Document Type : Original Article

Authors

1 Multiple Sclerosis Research Center, Neuroscience Institute, Tehran University of Medical Sciences, Tehran, Iran

2 Department of Epidemiology, School of Health, Arak University of Medical Sciences, Arak, Iran Traditional and Complementary Medicine Research Center, Arak University of Medical Sciences, Arak, Iran

3 Department of Respiratory Medicine, Faculty of Medicine, Hokkaido University, Sapporo, Japan Center for Medical Education and International Relations, Faculty of Medicine, Hokkaido University, Sapporo, Japan

Abstract

Background: Multiple sclerosis (MS) is a chronic central nervous system disease, and primary progressive multiple sclerosis (PPMS) is one the main types of MS, which has unknown environmental risk factors.   The present study was conducted with the aim to identify the association of waterpipe and cigarette smoking, substance abuse, and alcohol consumption with the risk of PPMS development.
Methods: A population-based, case-control study was conducted in Tehran, Iran, on 146 PPMS cases and 294 controls. PPMS cases were diagnosed and confirmed by neurologists. Standard random digit dialing was used to select sex-matched healthy control participants from the same source population as the cases. Logistic regression analysis was used to estimate unadjusted and adjusted odds ratios (OR).
Results: In total, 440 subjects participated in the study. 
PPMS was associated with ever smoking cigarettes [OR = 2.48; confidence interval (CI) = 1.44-4.27], and passive smoking (OR = 2.20; CI = 1.34-3.62). However, having ever smoked waterpipe was not significantly associated with PPMS risk (OR = 1.19; CI = 0.62-2.26). Those who had all 3 types of smoking had an accumulative OR that was 10.45 times higher than that in individuals without any type of smoking (OR: 10.45; 95% CI = 3.5-31.2). We did not find any significant association between PPMS risk and substance abuse and alcohol consumption.
Conclusion: Cigarette smoking and being exposed to passive smoking are important risk factors for developing PPMS; in addition, the use of 3 types of smoking, showed an OR higher than that in those without any smoking. Considering the global increase in tobacco smoking, this finding emphasizes the importance of interventional programs for the prevention of tobacco smoking.

Keywords

  1. Mahad DH, Trapp BD, Lassmann H. Pathological mechanisms in progressive multiple sclerosis. Lancet Neurol 2015; 14(2): 183-93.
  2. Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, et al. Rising prevalence of multiple sclerosis worldwide: Insights from the Atlas of MS, third edition. Mult Scler 2020; 26(14): 1816-21.
  3. Nasiri M, Maroufi H, Sahraian MA, Eskandarieh S. Prevalence of multiple sclerosis and its risks in Tehran, Iran, in 2019. Neurol Sci 2021; 42(6): 2575-6.
  4. Eskandarieh S, Sahraian M. Epidemiological evidence of the recent surge in MS in Asia and Australia: A systematic review. J Kermanshah Univ Med Sci 2021; 25(2): e111028.
  5. Miller DH, Leary SM. Primary-progressive multiple sclerosis. Lancet Neurol 2007; 6(10): 903-12.
  6. Briggs FBS, Yu JC, Davis MF, Jiangyang J, Fu S, Parrotta E, et al. Multiple sclerosis risk factors contribute to onset heterogeneity. Mult Scler Relat Disord 2019; 28: 11-6.
  7. Eskandarieh S, Maroufi H, Mortazavi SH, Sahraian MA. Systematic Review of Environmental Risk Factors of Multiple Sclerosis in Middle East and North Africa Region. Multiple Sclerosis and Related Disorders 2020; 37: 101501.
  8. 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.
  9. Hedstrom AK, Bomfim IL, Barcellos LF, Briggs F, Schaefer C, Kockum I, et al. Interaction between passive smoking and two HLA genes with regard to multiple sclerosis risk. Int J Epidemiol 2014; 43(6): 1791-8.
  10. Hedstrom AK, Olsson T, Alfredsson L. Smoking is a major preventable risk factor for multiple sclerosis. Mult Scler 2016; 22(8): 1021-6.
  11. Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol 2018; 17(2): 162-73.
  12. Hernan MA, Jick SS, Logroscino G, Olek MJ, Ascherio A, Jick H. Cigarette smoking and the progression of multiple sclerosis. Brain 2005; 128(Pt 6): 1461-5.
  13. McKay KA, Kwan V, Duggan T, Tremlett H. Risk factors associated with the onset of relapsing-remitting and primary progressive multiple sclerosis: A systematic review. Biomed Res Int 2015; 2015: 817238.
  14. Drope J, Schluger NW. The tobacco atlas. Atlanta, GA: American Cancer Society; 2018.
  15. Cobb C, Ward KD, Maziak W, Shihadeh AL, Eissenberg T. Waterpipe tobacco smoking: an emerging health crisis in the United States. Am J Health Behav 2010; 34(3): 275-85.
  16. GBD 2017 Risk Factor Collaborators. Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks for 195 countries and territories, 1990-2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet 2018; 392(10159): 1923-94.
  17. Clagett B, Nathanson KL, Ciosek SL, McDermoth M, Vaughn DJ, Mitra N, et al. Comparison of address-based sampling and random-digit dialing methods for recruiting young men as controls in a case-control study of testicular cancer susceptibility. Am J Epidemiol 2013; 178(11): 1638-47.
  18. Rezaeimanesh N, Moghadasi AN, Sahraian MA, Eskandarieh S. Dietary risk factors of primary progressive multiple sclerosis: A population-based case-control study. Mult Scler Relat Disord 2021; 56: 103233.
  19. Kish L. A procedure for objective respondent selection within the household. J Am Stat Assoc 1949; 44(247): 380-7.
  20. Pugliatti M, Casetta I, Drulovic J, Granieri E, Holmoy T, Kampman MT, et al. A questionnaire for multinational case-control studies of environmental risk factors in multiple sclerosis (EnvIMS-Q). Acta Neurol Scand Suppl 2012; (195): 43-50.
  21. Sahraian MA, Naghshineh H, Shati M, Jahromi SR, Rezaei N. Persian adaptation of a questionnaire of environmental risk factors in multiple sclerosis (EnvIMS-Q). Mult Scler Relat Disord 2016; 10: 82-5.
  22. Rafiee F, Tarjoman T, Moghadasi AN, Sahraian MA, Azimi A, Rezaeimanesh N, et al. Stressful life events, socioeconomic status, and the risk of neuromyelitis optica spectrum disorder: A population-based case-control study. Mult Scler Relat Disord 2020; 46: 102544.
  23. Adler NE, Epel ES, Castellazzo G, Ickovics JR. Relationship of subjective and objective social status with psychological and physiological functioning: preliminary data in healthy white women. Health Psychol 2000; 19(6): 586-92.
  24. Dar NA, Bhat GA, Shah IA, Iqbal B, Makhdoomi MA, Nisar I, et al. Hookah smoking, nass chewing, and oesophageal squamous cell carcinoma in Kashmir, India. Br J Cancer 2012; 107(9): 1618-23.
  25. Hedstrom AK, Baarnhielm M, Olsson T, Alfredsson L. Exposure to environmental tobacco smoke is associated with increased risk for multiple sclerosis. Mult Scler 2011; 17(7): 788-93.
  26. Abdollahpour I, Nedjat S, Mansournia MA, Schuster T. Estimation of the marginal effect of regular drug use on multiple sclerosis in the Iranian population. PLoS One 2018; 13(4): e0196244.
  27. Alonso R, Quarracino C, Eizaguirre B, Cohen L, Silva B, Pita C, et al. Clinical and demographic characteristics of primary progressive multiple sclerosis in Argentina: Argentinean registry cohort study (RelevarEM). Neurol Sci 2020; 41(11): 3329-35.
  28. Abdollahpour I, Nedjat S, Mansournia MA, Sahraian MA, Asgari N. Parental ethnicity associated with risk for multiple sclerosis: A population-based incident case-control study in Iran. Mult Scler Relat Disord 2018; 20: 100-3.
  29. Hyarat SY, Subih M, Rayan A, Salami I, Harb A. Health related quality of life among patients with multiple sclerosis: The role of psychosocial adjustment to illness. Arch Psychiatr Nurs 2019; 33(1): 11-6.
  30. World Health Organization. TobReg Advisory Note: Waterpipe Tobacco Smoking: Health Effects, Research Needs and Recommended Actions by Regulators. Geneva, Switzerland: WHO; 2005.
  31. Morton J, Song Y, Fouad H, Awa FE, Abou El Naga R, Zhao L, et al. Cross-country comparison of waterpipe use: Nationally representative data from 13 low and middle-income countries from the Global Adult Tobacco Survey (GATS). Tob Control 2014; 23(5): 419-27.
  32. Alkhawajah NM, Aljarallah S, Hussain-Alkhateeb L, Almohaini MO, Muayqil TA. Waterpipe tobacco smoking and other multiple sclerosis environmental risk factors. Neuroepidemiology 2022; 56(2): 97-103.
  33. Abdollahpour I, Nedjat S, Almasi-Hashiani A, Nazemipour M, Mansournia MA, Luque-Fernandez MA. Estimating the marginal causal effect and potential impact of waterpipe smoking on risk of multiple sclerosis using the targeted maximum likelihood estimation method: A large, population-based incident case-control study. Am J Epidemiol 2021; 190(7): 1332-40.
  34. Sundstrom P, Nystrom L. Smoking worsens the prognosis in multiple sclerosis. Mult Scler 2008; 14(8): 1031-5.
  35. Lambert C, McCue J, Portas M, Ouyang Y, Li J, Rosano TG, et al. Acrolein in cigarette smoke inhibits T-cell responses. J Allergy Clin Immunol 2005; 116(4): 916-22.
  36. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol 2002; 2(5): 372-7.
  37. Rejdak K, Eikelenboom MJ, Petzold A, Thompson EJ, Stelmasiak Z, Lazeron RH, et al. CSF nitric oxide metabolites are associated with activity and progression of multiple sclerosis. Neurology 2004; 63(8): 1439-45.
  38. Eftekharian MM, Ghannad MS, Taheri M, Roshanaei G, Mazdeh M, Musavi M, et al. Frequency of viral infections and environmental factors in multiple sclerosis. Hum Antibodies 2016; 24(1-2): 17-23.
  39. Lee J, Taneja V, Vassallo R. Cigarette smoking and inflammation: cellular and molecular mechanisms. J Dent Res 2012; 91(2): 142-9.
  40. Seror R, Henry J, Gusto G, Aubin HJ, Boutron-Ruault MC, Mariette X. Passive smoking in childhood increases the risk of developing rheumatoid arthritis. Rheumatology (Oxford) 2019; 58(7): 1154-62.
  41. Kiyohara C, Washio M, Horiuchi T, Asami T, Ide S, Atsumi T, et al. Cigarette smoking, alcohol consumption, and risk of systemic lupus erythematosus: A case-control study in a Japanese population. J Rheumatol 2012; 39(7): 1363-70.
  42. Badihian N, Riahi R, Goli P, Badihian S, Poursafa P, Kelishadi R. Prenatal and perinatal factors associated with developing multiple sclerosis later in life: A systematic review and meta-analysis. Autoimmun Rev 2021; 20(6): 102823.
  43. Graves JS, Chitnis T, Weinstock-Guttman B, Rubin J, Zelikovitch AS, Nourbakhsh B, et al. Maternal and perinatal exposures are associated with risk for pediatric-onset multiple sclerosis. Pediatrics 2017; 139(4): e20162838.
  44. Abdollahpour I, Nedjat S, Mansournia MA, Sahraian MA, van der Mei I. Lifestyle factors and multiple sclerosis: A population-based incident case-control study. Mult Scler Relat Disord 2018; 22: 128-33.
  45. Hedstrom AK, Hillert J, Olsson T, Alfredsson L. Alcohol as a modifiable lifestyle factor affecting multiple sclerosis risk. JAMA Neurol 2014; 71(3): 300-5.