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Association of sudomotor function with peripheral artery disease in type 2 diabetes

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Abstract

Peripheral artery disease (PAD) is the major risk factor for cardiovascular disease and lower extremity amputation in patients with diabetes. Autonomic neuropathy is a risk factor for cardiovascular-related morbidity and mortality. Sudomotor dysfunction is well established in type 2 diabetes mellitus (T2DM) and reflects small fibre neuropathy, cardiovascular autonomic neuropathy and peripheral sympathetic autonomic neuropathy. However, the relationship between sudomotor dysfunction and PAD remains unexplored. Therefore, the aim of present study was to explore the association of sudomotor function with ankle-brachial index (ABI) and C-reactive protein (CRP) in T2DM. In this cross-sectional study, we recruited 36 consecutive type 2 diabetes patients and 20 age- and sex-matched healthy controls. Sudomotor function was assessed using Sudoscan (Sudoscan-Impeto Medical Device, EZS 01750010193, Paris, France), which detects sweat gland function through measurement of electrochemical skin conductance of both hands and feet. Measurement of ankle-brachial ABI was carried out with sphygmomanometer and Doppler device (Hadeco Bidop ES-100V3). Glycated haemoglobin (HbA1c), fasting plasma glucose, and inflammatory marker CRP were also measured. Type 2 diabetic patients had significantly impaired sudomotor function (48.14 ± 8.28 vs. 76.48 ± 6.72 µs), lower ABI (0.89 ± 0.25 vs. 1.15 ± 0.11) and elevated CRP (5.32 ± 2.41 vs. 2.45 ± 1.11 mg/l) as compared to healthy controls, respectively (p < 0.01). Sudoscan scores were found to be inversely correlated with CRP and HbA1c, and directly correlated with ABI (p < 0.05) in the patients. Sudomotor dysfunction is associated with significant peripheral artery disease, vascular inflammation and impaired glycaemic status.

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References

  1. American Diabetes Association (2009) Diagnosis and classification of diabetes mellitus. Diabetes Care 32(1):S62–S67

    Article  PubMed Central  Google Scholar 

  2. Vinik AI, Mehrabyan A (2004) Diabetic neuropathies. Med Clin N Am 88:947–999

    Article  CAS  PubMed  Google Scholar 

  3. Zygmunt A, Stanczyk J (2010) Methods of evaluation of autonomic nervous system function. Arch Med Sci 6(1):11–18

    Article  PubMed  PubMed Central  Google Scholar 

  4. Luo KR, Chao CC, Chen YT et al (2011) Quantitation of sudomotor innervation in skin biopsies of patients with diabetic neuropathy. J Neuropathol Exp Neurol 70:930–938

    Article  PubMed  Google Scholar 

  5. Levy DM, Reid G, Rowley DA, Abraham RR (1992) Quantitative measures of sympathetic skin response in diabetes: relation to sudomotor and neurological function. J Neurol Neurosurg Psychiatry 55:902–908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Fealey RD, Low PA, Thomas JE (1989) Thermoregulatory sweating abnormalities in diabetes mellitus. Mayo Clin Proc 64:617–628

    Article  CAS  PubMed  Google Scholar 

  7. Chittaranjan S, Yajnik V, Kantikar V, Pande J, Deslypere P (2012) Quick and simple evaluation of sudomotor function for screening of diabetic neuropathy. ISRN Endocrinol 2012:103714

    Google Scholar 

  8. Boger MS, Hulgan T, Haas DW, Mitchell V, Smith AG, Singleton JR et al (2012) Measures of small-fiber neuropathy in HIV infection. Auton Neurosci 169:56–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Thaisetthawatkul P, Fernandes JA, Herrmann DN (2013) Contribution of QSART to the diagnosis of small fiber neuropathy. Muscle Nerve 48:883–888

    Article  PubMed  Google Scholar 

  10. Jenny E, Kanter Michelle M, Averill Renee C, LeBoeuf Karin E, Bornfeldt (2008) Diabetes-accelerated atherosclerosis and inflammation. Circ Res 103:e116–e117

    Article  Google Scholar 

  11. Aso Y, Okumura KI, Inoue T, Matsutomo R, Yoshida N, Wakabayashi S et al (2004) The results of the blood inflammatory markers are associated more strongly with the toe-brachial index than with the ankle-brachial index in patients with type 2 diabetes. Diabetes Care 27:1381–1386

    Article  PubMed  Google Scholar 

  12. Tzoulaki I, Murray GD, Lee AJ, Rumley A, Lowe GDO, Fowkes FGR (2005) The C-reactive protein, interleukin-6, and the soluble adhesion molecules as the predictors of the progressive peripheral atherosclerosis in the General Population Edinburgh Artery Study. Circulation 112:976–983

    Article  CAS  PubMed  Google Scholar 

  13. Francisco G, Hernandez C, Chacon P, Mesa J, Simo R (2005) The factors which influence the CRP levels in the diabetic population. Med Clin (Barc) 124(9):336–337

    Article  Google Scholar 

  14. Fowkes FG, Murray GD, Butcher I et al (2008) Ankle brachial index collaboration. Ankle brachial index combined with Framingham Risk Score to predict cardiovascular events and mortality: a meta-analysis. JAMA 300:197–208

    Article  CAS  PubMed  Google Scholar 

  15. Thejaswini KO, Roopakala Dayananda G, Chandrakala Kumar P (2012) A study of association of ankle brachial index (ABI) and the highly sensitive C-reactive protein (hsCRP) in type 2 diabetic patients and in normal subjects. J Clin Diagn 7(1):46–50

    Google Scholar 

  16. De Champlain J, Karas M, Toal C, Nadeau R, Larochelle P (1999) Effects of antihypertensive therapies on the sympathetic nervous system. Can J Cardiol 15 Suppl A:8A–14A

  17. Ikeda Y, Nomura S, Sawa Y, Nakazawa T (1982) The effects of antidepressants on the autonomic nervous system–a current investigation. J Neural Transm 54(1–2):65–73

    Article  CAS  PubMed  Google Scholar 

  18. Mayaudon H, Miloche PO, Bauduceau B (2010) A new simple method for assessing sudomotor function: relevance in type 2 diabetes. Diabetes Metab 36:450–454

    Article  CAS  PubMed  Google Scholar 

  19. Hubert D, Brunswick P, Calvet JH, Dusser D, Fajac (2011) Abnormal electrochemical skin conductance in cystic fibrosis. J Cyst Fibros 10:15–20

    Article  PubMed  Google Scholar 

  20. Clark N, Beauregard N, Alexandria (2003) Peripheral arterial disease in people with diabetes. Diabetes Care 26(12):3333–3341

    Article  Google Scholar 

  21. Potier L, Abi Khalil C, Mohammed K, Roussel R (2011) Use and utility of ankle brachial index in patients with diabetes. Eur J Vasc Endovasc Surg 41:110e116

    Article  Google Scholar 

  22. Marchello L, Donadio V, Montagna P (1996) The sympathetic skin response: a neurological perspective. Funct Neurol 11(6):283–299

    CAS  PubMed  Google Scholar 

  23. Young LH, Wackers FJ, Chyun DA, Davey JA, Barrett EJ, Taillefer R et al (2009) Cardiac outcomes after screening for asymptomatic coronary artery disease in patients with type 2 diabetes: the DIAD study: a randomized controlled trial. JAMA 301:1547–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Pop-Busui R, Evans G, Gerstein H, Fonseca V, Fleg J, Hoogwerf B et al (2010) Effects of cardiac autonomic dysfunction on mortality risk in the action to control cardiovascular risk in diabetes (ACCORD) trial. Diabetes Care 33:1578–1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Pop-Busui R (2010) Cardiac autonomic neuropathy in diabetes: a clinical perspective. Diabetes Care 33:434–441

    Article  PubMed  PubMed Central  Google Scholar 

  26. Wulsin L, Horn P, Perry J, Massaro J, D’Agostino R (2015) Autonomic imbalance as a predictor of metabolic risks, cardiovascular disease, diabetes, and mortality autonomic imbalance predicts CVD, DM, mortality. J Clin Endocrinol Metab 100(6):2443–2448

    Article  CAS  PubMed  Google Scholar 

  27. Maser R, Mitchell B, Vinik AI, Freeman R (2003) The association between cardiovascular autonomic neuropathy and mortality in individuals with diabetes: a meta-analysis. Diabetes Care 26:1895–1901

    Article  PubMed  Google Scholar 

  28. Casellini C, Parson HK, Richardson M, Nevoret L, Vinik AI (2013) Sudoscan, a noninvasive tool for detecting diabetic small fiber neuropathy and autonomic dysfunction. Diabetes Technol Ther 15:948–953

    Article  PubMed  PubMed Central  Google Scholar 

  29. Syngle A, Verma I, Krishan P, Garg N, Syngle V (2014) Minocycline improves peripheral and autonomic neuropathy in type-2 diabetes: MIND study. Neurol Sci 35(7):1067–1073

    Article  PubMed  Google Scholar 

  30. Luk AO, Fu WC, Li X, Ozaki R, Chung H, Wong R et al (2015) The clinical utility of SUDOSCAN in chronic kidney disease in chinese patients with type 2 diabetes. PLoS One 10(8):e0134981

    Article  PubMed  PubMed Central  Google Scholar 

  31. Yang Z, Xu B, Jieli L, Tian X, Li M, Sun K et al (2013) Autonomic test by EZSCAN in the screening for prediabetes and diabetes. PLoS One 8(2):e56480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sheikh A, Sheikh N, Badawi M, Mahran Abdelfattah M (2015) Insulin resistance, a co-factor to dysglycemia, predicting peripheral neuropathy in type 2 diabetic patients in an Egyptian population: a non-randomized retrospective study. Life Sci J 12(4s):15–22

    Google Scholar 

  33. Vinik AI, Nevoret ML, Casellini C (2015) The new age of sudomotor function testing: a sensitive and specific biomarker for diagnosis, estimation of severity, monitoring progression, and regression in response to intervention. Front Endocrinol 11(6):94

    Google Scholar 

  34. Casellini C, Parson H, Richardson M, Nevoret M, Vinik AI (2013) Sudoscan, a noninvasive tool for detecting diabetic small fiber neuropathy and autonomic dysfunction. Diabetes Technol Ther 15(11):948–953

    Article  PubMed  PubMed Central  Google Scholar 

  35. Hasimu B, Li J, Nakayama T, Yu J, Yang J, Li X et al (2006) Ankle brachial index as a marker of atherosclerosis in Chinese patients with high cardiovascular risk. Hypertens Res 29(1):23–28

    Article  PubMed  Google Scholar 

  36. Marius R, Luminita I, Suzana G, Crina S (2014) The role of ankle-brachial index for predicting peripheral arterial disease. Maedica (Buchar) 9(3):295–302

    Google Scholar 

  37. Leng GC, Fowkes F, Lee AJ, Dunbar J, Housley J, Ruckley CV (1996) Use of ankle brachial pressure index to predict cardiovascular events and death: a cohort study. BMJ 313:1440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Maeda Y, Inoguchi T, Tsubouchi H, Sawada F, Sasaki S, Fujii M et al (2008) High prevalence of peripheral arterial disease diagnosed by low ankle-brachial index in Japanese patients with diabetes: the Kyushu Prevention Study for Atherosclerosis. Diabetes Res Clin Pract 82(3):378–382

    Article  PubMed  Google Scholar 

  39. Argyriou AA, Tsolakis I, Papadoulas S, Polychronopoulos P, Gourzis P, Chroni E (2006) Sympathetic skin response in patients with peripheral arterial occlusive disease. Clin Neurophysiol 117(2):414–419

    Article  PubMed  Google Scholar 

  40. Ridker PM, Hennekens CH, Buring JE, Rifai N (2000) The C-reactive protein and other markers of inflammation in the prediction of cardiovascular diseases in women. N Eng J Med 342(836):43

    Google Scholar 

  41. Syngle A, Verma I, Garg N, Krishan P (2013) Autonomic dysfunction in psoriatic arthritis. Clin Rheumatol 32(7):1059–1064

    Article  PubMed  Google Scholar 

  42. Syngle A, Verma I, Garg N, Krishan P (2012) Autonomic neuropathy in rheumatoid arthritis and ankylosing spondylitis: peripheral sympathetic and cardiovascular autonomic function assessment. Int J Rheum Dis 15(1):85–88

    Article  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge academic contribution of Nidhi Garg, PhD Research scholar, Department of Pharmaceutical Sciences and Drug Research, Punjabi University, Patiala, Punjab, India in preparing the manuscript.

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Correspondence to Kanchan Vohra.

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Chahal, S., Vohra, K. & Syngle, A. Association of sudomotor function with peripheral artery disease in type 2 diabetes. Neurol Sci 38, 151–156 (2017). https://doi.org/10.1007/s10072-016-2742-3

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  • DOI: https://doi.org/10.1007/s10072-016-2742-3

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