Combination of Exercise and Vegetarian Diet: Relationship with High Density-Lipoprotein Cholesterol in Taiwanese Adults Based on MTHFR rs1801133 Polymorphism
by
Shu-Lin Chang
1, 
Oswald Ndi Nfor
2,
Chien-Chang Ho
3,4,
Kuan-Jung Lee
2,
Wen-Yu Lu
2,
Chia-Chi Lung
2,
Disline Manli Tantoh
2,5,
Shu-Yi Hsu
2,
Ming-Chih Chou
1,* and
Yung-Po Liaw
2,5,* 1
Institute of Medicine, Chung Shan Medical University, Taichung 40201, Taiwan
2
Department of Public Health and Institute of Public Health, Chung Shan Medical University, Taichung 40201, Taiwan
3
Department of Physical Education, Fu-Jen Catholic University, New Taipei City 24205, Taiwan
4
Research and Development Center for Physical Education, Health, and Information Technology, Fu Jen Catholic University, New Taipei 24205, Taiwan
5
Department of Medical Imaging, Chung Shan Medical University Hospital, Taichung City 40201, Taiwan
*
Authors to whom correspondence should be addressed.
Nutrients 2020, 12(6), 1564; https://doi.org/10.3390/nu12061564
Submission received: 25 April 2020
/
Revised: 26 May 2020
/
Accepted: 26 May 2020
/
Published: 27 May 2020
(This article belongs to the Special Issue Dietary Intake and Physical Activity for Human Health)
Abstract
:We examined the association between high-density lipoprotein cholesterol (HDL-C), and exercise and vegetarian diets, in Taiwanese adults, based on the Methylenetetrahydrofolate reductase (MTHFR) rs1801133 polymorphism. Using regression models, we analyzed historical data collected from 9255 Taiwan Biobank (TWB) participants from 2008 through 2015. Exposure to exercise was associated with higher HDL-C (β = 1.0508 and 1.4011 for GG and GA + AA individuals, respectively), whereas a vegetarian diet was associated with lower HDL-C (β = −6.2793 and −4.6359 for those with GG and GA + AA genotype, respectively). We found an interaction between exercise and diet among GG individuals (p = 0.0101). Compared with no exercise/no vegetarian diet, vegetarian diet/no exercise was associated with a 5.1514 mg/dl reduction in HDL-C among those with GG genotype (β = −5.1514, p < 0.0001) and a 4.8426 mg/dl reduction (β = −4.8426, p < 0.0001) among those with GA + AA genotype. Vegetarian diets in combination with exercise predicted a 6.5552 mg/dl reduction in HDL-C among GG individuals (β = −6.5552) and a 2.8668 mg/dl reduction among GA + AA individuals (p < 0.05). These findings demonstrated that vegetarian diet alone was associated with lower HDL-C, no matter the rs1801133 genotype. However, the inclusion of regular exercise predicted much lower levels among GG individuals, whereas levels among GA + AA individuals were relatively higher.
1. Introduction
High-density lipoprotein cholesterol is a well-known lipid fraction [1] that has been associated with the risk of heart diseases [2]. Lower levels of HDL-C (i.e., <40 mg/dl and <50 mg/dl for men and women, respectively) have been associated with heightened risk of cardiovascular disease, even though the epidemiological relationship between them remains complex [3]. Lower concentrations of HDL-C have also been associated with systemic inflammation and elevated risk of sepsis [4,5].
Vegetarian diets are important in the prevention and treatment of diseases [6]. However, previous works investigating lipid profiles have reported negative associations between HDL-C and vegetarian diets [7,8,9]. In a separate study, consumption of vegetarian diets was associated with decreased levels of HDL-C, low-density lipoprotein cholesterol (LDL-C), and total cholesterol (TC), but not with triglycerides (TG) [10]. In addition, vegetarian diets have also shown strong associations with total plasma homocysteine (Hcy) levels [11].
Exercise is among the lifestyle variables previously recommended for boosting lipid profiles [12]. More recent evidence [13] suggested dose–response relationships between HDL-C and exercise intensity. Habitual or a single bout of exercise can positively affect cholesterol metabolism [14]. According to MayoClinic, benefits can be seen with as little as 60 min of moderate aerobic exercise a week [15]. It has been hypothesized that exercise can increase the expression of liver ATP-binding cassette transporters A-1, which play an essential role in the reverse cholesterol transport system [16].
Exercise is believed to provide more benefits for HDL-C than those obtained by eating just vegetarian diets [17]. It is widely believed that exposure to exercise is a great way for vegetarians to boost their HDL cholesterol [15]. As far as we know, investigations have not been carried out to determine whether coupling a vegetarian diet with exercise would predict a reduction or an increase in HDL-C. Such investigations would help to enhance the knowledge of HDL-C response in terms of lifestyle variables.
Besides the lifestyle determinants, genetic factors contribute to variations in HDL-C concentrations. The methylenetetrahydrofolate reductase (MTHFR) gene, an important enzyme for folate metabolism, has been demonstrated to be associated with abnormal lipid levels and coronary artery diseases [18,19,20]. Rs1801133 (also known as C677T) is one of its most common and best-studied polymorphisms, which showed stronger associations with cardiovascular disease risk, especially among Asians [18]. This variant reduces enzyme activity and raises the concentration of total Hcy [21], which is a potential risk factor for dyslipidemia and cardiovascular disease [22]. The significance of this polymorphic variant has already been previously described [23]. Interactions previously reported between C677T and serum lipid levels have been partly linked to lifestyle and environmental factors [24]. Of these factors, exposure to regular exercise has been demonstrated to attenuate central artery stiffening caused by the C677T variant [25].
As stated earlier, exercise and vegetarian diets are some of the modifiable factors previously associated with HDL-C. However, whether the combined effect of these variables on HDL-C is modified by rs1801133 polymorphism has not yet been established. Therefore, we examined the interactive association of exercise and vegetarian diets with HDL-C among Taiwanese individuals, based on MTHFR rs1801133 polymorphism.
2. Methods
Data were obtained from the TWB, an established infrastructure holding data of Taiwanese individuals (aged 30–70 years) recruited from assessment centers across Taiwan, from 2008 through 2015. Before data collection, all participants signed written informed consent. Currently, TWB contains biological, experimental, questionnaire, and physical assessment data, collected from over 129,054 participants from different parts of Taiwan. We obtained ethical approval from the Institutional Review Board of Chung Shan Medical University (CS2-16114).
2.1. Study Participants
At the beginning of the study, data were available for 9287 TWB participants with no history of cancer. However, we excluded 32 individuals with incomplete or missing information. Finally, we analyzed data for 9255 participants (4938 women and 4317 men). Sociodemographic and clinical variables of the participants included sex, age, diet type, smoking, coffee drinking, alcohol intake, total cholesterol (TC), triglycerides (TG), low-density lipoprotein (LDL-C), body mass index (BMI), waist-hip ratio (WHR), uric acid and body fat.
Diet type, smoking, alcohol intake and coffee consumption were assessed through self-reported questionnaires held in the TWB dataset. In our analyses, participants were grouped based on rs1801133 genotypes (i.e., GG and GA + AA) and diet type. They were classified as former vegetarians if they were not currently on vegetarian diets but reported to have consistently consumed them for at least 6 months in their lifetime. Vegetarians included participants who had continuously consumed plant-based food for 6 months or more, and were currently on the diet during the recruitment period. Regular exercise was considered as engaging in at most 3 physical activities lasting 30 min each session, and at least 3 sessions a week. The exercise patterns contained in the TWB questionnaires have already been discussed in our previous publication [26]. Details of the other lifestyle variables included in our model have also been previously described [27].
2.2. Variant Selection/Genotyping
We selected MTHFR rs1801133, which is one of the most common and the best-studied polymorphisms previously associated with serum lipid levels [24]. We performed genotyping using the Axiom Genome-Wide Array Plate System (Affymetrix, Santa Clara, CA, USA). For quality control purposes, we included only participants whose call rates were over 90%, and excluded single nucleotide polymorphisms (SNPs) with low minor allele frequencies (i.e., <0.05). SNPs that were not in Hardy–Weinberg equilibrium (that is, p < 1.0 × 10−3) were also excluded.
2.3. Statistical Analysis
PLINK 1.09 beta and SAS 9.4 software (SAS Institute, Cary, NC, USA) were used to perform analyses. We separated participants into 3 diet categories that included non-vegetarians, former vegetarians and vegetarians (including lacto-ovo-vegetarian and vegan). In total, 443 participants were vegetarians. Among them, 142 were rs1801133-GG individuals without exercise, 100 were rs1801133-GG individuals with exercise, 125 were rs1801133-GA + AA individuals without exercise, and 76 were rs1801133-GA + AA individuals with exercise. We analyzed the categorical variables using the Chi-square test and the continuous variables were described as means ± standard error. Using multivariate linear regression analysis, we estimated the β coefficients and their corresponding p-values. Exercise and vegetarian diets each were considered to be 1 unit of change. A statistically significant beta coefficient indicated that the variable predicted an outcome.
3. Results
The baseline characteristics of participants according to rs1801133 are described in Table 1. There were 5016 individuals with the rs1801133-GG genotype and 4239 with the GG + AA genotype. Overall, vegetarian diet was associated with lower HDL-C among those with rs1801133-GG (β = −6.2793, p < 0.0001) and rs1801133-GG + AA (β = −4.6359, p < 0.0001) genotypes, respectively (Table 2). Exposure to exercise predicted a higher HDL-C among those with both genotypes, with β values of 1.0508 (p = 0.0015) for rs1801133-GG individuals and 1.4011 (p = 0.0001) for rs1801133-GG + AA individuals. Compared to women, men with rs1801133-GG and rs1801133-GG + AA genotypes were associated with lower HDL-C. Their β values were −7.9509 (p < 0.0001) and −7.2069 (p < 0.0001), respectively. The interaction between diet type and exercise exposure was significant only among those with the GG genotype (p = 0.0101). Compared with the non-vegetarian diet, vegetarian diet predicted a decrease in HDL-C in both GG and GA + AA individuals belonging to the exercise (β = −7.9361 and β = −4.5577, respectively, p < 0.05) and no exercise (β = −5.1297 and β = −4.6986, p < 0.0001) groups, respectively (Table 3). With non-vegetarian diet plus no exercise as the reference group, vegetarian diet/no exercise was associated with a 5.1514 mg/dl reduction in HDL-C among GG carriers (β = −5.1514, p < 0.0001) and a 4.8426 mg/dl decrease (β = −4.8426, p < 0.0001) among GA + AA carriers (Table 4). Likewise, a vegetarian diet/regular exercise was associated with a 6.5552 mg/dl reduction in HDL-C among GG carriers (β = −6.5552, p < 0.0001), and a 2.8668 mg/dl decrease in HDL-C among those with GA + AA genotypes. Regular exercise/non-vegetarian diet predicted a 1.3135 mg/dl (β = 1.3135, p < 0.0001) and 1.4301 mg/dl (β = 1.4301 p < 0.0002) reduction in HDL-C among GG and GA + AA individuals, respectively.
4. Discussion
As far as we understand, this study is the first to determine the relationship between HDL-C and a vegetarian diet together with exercise exposure in Taiwanese adults, based on MTHFR rs1801133 polymorphism. We found that exposure to exercise was linked to higher HDL-C levels in GG and GG + AA individuals, whereas the intake of vegetarian diets was associated with lower levels. Compared to a vegetarian diet alone, vegetarian diets combined with regular exercise led to much lower HDL-C levels among GG individuals, and comparatively higher levels among those with GA + AA genotype.
We believe that several studies have already examined associations between HDL-C, exercise and diets. However, such associations have not been analyzed based on the MTHFR rs1801133 polymorphism as we have done in the current study. In a systemic review [18], the rs1801133 polymorphic variant showed a strong association with lower HDL-C. The standard mean difference (SMD) was −0.10. In our study, we observed similar results in both GG and GA + AA individuals who were on vegetarian diets. As might have been expected, exercise exposure showed positive associations with HDL-C in individuals carrying both genotypes. The mechanism behind these associations needs to be further investigated. Despite this, exercise has been demonstrated to increase the expression of liver ATP-binding cassette transporters A-1, that help to strengthen the reverse cholesterol transport system as mentioned above. Exercise in combination with diet has been associated with biomarkers of metabolic disorders and variations in body composition [28]. However, the effective outcome of the combination was based on the exercise type.
In the current study, men had lower HDL-C compared to women, no matter the genotype. We also found that overweight/obese individuals had lower HDL-C levels than normal-weight individuals with both genotypes. Besides, high levels of triglycerides (TG) also predicted lower HDL-C. These findings are in line with those previously reported by Zhi and his team, wherein overweight and obesity were strongly associated with a higher TG but lower HDL-C in individuals with MTHFR rs1801133 genotypes [24]. Rs1801133 polymorphism has also been suggested to increase obesity risk in both adolescents and children [29]. Serum uric acid was also included in our model. We found that the uric acid levels did not differ greatly among the samples (Table S1). Our analyses also indicated that higher (i.e., men, ≥7 mg/dl and women, ≥6 mg/dl) compared to lower uric acid (men, <7 mg/dl and women, <6 mg/dl) was associated with lower HDL-C, no matter the genotype. Negative associations between serum uric acid and HDL-C have been previously described [30,31]. Of note, polymorphic variants were not included in the model as we have done.
It appears reasonable to state that exercise exposure is one of the great ways for vegetarians to boost their HDL cholesterol [16]. However, our investigation into this area suggests that the association of HDL-C with a vegetarian diet in combination with exercise appears to differ for each Taiwanese individual based on the genotype. Despite these findings, several shortfalls need to be considered. First, recall bias is possible in our study, considering that data on exercise patterns were collected based on self-report. Second, we did not have data on the average daily intake of macro and micronutrients. In addition, we could not present data that indicated how long participants might have followed a vegetarian diet. Moreover, our analyses had a total of 443 vegetarians, 35 of whom were vegans. Because of this, we could not perform a subgroup analysis separately for the vegans. However, we hope that our findings will serve as a base for future studies on HDL-C and the associated lifestyle and dietary changes.
5. Conclusions
In conclusion, our findings revealed that exercise exposure predicted a higher HDL-C among MTHFR rs1801133 GG and GA + AA individuals. A vegetarian diet alone was associated with lower HDL-C. However, the inclusion of regular exercise resulted in much lower levels among GG individuals, whereas levels in GA + AA individuals were somewhat higher. In summary, a vegetarian diet in combination with exercise predicted an increase in HDL-C levels only among individuals with MTHFR rs1801133-GA + AA genotype in Taiwan. These findings point to the likelihood that combination lifestyle therapies might not serve as an alternative means of boosting cholesterol levels in Taiwanese adults with the rs1801133-GG genotype.
Supplementary Materials
The following are available online at https://www.mdpi.com/2072-6643/12/6/1564/s1, Table S1: Mean serum uric acid (mg/dl) levels of the sample.
Author Contributions
Conceptualization, S.-L.C., O.N.N., C.-C.H., C.-C.L., D.M.T., S.-Y.H., M.-C.C. and Y.-P.L.; Data curation, W.-Y.L. and K.-J.L.; Formal analysis, W.-Y.L. and Y.-P.L.; Funding acquisition, K.-J.L.; Methodology, S.-L.C., O.N.N., C.-C.H., K.-J.L., C.-C.L., D.M.T., S.-Y.H., M.-C.C. and Y.-P.L.; Resources, Y.-P.L.; Supervision, M.-C.C. and Y.-P.L.; Validation, S.-L.C., O.N.N., C.-C.H., C.-C.L., D.M.T., W.-Y.L., S.-Y.H. and M.-C.C.; Writing—original draft, S.-L.C. and O.N.N.; Writing—review & editing, C.-C.H., K.-J.L., C.-C.L., D.M.T., S.-Y.H., W.-Y.L., M.-C.C. and Y.-P.L. All authors have read and agreed to the published version of the manuscript.
Funding
This study was supported by the Ministry of Science and Technology (MOST 105-2627-M-040-002; 106-2627-M-040-002; 107-2627-M-040-002).
Conflicts of Interest
The authors have no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
References
- Mann, S.; Beedie, C.; Jimenez, A. Differential effects of aerobic exercise, resistance training and combined exercise modalities on cholesterol and the lipid profile: Review, synthesis and recommendations. Sports Med. 2014, 44, 211–221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yusuf, S.; Hawken, S.; Ounpuu, S.; Dans, T.; Avezum, A.; Lanas, F.; McQueen, M.; Budaj, A.; Pais, P.; Varigos, J. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): Case-control study. Lancet 2004, 364, 937–952. [Google Scholar] [CrossRef]
- März, W.; Kleber, M.E.; Scharnagl, H.; Speer, T.; Zewinger, S.; Ritsch, A.; Parhofer, K.G.; von Eckardstein, A.; Landmesser, U.; Laufs, U. HDL cholesterol: Reappraisal of its clinical relevance. Clin. Res. Cardiol. 2017, 106, 663–675. [Google Scholar] [CrossRef] [Green Version]
- Parhofer, K.G. Interaction between glucose and lipid metabolism: More than diabetic dyslipidemia. Diabetes Metab. J. 2015, 39, 353–362. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shor, R.; Wainstein, J.; Oz, D.; Boaz, M.; Matas, Z.; Fux, A.; Halabe, A. Low HDL levels and the risk of death, sepsis and malignancy. Clin. Res. Cardiol. 2008, 97, 227–233. [Google Scholar] [CrossRef] [PubMed]
- Yeh, M.-C.; Glick-Bauer, M. Chapter 8—Vegetarian diets and disease outcomes. In Fruits, Vegetables, and Herbs; Watson, R.R., Preedy, V.R., Eds.; Academic Press: Cambridge, MA, USA, 2016; pp. 149–164. [Google Scholar]
- Picasso, M.C.; Lo-Tayraco, J.A.; Ramos-Villanueva, J.M.; Pasupuleti, V.; Hernandez, A.V. Effect of vegetarian diets on the presentation of metabolic syndrome or its components: A systematic review and meta-analysis. Clin. Nutr. 2019, 38, 1117–1132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, Y.-W.; Jian, Z.-H.; Chang, H.-C.; Nfor, O.N.; Ko, P.-C.; Lung, C.-C.; Lin, L.-Y.; Ho, C.-C.; Chiang, Y.-C.; Liaw, Y.-P. Vegan diet and blood lipid profiles: A cross-sectional study of pre and postmenopausal women. BMC Women’s Health 2014, 14, 55. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, F.; Zheng, J.; Yang, B.; Jiang, J.; Fu, Y.; Li, D. Effects of vegetarian diets on blood lipids: A systematic review and meta-analysis of randomized controlled trials. J. Am. Heart Assoc. 2015, 4, e002408. [Google Scholar] [CrossRef] [Green Version]
- Yokoyama, Y.; Levin, S.M.; Barnard, N.D. Association between plant-based diets and plasma lipids: A systematic review and meta-analysis. Nutr. Rev. 2017, 75, 683–698. [Google Scholar] [CrossRef]
- Sambol, S.Z.; Glišić, M.O.; Bašić, N.M.; Dvornik, Š; Grahovac, B.; Mihić, S.S.; Štimac, D. Influence of Dietary Pattern and Methylentetrahydrofolate Reductase C677t Polymorphism on the Plasma Homocysteine Level Among Healthy Vegetarians and Omnivores. Hrana Zdr. Boles. Znan. Stručni Časopis Za Nutr. Dijetetiku 2017, 6, 54–62. [Google Scholar]
- Kelley, G.A.; Kelley, K.S. Effects of diet, aerobic exercise, or both on non-HDL-C in adults: A meta-analysis of randomized controlled trials. Cholesterol 2012, 2012. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Drygas, W.; Kostka, T.; Jegier, A.; Kuski, H. Long-term effects of different physical activity levels on coronary heart disease risk factors in middle-aged men. Int. J. Sports Med. 2000, 21, 235–241. [Google Scholar] [CrossRef] [PubMed]
- Larrydurstine, J.; Haskell, W.L. Effects of exercise training on plasma lipids and lipoproteins. Exerc. Sport Sci. Rev. 1994, 22, 477–522. [Google Scholar] [CrossRef]
- MayoClinic.Com. HDL Cholesterol: How to Boost Your ‘Good’ Cholesterol. Available online: https://www.mayoclinic.org/diseases-conditions/high-blood-cholesterol/in-depth/hdl-cholesterol/art-20046388?pg=2 (accessed on 24 October 2018).
- Wang, Y.; Xu, D. Effects of aerobic exercise on lipids and lipoproteins. Lipids Health Dis. 2017, 16, 132. [Google Scholar] [CrossRef] [Green Version]
- Williams, P.T. Interactive effects of exercise, alcohol, and vegetarian diet on coronary artery disease risk factors in 9242 runners: The National Runners’ Health Study. Am. J. Clin. Nutr. 1997, 66, 1197–1206. [Google Scholar] [CrossRef] [Green Version]
- Luo, Z.; Lu, Z.; Muhammad, I.; Chen, Y.; Chen, Q.; Zhang, J.; Song, Y. Associations of the MTHFR rs1801133 polymorphism with coronary artery disease and lipid levels: A systematic review and updated meta-analysis. Lipids Health Dis. 2018, 17, 191. [Google Scholar] [CrossRef] [Green Version]
- Christensen, K.E.; Mikael, L.G.; Leung, K.-Y.; Lévesque, N.; Deng, L.; Wu, Q.; Malysheva, O.V.; Best, A.; Caudill, M.A.; Greene, N.D. High folic acid consumption leads to pseudo-MTHFR deficiency, altered lipid metabolism, and liver injury in mice. Am. J. Clin. Nutr. 2015, 101, 646–658. [Google Scholar] [CrossRef] [Green Version]
- Kukrele, P.; Sharma, R. High homocysteine level-An important risk factor for coronary artery disease in vegetarians. J. Assoc. Physicians India 2016, 64, 75. [Google Scholar]
- Frosst, P.; Blom, H.; Milos, R.; Goyette, P.; Sheppard, C.A.; Matthews, R.; Boers, G.; Den Heijer, M.; Kluijtmans, L.; Van Den Heuve, L. A candidate genetic risk factor for vascular disease: A common mutation in methylenetetrahydrofolate reductase. Nat. Genet. 1995, 10, 111. [Google Scholar] [CrossRef]
- Nie, Y.; Gu, H.; Gong, J.; Wang, J.; Gong, D.; Cong, X.; Chen, X.; Hu, S. Methylenetetrahydrofolate reductase C677T polymorphism and congenital heart disease: A meta-analysis. Clin. Chem. Lab. Med. (Cclm) 2011, 49, 2101–2108. [Google Scholar] [CrossRef]
- Tanaka, T.; Scheet, P.; Giusti, B.; Bandinelli, S.; Piras, M.G.; Usala, G.; Lai, S.; Mulas, A.; Corsi, A.M.; Vestrini, A. Genome-wide association study of vitamin B6, vitamin B12, folate, and homocysteine blood concentrations. Am. J. Hum. Genet. 2009, 84, 477–482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhi, X.; Yang, B.; Fan, S.; Wang, Y.; Wei, J.; Zheng, Q.; Sun, G. Gender-specific interactions of MTHFR C677T and MTRR A66G polymorphisms with overweight/obesity on serum lipid levels in a Chinese Han population. Lipids Health Dis. 2016, 15, 185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Iemitsu, M.; Murakami, H.; Sanada, K.; Yamamoto, K.; Kawano, H.; Gando, Y.; Miyachi, M. Lack of carotid stiffening associated with MTHFR 677TT genotype in cardiorespiratory fit adults. Physiol. Genom. 2010, 42, 259–265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chang, S.-L.; Lee, K.-J.; Nfor, O.N.; Chen, P.-H.; Lu, W.-Y.; Ho, C.C.; Lung, C.-C.; Chou, M.-C.; Liaw, Y.-P. Vegetarian Diets along with Regular Exercise: Impact on High-Density Lipoprotein Cholesterol Levels among Taiwanese Adults. Medicina 2020, 56, 74. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tantoh, D.M.; Lee, K.-J.; Nfor, O.N.; Liaw, Y.-C.; Lin, C.; Chu, H.-W.; Chen, P.-H.; Hsu, S.-Y.; Liu, W.-H.; Ho, C.-C. Methylation at cg05575921 of a smoking-related gene (AHRR) in non-smoking Taiwanese adults residing in areas with different PM 2.5 concentrations. Clin. Epigenetics 2019, 11, 69. [Google Scholar] [CrossRef]
- Clark, J.E. Diet, exercise or diet with exercise: Comparing the effectiveness of treatment options for weight-loss and changes in fitness for adults (18–65 years old) who are overfat, or obese; systematic review and meta-analysis. J. Diabetes Metab. Disord. 2015, 14, 31. [Google Scholar] [CrossRef] [Green Version]
- Borai, I.H.; Soliman, A.F.; Ahmed, H.M.; Ahmed, G.F.; Kassim, S.K. Association of MTHFR C677T and ABCA1 G656A polymorphisms with obesity among Egyptian children. Gene Rep. 2018, 11, 143–149. [Google Scholar] [CrossRef]
- Son, M.; Seo, J.; Yang, S. Association between dyslipidemia and serum uric acid levels in Korean adults: Korea National Health and Nutrition Examination Survey 2016–2017. PLoS ONE 2020, 15, e0228684. [Google Scholar] [CrossRef]
- Ali, N.; Rahman, S.; Islam, S.; Haque, T.; Molla, N.H.; Sumon, A.H.; Kathak, R.R.; Asaduzzaman, M.; Islam, F.; Mohanto, N.C. The relationship between serum uric acid and lipid profile in Bangladeshi adults. BMC Cardiovasc. Disord. 2019, 19, 42. [Google Scholar] [CrossRef] [Green Version]
Table 1.
Demographic characteristics of participants grouped by rs1801133 genotypes.
| Variable | rs1801133-GG (n = 5016) | rs1801133-GA + AA (n = 4239) | p-Value | ||
|---|---|---|---|---|---|
| N | Mean HDL-C (SE) | N | Mean HDL-C (SE) | ||
| Diet type | 0.9828 | ||||
| Non-vegetarian | 4542 | 54.056 (0.198) | 3842 | 54.010 (0.214) | |
| Former vegetarian | 232 | 54.297 (0.953) | 196 | 53.510 (0.960) | |
| Vegetarian | 242 | 49.591 (0.707) | 201 | 50.010 (0.867) | |
| Exercise | 0.8657 | ||||
| No | 2909 | 53.146 (0.244) | 2451 | 52.993 (0.262) | |
| Yes | 2107 | 54.826 (0.294) | 1788 | 54.900 (0.320) | |
| Sex | 0.5662 | ||||
| Women | 2690 | 58.455 (0.255) | 2248 | 58.363 (0.280) | |
| Men | 2326 | 48.529 (0.234) | 1991 | 48.642 (0.249) | |
| Age (years) | 0.9905 | ||||
| 30–40 | 1313 | 53.998 (0.364) | 1102 | 53.786 (0.394) | |
| 41–50 | 1407 | 53.684 (0.352) | 1182 | 53.483 (0.387) | |
| 51–60 | 1437 | 53.446 (0.353) | 1224 | 54.227 (0.377) | |
| 61–70 | 859 | 54.582 (0.462) | 731 | 53.603 (0.498) | |
| TG (mg/dl) | 0.0046 | ||||
| <150 | 3896 | 56.711 (0.207) | 3395 | 56.300 (0.223) | |
| ≥150 | 1120 | 43.907 (0.273) | 844 | 43.732 (0.297) | |
| LDL-C (mg/dl) | 0.6191 | ||||
| <130 | 3069 | 54.185 (0.257) | 2615 | 54.001 (0.270) | |
| ≥130 | 1947 | 53.327 (0.265) | 1624 | 53.470 (0.304) | |
| WHR | 0.0770 | ||||
| Men < 0.9; women < 0.85 (ref) | 2757 | 56.636 (0.259) | 2252 | 56.206 (0.288) | |
| Men ≥ 0.9; women ≥ 0.85 | 2259 | 50.455 (0.255) | 1987 | 51.067 (0.273) | |
| Body mass index, kg/m2 | 0.0233 | ||||
| 18.5–23.9 (ref) | 2489 | 58.039 (0.265) | 1969 | 57.837 (0.298) | |
| <18.5 | 128 | 66.828 (1.278) | 108 | 65.204 (1.391) | |
| 24–26.9 | 1443 | 50.338 (0.309) | 1298 | 51.276 (0.330) | |
| ≥27 | 956 | 46.517 (0.319) | 864 | 46.953 (0.360) | |
| Body fat (%) | 0.1882 | ||||
| Men < 25; women < 30 (ref) | 2711 | 55.969 (0.268) | 2233 | 55.456 (0.288) | |
| Men ≥ 25; women ≥ 30 | 2305 | 51.363 (0.251) | 2006 | 51.951 (0.280) | |
| Smoking | 0.3176 | ||||
| Nonsmokers | 3893 | 55.378 (0.213) | 3281 | 55.468 (0.233) | |
| Former smokers | 568 | 49.889 (0.513) | 516 | 48.953 (0.476) | |
| Current smokers | 555 | 47.205 (0.500) | 442 | 47.048 (0.549) | |
| Alcohol intake | 0.2371 | ||||
| nondrinkers | 4495 | 54.211 (0.197) | 3820 | 54.199 (0.216) | |
| Former drinkers | 160 | 45.531 (0.821) | 110 | 48.036 (1.005) | |
| Current drinkers | 361 | 53.066 (0.755) | 309 | 50.883 (0.658) | |
| Coffee drinking | 0.4381 | ||||
| No | 3333 | 53.361 (0.227) | 2849 | 53.448 (0.247) | |
| Yes | 1683 | 54.825 (0.332) | 1390 | 54.514 (0.356) | |
| Uric acid, mg/dl | 0.0334 | ||||
| men < 7, women < 6 (ref) | 3851 | 55.528 (0.217) | 3174 | 55.665 (0.236) | |
| men ≥ 7, women ≥ 6 | 1165 | 48.311 (0.328) | 1065 | 48.230 (0.350) | |
SE: standard error; WHR: waist-to-hip ratio; BMI: Body mass index; TG: triglyceride; LDL-C: Low-density lipoprotein cholesterol; HDL-C: High-density lipoprotein cholesterol.
Table 2.
Regression coefficients of lifestyle variables associated with HDL-C according to rs1801133 genotypes.
Table 2.
Regression coefficients of lifestyle variables associated with HDL-C according to rs1801133 genotypes.
| Variables | rs1801133-GG | rs1801133-GA + AA | ||
|---|---|---|---|---|
| β | p-Value | β | p-Value | |
| Diet type (ref: Non-vegetarian) | ||||
| Former vegetarian | −0.1917 | 0.7918 | −0.3995 | 0.6222 |
| Vegetarian | −6.2793 | <0.0001 | −4.6359 | <0.0001 |
| p-trend | <0.0001 | <0.0001 | ||
| Exercise (ref: No) | ||||
| Yes | 1.0508 | 0.0015 | 1.4011 | 0.0001 |
| Sex (ref: women) | ||||
| Men | −7.9509 | <0.0001 | −7.2069 | <0.0001 |
| Age (ref: 30–40) | ||||
| 41–50 | 0.5879 | 0.1630 | 0.5495 | 0.2453 |
| 51–60 | 1.0893 | 0.0131 | 1.2023 | 0.0149 |
| 61–70 | 1.7187 | 0.0009 | 1.0543 | 0.0673 |
| TG (ref: <150) | ||||
| ≥150 | −8.2129 | <0.0001 | −8.1116 | <0.0001 |
| LDL-C (ref: <130) | ||||
| ≥130 | 1.1095 | 0.0005 | 1.4316 | 0.0001 |
| WHR (ref: men < 0.9; women < 0.85) | ||||
| Men ≥ 0.9; women ≥ 0.85 | −2.6110 | <0.0001 | −2.4022 | <0.0001 |
| Body mass index, kg/m2 (ref: 18.5–23.9) | ||||
| <18.5 | 6.2828 | <0.0001 | 5.7646 | <0.0001 |
| 24–26.9 | −3.6743 | <0.0001 | −3.1293 | <0.0001 |
| ≥27 | −4.5426 | <0.0001 | −5.0012 | <0.0001 |
| Body fat (ref: Men < 25; women < 30) | ||||
| Men ≥ 25; women ≥ 30 | −1.9773 | <0.0001 | −0.6996 | 0.1201 |
| Smoking (ref: Nonsmokers) | ||||
| Former smokers | −0.0117 | 0.9824 | −0.9565 | 0.0988 |
| Current smokers | −2.7451 | <0.0001 | −1.9437 | 0.0019 |
| Alcohol intake (ref: Nondrinkers) | ||||
| Former drinkers | −1.0938 | 0.2265 | −0.4513 | 0.6793 |
| Current drinkers | 6.0734 | <0.0001 | 3.5075 | <0.0001 |
| Coffee drinking (ref: No) | ||||
| Yes | 0.7415 | 0.0230 | 0.5075 | 0.1650 |
| Uric acid, mg/dl (ref: men < 7, women <6) | ||||
| men ≥ 7, women ≥ 6 | −1.5541 | 0.0001 | −2.1708 | <0.0001 |
Table 3.
Association of vegetarian diet with HDL-C based on rs1801133 genotypes and exercise exposure.
Table 3.
Association of vegetarian diet with HDL-C based on rs1801133 genotypes and exercise exposure.
| Variables | rs1801133-GG | rs1801133-GA + AA | ||||||
|---|---|---|---|---|---|---|---|---|
| No Exercise | Exercise | No Exercise | Exercise | |||||
| β | p-Value | β | p-Value | β | p-Value | β | p-Value | |
| Diet type (ref: Non-vegetarian) | ||||||||
| Former vegetarian | 0.8314 | 0.3476 | −2.0019 | 0.1127 | 0.0519 | 0.9581 | −1.3033 | 0.3485 |
| Vegetarian | −5.1297 | <0.0001 | −7.9361 | <0.0001 | −4.6986 | <0.0001 | −4.5577 | 0.0008 |
| p-trend | <0.0001 | <0.0001 | <0.0001 | 0.0007 | ||||
| Sex (ref: women) | ||||||||
| Men | −8.1078 | <0.0001 | −7.7185 | <0.0001 | −6.6446 | <0.0001 | −8.0869 | <0.0001 |
| Age (ref: 30–40) | ||||||||
| 41–50 | 0.4769 | 0.3248 | 0.7870 | 0.3552 | 1.0190 | 0.0585 | −0.8985 | 0.3522 |
| 51–60 | 1.1302 | 0.0369 | 0.9529 | 0.2370 | 1.9337 | 0.0015 | −0.1497 | 0.8691 |
| 61–70 | 1.5450 | 0.0371 | 1.6555 | 0.0523 | 0.3052 | 0.6980 | 0.6124 | 0.5294 |
| TG (ref: <150) | ||||||||
| ≥150 | −7.7074 | <0.0001 | −8.9542 | <0.0001 | −7.7816 | <0.0001 | −8.6927 | <0.0001 |
| LDL-C (ref: <130) | ||||||||
| ≥130 | 1.0732 | 0.0102 | 1.1117 | 0.0276 | 2.1314 | <0.0001 | 0.4474 | 0.4294 |
| WHR (ref: Men < 0.9; women < 0.85) | ||||||||
| Men ≥ 0.9; women ≥ 0.85 | −2.6070 | <0.0001 | −2.6692 | <0.0001 | −2.5188 | <0.0001 | −2.4311 | 0.0001 |
| Body mass index, kg/m2 (ref: 18.5–23.9) | ||||||||
| BMI < 18.5 | 6.1337 | <0.0001 | 6.6755 | 0.0002 | 4.6449 | 0.0002 | 9.2076 | <0.0001 |
| 24–26.9 | −3.6149 | <0.0001 | −3.7077 | <0.0001 | −3.2793 | <0.0001 | −2.9512 | <0.0001 |
| ≥27 | −4.0139 | <0.0001 | −5.3350 | <0.0001 | −5.3062 | <0.0001 | −4.5617 | <0.0001 |
| Body fat (ref: Men < 25; women < 30) | ||||||||
| Men ≥ 25; women ≥ 30 | −2.2468 | <0.0001 | −1.6160 | 0.0119 | −0.7847 | 0.1727 | −0.6886 | 0.3386 |
| Smoking (ref: Nonsmokers) | ||||||||
| Former smokers | −0.1570 | 0.8269 | 0.1372 | 0.8636 | −1.0469 | 0.1701 | −0.5860 | 0.5120 |
| Current smokers | −2.8800 | <0.0001 | −2.5990 | 0.0096 | −2.6090 | 0.0004 | −1.0954 | 0.3494 |
| Alcohol intake (ref: Nondrinkers) | ||||||||
| Former drinkers | −0.7260 | 0.5865 | −1.4799 | 0.2390 | −1.3610 | 0.3676 | 0.6249 | 0.6957 |
| Current drinkers | 6.5085 | <0.0001 | 5.3821 | <0.0001 | 4.8254 | <0.0001 | 1.8587 | 0.0967 |
| Coffee drinking (ref: No) | ||||||||
| Yes | 0.9987 | 0.0167 | 0.3849 | 0.4616 | 0.5014 | 0.2790 | 0.5678 | 0.3391 |
| Uric acid, mg/dl (ref: men < 7, women < 6) | ||||||||
| men ≥ 7, women ≥ 6 | −1.3670 | 0.0065 | −1.7314 | 0.0044 | −1.8402 | 0.0006 | −2.7109 | 0.0001 |
β: beta coefficient; WHR: waist-to-hip ratio; BMI: Body mass index: TG triglyceride; LDL-C: Low-density lipoprotein cholesterol; HDL-C: High-density lipoprotein cholesterol.
Table 4.
Exercise exposure together with vegetarian diets and their association with HDL-C.
| Variables | rs1801133-GG | rs1801133-GA + AA | ||
|---|---|---|---|---|
| β | p-Value | β | p-Value | |
| Exercise and Diet type (ref: no exercise/non-vegetarian) | ||||
| No exercise/Former vegetarian | 0.8068 | 0.3724 | 0.0541 | 0.9577 |
| No exercise/Vegetarian | −5.1514 | <0.0001 | −4.8426 | <0.0001 |
| Regular exercise/non-vegetarian | 1.3135 | 0.0001 | 1.4301 | 0.0002 |
| Regular exercise/Former vegetarian | −0.6585 | 0.5862 | 0.2568 | 0.8464 |
| Regular exercise/Vegetarian | −6.5552 | <0.0001 | −2.8668 | 0.0273 |
| Sex (ref: women) | ||||
| Men | −7.9224 | <0.0001 | −7.2075 | <0.0001 |
| Age (ref: 30–40) | ||||
| 41–50 | 0.6059 | 0.1504 | 0.5663 | 0.2317 |
| 51–60 | 1.0645 | 0.0153 | 1.2121 | 0.0142 |
| 61–70 | 1.6897 | 0.0011 | 1.0612 | 0.0656 |
| TG (ref: <150) | ||||
| ≥150 | −8.2103 | <0.0001 | −8.1141 | <0.0001 |
| LDL-C (ref: <130) | ||||
| ≥130 | 1.1034 | 0.0006 | 1.4310 | 0.0001 |
| WHR (ref: Men < 0.9; women < 0.85) | ||||
| Men ≥ 0.9; women ≥ 0.85 | −2.6201 | <0.0001 | −2.4058 | <0.0001 |
| Body mass index, kg/m2 (ref: 18.5–23.9) | ||||
| <18.5 | 6.3076 | <0.0001 | 5.7872 | <0.0001 |
| 24–26.9 | −3.6710 | <0.0001 | −3.1217 | <0.0001 |
| ≥27 | −4.5409 | <0.0001 | −4.9955 | <0.0001 |
| Body fat (ref: Men < 25; women < 30) | ||||
| Men ≥ 25; women ≥ 30 | −1.9766 | <0.0001 | −0.6998 | 0.1200 |
| Smoking (ref: Nonsmokers) | ||||
| Former smokers | −0.0321 | 0.9518 | −0.9705 | 0.0942 |
| Current smokers | −2.7519 | <0.0001 | −1.9387 | 0.0020 |
| Alcohol intake (ref: Nondrinkers) | ||||
| Former drinkers | −1.1352 | 0.2093 | −0.4382 | 0.6882 |
| Current drinkers | 6.0677 | <0.0001 | 3.5075 | <0.0001 |
| Coffee drinking (ref: No) | ||||
| Yes | 0.7495 | 0.0215 | 0.5110 | 0.1625 |
| Uric acid, mg/dl (ref: men < 7, women < 6) | ||||
| men ≥ 7, women ≥ 6 | −1.5389 | 0.0001 | −2.1757 | <0.0001 |
β: beta coefficient; WHR: waist-to-hip ratio; BMI: Body mass index: TG triglyceride; LDL-C: Low-density lipoprotein cholesterol; HDL-C: High-density lipoprotein cholesterol.
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
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Chang, S.-L.; Nfor, O.N.; Ho, C.-C.; Lee, K.-J.; Lu, W.-Y.; Lung, C.-C.; Tantoh, D.M.; Hsu, S.-Y.; Chou, M.-C.; Liaw, Y.-P. Combination of Exercise and Vegetarian Diet: Relationship with High Density-Lipoprotein Cholesterol in Taiwanese Adults Based on MTHFR rs1801133 Polymorphism. Nutrients 2020, 12, 1564. https://doi.org/10.3390/nu12061564
AMA Style
Chang S-L, Nfor ON, Ho C-C, Lee K-J, Lu W-Y, Lung C-C, Tantoh DM, Hsu S-Y, Chou M-C, Liaw Y-P. Combination of Exercise and Vegetarian Diet: Relationship with High Density-Lipoprotein Cholesterol in Taiwanese Adults Based on MTHFR rs1801133 Polymorphism. Nutrients. 2020; 12(6):1564. https://doi.org/10.3390/nu12061564
Chicago/Turabian StyleChang, Shu-Lin, Oswald Ndi Nfor, Chien-Chang Ho, Kuan-Jung Lee, Wen-Yu Lu, Chia-Chi Lung, Disline Manli Tantoh, Shu-Yi Hsu, Ming-Chih Chou, and Yung-Po Liaw. 2020. "Combination of Exercise and Vegetarian Diet: Relationship with High Density-Lipoprotein Cholesterol in Taiwanese Adults Based on MTHFR rs1801133 Polymorphism" Nutrients 12, no. 6: 1564. https://doi.org/10.3390/nu12061564
APA StyleChang, S. -L., Nfor, O. N., Ho, C. -C., Lee, K. -J., Lu, W. -Y., Lung, C. -C., Tantoh, D. M., Hsu, S. -Y., Chou, M. -C., & Liaw, Y. -P. (2020). Combination of Exercise and Vegetarian Diet: Relationship with High Density-Lipoprotein Cholesterol in Taiwanese Adults Based on MTHFR rs1801133 Polymorphism. Nutrients, 12(6), 1564. https://doi.org/10.3390/nu12061564
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