Abstract

Evaluation of skin microcirculation allows for the assessment of functional states for neuroendocrine and endothelial regulation. We present a novel method to visualize skin microvessels in any area of the body, which is in contrast to classical capillaroscopy, in which the application areas are limited to the nailfold and retina capillaries. The technique is based on microscopic video-image analysis. It exploits a specific feature of irregularity of red-blood-cells motion. Feasibility of the method is demonstrated by mapping the skin capillaries in the forearm and face of 11 healthy volunteers. The proposed method is promising for the quantitative assessment of cutaneous microcirculation in a wide range of diseases and functional states.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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  1. B. Fagrell and M. Intaglietta, “Microcirculation: its significance in clinical and molecular medicine,” J. Intern. Med. 241(5), 349–362 (1997).
    [Crossref]
  2. S. Erikkson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices: Evidence Res. 7, 445–452 (2014).
    [Crossref]
  3. C. Lal and M. J. Leahy, “An updated review of methods and advancements in microvascular blood flow imaging,” Microcirculation 23(5), 345–363 (2016).
    [Crossref]
  4. P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
    [Crossref]
  5. M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
    [Crossref]
  6. F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
    [Crossref]
  7. M. Cutolo, A. Sulli, and V. Smith, “How to perform and interpret capillaroscopy,” Best Pract. Res. Clin. Rheumatol. 27(2), 237–248 (2013).
    [Crossref]
  8. E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
    [Crossref]
  9. M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
    [Crossref]
  10. E. C. LeRoy and T. A. Medsger, “Criteria for the classification of early systemic sclerosis,” J. Rheumatol. 28(7), 1573–1576 (2001).
  11. I. S. Sidorov, M. A. Volynsky, and A. A. Kamshilin, “Influence of polarization filtration on the information readout from pulsating blood vessels,” Biomed. Opt. Express 7(7), 2469–2474 (2016).
    [Crossref]
  12. A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
    [Crossref]
  13. I. P. Gurov, M. V. Volkov, N. B. Margaryants, A. Pimenov, and A. V. Potemkin, “High-speed video capillaroscopy method for imaging and evaluation of moving red blood cells,” Opt. Lasers Eng. 104, 244–251 (2018).
    [Crossref]
  14. J. Allen, “Photoplethysmography and its application in clinical physiological measurement,” Physiol. Meas. 28(3), R1–R39 (2007).
    [Crossref]
  15. A. A. Kamshilin, I. S. Sidorov, L. Babayan, M. A. Volynsky, R. Giniatullin, and O. V. Mamontov, “Accurate measurement of the pulse wave delay with imaging photoplethysmography,” Biomed. Opt. Express 7(12), 5138–5147 (2016).
    [Crossref]
  16. A. V. Moço, S. Stuijk, and G. de Haan, “Motion robust PPG-imaging through color channel mapping,” Biomed. Opt. Express 7(5), 1737–1754 (2016).
    [Crossref]
  17. S. Shin, Y. Yang, and J.-S. Suh, “Measurement of erythrocyte aggregation in a microchip stirring system by light transmission,” Clin. Hemorheol. Microcirc. 41(3), 197–207 (2009).
    [Crossref]
  18. M. Hahn, T. Klysz, and M. Junger, “Synchronous measurements of blood pressure and red blood cell velocity in capillaries of human skin,” J. Invest. Dermatol. 106(6), 1256–1259 (1996).
    [Crossref]
  19. M. Roustit and J.-L. Cracowski, “Assessment of endothelial and neurovascular function in human skin microcirculation,” Trends Pharmacol. Sci. 34(7), 373–384 (2013).
    [Crossref]
  20. B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
    [Crossref]
  21. M. Shibasaki, D. A. Low, S. L. Davis, and C. G. Crandall, “Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine,” J. Appl. Physiol. 105(5), 1504–1508 (2008).
    [Crossref]

2018 (2)

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

I. P. Gurov, M. V. Volkov, N. B. Margaryants, A. Pimenov, and A. V. Potemkin, “High-speed video capillaroscopy method for imaging and evaluation of moving red blood cells,” Opt. Lasers Eng. 104, 244–251 (2018).
[Crossref]

2017 (1)

M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
[Crossref]

2016 (4)

2015 (1)

A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
[Crossref]

2014 (1)

S. Erikkson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices: Evidence Res. 7, 445–452 (2014).
[Crossref]

2013 (4)

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

M. Cutolo, A. Sulli, and V. Smith, “How to perform and interpret capillaroscopy,” Best Pract. Res. Clin. Rheumatol. 27(2), 237–248 (2013).
[Crossref]

E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
[Crossref]

M. Roustit and J.-L. Cracowski, “Assessment of endothelial and neurovascular function in human skin microcirculation,” Trends Pharmacol. Sci. 34(7), 373–384 (2013).
[Crossref]

2009 (1)

S. Shin, Y. Yang, and J.-S. Suh, “Measurement of erythrocyte aggregation in a microchip stirring system by light transmission,” Clin. Hemorheol. Microcirc. 41(3), 197–207 (2009).
[Crossref]

2008 (2)

B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

M. Shibasaki, D. A. Low, S. L. Davis, and C. G. Crandall, “Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine,” J. Appl. Physiol. 105(5), 1504–1508 (2008).
[Crossref]

2007 (1)

J. Allen, “Photoplethysmography and its application in clinical physiological measurement,” Physiol. Meas. 28(3), R1–R39 (2007).
[Crossref]

2001 (1)

E. C. LeRoy and T. A. Medsger, “Criteria for the classification of early systemic sclerosis,” J. Rheumatol. 28(7), 1573–1576 (2001).

1997 (1)

B. Fagrell and M. Intaglietta, “Microcirculation: its significance in clinical and molecular medicine,” J. Intern. Med. 241(5), 349–362 (1997).
[Crossref]

1996 (1)

M. Hahn, T. Klysz, and M. Junger, “Synchronous measurements of blood pressure and red blood cell velocity in capillaries of human skin,” J. Invest. Dermatol. 106(6), 1256–1259 (1996).
[Crossref]

1975 (1)

P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
[Crossref]

Agostini, D.

B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

Allen, J.

J. Allen, “Photoplethysmography and its application in clinical physiological measurement,” Physiol. Meas. 28(3), R1–R39 (2007).
[Crossref]

Anliker, M.

P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
[Crossref]

Babayan, L.

Bertolazzi, C.

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

Bollinger, A.

P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
[Crossref]

Boracchi, P.

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

Butti, P.

P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
[Crossref]

Cracowski, J.-L.

M. Roustit and J.-L. Cracowski, “Assessment of endothelial and neurovascular function in human skin microcirculation,” Trends Pharmacol. Sci. 34(7), 373–384 (2013).
[Crossref]

Crandall, C. G.

M. Shibasaki, D. A. Low, S. L. Davis, and C. G. Crandall, “Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine,” J. Appl. Physiol. 105(5), 1504–1508 (2008).
[Crossref]

Cutolo, M.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

M. Cutolo, A. Sulli, and V. Smith, “How to perform and interpret capillaroscopy,” Best Pract. Res. Clin. Rheumatol. 27(2), 237–248 (2013).
[Crossref]

Davis, S. L.

M. Shibasaki, D. A. Low, S. L. Davis, and C. G. Crandall, “Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine,” J. Appl. Physiol. 105(5), 1504–1508 (2008).
[Crossref]

De Angelis, R.

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

de Haan, G.

Deschepper, E.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

Erikkson, S.

S. Erikkson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices: Evidence Res. 7, 445–452 (2014).
[Crossref]

Erofeev, N. P.

A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
[Crossref]

Fagrell, B.

B. Fagrell and M. Intaglietta, “Microcirculation: its significance in clinical and molecular medicine,” J. Intern. Med. 241(5), 349–362 (1997).
[Crossref]

Fornili, M.

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

Giniatullin, R.

Gronenschild, E. H. B. M.

E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
[Crossref]

Gualtierotti, R.

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

Gurov, I. P.

I. P. Gurov, M. V. Volkov, N. B. Margaryants, A. Pimenov, and A. V. Potemkin, “High-speed video capillaroscopy method for imaging and evaluation of moving red blood cells,” Opt. Lasers Eng. 104, 244–251 (2018).
[Crossref]

M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
[Crossref]

Gutierrez, M.

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

Hahn, M.

M. Hahn, T. Klysz, and M. Junger, “Synchronous measurements of blood pressure and red blood cell velocity in capillaries of human skin,” J. Invest. Dermatol. 106(6), 1256–1259 (1996).
[Crossref]

Holliger, C.

P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
[Crossref]

Houben, A. J. H. M.

E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
[Crossref]

Ingegnoli, F.

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

Intaglietta, M.

B. Fagrell and M. Intaglietta, “Microcirculation: its significance in clinical and molecular medicine,” J. Intern. Med. 241(5), 349–362 (1997).
[Crossref]

P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
[Crossref]

Junger, M.

M. Hahn, T. Klysz, and M. Junger, “Synchronous measurements of blood pressure and red blood cell velocity in capillaries of human skin,” J. Invest. Dermatol. 106(6), 1256–1259 (1996).
[Crossref]

Kamshilin, A. A.

M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
[Crossref]

I. S. Sidorov, M. A. Volynsky, and A. A. Kamshilin, “Influence of polarization filtration on the information readout from pulsating blood vessels,” Biomed. Opt. Express 7(7), 2469–2474 (2016).
[Crossref]

A. A. Kamshilin, I. S. Sidorov, L. Babayan, M. A. Volynsky, R. Giniatullin, and O. V. Mamontov, “Accurate measurement of the pulse wave delay with imaging photoplethysmography,” Biomed. Opt. Express 7(12), 5138–5147 (2016).
[Crossref]

A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
[Crossref]

Karaca, U.

E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
[Crossref]

Klysz, T.

M. Hahn, T. Klysz, and M. Junger, “Synchronous measurements of blood pressure and red blood cell velocity in capillaries of human skin,” J. Invest. Dermatol. 106(6), 1256–1259 (1996).
[Crossref]

Lal, C.

C. Lal and M. J. Leahy, “An updated review of methods and advancements in microvascular blood flow imaging,” Microcirculation 23(5), 345–363 (2016).
[Crossref]

Leahy, M. J.

C. Lal and M. J. Leahy, “An updated review of methods and advancements in microvascular blood flow imaging,” Microcirculation 23(5), 345–363 (2016).
[Crossref]

LeRoy, E. C.

E. C. LeRoy and T. A. Medsger, “Criteria for the classification of early systemic sclerosis,” J. Rheumatol. 28(7), 1573–1576 (2001).

Levy, B. I.

B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

Low, D. A.

M. Shibasaki, D. A. Low, S. L. Davis, and C. G. Crandall, “Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine,” J. Appl. Physiol. 105(5), 1504–1508 (2008).
[Crossref]

Lubatti, C.

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

Mamontov, O. V.

M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
[Crossref]

A. A. Kamshilin, I. S. Sidorov, L. Babayan, M. A. Volynsky, R. Giniatullin, and O. V. Mamontov, “Accurate measurement of the pulse wave delay with imaging photoplethysmography,” Biomed. Opt. Express 7(12), 5138–5147 (2016).
[Crossref]

Margaryants, N. B.

I. P. Gurov, M. V. Volkov, N. B. Margaryants, A. Pimenov, and A. V. Potemkin, “High-speed video capillaroscopy method for imaging and evaluation of moving red blood cells,” Opt. Lasers Eng. 104, 244–251 (2018).
[Crossref]

M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
[Crossref]

Medsger, T. A.

E. C. LeRoy and T. A. Medsger, “Criteria for the classification of early systemic sclerosis,” J. Rheumatol. 28(7), 1573–1576 (2001).

Melsens, K.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

Moço, A. V.

Mourad, J.-J.

B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

Muris, D. M. J.

E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
[Crossref]

Nilsson, J.

S. Erikkson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices: Evidence Res. 7, 445–452 (2014).
[Crossref]

Nippolainen, E.

A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
[Crossref]

Paolino, S.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

Pimenov, A.

I. P. Gurov, M. V. Volkov, N. B. Margaryants, A. Pimenov, and A. V. Potemkin, “High-speed video capillaroscopy method for imaging and evaluation of moving red blood cells,” Opt. Lasers Eng. 104, 244–251 (2018).
[Crossref]

Pizzorni, C.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

Podolian, N. P.

A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
[Crossref]

Potemkin, A. V.

I. P. Gurov, M. V. Volkov, N. B. Margaryants, A. Pimenov, and A. V. Potemkin, “High-speed video capillaroscopy method for imaging and evaluation of moving red blood cells,” Opt. Lasers Eng. 104, 244–251 (2018).
[Crossref]

M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
[Crossref]

Reimann, H.

P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
[Crossref]

Romashko, R. V.

A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
[Crossref]

Roustit, M.

M. Roustit and J.-L. Cracowski, “Assessment of endothelial and neurovascular function in human skin microcirculation,” Trends Pharmacol. Sci. 34(7), 373–384 (2013).
[Crossref]

Ruaro, B.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

Safar, M. E.

B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

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B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

Schram, M. T.

E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
[Crossref]

Shibasaki, M.

M. Shibasaki, D. A. Low, S. L. Davis, and C. G. Crandall, “Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine,” J. Appl. Physiol. 105(5), 1504–1508 (2008).
[Crossref]

Shin, S.

S. Shin, Y. Yang, and J.-S. Suh, “Measurement of erythrocyte aggregation in a microchip stirring system by light transmission,” Clin. Hemorheol. Microcirc. 41(3), 197–207 (2009).
[Crossref]

Sidorov, I. S.

Smith, V.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

M. Cutolo, A. Sulli, and V. Smith, “How to perform and interpret capillaroscopy,” Best Pract. Res. Clin. Rheumatol. 27(2), 237–248 (2013).
[Crossref]

Stehouwer, C. D. A.

E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
[Crossref]

Struijker-Boudier, H. A.

B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

Stuijk, S.

Sturesson, C.

S. Erikkson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices: Evidence Res. 7, 445–452 (2014).
[Crossref]

Suh, J.-S.

S. Shin, Y. Yang, and J.-S. Suh, “Measurement of erythrocyte aggregation in a microchip stirring system by light transmission,” Clin. Hemorheol. Microcirc. 41(3), 197–207 (2009).
[Crossref]

Sulli, A.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

M. Cutolo, A. Sulli, and V. Smith, “How to perform and interpret capillaroscopy,” Best Pract. Res. Clin. Rheumatol. 27(2), 237–248 (2013).
[Crossref]

Trombetta, A. C.

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

Vasilev, P. V.

A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
[Crossref]

Vicaut, E.

B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

Volkov, M. V.

I. P. Gurov, M. V. Volkov, N. B. Margaryants, A. Pimenov, and A. V. Potemkin, “High-speed video capillaroscopy method for imaging and evaluation of moving red blood cells,” Opt. Lasers Eng. 104, 244–251 (2018).
[Crossref]

M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
[Crossref]

Volynsky, M. A.

Yang, Y.

S. Shin, Y. Yang, and J.-S. Suh, “Measurement of erythrocyte aggregation in a microchip stirring system by light transmission,” Clin. Hemorheol. Microcirc. 41(3), 197–207 (2009).
[Crossref]

Best Pract. Res. Clin. Rheumatol. (1)

M. Cutolo, A. Sulli, and V. Smith, “How to perform and interpret capillaroscopy,” Best Pract. Res. Clin. Rheumatol. 27(2), 237–248 (2013).
[Crossref]

Biomed. Opt. Express (3)

Circulation (1)

B. I. Levy, E. L. Schiffrin, J.-J. Mourad, D. Agostini, E. Vicaut, M. E. Safar, and H. A. Struijker-Boudier, “Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus,” Circulation 118(9), 968–976 (2008).
[Crossref]

Clin. Hemorheol. Microcirc. (1)

S. Shin, Y. Yang, and J.-S. Suh, “Measurement of erythrocyte aggregation in a microchip stirring system by light transmission,” Clin. Hemorheol. Microcirc. 41(3), 197–207 (2009).
[Crossref]

J. Appl. Physiol. (1)

M. Shibasaki, D. A. Low, S. L. Davis, and C. G. Crandall, “Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine,” J. Appl. Physiol. 105(5), 1504–1508 (2008).
[Crossref]

J. Intern. Med. (1)

B. Fagrell and M. Intaglietta, “Microcirculation: its significance in clinical and molecular medicine,” J. Intern. Med. 241(5), 349–362 (1997).
[Crossref]

J. Invest. Dermatol. (1)

M. Hahn, T. Klysz, and M. Junger, “Synchronous measurements of blood pressure and red blood cell velocity in capillaries of human skin,” J. Invest. Dermatol. 106(6), 1256–1259 (1996).
[Crossref]

J. Rheumatol. (1)

E. C. LeRoy and T. A. Medsger, “Criteria for the classification of early systemic sclerosis,” J. Rheumatol. 28(7), 1573–1576 (2001).

Med. Devices: Evidence Res. (1)

S. Erikkson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices: Evidence Res. 7, 445–452 (2014).
[Crossref]

Microcirculation (2)

C. Lal and M. J. Leahy, “An updated review of methods and advancements in microvascular blood flow imaging,” Microcirculation 23(5), 345–363 (2016).
[Crossref]

M. Cutolo, A. C. Trombetta, K. Melsens, C. Pizzorni, A. Sulli, B. Ruaro, S. Paolino, E. Deschepper, and V. Smith, “Automated assessment of absolute nailfold capillary number on videocapillaroscopic images: Proof of principle and validation in systemic sclerosis,” Microcirculation 25(4), e12447 (2018).
[Crossref]

Microvasc. Res. (3)

F. Ingegnoli, R. Gualtierotti, C. Lubatti, C. Bertolazzi, M. Gutierrez, P. Boracchi, M. Fornili, and R. De Angelis, “Nailfold capillary patterns in healthy subjects: A real issue in capillaroscopy,” Microvasc. Res. 90, 90–95 (2013).
[Crossref]

E. H. B. M. Gronenschild, D. M. J. Muris, M. T. Schram, U. Karaca, C. D. A. Stehouwer, and A. J. H. M. Houben, “Semi-automatic assessment of skin capillary density: Proof of principle and validation,” Microvasc. Res. 90, 192–198 (2013).
[Crossref]

P. Butti, M. Intaglietta, H. Reimann, C. Holliger, A. Bollinger, and M. Anliker, “Capillary red blood cell velocity measurements in human nailfold by videodensitometric method,” Microvasc. Res. 10(2), 220–227 (1975).
[Crossref]

Opt. Lasers Eng. (1)

I. P. Gurov, M. V. Volkov, N. B. Margaryants, A. Pimenov, and A. V. Potemkin, “High-speed video capillaroscopy method for imaging and evaluation of moving red blood cells,” Opt. Lasers Eng. 104, 244–251 (2018).
[Crossref]

Physiol. Meas. (1)

J. Allen, “Photoplethysmography and its application in clinical physiological measurement,” Physiol. Meas. 28(3), R1–R39 (2007).
[Crossref]

Sci. Rep. (2)

A. A. Kamshilin, E. Nippolainen, I. S. Sidorov, P. V. Vasilev, N. P. Erofeev, N. P. Podolian, and R. V. Romashko, “A new look at the essence of the imaging photoplethysmography,” Sci. Rep. 5(1), 10494 (2015).
[Crossref]

M. V. Volkov, N. B. Margaryants, A. V. Potemkin, M. A. Volynsky, I. P. Gurov, O. V. Mamontov, and A. A. Kamshilin, “Video capillaroscopy clarifies mechanism of the photoplethysmographic waveform appearance,” Sci. Rep. 7(1), 13298 (2017).
[Crossref]

Trends Pharmacol. Sci. (1)

M. Roustit and J.-L. Cracowski, “Assessment of endothelial and neurovascular function in human skin microcirculation,” Trends Pharmacol. Sci. 34(7), 373–384 (2013).
[Crossref]

Supplementary Material (1)

NameDescription
» Visualization 1       This video shows the dynamics of the microscopic images of the forearm's skin area (on the left) with two magnified ROIs (on the right) from the image. The size of the forearm area is 2.5 x 2.5 mm2.

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Figures (6)

Fig. 1.
Fig. 1. Layout of the custom-made video-capillaroscopy setup providing visualization of capillaries in the forearm as an example.
Fig. 2.
Fig. 2. An exemplary frame of recorded microscopic image (a) and evolution of the pixel value averaged over the whole frame (b). The arrows in the panel (b) indicate the respective axes of the presented graphs.
Fig. 3.
Fig. 3. Particular realizations of PPG waveforms and their spectra. (a) Evolution of the mean pixel value estimated in four selected ROIs: red and pink are in the areas with moving RBCs, whereas blue and green – without. (b) PPG waveforms in the red and blue ROIs. (c) Power spectra of PPG waveforms in all four selected ROIs. Color of the graphs corresponds to the color of the squares marking ROI position in Fig. 2(a).
Fig. 4.
Fig. 4. Mean power spectra of PPG waveforms. (a) Averaging over 50 randomly chosen ROIs localized in the areas with moving RBCs (brown curve) and over other 50 ROIs localized in the areas without moving RBC (dark blue curve). (b) Similar graphs as in the panel (a) but the spectra from the same ROIs were averaged after suppression of the heart-related modulation.
Fig. 5.
Fig. 5. Microscopic images of the skin in the forearm and corresponding distribution of capillaries with moving RBCs. Demographic data of the subjects are listed in Table 1. Color scales on the right of each panel show the parameter FI.
Fig. 6.
Fig. 6. Microscopic images of the skin in the facial area (upper row – areas in cheeks, lower row – areas in the forehead) and corresponding distribution of capillaries with moving RBCs evaluated for two subjects: left column – subject MAK; right column – subject ZAA (see Table 2 for details). Color scales on the right of each panel show the parameter FI.

Tables (2)

Tables Icon

Table 1. Power spectrum dispersion measured in the forearm

Tables Icon

Table 2. Power spectrum dispersion measured in the facial area (cheek and forehead)