• 1

    Shaw JE, Sicree RA, Zimmet PZ: Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87: 4, 2010.

  • 2

    Gu K, Cowie CC, Harris MI: Mortality in adults with and without diabetes in a national cohort of the U.S. population, 1971-1993. Diabetes Care 21: 1138, 1998.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3

    Gregg EW, Mangione CM, Cauley JA, et al: Diabetes and incidence of functional disability in older women. Diabetes Care 25: 61, 2002.

  • 4

    Volpato S, Maraldi C, Fellin R: Type 2 diabetes and risk for functional decline and disability in older persons. Curr Diabetes Rev 6: 134, 2010.

  • 5

    Al-Homood I: Rheumatic conditions in patients with diabetes mellitus. Clin Rheumatol 32: 527, 2013.

  • 6

    Ursini F, Russo E, D'Angelo S, et al: Prevalence of undiagnosed diabetes in rheumatoid arthritis: an OGTT study. Medicine (Baltimore) 95: e2552, 2016.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Hernandez-Diaz C, Saavedra MA, Navarro-Zarza JE, et al: Clinical anatomy of the ankle and foot. Reumatol Clin 8(suppl 2): 46, 2012.

  • 8

    Cheung JT, Zhang M, An KN: Effect of Achilles tendon loading on plantar fascia tension in the standing foot. Clin Biomech 21: 194, 2006.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Abate M, Schiavone C, Salini V, et al: Occurrence of tendon pathologies in metabolic disorders. Rheumatology 52: 599, 2013.

  • 10

    Cheing GL, Chau RM, Kwan RL, et al: Do the biomechanical properties of the ankle-foot complex influence postural control for people with Type 2 diabetes? Clin Biomech 28: 88, 2013.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    D'Ambrogi E, Giurato L, D'Agostino MA, et al: Contribution of plantar fascia to the increased forefoot pressures in diabetic patients. Diabetes Care 26: 1525, 2003.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Frykberg RG, Lavery LA, Pham H, et al: Role of neuropathy and high foot pressures in diabetic foot ulceration. Diabetes Care 21: 1714, 1998.

  • 13

    Colen LB, Kim CJ, Grant WP, et al: Achilles tendon lengthening: friend or foe in the diabetic foot? Plast Reconstr Surg 131: 37e, 2013.

  • 14

    Zakaria MH, Davis WA, Davis TM: Incidence and predictors of hospitalization for tendon rupture in type 2 diabetes: the Fremantle diabetes study. Diabet Med 31: 425, 2014.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    David MA, Jones KH, Inzana JA, et al: Tendon repair is compromised in a high fat diet-induced mouse model of obesity and type 2 diabetes. PLoS One 9: e91234, 2014.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Batista F, Nery C, Pinzur M, et al: Achilles tendinopathy in diabetes mellitus. Foot Ankle Int 29: 498, 2008.

  • 17

    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 117: 645, 2009.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Benjamin M, McGonagle D: The enthesis organ concept and its relevance to the spondyloarthropathies. Adv Exp Med Biol 649: 57, 2009.

  • 19

    Moghtaderi A, Bakhshipour A, Rashidi H: Validation of Michigan neuropathy screening instrument for diabetic peripheral neuropathy. Clin Neurol Neurosurg 108: 477, 2006.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Feldman EL, Stevens MJ, Thomas PK, et al: A practical two-step quantitative clinical and electrophysiological assessment for the diagnosis and staging of diabetic neuropathy. Diabetes Care 17: 1281, 1994.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Bland JM, Altman DG: Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1: 307, 1986.

  • 22

    Bassiouni M: Incidence of calcaneal spurs in osteo-arthrosis and rheumatoid arthritis, and in control patients. Ann Rheum Dis 24: 490, 1965.

  • 23

    Shama SS, Kominsky SJ, Lemont H: Prevalence of non-painful heel spur and its relation to postural foot position. JAPA 73: 122, 1983.

  • 24

    Moroney PJ, O'Neill BJ, Khan-Bhambro K, et al: The conundrum of calcaneal spurs: do they matter? Foot Ankle Spec 7: 95, 2014.

  • 25

    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 20: 532, 2005.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Chatterton BD, Muller S, Roddy E: Epidemiology of posterior heel pain in the general population: cross-sectional findings from the clinical assessment study of the foot. Arthritis Care Res (Hoboken) 67: 996, 2015.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Daragon A, Mejjad O, Czernichow P, et al: Vertebral hyperostosis and diabetes mellitus: a case-control study. Ann Rheum Dis 54: 375, 1995.

  • 28

    Kang JH, Tseng SH, Jaw FS, et al: Comparison of ultrasonographic findings of the rotator cuff between diabetic and nondiabetic patients with chronic shoulder pain: a retrospective study. Ultrasound Med Biol 36: 1792, 2010.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Lin TT, Lin CH, Chang CL, et al: The effect of diabetes, hyperlipidemia, and statins on the development of rotator cuff disease: a nationwide, 11-year, longitudinal, population-based follow-up study. Am J Sports Med 43: 2126, 2015.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Akturk M, Ozdemir A, Maral I, et al: Evaluation of Achilles tendon thickening in type 2 diabetes mellitus. Exp Clin Endocrinol Diabetes 115: 92, 2007.

  • 31

    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 31: 1109, 2012.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Abate M, Salini V, Antinolfi P, et al: Ultrasound morphology of the Achilles in asymptomatic patients with and without diabetes. Foot Ankle Int 35: 44, 2014.

  • 33

    Abate M, Di Carlo L, Salini V, et al: Metabolic syndrome associated to non-inflammatory Achilles enthesopathy. Clin Rheumatol 33: 1517, 2014.

  • 34

    Benjamin M, Rufai A, Ralphs JR: The mechanism of formation of bony spurs (enthesophytes) in the achilles tendon. Arthritis Rheum 43: 576, 2000.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Rogers J, Shepstone L, Dieppe P: Bone formers: osteophyte and enthesophyte formation are positively associated. Ann Rheum Dis 56: 85, 1997.

  • 36

    de Oliveira RR, Martins CS, Rocha YR, et al: Experimental diabetes induces structural, inflammatory and vascular changes of Achilles tendons. PLoS One 8: e74942, 2013.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Boivin GP, Elenes EY, Schultze AK, et al: Biomechanical properties and histology of db/db diabetic mouse Achilles tendon. Muscles Ligaments Tendons J 4: 280, 2014.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Connizzo BK, Bhatt PR, Liechty KW, et al: Diabetes alters mechanical properties and collagen fiber re-alignment in multiple mouse tendons. Ann Biomed Eng 42: 1880, 2014.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    de Oliveira RR, de Lira KD, Silveira PV, et al: Mechanical properties of achilles tendon in rats induced to experimental diabetes. Ann Biomed Eng 39: 1528, 2011.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Ji J, Wang Z, Shi D, et al: Pathologic changes of Achilles tendon in leptin-deficient mice. Rheumatol Int 30: 489, 2010.

  • 41

    Reddy GK: Cross-linking in collagen by nonenzymatic glycation increases the matrix stiffness in rabbit achilles tendon. Exp Diabesity Res 5: 143, 2004.

  • 42

    Tsai WC, Liang FC, Cheng JW, et al: High glucose concentration up-regulates the expression of matrix metalloproteinase-9 and -13 in tendon cells. BMC Musculoskelet Disord 14: 255, 2013.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Burner T, Gohr C, Mitton-Fitzgerald E, et al: Hyperglycemia reduces proteoglycan levels in tendons. Connect Tissue Res 53: 535, 2012.

  • 44

    Morel M, Boutry N, Demondion X, et al: Normal anatomy of the heel entheses: anatomical and ultrasonographic study of their blood supply. Surg Radiol Anat 27: 176, 2005.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Holmes GB, Lin J: Etiologic factors associated with symptomatic achilles tendinopathy. Foot Ankle Int 27: 952, 2006.

High Prevalence of Achilles Tendon Enthesopathic Changes in Patients with Type 2 Diabetes Without Peripheral Neuropathy

Francesco Ursini Department of Health Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Franco Arturi Department of Medical and Surgical Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Salvatore D'Angelo Rheumatology Department of Lucania, San Carlo Hospital of Potenza and Madonna delle Grazie Hospital of Matera, Potenza, Italy.

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Lewa Amara Department of Health Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Kassandra Nicolosi Department of Health Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Emilio Russo Department of Health Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Saverio Naty Department of Health Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Caterina Bruno Department of Health Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Giovambattista De Sarro Department of Health Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Ignazio Olivieri Rheumatology Department of Lucania, San Carlo Hospital of Potenza and Madonna delle Grazie Hospital of Matera, Potenza, Italy.

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Rosa Daniela Grembiale Department of Health Sciences, University of Catanzaro “Magna Graecia,” Catanzaro, Italy.

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Background:

Metabolic disorders are known to alter the mechanical properties of tendons. We sought to evaluate the prevalence of asymptomatic Achilles tendon enthesopathic changes in patients with type 2 diabetes mellitus (T2DM) without peripheral neuropathy.

Methods:

We recruited 43 patients with T2DM and 40 controls. Neuropathy was excluded with the Michigan Neuropathy Scoring Instrument. Bilateral ultrasonography of the Achilles tendon enthesis was performed.

Results:

Patients with T2DM had a higher prevalence of hypoechogenicity (26.7% versus 2.5%; P = .0001), entheseal thickening (24.4% versus 8.7%; P = .007), and enthesophytes (74.4% versus 57.5%; P = .02). No differences were found in the number of patients with erosions (1.2% versus 0%; P > .99), cortical irregularities (11.6% versus 3.7%; P = .09), bursitis (5.8% versus 3.7%; P = .72), or tears (2.3% versus 1.2%; P > .99). The mean ± SD sum of abnormalities was higher in patients with T2DM (1.5 ± 1.1 versus 0.7 ± 0.6; P < .0001), as was the percentage of bilateral involvement (72.1% versus 45.0%; P = .01). Mean ± SD thickness did not differ between patients and controls (4.4 ± 1.1 mm versus 4.2 ± 0.8 mm; P = .07).

Conclusions:

According to our data, there is an elevated prevalence of asymptomatic Achilles tendon enthesopathic changes in patients with T2DM independent of peripheral neuropathy.

Corresponding author: Francesco Ursini, MD, Department of Health Sciences, University of Catanzaro “Magna Graecia,” viale Europa – 88100 Catanzaro, Italy. (E-mail: francesco.ursini@yahoo.it)