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Correlat Ion of Thiamine Metabolite Levels with Cognitive Function in the Non-Demented Elderly

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Correlat Ion of Thiamine Metabolite Levels with Cognitive Function in the Non-Demented Elderly Neurosci Bull December 1, 2015, 31(6): 676–684. http://www.neurosci.cn 676 DOI: 10.1007/s12264-015-1563-3 ·Original Article· Correlat ion of thiamine metabolite levels with cognitive function in the non-demented elderly Jingwen Lu1,*, Xiaoli Pan1,*, Guoqiang Fei1,*, Changpeng Wang1, Lei Zhao 1, Shaoming Sang2, Huimin Liu2, Meng Liu2, Hui Wang3, Zhiliang Wang3, Chunjiu Zhong1,2 1Department of Neurology, Zhongshan Hospital and Shanghai Medical College, Fudan University, Shanghai 200032, China 2State Key Laboratory of Medical Neurobiology and Institutes of Brain Science, Fudan University, Shanghai 200032, China 3Regional Health Service Center of Xujiahui, Xuhui District, Shanghai 200030, China *These authors contributed equally to this work. Corresponding author: Chunjiu Zhong. E-mail: [email protected] ABSTRACT but consumes nearly 25% of the total body glucose in the resting awake state[1]. Since glucose is the predominant Thiamine metabolism is critical for glucose metabolism energy substrate for oxidative processes in the brain[2], and also vital for brain function, which is susceptible to appropriate glucose metabolism is vital for sustaining brain decline in the elderly. This study aimed to investigate functions. The elderly are susceptible to a decline in brain whether thiamine metabolites correlate with cognitive functions[3, 4]. Further, the severity of cognitive impairment, function in the non-demented elderly and their impact the most common manifestation of declining brain function, factors. Volunteers >60 years old were recruited and is signifi cantly correlated with a reduction in brain glucose their blood thiamine metabolites and Mini-Mental metabolism[5–8]. Clarifying the cause and mechanism of State Examination (MMSE) scores were measured. reduced brain glucose metabolism in the elderly will help in The apolipoprotein E (APOE) genotype, routine blood the search for preventive and therapeutic target(s) against parameters, liver and kidney function, and levels of cognitive impairment. fasting blood glucose and triglycerides were also Thiamine metabolism is vital for glucose metabolism. measured. The results showed that the thiamine Thiamine diphosphate (TDP), the active form of thiamine, diphosphate (TDP) level weakly correlated with is a critical coenzyme of three key enzymes in glucose MMSE score in the non-demented elderly. Participants metabolism: pyruvate dehydrogenase complex and with high TDP levels performed better in Recall and α-ketoglutarate dehydrogenase complex in the Krebs cycle, Attention and Calculation than those with low TDP. and transketolase in the pentose phosphate pathway. It TDP levels were associated with the APOE ε2 allele, has been demonstrated that the elderly tend to suffer from body mass index, hemoglobin level, fasting blood thiamine defi ciency with aging itself, rather than co-existent glucose, and triglycerides. Our results suggest that illnesses[9]. Patients with Alzheimer’s disease (AD), the most TDP, which is easily affected by many factors, impacts common type of dementia, have reduced TDP content, cognitive function in the elderly. reduced activity of thiamine-dependent enzymes[10–12], Keywords: thiamine diphosphate; cognitive function; and brain glucose hypometabolism. Therefore, abnormal non-demented elderly thiamine metabolism may be a pathogenic factor for the declined brain glucose metabolism in the elderly. However, studies on the correlation between thiamine INTRODUCTION metabolism and cognitive function in the non-demented elderly are insuffi cient and t he results are controversial[13–15]. The human brain accounts for only 2% of body weight The inconsistent results may be partially attributed to the Jingwen Lu, et al. Correlat ion of thiamine metabolite levels with cognitive function in the non-demented elderly 677 small sample sizes in some studies. Also, the methodology in the non-demented elderly living on Xujiahui Street in the for determining the content of thiamine and its derivates Xuhui District of Shanghai, China. In addition, as multiple needs to be considered. The previous studies mainly factors such as apolipoprotein E (APOE) genotype, age, evaluated the thiamine metabolites indirectly, using and educational background are involved in cognitive methods such as the erythrocyte transketolase activity function, we also analyzed the relationship between TDP assay that records the difference in transketolase activity levels and these factors. before and after addition of TDP as a consequence of diminished coenzyme concentration[13, 15]. The precise levels PARTICIPANTS AND METHODS of thiamine and its derivates and the extent of thiamine deficiency are unknown. Recently, high-performance Participants liquid chromatographic (HPLC) fluoroscopy has been Volunteers were recruited from the Physical Examination used to determine the levels of free thiamine, thiamine Department at the Regional Health Service Center of monophosphate (TMP), and TDP in whole blood, and has Xujiahui from April 1 to December 31, 2012. Participants proved to be rapid, accurate, and convenient[16, 17]. were >60 years old and lived on Xujiahui Street, Xuhui So far, little is known about the status of thiamine District, Shanghai, China. All participants gave informed metabolites in the non-demented elderly i n China, which consent. Information on history of diseases, current has the largest and most rapidly ageing population in medications, and supplementation with vitamins and other the world. The aim of this study was to investigate the health-care products was collected by questionnaire. correlation of thiamine metabolites with cognitive function Participants with major disorders of the gastrointestinal Fig. 1. Flowchart of this study. 678 Neurosci Bull December 1, 2015, 31(6): 676–684 Table 1. Demographic and clinical characteristics of partici- participants with >9 years of education and scores >24 . pants with normal cognitive function (n=611, mean ± SD) Individuals who did not meet the above criteria were excluded. Routine blood parameters, liver and kidney Variables Value (range) functions, and levels of fasting blood glucose (FBG) and Age (years) 72.30 ± 5.89 (63–91) triglycerides were measured. Height and weight were used Males (%) 263 (43.04) to calculate body mass index (BMI). MMSE scores 27.83 ± 2.38 (18–30) Determination of Thiamine, TMP, and TDP Levels Education (years) 9.27 ± 4.96 (0–16) The levels of thiamine, TMP, and TDP were measured TDP (nmol/L) 118.60 ± 23.25 (61.75–189.2) using HPLC as previously described in detail[18]. Briefl y, 150 TMP (nmol/L) 3.70 ± 2.16 (0–12.16) μL of 7.4% perchloric acid was immediately added to 150 Thiamine (nmol/L) 3.47 ± 2.80 (0–29.65) μL of fresh blood anti-coagulated with heparin. After mixing Hemoglobin (g/L) 134.1 ± 13.72 (83.0–169.0) by vibration for 30 s for full deproteinization, the mixture Fasting plasma glucose (mmol/L) 6.04 ± 1.56 (4.01–15.82) was centrifuged at 10 000 rpm for 6 min at 4°C. Then, Triglyceride (mmol/L) 1.53 ± 0.98 (0.33–11.32) the supernatant was collected and stored at −20°C until Alanine aminotransferase (U/L) 22.19 ± 10.78 (6.7–91.6) determination. Thiamine and its phosphate esters were Creatinine (mmol/L) 66.02 ± 21.55 (5.64–307.1) derivatized into thiochromes using potassium ferricyanide 2 and separated by gradient elution on a C18 reversed-phase BMI (kg/m ) 23.92 ± 3.13 (13.31–34.03) analytical column (250 mm×4.6 mm). The derivatives were ApoE genotype (%) measured by HPLC fl uoroscopy (Agilent 1100, Santa Clara, ε2/ε2 n = 20 (3.27) CA) at 367 nm excitation and 435 nm emission. Thiamine, ε2/ε3 n = 66 (10.80) TMP, and TDP levels were quantified using standard ε2/ε4 n = 17 (2.78) samples of each compound (Sigma-Aldrich, St. Louis, MO). ε3/ε3 n = 414 (67.76) ε3/ε4 n = 88 (14.40) Apolipoprotein E Genotype Analysis ε4/ε4 n = 6 (0.98) APOE alleles were detected using the ABI real-time Taqman SNP genotyping assay (L ife Technologies, Carlsbad, CA) according to the manufacturer’s instructions. tract, chronic alcohol abuse, or thiamine supplementation Human genomic DNA was extracted from blood anti- during the previous month were excluded from this study. coagulated with heparin using a genome extraction kit A flowchart of the study protocol and demographic (Tiangen Biotech, Beijing, China). All participants were information on the participants are shown in Fig.1 and Table 1. divided into two subgroups by the APOE geneotype: The study design and procedures were approved by the according to the presence of APOE ε2 allele, an APOE ε2 Committee on Medical Ethics of Zhongshan Hospital, positive group with the ε2 /ε2, ε2/ε3, or ε2/ε4 genotype and Fudan University. a negative group with the ε3/ε3, ε3/ε4, or ε4/ε4 genotype; according to the presence of APOE ε4 allele, an APOE ε4- Clinical Assessments positive group with the ε2/ε4, ε3/ε4, or ε4/ε4 genotype and All participants completed the Mini-Mental State an APOE ε4-negative group with the ε2/ε2, ε2/ε3, or ε3/ε3 Examination (MMSE, Chinese version) as a measure genotype. of general cognitive function, with scores ranging from 0 (severe impairment) to 30 (no impairment). The non- Statistical Analysis demented elderly were identified according to the MMSE SP SS software (version 18.0; SPSS Inc., Chicago, IL) was score adjusted for educational background: illiterate used for statistical analyses. Pearson correlation analysis individuals with MMSE scores >17, participants with was used to assess the correlation between thiamine a preliminary school diploma and scores >21, and metabolite levels and MMSE scores. Two-tailed Student’s Jingwen Lu, et al. Correlat ion of thiamine metabolite levels with cognitive function in the non-demented elderly 679 t-test or one-way analysis of variance (ANOVA) was used excluded. Six hundred and sixty-three individuals then to assess differences in TDP, TMP, and thiamine levels. All received MMSE evaluation and 27 with low scores were data are shown as mean ± SD, with statistical signifi cance excluded.
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