Abstract
Purpose
Despite their effects on human health, the link between smokeless tobacco (ST) consumption and asthma severity in asthmatic patients is still unknown. Thus, the present study aims to complete the lack of information by investigating the aggravation of inflammation, aggravation of asthma, oxidative stress and cytotoxicity induced by ST in asthmatic patients.
Methods
The study recruited 80 male volunteers residing in Annaba town, Algeria, divided into four groups by using a questionnaire, each group consisting of 20 male volunteers. Herein, biochemical parameters, hematological parameters, C-reactive protein (CRP), total IgE, interleukin-5 (IL-5), nitric oxide and oxidative stress were measured.
Results
The obtained results showed that ST clearly enhanced lung inflammation and aggravation of asthma through total IgE, IL-5 and CRP increased production. In addition, ST was found to intensify oxidative stress via increased lipid peroxidation and decreased reduced glutathione (GSH) levels. Likewise, the biochemical and hematological parameters results showed that ST causes damage and inflammation to tissues.
Conclusion
Therefore, our study reveals that ST obviously enhances allergic inflammation in patients suffering from asthma.
Similar content being viewed by others
Availability of data and material
All data generated or analyzed during this study are included in this published article and its supplementary information files.
References
Enilari O, Sinha S (2019) The global impact of asthma in adult populations. Ann Glob Health. https://doi.org/10.5334/aogh.2412
Garzon-Siatoya WT, Carrillo-Martin I, Chiarella SE, Gonzalez-Estrada A (2022) State-of-the-art beta-adrenoreceptor agonists for the treatment of asthma. Expert Opin Pharmacother 23(2):243–254. https://doi.org/10.1080/14656566.2021.1988074
Sunkara K, Mehta M, Satija S, Dhanjal DS, Sharma P, Shukla SD, Allam VS (2022) An introduction to respiratory diseases and an emerging need for efficient drug delivery systems. In: Chellappan DK, Pabreja K, Faiyazuddin M (eds) Advanced drug delivery strategies for targeting chronic inflammatory lung diseases. Springer, Singapore, pp 1–24. https://doi.org/10.1007/978-981-16-4392-7_1
Tiotiu A (2018) Biomarkers in asthma: state of the art. Asthma Res Pract 4:10. https://doi.org/10.1186/s40733-018-0047-4
Network GA (2018) The Global Asthma Report, Auckland, New Zealand
Braman SS (2006) The global burden of asthma. Chest 130(1):4S-12S. https://doi.org/10.1378/chest.130.1_suppl.4S
World Health Organization (WHO) (2007) Global estimates of burden of disease caused by the environmental and occupational risks
National Institute of Public Health (2007) National Health Survey: Epidemiological transition and health system TAHINA project
Dworski R (2000) Oxidant stress in asthma. Thorax 55(suppl 2):S51–S53. https://doi.org/10.1136/thorax.55.suppl_2.S51
Khaldi T, Chekchaki N, Boumendjel M, Taibi F, Abdellaoui M, Messarah M, Boumendjel A (2018) Ameliorating effects of Nigella sativa oil on aggravation of inflammation, oxidative stress and cytotoxicity induced by smokeless tobacco extract in an allergic asthma model in Wistar rats. Allergol Immunopathol (Madr) 46(5):472–481. https://doi.org/10.1016/J.ALLER.2018.02.005
Shaik FB, Nagajothi G, Swarnalatha K, Kumar CS, Rajendra W, Maddu N (2021) Correlation between smokeless tobacco (Gutkha) and biomarkers of oxidative stress in plasma with cardiovascular effects. Heliyon 7(2):2405–8440. https://doi.org/10.1016/j.heliyon.2020.e05487
Kumar D, Binawara BK, Beniwal P, Sharma P (2017) Effect of chewing tobacco on hematological parameters in Bikaner city population. J Med Sci Clin Res 5(2):17721–17727. https://doi.org/10.18535/jmscr/v5i2.87
WHO Report on the Global Tobacco Epidemic (2019) World Health Organization, Geneva. ISBN 978-92-4-151620-4. Licence: CCBY-NC-SA 3.0 IGO
STEPwise Investigation Report Algeria (2017)
Kaur J, Prasad V (2013) Smokeless tobacco-countering the global epidemic. J Community Med Health Educ 3:198. https://doi.org/10.4172/2161-0711.1000198
Schivo M, Avdalovic MV, Murin S (2014) Non-cigarette tobacco and the lung. Clin Rev Allergy Immunol 46:34–53. https://doi.org/10.1007/s12016-013-8372-0
Kushner I, Gewurz H, Benson MD (1981) C-reactive protein and the acute-phase response. J Lab Clin Med 97:739–749
Navinés-Ferrer A, Serrano-Candelas E, Molina-Molina GJ, Martín M (2016) IgE-related chronic diseases and Anti-IgE-based treatments. J Immunol Res 2016:8163803. https://doi.org/10.1155/2016/8163803
Hamid Q, Tulic M (2009) Immunobiology of asthma. Annu Rev Physiol 71:489–507. https://doi.org/10.1146/annurev.physiol.010908.163200
Zhang X, Moilanen E, Kankaanranta H (2000) Enhancement of human eosinophil apoptosis by fluticasone propionate, budesonide, and beclomethasone. Eur J Pharmacol 406(3):325–332. https://doi.org/10.1016/s0014-2999(00)00690-7
Greenfeder S, Umland SP, Cuss FM, Chapman RW, Egan RW (2001) Th2 cytokines and asthma. The role of interleukin-5 in allergic eosinophilic disease. Respir Res 2(2):71–79. https://doi.org/10.1186/rr41
Keller AC, Rodriguez D, Russo M (2005) Nitric oxide paradox in asthma. Mem Inst Oswaldo Cruz 100(Suppl 1):19–23. https://doi.org/10.1590/s0074-02762005000900005
Khatri SB, Hammel J, Kavuru MS, Erzurum SC, Dweik RA (2003) Temporal association of nitric oxide levels and airflow in asthma after whole lung allergen challenge. J Appl Physiol 95:436–440. https://doi.org/10.1152/japplphysiol.01127.2002
Khatri SB, Ozkan M, McCarthy K, Laskowski D, Hammel J, Dweik RA, Erzurum SC (2001) Alterations in exhaled gas profile during allergen induced asthmatic response. Am J Respir Crit Care Med 164:1844–1848. https://doi.org/10.1164/ajrccm.164.10.2106119
Ricciardolo FL (2003) Multiple roles of nitric oxide in the airways. Thorax 58:175–182. https://doi.org/10.1136/thorax.58.2.175
Murray RL (1984) Aspartate aminotransferase. Clin Chem Toronto Princeton 1112–1116
Murray RL (1984) Alanine aminotransferase. Clin Chem Toronto. Princeton 1088–1090
Burtis CA, Edward RA, David EB (1999) “Tietz”. Texbook of Clinical Chemistry, 3rd edn. WB Saunders, Philadelphia
Sabokbar A, Millett PJ, Myer B, Rushton N (1994) A rapid quantitative assay for measuring alkaline phosphatase activity in osteoblastic cells in vitro. Bone 27(1):57–67. https://doi.org/10.1016/s0169-6009(08)80187-0
Kaplan A, Urea. Kaplan A et al. Clin Chem. The C.V Mosby Co. St Louis. Toronto. Princeton, (1984) 1257–1260.
Murray RL (1984) Creatinine. Kaplan A et al. Clin chem. The C.V. Mosby Co. St Louis. Toronto. Princeton, pp 1261–1266
Oswald IP, Wynn TA, Sher A, James SL (1992) Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proc Natl Acad Sci USA 89:8676–8680. https://doi.org/10.1073/pnas.89.18.8676
Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302
Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR (1974) Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11:151–169. https://doi.org/10.1159/000136485
Moerloose KB, Pauwels RA, Joos GF (2005) Short-term cigarette smoke exposure enhances allergic airway inflammation in mice. Am J Respir Crit Care Med 172:168–172. https://doi.org/10.1164/rccm.200409-1174OC
Ukoha U, Dimkpa U, Maduka S (2012) The effect of sub-lethal doses of smokeless tobacco (snuff) on certain hematological and hemostatic parameters in Wistar rats. J Exp Integrat Med 2(3):225–230. https://doi.org/10.5455/jeim.020412.or.027
Mukherjee R, Chatterjee A (2013) Assessment of the effects of smoking and consuming gutka (smokeless tobacco) on selected hematological and biochemical parameters: a study on healthy adult males of Hazaribag, Jharkhand. Int J Pharm Chem Biol Sci 3(4):1172–1178
Shukla AK, Khaitan T, Gupt P, Naik SR (2019) Smokeless tobacco and its adverse effects on hematological parameters: a cross-sectional study. Adv Prev Med 2019:3182946. https://doi.org/10.1155/2019/3182946
Yasmin S, Neha T, Mamta SS et al (2007) Negative impact of Gutkha on certain blood parameters of Swiss mice. Bull Pure Appl Sci-Zool 26(2):1–4
Thorat JS, Joshi AG, Wingkar KC (2021) Effect of vitamin C supplementation on hematological parameters in smokeless tobacco chewers. Int J Res Pharm Sci 12(3):2088–2094
Das A, Bhattacharya A, Chakrabarty S, Ganguli A, Chakrabarti G (2013) Smokeless tobacco extract (STE)-induced toxicity in mammalian cells is mediated by the disruption of cellular microtubule network: a key mechanism of cytotoxicity. PLoS ONE 8(7):e68224. https://doi.org/10.1371/journal.pone.0068224
Jaganmohan P, Sarma AP (2011) Studies on changes in hematological and biochemical parameters in smokeless tobacco (Gutka) chewing auto drivers in Nellore district of Andhra Pradesh, India. J Appl Natl Sci 3(1):106–107. https://doi.org/10.31018/jans.v3i1.165
Rajasekhar G, Ramgopal M, Sridevi A, Narasimha M (2007) Some hematological and biochemical parameters in smokeless tobacco (Jharda) chewers. Afr J Biotechnol 6:53–54
Memon SM, Kumar N, Atta-Ur-Rahman A, Syed BM (2021) Evaluation of C-reactive protein and hematological parameters in smokeless tobacco users: a comparative cross-sectional study. Pak J Med Sci 37(4):983–987. https://doi.org/10.12669/pjms.37.4.3841
Arimilli S, Damratoski BE, Bombick B, Borgerding MF, Prasad GL (2012) Evaluation of cytotoxicity of different tobacco product preparations. Regul Toxicol Pharmacol 64(3):350–360. https://doi.org/10.1016/j.yrtph.2012.09.004
Wirjatmadi B, Suryadinata RV (2020) The alteration on malondialdehyde content on Wistar rats’ blood and lungs tissue to ward the exposure of electric cigarette smoke. Indian J Public Health Res Develop 11(3):1881–1887
Bhatia RS, Vijayan VK (1994) Tobacco and health: What can the medical profession do? Lung India 12(4):178–185
Anandhalakshmi S, Kalaivani A, Shivasekar G, Saravanan A (2015) Evaluation of the impact of cigarette smoking on platelet parameters. Natl J Physiol Pharm Pharmacol 5:426–430. https://doi.org/10.5455/njppp.2015.5.1009201570
Mohammedi F, Hazari MA, Khatoon F, Husna K, Ali SI (2018) Effect of nicotine on platelet function. MedPulse Int J Physiol 5(2):13–16. https://doi.org/10.1159/000215800
Monadi M, Firouzjahi A, Hosseini A, Javadian Y, Sharbatdaran M, Heidari B (2016) Serum C-reactive protein in asthma and its ability in predicting asthma control, a case-control study. Casp J Intern Med 7:37–42
Shimoda T, Obase Y, Kishikawa R, Iwanaga T (2015) Serum high-sensitivity Creative protein can be an airway inflammation predictor in bronchial asthma. Allergy Asthma Proc 36:e23–e28. https://doi.org/10.2500/aap.2015.36.3816
Costello EJ, Copeland WE, Shanahan L, Worthman CM, Angold A (2013) C-reactive protein and substance use disorders in adolescence and early adulthood: A prospective analysis. Drug Alcohol Depend 133(2):712–717. https://doi.org/10.1016/j.drugalcdep.2013.08.027
Furie MB, Raffanello JA, Gergel EI, Lisinski TJ, Horb LD (2000) Extracts of smokeless tobacco induce pro-inflammatory changes in cultured human vascular endothelial cells. Immunopharmacology 47(1):13–23. https://doi.org/10.1016/s0162-3109(99)00181-2
Jebur MS, Saud AM (2020) Serum levels of total IgE and Interleukin-13 in a sample of allergic asthma patients in Baghdad. Iraqi J Sci. https://doi.org/10.24996/ijs.2020.61.12.8
Qasim AJ (2019) The role of vitamin D and interleukin-25 in Iraqi patients with allergic asthma. MSc. thesis. Mmustansiriyah University, College of Science
Davila I, Valero A, Entrenas LM, Valveny N, Herráez L, SIGE Study Group (2015) Relationship between serum total IgE and disease severity in patients with allergic asthma in Spain. J Investig Allergol Clin Immunol 25(2):120–127
Ahmed NJ, Husen AZ, Khoshnaw N, Getta HA, Hussein ZS, Yassin AK, Jalal SD, Mohammed RN, Alwan AF (2020) The effects of smoking on IgE, oxidative stress and haemoglobin concentration. Asian Pac J Cancer Prev 21(4):1069–1072. https://doi.org/10.31557/APJCP.2020.21.4.1069
Chhabra SK, Rajpal S, Gupta R (2001) Patterns of smoking in Delhi and comparison of chronic respiratory morbidity among bidi and cigarette smokers. Indian J Chest Dis Allied Sci 43:19–26
Dorman SC, Efthimiadis A, Babirad I, Watson RM, Denburg JA, Hargreave FE, Sehmi R (2004) Sputum CD34+ IL-5Rα+ cells increase after allergen: evidence for in situ eosinophilopoiesis. Am J Respir Crit Care Med 169(5):573–577. https://doi.org/10.1164/rccm.200307-1004OC
Broide DH, Paine MM, Firestein GS (1992) Eosinophils express interleukin 5 and granulocyte macrophage-colony-stimulating factor mRNA at sites of allergic inflammation. J Clin Invest 90:1414–1424. https://doi.org/10.1172/JCI116008
Sulakvelidze I, Inman MD, Rerecich TJ, O’Byrne PM (1998) Increases in airway eosinophils and interleukin-5 with minimal bronchoconstriction during repeated low dose allergen challenge in atopic asthmatics. Eur Resp J 11:821–827. https://doi.org/10.1183/09031936.98.11040821
Hallden G, Hellman C, Gronneberg R, Lundahl J (1999) Increased levels of IL5 positive peripheral blood eosinophils and lymphocytes in mild asthmatics after allergen inhalation provocation. Clin Exp Allergy 29:595–603. https://doi.org/10.1046/j.1365-2222.1999.00497.x
O’Byrne PM, Inman MD, Parameswaran K (2001) The trials and tribulations of IL-5, eosinophils, and allergic asthma. J Allergy Clin Immunol 108(4):503–508. https://doi.org/10.1067/mai.2001.119149
Ohnishi T, Kita H, Weiler D, Sur S, Sedgwick JB, Calhoun WJ, Busse WW, Abrams JS, Gleich GJ (1993) IL-5 is the predominant eosinophil-active cytokine in the antigen-induced pulmonary late-phase reaction. Am Rev Respir Dis 147(4):901–907. https://doi.org/10.1164/ajrccm/147.4.901
Teng Y, Gao Y (2014) Tobacco smoking associated with the increases of the bronchoalveolar levels of interleukin-5 and interleukin-1 receptor antagonist in acute eosinophilic pneumonia. Eur Rev Med Pharmacol Sci 18(6):887–893
Botelho FM, Llop-Guevara A, Trimble NJ, Nikota JK, Bauer CM, Lambert KN, Kianpour S, Jordana M, Stämpfli MR (2011) Cigarette smoke differentially affects eosinophilia and remodeling in a model of house dust mite asthma. Am J Respir Cell Mol Biol 45(4):753–760. https://doi.org/10.1165/rcmb.2010-0404OC
Ueha R, Ueha S, Kondo K, Nishijima H, Yamasoba T (2020) Effects of cigarette smoke on the nasal respiratory and olfactory mucosa in allergic rhinitis mice. Front Neurosci 14:126. https://doi.org/10.3389/fnins.2020.00126
Cozen W, Diaz-Sanchez D, James Gauderman W, Zadnick J, Cockburn MG, Gill PS, Masood R, Hamilton AS, Jyrala M, Mack TM (2004) Th1 and Th2 cytokines and IgE levels in identical twins with varying levels of cigarette consumption. J Clin Immunol 24(6):617–622. https://doi.org/10.1007/s10875-004-6247-0
Noakes PS, Holt PG, Prescott SL (2003) Maternal smoking in pregnancy alters neonatal cytokine responses. Allergy 58:1053–1058. https://doi.org/10.1034/j.1398-9995.2003.00290.x
Byron KA, Varigos GA, Wootton AM (1994) IL-4 production is increased in cigarette smokers. Clin Exp Immunol 95:333–336. https://doi.org/10.1111/j.1365-2249.1994.tb06533.x
Dweik RA, Comhair SA, Gaston B, Thunnissen FB, Farver C, Thomassen MJ, Kavuru M, Hammel J, Abu-Soud HM, Erzurum SC (2001) NO chemical events in the human airway during the immediate and late antigen-induced asthmatic response. Proc Natl Acad Sci USA 98:2622–2627. https://doi.org/10.1073/pnas.051629498
Szefler SJ, Phillips BR, Martinez FD, Chinchilli VM, Lemanske RF, Strunk RC, Zeiger RS, Larsen G, Spahn JD, Bacharier LB, Bloomberg GR, Guilbert TW, Heldt G, Morgan WJ, Moss MH, Sorkness CA, Taussig LM (2005) Characterization of within-subject responses to fluticasone and montelukast in childhood asthma. J Allergy Clin Immunol 115:233–242. https://doi.org/10.1016/j.jaci.2004.11.014
Guo FH, Comhair SA, Zheng S, Dweik RA, Eissa NT, Thomassen MJ, Calhoun W, Erzurum SC (2000) Molecular mechanisms of increased nitric oxide (NO) in asthma: evidence for transcriptional and post-translational regulation of NO synthesis. J Immunol 164(11):5970–5980. https://doi.org/10.4049/jimmunol.164.11.5970
Reid DW, Johns DP, Feltis B, Ward C, Walters EH (2003) Exhaled nitric oxide continues to reflect airway hyperresponsiveness and disease activity in inhaled corticosteroid-treated adult asthmatic patients. Respirology 8:479–486. https://doi.org/10.1046/j.1440-1843.2003.00495.x
Dweik RA, Boggs PB, Erzurum SC, Irvin CG, Leigh MW, Lundberg JO, Olin AC, Plummer AL, Taylor DR (2011) American Thoracic Society Committee on Interpretation of Exhaled Nitric Oxide Levels (FENO) for Clinical Applications. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med 184(5):602–615. https://doi.org/10.1164/rccm.9120-11ST
Prado CM, Martins MA, Tibério IF (2011) Nitric oxide in asthma physiopathology. ISRN Allergy. https://doi.org/10.5402/2011/832560
Lane C, Knight D, Burgess S, Franklin P, Horak F, Legg J, Moeller A, Stick S (2004) Epithelial inducible nitric oxide synthase activity is the major determinant of nitric oxide concentration in exhaled breath. Thorax 59:757–760. https://doi.org/10.1136/thx.2003.014894
Shaik FB, Nagajothi G, Swarnalatha K, Kumar CS, Rajendra W, Maddu N (2021) Correlation between smokeless tobacco (Gutkha) and biomarkers of oxidative stress in plasma with cardiovascular effects. Heliyon. 7(2):e05487. https://doi.org/10.1016/j.heliyon.2020.e05487
Preethi S, Jose JI, Sivapathasundharam B, Sabarinath B (2016) Evaluation of salivary nitric oxide levels in smokers, tobacco chewers and patients with oral lichenoid reactions. J Clin Diagn Res 10(1):ZC63–ZC66. https://doi.org/10.7860/JCDR/2016/16517.7126
Karthik B, Shruthi DK, Singh J, Tegginamani AS, Kudva S (2014) Do tobacco stimulate the production of nitric oxide by up regulation of inducible nitric oxide synthesis in cancer: Immunohistochemical determination of inducible nitric oxide synthesis in oral squamous cell carcinoma: a comparative study in tobacco habituers and non-habituers. J Cancer Res Ther 10(2):244–250. https://doi.org/10.4103/0973-1482.136542
Lam E, Kelley EE, Martin SM, Buettner GR (2003) Tobacco xenobiotics release nitric oxide. Tob Induc Dis 1(1):19. https://doi.org/10.1186/1617-9625-1-19
Cooper RG, Magwere T (2008) Nitric oxide-mediated pathogenesis during nicotine and alcohol consumption. Indian J Physiol Pharmacol 52:11–18
Barley RD, Pollock S, Shallow MC, Peters E, Lam EW (2004) Tobacco-related-compound-induced nitrosative stress injury in the hamster cheek pouch. J Dent Res 83:903–908. https://doi.org/10.1177/154405910408301203
Vleeming W, Rambali B, Opperhuizen A (2002) The role of nitric oxide in cigarette smoking and nicotine addiction. Nicotine Tob Res 4:341–348. https://doi.org/10.1080/14622200210142724
Chan HP, Tran V, Lewis C, Thomas PS (2009) Elevated levels of oxidative stress markers in exhaled breath condensate. J Thorac Oncol 4:172–178. https://doi.org/10.1097/JTO.0b013e3181949eb9
Aldakheel FM, Thomas PS, Bourke JE, Matheson MC, Dharmage SC, Lowe AJ (2016) Relationships between adult asthma and oxidative stress markers and pH in exhaled breath condensate: a systematic review. Allergy 71(6):741–757. https://doi.org/10.1111/all.12865
Barnes BJ (1990) Reactive oxygen species and airway inflammation. Free Radic Biol Med 9:235–243. https://doi.org/10.1016/0891-5849(90)90034-g
Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30:620–650. https://doi.org/10.1080/01926230290166724
Karadogan B, Beyaz S, Gelincik A, Buyukozturk S, Arda N (2022) Evaluation of oxidative stress biomarkers and antioxidant parameters in allergic asthma patients with different level of asthma control. J Asthma 59(4):663–672. https://doi.org/10.1080/02770903.2020.1870129
Bartoli ML, Novelli F, Costa F, Malagrinò L, Melosini L, Bacci E, Cianchetti S, Dente FL, Di Franco A, Vagaggini B, Paggiaro PL (2011) Malondialdehyde in exhaled breath condensate as a marker of oxidative stress in different pulmonary diseases. Mediators Inflamm. https://doi.org/10.1155/2011/891752
Romieu I, Barraza-Villarreal A, Escamilla-Nuñez C, Almstrand AC, Diaz-Sanchez D, Sly PD, Olin AC (2008) Exhaled breath malondialdehyde as a marker of effect of exposure to air pollution in children with asthma. J Allergy Clin Immunol 121(4):903–909. https://doi.org/10.1016/j.jaci.2007.12.004
Ozaras R, Tahan V, Turkmen S, Talay F, Besirli K, Aydin S, Uzun H, Cetinkaya A (2000) Changes in malondialdehyde levels in bronchoalveolar fluid and serum by the treatment of asthma with inhaled steroid and beta-agonist. Respirology 5(3):289–292. https://doi.org/10.1046/j.1440-1843.2000.00260.x
Fatani SH (2014) Biomarkers of oxidative stress in acute and chronic bronchial asthma. J Asthma 51(6):578–584. https://doi.org/10.3109/02770903.2014.892965
Sajid F, Bano S (2015) Effects of smokeless dipping tobacco (Naswar) consumption on antioxidant enzymes and lipid profile in its users. Pak J Pharm Sci 28(5):1829–1833
Khaitan T, Shukla AK, Gupta P, Naik SR, Verma P, Kumar S (2019) Liver and thyroid profile in educating smokeless tobacco users and its role in oral health promotion. J Educ Health Promot 8:224. https://doi.org/10.4103/jehp.jehp_6_19
Shrestha R, Nepal AK, Lal Das BK, Gelal B, Lamsal M (2012) Non-enzymatic antioxidant status and biochemical parameters in the consumers of Pan Masala containing tobacco. Asian Pac J Cancer Prev 13(9):4353–4356. https://doi.org/10.7314/apjcp.2012.13.9.4353
Yildiz D, Liu YS, Ercal N, Armstrong DW (1999) Comparison of pure nicotine and smokeless tobacco extract induced toxicities and oxidative stress. Arch Environ Contam Toxicol 37:434–439. https://doi.org/10.1007/s002449900537
Nakagome K, Nagata M (2011) Pathogenesis of airway inflammation in bronchial asthma. Auris Nasus Larynx 38:555–563. https://doi.org/10.1016/j.anl.2011.01.011
Nadeem A, Chhabra SK, Masood A, Raj HG (2003) Increased oxidative stress and altered levels of antioxidants in asthma. J Allerg Clin Immunol 111:72–78. https://doi.org/10.1067/mai.2003.17
Forman HJ, Zhang H, Rinna A (2009) Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 30(1–2):1–12. https://doi.org/10.1016/j.mam.2008.08.006
Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1):44–84. https://doi.org/10.1016/j.biocel.2006.07.001
Karadogan B, Beyaz S, Gelincik A, Buyukozturk S, Arda N (2021) Evaluation of oxidative stress biomarkers and antioxidant parameters in allergic asthma patients with different level of asthma control. J Asthma 8:1–15. https://doi.org/10.1080/02770903.2020.1870129
Celik M, Tuncer A, Soyer OU, Sackesen C, Tanju Besler H, Kalayci O (2012) Oxidative stress in the airways of children with asthma and allergic rhinitis. Pediatr Allerg Immunol 23:556–561. https://doi.org/10.1111/j.1399-3038.2012.01294.x
Fabian E, Poloskey P, Kosa L, Elmadfa I, Rethy LA (2011) Activities of antioxidant enzymes in relation to oxidative and nitrosative challenges in childhood asthma. J Asthma 48:351–357. https://doi.org/10.3109/02770903.2011.560319
Al-Afaleg NO, Al-Senaidy A, El-Ansary A (2011) Oxidative stress and antioxidant status in Saudi asthmatic patients. Clin Biochem 44:612–617. https://doi.org/10.1016/j.clinbiochem.2011.01.016
Ercan H, Birben E, Dizdar EA, Keskin O, Karaaslan C, Soyer OU, Dut R, Sackesen C, Besler T, Kalayci O (2006) Oxidative stress and genetic and epidemiologic determinants of oxidant injury in childhood asthma. J Allergy Clin Immunol 118(5):1097–1104. https://doi.org/10.1016/j.jaci.2006.08.012
Sackesen C, Ercan H, Dizdar E, Soyer O, Gumus P, Tosun BN, Buyuktuncer Z, Karabulut E, Besler T, Kalayci O (2008) A comprehensive evaluation of the enzymatic and nonenzymatic antioxidant systems in childhood asthma. J Allergy Clin Immunol 122(1):78–85. https://doi.org/10.1016/j.jaci.2008.03.035
Mak JC, Leung HC, Ho SP, Law BK, Lam WK, Tsang KW, Ip MS, Chan-Yeung M (2004) Systemic oxidative and antioxidative status in Chinese patients with asthma. J Allergy Clin Immunol 114(2):260–264. https://doi.org/10.1016/j.jaci.2004.05.013
Pennings HJ, Borm PJ, Evelo CT, Wouters EF (1999) Changes in levels of catalase and glutathione in erythrocytes of patients with stable asthma, treated with beclomethasone dipropionate. Eur Respir J 13(6):1260–1266. https://doi.org/10.1183/09031936.99.13612679
Kelly FJ, Mudway I, Blomberg A, Frew A, Sandstrom T (1999) Altered lung antioxidant status in patients with mild asthma. Lancet 354(9177):482–483. https://doi.org/10.1016/S0140-6736(99)01812-7
Koregol AC, Kalburgi NB, Pattanashetty P, Warad S, Shirigeri NS, Hunasikatti VC (2020) Effect of smokeless tobacco use on salivary glutathione levels among chronic periodontitis patients before and after non-surgical periodontal therapy. Tobacco Prevent Cessat 6:15. https://doi.org/10.18332/tpc/115062
Das S, Upadhaya P, Giri S (2016) Arsenic and smokeless tobacco induce genotoxicity, sperm abnormality as well as oxidative stress in mice in vivo. Genes Environ 38:4. https://doi.org/10.1186/s41021-016-0031-2
Avti PK, Kumar S, Pathak CM, Vaiphei K, Khanduja KL (2006) Smokeless tobacco impairs the antioxidant defense in liver, lung, and kidney of rats. Toxicol Sci 89(2):547–553. https://doi.org/10.1093/toxsci/kfj041
Hung CR (2004) Protective effects of lysozyme chloride and reduced glutathione on betel quid chewing-produced gastric oxidative stress and hemorrhagic ulcer in rats. Inflammopharmacology 12:115–129. https://doi.org/10.1163/1568560041352284
Jeng JH, Chang MC, Hahn LJ (2001) Role of areca nut in betel quid-associated chemical carcinogenesis: current awareness and future perspectives. Oral Oncol 37:477–492. https://doi.org/10.1016/s1368-8375(01)00003-3
Kumar M, Kannan A, Upreti RK (2000) Effect of betel/areca nut (Areca catechu) extracts on intestinal epithelial cell lining. Vet Hum Toxicol 42:257–260
Cotgreave IA, Johansson U, Moldeus P, Brattsand R (1987) The effect of acute cigarette smoke inhalation on pulmonary and systemic cysteine and glutathione redox states in the rat. Toxicology 45:203–212. https://doi.org/10.1016/0300-483x(87)90106-5
Stupin V, Abramov I, Gahramanov T, Kovalenko A, Manturova N, Litvitskiy P, Balkizov Z, Silina E (2022) Comparative study of the results of operations in patients with tumor and non-tumor obstructive jaundice who received and did not receive antioxidant therapy for the correction of endotoxemia, glycolysis, and oxidative stress. Antioxidants (Basel) 11(6):1203. https://doi.org/10.3390/antiox11061203
Feres CA, Madalosso RC, Rocha OA, Leite JP, Guimaraes TM, Toledo VP, Tagliati CA (2006) Acute and chronic toxicological studies of Dimorphandra mollis in experimental animals. J Ethnopharmacol 108:450–456. https://doi.org/10.1016/j.jep.2006.06.002
Green RM, Flamm S (2002) AGA technical review on the evaluation of liver chemistry tests. Gastroenterology 123:1367–1384. https://doi.org/10.1053/gast.2002.36061
Aragon G, Younossi ZM (2010) When and how to evaluate mildly elevated liver enzymes in apparently healthy patients. Cleve Clin J Med 77:195–204. https://doi.org/10.3949/ccjm.77a.09064
Khaldi T, Chekchaki N, Rouibah Z, Chouala K, Cheniti H, Boumendjel M, Taibi F, Messarah M, Boumendjel A (2022) Preventive effects of oral administration of Nigella sativa oil against smokeless tobacco induced toxicity and oxidative stress in the liver and kidney of allergic asthma induced rats. Toxicol Environ Health Sci 14:291–300. https://doi.org/10.1007/s13530-022-00142-9
Burtis CA, Ashwood ER, Bruns DE (2006) Tietz textbook of clinical chemistry and molecular diagnostics, 4th edn. Elsevier, Saunders
Davies KJ, Delsignore ME, Lin SW (1987) Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J Biol Chem 262(20):9902–9907. https://doi.org/10.1016/S0021-9258(18)48019-2
Cochrane CG (1991) Cellular injury by oxidants. Am J Med 91:23–30. https://doi.org/10.1016/0002-9343(91)90280-b
Funding
The authors would like to thank the Algerian Directorate General for Scientific Research and Technological Development (DGRSDT) and the Thematic Research Agency in Health Sciences (ATRSS) for the support of this research work via PNR project (33/DFPR/ATRSS).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Taha Khaldi, Mahfoud Messarah and Amel Boumendjel. The first draft of the manuscript was written by Taha Khaldi and Amira Aicha Beya. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Taha Khaldi, Karima Boughemara, Yasmine Khodja Hesnie, Aicha Beya Amira, Mahfoud Messarah and Amel Boumendje declare no competing interests.
Ethics approval
All protocols in this study were used in accordance with the guidelines of the Committee on Use of Laboratory Animals and approved under the PNR project (33/DFPR/ATRSS) by the Ethical Committee of Thematic Agency for Research in Health Sciences.
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Consent to publish
The authors affirm that human research participants provided informed consent for publication of the results of this study.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Khaldi, T., Boughemara, K., Khodja Hesnie, Y. et al. Smokeless tobacco enhances allergic inflammation, aggravation of asthma and oxidative stress in asthmatic patients from Algeria. Toxicol. Environ. Health Sci. 15, 275–287 (2023). https://doi.org/10.1007/s13530-023-00181-w
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13530-023-00181-w