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Current Bioactive Compounds

Editor-in-Chief

ISSN (Print): 1573-4072
ISSN (Online): 1875-6646

Review Article

Rinsing Chronic Wounds with a Nitric Oxide Containing Solution – A Safe Treatment Approach to Support Wound Healing

Author(s): Thorsten U. Meyer*

Volume 16, Issue 4, 2020

Page: [394 - 406] Pages: 13

DOI: 10.2174/1573407214666181119120027

Price: $65

Abstract

Background: Nitric oxide (NO) is known for decades to play a crucial role in many physiological processes: this includes acting as an anti-microbial mediator/agent, vasodilator, inhibitor of platelet aggregation, immune modulator, and tissue regeneration via regulation of epidermal cell migration, collagen deposition and cytokine/chemokine microenvironment, making it a key player in wound healing.

Methods: In order to demonstrate the therapeutic benefits as well as the safety of a NO wound irrigation solution, a broad literature review summarizing efficacy and safety data was conducted.

Results: Beneficial effects on wound healing have been demonstrated in several non-clinical and clinical studies. The combination of NO and wound rinsing seems to be a promising approach in terms of improved wound healing of chronic wounds.

Conclusion: Based on the results, no safety concerns are expected for a daily 15 minutes use of a NOgenerating rinsing solution system for wound irrigation of diabetic foot ulcers in adults.

Keywords: Nitric oxide, chronic wound, treatment, efficacy, toxicity, diabetic foot ulcer.

Graphical Abstract
[1]
Seabra, B.A.; Duran, N. Nanotechnology allied to nitric oxide release materials for dermatological applications. Curr. Nanosci., 2012, 8(4), 520-525.
[http://dx.doi.org/10.2174/157341312801784159]
[2]
Halpenny, M.G.; Mascharak, K.P. Emerging antimicrobial applications of Nitric Oxide (NO) and NO-releasing materials. Antiinfect. Agents Med. Chem., 2010, 9(4), 187-197.
[http://dx.doi.org/10.2174/187152110794785086]
[3]
Korhonen, R.; Lahti, A.; Kankaanranta, H.; Moilanen, E. Nitric oxide production and signaling in inflammation. Curr. Drug Targets Inflamm. Allergy, 2005, 4(4), 471-479.
[http://dx.doi.org/10.2174/1568010054526359] [PMID: 16101524]
[4]
Kovacic, P.; Somanathan, R. Nitric oxide, peroxynitrite, peroxynitrous acid, nitroxyl, nitrogen dioxide, nitrous oxide: Biochemical mechanisms and bioaction. Curr. Bioact. Compd., 2012, 8(4), 297-306.
[http://dx.doi.org/10.2174/1573407211208040001]
[5]
Pol, O. The involvement of the nitric oxide in the effects and expression of opioid receptors during peripheral inflammation. Curr. Med. Chem., 2007, 14(18), 1945-1955.
[http://dx.doi.org/10.2174/092986707781368469] [PMID: 17691937]
[6]
Blecher, K.; Martinez, L.R.; Tuckman-Vernon, C.; Nacharaju, P.; Schairer, D.; Chouake, J.; Friedman, J.M.; Alfieri, A.; Guha, C.; Nosanchuk, J.D.; Friedman, A.J. Nitric oxide-releasing nanoparticles accelerate wound healing in NOD-SCID mice. Nanomedicine (Lond.), 2012, 8(8), 1364-1371.
[http://dx.doi.org/10.1016/j.nano.2012.02.014] [PMID: 22406184]
[7]
Miller, C.C.; Miller, M.K.; Ghaffari, A.; Kunimoto, B. Treatment of chronic nonhealing leg ulceration with gaseous nitric oxide: A case study. J. Cutan. Med. Surg., 2004, 8(4), 233-238.
[http://dx.doi.org/10.1177/120347540400800406] [PMID: 16092001]
[8]
SmPC_NaNO2, Sodium nitrite: Summary of product charac-teris-tics Hope Pharmaceuticals Ltd,. www.medicines.org.uk/emc/product/7353/smpc [Accessed August 14, 2015].
[9]
Nguyen, K.T.; Wu, Z.; Huang, T.; Tay, C.Y. Molecular design and medicinal applications of nano-nitric oxide delivery systems. Curr. Med. Chem., 2018, 25(12), 1420-1432.
[http://dx.doi.org/10.2174/0929867324666170407141222] [PMID: 28403790]
[10]
Minniti, C.P.; Gorbach, A.M.; Xu, D.; Hon, Y.Y.; Delaney, K.M.; Seidel, M.; Malik, N.; Peters-Lawrence, M.; Cantilena, C.; Nichols, J.S.; Mendelsohn, L.; Conrey, A.; Grimes, G.; Kato, G.J. Topical sodium nitrite for chronic leg ulcers in patients with sickle cell anaemia: A phase 1 dose-finding safety and tolerability trial. Lancet Haematol., 2014, 1(3), e95-e103.
[http://dx.doi.org/10.1016/S2352-3026(14)00019-2] [PMID: 25938131]
[11]
Opländer, C.; Römer, A.; Paunel-Görgülü, A.; Fritsch, T.; van Faassen, E.E.; Mürtz, M.; Bozkurt, A.; Grieb, G.; Fuchs, P.; Pallua, N.; Suschek, C.V. Dermal application of nitric oxide in vivo: kinetics, biological responses, and therapeutic potential in humans. Clin. Pharmacol. Ther., 2012, 91(6), 1074-1082.
[http://dx.doi.org/10.1038/clpt.2011.366] [PMID: 22549282]
[12]
Vercelino, R.; Cunha, T.M.; Ferreira, E.S.; Cunha, F.Q.; Ferreira, S.H.; de Oliveira, M.G. Skin vasodilation and analgesic effect of a topical nitric oxide-releasing hydrogel. J. Mater. Sci. Mater. Med., 2013, 24(9), 2157-2169.
[http://dx.doi.org/10.1007/s10856-013-4973-7] [PMID: 23756965]
[13]
Yoon, S.S.; Coakley, R.; Lau, G.W.; Lymar, S.V.; Gaston, B.; Karabulut, A.C.; Hennigan, R.F.; Hwang, S.H.; Buettner, G.; Schurr, M.J.; Mortensen, J.E.; Burns, J.L.; Speert, D.; Boucher, R.C.; Hassett, D.J. Anaerobic killing of mucoid Pseudomonas aeruginosa by acidified nitrite derivatives under cystic fibrosis airway conditions. J. Clin. Invest., 2006, 116(2), 436-446.
[http://dx.doi.org/10.1172/JCI24684] [PMID: 16440061]
[14]
Hetrick, E.M.; Shin, J.H.; Paul, H.S.; Schoenfisch, M.H. Anti-biofilm efficacy of nitric oxide-releasing silica nanoparticles. Biomaterials, 2009, 30(14), 2782-2789.
[http://dx.doi.org/10.1016/j.biomaterials.2009.01.052] [PMID: 19233464]
[15]
Martinez, L.R.; Han, G.; Chacko, M.; Mihu, M.R.; Jacobson, M.; Gialanella, P.; Friedman, A.J.; Nosanchuk, J.D.; Friedman, J.M. Antimicrobial and healing efficacy of sustained release nitric oxide nanoparticles against Staphylococcus aureus skin infection. J. Invest. Dermatol., 2009, 129(10), 2463-2469.
[http://dx.doi.org/10.1038/jid.2009.95] [PMID: 19387479]
[16]
Nurhasni, H.; Cao, J.; Choi, M.; Kim, I.; Lee, B.L.; Jung, Y.; Yoo, J.W. Nitric oxide-releasing poly(lactic-co-glycolic acid)-polyethylenimine nanoparticles for prolonged nitric oxide release, antibacterial efficacy, and in vivo wound healing activity. Int. J. Nanomedicine, 2015, 10, 3065-3080.
[PMID: 25960648]
[17]
Hardwick, J.B.; Tucker, A.T.; Wilks, M.; Johnston, A.; Benjamin, N. A novel method for the delivery of nitric oxide therapy to the skin of human subjects using a semi-permeable membrane. Clin. Sci. (Lond.), 2001, 100(4), 395-400.
[http://dx.doi.org/10.1042/cs1000395] [PMID: 11256977]
[18]
Nablo, B.J.; Rothrock, A.R.; Schoenfisch, M.H. Nitric oxide-releasing sol-gels as antibacterial coatings for orthopedic implants. Biomaterials, 2005, 26(8), 917-924.
[http://dx.doi.org/10.1016/j.biomaterials.2004.03.031] [PMID: 15353203]
[19]
Nablo, B.J.; Schoenfisch, M.H. Poly(vinyl chloride)-coated sol-gels for studying the effects of nitric oxide release on bacterial adhesion. Biomacromolecules, 2004, 5(5), 2034-2041.
[http://dx.doi.org/10.1021/bm049727w] [PMID: 15360321]
[20]
Pegalajar-Jurado, A.; Wold, K. A.; Joslin, J. M.; Neufeld, B. H.; Arabea, K. A.; Suazo, L. A.; McDaniel, S. L.; Bowen, R. A.; Reynolds, M. M. Reprint of: Nitric oxide-releasing polysaccharide derivative exhibits 8-log reduction against Escherichia coli, Acinetobac-ter baumannii and Staphylococcus aureus. J. Cont. Rel., 2015, 220(Pt B), 617-623.
[21]
Sundaram, J.; Pant, J.; Goudie, M.J.; Mani, S.; Handa, H. Antimicrobial and physicochemical characterization of biodegradable, nitric oxide-releasing nanocellulose-chitosan packaging membranes. J. Agric. Food Chem., 2016, 64(25), 5260-5266.
[http://dx.doi.org/10.1021/acs.jafc.6b01936] [PMID: 27258235]
[22]
Study_40029837 Evaluation of the antimicrobial activity of NO solution generated by the CURASUL® NO System; Study condcuted by BSN medical GmbH; JB1 40029837 000 01; Data on file: 2017, 2017.
[23]
Cals-Grierson, M.M.; Ormerod, A.D. Nitric oxide function in the skin. Nitric Oxide, 2004, 10(4), 179-193.
[http://dx.doi.org/10.1016/j.niox.2004.04.005] [PMID: 15275864]
[24]
Ormerod, A.D.; Copeland, P.; Hay, I.; Husain, A.; Ewen, S.W. The inflammatory and cytotoxic effects of a nitric oxide releasing cream on normal skin. J. Invest. Dermatol., 1999, 113(3), 392-397.
[http://dx.doi.org/10.1046/j.1523-1747.1999.00692.x] [PMID: 10469339]
[25]
Weller, R. Nitric oxide: a key mediator in cutaneous physiology. Clin. Exp. Dermatol., 2003, 28(5), 511-514.
[http://dx.doi.org/10.1046/j.1365-2230.2003.01365.x] [PMID: 12950342]
[26]
Frank, S.; Kämpfer, H.; Wetzler, C.; Pfeilschifter, J. Nitric oxide drives skin repair: novel functions of an established mediator. Kidney Int., 2002, 61(3), 882-888.
[http://dx.doi.org/10.1046/j.1523-1755.2002.00237.x] [PMID: 11849442]
[27]
Lee, R.H.; Efron, D.; Tantry, U.; Barbul, A. Nitric oxide in the healing wound: a time-course study. J. Surg. Res., 2001, 101(1), 104-108.
[http://dx.doi.org/10.1006/jsre.2001.6261] [PMID: 11676563]
[28]
Schwentker, A.; Billiar, T.R. Nitric oxide and wound repair. Surg. Clin. North Am., 2003, 83(3), 521-530.
[http://dx.doi.org/10.1016/S0039-6109(02)00207-4] [PMID: 12822723]
[29]
Fukumura, D.; Gohongi, T.; Kadambi, A.; Izumi, Y.; Ang, J.; Yun, C.O.; Buerk, D.G.; Huang, P.L.; Jain, R.K. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. USA, 2001, 98(5), 2604-2609.
[http://dx.doi.org/10.1073/pnas.041359198] [PMID: 11226286]
[30]
Pollock, J.S.; Webb, W.; Callaway, D.; Sathyanarayana, S.; O’Brien, W.; Howdieshell, T.R. Nitric oxide synthase isoform expression in a porcine model of granulation tissue formation. Surgery, 2001, 129(3), 341-350.
[http://dx.doi.org/10.1067/msy.2001.111700] [PMID: 11231463]
[31]
Shi, H.P.; Most, D.; Efron, D.T.; Witte, M.B.; Barbul, A. Supplemental L-arginine enhances wound healing in diabetic rats. Wound Repair Regen., 2003, 11(3), 198-203.
[http://dx.doi.org/10.1046/j.1524-475X.2003.11308.x] [PMID: 12753601]
[32]
Kane, A.J.; Barker, J.E.; Mitchell, G.M.; Theile, D.R.; Romero, R.; Messina, A.; Wagh, M.; Fraulin, F.O.; Morrison, W.A.; Stewart, A.G. Inducible Nitric Oxide Synthase (iNOS) activity promotes ischaemic skin flap survival. Br. J. Pharmacol., 2001, 132(8), 1631-1638.
[http://dx.doi.org/10.1038/sj.bjp.0703944] [PMID: 11309233]
[33]
Most, D.; Efron, D.T.; Shi, H.P.; Tantry, U.S.; Barbul, A. Characterization of incisional wound healing in inducible nitric oxide synthase knockout mice. Surgery, 2002, 132(5), 866-876.
[http://dx.doi.org/10.1067/msy.2002.127422] [PMID: 12464872]
[34]
Yamasaki, K.; Edington, H.D.; McClosky, C.; Tzeng, E.; Lizonova, A.; Kovesdi, I.; Steed, D.L.; Billiar, T.R. Reversal of impaired wound repair in iNOS-deficient mice by topical adenoviral-mediated iNOS gene transfer. J. Clin. Invest., 1998, 101(5), 967-971.
[http://dx.doi.org/10.1172/JCI2067] [PMID: 9486966]
[35]
Stallmeyer, B.; Kämpfer, H.; Kolb, N.; Pfeilschifter, J.; Frank, S. The function of nitric oxide in wound repair: inhibition of inducible nitric oxide-synthase severely impairs wound reepithelialization. J. Invest. Dermatol., 1999, 113(6), 1090-1098.
[http://dx.doi.org/10.1046/j.1523-1747.1999.00784.x] [PMID: 10594757]
[36]
Huszka, M.; Kaplar, M.; Rejto, L.; Tornai, I.; Palatka, K.; Laszlo, P.; Udvardy, M. The association of reduced endothelium derived relaxing factor-NO production with endothelial damage and increased in vivo platelet activation in patients with diabetes mellitus. Thromb. Res., 1997, 86(2), 173-180.
[http://dx.doi.org/10.1016/S0049-3848(97)00060-1] [PMID: 9175238]
[37]
Maejima, K.; Nakano, S.; Himeno, M.; Tsuda, S.; Makiishi, H.; Ito, T.; Nakagawa, A.; Kigoshi, T.; Ishibashi, T.; Nishio, M.; Uchida, K. Increased basal levels of plasma nitric oxide in Type 2 diabetic subjects. Relationship to microvascular complications. J. Diabetes Complications, 2001, 15(3), 135-143.
[http://dx.doi.org/10.1016/S1056-8727(01)00144-1] [PMID: 11358682]
[38]
Efron, D.T.; Most, D.; Barbul, A. Role of nitric oxide in wound healing. Curr. Opin. Clin. Nutr. Metab. Care, 2000, 3(3), 197-204.
[http://dx.doi.org/10.1097/00075197-200005000-00006] [PMID: 10871235]
[39]
Isenberg, J.S.; Ridnour, L.A.; Espey, M.G.; Wink, D.A.; Roberts, D.D. Nitric oxide in wound-healing. Microsurgery, 2005, 25(5), 442-451.
[http://dx.doi.org/10.1002/micr.20168] [PMID: 16044466]
[40]
Nichols, S.P.; Storm, W.L.; Koh, A.; Schoenfisch, M.H. Local delivery of nitric oxide: Targeted delivery of therapeutics to bone and connective tissues. Adv. Drug Deliv. Rev., 2012, 64(12), 1177-1188.
[http://dx.doi.org/10.1016/j.addr.2012.03.002] [PMID: 22433782]
[41]
Laing, T.; Hanson, R.; Chan, F.; Bouchier-Hayes, D. The role of endothelial dysfunction in the pathogenesis of impaired diabetic wound healing: a novel therapeutic target? Med. Hypotheses, 2007, 69(5), 1029-1031.
[http://dx.doi.org/10.1016/j.mehy.2007.02.040] [PMID: 17502127]
[42]
Schäffer, M.; Bongartz, M.; Fischer, S.; Proksch, B.; Viebahn, R. Nitric oxide restores impaired healing in normoglycaemic diabetic rats. J. Wound Care, 2007, 16(7), 311-316.
[http://dx.doi.org/10.12968/jowc.2007.16.7.27057] [PMID: 17708383]
[43]
Mikaili, P.; Moloudizargari, M.; Aghajanshakeri, S. Treatment with topical nitroglycerine may promote the healing process of diabetic foot ulcers. Med. Hypotheses, 2014, 83(2), 172-174.
[http://dx.doi.org/10.1016/j.mehy.2014.05.002] [PMID: 24880867]
[44]
Witte, M.B.; Kiyama, T.; Barbul, A. Nitric oxide enhances experimental wound healing in diabetes. Br. J. Surg., 2002, 89(12), 1594-1601.
[http://dx.doi.org/10.1046/j.1365-2168.2002.02263.x] [PMID: 12445072]
[45]
Suschek, C.V.; Opländer, C.; van Faassen, E.E. Non-enzymatic NO production in human skin: Effect of UVA on cutaneous NO stores. Nitric Oxide, 2010, 22(2), 120-135.
[http://dx.doi.org/10.1016/j.niox.2009.10.006] [PMID: 19879370]
[46]
Opländer, C.; Suschek, C.V. The role of photolabile dermal nitric oxide derivates in Ultraviolet radiation (UVR)-induced cell death. Int. J. Mol. Sci., 2012, 14(1), 191-204.
[http://dx.doi.org/10.3390/ijms14010191] [PMID: 23344028]
[47]
Dessy, C.; Feron, O. Pathophysiological roles of nitric oxide: In the heart and the coronary vasculature. Curr. Med. Chem. Anti Inflamm. Anti Allergy Agents, 2004, 3(3), 207-216.
[http://dx.doi.org/10.2174/1568014043355348]
[48]
EPAR_INOmax, INOmax: EPAR: Scientific Discussion by European Medicines Agency,. www.ema.europa.eu/medicines/human/EPAR/inomax#assessment-history-section [Accessed on 11 Nov 2018].
[49]
Dejam, A.; Hunter, C.J.; Tremonti, C.; Pluta, R.M.; Hon, Y.Y.; Grimes, G.; Partovi, K.; Pelletier, M.M.; Oldfield, E.H.; Cannon, R.O., III; Schechter, A.N.; Gladwin, M.T. Nitrite infusion in humans and nonhuman primates: endocrine effects, pharmacokinetics, and tolerance formation. Circulation, 2007, 116(16), 1821-1831.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.107.712133] [PMID: 17893272]
[50]
Groll-Knapp, E.; Haider, M.; Kienzl, K.; Handler, A.; Trimmel, M. Changes in discrimination learning and brain activity (ERP’s) due to combined exposure to NO and CO in rats. Toxicology, 1988, 49(2-3), 441-447.
[http://dx.doi.org/10.1016/0300-483X(88)90030-3] [PMID: 3376142]
[51]
Opländer, C.; Müller, T.; Baschin, M.; Bozkurt, A.; Grieb, G.; Windolf, J.; Pallua, N.; Suschek, C.V. Characterization of novel nitrite-based nitric oxide generating delivery systems for topical dermal application. Nitric Oxide, 2013, 28, 24-32.
[http://dx.doi.org/10.1016/j.niox.2012.09.003] [PMID: 23036613]
[52]
Opländer, C.; Volkmar, C.M.; Paunel-Görgülü, A.; Fritsch, T.; van Faassen, E.E.; Mürtz, M.; Grieb, G.; Bozkurt, A.; Hemmrich, K.; Windolf, J.; Suschek, C.V. Dermal application of nitric oxide releasing acidified nitrite-containing liniments significantly reduces blood pressure in humans. Nitric Oxide, 2012, 26(2), 132-140.
[http://dx.doi.org/10.1016/j.niox.2012.01.007] [PMID: 22306967]
[53]
Saito, T.; Takeichi, S.; Nakajima, Y.; Yukawa, N.; Osawa, M. Experimental studies of methemoglobinemia due to percutaneous absorption of sodium nitrite. J. Toxicol. Clin. Toxicol., 1997, 35(1), 41-48.
[http://dx.doi.org/10.3109/15563659709001164] [PMID: 9022651]
[54]
BSN_medical In vitro NO skin penetration measurements us-ing human intact skin and Franzkammer technique BSN medical GmbH: inhouse data on file 2015, 2015.
[55]
Oplander, C. Measurement of nitric oxide penetration through human split thickness and full thickness skin; , 2016, p. 7.
[56]
Bos, J.D.; Meinardi, M.M. The 500 Dalton rule for the skin penetration of chemical compounds and drugs. Exp. Dermatol., 2000, 9(3), 165-169.
[http://dx.doi.org/10.1034/j.1600-0625.2000.009003165.x] [PMID: 10839713]
[57]
da Silva, G.; Kennedy, E.M.; Dlugogorski, B.Z. Ab initio procedure for aqueous-phase pKa calculation: The acidity of nitrous acid. J. Phys. Chem. A, 2006, 110(39), 11371-11376.
[http://dx.doi.org/10.1021/jp0639243] [PMID: 17004748]
[58]
Garcia-Saura, M.F.; Fernandez, B.O.; McAllister, B.P.; Whitlock, D.R.; Cruikshank, W.W.; Feelisch, M. Dermal nitrite application enhances global nitric oxide availability: new therapeutic potential for immunomodulation? J. Invest. Dermatol., 2010, 130(2), 608-611.
[http://dx.doi.org/10.1038/jid.2009.303] [PMID: 19812594]
[59]
van Ravenzwaay, B.; Leibold, E. The significance of in vitro rat skin absorption studies to human risk assessment. Toxicol. In Vitro, 2004, 18(2), 219-225.
[http://dx.doi.org/10.1016/j.tiv.2003.08.002] [PMID: 14757113]
[60]
van Ravenzwaay, B.; Leibold, E. A comparison between in vitro rat and human and in vivo rat skin absorption studies. Hum. Exp. Toxicol., 2004, 23(9), 421-430.
[http://dx.doi.org/10.1191/0960327104ht471oa] [PMID: 15497817]
[61]
Eich, R.F.; Li, T.; Lemon, D.D.; Doherty, D.H.; Curry, S.R.; Aitken, J.F.; Mathews, A.J.; Johnson, K.A.; Smith, R.D.; Phillips, G.N., Jr; Olson, J.S. Mechanism of NO-induced oxidation of myoglobin and hemoglobin. Biochemistry, 1996, 35(22), 6976-6983.
[http://dx.doi.org/10.1021/bi960442g] [PMID: 8679521]
[62]
Yoshida, K.; Kasama, K. Biotransformation of nitric oxide. Environ. Health Perspect., 1987, 73, 201-205.
[http://dx.doi.org/10.1289/ehp.8773201] [PMID: 3665863]
[63]
Kelm, M. Nitric oxide metabolism and breakdown. Biochim. Biophys. Acta, 1999, 1411(2-3), 273-289.
[http://dx.doi.org/10.1016/S0005-2728(99)00020-1] [PMID: 10320663]
[64]
Schneider, N.R.; Yeary, R.A. Nitrite and nitrate pharmacokinetics in the dog, sheep, and pony. Am. J. Vet. Res., 1975, 36(7), 941-947.
[PMID: 1147360]
[65]
Gilchrist, M.; Shore, A.C.; Benjamin, N. Inorganic nitrate and nitrite and control of blood pressure. Cardiovasc. Res., 2011, 89(3), 492-498.
[http://dx.doi.org/10.1093/cvr/cvq309] [PMID: 20884639]
[66]
Kim-Shapiro, D.B.; Gladwin, M.T.; Patel, R.P.; Hogg, N. The reaction between nitrite and hemoglobin: the role of nitrite in hemoglobin-mediated hypoxic vasodilation. J. Inorg. Biochem., 2005, 99(1), 237-246.
[http://dx.doi.org/10.1016/j.jinorgbio.2004.10.034] [PMID: 15598504]
[67]
Kim, Y.M.; Lancaster, J.R. Tetrahydrobiopterin-dependent nitrite oxidation to nitrate in isolated rat hepatocytes. FEBS Lett., 1993, 332(3), 255-259.
[http://dx.doi.org/10.1016/0014-5793(93)80644-A] [PMID: 7691663]
[68]
European_Chemicals_Bureau, Sodium nitrite. europa.eu/ [August 14, 2015].
[69]
WHO/JECFA Nitrite. http://www.who.int/foodsafety/publications/ monographs/en/ [Accessed 17 August 2015].
[70]
NTP_Nitrite National Toxicology Program: Technical report on the toxicology and carcinogenesis studies of sodium nitrite (CAS NO. 7632-00-0). https://ntp.niehs.nih.gov/ [Accessed 14 August 2015].
[71]
Arroyo, P.L.; Hatch-Pigott, V.; Mower, H.F.; Cooney, R.V. Mutagenicity of nitric oxide and its inhibition by antioxidants. Mutat. Res., 1992, 281(3), 193-202.
[http://dx.doi.org/10.1016/0165-7992(92)90008-6] [PMID: 1371842]
[72]
Balimandawa, M.; de Meester, C.; Léonard, A. [In vitro study of clastogenic properties of nitrites and nitrates]. C. R. Seances Soc. Biol. Fil., 1993, 187(6), 744-750.
[PMID: 7834497]
[73]
EFSA_Nitrite, Nitrite as undesirable substances in animal feed - Scientific opinion of the panel on contaminants in the food chain. EFSA Journal, 2009, 7(4), 101.
[74]
SmPC_INOmax, Summary of product charcteristics: INOmax 400 ppm mol/mol inhalation gas Linde Healthcare AB. www.ema.europa.eu/medicines/ human/EPAR/inomax [Accessed on 6th August 2015].
[75]
IARC working group on the evaluation of carcinogenic risks to humans.. IARC monographs on the evaluation of carcinogenic risks to humans. Ingested nitrate and nitrite, and cyanobacterial peptide toxins. IARC Monogr. Eval. Carcinog. Risks Hum., 2010, 94(v-vii), 1-412.
[76]
Campbell, M. Evidence on developmental and reproductive toxicity of so-dium nitrite Draft Report. 2000.
[77]
Shimada, T. Lack of teratogenic and mutagenic effects of nitrite on mouse fetuses. Arch. Environ. Health, 1989, 44(1), 59-63.
[http://dx.doi.org/10.1080/00039896.1989.9935874] [PMID: 2916857]
[78]
Fan, A.M.; Steinberg, V.E. Health implications of nitrate and nitrite in drinking water: an update on methemoglobinemia occurrence and reproductive and developmental toxicity. Regul. Toxicol. Pharmacol., 1996, 23(1 Pt 1), 35-43.
[http://dx.doi.org/10.1006/rtph.1996.0006] [PMID: 8628918]
[79]
Nyakas, C.; Buwalda, B.; Kramers, R.J.; Traber, J.; Luiten, P.G. Postnatal development of hippocampal and neocortical cholinergic and serotonergic innervation in rat: effects of nitrite-induced prenatal hypoxia and nimodipine treatment. Neuroscience, 1994, 59(3), 541-559.
[http://dx.doi.org/10.1016/0306-4522(94)90176-7] [PMID: 8008208]
[80]
Roth, A.C.; Herkert, G.E.; Bercz, J.P.; Smith, M.K. Evaluation of the developmental toxicity of sodium nitrite in Long-Evans rats. Fundam. Appl. Toxicol., 1987, 9(4), 668-677.
[http://dx.doi.org/10.1016/0272-0590(87)90173-4] [PMID: 3692023]
[81]
Vorhees, C.V.; Butcher, R.E.; Brunner, R.L.; Wootten, V. Developmental toxicity and psychotoxicity of sodium nitrite in rats. Food Chem. Toxicol., 1984, 22(1), 1-6.
[http://dx.doi.org/10.1016/0278-6915(84)90044-9] [PMID: 6537931]
[82]
Globus, M.; Samuel, D. Effect of maternally administered sodium nitrite on hepatic erythropoiesis in fetal CD-1 mice. Teratology, 1978, 18(3), 367-378.
[http://dx.doi.org/10.1002/tera.1420180311] [PMID: 741389]
[83]
Chapin, R. Reproductive toxicology. Sodium nitrite. Environ. Health Perspect., 1997, 105(Suppl. 1), 345-346.
[PMID: 9114354]
[84]
Ghaffari, A.; Jalili, R.; Ghaffari, M.; Miller, C.; Ghahary, A. Efficacy of gaseous nitric oxide in the treatment of skin and soft tissue infections. Wound Repair Regen., 2007, 15(3), 368-377.
[http://dx.doi.org/10.1111/j.1524-475X.2007.00239.x] [PMID: 17537124]
[85]
Mowbray, M.; Tan, X.; Wheatley, P.S.; Rossi, A.G.; Morris, R.E.; Weller, R.B. Topically applied nitric oxide induces T-lymphocyte infiltration in human skin, but minimal inflammation. J. Invest. Dermatol., 2008, 128(2), 352-360.
[http://dx.doi.org/10.1038/sj.jid.5701096] [PMID: 17914444]
[86]
Nitrite (and potential endogenous formation of N-nitroso com-pounds) WHO Fodd Additives Series, http://www.inchem.org/documents/ jecfa/jecmono/v50je05.htm [Accessed on 11th Nov 2018].
[87]
Pluta, R.M.; Oldfield, E.H.; Bakhtian, K.D.; Fathi, A.R.; Smith, R.K.; Devroom, H.L.; Nahavandi, M.; Woo, S.; Figg, W.D.; Lonser, R.R. Safety and feasibility of long-term intravenous sodium nitrite infusion in healthy volunteers. PLoS One, 2011, 6(1)e14504
[http://dx.doi.org/10.1371/journal.pone.0014504] [PMID: 21249218]
[88]
Bryan, N.S.; Rassaf, T.; Maloney, R.E.; Rodriguez, C.M.; Saijo, F.; Rodriguez, J.R.; Feelisch, M. Cellular targets and mechanisms of nitros(yl)ation: An insight into their nature and kinetics in vivo. Proc. Natl. Acad. Sci. USA, 2004, 101(12), 4308-4313.
[http://dx.doi.org/10.1073/pnas.0306706101] [PMID: 15014175]
[89]
Honda, H.M.; Korge, P.; Weiss, J.N. Mitochondria and ischemia/reperfusion injury. Ann. N. Y. Acad. Sci., 2005, 1047, 248-258.
[http://dx.doi.org/10.1196/annals.1341.022] [PMID: 16093501]
[90]
Sack, M.N. Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance. Cardiovasc. Res., 2006, 72(2), 210-219.
[http://dx.doi.org/10.1016/j.cardiores.2006.07.010] [PMID: 16914124]
[91]
Hall, C.N.; Garthwaite, J. What is the real physiological NO concentration in vivo? Nitric Oxide, 2009, 21(2), 92-103.
[http://dx.doi.org/10.1016/j.niox.2009.07.002] [PMID: 19602444]
[92]
Lauer, T.; Preik, M.; Rassaf, T.; Strauer, B.E.; Deussen, A.; Feelisch, M.; Kelm, M. Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proc. Natl. Acad. Sci. USA, 2001, 98(22), 12814-12819.
[http://dx.doi.org/10.1073/pnas.221381098] [PMID: 11606734]
[93]
Kleinbongard, P.; Dejam, A.; Lauer, T.; Rassaf, T.; Schindler, A.; Picker, O.; Scheeren, T.; Gödecke, A.; Schrader, J.; Schulz, R.; Heusch, G.; Schaub, G.A.; Bryan, N.S.; Feelisch, M.; Kelm, M. Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radic. Biol. Med., 2003, 35(7), 790-796.
[http://dx.doi.org/10.1016/S0891-5849(03)00406-4] [PMID: 14583343]
[94]
Vleeming, W.; van de Kuil, A.; te Biesebeek, J.D.; Meulenbelt, J.; Boink, A.B. Effect of nitrite on blood pressure in anaesthetized and free-moving rats. Food Chem. Toxicol., 1997, 35(6), 615-619.
[http://dx.doi.org/10.1016/S0278-6915(97)00015-X] [PMID: 9225020]
[95]
Miller, C.; McMullin, B.; Ghaffari, A.; Stenzler, A.; Pick, N.; Roscoe, D.; Ghahary, A.; Road, J.; Av-Gay, Y. Gaseous nitric oxide bactericidal activity retained during intermittent high-dose short duration exposure. Nitric Oxide, 2009, 20(1), 16-23.
[http://dx.doi.org/10.1016/j.niox.2008.08.002] [PMID: 18789393]
[96]
Ghaffari, A.; Miller, C.C.; McMullin, B.; Ghahary, A. Potential application of gaseous nitric oxide as a topical antimicrobial agent. Nitric Oxide, 2006, 14(1), 21-29.
[http://dx.doi.org/10.1016/j.niox.2005.08.003] [PMID: 16188471]
[97]
Sulemankhil, I.; Ganopolsky, J.G.; Dieni, C.A.; Dan, A.F.; Jones, M.L.; Prakash, S. Prevention and treatment of virulent bacterial biofilms with an enzymatic nitric oxide-releasing dressing. Antimicrob. Agents Chemother., 2012, 56(12), 6095-6103.
[http://dx.doi.org/10.1128/AAC.01173-12] [PMID: 22948868]
[98]
Lee, W.H.; Ren, H.; Wu, J.; Novak, O.; Brown, R.B.; Xi, C.; Meyerhoff, M.E. Electrochemically modulated nitric oxide release from flexible silicone rubber patch: Antimicrobial activity for potential wound healing applications. ACS Biomater. Sci. Eng., 2016, 2(9), 1432-1435.
[http://dx.doi.org/10.1021/acsbiomaterials.6b00360] [PMID: 27660818]
[99]
Sun, B.; Slomberg, D.L.; Chudasama, S.L.; Lu, Y.; Schoenfisch, M.H. Nitric oxide-releasing dendrimers as antibacterial agents. Biomacromolecules, 2012, 13(10), 3343-3354.
[http://dx.doi.org/10.1021/bm301109c] [PMID: 23013537]

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