Exhaled Nitric Oxide Level in Pharynx Angioedema
Abstract
:1. Introduction
2. Material and Methods
3. Statistical Analysis
4. Results
5. Discussions
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Coleman, J.W. Nitric oxide: A regulator of mast cell activation and mast cell-mediated inflammation. Clin. Exp. Immunol. 2002, 129, 4–10. [Google Scholar] [CrossRef] [PubMed]
- Cinelli, M.A.; Do, H.T.; Miley, G.P.; Silverman, R.B. Inducible nitric oxide synthase: Regulation, structure, and inhibition. Med. Res. Rev. 2020, 40, 158–189. [Google Scholar] [CrossRef] [PubMed]
- Cals-Grierson, M.M.; Ormerod, A.D. Nitric oxide function in the skin. Nitric Oxide-Biol. Chem. 2004, 10, 179–193. [Google Scholar] [CrossRef] [PubMed]
- Claesson-Welsh, L. Vascular permeability—The essentials. Ups. J. Med. Sci. 2015, 120, 135–143. [Google Scholar] [CrossRef] [Green Version]
- Abramson, S.B.; Amin, A.R.; Clancy, R.M.; Attur, M. The role of nitric oxide in tissue destruction. Best Pract. Res. Clin. Rheumatol. 2001, 15, 831–845. [Google Scholar] [CrossRef] [PubMed]
- Kröncke, K.D.; Fehsel, K.; Kolb-Bachofen, V. Inducible nitric oxide synthase in human diseases. Clin. Exp. Immunol. 1998, 113, 147–156. [Google Scholar] [CrossRef]
- Förstermann, U.; Sessa, W.C. Nitric oxide synthases: Regulation and function. Eur. Heart J. 2012, 33, 829. [Google Scholar] [CrossRef] [Green Version]
- Bécherel, P.A.; Chosidow, O.; Le Goff, L.; Francès, C.; Debré, P.; Mossalayi, M.D.; Arock, M. Inducible nitric oxide synthase and proinflammatory cytokine expression by human keratinocytes during acute urticaria. Mol. Med. 1997, 3, 686–694. [Google Scholar] [CrossRef] [Green Version]
- Pinke, K.H.; de Lima, H.G.; Cunha, F.Q.; Lara, V.S. Mast cells phagocyte Candida albicans and produce nitric oxide by mechanisms involving TLR2 and Dectin-1. Immunobiology 2016, 221, 220–227. [Google Scholar] [CrossRef]
- de Lima, H.G.; Pinke, K.H.; Lopes, M.M.R.; Buzalaf, C.P.; Campanelli, A.P.; Lara, V.S. Mast cells exhibit intracellular microbicidal activity against Aggregatibacter actinomycetemcomitans. J. Periodontal Res. 2020, 55, 744–752. [Google Scholar] [CrossRef]
- Park, E.-A.; Han, I.-H.; Kim, J.-H.; Park, S.-J.; Ryu, J.-S.; Ahn, M.-H. Production of Inflammatory Cytokines and Nitric Oxide by Human Mast Cells Incubated with Toxoplasma gondii Lysate. Korean J. Parasitol. 2019, 57, 201. [Google Scholar] [CrossRef] [PubMed]
- Pignatti, P.; Visca, D.; Loukides, S.; Märtson, A.G.; Alffenaar, J.W.C.; Migliori, G.B.; Spanevello, A. A snapshot of exhaled nitric oxide and asthma characteristics: Experience from high to low income countries. Pulmonology 2020, 28, 44–58. [Google Scholar] [CrossRef] [PubMed]
- Galiniak, S.; Rachel, M. Comparison of fractional exhaled nitric oxide in asthmatics with and without allergic rhinitis. Biomarkers 2021, 26, 174–183. [Google Scholar] [CrossRef] [PubMed]
- Rachel, M.; Biesiadecki, M.; Aebisher, D.; Galiniak, S. Exhaled nitric oxide in pediatric patients with respiratory disease. J. Breath Res. 2019, 13, 046007. [Google Scholar] [CrossRef] [PubMed]
- Dinh-Xuan, A.T.; Annesi-Maesano, I.; Berger, P.; Chambellan, A.; Chanez, P.; Chinet, T.; Degano, B.; Delclaux, C.; Demange, V.; Didier, A.; et al. Contribution of exhaled nitric oxide measurement in airway inflammation assessment in asthma. A position paper from the French Speaking Respiratory Society. Rev. Mal. Respir. 2015, 32, 193–215. [Google Scholar] [CrossRef] [PubMed]
- Cameli, P.; Bargagli, E.; Bergantini, L.; D’Alessandro, M.; Pieroni, M.; Fontana, G.A.; Sestini, P.; Refini, R.M. Extended Exhaled Nitric Oxide Analysis in Interstitial Lung Diseases: A Systematic Review. Int. J. Mol. Sci. 2020, 21, 6187. [Google Scholar] [CrossRef]
- Kharitonov, S.A.; Wells, A.U.; O’Connor, B.J.; Cole, P.J.; Hansell, D.M.; Logan- Sinclair, R.B.; Barnes, P.J. Elevated levels of exhaled nitric oxide in bronchiectasis. Am. J. Respir. Crit. Care Med. 1995, 151, 1889–1893. [Google Scholar] [CrossRef]
- Rizzi, M.; Radovanovic, D.; Airoldi, A.; Cristiano, A.; Frassanito, F.; Gaboardi, P.; Saad, M.; Atzeni, F.; Sarzi-Puttini, P.; Santus, P. Rationale underlying the measurement of fractional exhaled nitric oxide in systemic sclerosis patients. Clin. Exp. Rheumatol. 2019, 37 (Suppl. 1), 125–132. [Google Scholar]
- Terrington, D.L.; Hayton, C.; Peel, A.; Fowler, S.J.; Fraser, W.; Wilson, A.M. The role of measuring exhaled breath biomarkers in sarcoidosis: A systematic review. J. Breath Res. 2019, 13, 036015. [Google Scholar] [CrossRef] [Green Version]
- Kasperska-Zajac, A.; Brzoza, Z.; Czecior, E.; Rogala, B.; Polok, A.; Namyslowski, G. Elevated levels of exhaled nitric oxide in recurrent tonsillitis. Eur. Respir. J. 2008, 31, 909–910. [Google Scholar] [CrossRef] [Green Version]
- Damiani, G.; Pacifico, A.; Rizzi, M.; Santus, P.; Bridgewood, C.; Bragazzi, N.L.; Adawi, M.; Watad, A. Patients with psoriatic arthritis have higher levels of FeNO than those with only psoriasis, which may reflect a higher prevalence of a subclinical respiratory involvement. Clin. Rheumatol. 2020, 39, 2981–2988. [Google Scholar] [CrossRef] [PubMed]
- Santus, P.; Rizzi, M.; Radovanovic, D.; Airoldi, A.; Cristiano, A.; Conic, R.; Petrou, S.; Pigatto, P.D.M.; Bragazzi, N.; Colombo, D.; et al. Psoriasis and Respiratory Comorbidities: The Added Value of Fraction of Exhaled Nitric Oxide as a New Method to Detect, Evaluate, and Monitor Psoriatic Systemic Involvement and Therapeutic Efficacy. Biomed Res. Int. 2018, 2018, 3140682. [Google Scholar] [CrossRef] [PubMed]
- Linhares, D.; Jacinto, T.; Pereira, A.M.; Fonseca, J.A. Effects of atopy and rhinitis on exhaled nitric oxide values—A systematic review. Clin. Transl. Allergy 2011, 1, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olin, A.C.; Alving, K.; Torén, K. Exhaled nitric oxide: Relation to sensitization and respiratory symptoms. Clin. Exp. Allergy 2004, 34, 221–226. [Google Scholar] [CrossRef] [PubMed]
- Asero, R.; Madonini, E. Bronchial hyperresponsiveness is a common feature in patients with chronic urticaria. J. Investig. Allergol. Clin. Immunol. 2006, 16, 19–23. [Google Scholar]
- Anania, A.; Striglia, E. Bronchial reactivity in subjects with urticaria. Panminerva Med. 1999, 41, 311–313. [Google Scholar]
- Petalas, K.; Kontou-Fili, K.; Gratziou, C. Bronchial hyperresponsiveness in patients with cholinergic urticaria. Ann. Allergy Asthma Immunol. 2009, 102, 416–421. [Google Scholar] [CrossRef]
- Henz, B.M.; Jeep, S.; Ziegert, F.S.; Niemann, J.; Kunkel, G. Dermal and bronchial hyperreactivity in urticarial dermographism and urticaria factitia. Allergy Eur. J. Allergy Clin. Immunol. 1996, 51, 171–175. [Google Scholar] [CrossRef]
- Demirtürk, M.; Gelincik, A.; Çinar, S.; Kilercik, M.; Onay-Ucar, E.; Çolakoǧlu, B.; Arda, N.; Büyüköztürk, S.; Deniz, G. Increased eNOS levels in hereditary angioedema. Int. Immunopharmacol. 2014, 20, 264–268. [Google Scholar] [CrossRef]
- Chen, W.; Purohit, A.; Barnig, C.; Casset, A.; De Blay, F. Niox® and Niox Mino®: Comparison of exhaled NO in grass pollen allergic adult volunteers. Allergy Eur. J. Allergy Clin. Immunol. 2007, 62, 571–572. [Google Scholar] [CrossRef]
- Rolla, G.; Brussino, L.; Bertero, M.T.; Colagrande, P.; Converso, M.; Bucca, C.; Polizzi, S.; Caligaris-Cappio, F. Increased nitric oxide in exhaled air of patients with systemic lupus erythematosus. J. Rheumatol. 1997, 24, 1066–1071. [Google Scholar] [PubMed]
- Binion, D.G.; Fu, S.; Ramanujam, K.S.; Chai, Y.C.; Dweik, R.A.; Drazba, J.A.; Wade, J.G.; Ziats, N.P.; Erzurum, S.C.; Wilson, K.T. iNOS expression in human intestinal microvascular endothelial cells inhibits leukocyte adhesion. Am. J. Physiol.-Gastrointest. Liver Physiol. 1998, 275, G592–G603. [Google Scholar] [CrossRef] [PubMed]
- Vento, P.; Kiviluoto, T.; Järvinen, H.J.; Soinila, S. Changes in distribution of three isoforms of nitric oxide synthase in ulcerative colitis. Scand. J. Gastroenterol. 2001, 36, 180–189. [Google Scholar] [CrossRef] [PubMed]
- Belmont, H.M.; Levartovsky, D.; Goel, A.; Amin, A.; Giorno, R.; Rediske, J.; Skovron, M.L.; Abramson, S.B. Increased nitric oxide production accompanied by the up-regulation of inducible nitric oxide synthase in vascular endothelium from patients with systemic lupus erythematosus. Arthritis Rheum. 1997, 40, 1810–1816. [Google Scholar] [CrossRef]
- Heemskerk, S.; Masereeuw, R.; Russel, F.G.M.; Pickkers, P. Selective iNOS inhibition for the treatment of sepsis-induced acute kidney injury. Nat. Rev. Nephrol. 2009, 5, 629–640. [Google Scholar] [CrossRef] [PubMed]
- Camuesco, D.; Comalada, M.; Rodríguez-Cabezas, M.E.; Nieto, A.; Lorente, M.D.; Concha, A.; Zarzuelo, A.; Gálvez, J. The intestinal anti-inflammatory effect of quercitrin is associated with an inhibition in iNOS expression. Br. J. Pharmacol. 2004, 143, 908–918. [Google Scholar] [CrossRef] [Green Version]
- Ekmekcioglu, S.; Grimm, E.A.; Roszik, J. Targeting iNOS to increase efficacy of immunotherapies. Hum. Vaccines Immunother. 2017, 13, 1105–1108. [Google Scholar] [CrossRef] [Green Version]
- Taniuchi, S.; Kojima, T.; Hara Mt, K.; Yamamoto, A.; Sasai, M.; Takahashi, H.; Kobayashi, Y. Increased serum nitrate levels in infants with atopic dermatitis. Allergy Eur. J. Allergy Clin. Immunol. 2001, 56, 693–695. [Google Scholar] [CrossRef]
- Ferrara, A.L.; Bova, M.; Petraroli, A.; Veszeli, N.; Galdiero, M.R.; Braile, M.; Marone, G.; Cristinziano, L.; Marcella, S.; Modestino, L.; et al. Hereditary angioedema attack: What happens to vasoactive mediators? Int. Immunopharmacol. 2020, 78, 17–22. [Google Scholar] [CrossRef]
- Kharitonov, S.A.; Barnes, P.J. State of the Art Exhaled Markers of Pulmonary Disease. Am. J. Respir. Crit. Care Med. 2001, 163, 1693–1722. [Google Scholar] [CrossRef] [Green Version]
- Chibana, K.; Trudeau, J.B.; Mustovitch, A.T.; Hu, H.; Zhao, J.; Balzar, S.; Chu, H.W.; Wenzel, S.E. IL-13 induced increases in nitrite levels are primarily driven by increases in inducible nitric oxide synthase as compared with effects on arginases in human primary bronchial epithelial cells. Clin. Exp. Allergy 2008, 38, 936–946. [Google Scholar] [CrossRef] [PubMed]
- Ferrer, M.; Luquin, E.; Sanchez-Ibarrola, A.; Moreno, C.; Sanz, M.L.; Kaplan, A.P. Secretion of cytokines, histamine and leukotrienes in chronic urticaria. Int. Arch. Allergy Immunol. 2002, 129, 254–260. [Google Scholar] [CrossRef] [PubMed]
- Bae, Y.; Izuhara, K.; Ohta, S.; Ono, J.; Hong, G.U.; Ro, J.Y.; Park, G.H.; Choi, J.H. Periostin and Interleukin-13 Are Independently Related to Chronic Spontaneous Urticaria. Allergy. Asthma Immunol. Res. 2016, 8, 457–460. [Google Scholar] [CrossRef] [PubMed]
- Toubi, E.; Vadasz, Z. The Emerging Role of IL-17 in the Immune-Pathogenesis of Chronic Spontaneous Urticaria. ImmunoTargets Ther. 2020, 9, 217–223. [Google Scholar] [CrossRef] [PubMed]
- Kasperska-Zajac, A.; Brzoza, Z.; Rogala, B. Plasma concentration of interleukin 6 (IL-6), and its relationship with circulating concentration of dehydroepiandrosterone sulfate (DHEA-S) in patients with chronic idiopathic urticaria. Cytokine 2007, 39, 142–146. [Google Scholar] [CrossRef]
- Zheng, R.; Qian, L.; Yu, J.; Li, M.; Qian, Q. Analysis of the changes in Th9 cells and related cytokines in the peripheral blood of spontaneous urticaria patients. Biomed. Rep. 2017, 6, 633–639. [Google Scholar] [CrossRef] [Green Version]
- Kocatürk, E.; Maurer, M.; Metz, M.; Grattan, C. Looking forward to new targeted treatments for chronic spontaneous urticaria. Clin. Transl. Allergy 2017, 7, 1. [Google Scholar] [CrossRef] [Green Version]
- Axelrod, D.; Bielory, L. Fexofenadine hydrochloride in the treatment of allergic disease: A review. J. Asthma Allergy 2008, 1, 19–29. [Google Scholar]
- Zheng, D.; Yang, X. Clinical observation on the therapeutic effect of desloratadine citrate disodium in the treatment of chronic urticaria and changes in IL4, IL18, IL23 and IL-33 levels before and after treatment. Pak. J. Pharm. Sci. 2017, 30, 1139–1142. [Google Scholar]
- Matsumoto, A.; Ogura, K.; Hirata, Y.; Kakoki, M.; Watanabe, F.; Takenaka, K.; Shiratori, Y.; Momomura, S.I.; Omata, M. Increased nitric oxide in the exhaled air of patients with decompensated liver cirrhosis. Ann. Intern. Med. 1995, 123, 110–113. [Google Scholar] [CrossRef]
- Änggård, E. Nitric oxide: Mediator, murderer, and medicine. Lancet 1994, 343, 1199–1206. [Google Scholar] [CrossRef]
- Húgman, M.; Holmkvist, T.; Wegener, T.; Emtner, M.; Andersson, M.; Hedenstrúm, H.; Meriløinen, P. Extended NO analysis applied to patients with COPD, allergic asthma and allergic rhinitis. Respir. Med. 2002, 96, 24–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brzoza, Z.; Kasperska-Zajac, A.; Badura-Brzoza, K.; Matysiakiewicz, J.; Hese, R.T.; Rogala, B. Decline in Dehydroepiandrosterone Sulfate Observed in Chronic Urticaria is Associated With Psychological Distress. Psychosom. Med. 2008, 70, 723–728. [Google Scholar] [CrossRef] [PubMed]
- Kasperska-Zajac, A.; Brzoza, Z.; Rogala, B. Lower serum concentration of dehydroepiandrosterone sulphate in patients suffering from chronic idiopathic urticaria. Allergy 2006, 61, 1489–1490. [Google Scholar] [CrossRef]
- Kasperska-Zając, A.; Brzoza, Z.; Rogala, B. Serum concentration of dehydroepiandrosterone sulphate in female patients with chronic idiopathic urticaria. J. Dermatol. Sci. 2006, 41, 80–81. [Google Scholar] [CrossRef]
- Brzoza, Z.; Kasperska-Zajac, A.; Rogala, B. Serum prolactin concentration and its relationship with dehydroepiandrosterone sulfate concentration in chronic urticaria patients with positive and negative response to autologous serum skin test. Allergy 2007, 62, 566–567. [Google Scholar] [CrossRef]
Analysed Parameters (Unit) | Healthy Controls (N = 29) | Angioedema Patients (N = 26) | Statistical Analysis p |
---|---|---|---|
Median Range 25–75% | Median Range 25–75% | ||
eNO (ppb) | 17.0 9.00–27.0 13.0–20.0 | 15.5 5.00–37.0 11.0–19.0 | 0.45 |
age (years) | 22.0 21.0–58.0 22.0–48.0 | 35.0 18.0–60.0 25.0–50.0 | 0.39 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Moos, Ł.; Zajac, M.; Brzoza, Z. Exhaled Nitric Oxide Level in Pharynx Angioedema. J. Clin. Med. 2022, 11, 637. https://doi.org/10.3390/jcm11030637
Moos Ł, Zajac M, Brzoza Z. Exhaled Nitric Oxide Level in Pharynx Angioedema. Journal of Clinical Medicine. 2022; 11(3):637. https://doi.org/10.3390/jcm11030637
Chicago/Turabian StyleMoos, Łukasz, Magdalena Zajac, and Zenon Brzoza. 2022. "Exhaled Nitric Oxide Level in Pharynx Angioedema" Journal of Clinical Medicine 11, no. 3: 637. https://doi.org/10.3390/jcm11030637