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Assessment of vascular autonomic function using peripheral arterial tonometry

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Abstract

Peripheral autonomic function is impaired in diabetic polyneuropathy. However, it is difficult to evaluate it due to the lack of non-invasive quantitative assessment. We aimed to establish a novel index to evaluate vascular autonomic function using reactive hyperemia peripheral arterial tonometry (RH-PAT), a widely performed endothelial function test. Sixty-five subjects were enrolled, including healthy subjects, cases with sympathetic nerve blockers, and diabetic patients. RH-PAT was performed with 5-min blood flow occlusion in unilateral arm. We calculated the reduction ratio of the post-occlusion pulse amplitude to the baseline in the non-occluded arm (RPN), with 1-min sliding window. In healthy subjects, RPN gradually increased with time-dependent manner. However, this phenomenon was eliminated in cases with sympathetic nerve blockers. Plasma concentration of norepinephrine was measured before and after the blood flow occlusion, which showed a significant increase. We then compared RPNs with the change in heart rate variability (HRV) parameters. RPN calculated at 5 min after the reperfusion had the highest correlation with the change in sympathetic HRV parameter, and thus, we named sympathetic hypoemia index (SHI). Finally, we studied the relationship between SHI and diabetes. SHI was significantly lower in diabetic patients than matched controls. SHI, a novel index derived from RH-PAT, represented the peripheral sympathetic activity. SHI may be useful for assessing the vascular autonomic activity in diabetic patients.

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References

  1. Bruno RM, Ghiadoni L, Seravalle G, Dell’oro R, Taddei S, Grassi G (2012) Sympathetic regulation of vascular function in health and disease. Front Physiol 3:284

    Article  PubMed  PubMed Central  Google Scholar 

  2. Boulton AJ, Vinik AI, Arezzo JC, Bril V, Feldman EL, Freeman R, Malik RA, Maser RE, Sosenko JM, Ziegler D (2005) Diabetic neuropathies: a statement by the American Diabetes Association. Diabetes Care 28:956–962

    Article  PubMed  Google Scholar 

  3. Balcioglu AS, Muderrisoglu H (2015) Diabetes and cardiac autonomic neuropathy: clinical manifestations, cardiovascular consequences, diagnosis and treatment. World J Diabetes 6:80–91

    Article  PubMed  PubMed Central  Google Scholar 

  4. Matsuda M, Gono T, Morita H, Katoh N, Kodaira M, Ikeda S (2011) Peripheral nerve involvement in primary systemic AL amyloidosis: a clinical and electrophysiological study. Eur J Neurol 18:604–610

    Article  CAS  PubMed  Google Scholar 

  5. Chandler MP, Mathias CJ (2002) Haemodynamic responses during head-up tilt and tilt reversal in two groups with chronic autonomic failure: pure autonomic failure and multiple system atrophy. J Neurol 249:542–548

    Article  PubMed  Google Scholar 

  6. Kim JB, Kim BJ, Koh SB, Park KW (2014) Autonomic dysfunction according to disease progression in Parkinson’s disease. Parkinsonism Relat Disord 20:303–307

    Article  PubMed  Google Scholar 

  7. Grassi G, Esler M (1999) How to assess sympathetic activity in humans. J Hypertens 17:719–734

    Article  CAS  PubMed  Google Scholar 

  8. White DW, Shoemaker JK, Raven PB (2015) Methods and considerations for the analysis and standardization of assessing muscle sympathetic nerve activity in humans. Auton Neurosci 193:12–21

    Article  PubMed  PubMed Central  Google Scholar 

  9. Vallbo AB, Hagbarth KE, Wallin BG (2004) Microneurography: how the technique developed and its role in the investigation of the sympathetic nervous system. J Appl Physiol 96:1262–1269

    Article  PubMed  Google Scholar 

  10. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93:1043–1065

    Article  Google Scholar 

  11. Pomeranz B, Macaulay RJ, Caudill MA, Kutz I, Adam D, Gordon D, Kilborn KM, Barger AC, Shannon DC, Cohen RJ et al (1985) Assessment of autonomic function in humans by heart rate spectral analysis. Am J Physiol 248:H151–153

    CAS  PubMed  Google Scholar 

  12. Huikuri HV, Makikallio TH, Peng CK, Goldberger AL, Hintze U, Moller M (2000) Fractal correlation properties of R–R interval dynamics and mortality in patients with depressed left ventricular function after an acute myocardial infarction. Circulation 101:47–53

    Article  CAS  PubMed  Google Scholar 

  13. Cacciatori V, Dellera A, Bellavere F, Bongiovanni LG, Teatini F, Gemma ML, Muggeo M (1997) Comparative assessment of peripheral sympathetic function by postural vasoconstriction arteriolar reflex and sympathetic skin response in NIDDM patients. Am J Med 102:365–370

    Article  CAS  PubMed  Google Scholar 

  14. Shahani BT, Halperin JJ, Boulu P, Cohen J (1984) Sympathetic skin response—a method of assessing unmyelinated axon dysfunction in peripheral neuropathies. J Neurol Neurosurg Psychiatry 47:536–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bonetti PO, Pumper GM, Higano ST, Holmes DR Jr, Kuvin JT, Lerman A (2004) Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol 44:2137–2141

    Article  PubMed  Google Scholar 

  16. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R (2002) Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 39:257–265

    Article  PubMed  Google Scholar 

  17. Shimokawa H (1999) Primary endothelial dysfunction: atherosclerosis. J Mol Cell Cardiol 31:23–37

    Article  CAS  PubMed  Google Scholar 

  18. Miura H, Wachtel RE, Liu Y, Loberiza FR Jr, Saito T, Miura M, Gutterman DD (2001) Flow-induced dilation of human coronary arterioles: important role of Ca(2 +)-activated K(+) channels. Circulation 103:1992–1998

    Article  CAS  PubMed  Google Scholar 

  19. Tabata N, Hokimoto S, Akasaka T, Arima Y, Sakamoto K, Yamamoto E, Tsujita K, Izumiya Y, Yamamuro M, Kojima S, Kaikita K, Ogawa H (2015) Differential impact of peripheral endothelial dysfunction on subsequent cardiovascular events following percutaneous coronary intervention between chronic kidney disease (CKD) and non-CKD patients. Heart Vessels. doi:10.1007/s00380-015-0713-x

    Google Scholar 

  20. Takata M, Amiya E, Watanabe M, Ozeki A, Watanabe A, Kawarasaki S, Nakao T, Hosoya Y, Uno K, Saito A, Murasawa T, Ono M, Nagai R, Komuro I (2015) Brachial artery diameter has a predictive value in the improvement of flow-mediated dilation after aortic valve replacement for aortic stenosis. Heart Vessels 30:218–226

    Article  PubMed  Google Scholar 

  21. Kuvin JT, Patel AR, Sliney KA, Pandian NG, Sheffy J, Schnall RP, Karas RH, Udelson JE (2003) Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J 146:168–174

    Article  PubMed  Google Scholar 

  22. Tarvainen MP, Niskanen JP, Lipponen JA, Ranta-Aho PO, Karjalainen PA (2014) Kubios HRV—heart rate variability analysis software. Comput Methods Programs Biomed 113:210–220

    Article  PubMed  Google Scholar 

  23. Berthiaume F, Frangos JA (1992) Flow-induced prostacyclin production is mediated by a pertussis toxin-sensitive G protein. FEBS Lett 308:277–279

    Article  CAS  PubMed  Google Scholar 

  24. Nohria A, Gerhard-Herman M, Creager MA, Hurley S, Mitra D, Ganz P (2006) Role of nitric oxide in the regulation of digital pulse volume amplitude in humans. J Appl Physiol 101:545–548

    Article  CAS  PubMed  Google Scholar 

  25. Levine AB, Punihaole D, Levine TB (2012) Characterization of the role of nitric oxide and its clinical applications. Cardiology 122:55–68

    Article  CAS  PubMed  Google Scholar 

  26. Rassaf T, Kleinbongard P, Preik M, Dejam A, Gharini P, Lauer T, Erckenbrecht J, Duschin A, Schulz R, Heusch G, Feelisch M, Kelm M (2002) Plasma nitrosothiols contribute to the systemic vasodilator effects of intravenously applied NO: experimental and clinical Study on the fate of NO in human blood. Circ Res 91:470–477

    Article  CAS  PubMed  Google Scholar 

  27. Grote L, Zou D, Kraiczi H, Hedner J (2003) Finger plethysmography—a method for monitoring finger blood flow during sleep disordered breathing. Respir Physiol Neurobiol 136:141–152

    Article  PubMed  Google Scholar 

  28. Wu JS, Yang YC, Lin TS, Huang YH, Chen JJ, Lu FH, Wu CH, Chang CJ (2007) Epidemiological evidence of altered cardiac autonomic function in subjects with impaired glucose tolerance but not isolated impaired fasting glucose. J Clin Endocrinol Metab 92:3885–3889

    Article  CAS  PubMed  Google Scholar 

  29. Wawryk AM, Bates DJ, Couper JJ (1997) Power spectral analysis of heart rate variability in children and adolescents with IDDM. Diabetes Care 20:1416–1421

    Article  CAS  PubMed  Google Scholar 

  30. Singh JP, Larson MG, O’Donnell CJ, Wilson PF, Tsuji H, Lloyd-Jones DM, Levy D (2000) Association of hyperglycemia with reduced heart rate variability (The Framingham Heart Study). Am J Cardiol 86:309–312

    Article  CAS  PubMed  Google Scholar 

  31. Wheeler SG, Ahroni JH, Boyko EJ (2002) Prospective study of autonomic neuropathy as a predictor of mortality in patients with diabetes. Diabetes Res Clin Pract 58:131–138

    Article  PubMed  Google Scholar 

  32. May O, Arildsen H (2011) Long-term predictive power of heart rate variability on all-cause mortality in the diabetic population. Acta Diabetol 48:55–59

    Article  PubMed  Google Scholar 

  33. Nunan D, Sandercock GR, Brodie DA (2010) A quantitative systematic review of normal values for short-term heart rate variability in healthy adults. Pacing Clin Electrophysiol 33:1407–1417

    Article  PubMed  Google Scholar 

  34. Kannel WB, Wolf PA, Benjamin EJ, Levy D (1998) Prevalence, incidence, prognosis, and predisposing conditions for atrial fibrillation: population-based estimates 1. Am J Cardiol 82:2N–9N

    Article  CAS  PubMed  Google Scholar 

  35. Martelli D, Silvani A, May CN, Ramchandra R (2014) The low frequency power of heart rate variability is neither a measure of cardiac sympathetic tone nor of baroreflex sensitivity. Am J Physiol Heart Circ Physiol 307:H1005–H1012

    Article  CAS  PubMed  Google Scholar 

  36. Taverner D, Nunan TA, Tonkin AL (1996) Reproducibility of conventional and power spectral measurements of cardiovascular sympathetic activation in normal subjects. Clin Exp Pharmacol Physiol 23:804–806

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We really appreciate Mr. John Martin for his linguistic assistance.

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Correspondence to Tetsuo Sasano.

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All authors have no conflict of interest regarding this study.

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Hamada, S., Oono, A., Ishihara, Y. et al. Assessment of vascular autonomic function using peripheral arterial tonometry. Heart Vessels 32, 260–268 (2017). https://doi.org/10.1007/s00380-016-0870-6

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