Association of cigarette smoking with neuromyelitis optica-immunoglobulin G sero-positivity in neuromyelitis optica spectrum disorder
Background: Neuromyelitis optica spectrum disorder (NMOSD) is a neuroinflammatory demyelinating disease caused by the presence of a highly specific serum autoantibody marker, NMO-immunoglobulin G (NMO-IgG), that reacts against the water channel aquaporin-4 (AQP4). The present study examined the association between NMO-IgG sero-positivity and environmental factors such as cigarette smoking.
Methods: A cross-sectional study was conducted in Sina Hospital, a tertiary referral center in Tehran, Iran. All the patients with a definite diagnosis of NMOSD were involved in this study. The enzyme-linked immunosorbent assay (ELISA) was used to examine the AQP4-IgG status. To assess the association between NMO-IgG sero-positivity and cigarette smoking, a researcher-made questionnaire covering patients’ lifestyle information on smoking habits was designed and administered using the structured face-to-face interviews with the patients.
Results: The positive and negative NMO-IgG results were found in 44 (46.8%) and 50 (53.2%) patients, respectively. The increased NMO-IgG sero-positivity odds were observed among the lifetime smokers [odds ratio (OR) = 3.24, 95% confidence interval (CI): 1.16-9.08], current smokers (OR = 6.08, 95% CI: 1.26-29.39), and passive smokers (OR = 2.22, 95% CI: 1.10-4.50).
Conclusion: Lifetime and current smoking as well as passive smoking can be regarded as risk factors for NMO-IgG sero-positivity. Smoking with its immunological effects can lead to the production of autoantibodies such as NMO-IgG.
2. Eskandarieh S, Nedjat S, Azimi AR, Moghadasi AN, Sahraian MA. Neuromyelitis optica spectrum disorders in Iran. Mult Scler Relat Disord 2017; 18: 209-12.
3. Eskandarieh S, Nedjat S, Abdollahpour I, Azimi AR, Moghadasi AN, Asgari N, et al. Environmental risk factors in neuromyelitis optica spectrum disorder: A case-control study. Acta Neurol Belg 2018; 118(2): 277-87.
4. Costenbader KH, Karlson EW. Cigarette smoking and autoimmune disease: What can we learn from epidemiology? Lupus 2006; 15(11): 737-45.
5. Lee J, Taneja V, Vassallo R. Cigarette smoking and inflammation: Cellular and molecular mechanisms. J Dent Res 2012; 91(2): 142-9.
6. Bauer M, Fink B, Thurmann L, Eszlinger M, Herberth G, Lehmann I. Tobacco smoking differently influences cell types of the innate and adaptive immune system-indications from CpG site methylation. Clin Epigenetics 2016; 7: 83.
7. Hutchinson D, Shepstone L, Moots R, Lear JT, Lynch MP. Heavy cigarette smoking is strongly associated with rheumatoid arthritis (RA), particularly in patients without a family history of RA. Ann Rheum Dis 2001; 60(3): 223-7.
8. Ekblom-Kullberg S, Kautiainen H, Alha P, Leirisalo-Repo M, Julkunen H. Smoking and the risk of systemic lupus erythematosus. Clin Rheumatol 2013; 32(8): 1219-22.
9. Abdollahpour I, Nedjat S, Sahraian MA, Mansournia MA, Otahal P, van der Mei I. Waterpipe smoking associated with multiple sclerosis: A population-based incident case-control study. Mult Scler 2017; 23(10): 1328-35.
10. Bufalo NE, Santos RB, Cury AN, Andrade RA, Morari J, Morari EC, et al. Genetic polymorphisms associated with cigarette smoking and the risk of Graves' disease. Clin Endocrinol (Oxf) 2008; 68(6): 982-7.
11. Ruiz-Gaviria R, Baracaldo I, Castaneda C, Ruiz-Patino A, Acosta-Hernandez A, Rosselli D. Specificity and sensitivity of aquaporin 4 antibody detection tests in patients with neuromyelitis optica: A meta-analysis. Mult Scler Relat Disord 2015; 4(4): 345-9.
12. Eskandarieh S, Nedjat S, Abdollahpour I, Moghadasi AN, Azimi AR, Sahraian MA. Comparing epidemiology and baseline characteristic of multiple sclerosis and neuromyelitis optica: A case-control study. Mult Scler Relat Disord 2017; 12: 39-43.
13. Jarius S, Paul F, Aktas O, Asgari N, Dale RC, de SJ, et al. MOG encephalomyelitis: international recommendations on diagnosis and antibody testing. Nervenarzt 2018; 89(12): 1388-99. [In German].
14. Waters P, Reindl M, Saiz A, Schanda K, Tuller F, Kral V, et al. Multicentre comparison of a diagnostic assay: aquaporin-4 antibodies in neuromyelitis optica. J Neurol Neurosurg Psychiatry 2016; 87(9): 1005-15.
15. Chanson JB, de Seze J, Eliaou JF, Vincent T. Immunological follow-up of patients with neuromyelitis optica: is there a good biomarker? Lupus 2013; 22(3): 229-32.
16. Hinson SR, McKeon A, Fryer JP, Apiwattanakul M, Lennon VA, Pittock SJ. Prediction of neuromyelitis optica attack severity by quantitation of complement-mediated injury to aquaporin-4-expressing cells. Arch Neurol 2009; 66(9): 1164-7.
17. Lin N, Liu Q, Wang X, Ma J, Li Y. Role of AQP4 antibody serostatus and its prediction of visual outcome in neuromyelitis optica: A systematic review and meta-analysis. Protein Pept Lett 2017; 24(3): 245-52.
18. Heydarpour P, Manouchehrinia A, Beiki O, Mousavi SE, Abdolalizadeh A, Lakeh MM, et al. Smoking and worsening disability in multiple sclerosis: A meta-analysis. Acta Neurol Scand 2018; 138(1): 62-9.
19. Briggs FB, Gunzler DD, Ontaneda D, Marrie RA. Smokers with MS have greater decrements in quality of life and disability than non-smokers. Mult Scler 2017; 23(13): 1772-81.
20. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol 2002; 2(5): 372-7.
21. Piao WH, Campagnolo D, Dayao C, Lukas RJ, Wu J, Shi FD. Nicotine and inflammatory neurological disorders. Acta Pharmacol Sin 2009; 30(6): 715-22.
22. Vargas-Rojas MI, Ramirez-Venegas A, Limon-Camacho L, Ochoa L, Hernandez-Zenteno R, Sansores RH. Increase of Th17 cells in peripheral blood of patients with chronic obstructive pulmonary disease. Respir Med 2011; 105(11): 1648-54.
23. Galitovskiy V, Qian J, Chernyavsky AI, Marchenko S, Gindi V, Edwards RA, et al. Cytokine-induced alterations of alpha7 nicotinic receptor in colonic CD4 T cells mediate dichotomous response to nicotine in murine models of Th1/Th17- versus Th2-mediated colitis. J Immunol 2011; 187(5): 2677-87.
24. Chen G, Zhou M, Chen L, Meng ZJ, Xiong XZ, Liu HJ, et al. Cigarette smoke disturbs the survival of CD8+ Tc/Tregs partially through muscarinic receptors-dependent mechanisms in chronic obstructive pulmonary disease. PLoS One 2016; 11(1): e0147232.
25. Qiu F, Liang CL, Liu H, Zeng YQ, Hou S, Huang S, et al. Impacts of cigarette smoking on immune responsiveness: Up and down or upside down? Oncotarget 2017; 8(1): 268-84.
26. Fatemi K, Radvar M, Rezaee A, Rafatpanah H, Azangoo kH, Dadpour Y, et al. Comparison of relative TLR-2 and TLR-4 expression level of disease and healthy gingival tissue of smoking and non-smoking patients and periodontally healthy control patients. Aust Dent J 2013; 58(3): 315-20.
27. Mysikova D, Adkins I, Hradilova N, Palata O, Simonek J, Pozniak J, et al. Case-control study: Smoking history affects the production of tumor antigen-specific antibodies NY-ESO-1 in patients with lung cancer in comparison with cancer disease-free group. J Thorac Oncol 2017; 12(2): 249-57.
28. Ikeshima-Kataoka H. Neuroimmunological Implications of AQP4 in Astrocytes. Int J Mol Sci 2016; 17(8): E1306.
29. Lucchinetti CF, Guo Y, Popescu BF, Fujihara K, Itoyama Y, Misu T. The pathology of an autoimmune astrocytopathy: Lessons learned from neuromyelitis optica. Brain Pathol 2014; 24(1): 83-97.
30. Lee SB, Kim JH, Cho MH, Choe ES, Kim KS, Shim SM. Impact of commercial cigarette smoke condensate on brain tissue co-cultured with astrocytes and blood-brain barrier endothelial cells. J Toxicol Environ Health A 2017; 80(10-12): 533-41.
31. Suzuki H, Oku H, Horie T, Morishita S, Tonari M, Oku K, et al. Changes in expression of aquaporin-4 and aquaporin-9 in optic nerve after crushing in rats. PLoS One 2014; 9(12): e114694.