U-EDBCSA) was 116 ± 65 vs. 214 ± 38 mm2 in control subjects (P < 0.001). The MRI-FMvol was directly related to U-EDBt (r = 0.77), U-MILt (r = 0.71), and U-EDBCSA (r = 0.74). U-EDBt and U-MILt were thinner in neuropathic than in nonneuropathic diabetic patients (5.8 ± 2.1 vs. 7.5 ± 1.7 mm [P < 0.05] and 28.3 ± 8.8 vs. 35.6 ± 4.3 mm [P < 0.03], respectively).

CONCLUSIONS—Atrophy of intrinsic foot muscles determined at ultrasonography is directly related to foot muscle volume determined by MRI and to various measures of diabetic neuropathy. Ultrasonography seems to be useful for detection of foot muscle atrophy in diabetes.

Motor dysfunction is an established part of diabetic polyneuropathy, resulting in distal atrophy and weakness. At the clinical examination, foot deformities clearly indicate muscle atrophy, whereas detection of atrophy at earlier stages is difficult.

Atrophy of small foot muscles has been reported using magnetic resonance imaging (MRI) (13). Due to excellent soft-tissue contrast, MRI enables detection of even subtle changes in size and structure of foot muscles (13). In a previous study (1), we found substantial atrophy in neuropathic patients without any foot deformity, whereas muscle volume was preserved in nonneuropathic diabetic patients. Recently, a study using 31P MRI at 3 Tesla observed minor loss of muscle tissues in nonneuropathic patients (3).

MRI is the gold standard for visualization of soft-tissue structures in the foot due to its high spatial resolution enabling identification of the individual small foot muscles (2). However, MRI is time consuming, cannot be performed bedside, and is more expensive than ultrasonography. Ultrasonography is an established method for examination of various musculoskeletal structures in children and adults with chronic neuromuscular diseases and traumatic muscle injuries (46). Also, animal experiments in acute muscle denervation indicate consistency between MRI, electromyography, and ultrasonography 1–64 days after denervation (7).

In the present study, the size of individual foot muscles was examined with ultrasonography in diabetic patients with and without neuropathy and in matched control subjects compared with the total volume of all foot muscles determined by MRI.

Twenty-six diabetic patients (22 with type 1 and 4 with type 2 diabetes) and 26 control subjects matched for age, sex, height, and weight were included in the study. Demographic and baseline clinical data are shown in Table 1. Patients were recruited from the outpatient diabetes clinic, and control subjects were recruited among hospital staffs. All patients were able to walk unsupported, and none had a history of foot surgery or had symptoms or signs of arterial insufficiency of the lower extremities.

Patients with severe cardiac or lung disease, cancer, alcoholism, acute or chronic musculoskeletal disease, other neurological disease, other endocrine disorders, or symptomatic peripheral artery disease were excluded. All subjects gave informed consent to the study, which was approved by the local ethics committee.

All ultrasonographic examinations were made by the same examiner (K.S.) using a scanner with a linear array real-time ultrasonic probe (Toshiba Powervision 6000 duplex). The subjects were placed in a supine position with the nondominant foot placed on a plastic ramp to keep the ankle joint in a neutral position.

At ultrasonographic evaluation, the extensor digitorum brevis muscle (EDB) and the muscle group between the first and second metatarsal bone (MIL), including the first dorsal interosseus muscle, the adductor hallucis muscle, and the first lumbrical muscle, could be unambigiously identified. The EDB thickness (U-EDBt) and cross-sectional area (U-EDBCSA) was determined by scanning transverse to the muscle fibers (Fig. 1), whereas the MIL (U-MILt) was scanned longitudinal to the fibers (Fig. 1). The frequency of the ultrasonic beam was 15 MHz for the EDB and 8 MHz for the MIL. In each case, the position of the ultrasound probe was marked externally on the skin using easily defined bone landmarks.

For evaluation of the EDB muscle, a line drawn perpendicular to the midpoint of a straight line between the lateral malleolus and the tuberositas of the fifth metatarsal bone defined the scanning plane. The exact position along this line for maximum cross-sectional muscle thickness differs between individuals and was defined at each scanning procedure. For examination of the MIL, the distal position of the ultrasound probe was defined by a line between the first and second metatarso-phalangeal joint and two lines marking the first and second metatarsal bone.

The ultrasonographic measurements were performed with the ultrasound probe perpendicular to the muscle surface, gently placed on the skin to avoid any pressure-induced alterations of muscle tissue dimension using generous amounts of gel (ULTRA/PHONIC conductivity gel; Pharmaceutical Innovations, Newark, NJ). During ultrasonographic scanning, the patients were initially asked to perform a voluntary contraction of the muscles facilitating the definition of the borders of the muscle. Then, the patient was asked to relax while the ultrasonographic image was recorded. For each parameter, five measurements were made. The images were saved on a magneto-optical media for digital storage for later analysis on a personal computer. Afterward, the lowest and highest values were excluded, and the average of the remaining values was used for further analysis. The average time spent for ultrasonography was 5 min for preparation of the scanning session and identification and demarcation of the bone landmarks followed by 10–15 min for making the 15 ultrasonographic measurements.

The nondominant foot of all patients and control subjects was visualized by MRI using a 1.5-Tesla scanner (Sigma GE), adopting the principles for MRI estimation of foot muscle size as described in earlier studies (2). All magnetic resonance scans were obtained with a conventional T1-weighted Spin-Echo sequence (echo time = 20 ms, repetition time = 540 ms) using cross-sectional magnetic resonance images with a slice thickness of 1.5 mm and an intersection interval of 10 mm. A 256 × 256 matrix and two excitations were used. The images were stored on a personal computer and transferred from the 256 × 256 matrix to a 512 × 512 bitmap color picture. The identity of the magnetic resonance images was blinded to the observer. Within the muscle compartments, an upper level of signal intensity for muscle tissues was defined for each patient by the examiner because a fixed limit could not be applied due to autoscaling. Signal intensities above the upper level were defined as signal intensities of fat, allowing separation of muscle tissues from “nonmuscle tissues” within the muscle compartments. Muscle fasciae, tendons, and blood vessels were excluded. At each image, the cross-sectional area (CSA) of all muscles was estimated using a stereological point-counting technique described elsewhere (1,8,9). The total volume of all foot muscles (MRI-FMvol) was calculated by multiplying the distance (10 mm) between the sections by the total CSA, the first section being randomly placed within the first interslice interval. It was not possible to study the same muscles at MRI and ultrasonography because the largest CSA could not be determined beforehand at MRI. Furthermore, it was difficult to obtain enough slices to ensure a reliable estimate using the point-counting technique (9).

All patients were clinically evaluated according to a neuropathy symptom score (10) and a neurological impairment scale (NIS) (11). Vibratory perception thresholds were evaluated at the dorsum part of the dominant index finger and the nondominant great toe using the 4, 2, and 1 stepping algorithm (12) (CASE IV; WR Medical Electronics, Stillwater, MN). The perception thresholds for each patient were compared with results from a large group of healthy control subjects (CASE IV) (P. J. Dyck, unpublished data).

Nerve conduction studies were performed using an electromyograph (KeyPoint; Medtronic, Skovlunde, Denmark) and standard methods as described elsewhere (13,14). Motor conduction velocity (MNCV) and amplitude of the compound muscle action potential were measured of the nondominant peroneal and tibial nerve. Sensory nerve conduction velocity (SNCV) and sensory nerve amplitude of the sensory nerve action potential were measured of the nondominant sural nerve, skin temperatures ranging between 31 and 34 centigrades. Z scores reflecting the degree of deviation from the expected mean were calculated for MNCV and SNCV using values of healthy volunteers obtained with similar techniques (13,14).

Patients were defined as neuropathic in accordance with the minimal criteria for diabetic neuropathy (15). For quantification of severity of neuropathy, a neuropathy rank-sum score was calculated for each patient, including rank scores of the neuropathy symptom score, the NIS, the vibratory perception thresholds, and the average of the rank scores of the MNCVs and SNCVs (1).

Statistical comparisons of muscle size determined at ultrasonography and at MRI between groups were made with unpaired t tests, and correlations were sought for using linear regression analysis. Microsoft Excel was applied for the statistical comparisons using a significance level of 0.05. Reproducibility analyses of the five ultrasononographic measurements were performed with ANOVA using STATA.

According to the minimal criteria for diabetic neuropathy, 17 patients were neuropathic and 9 patients were nonneuropathic. Among the 17 neuropathic patients, 13 patients were symptomatic. Patients with and without neuropathy had a median diabetes duration of 32 years (range 8–46) and 31 years (14–49), respectively.

For all diabetic patients, the NIS has a median of 13 (range 0–40). The neuropathic and nonneuropathic patients had an NIS of 20 (2–40) vs. 2 (0–17), respectively (P < 0.001). Furthermore, the neuropathic patients had significantly higher vibratory perception threshold, lower peroneal MNCV, and lower peroneal compound muscle action potential compared with the nonneuropathic patients (Table 1).

In patients, mean U-EDBCSA was (means ± SD) 116 ± 65 vs. 214 ± 38 mm2 in control subjects (P < 0.001), U-EDBt was 6.4 ± 2.1 vs. 9.0 ± 1.0 mm in control subjects (P < 0.001), and U-MILt was 29.6 ± 8.3 vs. 40.2 ± 3.6 mm in control subjects (P < 0.001). For the neuropathic and nonneuropathic patients, U-EDBCSA, U-EDBt, and MRI-FMvol expressed as a percentage of individually matched control subjects were significantly reduced (Table 2). The reduction of U-MILt reached significance in the neuropathic patients only (Table 2). Comparing the neuropathic and nonneuropathic patients, U-EDBCSA, U-MILt, and MRI-FMvol were significantly reduced in the neuropathic patients compared with the nonneuropathic diabetic patients (Table 2).

Close correlations were found between the distally placed U-MILt and the proximally placed U-EDBCSA and U-EDBt in the neuropathic group and in the nonneuropathic group as well (online appendix Table 3 [available at http://dx.doi.org/10.2337/dc07-0108]).

For diabetic patients and healthy control subjects, close relationships could be established between MRI-FMvol on the one side and U-EDBCSA (r = 0.74 and r = 0.64), U-EDBt (r = 0.77 and r = 0.76), and U-MILt (r = 0.71 and r = 0.58) on the other side (Tables 3 and 4 and Fig. 2 of the online appendix). Reproducibility analysis of the five repeated ultrasonographic measurements using ANOVA showed a coefficient of variation of U-EDBCSA, U-EDBt, and U-MILt, amounting to 0.031, 0.034, and 0.015, respectively, in control subjects and 0.046, 0.059, and 0.026, respectively, in diabetic patients.

In all patients, close correlations were found between the neuropathy rank-sum score and the ultrasonographic measurements of U-EDBCSA (r = −0.76), U-EDBt (r = −0.73), and U-MILt (r = −0.71). Results of regression analyses performed for the neuropathic and nonneuropathic subgroups are shown in Fig. 2 and Table 3 of the online appendix.

In this study, ultrasonography could detect atrophy of individual foot muscles in a group of diabetic patients. Muscular atrophy was more pronounced in diabetic patients with clinical neuropathy. In addition, a significant reduction of muscle size was observed in nonneuropathic diabetic patients. Close relationships were found between ultrasonographic estimates of foot muscle size and MRI-determined volume of all foot muscles. Furthermore, ultrasonographic measurements of foot muscle size were closely related to the clinical severity of neuropathy in diabetic patients when expressed with a neuropathy rank-sum score.

In previous studies (8,9), substantial muscular atrophy has been found in diabetic patients with neuropathy. There was a proximal to distal gradient of atrophy at the leg (8), and pronounced atrophy of the foot muscles in diabetic subjects with neuropathy have been found in recent studies (13) using different MRI techniques. Brash et al. (16) observed increased fatty infiltration as well as indications of muscle fiber depletion of the intrinsic foot muscles at the first metatarsal joint in 19 patients suffering from diabetic neuropathy using MRI and magnetization transfer sequences. The quantitative techniques in that study are not comparable with those used in the present study because the magnetization transfer method provides an indirect estimate of muscle size. The method, however, has the potential to discover even subtle tissue changes in non-neuropathic diabetic patients. Using standard MRI techniques and analysis of single-pixel relaxation times, Bus et al. (2) found atrophy of the intrinsic foot muscles at the level of the metatarsal heads in eight diabetic patients with neuropathy, amounting to a 73% reduction of muscle CSA. In our study, less pronounced atrophy was observed, the U-MIL and MRI-FMvol muscle size amounting to 71 and 42% of the matched control subjects, respectively. In a previous study, we found pronounced atrophy of all foot muscles with reduction in the total muscle volume of 15 patients suffering from diabetic neuropathy using traditional MRI technique combined with unbiased stereological methods (1). Greenman et al. (3) used 31P RARE MRI and found significant foot muscle atrophy at the level of the metatarsal joint not only in neuropathic patients but also in diabetic patients without clinical neuropathy. Their finding suggests that muscular atrophy may occur very early in the neuropathic process even before the minimal criteria of diabetic neuropathy are fulfilled. In accordance with their observation, we found a statistically significant reduction in total foot muscle volume in non-neuropathic patients. These observations suggest that even subtle changes in nerve function may lead to muscle loss and that the applied clinical criteria for neuropathy are too insensitive for detection of the earliest neuropathic changes.

In this study we have introduced ultrasonography as a new method to estimate the size of foot muscles. We found that the ultrasonographic method had high reproducibility with a coefficient of variation ≤0.06 for all muscles evaluated. Ultrasonography has been used in evaluation of muscular dystrophies (1720) and other neuromuscular diseases in adults (2123). Comparative studies of ultrasonography and MRI indicate that the lower spatial resolution in ultrasonography is in part compensated for by its bedside availability and higher cost-effectiveness (20,24,25). In a study by Küllmer et al. (7) in experimental denervated rabbits, MRI and sonography were equally informative.

In our study, the foot muscles were evaluated differently applying MRI and ultrasonography. At ultrasonography the thickness and CSA of the whole muscle of interest was determined, whereas at MRI the tissue with increased signal intensity within the muscles reflecting degeneration was excluded from the analysis of the volume of the foot muscles. Therefore, the ultrasonographic measurements might underestimate the degree of loss of muscle tissue.

In Fig. 2 of the online appendix, there is a close correlation between MRI-FMvol and U-EDBCSA; however, this does not necessarily imply that there is a high level of agreement comparing these two methods (26). In our study, we applied two different visualization techniques on different muscle structures including a single foot muscle and all foot muscles, respectively. Since different muscular structures were evaluated, a direct analysis of limits of agreement was not performed.

A frequent objection to quantification of structures using ultrasonography is the operator dependency. However, in a study by Bargfrede et al. (21) investigating focal neuropathies, an interobserver correlation of 0.85 of measurements of muscle size was obtained after scanning of several muscles. In accordance with this observation, Maurits et al. (27) found an interobserver correlation of 0.845 at determination of the thickness of the biceps brachii muscles. Furthermore, Maurits et al. found an intraobserver correlation coefficient of 0.93, confirming the observations made by Reimers et al. in idiopathic inflamatory myopathies (test-retest) (28).

In the present study, five measurements at each of the various scanning positions were performed to obtain information about the variation of the estimate. In the clinical setting, however, one or two standardized measurements are sufficient for an experienced examiner. The costs for ultrasonographic evaluation are low because the equipment is affordable and needs one operator only.

In the present study, we evaluated the size of small foot muscles at a proximal and at a distal position. The two muscles evaluated (EDB and MIL) are innervated from branches of the peroneal and tibial nerves. The examination of the two muscles with different nerve supply ensures that atrophy of the EDB muscle was not due to compression of the peroneal nerve at the fibular head. The close correlations between the size of the two muscle groups and the volume of all foot muscles suggest that all measures reflect the same pathophysiological process.

During ultrasonographic scanning of the MIL muscles, segmentation of individual muscles was not feasible. However, strong correlations were established between MRI-FMvol and the MIL muscle group, indicating that ultrasonographic estimates reflect atrophy of individual muscles. The ultrasonography technique has the advantage that it can be performed in almost all patients. The technique is noninvasive and requires some experience of the examiner to obtain robust and reproducible results. The present study suggests that ultrasonography is a reliable technique for screening and monitoring of muscle atrophy in the diabetic foot. Despite its lower resolution, this method supplies the examiner with sufficient anatomical and functional information for evaluation of muscle size.

Figure 1—

A: Ultrasonographic image of CSA of the EDB muscle (U-EDB-CSA) and thickness of the EDB muscle (U-EDBt). B: Ultrasonographic image of thickness of the first dorsal interosseus muscle, the adductor hallucis muscle, and the first lumbrical muscle (U-MILt).

Figure 1—

A: Ultrasonographic image of CSA of the EDB muscle (U-EDB-CSA) and thickness of the EDB muscle (U-EDBt). B: Ultrasonographic image of thickness of the first dorsal interosseus muscle, the adductor hallucis muscle, and the first lumbrical muscle (U-MILt).

Close modal
Table 1—

Clinical and electrophysiologic findings in diabetic patients and control subjects

nAge (years)Weight (kg)Height (cm)Male/ femaleType 1/ type 2 diabetesDiabetes duration (years)A1C (%)Vibratory perception threshold (first toe) (JND)NISPeroneal MNCV (m/s)Peroneal CMAP (mV)
Diabetic patients 26 50 (26–64) 73 (56–104) 176 (158–190) 16/10 21/4 32 (8–49) 8.9 (6.4–11.3) 22 (14–25) 13 (0–40) 36 (23–48) 3 (0–10) 
    With diabetic neuropathy 17 47 (26–64) 72 (60–95) 175 (158–190) 10/7 15/2 32 (8–46) 9.1 (6.4–11.3) 22 (14–25) 20 (2–40) 35 (23–41) 2 (0–4) 
    Without diabetic neuropathy 49 (37–63) 72 (56–104) 175 (167–187) 6/3 7/2 31 (14–49) 8.1 (6.5–9.5) 19 (15–21) 2 (0–17) 44 (43–48) 6 (1–10) 
Control subjects 26 49 (25–67) 78 (54–102) 176 (160–185) 16/10 — — — — — — — 
nAge (years)Weight (kg)Height (cm)Male/ femaleType 1/ type 2 diabetesDiabetes duration (years)A1C (%)Vibratory perception threshold (first toe) (JND)NISPeroneal MNCV (m/s)Peroneal CMAP (mV)
Diabetic patients 26 50 (26–64) 73 (56–104) 176 (158–190) 16/10 21/4 32 (8–49) 8.9 (6.4–11.3) 22 (14–25) 13 (0–40) 36 (23–48) 3 (0–10) 
    With diabetic neuropathy 17 47 (26–64) 72 (60–95) 175 (158–190) 10/7 15/2 32 (8–46) 9.1 (6.4–11.3) 22 (14–25) 20 (2–40) 35 (23–41) 2 (0–4) 
    Without diabetic neuropathy 49 (37–63) 72 (56–104) 175 (167–187) 6/3 7/2 31 (14–49) 8.1 (6.5–9.5) 19 (15–21) 2 (0–17) 44 (43–48) 6 (1–10) 
Control subjects 26 49 (25–67) 78 (54–102) 176 (160–185) 16/10 — — — — — — — 

Data are median(range). CMAP, compound muscle action potential; JND, just noticeable difference.

Table 2—

Muscle size (%) in diabetic patients with and without neuropathy relative to muscle size of individually matched control subjects

Diabetic patients with neuropathyDiabetic patients without neuropathyP value (diabetic patients with and without neuropathy are compared)
U-EDBCSA (mm250 ± 33 79 ± 27 0.05 
U-EDBt (mm) 66 ± 26 85 ± 21 NS 
U-MILt (mm) 71 ± 22 90 ± 8.2 0.01 
MRI-FMvol (mm342 ± 30 74 ± 34 0.05 
Diabetic patients with neuropathyDiabetic patients without neuropathyP value (diabetic patients with and without neuropathy are compared)
U-EDBCSA (mm250 ± 33 79 ± 27 0.05 
U-EDBt (mm) 66 ± 26 85 ± 21 NS 
U-MILt (mm) 71 ± 22 90 ± 8.2 0.01 
MRI-FMvol (mm342 ± 30 74 ± 34 0.05 

Data are means ± SD. U-EDBCSA, CSA of EDB muscle; U-EDBt, thickness of EDB muscle; U-MILt, thickness of MIL; MRI-FMvol, total volume of all foot muscles.

The Danish Diabetes Association (Diabetesforeningen) and the Danish Foundation of Neurological Research (Neurologisk Forskningsfond) are acknowledged for economic support.

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Published ahead of print at http://care.diabetesjournals.org on 23 August 2007. DOI: 10.2337/dc07-0108.

Additional information for this article can be found in an online appendix at http://dx.doi.org/10.2337/dc07-0108.

A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C Section 1734 solely to indicate this fact.