Abstract
Background
The inhalation injury is usually initiated by uninhibited absorption of smoke, favoring the release of cytokines and other lipid mediators from inflammatory cells in lung airways and parenchyma.
Objectives
To systematically review, examine, and synthesize the main inflammatory mediators analyzed in published studies in animals subjected to smoke inhalation, as well as oxidative stress.
Search Strategy
A comprehensive literature search was conducted through MEDLINE-PubMed, Web of Science, and Scopus.
Selection Criteria
Studies with animals subjected to lung damage from smoke inhalation that evaluated the presence and the action of inflammatory mediators and oxidative stress.
Results
A total of 1332 studies were initially identified, with only 31 meeting the inclusion criteria. The inflammatory mediators and oxidative stress markers studied and presented in the articles described herein were varied; however, the most cited ones were tumor necrosis factor-alpha (6), IL-8 and IL-6 (both studied in five articles), IL-1β and nuclear factor kappa β (both studied in 4 articles), malondialdehyde (11 studies), and myeloperoxidase (7). It is worth noting that most studies evaluated more than one inflammatory mediator and oxidative stress marker.
Conclusion
Based on this review, we could observe that the main inflammatory mediators and oxidative stress markers analyzed were TNF-α, IL-8, IL-6, IL-1β, nuclear factor kappa β, MDA, and MPO. However, it is necessary to increase the rigor of study design and data, in order to have studies that are more homogeneous and with appropriate methodological quality.
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References
Souza R, Jardim C, Salge J et al (2004) Lesão por inalação de fumaça. J Bras Pneumol 30(6):557–565
Rivero C, Rivera J, Cabezas MC et al (2006) Manejo de quemados. Guias de practica clinica basadas en la evidencia (Proyecto ISS - ASCOFAME) p 14–69
Demling R, Lalonde C, Youn YK et al (1995) Effect of graded increases in smoke inhalation injury on the early systemic response to a body burn. Crit Care Med 23(1):171–178
Shimoda K, Nakazawa H, Traber MG et al (2008) Plasma and tissue vitamin E depletion in sheep with burn and smoke inhalation injury. Burns 34:1137–1141
Musch G, Winkler T, Harris RS et al (2014) Lung [(18)F]fluorodeoxyglucose uptake and ventilation-perfusion mismatch in the early stage of experimental acute smoke inhalation. Anesthesiology 120(3):683–693
Rajpura A (2002) The epidemiology of burns and smoke inhalation in secondary care: a population-based study covering Lancashire and South Cumbria. Burns. 28(2):121–130
Mosier MJ, Pham TN, Park DR et al (2012) Predictive value of bronchoscopy in assessing the severity of inhalation injury. J Burn Care Res 33(1):65–73
Li W, Qiu X, Wang J et al (2013) The therapeutic efficacy of glutamine for rats with smoking inhalation injury. Int Immunopharmacol 16(2):248–253
Boateng JS, Matthews KH, Stevens HNE et al (2008) Wound healing dressings and drug delivery systems: a review. J Pharm Sci. 97(8):2892–2923
Tasaki O, Mozingo D, Ishihara S et al (1998) Effect of Sulfo Lewis C on smoke inhalation injury in an ovine model. Crit Care Med 26(7):1238–1243
Tasaki O, Mozingo DW, Dubick MA et al (2002) Effects of heparin and lisofylline on pulmonary function after smoke inhalation injury in an ovine model. Crit Care Med 30(3):637–643
Ikeuchi H, Sakano T, Sanchez J et al (1992) The effects of platelet-activating factor (PAF) and a PAF antagonist (CV-3988) on smoke inhalation injury in an ovine model. J Trauma 32(3):344–349
Abali A, Karakayali H, Ozdemir B et al (2013) Destructive pulmonary effects of smoke inhalation and simultaneous alterations in circulating IL-6, TNF- α, and IFN- γ levels at different burn depths : an experimental study on rats. J Burn Care Res 34(3):334–341
Fang Y, Fu X, Gu C et al (2011) Hydrogen-rich saline protects against acute lung injury induced by extensive burn in rat model. J Burn Care Res 32(3):e82–e91
Cox RA, Burke AS, Jacob S et al (2009) Activated nuclear factor kappa B and airway inflammation after smoke inhalation and burn injury in sheep. J Burn Care Res 30(3):489–498
Herndon DN, Spies M (2001) Modern burn care. Semin Pediatr Surg 10:28–31
Traber MG, Shimoda K, Murakami K et al (2007) Burn and smoke inhalation injury in sheep depletes vitamin E: kinetic studies using deuterated tocopherols. Free Radic Biol Med. 42(9):1421–1429
Morita N, Shimoda K, Traber MG et al (2006) Vitamin E attenuates acute lung injury in sheep with burn and smoke inhalation injury. Redox Rep. 11(2):61–70
McMillen C (2001) The sheep—an ideal model for biomedical research? ANZCCART News 14(2):1–4
Herndon DN, Traber DL, Niehaus GD et al (1984) The pathophysiology of smoke inhalation injury in sheep model. J Trauma 24:1044–1051
Herndon DN, Traber LD, Linares H et al (1986) Etiology of the pulmonary pathophysiology associated with inhalation injury. Resuscitation 14:43–59
Cox RA, Burke AS, Oliveras G et al (2005) Acute bronchial obstruction in sheep: histopathology and gland cytokine expression. Exp Lung Res 31(9–10):819–837
Dubick MA, Carden SC, Jordan BS et al (2002) Indices of antioxidant status in rats subjected to wood smoke inhalation and/or thermal injury. Toxicology 176(1–2):145–157
Belli S, Basaran O, Ozdemir BH et al (2011) Protective role of simvastatin on lung damage caused by burn and cotton smoke inhalation in rats. J Surg Res 167(2):e283–e290
Peters W (1981) Inhalation injury caused by the products of combustion. Can Med Assoc J 125(3):249–252
Benzie IF (1996) Lipid peroxidation: a review of causes, consequences, measurements and dietary influences. Int J Food Sci Nutr 47(3):233–261
Greenhalgh DG, Saffle JR, Holmes JH 4th et al (2007) American Burn Association consensus conference to define sepsis and infection in burns. J Burn Care Res 28(6):776–790
Ferreira A, Matsubara L (1997) Radicais livres: conceitos, doenças relacionadas, sistema de defesa e estresse oxidativo. Rev Ass Med Brasil 43(1):61–68
Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15(4):316–328
Bagis S, Tamer L, Sahin G et al (2005) Free radicals and antioxidants in primary fibromyalgia: an oxidative stress disorder? Rheumatol Int 25(3):188–190
Hamahata A, Enkhbaatar P, Lange M et al (2011) Direct delivery of low-dose 7-nitroindazole into the bronchial artery attenuates pulmonary pathophysiology after smoke inhalation and burn injury in an ovine model. Shock 36(6):575–579
Demling R, LaLonde C, Ikegami K (1996) Fluid resuscitation with deferoxamine hetastarch complex attenuates the lung and systemic response to smoke inhalation. Surgery 119(3):340–348
Hamahata A, Enkhbaatar P, Kraft ER et al (2008) γ-Tocopherol nebulization by a lipid aerosolization device improves pulmonary function in sheep with burn and smoke inhalation injury. Free Radic Biol Med 45:425–433
Park MS, Cancio LC, Jordan BS et al (2004) Assessment of oxidative stress in lungs from sheep after inhalation of wood smoke. Toxicology 195(2–3):97–112
Tasaki O, Goodwin CW, Saitoh D et al (1997) Effects of Burns on Inhalation Injury. J Trauma 43(4):603–607
Yamamoto Y, Sousse LE, Enkhbaatar P et al (2012) γ-Tocopherol nebulization decreases oxidative stress, arginase activity, and collagen deposition after burn and smoke inhalation in the ovine model. Shock 38(6):671–676
Ramos C, Pedraza-Chaverri J, Becerril C et al (2013) Oxidative stress and lung injury induced by short-term exposure to wood smoke in guinea pigs. Toxicol Mech Methods 23(9):711–722
Demling R, Lalonde C, Picard L et al (1994) Changes in lung and systemic oxidant and antioxidant activity after smoke inhalation. Shock 1(2):101–107
Wang Y, Wang W, Zhang Y et al (2010) Clinical significance of a myeloperoxidase gene polymorphism and inducible nitric oxide synthase expression in cirrhotic patients with hepatopulmonary syndrome. J Huazhong Univ Sci Technolog Med Sci 30(4):437–442
Esechie A, Enkhbaatar P, Traber DL et al (2009) Beneficial effect of a hydrogen sulphide donor (sodium sulphide) in an ovine model of burn- and smoke-induced acute lung injury. Br J Pharmacol 158(6):1442–1453
Qiu X, Ji S, Wang J et al (2012) The therapeutic efficacy of Ulinastatin for rats with smoking inhalation injury. Int Immunopharmacol 14:289–295
Ischiropoulos H, Mendiguren I, Fisher D et al (1994) Role of neutrophils and nitric oxide in lung alveolar injury from smoke inhalation. Am J Respir Crit Care Med 150(2):337–341
Monroy RL, Skelly RR, Davis TA et al (1992) Therapeutic evaluation of interleukin-1 for estimulation of hematopoiesis in primates after autologous bone marrow transplantation. Biotherapy 4:97–108
Dinarello CA (1989) Biologic basis for interleukin-1 in disease. Blood 87(6):2095–2147
Arend WP (1991) Interleukin 1 receptor antagonist. A new member of the interleukin 1 family. J Clin Invest 88:1445–1451
Varella PPV, Forte WCN (2001) Citokines: a review. Rev Bras Alerg Imunopatol 24(4):146–154
Rothewell NJ (1991) Functions and mechanisms of interleukin 1 in the brain. Trends Pharmacol Sci 12:430–436
Heinrich PC, Castell JV, Andus T (1990) Interleukin-6 and the acute phase response. Biochem J 265(3):621–636
Mackay F, Loester H, Stueber D et al (1993) Tumor necrosis factor alpha (TNF-al-pha)-induced cell adhesion to human endotelial cells is under dominant control of one TNF recep-tor type, TNF-R55. J Exp Med 177:1277–1286
Tartaglia LA, Ayres TM, Wong GH et al (1993) A novel domain within the 55 kd TNF recep-tor signals cell death. Cell 74:845–853
Kunkel SL, Striter RM, Chensue SW et al (1991) The role of TNF in diverse pathologic processes. Biotherapy 3:135–141
Riyami BM, Kinsella J, Pollok AJ et al (1991) Alveolar macrophage chemotaxis in fire victims with smoke inhalation and burns injury. Eur J Clin Invest 21:485–489
Moores HK, Janigan DT, Hajela RP (1993) Lung injury after experimental smoke inhalation: particle-associated changes in alveolar macrophages. Toxicol Pathol 21:521–527
Bidani A, Wang CZ, Heming TA (1998) Cotton smoke inhalation primes alveolar macrophages for tumor necrosis factor-alpha production and suppresses macrophage antimicrobial activities. Lung 176(5):325–336
Zwahlen R, Walz A, Rot A (1993) In vitro and in vivo activity and pathophysiology of human interleukin-8 and related peptides. Int Rev Exp Pathol 34:27–42
Christman JW, Sadikot RT, Blackwell TS (2000) The role of nuclear factor-kappa B in pulmonary diseases. Chest 117:1482–1487
Madjdpour L, Kneller S, Booy C et al (2003) Acid-induced lung injury: role of nuclear factor-kappaB. Anesthesiology 99:1323–1332
Laffon M, Pittet J, Modelska K et al (1999) Interleukin-8 mediates injury from smoke inhalation to both the lung endothelial and the alveolar epithelial barriers in rabbits. Am J Respir Crit Care Med 160(5 Pt 1):1443–1449
Albright JM, Davis CS, Bird MD et al (2012) The acute pulmonary inflammatory response to the graded severity of smoke inhalation injury. Crit Care Med 40:1113–1121
Kurzius-Spencer M, Foster K, Littau S et al (2008) Tracheobronchial markers of lung injury in smoke inhalation victims. J Burn Care Res 29:311–318
Hamahata A, Enkhbaatar P, Kraft ER et al (2008) γ-Tocopherol nebulization by a lipid aerosolization device improves pulmonary function in sheep with burn and smoke inhalation injury. Free Radic Biol Med 45:425–433
Wang S, Lantz RC, Rider ED et al (1997) A free radical scavenger (Lazaroid U75412E) attenuates tumor necrosis factor-alpha generation in a rabbit model of smoke-induced lung injury. Respiration 64(5):358–363
Wang S, Land RC, Chen GJ et al (1996) The prophylactic effects of U75412E pretreatment in a smoke-induced lung injury rabbit model. Pharmacol Toxicol 79(5):231–237
Farrell KE, Keely S, Graham B et al (2014) A systematic review of the evidence for central nervous system plasticity in animal models of inflammatory-mediated gastrointestinal pain. Inflamm Bowel Dis 20(1):176–195
Sena E, van der Worp HB, Howells D et al (2007) How can we improve the pre-clinical development of drugs for stroke? Trends Neurosci 30:433–439
Tsilidis KK, Panagiotou OA, Sena ES et al (2013) Evaluation of excess significance bias in animal studies of neurological diseases. PLoS Biol 11:e1001609
Bidani A, Hawkins HK, Wang CZ et al (1999) Dose dependence and time course of smoke inhalation injury in a rabbit model. Lung. 177(2):111–122
Murakami K, Enkhbaatar P, Yu YM et al (2007) L-arginine attenuates acute lung injury after smoke inhalation and burn injury in sheep. Shock 28(4):477–483
Acknowledgments
We would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico/CNPq/Brazil and Fundação de Amparo à Pesquisa do Estado de Sergipe/FAPITEC-SE for the financial support.
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de Carvalho, F.O., Felipe, F.A., de Melo Costa, A.C.S. et al. Inflammatory Mediators and Oxidative Stress in Animals Subjected to Smoke Inhalation: A Systematic Review. Lung 194, 487–499 (2016). https://doi.org/10.1007/s00408-016-9879-y
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DOI: https://doi.org/10.1007/s00408-016-9879-y