Detection of skin microvascular vasodilation disorders in patients with diabetic foot syndrome during the local heating test

Introduction and purpose. The aim of investigation was to evaluate the possibility of using the method of wavelet analysis of skin temperature during the local heating test for the study of the microvascular tone regulation in patients with diabetic foot syndrome (DFS). Materials and methods. The study was performed in 15 healthy subjects and 10 patients with neuro-ischemic form of DFS complicated by trophic ulcers. The temperature of the plantar surface of the hallux was recorded by «Microtest» (Perm, Russia) with temperature resolution 0,002°C. Time-frequency analysis of temperature fluctuations was performed using wavelet analysis. For the reconstruction of the oscillations in endothelial (0.02-0.0095 Hz), neurogenic (0.05-0.02 Hz) and myogenic (0.05-0.14 Hz) frequency ranges we used inverse wavelet transform. Results. In healthy people, indexes of vasodilation (relative changes in the oscillation amplitudes) in the myogenic, neurogenic, and endothelial frequency ranges were 3.04, 4.01 and 2.25 respectively. In patients with DFS the values were significantly lower than in healthy subjects (0.60, 0.67 and 0.51, respectively). Conclusion. In contrast to healthy subjects, the combination of diabetic polyneuropathy with endothelial dysfunction and macroangiopathy in patients with neuro-ischemic form of DFS leads to the progression of mutually aggravating pathological processes and lower limb ischemia. Further implementation of the local heating test at the early stages of diabetic foot is of interest for the prognosis of the disease, evaluating the effectiveness of conservative treatment and endovascular interventions.

синдром диабетической стопы, кожная микроциркуляция, вейвлет-анализ, локальная тепловая проба, diabetic foot syndrome, cutaneous microcirculation, local heating test, wavelet analysis

1. Герасимчук П.А., Кисиль П.В., Влесенко В.Г., Павлышин А.В. Показатели эндотелиальной дисфункции у больных с синдромом диабетической стопы // Вестник РАМН. 2014. № 5-6. С. 107-110.

2. Игнатович И.Н., Кондратенко Г.Г., Леонович С.И. Особенности поражения артерий у пациентов с критической ишемией на фоне синдрома диабетической стопы // Ангиол. и сосудистая хирургия. 2012. Т. 18. № 2. С. 15-18.

3. Крупаткин А.И., Сидоров В.В. Функциональная диагностика состояния микроциркуляторно-тканевых систем: колебания, информация, нелинейность: рук-во для врачей / под ред. А. И. Крупаткина, В. В. Сидорова. М.: Либроком. 2014. 498 с.

4. Максимов А.В., Корейба К.А., Нуретдинов Р.М. и др. Мультидисциплинарный подход к лечению больных с критической ишемией конечностей // Ангиол. и сосудистая хирургия. 2013. Т. 19. № 4. С. 122-125.

5. Подтаев С.Ю., Попов А.В., Морозов М.К., Фрик П.Г. Исследование микроциркуляции крови с помощью вейвлет-анализа колебаний температуры кожи // Регионарное кровообращение и микроциркуляция. 2009. № 3. С. 14-20.

6. Сагайдачный А.А., Скрипаль А.В., Фомин А.В., Усанов Д.А. Восстановление спектра колебаний кровотока из спектра колебаний температуры пальцев рук, дисперсия температурного сигнала в биоткани // Регионарное кровообращение и микроциркуляция. 2013. Т. 12. № 1 (45). С. 76-82.

7. Смирнова Е.Н., Подтаев С.Ю., Мизева И.А., Жукова Е.А. Нарушение механизмов вазодилатации у больных сахарным диабетом 2 типа при проведении контралатеральной холодовой пробы // Регионарное кровообращение и микроциркуляция. 2012. № 1. С. 30-34.

8. Boodhwani M., Sodha N.R., Mieno S. et al. Functional, cellular, and molecular characterization of the angiogenic response to chronic myocardial ischemia in diabetes // Circulation. 2007. Vol. 116. P 131-137.

9. Cahn A., Elishuv O., Olshtain-Pops K. Establishing a multidisciplinary diabetic foot team in a large tertiary hospital: a workshop // Diabetes Metab Res Rev. 2014. Vol. 30 № 5. P. 350-353.

10. Collins R., Burch J., Cranny G. et al. Duplex ultrasonography, magnetic resonance angiography, and computed tomography angiography for diagnosis and assessment of symptomatic, lower limb peripheral arterial disease: systematic review // BMJ. 2007. Vol. 334. P. 1257-1266.

11. Harbi P., Thacher T. Body mapping of human cutaneous microcirculatory perfusion using a real-time laser Doppler imager // Diab. Vasc. Dis. Res. 2013. Vol. 10 № 2. Р. 187-190.

12. Holowatz L.A., Thompson-Torgerson C.S., Kenney W.L. The human cutaneous circulation as a model of generalized microvascular function // J. Appl. Physiol. 2008. Vol. 105. № 1. Р. 370-372.

13. International Diabetes Federation. 2013. URL: http://www.idf.org/diabetesatlas (дата обращения 25.02.2014).

14. Jan Y.K., Lung C. W., Cuaderes E. et al. Effect of viscoelastic properties of plantar soft tissues on plantar pressure sat the first metatarsal head in diabetics with peripheral neuropathy // Physiol. Meas. 2013. Vol. 34. P. 53-66.

15. Jan Y.K., Shen S., Foreman R., Ennis W.J. Skin blood flow response to locally applied mechanical and thermal stresses in the diabetic foot // Microvasc. Research. 2013. Vol. 89. P. 40-46.

16. Johnson J., Kellogg D.L. Local thermal control of the human cutaneous circulation // Jr. Journal of Applied Physiology. 2010. Vol. 109. P. 1229-1238.

17. Jude E. B., Eleftheriadou I., Tentolouris N. Peripheral arterial disease in diabetes // Diabet Med. 2010. Vol. 27. P. 4-14.

18. Khan F., Elhadd T.A., Greene S.A. et al. Impaired skin microvascular function in children, adolescents, and young adults with type 1 diabetes // Diabetes Care. 2000. Vol. 23. P. 215-220.

19. Kim P.J, Steinberg J.S. Complications of the diabetic foot // Endocrinol. Metab. Clin. North Am. 2013. Vol. 42. № 4. P. 833-847.

20. Kvandal P., Stefanovska A., Veber M. et al. Regulation of human cutaneous circulation evaluated by laser Doppler flowmetry, iontophoresis, and spectral analysis: Importance of nitric oxide and prostaglandins // Microvasc. Res. 2003. Vol. 65. № 3. Р. 160-171.

21. Lefrandt J.D., Bosma E., Oomen P. et al. Sympathetic mediated vasomotion and capillary permeability in diabetic patients with peripheral neuropathy // Diebetol. 2003. Vol. 46. P. 40-47.

22. Minson C.T., Berry L.T., Joyner M.J. Nitric oxide and neurally mediated regulation of skin blood flow during local heating // J. Appl. Physiol. 2001. Vol. 91. № 4. Р. 1619-1626.

23. Nandi A., Poretsky L. Diabetes and the female reproductive system // Endocrinol. Metab. Clin. North Am. 2013. Vol. 42. P. 915-946.

24. Olesen P., Ledet T., Rasmussen L.M. Arterial osteoprotegerin: increased amounts in diabetes and modifiable synthesis from vascular smooth muscle cells by insulin and TNF alfa // Diabetologia. 2005. Vol. 48. P. 561-568.

25. Ozdemir B.A., Brownrigg J.R., Jones K.G. et al. Systematic review of screening investigations for peripheral arterial disease in patients with diabetes mellitus // Surg. Technol. Int. 2013. Vol. 23. P. 51-58.

26. Polovina M.M., Potpara T.S. Endothelial dysfunction in metabolic and vascular disorders // Postgrad Med. 2014. Vol. 126. № 2. Р. 38-53.

27. Podtaev S., Morozov M., Frick P. Wavelet-based correlations of skin temperature and bloodflow oscillations // Cardiovasc. Eng. 2008. Vol. 8 № 3. Р. 185-189.

28. Prompers L., Schaper N., Apelqvist J. et al. Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. EURODIALE Study // Diabetologia. 2008. Vol. 51. P. 747-755.

29. Ruiter M.S, van Golde J.M., Schaper N.C. et al. Diabetes impairs arteriogenesis in the peripheral circulation: review of molecular mechanisms // Clin Sci. 2010. Vol. 119. P. 225-238.

30. Santos V.P., Alves C.A., Fidelis C., Araujo Filho J.S. Arteriographic findings in diabetic and non-diabetic with critical limb ischemia // Rev. Assoc. Med. Bras. 2013. Vol. 59 № 6. Р. 557-662.

31. Shiogai Y., Stefanovska A., McClintock P. Nonlinear dynamics of cardiovascular ageing // Phys Rep. 2010. Vol. 488. P. 51-110.

32. Shusterman V., Anderson K.P., Barnea O. Spontaneous skin temperature oscillations in normal human subjects // Am. J. Physiol. 1997. Vol. 273 (3 Pt 2). Р. R1173-R1181.

33. Trivedi U., Parameswaran S., Armstrong A. et al. Prevalence of Multiple Antibiotic Resistant Infections in Diabetic versus Nondiabetic Wounds // J. Pathog. 2014. doi: 10.1155/2014/173053.

34. Vlassara H., Striker G. E. Advanced glycation and products in diabetes and diabetic complications // Endocrinol. Metab. Clin. N. Am. 2013. Vol. 42. P 697-719.