Probiotics supplementation reduces cigarette smoke-induced damage in the respiratory micro-architecture of mice

Authors

DOI:

https://doi.org/10.11606/issn.1678-4456.bjvras.2023.201873

Keywords:

Emphysema, Respiratory epithelium, Asthma, Goblet cells, Lungs

Abstract

This study evaluated the protective efficacy of probiotics supplementation against cigarette smoke-induced lung emphysema, inflammation, and loss of cilia in mice. Probiotics are known to promote mucosal tolerance and mitigate respiratory injuries. Twenty-four adult mice were randomly divided into three groups: control (Ctr), cigarette smoke (CS), and cigarette smoke + probiotics (CS+P). Probiotics were given for 7 days before exposure to smoke in the CS+P group. Tissue samples of the trachea (goblet cell count and index, loss of cilia), lungs (airspace distention), and bronchoalveolar lavage fluid (BALF) were collected and processed. The results showed a significant increase in acidic and neutral goblet cells in the CS group compared to the Ctr and CS+P groups (P < 0.05). Overall, goblet cell number and index were lower in the CS+P group (41.71 ± 5.76, 0.67 ± 0.073) than CS group (56.28 ± 5.34, 1.31 ± 0.28). Inflammatory cells and loss of cilia significantly decreased in mice fed probiotics before exposure to cigarette smoke (P < 0.05). Lung emphysema was also significantly reduced in the CS+P group compared to the CS group (P < 0.05). In conclusion, dietary supplementation of probiotics reduced lung emphysema, inflammatory cells, goblet cell index, and loss of cilia under conditions of cigarette smoke exposure in mice.

Downloads

Download data is not yet available.

References

Ardite E, Peinado VI, Rabinovich RA, Fernández-Checa JC, Roca J, Barberà JA. Systemic effects of cigarette smoke exposure in the guinea pig. Respir Med. 2006;100(7):1186-94. http://doi.org/10.1016/j.rmed.2005.10.023. PMid:16330198.

Arinola O, Akinosun O, Olaniyi J. Passive-and active-cigarette smoking: effects on the levels of antioxidant vitamins, immunoglobulin classes and acute phase reactants. Afr J Biotechnol [Internet]. 2011 [cited 2022 Sept 4];10(32):6130-2. Available from: https://www.ajol.info/index.php/ajb/article/view/94493.

Arunachalam K, Gill HS, Chandra RK. Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur J Clin Nutr. 2000;54(3):263-7. http://doi.org/10.1038/sj.ejcn.1600938. PMid:10713750.

Bancroft JD, Gamble M. Theory and practice of histological techniques. London: Churchill Livingstone; 2008.

Baughman RP, Drent M. Role of bronchoalveolar lavage in interstitial lung disease. Clin Chest Med. 2001;22(2):331-41. http://doi.org/10.1016/S0272-5231(05)70047-2. PMid:11444116.

Biselli PJ, Lopes FD, Moriya HT, Rivero DH, Toledo AC, Saldiva PH, Mauad T, Martins MA. Short-term exposure of mice to cigarette smoke and/or residual oil fly ash produces proximal airspace enlargements and airway epithelium remodeling. Braz J Med Biol Res. 2011;44(5):460-8. http://doi.org/10.1590/S0100-879X2011007500040. PMid:21445523.

Dec M, Nowaczek A, Urban-Chmiel R, Stępień-Pyśniak D, Wernicki A. Probiotic potential of Lactobacillus isolates of chicken origin with anti-Campylobacter activity. J Vet Med. 2018;80(8):1195-203. PMid:29877314.

Elliott MK, Sisson JH, Wyatt TA. Effects of cigarette smoke and alcohol on ciliated tracheal epithelium and inflammatory cell recruitment. Am J Respir Cell Mol Biol. 2007;36(4):452-9. http://doi.org/10.1165/rcmb.2005-0440OC. PMid:17079783.

Ezendam J, van Loveren H. Probiotics: immunomodulation and evaluation of safety and efficacy. Nutr Rev. 2006;64(1):1-14. http://doi.org/10.1111/j.1753-4887.2006.tb00168.x. PMid:16491665.

Forsythe P, Inman MD, Bienenstock J. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am J Respir Crit Care Med. 2007;175(6):561-9. http://doi.org/10.1164/rccm.200606-821OC. PMid:17204726.

Işik AC, Kalender Y, Yardimci S, Ergün A. Environmental tobacco smoke in rats. J Otolaryngol. 2004;33(6):382-6. http://doi.org/10.2310/7070.2004.03026. PMid:15971655.

Jung B, Ko J, Cho S, Koh H, Yoon S, Han D, Lee BJ. Immune-enhancing effect of fermented Maesil (Prunus mume Siebold & Zucc.) with probiotics against Bordetella bronchiseptica in mice. J Vet Med Sci. 2010;72(9):1195-202. PMid:20453453.

Knudsen L, Weibel ER, Gundersen HJG, Weinstein FV, Ochs M. Assessment of air space size characteristics by intercept (chord) measurement: an accurate and efficient stereological approach. J Appl Physiol. 2010;108(2):412-21. http://doi.org/10.1152/japplphysiol.01100.2009. PMid:19959763.

Komori M, Inoue H, Matsumoto K, Koto H, Fukuyama S, Aizawa H, Hara N. PAF mediates cigarette smoke-induced goblet cell metaplasia in guinea pig airways. Am J Physiol Lung Cell Mol Physiol. 2001;280(3):L436-41. http://doi.org/10.1152/ajplung.2001.280.3.L436. PMid:11159026.

Luppi F, Aarbiou J, Van Wetering S, Rahman I, De Boer WI, Rabe KF, Hiemstra PS. Effects of cigarette smoke condensate on proliferation and wound closure of bronchial epithelial cells in vitro: role of glutathione. Respir Res. 2005;6(1):140. http://doi.org/10.1186/1465-9921-6-140. PMid:16309548.

MacNee W, Rahman I. Is oxidative stress central to the pathogenesis of chronic obstructive pulmonary disease? Trends Mol Med. 2001;7(2):55-62. http://doi.org/10.1016/S1471-4914(01)01912-8. PMid:11286755.

Mortaz E, Adcock IM, Ricciardolo FL, Varahram M, Jamaati H, Velayati AA, Folkerts G, Garssen J. Anti-Inflammatory effects of lactobacillus rahmnosus and bifidobacterium breve on cigarette smoke activated human macrophages. PLoS One. 2015;10(8):e0136455. http://doi.org/10.1371/journal.pone.0136455. PMid:26317628.

Nagamma T, Anjaneyulu K, Baxi J, Dayaram P, Singh PP. Effects of cigarette smoking on lipid peroxidation and antioxidant status in cancer patients from Western Nepal. Asian Pac J Cancer Prev. 2011;12(1):313-6. PMid:21517278.

Plopper CG, St George J, Nishio SJ, Etchison JR, Nettesheim P. Carbohydrate cytochemistry of tracheobronchial airway epithelium of the rabbit. J Histochem Cytochem. 1984;32(2):209-18. http://doi.org/10.1177/32.2.6693755. PMid:6693755.

Podowski M, Calvi C, Metzger S, Misono K, Poonyagariyagorn H, Lopez-Mercado A, Ku T, Lauer T, McGrath-Morrow S, Berger A, Cheadle C, Tuder R, Dietz HC, Mitzner W, Wise R, Neptune E. Angiotensin receptor blockade attenuates cigarette smoke–induced lung injury and rescues lung architecture in mice. J Clin Invest. 2012;122(1):229-40. http://doi.org/10.1172/JCI46215. PMid:22182843.

Rennard SI. Inflammation and repair processes in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1999;160(5, Suppl 1):S12-6. http://doi.org/10.1164/ajrccm.160.supplement_1.5. PMid:10556162.

Simet SM, Sisson JH, Pavlik JA, DeVasure JM, Boyer C, Liu X, Kawasaki S, Sharp JG, Rennard SI, Wyatt TA. Long-term cigarette smoke exposure in a mouse model of ciliated epithelial cell function. Am J Respir Cell Mol Biol. 2010;43(6):635-40. http://doi.org/10.1165/rcmb.2009-0297OC. PMid:20042711.

Smith TD, Watt H, Gunn L, Car J, Boyle RJ. Recommending oral probiotics to reduce winter antibiotic prescriptions in people with asthma: a pragmatic randomized controlled trial. Ann Fam Med. 2016;14(5):422-30. http://doi.org/10.1370/afm.1970. PMid:27621158.

Sun L, Chen Y, Wu R, Lu M, Yao W. Changes in definition lead to changes in the clinical characteristics across COPD categories according to GOLD 2017: a national cross-sectional survey in China. Int J Chron Obstruct Pulmon Dis. 2017;12:3095-102. http://doi.org/10.2147/COPD.S142801. PMid:29118578.

Tannock GW, Munro K, Harmsen HJ, Welling GW, Smart J, Gopal PK. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosusDR20. Appl Environ Microbiol. 2000;66(6):2578-88. http://doi.org/10.1128/AEM.66.6.2578-2588.2000. PMid:10831441.

Valença SS, da Hora K, Castro P, Moraes VG, Carvalho L, Porto LC. Emphysema and metalloelastase expression in mouse lung induced by cigarette smoke. Toxicol Pathol. 2004;32(3):351-6. http://doi.org/10.1080/01926230490431466. PMid:15204978.

Vasconcelos FM, Silva HL, Poso SM, Barroso MV, Lanzetti M, Rocha RS, Graça JS, Esmerino EA, Freitas MQ, Silva MC, Raices RSL, Granato D, Pimentel TC, Sant’Ana AS, Cruz AG, Valença SS. Probiotic Prato cheese attenuates cigarette smoke-induced injuries in mice. Food Res Int. 2019;123:697-703. http://doi.org/10.1016/j.foodres.2019.06.001. PMid:31285019.

Wang X, Hui Y, Zhao L, Hao Y, Guo H, Ren F. Oral administration of Lactobacillus paracasei L9 attenuates PM2. 5-induced enhancement of airway hyperresponsiveness and allergic airway response in murine model of asthma. PLoS One. 2017;12(2):e0171721. http://doi.org/10.1371/journal.pone.0171721. PMid:28199353.

Wen Y, Reid DW, Zhang D, Ward C, Wood-Baker R, Walters EH. Assessment of airway inflammation using sputum, BAL, and endobronchial biopsies in current and ex-smokers with established COPD. Int J Chron Obstruct Pulmon Dis. 2010;5:327-34. http://doi.org/10.2147/COPD.S11343. PMid:21037956.

Wheeler JG, Shema SJ, Bogle ML, Shirrell MA, Burks AW, Pittler A, Helm RM. Immune and clinical impact of Lactobacillus acidophilus on asthma. Ann Allergy Asthma Immunol. 1997;79(3):229-33. http://doi.org/10.1016/S1081-1206(10)63007-4. PMid:9305229.

Yu J, Jang S-O, Kim B-J, Song Y-H, Kwon J-W, Kang M-J, Choi WA, Jung HD, Hong SJ. The effects of Lactobacillus rhamnosus on the prevention of asthma in a murine model. Allergy Asthma Immunol Res. 2010;2(3):199-205. http://doi.org/10.4168/aair.2010.2.3.199. PMid:20592920.

Downloads

Published

2023-03-20

Issue

Section

FULL ARTICLE

How to Cite

1.
Khan K, Zaneb H, Masood S, Ashraf S, Usman MM, Faseehur-Rehman H, et al. Probiotics supplementation reduces cigarette smoke-induced damage in the respiratory micro-architecture of mice. Braz. J. Vet. Res. Anim. Sci. [Internet]. 2023 Mar. 20 [cited 2024 Apr. 14];60:e201873. Available from: https://www.revistas.usp.br/bjvras/article/view/201873