Disease relapses in multiple sclerosis can be influenced by air pollution and climate seasonal conditions

Slobodan Vojinović; Dejan Savić; Stevo Lukić; Ljiljana Savić; Jelena Vojinović

doi:10.2298/5372

Slobodan Vojinović Clinic for Neurology, Clinical Center, Niš, Serbia; Faculty of Medicine, University of Niš, Niš, Serbia
Dejan Savić Clinic for Neurology, Clinical Center, Niš, Serbia; Faculty of Medicine, University of Niš, Niš, Serbia
Stevo Lukić Clinic for Neurology, Clinical Center, Niš, Serbia; Faculty of Medicine, University of Niš, Niš, Serbia
Ljiljana Savić General Practice, Health Center Niš, Niš, Serbia.
Jelena Vojinović Faculty of Medicine, University of Niš, Niš, Serbia

DOI: https://doi.org/10.2298/5372

Keywords: multiple sclerosis, recurrence, air pollution, climate, sunlight, vitamin d,

Abstract

Background/Aim. Environmental factors may influence the disease activity in patients with relapsing-remitting multiple sclerosis (MS). The aim of this study was to evaluate the influence of air pollution and seasonal climate factors of any on number of relapses in MS patients during a consecutive 5 years of observation. Methods. We retrospectively analyzed data of MS patients from the town of Niš, hospitalized at the Clinic of Neurology, Clinical Center Niš, Serbia, from 2005 to 2009. Climate data: mean daily sun shining; mean monthly sun shining, mean whole daily cloudiness, daily cloudiness at 7 a.m, 2 p.m. and 9 p.m. and air pollution expressed by NSR (New Source Review) were obtained from the Meteorology Observatory Niš. Results. During a 5-year of observation there were 260 relapses in 101 MS patients. The number of relapses showed a significantly negative correlation with the number of days with NSR < 2 (ρ = -0.31; p < 0.01) and a positive correlation with the mean whole daily cloudiness (p < 0.05), mean daily cloudiness at 7 a.m. (p < 0.05) and 2 p.m. (p < 0.01). We found a significantlly positive correlation (p < 0.05) between the reduced number of relapses during the period of high vitamin D season, i.e. July–October. There was a statistically significant increase (p < 0.01) of the number of relapses during spring (ґ = 6.53; SD = 3.98) compared to the other three seasons. The joint presence of lower number of days with NSR < 2 during low vitamin D season (January–April) correlated with a statistically significant increase of the number of relapses in MS patients (F = 5.06, p < 0.01). Conclusion. The obtained results confirmed the influence of air pollution and climate seasonal conditions on disease relapses in MS patients based on a long-term observation. Lower numbers of days with low air pollution during the periods with low vitamin D (January–April), especially with increased cloudiness at 2 p.m, induce a higher risk of MS relapses in southern continental parts of Europe.

References

Ebers GC. Environmental factors and multiple sclerosis. Lan-cet Neurol 2008; 7(3): 268−77.

Gale CR, Martyn CN. Migrant studies in multiple sclerosis. Prog Neurobiol 1995; 47(4−5): 425−48.

Kurtzke JF. MS epidemiology worldwide. One view of current status. Acta Neurol Scand 1995; 91(Suppl 161): 23−33.

Acheson ED, Bachrach CA, Wright FM. Some comments on the relationship of the distribution of multiple sclerosis to latitude, solar radiation, and other variables. Acta Psychiatr Scand Suppl 1960; 35(147): 132−47.

Kampman MT, Wilsgaard T, Mellgren SI. Outdoor activities and diet in childhood and adolescence relate to MS risk above the Arctic Circle. J Neurol 2007; 254(4): 471−7.

Smolders J, Damoiseaux J, Menheere P, Hupperts R. Vitamin D as an immune modulator in multiple sclerosis, a review. J Neu-roimmunol 2008; 194(1−2): 7−17.

Dwyer T, van der Mei I, Ponsonby AL, Taylor BV, Stankovich J, Mckay JD, et al. Melanocortin 1 receptor genotype, past envi-ronmental sun exposure, and risk of multiple sclerosis. Neu-rology 2008; 71(3): 583−9.

Auer DP, Schumann EM, Kümpfel T, Gössl C, Trenkwalder C. Seasonal fluctuations of gadolinium-enhancing magnetic resonance imaging lesions in multiple sclerosis. Ann Neurol 2000; 47(2): 276−7.

Ogawa G, Mochizuki H, Kanzaki M, Kaida K, Motoyoshi K, Kama-kura K. Seasonal variation of multiple sclerosis exacerbations in Japan. Neurol Sci 2004; 24(6): 417−9.

Abella-Corral J, Prieto JM, Dapena-Bolaño D, Iglesias-Gómez S, Noya-García M, Lema M. Seasonal variations in the outbreaks in patients with multiple sclerosis. Rev Neurol 2005; 40(7): 394−6. (Spanish)

Tremlett H, van der Mei IA, Pittas F, Blizzard L, Paley G, Mesaros D, Ponsonby A. Monthly Ambient Sunlight, Infections and Re-lapse Rates in Multiple Sclerosis. Neuroepidemiology 2008; 31(4): 271−9.

Sayers A, Tilling K, Boucher BJ, Noonan K, Tobias JH. Predicting ambient ultraviolet from routine meteorological data; its po-tential use as an instrumental variable for vitamin D status in pregnancy in a longitudinal birth cohort in the UK. Int J Epi-demiol 2009; 38(6): 1681−8.

Soilu-Hänninen M, Airas L, Mononen I, Heikkilä A, Viljanen M, Hänninen A. 25-Hydroxyvitamin D levels in serum at the onset of multiple sclerosis. Mult Scler 2005; 11(3): 266−71.

Simpson S, Taylor B, Blizzard L, Ponsonby A, Pittas F, Tremlett H, van der Mei I. Higher 25-hydroxyvitamin D is associated with lower relapse risk in multiple sclerosis. Ann Neurol 2010; 68(2): 193−203.

Genc S, Zadeoglulari Z, Fuss HS, Genc K. The Adverse Effects of Air Pollution on the Nervous System. J Toxicol 2012; 2012: 782462.

Gregory A, Shendell DG, Okosun IS, Gieseker KE. Multiple Scle-rosis disease distribution and potential impact of environmen-tal air pollutants in Georgia. Sci Total Environ 2008; 396(1): 42−51.

Oikonen M, Laaksonen M, Laippala P, Oksaranta O, Lilius EM, Lindgren S, et al. Ambient air quality and occurrence of multiple sclerosis relapse. Neuroepidemiology 2003; 22(1): 95−9.

Fonseca AC, Costa J, Cordeiro C, Geraldes R, de Sá J. Influence of climatic factors in the incidence of multiple sclerosis relapses in a Portuguese population. Eur J Neurol 2009; 16(4): 537−9.

Guerrero-Peral AL, Carrasco-Cavia E, Diez-Gonzalez S, Fernandez MJ, Martin-Polo JM, Bueno-Rodriguez V. Seasonal analysis of out-breaks of multiple sclerosis and their relation to different climatologic variables. Rev Neurol 2005; 41(7): 446−8. (Span-ish)

O'Reilly MA, O'Reilly PM. Temporal Influences on Relapses of Multiple Sclerosis. Eur Neurol 1991; 31(6): 391−5.

Polman CH, Reingold SC, Edan G, Filippi M, Hartung H, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”. Ann Neurol 2005; 58(6): 840−6.

Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983; 33(11): 1444−52.

EPA New Source Review. Regulations and Standards. Availa-ble from: http://www.epa.gov/nsr/index.html

Bell GS, Peacock JL, Sander JW. Seasonality as a risk factor for sudden unexpected death in epilepsy: a study in a large cohort. Epilepsia 2010; 51(5): 773−6.

Shoben AB, Kestenbaum B, Levin G, Hoofnagle AN, Psaty BM, Sis-covick DS, et al. Seasonal Variation in 25-Hydroxyvitamin D Concentrations in the Cardiovascular Health Study. Am J Epi-demiol 2011; 174(12): 1363−72.

Kasahara AK, Singh RJ, Noymer A. Vitamin D (25OHD) Serum Seasonality in the United States. PloS One 2013; 8(6): e65785.

Vojinović S, Vojinovic J, Cosic V, Savic V. Effects of alfacalcidol therapy on serum cytokine levels in patients with multiple sclerosis. Srp Arh Celok Lek 2005; 133(Suppl 2): 124−8. (Serbian)

Pedersen LB, Nashold FE, Spach KM, Hayes CE. 1,25-dihydroxyvitamin D3 reverses experimental autoimmune en-cephalomyelitis by inhibiting chemokine synthesis and mono-cyte trafficking. J Neurosci Res 2007; 85(11): 2480−90.

Raghuwanshi A, Joshi SS, Christakos S. Vitamin D and multiple sclerosis. J Cell Bioch 2008; 105(2): 338−43.

Correale J, Ysrraelit MC, Gaitán MI. Immunomodulatory effects of Vitamin D in multiple sclerosis. Brain 2009; 132(Pt 5): 1146−60.

Gillie O. A new government policy is needed for sunlight and vitamin D. Br J Dermatol 2006; 154(5): 1052−61.

Becklund BR, Severson KS, Vang SV, DeLuca HF. UV radiation suppresses experimental autoimmune encephalomyelitis inde-pendent of vitamin D production. Proc Natl Acad Sci U S A 2010; 107(14): 6418−23.

Koepke P. Radiative models for the evaluation of the UV radia-tion at the ground. Radiat Prot Dosimetry 2009; 137(3−4): 188−92.

Feister U, Laschewski G, Grewe R. UV index forecasts and mea-surements of health-effective radiation. J Photochem Photo-biol B 2011; 102(1): 55−68.

Turnbull DJ, Parisi AV, Schouten PW. Empirical evaluation of global vitamin D effective ultraviolet irradiances under cloudy conditions for a subtropical southern hemisphere site. Radiat Res 2010; 173(5): 703−8.

Bamford CR, Sibley WA, Thies C. Seasonal variation of multiple sclerosis exacerbations in Arizona. Neurology 1983; 33(6): 697−701.

Wuthrich R, Rieder HP. The Seasonal Incidence of Multiple Sclerosis in Switzerland. Eur Neurol 1970; 3(5): 257−64.

Koziol JA, Feng AC. Seasonal variations in exacerbations and MRI parameters in relapsing-remitting multiple sclerosis. Neu-roepidemiology 2004; 23(5): 217−23.

Tataru N, Vidal C, Decavel P, Berger E, Rumbach L. Limited im-pact of the summer heat wave in France (2003) on hospital admissions and relapses for multiple sclerosis. Neuroepidemi-ology 2006; 27(1): 28−32.

Embry AF, Snowdon LR, Veith R. Vitamin D and Seasonal Fluc-tuations of Gadolinium-Enhancing Magnetic Resonance Imaging Lesions in Multiple Sclerosis. Ann Neurol 2000; 48(2): 271−2.

Szodoray P, Nakken B, Gaal J, Jonsson R, Szegedi A, Zold E, Bodolay E. The Complex Role of Vitamin D in Autoimmune Diseases. Scand J Immunol 2008; 68(3): 261−9.