Rapid multi-wavelength optical assessment of circulating blood volume without a priori data

Abstract

The measurement of circulating blood volume (CBV) is crucial in various medical conditions including surgery, iatrogenic problems, rapid fluid administration, transfusion of red blood cells, or trauma with extensive blood loss including battlefield injuries and other emergencies. Currently, available commercial techniques are invasive and time-consuming for trauma situations. Recently, we have proposed high-speed multi-wavelength photoacoustic/photothermal (PA/PT) flow cytometry for in vivo CBV assessment with multiple dyes as PA contrast agents (labels). As the first step, we have characterized the capability of this technique to monitor the clearance of three dyes (indocyanine green, methylene blue, and trypan blue) in an animal model. However, there are strong demands on improvements in PA/PT flow cytometry. As additional verification of our proof-of-concept of this technique, we performed optical photometric CBV measurements in vitro. Three label dyes—methylene blue, crystal violet and, partially, brilliant green—were selected for simultaneous photometric determination of the components of their two-dye mixtures in the circulating blood in vitro without any extra data (like hemoglobin absorption) known a priori. The tests of single dyes and their mixtures in a flow system simulating a blood transfusion system showed a negligible difference between the sensitivities of the determination of these dyes under batch and flow conditions. For individual dyes, the limits of detection of 3×10^–6 M‒3×10^–6 M in blood were achieved, which provided their continuous determination at a level of 10^–5 M for the CBV assessment without a priori data on the matrix. The CBV assessment with errors no higher than 4% were obtained, and the possibility to apply the developed procedure for optical photometric (flow cytometry) with laser sources was shown.

Keywords

Circulating blood volume assessment / spectrophotometry / methylene blue / crystal violet

References

[1] Lozhkin A., Makedonskaya T., Pakhomova G., Loran O.. Estimation of the trauma severity degree in injured with associated injuries depending on the blood loss. Vox Sanguinis, 2010, 99(1): 435-436.

[2] Takanishi D. M. Jr., Biuk-Aghai E. N., Yu M., Lurie F., Yamauchi H., Ho H. C., . The availability of circulating blood volume values alters fluid management in critically ill surgical patients. American Journal of Surgery, 2009, 197(2): 232-237.

[3] Baulig W., Bernhard E. O., Bettex D., Schmidlin D., Schmid E. R.. Cardiac output measurement by pulse dye densitometry in cardiac surgery. Anaesthesia, 2005, 60(10): 968-973.

[4] Kroon M., Groeneveld A. B., Smulders Y. M.. Cardiac output measurement by pulse dye densitometry: comparison with pulmonary artery thermodilution in post-cardiac surgery patients. Journal of Clinical Monitoring and Computing, 2005, 19(6): 395-399.

[5] Henschen S., Busse M. W., Zisowsky S., Panning B.. Determination of plasma volume and total blood volume using indocyanine green: a short review. Journal of Medicine, 1993, 24(1): 10-27.

[6] Donner L., Maly V.. Total blood volume in some blood diseases. II. results in pernicious anemia, anemia following hemorrhage, polycythemia vera, secondary polyglobulia and leukemia. Sbornik Lekarsky, 1955, 57(5): 125-136.

[7] American Journal of Obstetrics and Gynecology, 2015, 213(3

[8] Joffe A., Khandelwal N., Hallman M., Treggiari M.. Assessment of circulating blood volume with fluid administration targeting euvolemia or hypervolemia. Neurocritical Care, 2015, 22(1): 82-88.

[9] Konno D., Nishino R., Ejima Y., Ohnishi E., Sato K., Kurosawa S.. Assessment of the perioperative factors contributing to the hemodynamic changes during surgery in ten patients with pheochromocytoma. Masui. Japanese Journal of Anesthesiology, 2013, 62(4): 421-425.

[10] Tanaka K., Sato T., Kondo C., Yada I., Yuasa H., Kusagawa M., . Hematological problems during the use of cardiac assist devices: clinical experiences in Japan. Artificial Organs, 1992, 16(2): 182-188.

[11] Keith N. M., Rowntree L. G., Geraghty J. T.. A method for the determination of plasma and blood volume. Archives of Internal Medicine, 1915, 16(4): 547-557.

[12] Jegier W., Maclaurin J., Blankenship W., Lind J.. Comparative study of blood volume estimation in the newborn infant using I-131 labeled human serum albumin (Ihsa) and T-1824. Scandinavian Journal of Clinical and Laboratory Investigation, 1964, 16, 125-132.

[13] Uglova N. N., Volozhin A. I., Potkin V. E.. Method for determination of the circulating blood volume with Evans blue T-1824. Patologicheskaia Fiziologiia i Eksperimentalnaia Terapiia, 1972, 16(2): 80-82.

[14] Glants S. A., Shevchuk V. V.. A micromethod for the determination of blood volume in laboratory animals. Laboratornoe Delo, 1963, 16, 49.

[15] Kovalev O. A., Grishanov V. N.. Determination of the volume of circulating blood by using Evans blue dye. Laboratornoe Delo, 1976, 11, 664-667.

[16] Gillen C. M., Takamata A., Mack G. W., Nadel E. R.. Measurement of plasma volume in rats with use of fluorescent-labeled albumin molecules. Journal of Applied Physiology, 1994, 76(1): 485-489.

[17] Tudhope G. R., Wilson G. M.. A comparison of 86Rb, 32P and 51Cr as labels for red blood cells. Journal of Physiology, 1955, 128(3): 61-62.

[18] Sivachenko T. P., Kalina V. K., Ishchenko V. P., Belous A. K., Kapustnik V. I.. Repeated semi-automatic determination of circulating blood volume. Vrachebnoe Delo, 1977, 7, 25-28.

[19] Gray S. J., Sterling K.. Determination of circulating red cell volume by radioactive chromium. Science, 1950, 112(2902): 179-180.

[20] Datsenko B. M., Pilipenko N. I., Gubskii V. I., Sherlanov R. A.. The determination of the volume of circulating plasma using the indicator T-1824. Laboratornoe Delo, 1990, 11, 32-34.

[21] Gibson J. G., Seligman A. M., Peacock W. C., Aub J. C., Fine J., Evans R. D.. The distribution of red cells and plasma in large and minute vessels of the normal dog, determined by radioactive isotopes of iron and iodine. Journal of Clinical Investigation, 1946, 25(6): 848-857.

[22] Modestov V. K., Tsygankov A. T.. Thyroid function tests using triiodothyronine labeled with I-131. Meditsinskaia Radiologiia, 1965, 10, 11-13.

[23] Frid I. A., Stoliarov V. I., Evtiukhin A. I., Bernshtein M. I.. Hemodynamic indices and the volume of circulating blood in the surgical treatment of cancer of the esophagus and cardial portion of the stomach. Vestnik Khirurgii Imeni I. I. Grekova, 1976, 117(10): 92-96.

[24] Haruna M., Kumon K., Yahagi N., Watanabe Y., Ishida Y., Kobayashi N., Aoyagi T.. Blood volume measurement at the bedside using ICG pulse spectrophotometry. Anesthesiology, 1998, 89(6): 1322-1328.

[25] Imai T., Takahashi K., Fukura H., Morishita Y.. Measurement of cardiac output by pulse dye densitometry using indocyanine green: a comparison with the thermodilution method. Anesthesiology, 1997, 87(4): 816-822.

[26] Tichy J. A., Loucka M., Trefny Z. M., Hojerova M., Svacinka J., Muller J., . New clearance evaluation method for hepatological diagnostics. Physiological Research, 2009, 58(2): 287-292.

[27] Hofer C. K., Ganter M. T., Zollinger A.. What technique should I use to measure cardiac output?. Current Opinion in Critical Care, 2007, 13(3): 308-317.

[28] Goy R. W., Chiu J. W., Loo C. C.. Pulse dye densitometry: a novel bedside monitor of circulating blood volume. Annals of the Academy of Medicine, 2001, 30(2): 192-198.

[29] Sugimoto H., Okochi O., Hirota M., Kanazumi N., Nomoto S., Inoue S., . Early detection of liver failure after hepatectomy by indocyanine green elimination rate measured by pulse dyedensitometry. Journal of Hepato-Biliary- Pancreatic Surgery, 2006, 13(6): 543-548.

[30] Hoff R. G., Algra A., Kalkman C. J., Rinkel G. J.. Fluid balance and blood volume measurement after aneurysmal subarachnoid hemorrhage. Neurocritical Care, 2008, 8(3): 391-397.

[31] Sha K., Shimokawa M., Morii M., Kikumoto K., Inoue S., Kishi K., . Optimal dose of indocyanine-green injected from the peripheral vein in cardiac output measurement by pulse dyedensitometry. Masui. Japanese Journal of Anesthesiology, 2000, 49(2): 172-176.

[32] Taguchi N., Nakagawa S., Miyasaka K., Fuse M., Aoyagi T.. Cardiac output measurement by pulse dye densitometry using three wavelengths. Pediatric Critical Care Medicine, 2004, 5(4): 343-350.

[33] Fujita Y., Yamamoto T., Fuse M., Kobayashi N., Takeda S., Aoyagi T.. Pulse dye densitometry using indigo carmine is useful for cardiac output measurement, but not for circulating blood volume measurement. European Journal of Anaesthesiology, 2004, 21(8): 632-637.

[34] Imai T., Mitaka C., Nosaka T., Koike A., Ohki S., Isa Y., . Accuracy and repeatability of blood volume measurement by pulse dye densitometry compared to the conventional method using 51Cr-labeled red blood cells. Intensive Care Medicine, 2000, 26(9): 1343-1349.

[35] Kunihara T., Wakamatsu Y., Adachi A., Koyama M., Shiiya N., Sasaki S., . Clinical evaluation of hepatic blood flow and oxygen metabolism during thoracoabdominal aortic surgery using pulse dye-densitometry combined with hepatic venous oxygen saturation. Kyobu Geka. Japanese Journal of Thoracic Surgery, 2000, 53(7): 551-557.

[36] Hori T., Yagi S., Iida T., Taniguchi K., Yamagiwa K., Yamamoto C., . Stability of cirrhotic systemic hemodynamics ensures sufficient splanchnic blood flow after living-donor liver transplantation in adult recipients with liver cirrhosis. World Journal of Gastroenterology, 2007, 13(44): 5918-5925.

[37] Akita H., Sasaki Y., Yamada T., Gotoh K., Ohigashi H., Eguchi H., . Real-time intraoperative assessment of residual liver functional reserve using pulse dye densitometry. World Journal of Surgery, 2008, 32(12): 2668-2674.

[38] Stauber R. E., Wagner D., Stadlbauer V., Palma S., Gurakuqi G., Kniepeiss D., . Evaluation of indocyanine green clearance and model for end-stage liver disease for estimation of short-term prognosis in decompensated cirrhosis. Liver International: Official Journal of the International Association for the Study of the Liver, 2009, 29(10): 1516-1520.

[39] Takazawa T., Nishikawa K., Watanabe I., Goto F.. Preoperative evaluation of hemodynamics using indocyanine green clearance meter in patients with peritonitis from gastrointestinal perforation. Masui the Japanese Journal of Anesthesiology, 2005, 54(3): 260-264.

[40] Hoff R., Rinkel G., Verweij B., Algra A., Kalkman C.. Blood volume measurement to guide fluid therapy after aneurysmal subarachnoid hemorrhage: a prospective controlled study. Stroke, 2009, 40(7): 2575-2577.

[41] Okochi O., Kaneko T., Sugimoto H., Inoue S., Takeda S., Nakao A.. ICG pulse spectrophotometry for perioperative liver function in hepatectomy. Journal of Surgical Research, 2002, 103(1): 109-113.

[42] Bradley E. C., Barr J. W.. Determination of blood volume using indocyanine green (cardio-green) dye. Life Sciences, 1968, 7(17): 1001-1007.

[43] Fukuda H., Kawamoto M., Yuge O.. A comparison of finger and nose probes in pulse dye-densitometry measurements of cardiac output, blood volume and mean transit time. Masui the Japanese Journal of Anesthesiology, 2001, 50(12): 1351-1356.

[44] Bremer F., Schiele A., Tschaikowsky K.. Cardiac output measurement by pulse dye densitometry: a comparison with the Fick's principle and thermodilution method. Intensive Care Medicine, 2002, 28(4): 399-405.

[45] Nedosekin D. A., Galanzha E. I., Dervishi E., Biris A. S., Zharov V. P.. Super-resolution nonlinear photothermal microscopy. Small, 2014, 10(1): 135-142.

[46] Nedosekin D. A., Sarimollaoglu M., Galanzha E. I., Sawant R., Torchilin V. P., Verkhusha V. V., . Synergy of photoacoustic and fluorescence flow cytometry of circulating cells with negative and positive contrasts. Journal of Biophotonics, 2013, 6(5): 425-434.

[47] Menyaev Y. A., Nedosekin D. A., Sarimollaoglu M., Juratli M. A., Galanzha E. I., Tuchin V. V., . Optical clearing in photoacoustic flow cytometry. Biomedical Optics Express, 2013, 4(12): 3030-3041.

[48] Proskurnin M. A., Zhidkova T. V., Volkov D. S., Sarimollaoglu M., Galanzha E. I., Mock D., . In vivo multispectral photoacoustic and photothermal flow cytometry with multicolor dyes: A potential for real-time assessment of circulation, dye-cell interaction, and blood volume. Cytometry Part A the Journal of the International Society for Analytical Cytology, 2011, 79A(10): 834-847.

[49] S. E. Bialkowski, Photothermal spectroscopy methods for chemical analysis. New York: Wiley-Interscience, 1996.

[50] Wang L. V.. Multiscale photoacoustic microscopy and computed tomography. Nature Photonics, 2009, 3(9): 503-509.

[51] Mallidi S., Larson T., Tam J., Joshi P. P., Karpiouk A., Sokolov K., . Multiwavelength photoacoustic imaging and plasmon resonance coupling of gold nanoparticles for selective detection of cancer. Nano Letters, 2009, 9(8): 2825-2831.

[52] V. P. Zharov and V. S. Letokhov, Laser optoacoustic spectroscopy. Berlin-Heidelberg: Springer-Verlag, 1986.

[53] Zharov V. P.. Laser optoacoustic spectroscopy in chromatography. in Laser analytical spectrochemistry, 1986, Boston, MA: Bristol, 229-271.

[54] Harada M., Shibata M., Kitamori T., Sawada T.. Application of coaxial beam photothermal microscopy to the analysis of a single biological cell in water. Analytica Chimica Acta, 1995, 299(3): 343-347.

[55] Wang L. V.. Photoacoustic imaging and spectroscopy., 2009, New York: Taylor & Francis/CRC Press

[56] Proskurnin M. A.. Photothermal spectroscopy. in Laser spectroscopy for sensing: fundamentals, techniques and applications, 2014, Cambridge: Woodhead Publ Ltd, 313-361.

[57] Zharov V. P., Lapotko D. O.. Photothermal imaging of nanoparticles and cells. IEEE Journal of Selected Topics in Quantum Electronics, 2005, 11(4): 733-751.

[58] Petrova I. Y., Esenaliev R. O., Petrov Y. Y., Brecht H. P., Svensen C. H., Olsson J., . Optoacoustic monitoring of blood hemoglobin concentration: a pilot clinical study. Optics Letters, 2005, 30(13): 1677-1679.

[59] Petrov Y. Y., Petrova I. Y., Patrikeev I. A., Esenaliev R. O., Prough D. S.. Multiwavelength optoacoustic system for noninvasive monitoring of cerebral venous oxygenation: a pilot clinical test in the internal jugular vein. Optics Letters, 2006, 31(12): 1827-1829.

[60] Kolkman R. G., Steenbergen W., van Leeuwen T. G.. In vivo photoacoustic imaging of blood vessels with a pulsed laser diode. Lasers in Medical Science, 2006, 21(3): 134-139.

[61] Ermilov S., Stein A., Conjusteau A., Gharieb R., Lacewell R., Miller T., . 2007 Detection and noninvasive diagnostics of breast cancer with 2-color laser optoacoustic imaging system. in Proc. SPIE, 2007, 6437, 643703-643711.

[62] Vaartjes S. E., Klaase J. M., . 2007 First clinical trials of the Twente photoacoustic mammoscope (PAM). in Proc. SPIE, 2007, 6629, 662912-662917.

[63] Razansky D., Distel M., Vinegoni C., Ma R., Perrimon N., Koster R. W., . Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo. Nature Photonics, 2009, 3(7): 412-417.

[64] Tuchin V. V., Zharov V. P.. In vivo flow cytometry: a horizon of opportunities. Cytometry Part A, 2011, 79A(10): 737-745.

[65] Brusnichkin A. V., Nedosekin D. A., Galanzha E. I., Vladimirov Y. A., Shevtsova E. F., Proskurnin M. A., . Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions. Journal of Biophotonics, 2010, 3(12): 791-806.

[66] Galanzha E. I., Kokoska M. S., Shashkov E. V., Kim J. W., Tuchin V. V., Zharov V. P.. In vivo fiber-based multicolor photoacoustic detection and photothermal purging of metastasis in sentinel lymph nodes targeted by nanoparticles. Journal of Biophotonics, 2009, 2(8‒9): 528-539.

[67] Galanzha E. I., Kim J. W., Zharov V. P.. Nanotechnology-based molecular photoacoustic and photothermal flow cytometry platform for in-vivo detection and killing of circulating cancer stem cells. Journal of Biophotonics, 2009, 2(12): 725-735.

[68] Zharov V. P., Galanzha E. I., Shashkov E. V., Kim J. W., Khlebtsov N. G., Tuchin V. V.. Photoacoustic flow cytometry: principle and application for real-time detection of circulating single nanoparticles, pathogens, and contrast dyes in vivo. Journal of Biomedical Optics, 2007, 12(5): 1-14.

[69] Modestov A. D., Pleskov Y. V., Varnin V. P., Teremetskaya I. G.. Synthetic semiconductor diamond electrodes: a study of electrochemical activity in a redox system solution. Russian Journal of Electrochemistry, 1997, 33(1): 55-60.

[70] Galanzha E. I., Zharov V. P.. In vivo photoacoustic and photothermal cytometry for monitoring multiple blood rheology parameters. Cytometry Part A, 2011, 79A(10): 746-757.

[71] Lozhkin S. A.. Depth of Boolean functions in a complete basis. Vestnik Moskovskogo Universiteta Seriya 1 Matematika Mekhanika, 1996, 51(2): 80-83.

[72] Brusnichkin A., Nedosekin D., Ryndina E., Proskurnin M., Gleb E., Lapotko D., . Determination of various hemoglobin species with thermal-lens spectrometry. Moscow University Chemistry Bulletin, 2009, 64(1): 45-54.

[73] Proskurnin M. A., Abroskin A. G., Radushkevich D. Y.. A dual-beam thermal lens spectrometer for flow analysis. Journal of Analytical Chemistry, 1999, 54(1): 91-97.

[74] Riley A. A., Arakawa Y., Worley S., Duncan B. W., Fukamachi K.. Circulating blood volumes: a review of measurement techniques and a meta-analysis in children. ASAIO Journal, 2010, 56(3): 260-264.

[75] Karpinska J., Sokol A., Rozko M.. Applicability of derivative spectrophotometry, bivariate calibration algorithm, and the vierordt method for simultaneous determination of ranitidine and amoxicillin in their binary mixtures. Analytical Letters, 2009, 42(8): 1203-1218.

[76] Dinc E., Onur F.. Comparative study of the ratio spectra derivative spectrophotometry, derivative spectrophotometry and Vierordt's method applied to the analysis of oxfendazole and oxyclozanide in a veterinary formulation. Analusis, 1997, 25(3): 55-59.

[77] Yaseen M. A., Yu J., Jung B., Wong M. S., Anvari B.. Biodistribution of encapsulated indocyanine green in healthy mice. Molecular Pharmaceutics, 2009, 6(5): 1321-1332.

[78] Saxena V., Sadoqi M., Shao J.. Enhanced photo-stability, thermal-stability and aqueous-stability of indocyanine green in polymeric nanoparticulate systems. Journal of Photochemistry and Photobiology. B: Biology, 2004, 74(1): 29-38.

[79] Shestakov N. M.. Complexity and inadequacy of current methods of determining circulating blood volume and the feasibility of a simpler and faster method of determining it. Terapevticheskii Arkhiv, 1977, 49(3): 115-120.

[80] Tsopelas C., Sutton R.. Why certain dyes are useful for localizing the sentinel lymph node. Journal of Nuclear Medicine, 2002, 43(10): 1377-1382.

[81] Dawson A. B., Evans H. M., Whipple G. H.. Blood volume studies: III. behavior of large series of dyes introduced into the circulating blood. American Journal of Physiology, 1920, 51(2): 232-256.

[82] Shoemaker K., Rubin J., Zumbro G. L., Tackett R.. Evans blue and gentian violet: alternatives to methylene blue as a surgical marker dye. Journal of Thoracic and Cardiovascular Surgery, 1996, 112(2): 542-544.

[83] Smirnova A., Proskurnin M. A., Bendrysheva S. N., Nedosekin D. A., Hibara A., Kitamori T.. Thermooptical detection in microchips: From macro- to micro-scale with enhanced analytical parameters. Electrophoresis, 2008, 29(13): 2741-2753.

[84] Proskurnin M. A., Abroskin A. G.. Optimization of optical system parameters in dual-beam thermal lens spectrometry. Journal of Analytical Chemistry, 1999, 54(5): 401-408.

[85] Nedosekin D. A., Sarimollaoglu M., Shashkov E. V., Galanzha E. I., Zharov V. P.. Ultra-fast photoacoustic flow cytometry with a 0.5 MHz pulse repetition rate nanosecond laser. Optics Express, 2010, 18(8): 8605-8620.

[86] Nedosekin D. A., Shashkov E. V., Galanzha E. I., Hennings L., Zharov V. P.. Photothermal multispectral image cytometry for quantitative histology of nanoparticles and micrometastasis in intact, stained and selectively burned tissues. Cytometry A, 2010, 77(11): 1049-1058.

[87] Shashkov E. V., Everts M., Galanzha E. I., Zharov V. P.. Quantum dots as multimodal photoacoustic and photothermal contrast agents. Nano Letters, 2008, 8(11): 3953-3958.

[88] Zharov V. P., Galanzha E. I., Menyaev Y., Tuchin V. V.. In vivo high-speed imaging of individual cells in fast blood flow. Journal of Biomedical Optics, 2006, 11(5): 054034.

[89] Zharov V. P., Galanzha E. I., Shashkov E. V., Khlebtsov N. G., Tuchin V. V.. In vivo photoacoustic flow cytometry for monitoring of circulating single cancer cells and contrast agents. Optics Letters, 2006, 31(24): 3623-3625.

[90] Zharov V. P., Galanzha E. I., Tuchin V. V.. Photothermal flow cytometry in vitro for detection and imaging of individual moving cells. Cytometry A, 2007, 71(4): 191-206.

[91] S. E. Bialkowski, Photothermal spectroscopy methods for chemical analysis. New York: A Wiley-Interscience publication, 1996.

[92] Proskurnin M. A., Volkov M. E.. Mode-mismatched dual-beam differential thermal lensing with optical scheme design optimized using expert estimation for analytical measurements. Applied Spectroscopy, 2008, 62(4): 439-449.

[93] Bialkowski S. E., Gu X., Poston P. E., Powers L. S.. Pulsed-laser excited differential photothermal deflection spectroscopy. Applied Spectroscopy, 1992, 46(9): 1335-1345.

[94] Luk’yanov A. Y., Vladykin G. B., Novikov M. A., Yashin Y. I.. Comparison of the capability limits of some optical detectors for liquid chromatography. Journal of Analytical Chemistry, 1999, 54(7): 633-638.

[95] Roriz P., Ramos A., Santos J., Simões J.. Fiber optic intensity-modulated sensors: a review in biomechanics. Photonic Sensors, 2012, 2(4): 315-330.