Laser-Induced Fluorescence Spectroscopy in the Diagnosis of Tissue Hypoxia (Review)
https://doi.org/10.15360/1813-9779-2019-6-50-61
Abstract
The aim of review is to discuss the results of studies on diagnosis of tissue hypoxia by laser-induced spectroscopy, as well as to identify promising trends and prospects of this technique for its further application in experimental and clinical medicine.
The review presents the findings of studies of the fluorescence intensity of endogenous fluorophore molecules (reduced nicotinamide adenine dinucleotide, oxidized flavin adenine dinucleotide) as markers of ischemic injury of internal organs (brain, heart, liver, kidneys, etc.). The principles of fluorescence laser-induced spectroscopy in vivo are discussed. The historical aspects of the subject are also covered. The results of the use of the technique in experimental and clinical studies of tissue hypoxia and ischemia are shown. Difficulties in interpreting the intensity values of autofluorescent signal of the studied molecules are revealed. It was noted that the tissue autofluorescence in a long-term anoxia remains unknown, and there are no structured ideas about the impact of exogenous and endogenous factors on autofluorescence intensity.
In conclusion, the use of laser-induced fluorescence spectroscopy to diagnose tissue ischemia is a promising area of experimental and clinical medicine, which still has various unresolved issues, despite a large number of studies in this domain.
Keywords
About the Author
Anastasiya S. BabkinaRussian Federation
25 Petrovka Str., Build. 2, 107031 Moscow;
6 Miklukho-Maсlaya Str., 117198 Moscow
References
1. Abramova E.A., Voennov O.V., Boyarinov G.A., Trofimov А.O. Cerebral Circulation and Metabolism of Patients with Cerebral Injury. Obshchaya reanimatologiya=General Reanimatology. 2018; 14 (1): 4–11. [In Russ.] DOI: 10.15360/1813-9779-2018-1-4-11
2. Ryzhkov I.A., Zarzhetsky Y.V., Novoderzhkina I.S. Comparative Aspects of the Regulation of Cutaneous and Cerebral Microcirculation During Acute Blood Loss. Obshchaya reanimatologiya=General Reanimatology. 2017; 13 (6): 18–27. [In Russ.]. DOI: 10.15360/1813-9779-2017-6-18-27
3. Babkina A.S., Golubev A.M., Sundukov D.V., Bashirova A.R., Golubev M.A. Clozapine: Mechanisms of Toxicity and Side Effects. Obshchaya reanimatologiya=General Reanimatology. 2018; 14 (2): 35–45. [In Russ.] DOI: 10.15360/1813-9779-2018-2-35-45
4. Rogatkin D.A. Physical fundamentals of in vivo laser clinical fluorescence spectroscopy. Meditsinskaya fizika. 2014; 4 (64): 78–96 [In Russ.]
5. Vekshin N. L. fluorescence spectroscopy of polymers. Pushchino: Photon-vek; 2008. [In Russ.] ISBN: 978-5-903789-07-8
6. Monici M. Cell and tissue autofluorescence research and diagnostic applications. Biotechnol. Annu. Rev. 2005; 11: 227–256. PMID: 16216779 DOI: 10.1016/S1387-2656 (05)11007-2
7. Lukina M.M., Shirmanova M.V., Sergeeva T.F., Zagajnova E.V. Metabolic imaging in the study of cancer processes (review). Sovremennye tekhnologii v medicine 2016; 8 (4): 113–128. [In Russ.] DOI: 10.17691/stm2016.8.4.16
8. Danylovych H.V. Evaluation of functioning of mitochondrial electron transport chain with NADH and FAD autofluorescence. Ukr. Biochem. J. 2016; 88 (1): 31–43. PMID: 29227076 DOI: 10.15407/ubj88.01.031
9. Syasin N.I., Borisova O.N. Autofluorescence, cellular respiration and the modern possibilities of its non-invasive research (literature review). Vestnik novyh medicinskih tekhnologij. Elektronnyj zhurnal 2014; 1. [In Russ.] DOI 10.12737/3438
10. Bartolomé F., Abramov A.Y. Measurement of mitochondrial NADH and FAD autofluorescence in live cells. Methods. Mol. Biol. 2015; 1264: 263–720. PMID: 25631020 DOI: 10.1007/978-1-4939-2257-4_23
11. Blacker T.S., Duchen M.R. Investigating mitochondrial redox state using NADH and NADPH autofluorescence. Free Radic. Biol. Med. 2016; 100: 53–65. PMID: 27519271 DOI: 10.1016/j.freeradbiomed.2016.08.010
12. Danylovych H.V. Evaluation of functioning of mitochondrial electron transport chain with NADH and FAD autofluorescence. Ukr. Biochem. J. 2016; 88 (1): 31–43. PMID: 29227076 DOI: 10.15407/ubj88.01.031
13. Croce A.C., Bottiroli G. Autofluorescence Spectroscopy for Monitoring Metabolism in Animal Cells and Tissues. Methods Mol. Biol. 2017; 1560: 15–43. PMID: 28155143 DOI: 10.1007/978-1-4939-6788-9_2
14. Kolenc O.I., Quinn K.P. Evaluating Cell Metabolism Through Autofluorescence Imaging of NAD (P)H and FAD. Antioxid. Redox Signal. 2019; 30 (6): 875–889. PMID: 29268621 DOI: 10.1089/ars.2017.7451
15. Plettenberg H.K., Hoffmann M. Applications of autofluorescence for characterisation of biological systems (biomonitoring). Biomed. Tech. (Berl). 2002; 47 (2): 596–597. PMID: 12465247 DOI: 10.1515/bmte.2002.47.s1b.596
16. Chacko J.V., Eliceiri K.W. Autofluorescence lifetime imaging of cellular metabolism: Sensitivity toward cell density, pH, intracellular, and intercellular heterogeneity. Cytometry A. 2019; 95 (1): 56–69. PMID: 30296355 DOI: 10.1002/cyto.a.23603
17. Schaefer P.M., Kalinina S., Rueck A., von Arnim C.A.F., von Einem B. NADH Autofluorescence-A Marker on its Way to Boost Bioenergetic Research. Cytometry A. 2019; 95 (1): 34–46. PMID: 30211978 DOI: 10.1002/cyto.a.23597
18. Raghushaker C.R., Chandra S., Chakrabarty S., Kabekkodu S.P., Satyamoorthy K., Mahato K.K. Detection of mitochondrial dysfunction in vitro by laser-induced autofluorescence. J. Biophotonics. 2019; 28: e201900056. PMID: 31251452 DOI: 10.1002/jbio.201900056
19. Mayevsky A., Barbiro-Michaely E. Shedding light on mitochondrial function by real time monitoring of NADH fluorescence: I. Basic methodology and animal studies. J. Clin. Monit. Comput. 2013; 27 (1): 1–34. PMID: 23203204 DOI: 10.1007/s10877-012-9414-5
20. Mayevsky A., Rogatsky G.G.. Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies. Am. J. Physiol. Cell Physiol. 2007; 292 (2): 615–640. PMID: 16943239 DOI: 10.1152/ajpcell.00249.2006
21. Heikal A.A. Intracellular coenzymes as natural biomarkers for metabolic activities and mitochondrial anomalies. Biomark. Med. 2010; 4 (2): 241–263. DOI: 10.2217/bmm.10.1
22. Shehada R.E., Marmarelis V.Z., Mansour H.N, Grundfest W.S. Laser induced fluorescence attenuation spectroscopy: detection of hypoxia. IEEE Trans. Biomed. Eng. 2000; 47 (3): 301–312. PMID: 10743771 DOI: 10.1109/10.827290
23. Lu H.H., Wu Y.M., Chang W.T., Luo T., Yang Y.C., Cho H.D., Liau I. Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence. Anal. Chem. 2014; 86 (10): 5024–5031. PMID: 24720791 DOI: 10.1021/ac5006469
24. Hosseini L., Vafaee M.S., Mahmoudi J., Badalzadeh R. Nicotinamide adenine dinucleotide emerges as a therapeutic target in aging and ischemic conditions. Biogerontology. 2019; 20 (4): 381–395. PMID: 30838484 DOI: 10.1007/s10522-019-09805-6
25. Aboumarzouk O., Valentine R., Buist R., Ahmad S., Nabi G., Eljamel S., Moseley H., Kata S.G. Laser-induced autofluorescence spectroscopy: can it be of importance indetection of bladder lesions? Photodiagnosis. Photodyn. Ther. 2015; 12 (1): 76–83. PMID: 25560417 DOI: 10.1016/j.pdpdt.2014.12.003
26. Iga N., Oto T., Okada M., Harada M., Nishikawa H., Miyoshi K., Otani S., Sugimoto S., Yamane M., Toyooka S., Miyoshi S. Detection of airway ischaemic damage after lung transplantation by using autofluorescence imaging bronchoscopy. Eur. J. Cardiothorac. Surg. 2014; 45 (3): 509–513. PMID: 23999558 DOI: 10.1093/ejcts/ezt437
27. Kretschmer S., Pieper M., Hüttmann G., Bölke T., Wollenberg B., Marsh L.M., Garn H., König P. Autofluorescence multiphoton microscopy for visualization of tissue morphology and cellular dynamics in murine and human airways. Lab. Invest. 2016; 96 (8): 918–931. PMID: 27400364 PMCID: PMC4972900 DOI: 10.1038/labinvest.2016.69
28. Chacko J.V., Eliceiri K.W. Autofluorescence lifetime imaging of cellular metabolism: Sensitivity toward cell density, pH, intracellular, and intercellular heterogeneity. Cytometry A. 2019; 95 (1): 56–69. PMID: 30296355 DOI: 10.1002/cyto.a.23603
29. Alam S.R., Wallrabe H., Svindrych Z., Chaudhary A.K., Christopher K.G., Chandra D., Periasamy A. Investigation of Mitochondrial Metabolic Response to Doxorubicin in Prostate Cancer Cells: An NADH, FAD and Tryptophan FLIM Assay. Sci. Rep. 2017; 7 (1): 10451. PMID: 28874842 DOI: 10.1038/s41598-017-10856-3
30. Li B.H., Xie S.S. Autofluorescence excitation-emission matrices for diagnosis of colonic cancer. World J. Gastroenterol. 2005; 11 (25): 3931–3934. PMID: 15991296 DOI: 10.3748/wjg.v11.i25.3931
31. Salmin V.V., Salmina A.B., Fursov A.A., Frolova O.V., Laletin D.I., Fursov M.A., YUdin G.V., Malinovskaya N.A., Zykova L.D., Provorova A.S. The use of fluorescence spectroscopy to assess ischemic myocardial damage. Journal of Siberian Federal University 2011; 2 (4): 142–157 [In Russ.]
32. Fitzgerald J.T., Michalopoulou A., Pivetti C.D., Raman R.N., Troppmann C., Demos S.G. Real-time assessment of in vivo renal ischemia using laser autofluorescence imaging. J. Biomed. Opt. 2005; 10 (4): 44018. PMID: 16178651 DOI: 10.1117/1.1993327
33. Tirapelli L.F., Bagnato V.S., Tirapelli D.P., Kurachi C., Barione D.F., Tucci S. Jr., Suaid H.J., Cologna A.J, Martins A.C. Renal ischemia in rats: mitochondria function and laser autofluorescence. Transplant. Proc. 2008; 40 (5): 1679–1684. PMID: 18589172 DOI: 10.1016/j.transproceed.2008.02.081
34. Tirapelli L.F., Trazzi B.F., Bagnato V.S., Tirapelli D.P, Kurachi C., da Costa M.M., Tucci S. Jr., Cologna A.J., Martins A.C. Histopathology and laser autofluorescence of ischemic kidneys of rats. Lasers Med. Sci. 2009; 24 (3): 397–404. PMID: 18581159 DOI: 10.1007/s10103-008-0578-74
35. Raman R.N., Pivetti C.D., Ramsamooj R., Troppmann C., Demos S.G. Predictive assessment of kidney functional recovery following ischemic injury using optical spectroscopy. J. Biomed. Opt. 2017; 22 (5): 56001. PMID: 28467536 DOI: 10.1117/1.JBO.22.5.056001
36. Croce A.C., Ferrigno A., Bottiroli G., Vairetti M. Autofluorescencebased optical biopsy: An effective diagnostic tool in hepatology. Liver Int. 2018; 38 (7): 1160–1174. PMID: 29624848 DOI: 10.1111/liv.13753
37. Nazeer S.S., Saraswathy A., Shenoy S.J., Jayasree R.S. Fluorescence spectroscopy as an efficient tool for staging the degree of liver fibrosis: an in vivo comparison with MRI. Sci. Rep. 2018; 8 (1): 10967. PMID: 30030510 DOI: 10.1038/s41598-018-29370-1
38. La Cour M.F., Mehrvar S., Kim J., Martin A., Zimmerman M.A., Hong J.C., Ranji M. Optical imaging for the assessment of hepatocyte metabolic state in ischemia and reperfusion injuries. Biomed. Opt. Express. 2017; 8 (10): 4419–4426. PMID: 29082074 DOI: 10.1364/BOE.8.004419
39. Croce A.C., Ferrigno A., Santin G., Piccolini V.M., Bottiroli G., Vairetti M. Autofluorescence of liver tissue and bile: organ functionality monitoring during ischemia and reoxygenation. Lasers Surg. Med. 2014; 46 (5): 412–421. PMID: 24619664 DOI: 10.1002/lsm.22241
40. Arutyunyan A.V., Cherdancev D.V., Salmin V.V., Skomorokha D.P., Salmina A.B. Intraoperative laser-induced fluorescence spectroscopy in experimental pancreatitis. Sibirskoe medicinskoe obozrenie 2012; 77 (5): 20–24 [In Russ.]
41. Smelt M.J., Faas M.M., de Haan B.J., de Vos P. Pancreatic beta-cell purification by altering FAD and NAD (P)H metabolism. Exp. Diabetes Res. 2008; 2008: 165360. PMID: 18670618 DOI: 10.1155/2008/165360
42. Shinkin M.V., Zvenigorodskaya L.A., Mkrtumyan A.M. Laser Doppler flowmetry and fluorescence spectroscopy as methods for assessing the preclinical manifestations of diabetic foot syndrome. Effektivnaya farmakoterapiya 2018; 18: 6–12 [In Russ.]
43. Staniszewski K., Audi S.H., Sepehr R., Jacobs E.R., Ranji M. Surface fluorescence studies of tissue mitochondrial redox state in isolated perfused rat lungs. Ann Biomed Eng. 2013 Apr; 41 (4): 827–836. PMID: 23238793 PMCID: PMC3606690 DOI: 10.1007/s10439-012-0716-z
44. Kosterin P., Kim G.H., Muschol M., Obaid A.L., Salzberg B.M. Changes in FAD and NADH fluorescence in neurosecretory terminals are triggered by calcium entry and by ADP production. J. Membr. Biol. 2005; 208 (2): 113–124. PMID: 16645741 DOI: 10.1007/s00232-005-0824-x
45. Reinert K.C., Dunbar R.L., Gao W., Chen G., Ebner T.J. Flavoprotein autofluorescence imaging of neuronal activation in the cerebellar cortex in vivo. J. Neurophysiol. 2004; 92 (1): 199–211. PMID: 14985415 DOI: 10.1152/jn.01275.2003
46. Mayevsky A. Brain NADH redox state monitored in vivo by fiber optic surface fluorometry. Brain Res. 1984; 319 (1): 49–68. PMID: 6370376 DOI: 10.1016/0165-0173 (84)90029-8
47. Salmina A.B., Salmin V.V., Frolova O.V., Laletin D.I., Fursov M.A., Skomoroha D.P., Fursov A.A., Kondrashov M.A., Medvedeva N.N., Malinovskaya N.A., Mantorova N.S. Laser-induced autofluorescence to evaluate brain metabolism and hemodynamics. Klinicheskaya nevrologiya 2011; 5 (3): 32–38 [In Russ.]
48. Yaseen M.A., Srinivasan V.J., Gorczynska I., Fujimoto J.G., Boas D.A., Sakadžić S. Multimodal optical imaging system for in vivo investigation of cerebral oxygen delivery and energy metabolism. Biomed Opt. Express. 2015; 6 (12): 4994–5007. PMID: 26713212 DOI: 10.1364/BOE.6.004994
49. Ivanov A., Zilberter Y. Critical state of energy metabolism in brain slices: the principal role of oxygen delivery and energy substrates in shaping neuronal activity. Front Neuroenergetics. 2011; 3: 9. PMID: 22232599 DOI: 10.3389/fnene.2011.00009
50. Yaseen M.A., Sakadžić S., Wu W., Becker W., Kasischke K.A., Boas D.A. In vivo imaging of cerebral energy metabolism with two-photon fluorescence lifetime microscopy of NADH. Biomed Opt. Express. 2013; 4 (2): 307–321. PMID: 23412419 DOI: 10.1364/BOE.4.000307
51. Ten V., Galkin A. Mechanism of mitochondrial complex I damage in brain ischemia/reperfusion injury. A hypothesis. Mol. Cell Neurosci. 2019; 100: 103408. PMID: 31494262 DOI: 10.1016/j.mcn.2019.103408
52. Sahni P.V., Zhang J., Sosunov S., Galkin A., Niatsetskaya Z., Starkov A., Brookes P.S., Ten V.S. Krebs cycle metabolites and preferential succinate oxidation following neonatal hypoxic-ischemic brain injury in mice. Pediatr. Res. 2018; 83 (2): 491–497. PMID: 29211056 DOI: 10.1038/pr.2017.277
53. Stuntz E., Gong Y., Sood D., Liaudanskaya V., Pouli D., Quinn K.P., Alonzo C., Liu Z., Kaplan D.L., Georgakoudi I. Endogenous Two-Photon Excited Fluorescence Imaging Characterizes Neuron and Astrocyte Metabolic Responses to Manganese. Toxicity. Sci. Rep. 2017; 7 (1): 1041. PMID: 28432298 DOI: 10.1038/s41598-017-01015-9
54. Yanagawa Y., Osanai H., Tateno T.. Transcranial flavoprotein-autofluorescence imaging of sound-evoked responses in the mouse auditory cortex under three types of anesthesia. Neurosci. Lett. 2016; 633: 189–195. PMID: 27641319 DOI: 10.1016/j.neulet.2016.09.021
55. Yaseen M.A., Sutin J., Wu W., Fu B., Uhlirova H., Devor A., Boas DюA., Sakadžić S. Fluorescence lifetime microscopy of NADH distinguishes alterations in cerebral metabolism in vivo. Biomed. Opt. Express. 2017; 8 (5): 2368–2385. PMID: 28663879 DOI: 10.1364/BOE.8.002368
56. Kahraman S., Fiskum G. Anoxia-induced changes in pyridine nucleotide redox state in cortical neurons and astrocytes. Neurochem. Res. 2007; 32 (4–5): 799–806. PMID: 17191134 DOI: 10.1007/s11064-006-9206-8
57. Polesskaya O., Sun A., Salahura G., Silva J.N., Dewhurst S., Kasischke K. Detection of microregional hypoxia in mouse cerebral cortex by two-photon imaging of endogenous NADH fluorescence. J. Vis. Exp. 2012; (60). pii: 3466. DOI: 10.3791/3466
58. Shi L., Lu L., Harvey G., Harvey T., Rodríguez-Contreras A., Alfano R.R. Label-free fluorescence spectroscopy for detecting key biomolecules in brain tissue from a mouse model of Alzheimer’s disease. Sci. Rep. 2017; 7 (1): 2599. DOI: 10.1038/s41598-017-02673-5
59. Pascu A., Romanitan M.O., Delgado J.M., Danaila L., Pascu M.L. Laser-induced autofluorescence measurements on brain tissues. Anat. Rec. (Hoboken). 2009; 292 (12): 2013–2022. PMID: 19943354 DOI: 10.1002/ar.21034
60. Zhu M., Chang W., Jing L., Fan Y., Liang P., Zhang X., Wang G., Liao H. Dual-modality optical diagnosis for precise in vivo identification of tumors in neurosurgery. Theranostics. 2019; 9 (10): 2827–2842. PMID: 31244926 DOI: 10.7150/thno.33823
61. Ibrahim B.A., Wang H., Lesicko A.M.H., Bucci B., Paul K., Llano D.A. Effect of temperature on FAD and NADH-derived signals and neurometabolic coupling in the mouse auditory and motor cortex. Pflugers. Arch. 2017 Dec.; 469 (12): 1631–1649. PMID: 28785802 DOI: 10.1007/s00424-017-2037-4
62. Reinert K.C., Gao W., Chen G., Ebner T.J. Flavoprotein autofluorescence imaging in the cerebellar cortex in vivo. J. Neurosci Res. 2007; 85 (15): 3221–3232. PMID: 17520745 DOI: 10.1002/jnr.21348
63. Huang Q., Sun M., Li M., Zhang D., Han F., Wu J.C., Fukunaga K., Chen Z., Qin Z.H. Combination of NAD+ and NADPH Offers Greater Neuroprotection in Ischemic Stroke Models by Relieving Metabolic Stress. Mol. Neurobiol. 2018; 55 (7): 6063-6075 PMID: 29164394 DOI: 10.1007/s12035-017-0809-7
64. Papayan G., Petrishchev N., Galagudza M.. Autofluorescence spectroscopy for NADH and flavoproteins redox state monitoring in the isolated rat heart subjected to ischemia-reperfusion. Photodiagnosis Photodyn. Ther. 2014; 11 (3): 400–408. PMID: 24854770 DOI: 10.1016/j.pdpdt.2014.05.003
65. Lagarto J.L, Dyer B.T, Peters N.S., French P.M.W, Dunsby C., Lyon A.R. In vivo label-free optical monitoring of structural and metabolic remodeling of myocardium following infarction. Biomed. Opt. Express. 2019; 10 (7): 3506–3521. DOI: 10.1364/BOE.10.003506
66. Lagarto J.L., Dyer B.T., Talbot C.B., Peters N.S., French P.M.W., Lyon A.R., Dunsby C. Characterization of NAD (P)H and FAD autofluorescence signatures in a Langendorff isolated-perfused rat heart model. Biomed Opt. Express. 2018; 9 (10): 4961–4978. DOI: 10.1364/BOE.9.004961
67. Lagarto J., Dyer B.T., Talbot C., Sikkel M.B., Peters N.S., French P.M., Lyon A.R., Dunsby C. Application of time-resolved autofluorescence to label-free in vivo optical mapping of changes in tissue matrix and metabolism associated with myocardial infarction and heart failure. Biomed. Opt. Express. 2015; 6 (2): 324–346. PMID: 25780727 DOI: 10.1364/BOE.6.000324
68. Yamani M.H., van de Poll S.W., Ratliff N.B., Kuban B.E., Starling R.C., McCarthy P.M., Young J.B. Fluorescence spectroscopy of endomyocardial tissue post-human heart transplantation: does it correlate with histopathology? J. Heart Lung Transplant. 2000; 19 (11): 1077–1080. DOI: 10.1016/s1053-2498 (00)00161-3
69. Horvath K.A., Schomacker K.T., Lee C.C., Cohn L.H. Intraoperative myocardial ischemia detection with laser-induced fluorescence. J. Thorac. Cardiovasc. Surg. 1994; 107 (1): 220–225. PMID: 8283889
70. Aldakkak M., Stowe D.F., Lesnefsky E.J., Heisner J.S., Chen Q., Camara A.K. Modulation of mitochondrial bioenergetics in the isolated Guinea pig beating heart by potassium and lidocaine cardioplegia: implications for cardioprotection. J. Cardiovasc. Pharmacol. 2009; 54 (4): 298–309. DOI: 10.1097/FJC.0b013e3181b2b842
71. Ranji M., Motlagh M.M., Salehpour F., Sepehr R., Heisner J.S., Dash R.K., Camara A.K. Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion. IEEE J. Transl. Eng. Health Med. 2016; 4: 1800210. PMID: 27574574 DOI: 10.1109/JTEHM.2016.2570219
72. Wengrowski A.M., Kuzmiak-Glancy S., Jaimes R., Kay M.W. NADH changes during hypoxia, ischemia, and increased work differ between isolated heart preparations. Am. J. Physiol. Heart Circ. Physiol. 2014; 306 (4): H529–537. PMID: 24337462 DOI: 10.1152/ajpheart.00696.2013
73. Taylor D., Bhandari S., Seymour A.M. Mitochondrial dysfunction in uremic cardiomyopathy. Am. J. Physiol. Renal Physiol. 2015; 308 (6): F579-87. DOI: 10.1152/ajprenal.00442.2014
74. La Cour M.F., Mehrvar S., Heisner J.S, Motlagh M.M., Medhora M., Ranji M., Camara AKS. Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury. J. Biomed. Opt. 2018; 23 (1): 1–9. DOI: 10.1117/1.JBO.23.1.016011
75. Stowe D.F., Gadicherla A.K., Zhou Y., Aldakkak M., Cheng Q., Kwok W.M., Jiang M.T., Heisner J.S., Yang M., Camara A.K. Protection against cardiac injury by small Ca (2+)-sensitive K (+) channels identified in guinea pig cardiac inner mitochondrial membrane. Biochim. Biophys. Acta. 2013; 1828 (2): 427–442. DOI: 10.1016/j.bbamem.2012.08.031
76. Wüst R.C., Helmes M., Stienen G.J. Rapid changes in NADH and flavin autofluorescence in rat cardiac trabeculae reveal large mitochondrial complex II reserve capacity. J. Physiol. 2015; 593 (8): 1829–1840. PMID: 25640645 DOI: 10.1113/jphysiol.2014.286153
77. Xu Z.H., Zhang Z.X., Wang J., Li Z., Liu X.L. Research on the autofluorescence spectroscopy of heart tissues. Guang Pu Xue Yu Guang Pu Fen Xi. 2009; 29 (6): 1651–1655. PMID: 19810552
78. Murphy T.H. Two-Photon Imaging of Neuronal Structural Plasticity in Mice during and after Ischemia. Cold Spring Harb. Protoc. 2015; 2015 (6): 548–557. PMID: 26034310 DOI: 10.1101/pdb.prot087486
79. Hershberger K.A., Martin A.S., Hirschey M.D. Role of NAD+ and mitochondrial sirtuins in cardiac and renal diseases. Nat. Rev. Nephrol. 2017; 13 (4): 213–225. PMID: 28163307 DOI: 10.1038/nrneph.2017.5
80. Akbar N., Sokolovski S., Dunaev A., Belch J.J., Rafailov E., Khan F. In vivo noninvasive measurement of skin autofluorescence biomarkers relate to cardiovascular disease in mice. J. Microsc. 2014; 255 (1): 42–48. PMID: 24811729 DOI: 10.1111/jmi.12135
Review
For citations:
Babkina A.S. Laser-Induced Fluorescence Spectroscopy in the Diagnosis of Tissue Hypoxia (Review). General Reanimatology. 2019;15(6):50-61. https://doi.org/10.15360/1813-9779-2019-6-50-61