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Published in: Diabetologia 6/2009

01-06-2009 | Article

Accelerated atrophy of lower leg and foot muscles—a follow-up study of long-term diabetic polyneuropathy using magnetic resonance imaging (MRI)

Authors: C. S. Andreassen, J. Jakobsen, S. Ringgaard, N. Ejskjaer, H. Andersen

Published in: Diabetologia | Issue 6/2009

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Abstract

Aims/hypothesis

The aim of the study was to determine the loss of muscle volume in the lower leg and foot in long-term diabetic patients in relation to the presence of neuropathy.

Methods

We re-examined 26 type 1 diabetic patients who had participated in magnetic resonance imaging (MRI) studies on muscle volume in the lower leg and foot 9 to 12 years earlier. Re-examination involved MRI, isokinetic dynamometry, clinical examination, electrophysiological studies and quantitative sensory examinations.

Results

Annual loss of muscle volume of ankle dorsal and plantar flexors was 4.5 (5.5–3.9)% (median [range]) and 5.0 (7.0–4.2)% in neuropathic patients, 1.9 (3.2–1.0)% and 1.8 (2.6–1.3)% in non-neuropathic patients, and 1.7 (2.8–0.8)% and 1.8 (2.4–0.8)% in controls, respectively (p < 0.01). Annual change of volume and strength correlated for ankle dorsal flexors (r s = 0.73, p < 0.01) and for ankle plantar flexors (r s = 0.63, p < 0.05) in diabetic patients. In addition, annual change of muscle volume for dorsal and plantar flexors was related to the combined score of all measures of neuropathy (r s = −0.68, p < 0.02 and r s = −0.73, p < 0.01, respectively). Foot muscle volume declined annually by 3.0 (3.4–1.0)% in neuropathic patients and by 1.1 (4.0–0.2)% in non-neuropathic patients, both values being significantly different from controls (0.2 [−2.5 to 2.4]%). Loss of foot muscle volume was related to severity of neuropathy assessed at clinical evaluation (r s = −0.6, p < 0.05).

Conclusions/interpretation

Muscular atrophy in long-term diabetic neuropathy occurs early in the feet, progresses steadily in the lower legs, relates to severity of neuropathy and leads to weakness at the ankle.
Literature
1.
go back to reference Menz HB, Lord SR, St George R, Fitzpatrick RC (2004) Walking stability and sensorimotor function in older people with diabetic peripheral neuropathy. Arch Phys Med Rehabil 85:245–252PubMedCrossRef Menz HB, Lord SR, St George R, Fitzpatrick RC (2004) Walking stability and sensorimotor function in older people with diabetic peripheral neuropathy. Arch Phys Med Rehabil 85:245–252PubMedCrossRef
2.
go back to reference Akashi PM, Sacco IC, Watari R, Hennig E (2008) The effect of diabetic neuropathy and previous foot ulceration in EMG and ground reaction forces during gait. Clin Biomech (Bristol, Avon) 23:584–592CrossRef Akashi PM, Sacco IC, Watari R, Hennig E (2008) The effect of diabetic neuropathy and previous foot ulceration in EMG and ground reaction forces during gait. Clin Biomech (Bristol, Avon) 23:584–592CrossRef
3.
go back to reference Abboud RJ, Rowley DI, Newton RW (2000) Lower limb muscle dysfunction may contribute to foot ulceration in diabetic patients. Clin Biomech (Bristol, Avon) 15:37–45CrossRef Abboud RJ, Rowley DI, Newton RW (2000) Lower limb muscle dysfunction may contribute to foot ulceration in diabetic patients. Clin Biomech (Bristol, Avon) 15:37–45CrossRef
4.
go back to reference Caselli A, Pham H, Giurini JM, Armstrong DG, Veves A (2002) The forefoot-to-rearfoot plantar pressure ratio is increased in severe diabetic neuropathy and can predict foot ulceration. Diabetes Care 25:1066–1071PubMedCrossRef Caselli A, Pham H, Giurini JM, Armstrong DG, Veves A (2002) The forefoot-to-rearfoot plantar pressure ratio is increased in severe diabetic neuropathy and can predict foot ulceration. Diabetes Care 25:1066–1071PubMedCrossRef
5.
go back to reference Andersen H, Poulsen PL, Mogensen CE, Jakobsen J (1996) Isokinetic muscle strength in long-term IDDM patients in relation to diabetic complications. Diabetes 45:440–445PubMedCrossRef Andersen H, Poulsen PL, Mogensen CE, Jakobsen J (1996) Isokinetic muscle strength in long-term IDDM patients in relation to diabetic complications. Diabetes 45:440–445PubMedCrossRef
6.
go back to reference Andersen H, Nielsen S, Mogensen CE, Jakobsen J (2004) Muscle strength in type 2 diabetes. Diabetes 53:1543–1548PubMedCrossRef Andersen H, Nielsen S, Mogensen CE, Jakobsen J (2004) Muscle strength in type 2 diabetes. Diabetes 53:1543–1548PubMedCrossRef
7.
go back to reference Andreassen CS, Jakobsen J, Andersen H (2006) Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes 55:806–812PubMedCrossRef Andreassen CS, Jakobsen J, Andersen H (2006) Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes 55:806–812PubMedCrossRef
8.
go back to reference Andersen H, Gadeberg PC, Brock B, Jakobsen J (1997) Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study. Diabetologia 40:1062–1069PubMedCrossRef Andersen H, Gadeberg PC, Brock B, Jakobsen J (1997) Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study. Diabetologia 40:1062–1069PubMedCrossRef
9.
go back to reference Andersen H, Gjerstad MD, Jakobsen J (2004) Atrophy of foot muscles: a measure of diabetic neuropathy. Diabetes Care 27:2382–2385PubMedCrossRef Andersen H, Gjerstad MD, Jakobsen J (2004) Atrophy of foot muscles: a measure of diabetic neuropathy. Diabetes Care 27:2382–2385PubMedCrossRef
10.
go back to reference Bus SA, Yang QX, Wang JH, Smith MB, Wunderlich R, Cavanagh PR (2002) Intrinsic muscle atrophy and toe deformity in the diabetic neuropathic foot: a magnetic resonance imaging study. Diabetes Care 25:1444–1450PubMedCrossRef Bus SA, Yang QX, Wang JH, Smith MB, Wunderlich R, Cavanagh PR (2002) Intrinsic muscle atrophy and toe deformity in the diabetic neuropathic foot: a magnetic resonance imaging study. Diabetes Care 25:1444–1450PubMedCrossRef
11.
go back to reference Greenman RL, Khaodhiar L, Lima C, Dinh T, Giurini JM, Veves A (2005) Foot small muscle atrophy is present before the detection of clinical neuropathy. Diabetes Care 28:1425–1430PubMedCrossRef Greenman RL, Khaodhiar L, Lima C, Dinh T, Giurini JM, Veves A (2005) Foot small muscle atrophy is present before the detection of clinical neuropathy. Diabetes Care 28:1425–1430PubMedCrossRef
12.
go back to reference Andersen H, Stalberg E, Gjerstad MD, Jakobsen J (1998) Association of muscle strength and electrophysiological measures of reinnervation in diabetic neuropathy. Muscle Nerve 21:1647–1654PubMedCrossRef Andersen H, Stalberg E, Gjerstad MD, Jakobsen J (1998) Association of muscle strength and electrophysiological measures of reinnervation in diabetic neuropathy. Muscle Nerve 21:1647–1654PubMedCrossRef
13.
go back to reference Dyck PJ, Kratz KM, Lehman KA et al (1991) The Rochester Diabetic Neuropathy Study: design, criteria for types of neuropathy, selection bias, and reproducibility of neuropathic tests. Neurology 41:799–807PubMed Dyck PJ, Kratz KM, Lehman KA et al (1991) The Rochester Diabetic Neuropathy Study: design, criteria for types of neuropathy, selection bias, and reproducibility of neuropathic tests. Neurology 41:799–807PubMed
14.
go back to reference Ferner H, Staubesand J (1982) Sobotta atlas of human anatomy 2. Urban and Schwarzenberg, Munich Ferner H, Staubesand J (1982) Sobotta atlas of human anatomy 2. Urban and Schwarzenberg, Munich
15.
go back to reference Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229–263PubMed Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229–263PubMed
16.
go back to reference Andersen H (1996) Reliability of isokinetic measurements of ankle dorsal and plantar flexors in normal subjects and in patients with peripheral neuropathy. Arch Phys Med Rehabil 77:265–268PubMedCrossRef Andersen H (1996) Reliability of isokinetic measurements of ankle dorsal and plantar flexors in normal subjects and in patients with peripheral neuropathy. Arch Phys Med Rehabil 77:265–268PubMedCrossRef
17.
go back to reference Dyck PJ (1993) Quantitating severity of neuropathy. In: Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF (eds) Peripheral neuropathy. Saunders, Philadelphia, pp 686–697 Dyck PJ (1993) Quantitating severity of neuropathy. In: Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF (eds) Peripheral neuropathy. Saunders, Philadelphia, pp 686–697
18.
go back to reference Dyck PJ, O’Brien PC, Kosanke JL, Gillen DA, Karnes JL (1993) A 4, 2, and 1 stepping algorithm for quick and accurate estimation of cutaneous sensation threshold. Neurology 43:1508–1512PubMed Dyck PJ, O’Brien PC, Kosanke JL, Gillen DA, Karnes JL (1993) A 4, 2, and 1 stepping algorithm for quick and accurate estimation of cutaneous sensation threshold. Neurology 43:1508–1512PubMed
19.
go back to reference Stalberg E, Falck B (1993) Clinical motor nerve conduction studies. Methods Clin Neurophysiol 4:61–80 Stalberg E, Falck B (1993) Clinical motor nerve conduction studies. Methods Clin Neurophysiol 4:61–80
20.
go back to reference Falck B, Stalberg E, Bischoff C (1994) Sensory nerve conduction studies with surface electrodes. Methods Clin Neurophysiol 5:1–20 Falck B, Stalberg E, Bischoff C (1994) Sensory nerve conduction studies with surface electrodes. Methods Clin Neurophysiol 5:1–20
21.
go back to reference The Diabetic Retinopathy Study Research Group (1981) A modification of the Airlie House classification of diabetic retinopathy (DRS report no. 7). Invest Ophthalmol Vis Sci 21:210–226 The Diabetic Retinopathy Study Research Group (1981) A modification of the Airlie House classification of diabetic retinopathy (DRS report no. 7). Invest Ophthalmol Vis Sci 21:210–226
22.
go back to reference Dyck PJ, Davies JL, Litchy WJ, O’Brien PC (1997) Longitudinal assessment of diabetic polyneuropathy using a composite score in the Rochester Diabetic Neuropathy Study cohort. Neurology 49:229–239PubMed Dyck PJ, Davies JL, Litchy WJ, O’Brien PC (1997) Longitudinal assessment of diabetic polyneuropathy using a composite score in the Rochester Diabetic Neuropathy Study cohort. Neurology 49:229–239PubMed
23.
go back to reference Fransson A, Andreo P, Potter R (2001) Aspects of MR image distortions in radiotherapy treatment planning. Strahlenther Onkol 177:59–73PubMedCrossRef Fransson A, Andreo P, Potter R (2001) Aspects of MR image distortions in radiotherapy treatment planning. Strahlenther Onkol 177:59–73PubMedCrossRef
24.
go back to reference McDermott MM, Hoff F, Ferrucci L et al (2007) Lower extremity ischemia, calf skeletal muscle characteristics, and functional impairment in peripheral arterial disease. J Am Geriatr Soc 55:400–406PubMedCrossRef McDermott MM, Hoff F, Ferrucci L et al (2007) Lower extremity ischemia, calf skeletal muscle characteristics, and functional impairment in peripheral arterial disease. J Am Geriatr Soc 55:400–406PubMedCrossRef
25.
go back to reference McDermott MM, Tian L, Ferrucci L et al (2008) Associations between lower extremity ischemia, upper and lower extremity strength, and functional impairment with peripheral arterial disease. J Am Geriatr Soc 56:724–729PubMedCrossRef McDermott MM, Tian L, Ferrucci L et al (2008) Associations between lower extremity ischemia, upper and lower extremity strength, and functional impairment with peripheral arterial disease. J Am Geriatr Soc 56:724–729PubMedCrossRef
26.
go back to reference Dolan NC, Liu K, Criqui MH et al (2002) Peripheral artery disease, diabetes, and reduced lower extremity functioning. Diabetes Care 25:113–120PubMedCrossRef Dolan NC, Liu K, Criqui MH et al (2002) Peripheral artery disease, diabetes, and reduced lower extremity functioning. Diabetes Care 25:113–120PubMedCrossRef
27.
go back to reference Park SW, Goodpaster BH, Strotmeyer ES et al (2007) Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care 30:1507–1512PubMedCrossRef Park SW, Goodpaster BH, Strotmeyer ES et al (2007) Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care 30:1507–1512PubMedCrossRef
28.
go back to reference Shields RW Jr (1987) Single-fiber electromyography is a sensitive indicator of axonal degeneration in diabetes. Neurology 37:1394–1397PubMed Shields RW Jr (1987) Single-fiber electromyography is a sensitive indicator of axonal degeneration in diabetes. Neurology 37:1394–1397PubMed
29.
go back to reference Bril V, Werb MR, Greene DA, Sima AA (1996) Single-fiber electromyography in diabetic peripheral polyneuropathy. Muscle Nerve 19:2–9PubMedCrossRef Bril V, Werb MR, Greene DA, Sima AA (1996) Single-fiber electromyography in diabetic peripheral polyneuropathy. Muscle Nerve 19:2–9PubMedCrossRef
30.
go back to reference Meijer JW, Lange F, Links TP, van der Hoeven JH (2008) Muscle fiber conduction abnormalities in early diabetic polyneuropathy. Clin Neurophysiol 119:1379–1384PubMedCrossRef Meijer JW, Lange F, Links TP, van der Hoeven JH (2008) Muscle fiber conduction abnormalities in early diabetic polyneuropathy. Clin Neurophysiol 119:1379–1384PubMedCrossRef
31.
go back to reference van der Hoeven JH, Zwarts MJ, van Weerden TW (1993) Muscle fiber conduction velocity in amyotrophic lateral sclerosis and traumatic lesions of the plexus brachialis. Electroencephalogr Clin Neurophysiol 89:304–310PubMedCrossRef van der Hoeven JH, Zwarts MJ, van Weerden TW (1993) Muscle fiber conduction velocity in amyotrophic lateral sclerosis and traumatic lesions of the plexus brachialis. Electroencephalogr Clin Neurophysiol 89:304–310PubMedCrossRef
32.
go back to reference Blijham PJ, ter Laak HJ, Schelhaas HJ, van Engelen BG, Stegeman DF, Zwarts MJ (2006) Relation between muscle fiber conduction velocity and fiber size in neuromuscular disorders. J Appl Physiol 100:1837–1841PubMedCrossRef Blijham PJ, ter Laak HJ, Schelhaas HJ, van Engelen BG, Stegeman DF, Zwarts MJ (2006) Relation between muscle fiber conduction velocity and fiber size in neuromuscular disorders. J Appl Physiol 100:1837–1841PubMedCrossRef
33.
go back to reference The Diabetes Control and Complications Trial Research Group (1995) The effect of intensive diabetes therapy on the development and progression of neuropathy. Ann Intern Med 122:561–568 The Diabetes Control and Complications Trial Research Group (1995) The effect of intensive diabetes therapy on the development and progression of neuropathy. Ann Intern Med 122:561–568
34.
go back to reference Martin CL, Albers J, Herman WH et al (2006) Neuropathy among the diabetes control and complications trial cohort 8 years after trial completion. Diabetes Care 29:340–344PubMedCrossRef Martin CL, Albers J, Herman WH et al (2006) Neuropathy among the diabetes control and complications trial cohort 8 years after trial completion. Diabetes Care 29:340–344PubMedCrossRef
35.
go back to reference Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA (2002) Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 76:473–481PubMed Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA (2002) Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 76:473–481PubMed
37.
go back to reference Saltin B, Gollnick PD (1983) Skeletal muscle adaptability: significance for metabolism and performance. In: Peachey LD, Adrian PH, Geiger SR (eds) Handbook of physiology—skeletal muscle. American Physiological Society, Washington, DC, pp 555–631 Saltin B, Gollnick PD (1983) Skeletal muscle adaptability: significance for metabolism and performance. In: Peachey LD, Adrian PH, Geiger SR (eds) Handbook of physiology—skeletal muscle. American Physiological Society, Washington, DC, pp 555–631
38.
go back to reference Faulkner JA, Larkin LM, Claflin DR, Brooks SV (2007) Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol 34:1091–1096PubMed Faulkner JA, Larkin LM, Claflin DR, Brooks SV (2007) Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol 34:1091–1096PubMed
39.
go back to reference Berg HE, Eiken O, Miklavcic L, Mekjavic IB (2007) Hip, thigh and calf muscle atrophy and bone loss after 5-week bedrest inactivity. Eur J Appl Physiol 99:283–289PubMedCrossRef Berg HE, Eiken O, Miklavcic L, Mekjavic IB (2007) Hip, thigh and calf muscle atrophy and bone loss after 5-week bedrest inactivity. Eur J Appl Physiol 99:283–289PubMedCrossRef
40.
go back to reference Park SW, Goodpaster BH, Strotmeyer ES et al (2006) Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes 55:1813–1818PubMedCrossRef Park SW, Goodpaster BH, Strotmeyer ES et al (2006) Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes 55:1813–1818PubMedCrossRef
41.
go back to reference Delmonico MJ, Kostek MC, Johns J, Hurley BF, Conway JM (2007) Can dual energy X-ray absorptiometry provide a valid assessment of changes in thigh muscle mass with strength training in older adults? Eur J Clin Nutr 62:1372–1378PubMedCrossRef Delmonico MJ, Kostek MC, Johns J, Hurley BF, Conway JM (2007) Can dual energy X-ray absorptiometry provide a valid assessment of changes in thigh muscle mass with strength training in older adults? Eur J Clin Nutr 62:1372–1378PubMedCrossRef
42.
go back to reference Dube MC, Joanisse DR, Prud’homme D et al (2006) Muscle adiposity and body fat distribution in type 1 and type 2 diabetes: varying relationships according to diabetes type. Int J Obes (Lond) 30:1721–1728CrossRef Dube MC, Joanisse DR, Prud’homme D et al (2006) Muscle adiposity and body fat distribution in type 1 and type 2 diabetes: varying relationships according to diabetes type. Int J Obes (Lond) 30:1721–1728CrossRef
43.
go back to reference Mueller MJ, Minor SD, Sahrmann SA, Schaaf JA, Strube MJ (1994) Differences in the gait characteristics of patients with diabetes and peripheral neuropathy compared with age-matched controls. Phys Ther 74:299–308PubMed Mueller MJ, Minor SD, Sahrmann SA, Schaaf JA, Strube MJ (1994) Differences in the gait characteristics of patients with diabetes and peripheral neuropathy compared with age-matched controls. Phys Ther 74:299–308PubMed
44.
go back to reference Kwon OY, Minor SD, Maluf KS, Mueller MJ (2003) Comparison of muscle activity during walking in subjects with and without diabetic neuropathy. Gait Posture 18:105–113PubMedCrossRef Kwon OY, Minor SD, Maluf KS, Mueller MJ (2003) Comparison of muscle activity during walking in subjects with and without diabetic neuropathy. Gait Posture 18:105–113PubMedCrossRef
45.
go back to reference van Schie CH (2005) A review of the biomechanics of the diabetic foot. Int J Low Extrem Wounds 4:160–170PubMedCrossRef van Schie CH (2005) A review of the biomechanics of the diabetic foot. Int J Low Extrem Wounds 4:160–170PubMedCrossRef
Metadata
Title
Accelerated atrophy of lower leg and foot muscles—a follow-up study of long-term diabetic polyneuropathy using magnetic resonance imaging (MRI)
Authors
C. S. Andreassen
J. Jakobsen
S. Ringgaard
N. Ejskjaer
H. Andersen
Publication date
01-06-2009
Publisher
Springer-Verlag
Published in
Diabetologia / Issue 6/2009
Print ISSN: 0012-186X
Electronic ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-009-1320-0

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