Cognitive impairment in multiple sclerosis: An exploratory analysis of environmental and lifestyle risk factors
Autoři:
Maria Pia Amato aff001; Elio Prestipino aff001; Angelo Bellinvia aff001; Claudia Niccolai aff001; Lorenzo Razzolini aff001; Luisa Pastò aff003; Roberto Fratangelo aff001; Laura Tudisco aff001; Mattia Fonderico aff001; Paolo Luca Mattiolo aff001; Benedetta Goretti aff001; Giovanni Bosco Zimatore aff004; Nunzia Alessandra Losignore aff004; Emilio Portaccio aff005; Francesco Lolli aff001
Působiště autorů:
Department NEUROFARBA, Section of Neurosciences, University of Florence, Florence, Italy
aff001; IRCCS Fondazione Don Carlo Gnocchi, Florence, Italy
aff002; SOD Neurological Rehabilitation, Careggi University Hospital, Florence, Italy
aff003; Operative Unit of Neurology, Dimiccoli General Hospital, Barletta, Italy
aff004; SOC Neurology, San Giovanni di Dio Hospital, Florence, Italy
aff005
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0222929
Souhrn
Background
Many potentially modifiable risk factors for MS are investigated. It is not known, however, if these factors also apply to MS-related cognitive impairment (CI), a frequent consequence of MS.
Objective
The aim of our study was to assess risk factors for CI in MS patients, focusing on environmental exposures, lifestyle and comorbidities.
Methods
We included MS patients referring to MS Centers in Florence and Barletta between 2014 and 2017. Neuropsychological performance was assessed through the Rao’s battery and Stroop test, cognitive reserve (premorbid intelligence quotient–IQ) was evaluated using the National Adult Reading Test (NART). Potential risk factors were investigated through a semi-structured questionnaire.
Results
150 patients were included. CI was detected in 45 (30%) subjects and was associated with older age (p<0.005), older age at MS onset (p = 0.016), higher EDSS score (p<0.005), progressive disease course (p = 0.048) and lower premorbid IQ score (p<0.005). As for risk factors, CI was related with lower physical activity in childhood-adolescence (p<0.005). In women, hormonal therapy resulted to be protective against CI (p = 0.041). However, in the multivariable analysis, the only significant predictors of CI were older age (p<0.05; OR 1.06, 95% CI 1.02–1.10) and lower premorbid IQ (p<0.05; OR 0.93, 95% CI: 0.88–0.98). Removing IQ from the model, CI was associated with higher EDSS (p = 0.030; OR 1.25, 95% CI 1.02–1.53) and, marginally, previous physical activity (p = 0.066; OR 0.49, 95% CI: 0.23–1.05)
Conclusions
Our findings suggest that physical activity in childhood-adolescence could be a contributor to cognitive reserve building, thus representing a potential protective factors for MS-related CI susceptible to preventive strategies.
Klíčová slova:
Cannabis – Cognitive impairment – Hormonal therapy – Medical risk factors – Multiple sclerosis – Neuropsychological testing – Neuropsychology – Physical activity
Zdroje
1. Filippi M, Bar- A, Piehl F, Preziosa P, Solari A, Vukusic S, et al. Multiple Sclerosis. Nat Rev Dis Prim. 2018;4: 1–27. doi: 10.1038/s41572-018-0001-z
2. Amato MP, Derfuss T, Hemmer B, Liblau R, Montalban X, Soelberg Sørensen P, et al. Environmental modifiable risk factors for multiple sclerosis: Report from the 2016 ECTRIMS focused workshop. Multiple Sclerosis Journal. 2018. doi: 10.1177/1352458516686847 28671487
3. Sumowski JF, Benedict R, Enzinger C, Filippi M, Geurts JJ, Hamalainen P, et al. Cognition in multiple sclerosis: State of the field and priorities for the future. Neurology. 2018;90: 278–288. doi: 10.1212/WNL.0000000000004977 29343470
4. Fenu G, Fronza M, Lorefice L, Arru M, Coghe G, Frau J, et al. Performance in daily activities, cognitive impairment and perception in multiple sclerosis patients and their caregivers. BMC Neurol. 2018; doi: 10.1186/s12883-018-1224-z 30567519
5. Amato MP, Zipoli V, Portaccio E. Multiple sclerosis-related cognitive changes: A review of cross-sectional and longitudinal studies. J Neurol Sci. 2006; doi: 10.1016/j.jns.2005.08.019 16643953
6. Goretti B, Portaccio E, Zipoli V, Hakiki B, Siracusa G, Sorbi S, et al. Coping strategies, psychological variables and their relationship with quality of life in multiple sclerosis. Neurol Sci. 2009; doi: 10.1007/s10072-008-0009-3 19153648
7. Lublin FD, Reingold SC, Cohen JA, Cutter GR, Sørensen PS, Thompson AJ, et al. Defining the clinical course of multiple sclerosis: The 2013 revisions. Neurology. 2014. doi: 10.1212/WNL.0000000000000560 24871874
8. Trojano M, Bergamaschi R, Amato MP, Comi G, Ghezzi A, Lepore V, et al. The Italian multiple sclerosis register. Neurol Sci. 2019; doi: 10.1007/s10072-018-3610-0 30426289
9. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology. 1983; doi: 10.1212/WNL.33.11.1444 6685237
10. Rao SM and the CFSG of the NMSS. A manual for brief repeatable battery of the neuropsychological tests in multiple sclerosis. Medical College of Wisconsin, Milwaukee, WI.; 1990.
11. Stroop JR. Studies of interference in serial verbal reactions. J Exp Psychol. 1935; doi: 10.1037/h0054651
12. Amato MP, Portaccio E, Goretti B, Zipoli V, Ricchiuti L, De Caro MF, et al. The Rao’s Brief Repeatable Battery and Stroop test: normative values with age, education and gender corrections in an Italian population. Mult Scler J. 2006;12: 787–793. doi: 10.1177/1352458506070933 17263008
13. Amato MP, Goretti B, Ghezzi A, Lori S, Zipoli V, Portaccio E, et al. Cognitive and psychosocial features of childhood and juvenile MS. Neurology. 2008; doi: 10.1212/01.wnl.0000312276.23177.fa 18474844
14. Amato MP, Goretti B, Ghezzi A, Lori S, Zipoli V, Moiola L, et al. Cognitive and psychosocial features in childhood and juvenile MS: Two-year follow-up. Neurology. 2010; doi: 10.1212/WNL.0b013e3181f4d821 20876467
15. Amato MP, Goretti B, Ghezzi A, Hakiki B, Niccolai C, Lori S, et al. Neuropsychological features in childhood and juvenile multiple sclerosis: Five-year follow-up. Neurology. 2014; doi: 10.1212/WNL.0000000000000885 25217060
16. Colombo L, Sartori G, Brivio C. Stima del quoziente intellettivo tramite l’applicazione del TIB (test breve di intelligenza). G Ital di Psicol. 2002;
17. Sumowski JF, Wylie GR, Gonnella A, Chiaravalloti N, Deluca J. Premorbid cognitive leisure independently contributes to cognitive reserve in multiple sclerosis. Neurology. 2010; doi: 10.1212/WNL.0b013e3181f881a6 20956787
18. Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979; doi: 10.1192/bjp.134.4.382 444788
19. Krupp LB, Larocca NG, Muir Nash J, Steinberg AD. The fatigue severity scale: Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol. 1989; doi: 10.1001/archneur.1989.00520460115022 2803071
20. Craig Marshall A. L., Sjöström M., Bauman A. E., Booth M. L., Ainsworth B. E., et al. CL. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;
21. Williams B, Mancia G, Spiering W, Rosei EA, Azizi M, Burnier M, et al. 2018 practice guidelines for the management of arterial hypertension of the European society of cardiology and the European society of hypertension ESC/ESH task force for the management of arterial hypertension. Journal of Hypertension. 2018. doi: 10.1097/HJH.0000000000001961 30379783
22. Ruano L, Portaccio E, Goretti B, Niccolai C, Severo M, Patti F, et al. Age and disability drive cognitive impairment in multiple sclerosis across disease subtypes. Mult Scler. 2017;23: 1258–1267. doi: 10.1177/1352458516674367 27738090
23. Benedict RHB, Zivadinov R. Risk factors for and management of cognitive dysfunction in multiple sclerosis. Nat Rev Neurol. 2011;7: 332–342. doi: 10.1038/nrneurol.2011.61 21556031
24. Patti F, Amato MP, Trojano M, Bastianello S, Tola MR, Goretti B, et al. Cognitive impairment and its relation with disease measures in mildly disabled patients with relapsing-remitting multiple sclerosis: baseline results from the Cognitive Impairment in Multiple Sclerosis ({COGIMUS}) study. Mult Scler. 2009;15: 779–788. doi: 10.1177/1352458509105544 19542262
25. Rocca MA, Amato MP, De Stefano N, Enzinger C, Geurts JJ, Penner I-K, et al. Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol. 2015;14: 302–317. doi: 10.1016/S1474-4422(14)70250-9 25662900
26. Amato MP, Ponziani G, Siracusa G, Sorbi S. Cognitive dysfunction in early-onset multiple sclerosis: A reappraisal after 10 years. Arch Neurol. 2001; doi: 10.1001/archneur.58.10.1602 11594918
27. Amato MP, Langdon D, Montalban X, Benedict RHB, DeLuca J, Krupp LB, et al. Treatment of cognitive impairment in multiple sclerosis: position paper. J Neurol. 2013;260: 1452–1468. doi: 10.1007/s00415-012-6678-0 23180174
28. Marrie RA, Horwitz RI. Emerging effects of comorbidities on multiple sclerosis. The Lancet Neurology. 2010. doi: 10.1016/S1474-4422(10)70135-6
29. Kappus N, Weinstock-Guttman B, Hagemeier J, Kennedy C, Melia R, Carl E, et al. Cardiovascular risk factors are associated with increased lesion burden and brain atrophy in multiple sclerosis. J Neurol Neurosurg Psychiatry. 2016; doi: 10.1136/jnnp-2014-310051 25722366
30. Vňuková M, Ptáček R, Raboch J, Stefano GB. Decreased Central Nervous System Grey Matter Volume (GMV) in Smokers Affects Cognitive Abilities: A Systematic Review. Med Sci Monit. 2017; doi: 10.12659/MSM.901870
31. Zivadinov R, Weinstock-Guttman B, Hashmi K, Abdelrahman N, Stosic M, Dwyer M, et al. Smoking is associated with increased lesion volumes and brain atrophy in multiple sclerosis. Neurology. 2009; doi: 10.1212/WNL.0b013e3181b2a706 19687451
32. Ozcan ME, Asil T, Ince B, Bingol A, Erturk S, Altinoz MA, et al. Association between smoking and cognitive impairment in multiple sclerosis. Neuropsychiatr Dis Treat. 2014;10: 1715. doi: 10.2147/NDT.S68389 25246792
33. Honarmand K, Tierney MC, O’Connor P, Feinstein A. Effects of cannabis on cognitive function in patients with multiple sclerosis. Neurology. 2011; doi: 10.1212/WNL.0b013e318212ab0c 21444900
34. Pavisian B, MacIntosh BJ, Szilagyi G, Staines RW, O’Connor P, Feinstein A. Effects of cannabis on cognition in patients with MS: A psychometric and MRI study. Neurology. 2014; doi: 10.1212/WNL.0000000000000446 24789863
35. Topiwala A, Ebmeier KP. Effects of drinking on late-life brain and cognition. Evid Based Ment Heal. 2018;21: 12–15. doi: 10.1136/eb-2017-102820 29273599
36. Sumowski JF, Leavitt VM. Cognitive reserve in multiple sclerosis. Multiple Sclerosis Journal. 2013. doi: 10.1177/1352458513498834 23897894
37. Amato MP, Razzolini L, Goretti B, Stromillo ML, Rossi F, Giorgio A, et al. Cognitive reserve and cortical atrophy in multiple sclerosis: A longitudinal study. Neurology. 2013; doi: 10.1212/WNL.0b013e3182918c6f 23576622
38. De Giglio L, Marinelli F, Barletta VT, Pagano VA, De Angelis F, Fanelli F, et al. Effect on Cognition of Estroprogestins Combined with Interferon Beta in Multiple Sclerosis: Analysis of Secondary Outcomes from a Randomised Controlled Trial. CNS Drugs. 2017; doi: 10.1007/s40263-016-0401-0 27995531
39. Krug R, Born J, Rasch B. A 3-day estrogen treatment improves prefrontal cortex-dependent cognitive function in postmenopausal women. Psychoneuroendocrinology. 2006; doi: 10.1016/j.psyneuen.2006.05.007 16831520
40. Krug R, Mölle M, Dodt C, Fehm HL, Born J. Acute influences of estrogen and testosterone on divergent and convergent thinking in postmenopausal women. Neuropsychopharmacology. 2003; doi: 10.1038/sj.npp.1300200 12784108
41. Linzmayer L, Semlitsch H V., Saletu B, Böck G, Saletu-Zyhlarz G, Zoghlami A, et al. Double-blind, placebo-controlled psychometric studies on the effects of a combined estrogen-progestin regimen versus estrogen alone on performance, mood and personality of menopausal syndrome patients. Arzneimittelforschung. 2001; doi: 10.1055/s-0031-1300030 11304940
42. Shaywitz SE, Naftolin F, Zelterman D, Marchione KE, Holahan JM, Palter SF, et al. Better oral reading and short-term memory in midlife, postmenopausal women taking estrogen. Menopause. 2003; doi: 10.1097/01.GME.0000060241.02837.29 14501603
43. Sherwin BB, Henry JF. Brain aging modulates the neuroprotective effects of estrogen on selective aspects of cognition in women: A critical review. Frontiers in Neuroendocrinology. 2008. doi: 10.1016/j.yfrne.2007.08.002 17980408
44. Hogervorst E, Yaffe K, Richards M, Huppert F. Hormone replacement therapy for cognitive function in postmenopausal women [Systematic Review]. Cochrane Database Syst Rev. 2005;
45. Gibbs RB. Estrogen therapy and cognition: A review of the cholinergic hypothesis. Endocrine Reviews. 2010. doi: 10.1210/er.2009-0036 20019127
46. Suijo K, Inoue S, Ohya Y, Odagiri Y, Takamiya T, Ishibashi H, et al. Resistance exercise enhances cognitive function in mouse. Int J Sports Med. 2013; doi: 10.1055/s-0032-1323747 23041964
47. Erickson KI, Hillman CH, Kramer AF. Physical activity, brain, and cognition. Current Opinion in Behavioral Sciences. 2015. doi: 10.1016/j.cobeha.2015.01.005
48. Pereira AC, Huddleston DE, Small SA, Sosunov AA, Gage FH, Brown TR, et al. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci. 2007; doi: 10.1073/pnas.0611721104 17374720
49. Motl RW, Sandroff BM, DeLuca J. Exercise Training and Cognitive Rehabilitation: A Symbiotic Approach for Rehabilitating Walking and Cognitive Functions in Multiple Sclerosis? Neurorehabil Neural Repair. 2016; doi: 10.1177/1545968315606993 27261483
50. Mavrovouniotis F. Inactivity in Childhood and Adolescence: A Modern Lifestyle Associated with Adverse Health Consequences. Sport Sci Rev. 2012; doi: 10.2478/v10237-012-0011-9
51. Wesnes K, Myhr KM, Riise T, Cortese M, Pugliatti M, Boström I, et al. Physical activity is associated with a decreased multiple sclerosis risk: The EnvIMS study. Mult Scler. 2018; doi: 10.1177/1352458517694088 28273774
52. McLellan TM, Caldwell JA, Lieberman HR. A review of caffeine’s effects on cognitive, physical and occupational performance. Neuroscience and Biobehavioral Reviews. 2016. doi: 10.1016/j.neubiorev.2016.09.001 27612937
53. Darwish H, Haddad R, Osman S, Ghassan S, Yamout B, Tamim H, et al. Effect of Vitamin D Replacement on Cognition in Multiple Sclerosis Patients. Sci Rep. 2017; doi: 10.1038/srep45926 28374837
54. Attia JR, Oldmeadow C, Holliday EG, Jones MP. Deconfounding confounding part 2: using directed acyclic graphs (DAGs). Med J Aust. 2017; doi: 10.5694/mja16.01167 28918727
55. Williamson EJ, Aitken Z, Lawrie J, Dharmage SC, Burgess JA, Forbes AB. Introduction to causal diagrams for confounder selection. Respirology. 2014. doi: 10.1111/resp.12238 24447391
56. Zivadinov R, Weinstock-Guttman B, Benedict R, Tamaño-Blanco M, Hussein S, Abdelrahman N, et al. Preservation of gray matter volume in multiple sclerosis patients with the Met allele of the rs6265 (Val66Met) SNP of brain-derived neurotrophic factor. Hum Mol Genet. 2007; doi: 10.1093/hmg/ddm189 17656372
Článek vyšel v časopise
PLOS One
2019 Číslo 10
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Je libo čepici místo mozkového implantátu?
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
- AI může chirurgům poskytnout cenná data i zpětnou vazbu v reálném čase
- Nová metoda odlišení nádorové tkáně může zpřesnit resekci glioblastomů
Nejčtenější v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy