Irregularity in Plantar Fascia, Muscle Edema and Tendon Thickness in
                    Patients with High-Risk for Diabetic Foot

Busra Yurumez Korkmaz; Mujde Akturk; Murat Ucar; Alev Eroglu Altınova; Mehmet Ali Can; Emre Arslan; Nil Tokgoz; Fusun Toruner

doi:10.1055/a-1642-2056

Experimental and Clinical Endocrinology & Diabetes, Inhaltsverzeichnis

Exp Clin Endocrinol Diabetes 2022; 130(08): 525-531
DOI: 10.1055/a-1642-2056

Article

Irregularity in Plantar Fascia, Muscle Edema and Tendon Thickness in Patients with High-Risk for Diabetic Foot

Authors

Busra Yurumez Korkmaz

¹Department of Internal Medicine, Gazi University Faculty of Medicine, Ankara, Turkey
Mujde Akturk

²Department of Endocrinology and Metabolism, Gazi University Faculty of Medicine, Ankara, Turkey
Murat Ucar

³Department of Radiology, Gazi University Faculty of Medicine, Ankara, Turkey
Alev Eroglu Altınova

²Department of Endocrinology and Metabolism, Gazi University Faculty of Medicine, Ankara, Turkey
Mehmet Ali Can

³Department of Radiology, Gazi University Faculty of Medicine, Ankara, Turkey
Emre Arslan

²Department of Endocrinology and Metabolism, Gazi University Faculty of Medicine, Ankara, Turkey
Nil Tokgoz

³Department of Radiology, Gazi University Faculty of Medicine, Ankara, Turkey
Fusun Toruner

²Department of Endocrinology and Metabolism, Gazi University Faculty of Medicine, Ankara, Turkey

Abstract

Aim To investigate the alterations in the plantar fascia (PF), intrinsic muscles, and tendons in the feet of patients at high risk for developing diabetic foot.

Methods The healthy feet of 22 patients with type 2 diabetes, who had developed diabetic foot ulcers on a single foot without any pathology on the contralateral extremity, and those of 22 healthy volunteers were evaluated by magnetic resonance imaging. The volume of the Achilles tendon (AT), the surface area of the PF, the thickness of AT, flexor hallucis longus, flexor digitorum longus, tibialis posterior, and peroneus longus tendons, irregularity in the PF, and edema of intrinsic foot muscles were examined.

Results Nineteen patients (86%) had irregularity in the PF, whereas none of the healthy controls had any (p<0.001). Intrinsic muscle edema was more common in the group with diabetes (p=0.006). The volume of AT and the surface area of PF were decreased in patients with peripheral arterial disease (PAD) (p<0.05). Patients with diabetes mellitus but without PAD had a larger surface area of PF than that of controls (p<0.05). There were no differences in the volume of AT, the surface area of the PF, and other tendon thickness between the groups.

Conclusion Irregularity in the PF and muscle edema may indicate a high risk for the diabetic foot. The presence of PAD may lead to regression in the structure of AT and PF.

Key words

diabetes mellitus - tendon - Achilles - MRI - peripheral arterial disease

Volltext

Referenzen

References
1 Fu XL, Ding H, Miao WW. et al. Global recurrence rates in diabetic foot ulcers: a systematic review and meta-analysis. Diabetes Metab Res Rev 2019; 35: e3160
2 Kumar S, Ashe H, Parnell L. et al. The prevalence of foot ulceration and its correlates in type 2 diabetic patients: A population-based study. Diabet Med 1994; 11: 480-484
3 Lauterbach S, Kostev K, Kohlmann T. Prevalence of diabetic foot syndrome and its risk factors in the UK. J Wound Care 2010; 19: 333-337
4 Bus S, van Netten J, Lavery L. et al. IWGDF guidance on the prevention of foot ulcers in at-risk patients with diabetes. Diabetes Metab Res Rev 2016; 32: 16-24
5 May D, Disler D, Jones E. et al. Abnormal signal intensity in skeletal muscle at MR imaging: patterns, pearls and pitfalls. Radiographics 2000; 20: 295-315
6 İyidir ÖT, Rahatlı FK, Bozkuş Y. et al. Acoustic radiation force impulse elastography and ultrasonographic findings of Achilles tendon in patients with and without diabetic peripheral neuropathy: A cross-sectional study. Exp Clin Endocrinol Diabetes 2021; 129: 99-103
7 D’Ambrogi E, Giurato L, D’Agostino A. et al. Contribution of plantar fascia to the increased forefoot pressures in diabetic ptients. Diabetes Care 2003; 26: 1525-1529
8 Giacomozzi C, D’Ambrogi E, Uccioli L. et al. Does the thickening of Achilles tendon and plantar fascia contribute to the alteration of diabetic foot loading?. Clin Biomech 2005; 20: 532-539
9 Abate M, Schiavone C, Di Carlo L. et al. Achilles tendon and plantar fascia in recently diagnosed type II diabetes: role of body mass index. Clin Rheumatol 2012; 31: 1109-1113
10 Kumar C, Rajagopal K, Hande H. et al. Intrinsic foot muscle and plantar tissue changes in type 2 diabetes mellitus. J Diabetes 2015; 7: 850-857
11 Ursini F, Arturi F, Nicolosi K. et al. Plantar fascia enthesopathy is highly prevalent in diabetic patients without peripheral neuropathy and correlates with retinopathy and impaired kidney function. PLoS One 2017; 12: e0174529
12 Akturk M, Karaahmetoglu S, Kacar M. et al. Thickness of the supraspinatus and biceps tendons in diabetic patients. Diabetes Care 2002; 25: 408
13 de Oliveira R, Lemos A, de Castro Silveira P. et al. Alterations of tendons in patients with diabetes mellitus: a systematic review. Diabet Med 2011; 28: 886-895
14 Akturk M, Ozdemir A, Maral I. et al. Evaluation of achilles tendon thickening in type 2 diabetes mellitus. Exp Clin Endocrinol Diabetes 2007; 115: 92-96
15 de Oliveira RR, Bezerra MA, de Lira KD. et al. Aerobic physical training restores biomechanical properties of Achilles tendon in rats chemically induced to diabetes mellitus. J Diabetes Complications 2012; 26: 163-168
16 Papanas N, Courcoutsakis N, Papatheodorou K. et al. Achilles tendon volume in type 2 diabetic patients with or without peripheral neuropathy: MRI study. Exp Clin Endocrinol Diabetes 2009; 117: 645-648
17 Bolton N, Smith K, Pilgram T. et al. Computed tomography to visualize and quantify the plantar aponeurosis and flexor hallucis longus tendon in the diabetic foot. Clin Biomech 2005; 20: 540-546
18 de Oliveira RR, Martins CS, Rocha YR. et al. Experimental diabetes induces structural, inflammatory and vascular changes of achilles tendons. PLoS One 2013; 8: e74942
19 Morrison W, Ledermann H. Work-up of the diabetic foot. Radiol Clin North Am 2002; 40: 1171-1192
20 Craig M, Duffin A, Gallego P. et al. Plantar fascia thickness, a measure of tissue glycation, predicts the development of complications in adolescents with type 1 diabetes. Diabetes Care 2008; 31: 1201-1206
21 Örneholm H, Apelqvist J, Larsson J. et al. Recurrent and other new foot ulcers after healed plantar forefoot diabetic ulcer. Wound Repair Regen 2017; 25: 309-315
22 Mueller M. Identifying patients with diabetes mellitus who are at risk for lower-extremity complications: use of Semmes-Weinstein Monofilaments. Phys Ther 1996; 76: 68-71
23 Hirsch AT, Haskal ZJ, Hertzer NR. et al. ACC/AHA 2005 practice guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic). Circulation 2006; 113: 463-654
24 Hodgson RJ, O’Connor PJ, Grainger AJ. Tendon and ligament imaging. Br J Radiol 2012; 85: 1157-1172
25 Moraes do Carmo C, Fonseca de Almeida Melao L, Valle de Lemos Weber M. et al. Anatomical features of plantar aponeurosis: cadaveric study using ultrasonography and magnetic resonance imaging. Skeletal Radiol 2008; 37: 929-935
26 Pang B, Ying M. Sonographic measurement of achilles tendons in asymptomatic subjects: variation with age, body height and dominance of ankle. J Ultrasound Med 2006; 25: 1291-1296
27 Grant W, Sullivan R, Sonenshine D. et al. Electron microscopic investigation of the effects of diabetes mellitus on the achilles tendon. J Foot Ankle Surg 1997; 36: 272-278
28 Hicks J. The mechanics of the foot II. The plantar aponeurosis and the arch. J Anat 1954; 88: 25-30
29 Kane D, Greaney T, Shanahan M. et al. The role of ultrasonography in the diagnosis and management of idiopathic plantar fasciitis. Rheumatology 2001; 40: 1002-1008
30 Abul K, Ozer D, Sakizlioglu S. et al. Detection of normal plantar fascia thickness in adults via the ultrasonographic method. J Am Podiatr Med Assoc 2015; 105: 8-13
31 Draghi F, Gitto S, Bortolotto C. et al. Imaging of plantar fascia disorders: findings on plain radiography, ultrasound and magnetic resonance imaging. Insights Imaging 2017; 8: 69-78
32 Ursini F, Arturi F, Angelo SD. et al. High prevalence of achilles tendon enthesopathic changes in patients with type 2 diabetes without peripheral neuropathy. J Am Podiatr Med Assoc 2017; 107: 99-105
33 Cheing GLY, Chau RMW, Kwan RLC. et al. Do the biomechanical properties of the ankle-foot complex influence postural control for people with type 2 diabetes ?. Clin Biomech 2013; 28: 88-92
34 Evranos B, Idilman I, Ipek A. et al. Real-time sonoelastography and ultrasound evaluation of the achilles tendon in patients with diabetes with or without foot ulcers: a cross sectional study. J Diabetes Complications 2015; 29: 1124-1129
35 Guimarães JB, Nico MA, Omond AG. et al. Diagnostic imaging of inflammatory myopathies: new concepts and a radiological approach. Curr Rheumatol Rep 2019; 21: 1-3
36 Moore T, Yuh W, Kathol M. et al. Abnormalities of the foot in patients with diabetes mellitus: findings on MR imaging. Am J Roentgenol 1991; 157: 813-816
37 Baker J, Demertzis J, Rhodes N. et al. Diabetic musculoskeletal complications and their imaging mimics. Radiographics 2012; 32: 1959-1974
38 Chatha DS, Cunningham PM, Schweitzer ME. MR Imaging of the diabetic foot: Diagnostic challenges. Radiol Clin North Am 2005; 43: 747-759
39 El-Khoury G, Brandser E, Saltzman C. MRI of tendon injuries. Iowa Orthop J 1994; 14: 65-80
40 Docking S, Ooi C, Connell D. Tendinopathy: is imaging telling us the entire story?. J Orthop Sports Phys Ther 2015; 45: 842-852