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Association of Methionine to Homocysteine Status with Brain Magnetic Resonance Imaging Measures and Risk of Dementia

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Association of Methionine to Homocysteine Status with Brain Magnetic Resonance Imaging Measures and Risk of Dementia Research JAMA Psychiatry | Original Investigation Association of Methionine to Homocysteine Status With Brain Magnetic Resonance Imaging Measures and Risk of Dementia Babak Hooshmand, MD, PhD, MPH; Helga Refsum, MD, PhD; A. David Smith, DPhil; Grégoria Kalpouzos, PhD; Francesca Mangialasche, MD, PhD; Christine A. F. von Arnim, MD; Ingemar Kåreholt, PhD; Miia Kivipelto, MD, PhD; Laura Fratiglioni, MD, PhD Supplemental content IMPORTANCE Impairment of methylation status (ie, methionine to homocysteine ratio) may be a modifiable risk factor for structural brain changes and incident dementia. OBJECTIVE To investigate the association of serum markers of methylation status and sulfur amino acids with risk of incident dementia, Alzheimer disease (AD), and the rate of total brain tissue volume loss during 6 years. DESIGN, SETTING, AND PARTICIPANTS This population-based longitudinal study was performed from March 21, 2001, to October 10, 2010, in a sample of 2570 individuals aged 60 to 102 years from the Swedish Study on Aging and Care in Kungsholmen who were dementia free at baseline and underwent comprehensive examinations and structural brain magnetic resonance imaging (MRI) on 2 to 3 occasions during 6 years. Data analysis was performed from March 1, 2018, to October 1, 2018. MAIN OUTCOMES AND MEASURES Incident dementia, AD, and the rate of total brain volume loss. RESULTS This study included 2570 individuals (mean [SD] age, 73.1 [10.4] years; 1331 [56.5%] female). The methionine to homocysteine ratio was higher in individuals who consumed vitamin supplements (median, 1.9; interquartile range [IQR], 1.5–2.6) compared with those who did not (median, 1.8; IQR, 1.3–2.3; P < .001) and increased per each quartile increase of vitamin B12 or folate. In the multiadjusted model, an elevated baseline serum total homocysteine level was associated with an increased risk of dementia and AD during 6 years: for the highest homocysteine quartile compared with the lowest, the hazard ratios (HRs) were 1.60 (95% CI, 1.01-2.55) for dementia and 2.33 (95% CI, 1.26-4.30) for AD. In contrast, elevated concentrations of methionine were associated with a decreased risk of dementia (HR, 0.54; 95% CI, 0.36-0.81) for the highest quartile compared with the lowest. Higher values of the methionine to homocysteine ratio were significantly associated with lower risk of dementia and AD: for the fourth methionine-homocysteine quartile compared with the first quartile, the HR was 0.44 (95% CI, 0.27-0.71) for incident dementia and 0.43 (95% CI, 0.23-0.80) for AD. In the multiadjusted linear mixed models, a higher methionine to homocysteine ratio was associated with a decreased rate of total brain tissue volume loss during the study period (β [SE] per 1-SD increase, 0.038 [0.014]; P = .007). CONCLUSIONS AND RELEVANCE The methionine to homocysteine status was associated with dementia development and structural brain changes during the 6-year study period, suggesting that a higher methionine to homocysteine ratio may be important in reducing the rate of brain atrophy and decreasing the risk of dementia in older adults. Author Affiliations: Author affiliations are listed at the end of this article. Corresponding Author: Babak Hooshmand, MD, PhD, MPH, Aging Research Center, Karolinska Institute, Tomtebodavägen 18A, JAMA Psychiatry. 2019;76(11):1198-1205. doi:10.1001/jamapsychiatry.2019.1694 Plan 9, Solna 171 65, Sweden Published online July 24, 2019. ([email protected]). 1198 (Reprinted) jamapsychiatry.com © 2019 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 Association of Methionine to Homocysteine Ratio With Brain MRI Measures and Risk of Dementia Original Investigation Research itamin B12 and folate are essential vitamins for the re- methylation of homocysteine to methionine and the Key Points subsequent formation of S-adenosylmethionine (SAM), V Question Is methylation status (ie, methionine to homocysteine the primary methyl donor for many biochemical reactions in- ratio) associated with incident dementia and structural brain volved in normal brain functions.1-4 Interference with this pro- changes in older adults? cess may lead to impairment in the formation of methionine Findings In this cohort study of longitudinal data from 2570 and an unfavorable methylation status and may result in the elderly individuals who were dementia free at baseline, a higher accumulation of serum total homocysteine (tHcy), which has methionine to homocysteine ratio was observed in participants been associated with several cerebrovascular and cardiovas- with better B12 or folate status and was associated with decreased cular conditions.5 Elevated tHcy levels may further impair the risk of incident dementia and Alzheimer disease. A higher methylation status by converting to S-adenosyl homocyste- methionine to homocysteine ratio was associated with a ine (SAH), a potent competitive inhibitor of several methyl decreased rate of total brain tissue volume loss during 6 years. transferases.2,6 Meanings Markers of methylation status were associated with Whereas several studies7-9 have reported an association dementia development and structural brain changes during between increased tHcy values and dementia or structural 6 years, suggesting that a higher methionine to homocysteine brain changes, only a few cross-sectional studies10-12 have ratio may be important in reducing the rate of brain atrophy and decreasing the risk of dementia in older adults. investigated the associations between methylation status (ie, methionine to homocysteine ratio) and cognitive impair- ment or dementia with mixed results. Furthermore, the ef- The Ethics Committee at Karolinska Institutet and the Re- fects of sulfur amino acids other than tHcy on dementia have gional Ethical Review Board in Stockholm approved the pro- rarely been investigated.13,14 tocols of each phase of SNAC-K and approved this study, and The potential association of sulfur amino acids with de- written informed consent was provided by all participants. mentia is important because they are modifiable risk factors At baseline and each follow-up, the SNAC-K participants and thus a potential target in preventive interventions. We pre- underwent a thorough clinical examination, interview, and as- viously reported that the rate of total brain volume loss in older sessments by a physician, a registered nurse, and a psycholo- adults was associated with tHcy and vitamin B12 status 6 years gist. Data on sociodemographic characteristics, medical his- earlier.15 However, the methionine to homocysteine status was tory, drug use, and cognitive function were collected according not investigated in relation to brain magnetic resonance to a structured protocol, and the diagnoses of dementia and imaging (MRI) measures in that report.15 The aim of the cur- Alzheimer disease (AD) were made according to DSM-IV rent study was to investigate the associations of methionine criteria18 in which a validated 3-step diagnostic procedure was 19 to homocysteine status, other sulfur amino acids, vitamin B12, used as previously reported. In brief, 2 examining physi- and red blood cell (RBC) folate with the risk of incident de- cians independently made a preliminary diagnosis, and in the mentia during 6 years in a population-based cohort of older case of disagreement, a third opinion was sought to reach a con- adults without mandatory folic acid fortification. We pro- sensus diagnosis. For the deceased participants, the diagno- posed that methylation status may be reflected by the serum sis of dementia was made by 2 physicians through reviewing methionine to homocysteine status. In a supplementary analy- the medical records and death certificates. sis, we examined the association between methionine to Data on vitamin supplement use were collected from study homocysteine ratio and the rate of total brain volume loss in participants and verified by inspecting drug prescriptions and a subsample with available brain MRI data. containers. Systolic blood pressure (SBP) was measured twice using the participant’s left arm after the patient had been sitting for 5 minutes, and the mean of the measurements was Methods calculated. Blood samples obtained after clinical examination were Study Population routinely analyzed for RBC folate levels. Of the initial sample, The study population was derived from the Swedish National participants who were diagnosed with prevalent dementia Study on Aging and Care in Kungsholmen (SNAC-K), a popu- (DSM-IV criteria, n = 311) and those who did not have blood lation-based, prospective study conducted in the Kungshol- samples obtained (n = 271) were excluded, leaving 2903 par- men area of central Stockholm, Sweden. SNAC-K involved a ticipants with available RBC folate values at baseline. Of these random sample of persons 60 years or older who live at home individuals, 333 refused to participate in the follow-up exami- or in an institution. Because of more rapid changes in health nation or had moved before examination (213 individuals from and a higher attrition rate among older age groups, sampling the younger age group and 120 individuals from the older age was stratified by age cohort. Assessments took place at 6-year group). Therefore, the study population for the current analy- intervals for younger cohorts (60, 66, 72, and 78 years of age) sis consisted of 2570 individuals without dementia at base- and at 3-year intervals for older cohorts (81, 84, 87, 90, 93, 96, line. Of these individuals, 501 underwent MRI on a 1.5-T mag- and ≥99 years of age). From March 21, 2001, to August 30, netic resonance scanner (eAppendix in the Supplement)at 2004, of the 4590 living and eligible individuals randomly se- baseline and every 3 years thereafter for the older cohort (ie, lected for SNAC-K, 3363 (73.3%) participated in the baseline those ≥78 years of age at baseline; n = 92 at 3-year follow-up) examination; the end of follow-up was October 10, 2010.16,17 and every 6 years thereafter for the whole cohort (n = 260; jamapsychiatry.com (Reprinted) JAMA Psychiatry November 2019 Volume 76, Number 11 1199 © 2019 American Medical Association.
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