DOI QR코드

DOI QR Code

Association Between the Risk of Multiple Sclerosis and Dietary Proinflammatory/Anti-Inflammatory Food Intake and Dietary Diversity: A Case-Control Study

  • Alireza Hatami (Department of Nutrition, School of Medicine, Mashhad University of Medical Sciences) ;
  • Maryam Ahmadi-khorram (Department of Nutrition, School of Medicine, Mashhad University of Medical Sciences) ;
  • Fatemeh Keykhaei (Department of Nutrition, School of Medicine, Mashhad University of Medical Sciences) ;
  • Ali Jafarzadeh Esfehani (Metabolic Syndrome Research Center, Mashhad University of Medical Sciences) ;
  • Mohsen Nematy (Department of Nutrition, School of Medicine, Mashhad University of Medical Sciences)
  • 투고 : 2023.11.22
  • 심사 : 2024.01.31
  • 발행 : 2024.01.31

초록

A diet rich in proinflammatory components and inflammation are suggested to be significant risk factors for multiple sclerosis (MS). This study aimed to investigate the association between the risk of MS and the inflammatory potential of an individual's diet and dietary diversity through pro-inflammatory/anti-inflammatory food intake score (PAIFIS) and dietary diversity score (DDS). In a hospital-based case-control study, 397 participants, including 197 patients with MS and 200 healthy participants aged over 18 years, were evaluated. The history of smoking, dietary intake, and anthropometric characteristics, including body mass index, waist circumference, total body fat, and fat-free mass were assessed. A validated 160-item semiquantitative food frequency questionnaire was used to calculate the PAIFIS and DDS scores. The mean age of the participants was 32.45 ± 8.66 years, and most were females (274, 79.4%). The PAIFIS score was significantly higher among MS patients than healthy participants (p = 0.001). Between PAIFIS and DDS, only PAFIS was significantly related to MS risk (odds ratio, 1.002; 95% confidence interval, 1.001-1.004; p = 0.001). PAIFIS, as an index of dietary inflammation, can predict MS. Further studies are needed to document these findings.

키워드

과제정보

The authors would like to thank the participation of all individuals for their assistance in this research project.

참고문헌

  1. Dobson R, Giovannoni G. Multiple sclerosis - a review. Eur J Neurol 2019;26:27-40. https://doi.org/10.1111/ene.13819
  2. Keykhaei F, Norouzy S, Froughipour M, Nematy M, Saeidi M, Jarahi L, Amiri F, Malek Ahmadi M, Norouzy A. Adherence to healthy dietary pattern is associated with lower risk of multiple sclerosis. J Cent Nerv Syst Dis 2022;14:11795735221092516.
  3. Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, Robertson N, La Rocca N, Uitdehaag B, van der Mei I, Wallin M, Helme A, Angood Napier C, Rijke N, Baneke P. Rising prevalence of multiple sclerosis worldwide: insights from the atlas of MS, third edition. Mult Scler 2020;26:1816-21. https://doi.org/10.1177/1352458520970841
  4. Bagheri M, Maghsoudi Z, Fayazi S, Elahi N, Tabesh H, Majdinasab N. Several food items and multiple sclerosis: a case-control study in Ahvaz (Iran). Iran J Nurs Midwifery Res 2014;19:659-65.
  5. Saul AM, Taylor BV, Blizzard L, Simpson-Yap S, Oddy WH, Shivappa N, Hebert JR, Black LJ, Ponsonby AL, Broadley SA, Lechner-Scott J, van der Mei I, Lucas RM, Dear K, Dwyer T, Broadley S, Kilpatrick T, Williams D, Shaw C, Chapman C, Coulthard A, Pender MP, Valery P; Ausimmune/AusLong Investigators. A pro-inflammatory diet in people with multiple sclerosis is associated with an increased rate of relapse and increased FLAIR lesion volume on MRI in early multiple sclerosis: a prospective cohort study. Mult Scler 2023;29:1012-23. https://doi.org/10.1177/13524585231167739
  6. Jahromi SR, Toghae M, Jahromi MJ, Aloosh M. Dietary pattern and risk of multiple sclerosis. Iran J Neurol 2012;11:47-53.
  7. Stoiloudis P, Kesidou E, Bakirtzis C, Sintila SA, Konstantinidou N, Boziki M, Grigoriadis N. The role of diet and interventions on multiple sclerosis: a review. Nutrients 2022;14:1150.
  8. da Costa Silva BY, de Carvalho Sampaio HA, Shivappa N, Hebert JR, da Silva Albuquerque L, Carioca AA, D'Almeida JA, Maia CS, de Melo ML. Dietary inflammatory index and clinical course of multiple sclerosis. Eur J Clin Nutr 2019;73:979-88. https://doi.org/10.1038/s41430-018-0294-8
  9. Azevedo-Garcia LG, Torres-Leal FL, Aristizabal JC, Berg G, Carvalho HB, De Moraes AC. Reliability and validity estimate of the pro-inflammatory/anti-inflammatory food intake score in South American pediatric population: SAYCARE study. Int J Environ Res Public Health 2023;20:1038.
  10. Saghafi-Asl M, Mirmajidi S, Asghari Jafarabadi M, Vahid F, Shivappa N, Hebert JR, Ebrahimzadeh Attari V. The association of dietary patterns with dietary inflammatory index, systemic inflammation, and insulin resistance, in apparently healthy individuals with obesity. Sci Rep 2021;11:7515.
  11. Lucas M, Chocano-Bedoya P, Schulze MB, Mirzaei F, O'Reilly EJ, Okereke OI, Hu FB, Willett WC, Ascherio A. Inflammatory dietary pattern and risk of depression among women. Brain Behav Immun 2014;36:46-53. https://doi.org/10.1016/j.bbi.2013.09.014
  12. Barbaresko J, Koch M, Schulze MB, Nothlings U. Dietary pattern analysis and biomarkers of low-grade inflammation: a systematic literature review. Nutr Rev 2013;71:511-27. https://doi.org/10.1111/nure.12035
  13. Khosravi-Largani M, Pourvali-Talatappeh P, Rousta AM, Karimi-Kivi M, Noroozi E, Mahjoob A, Asaadi Y, Shahmohammadi A, Sadeghi S, Shakeri S, Ghiyasvand K, Tavakoli-Yaraki M. A review on potential roles of vitamins in incidence, progression, and improvement of multiple sclerosis. eNeurologicalSci 2018;10:37-44. https://doi.org/10.1016/j.ensci.2018.01.007
  14. Zhao W, Yu K, Tan S, Zheng Y, Zhao A, Wang P, Zhang Y. Dietary diversity scores: an indicator of micronutrient inadequacy instead of obesity for Chinese children. BMC Public Health 2017;17:440.
  15. Kong W, Jiang T, Ning Y, Guo Y, Liu H, Lyu X, Li M. Dietary diversity, diet quality, and oxidative stress in older adults. Geriatr Nurs 2022;48:158-63. https://doi.org/10.1016/j.gerinurse.2022.09.013
  16. Marck CH, Probst Y, Chen J, Taylor B, van der Mei I. Dietary patterns and associations with health outcomes in Australian people with multiple sclerosis. Eur J Clin Nutr 2021;75:1506-14. https://doi.org/10.1038/s41430-021-00864-y
  17. Centers for Disease Control and Prevention. National Health and Nutrition Examination Survey (NHANES): anthropometry procedures manual. Atlanta, GA: Centers for Disease Control and Prevention; 2007. 
  18. Ghazizahedi S, Nouri M, Norouzy A, Nemati M, Safarian M, Mohajeri SAR, Esmaeely H, Shalaie N. Scientific: validity and reproducibility of Iranian food frequency questionnaire. Nutr Food Sci Res 2014;1:16. 
  19. Nachvak SM, Abdollahzad H, Mostafai R, Moradi S, Pasdar Y, Rezaei M, Esksndari S. Dietary diversity score and its related factors among employees of Kermanshah University of Medical Sciences. Clin Nutr Res 2017;6:247-55. https://doi.org/10.7762/cnr.2017.6.4.247
  20. Kant AK, Block G, Schatzkin A, Ziegler RG, Nestle M. Dietary diversity in the US population, NHANES II, 1976-1980. J Am Diet Assoc 1991;91:1526-31. https://doi.org/10.1016/S0002-8223(21)01428-0
  21. Esposito S, Bonavita S, Sparaco M, Gallo A, Tedeschi G. The role of diet in multiple sclerosis: a review. Nutr Neurosci 2018;21:377-90. https://doi.org/10.1080/1028415X.2017.1303016
  22. Foote JA, Murphy SP, Wilkens LR, Basiotis PP, Carlson A. Dietary variety increases the probability of nutrient adequacy among adults. J Nutr 2004;134:1779-85. https://doi.org/10.1093/jn/134.7.1779
  23. Saeedirad Z, Ariyanfar S, Noormohammadi M, Ghorbani Z, Naser Moghadasi A, Shahemi S, Ghanaatgar M, Rezaeimanesh N, Hekmatdoost A, Ghaemi A, Razeghi Jahromi S. Higher dietary acid load might be a potent derivative factor for multiple sclerosis: the results from a case-control study. Nutrients 2023;15:3311.
  24. Shivappa N, Hebert JR, Behrooz M, Rashidkhani B. Dietary inflammatory index and risk of multiple sclerosis in a case-control study from Iran. Neuroepidemiology 2016;47:26-31. https://doi.org/10.1159/000445874
  25. Sedaghat F, Jessri M, Behrooz M, Mirghotbi M, Rashidkhani B. Mediterranean diet adherence and risk of multiple sclerosis: a case-control study. Asia Pac J Clin Nutr 2016;25:377-84.
  26. World Health Organization. Increasing fruit and vegetable consumption to reduce the risk of noncommunicable diseases [Internet]. Available from https://www.who.int/tools/elena/interventions/fruit-vegetables-ncds [cited 2023 August 9]. 2023. 
  27. Li Y, Yu Q, Zhao W, Zhang J, Liu W, Huang M, Zeng X. Oligomeric proanthocyanidins attenuate airway inflammation in asthma by inhibiting dendritic cells maturation. Mol Immunol 2017;91:209-17. https://doi.org/10.1016/j.molimm.2017.09.012
  28. Lin W, Wang W, Wang D, Ling W. Quercetin protects against atherosclerosis by inhibiting dendritic cell activation. Mol Nutr Food Res 2017;61:1700031.
  29. Maleki SJ, Crespo JF, Cabanillas B. Anti-inflammatory effects of flavonoids. Food Chem 2019;299:125124.
  30. Masilamani M, Wei J, Bhatt S, Paul M, Yakir S, Sampson HA. Soybean isoflavones regulate dendritic cell function and suppress allergic sensitization to peanut. J Allergy Clin Immunol 2011;128:1242-1250.e1. https://doi.org/10.1016/j.jaci.2011.05.009
  31. Peeters LM, Vanheusden M, Somers V, Van Wijmeersch B, Stinissen P, Broux B, Hellings N. Cytotoxic CD4+ T cells drive multiple sclerosis progression. Front Immunol 2017;8:1160.
  32. Chitnis T. The role of CD4 T cells in the pathogenesis of multiple sclerosis. Int Rev Neurobiol 2007:79:43-72. https://doi.org/10.1016/S0074-7742(07)79003-7
  33. Rotstein DL, Cortese M, Fung TT, Chitnis T, Ascherio A, Munger KL. Diet quality and risk of multiple sclerosis in two cohorts of US women. Mult Scler 2019;25:1773-80. https://doi.org/10.1177/1352458518807061
  34. Azary S, Schreiner T, Graves J, Waldman A, Belman A, Guttman BW, Aaen G, Tillema JM, Mar S, Hart J, Ness J, Harris Y, Krupp L, Gorman M, Benson L, Rodriguez M, Chitnis T, Rose J, Barcellos LF, Lotze T, Carmichael SL, Roalstad S, Casper CT, Waubant E. Contribution of dietary intake to relapse rate in early paediatric multiple sclerosis. J Neurol Neurosurg Psychiatry 2018;89:28-33. https://doi.org/10.1136/jnnp-2017-315936
  35. Ochoa-Reparaz J, Kirby TO, Kasper LH. The gut microbiome and multiple sclerosis. Cold Spring Harb Perspect Med 2018;8:a029017.
  36. Riccio P, Rossano R. Nutrition facts in multiple sclerosis. ASN Neuro 2015;7:1759091414568185.
  37. Riccio P. The molecular basis of nutritional intervention in multiple sclerosis: a narrative review. Complement Ther Med 2011;19:228-37. https://doi.org/10.1016/j.ctim.2011.06.006
  38. Wens I, Dalgas U, Stenager E, Eijnde BO. Risk factors related to cardiovascular diseases and the metabolic syndrome in multiple sclerosis - a systematic review. Mult Scler 2013;19:1556-64. https://doi.org/10.1177/1352458513504252
  39. Oliveira SR, Simao AN, Kallaur AP, de Almeida ER, Morimoto HK, Lopes J, Dichi I, Kaimen-Maciel DR, Reiche EM. Disability in patients with multiple sclerosis: influence of insulin resistance, adiposity, and oxidative stress. Nutrition 2014;30:268-73. https://doi.org/10.1016/j.nut.2013.08.001
  40. Jelinek GA, De Livera AM, Marck CH, Brown CR, Neate SL, Taylor KL, Weiland TJ. Associations of lifestyle, medication, and socio-demographic factors with disability in people with multiple sclerosis: an international cross-sectional study. PLoS One 2016;11:e0161701.
  41. Altowaijri G, Fryman A, Yadav V. Dietary interventions and multiple sclerosis. Curr Neurol Neurosci Rep 2017;17:1-10.  https://doi.org/10.1007/s11910-017-0714-5
  42. Endo Y, Yokote K, Nakayama T. The obesity-related pathology and Th17 cells. Cell Mol Life Sci 2017;74:1231-45. https://doi.org/10.1007/s00018-016-2399-3
  43. Hagan KA, Munger KL, Ascherio A, Grodstein F. Epidemiology of major neurodegenerative diseases in women: contribution of the nurses' health study. Am J Public Health 2016;106:1650-5. https://doi.org/10.2105/AJPH.2016.303324
  44. Greer JM, McCombe PA. Role of gender in multiple sclerosis: clinical effects and potential molecular mechanisms. J Neuroimmunol 2011;234:7-18. https://doi.org/10.1016/j.jneuroim.2011.03.003
  45. Amato MP, Ponziani G. A prospective study on the prognosis of multiple sclerosis. Neurol Sci 2000;21:S831-8. https://doi.org/10.1007/s100720070021
  46. Hammond SR, de Wytt C, Maxwell IC, Landy PJ, English D, McLeod JG, McCall MG. The epidemiology of multiple sclerosis in Queensland, Australia. J Neurol Sci 1987;80:185-204. https://doi.org/10.1016/0022-510X(87)90154-7
  47. Thorogood M, Hannaford PC. The influence of oral contraceptives on the risk of multiple sclerosis. Br J Obstet Gynaecol 1998;105:1296-9. https://doi.org/10.1111/j.1471-0528.1998.tb10008.x
  48. Antonovsky A, Leibowitz U, Smith HA, Medalie JM, Balogh M, Kats R, Halpern L, Alter M. Epidemiologic study of multiple sclerosis in Israel: I. An overall review of methods and findings. Arch Neurol 1965;13:183-93. https://doi.org/10.1001/archneur.1965.00470020073010
  49. Carlens C, Hergens MP, Grunewald J, Ekbom A, Eklund A, Hoglund CO, Askling J. Smoking, use of moist snuff, and risk of chronic inflammatory diseases. Am J Respir Crit Care Med 2010;181:1217-22. https://doi.org/10.1164/rccm.200909-1338OC
  50. Hedstrom AK, Baarnhielm M, Olsson T, Alfredsson L. Tobacco smoking, but not Swedish snuff use, increases the risk of multiple sclerosis. Neurology 2009;73:696-701. https://doi.org/10.1212/WNL.0b013e3181b59c40
  51. Jafari N, Hoppenbrouwers IA, Hop WC, Breteler MM, Hintzen RQ. Cigarette smoking and risk of MS in multiplex families. Mult Scler 2009;15:1363-7. https://doi.org/10.1177/1352458509345907
  52. Silva KRP, Alvarenga RMP, Fernandez y Fernandez O, Alvarenga H, Thuler LCS. Potential risk factors for multiple sclerosis in Rio de Janeiro: a case-control study. Arq Neuropsiquiatr 2009;67:229-34. https://doi.org/10.1590/S0004-282X2009000200011
  53. Rodriguez Regal A, del Campo Amigo M, Paz-Esquete J, Martinez Feijoo A, Cebrian E, Suarez Gil P, Mourino MA. A case-control study of the influence of the smoking behaviour in multiple sclerosis. Neurologia 2009;24:177-80.
  54. Russo C, Morabito F, Luise F, Piromalli A, Battaglia L, Vinci A, Trapani Lombardo V, de Marco V, Morabito P, Condino F, Quattrone A, Aguglia U. Hyperhomocysteinemia is associated with cognitive impairment in multiple sclerosis. J Neurol 2008;255:64-9. https://doi.org/10.1007/s00415-007-0668-7
  55. Fowles J, Christophersen A, Fernando D, Lea R, Woodward A, Dickson S, Hosking M, Berezowski R. Secondhand tobacco smoke exposure in New Zealand bars: results prior to implementation of the bar smoking ban. N Z Med J 2006;119:U1931.
  56. Ghadirian P, Jain M, Ducic S, Shatenstein B, Morisset R. Nutritional factors in the aetiology of multiple sclerosis: a case-control study in Montreal, Canada. Int J Epidemiol 1998;27:845-52. https://doi.org/10.1093/ije/27.5.845
  57. Slattery ML. Analysis of dietary patterns in epidemiological research. Appl Physiol Nutr Metab 2010;35:207-10. https://doi.org/10.1139/H10-006
  58. Ruel MT. Is dietary diversity an indicator of food security or dietary quality? A review of measurement issues and research needs. Food Nutr Bull 2003;24:231-2. https://doi.org/10.1177/156482650302400217
  59. Arimond M, Wiesmann D, Becquey E, Carriquiry A, Daniels MC, Deitchler M, Fanou-Fogny N, Joseph ML, Kennedy G, Martin-Prevel Y, Torheim LE. Simple food group diversity indicators predict micronutrient adequacy of women's diets in 5 diverse, resource-poor settings. J Nutr 2010;140:2059S-2069S. P  https://doi.org/10.3945/jn.110.123414
  60. McCullough ML, Feskanich D, Stampfer MJ, Giovannucci EL, Rimm EB, Hu FB, Spiegelman D, Hunter DJ, Colditz GA, Willett WC. Diet quality and major chronic disease risk in men and women: moving toward improved dietary guidance. Am J Clin Nutr 2002;76:1261-71. https://doi.org/10.1093/ajcn/76.6.1261
  61. Fernandez E, Negri E, La Vecchia C, Franceschi S. Diet diversity and colorectal cancer. Prev Med 2000;31:11-4. https://doi.org/10.1006/pmed.2000.0667
  62. Miller WL, Crabtree BF, Evans DK. Exploratory study of the relationship between hypertension and diet diversity among Saba Islanders. Public Health Rep 1992;107:426-32.
  63. Raynor HA, Epstein LH. Dietary variety, energy regulation, and obesity. Psychol Bull 2001;127:325-41. https://doi.org/10.1037/0033-2909.127.3.325
  64. Tseng M. Validation of dietary patterns assessed with a food-frequency questionnaire. Am J Clin Nutr 1999;70:422.
  65. Melamed A, Robinson JN. Case-control studies can be useful but have many limitations: study design: case-control studies. BJOG 2019;126:23.