The beneficial effects of photobiomodulation (PBM) on cellular function are well characterized, principally deriving from the absorption of red to near-infrared radiation by chromophores such as cytochrome-c-oxidase. However, the effects and underlying mechanisms of PBM on non-mitochondria containing cells, such as red blood cells (RBCs), are relatively unknown. In this review, we evaluate studies that investigated the effects of PBM on RBCs in the peripheral circulation, with particular attention on changes in the structural and functional features of RBC membrane dynamics, as well as the potential implications of PBM as an intervention for pathologies related to RBC dysfunction.
Methods:
A literature review was performed in concordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses protocol, using the following databases: PubMed; Ovid (OvidMedline); Scopus; Web of Science; Google Scholar; Scholar.ru; eLIBRARY.ru; Digital Library: Dissertation; and Russian State Library. Search results included publications in Russian, Ukrainian, and English languages after 1995. Eligible articles included the effects of PBM on RBC membrane morphology and function in the peripheral circulation, used either in isolation or alongside other interventions.
Results:
The majority of articles indicated beneficial changes in RBC structure and function following exposure to PBM, including increased osmotic resistance, normalization of membrane permeability, decreased free radical oxidation and concentration of intermediate products of lipid peroxidation, reduced phospholipase A2 membrane activity, and normalization of the viscoelastic properties of RBCs and erythrocyte deformability index. Most trials had small patient numbers with no long-term follow-up.
Conclusions:
The importance of RBC membrane dysfunction as a potential marker and mechanism for RBC pathologies was highlighted. PBM has shown to have membrane protective effects. Further clinical trials are recommended to provide more evidence PBM therapy to treat RBC-related diseases, which may, at the correct dose, improve RBC stability and deformability in RBC-related pathologies.
Get full access to this article
View all access options for this article.
References
1.
TafurJ, Van WijkEP, Van WijkR, MillsPJ. Biophoton detection and low-intensity light therapy: a potential clinical partnership. Photomed Laser Surg, 2010; 28:23–30.
2.
ShiraniA, St LouisEK. Illuminating rationale and uses for light therapy. J Clin Sleep Med, 2009; 5:155–163.
3.
de FreitasLF, HamblinMR. Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Sel Top Quantum Electron, 2016; 22:7000417.
4.
LiebertA, KiatH. The history of light therapy in hospital physiotherapy and medicine with emphasis on Australia: evolution into novel areas of practice. Physiother Theory Pract, 2021; 37:389–400.
5.
ChungH, DaiT, SharmaSK, HuangYY, CarrollJD, HamblinMR. The nuts and bolts of low-level laser (light) therapy. Ann Biomed Eng, 2012; 40:516–533.
6.
HamblinMR. Mechanisms and mitochondrial redox signaling in photobiomodulation. Photochem Photobiol, 2018; 94:199–212.
7.
LinaresSN, BeltrameT, FerraresiC, GaldinoGAM, CataiAM. Photobiomodulation effect on local hemoglobin concentration assessed by near-infrared spectroscopy in humans. Lasers Med Sci, 2020; 35:641–649.
8.
FernandesAB, de LimaCJ, VillaverdeAGJB, PereiraPC, CarvalhoHC, ZângaroRA. Photobiomodulation: shining light on COVID-19. Photobiomodul Photomed Laser Surg, 2020; 38:395–397.
9.
TomaiuoloG. Biomechanical properties of red blood cells in health and disease towards microfluidics. Biomicrofluidics, 2014; 8:051501.
10.
BurduliN, AleksandrovaO. Clinical and hemorheological efficiency of intravenous laser blood irradiation. Laser Med, 2008; 12:8.
11.
AmirovNB. Permeability of cell membranes, microelement content and microcirculation in combined treatment of CHD. Russ Cardiol J, 2001; 6:18–21.
12.
AmirovNB. Indicators of membrane permeability, microcirculation, function of external respiration and content of microelements in medicament-laser therapy of pneumonia. Ther Arch, 2002; 3:40–43.
13.
BurduliNM, GazdanovaAA. [Laser Doppler fluometry in assessment of endothelium state in patients with coronary heart disease and its correction by intravenous laser irradiation of blood]. Klin Med (Mosk), 2008; 86:44–47.
14.
BurduliNM, GutnovaSK. Effect of intravenous laser irradiation of the blood on plasma content of ceruloplasmin in patients with chronic pancreatitis. Bull Exp Biol Med, 2010; 149:697–698.
15.
BurduliN, GireyevaE. Changes in homocystein levels in blood lipid spectrum, in peroxide lipid oxidation and in endothelial functions in patients with stable angina pectoris on exertion under low-level laser irradiation. Laser Med, 2010; 14:26–30.
16.
BurduliNM, GabuevaAA. [The influence of low-intensity laser radiation on the functional activity of neutrophils in the patients presenting with community-acquired pneumonia]. Vopr Kurortol Fizioter Lech Fiz Kult, 2016; 93:9–12.
17.
BurduliN, CrifaridiA. Disturbance of microcirculation in patients with chronic hepatitis and their correction by low-intensity laser. Herald of New Medical Technologies, 2008; VX:160–162.
18.
GazdanovaA. Influence of laser therapy on the function of endothelia, microcirculation and some hemorheology indicies in patients with stable stenocardia. Vladikavkaz 2009.
19.
KehoevaA. Influence of low-intensive laser radiation on the function of endothelia, microcirculation and some hemoreology indicies in patients with ischemic heart disease with accompanying sugar diabetes of type 2. In: Thesis. 2010; p. 150.
20.
KhomerikiSG, MorozovIA. [A quantitative analysis of the ultrastructures of the blood polymorphonuclear neutrophils in patients with ischemic heart disease after a session of intravenous laser therapy]. Arkh Patol, 1998; 60:24–26.
21.
KondrakovVM, ChuntulVV, DerkachAV, BobyrevIA, KhmelevskaiaTB. [Laser therapy in the treatment of patients with ischemic heart disease in a therapeutic department]. Aviakosm Ekolog Med, 1996; 30:57–58.
22.
SimonenkoVB, SiuchNI, VokuevIA. [Diagnostic implications of changed red cell count in low-intensity laser radiation of blood in elderly patients with coronary heart disease]. Klin Med (Mosk), 2002; 80:31–33.
23.
VakhliaevVD, SmirnovaIE, UchaĭkinaLV, et al.[The effect of transvenous laser therapy on lipid peroxidation function in patients with ischemic heart disease]. Kardiologiia, 1992; 32:43–45.
24.
Vasil'evAP, SenatorovIN, Strel'tsovaNN, GorbunovaTIu. [Clinico-functional efficacy of medicinal and photon stabilization of cell membrane in patients with angina pectoris]. Klin Med (Mosk), 2003; 81:24–27.
25.
Vasil'evAP, SenatorovIN, Strel'tsovaNN, MalishevskiĭMV, DubovaTV, ZykovaEL. [Effect of membrane-stabilizing magnetolaser therapy on cardiodynamics in patients with ischemic heart disease]. Ter Arkh, 2003; 75:19–23.
26.
VasilyevA, StreltsovaN, SekisovaM, DubovaT, ZykovaE. Cell membranes in the realization of the clinical effect of laser radiation in patients with coronary heart disease. Laser Med, 2011; 15:4–9.
27.
AsimovM, RubinovA, BatianA, TrusevichM. Effect of low-intensity laser radiation on thermal denaturing of oxyhemoglobin and hemolysis of human erythrocytes. J Appl Spectrosc, 2013; 80:280–283.
28.
Azbel’DI, ZaparaTA, KuznetsovaIIu, et al.[Changes in the neural activity of the blood serum from patients with ischemic heart disease]. Biull Eksp Biol Med, 1993; 116:161–163.
29.
BaibekovIM, IbragimovAF, BaibekovAI. Effect of laser irradiation of donor blood on erythrocyte shape. Bull Exp Biol Med, 2012; 152:756–759.
30.
EnikeevD, SrubilinD, MyshkinV, IdrisovaL, IsakovI. Antioxidant and laser therapy in correction of functional infriations of erythrocytes at endogenous intoxication of peritoneal genesis. Fundam Res, 2010; 5:26–34.
31.
GeningT, ArslanovaD, AbakumovaT, SvetukhinV, AntoneevaI, GeningS. Morphofunctional state of peripheral blood erythrocytes after femtosecond laser treatment. Clin Med, 2013; 5:58–62.
32.
GizingerOA, MoskvinSV, ZiganshinOR, ShemetovaM. [The effect of continuous low-intensity laser irradiation of the red spectrum on the changes in the functional activity and speed of NADPH-oxidase response of human peripheral blood neutrophils]. Vopr Kurortol Fizioter Lech Fiz Kult, 2016; 93:28–33.
33.
KhomerikiSG, MorozovIA. [Ultrastructural changes of neutrophilic granulocytes in dilated cardiomyopathy and their dynamics after blood irradiation with Helium-Neon laser in vitro]. Arkh Patol, 1998; 60:28–31.
34.
KipshidzeNN, KhomerikiSG, KubatievAA, ShliapnikovVN. [Changes in lectin-induced chemiluminescence of neutrophilic granulocytes after irradiation of blood with helium-neon lasers]. Biull Eksp Biol Med, 1992; 113:24–26.
35.
KujawaJ, ZavodnikL, ZavodnikI, BryszewskaM. Low-intensity near-infrared laser radiation-induced changes of acetylcholinesterase activity of human erythrocytes. J Clin Laser Med Surg, 2003; 21:351–355.
36.
KujawaJ, ZavodnikL, ZavodnikI, BukoV, LapshynaA, BryszewskaM. Effect of low-intensity (3.75–25J/cm2) near-infrared (810nm) laser radiation on red blood cell ATPase activities and membrane structure. J Clin Laser Med Surg, 2004; 22:111–117.
37.
KujawaJ, ZavodnikIB, LapshinaA, LabieniecM, BryszewskaM. Cell survival, DNA, and protein damage in B14 cells under low-intensity near-infrared (810nm) laser irradiation. Photomed Laser Surg, 2004; 22:504–508.
38.
KujawaJ, PasternakK, ZavodnikI, IrzmańskiR, WróbelD, BryszewskaM. The effect of near-infrared MLS laser radiation on cell membrane structure and radical generation. Lasers Med Sci, 2014; 29:1663–1668.
39.
LeeS, McAuliffeDJ, ZhangH, et al.Stress-wave-induced membrane permeation of red blood cells is facilitated by aquaporins. Ultrasound Med Biol, 1997; 23:1089–1094.
40.
LuoG-Y, SunL, LieTC-Y. Aquaporin-1-mediated effects of low level He-Ne laser irradiation on human erythrocytes. Int J Photoenergy, 2012; 2012:5.
41.
LuoGY, SunL, WeiEX, TanX, LiuTC. The effects of low-intensity He-Ne laser irradiation on erythrocyte metabolism. Lasers Med Sci, 2015; 30:2313–2318.
42.
MalinosvkayaS. Influence of low-intensity electromagnetic radiations on the functional activity of biological objects at different levels of organization. Novosibirsk State University & Institute of Chemical Kinetics and Combustion: Novosibirsk. 2008; p. 246.
43.
NemtsevI, LapshinV. On the mechanism of action of low-intensity laser radiation. Questions Balneol Physiother, 1997; 1:1–6.
44.
PasternakK, NowackaO, WróbelD, PieszyńskiI, BryszewskaM, KujawaJ. Influence of MLS laser radiation on erythrocyte membrane fluidity and secondary structure of human serum albumin. Mol Cell Biochem, 2014; 388:261–267.
45.
RadionovB, KogosovY, KonovalovE, KhmelO, GumeniukM. Influence of low intensity laser radiation on blood vessels in the clinic and experiment. Sov Med, 1991; 1:27–29.
46.
SimonianR, SimonianG, SimonianM, SekoianE. Effect of low intensive helium-neon laser on superoxide-producing and methemoglobin-restoring activity of cytochrome b558III of red cell membranes in experiment. Vopr Kurortol Fizioter Lech Fiz Kult, 2007; 4:9–11.
47.
SiposanDG, LukacsA. Effect of low-level laser radiation on some rheological factors in human blood: an in vitro study. J Clin Laser Med Surg, 2000; 18:185–195.
48.
SiposanDG, LukacsA. Relative variation to received dose of some erythrocytic and leukocytic indices of human blood as a result of low-level laser radiation: an in vitro study. J Clin Laser Med Surg, 2001; 19:89–103.
49.
SorokinaL. Investigation of changes in membrane-receptor features of erythrocytes under conditions of photomodifying action of low-intensity laser radiation in bronchial asthma. Moscow: Moscow State Universtiy, 2005.
50.
WangH, LiuW, FangX, et al.Effect of 405nm low intensity irradiation on the absorption spectrum of in-vitro hyperlipidemia blood. Technol Health Care, 2018; 26:135–143.
51.
Pasternak-MnichK, WróbelD, NowackaO, PieszyńskiI, BryszewskaM, KujawaJ. The effect of MLS laser radiation on cell lipid membrane. Ann Agric Environ Med, 2018; 108–113.
52.
DeryuginaAV, IvashchenkoMN, IgnatievPS, BalalaevaIV, SamodelkinAG. Low-level laser therapy as a modifier of erythrocytes morphokinetic parameters in hyperadrenalinemia. Lasers Med Sci, 2019; 34:1603–1612.
53.
VoronovaO, GeningT, AbakumovaT, et al.The effect of picosecond laser pulses on redox-dependent processes in mice red blood cells studied in vivo. In: Optical Interactions with Tissue and Cells; and Terahertz for Biomedical Applications, Volume No. 8941. 2014. International Society for Optics and Photonics, San Francisco, CA.
54.
MillerK, SergeevI. Effect of low intensity red laser irradiation on osmotic resistance and deformability of erythrocytes. Reg Blood Circ Microcirc, 2008; 1:26–30.
55.
MonichV, MalinovskayaS. Influence of a low-intensive red light on a functional state of the rat cardiovascular system and blood at a clinical death simulation. Bull Univ Nizhny Novgorod, 2010; 3:153–157.
56.
MorozV, KirsanovaA, NovoderzhkinaI, et al.Changes in the surface of red blood cell membranes after blood loss and their correction with laser irradiation. Gen Reanimatol, 2010; 6:5.
57.
SrubilinD, EnikeezD, MyshkinV, IsakovaM, IsakovI, IdrisovaL. Influence of antioxidants and laser therapy on the condition of erythrocyte membranes in experimental peritonitis. Med Bull Bashkorotostan, 2009; 4:102–106.
58.
SrubilinD, EnikeezD, IsakovI. The structural-functional damages of erythrocytes and their correction by low intensive laser radiation in subchronic intoxication with dichlorethane. Bull N Med Technol, 2012; 19:105–108.
59.
WalskiT, DrohomireckaA, BujokJ, et al.Low-level light therapy protects red blood cells against oxidative stress and hemolysis during extracorporeal circulation. Front Physiol, 2018; 9:647.
60.
WagshulME, EidePK, MadsenJR. The pulsating brain: a review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS, 2011; 8:5.
61.
DorvalAD. The rhythmic consequences of ion channel stochasticity. Neuroscientist, 2006; 12:442–448.
62.
MohandasN, GallagherPG. Red cell membrane: past, present, and future. Blood, 2008; 112:3939–3948.
63.
HuisjesR, BogdanovaA, van SolingeWW, SchiffelersRM, KaestnerL, van WijkR. Squeezing for life - properties of red blood cell deformability. Front Physiol, 2018; 9:656.
64.
KuhnV, DiederichL, KellerTCS, et al.Red blood cell function and dysfunction: redox regulation, nitric oxide metabolism, anemia. Antioxid Redox Signal, 2017; 26:718–742.
65.
GovN, SafranSA. Red blood cell shape and fluctuations: cytoskeleton confinement and ATP activity. J Biol Phys, 2005; 31:453–464.
MoskvinS, UtzS, SchneiderD, GuskovaO. The efficiency of combined laser therapy in complex treatment of patients with atopic dermatitis. Sarator J Med Sci Res, 2015; 11:396–400.
68.
RheeYH, MoonJH, JungJY, OhC, AhnJC, ChungPS. Effect of photobiomodulation therapy on neuronal injuries by ouabain: the regulation of Na, K-ATPase; Src; and mitogen-activated protein kinase signaling pathway. BMC Neurosci, 2019; 20:19.
69.
GolovynskaI, GolovynskyiS, StepanovYV, StepanovaLI, QuJ, OhulchanskyyTY. Red and near-infrared light evokes Ca. J Photochem Photobiol B, 2021; 214:112088.
70.
ChasisJA, AgreP, MohandasN. Decreased membrane mechanical stability and in vivo loss of surface area reflect spectrin deficiencies in hereditary spherocytosis. J Clin Invest, 1988; 82:617–623.
71.
KarstenE, BreenE, HerbertBR. Red blood cells are dynamic reservoirs of cytokines. Sci Rep, 2018; 8:3101.
72.
OrlovD, KarkoutiK. The pathophysiology and consequences of red blood cell storage. Anaesthesia, 2015; 70Suppl 1:29–37, e29–12.
73.
MohantyJG, NagababuE, RifkindJM. Red blood cell oxidative stress impairs oxygen delivery and induces red blood cell aging. Front Physiol, 2014; 5:84.
74.
MatsumotoJ, StewartT, ShengL, et al.Transmission of α-synuclein-containing erythrocyte-derived extracellular vesicles across the blood-brain barrier via adsorptive mediated transcytosis: another mechanism for initiation and progression of Parkinson's disease?. Acta Neuropathol Commun, 2017; 5:71.
75.
TsudaK. Red blood cell abnormalities and hypertension. Hypertens Res, 2020; 43:72–73.
76.
TsudaK, NishioI. Membrane fluidity and hypertension. Am J Hypertens, 2003; 16:259–261.
77.
TangL, KazanR, TaddeiR, ZaouterC, CyrS, HemmerlingTM. Reduced cerebral oxygen saturation during thoracic surgery predicts early postoperative cognitive dysfunction. Br J Anaesth, 2012; 108:623–629.
78.
KnepperMA. The aquaporin family of molecular water channels. Proc Natl Acad Sci U S A, 1994; 91:6255–6258.
79.
MobasheriA, MarplesD, YoungIS, FloydRV, MoskalukCA, FrigeriA. Distribution of the AQP4 water channel in normal human tissues: protein and tissue microarrays reveal expression in several new anatomical locations, including the prostate gland and seminal vesicles. Channels (Austin), 2007; 1:29–38.
80.
PapadopoulosMC, VerkmanAS. Aquaporin water channels in the nervous system. Nat Rev Neurosci, 2013; 14:265–277.
81.
HoshiA, YamamotoT, ShimizuK, et al.Characteristics of aquaporin expression surrounding senile plaques and cerebral amyloid angiopathy in Alzheimer disease. J Neuropathol Exp Neurol, 2012; 71:750–759.
82.
MisawaT, ArimaK, MizusawaH, SatohJ. Close association of water channel AQP1 with amyloid-beta deposition in Alzheimer disease brains. Acta Neuropathol, 2008; 116:247–260.
83.
BadautJ, LasbennesF, MagistrettiPJ, RegliL. Aquaporins in brain: distribution, physiology, and pathophysiology. J Cereb Blood Flow Metab, 2002; 22:367–378.
