Abstract
Background
Being a major cardiovascular risk factor, dyslipidemia is a critical problem in public health. Recommendations in performing regular physical exercise are important to prevent dyslipidemia.
Methods
Based on a discovery cohort with 27,735 subjects and a replication cohort with 67,512 subjects, we evaluated the associations of regularly performing 23 exercises with 4 dyslipidemia indices measured from serum, including triglyceride (TG), low-density lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), and TG/HDL-C ratio. Regular exercise was defined as performing 30 min of “exercise” three times a week. “Exercise” includes leisure-time activities such as jogging, swimming, etc. Sex, age, body mass index, alcohol drinking, cigarette smoking, and education level were adjusted in all statistical analyses.
Results
Among the 23 exercises, only jogging was associated with a decreased level of TG (95% confidence interval [C.I.] = 5.9–14.5 mg/dL) and TG/HDL-C ratio (95% C.I. = 0.22–0.49). A total of 5 exercises were associated with an increased level of HDL-C, including jogging (95% C.I. = 2.1–3.3 mg/dL), swimming (95% C.I. = 1.6–3.3 mg/dL), dance dance revolution (95% C.I. = 1.5–3.4 mg/dL), international standard dancing (95% C.I. = 1.0–2.7 mg/dL), and cycling (95% C.I. = 0.6–1.8 mg/dL). These significant findings were further well replicated in the cohort of 67,512 subjects.
Conclusion
Regular jogging was not only associated with an increased level of HDL-C, but also the only one exercise associated with a decreased level of TG and TG/HDL-C ratio. Nonetheless, jogging may be difficult to engage in for subjects with limited exercise capacity. We here found that swimming, dancing, and cycling are also significantly associated with an increased level of HDL-C. People who are seeking exercise to improve their lipoprotein-lipid profiles can have other choices now.
Background
Dyslipidemia is an unhealthy level of lipids in blood, including elevated triglyceride (TG) or low-density lipoprotein cholesterol (LDL-C), and decreased high-density lipoprotein cholesterol (HDL-C). Moreover, the ratio of TG to HDL-C (TG/HDL-C ratio) is a useful indicator to detect metabolic syndrome [Citation1].
Around ~ 25% of people in the United States are living with hypertriglyceridemia (TG > 150 mg/dL), which is a type of dyslipidemia and is associated with an increased risk of cardiovascular diseases [Citation2]. According to the Ministry of Health and Welfare in Taiwan, a TG level > 150 mg/dL; an LDL-C level > 130 mg/dL; a HDL-C level < 40 mg/dL for males or a HDL-C level < 50 mg/dL for females, are considered dyslipidemia. As a major cardiovascular risk factor, dyslipidemia is a critical problem in public health. Lifestyle modification such as performing physical exercise is a low-cost and non-pharmacological strategy to improve one’s lipoprotein-lipid profile.
Studies have shown that TG decreased and HDL-C increased after 24 h of aerobic exercise training, and lasted through 48 h [Citation3]. Some studies found that HDL-C is more sensitive to aerobic exercise than TG and LDL-C [Citation4]. Regular exercise increases the level of HDL-C in a dose-response manner [Citation5–Citation8]. Almost all studies indicated that exercise increases HDL-C to some degree, which is a consistent result from both human [Citation4, Citation9–Citation13] and rats [Citation14–Citation16]. Moreover, regular exercise was found to improve “cholesterol efflux capacity”, the ability of HDL-C to carry cholesterol from one’s bloodstream to the liver for clearance [Citation17].
Different from HDL-C, exercise effects on LDL-C have been inconsistent across studies. Some studies even provided completely contradictory results [Citation4, Citation9–Citation12]. It has been suggested that exercise alone may not lower LDL-C, unless a loss of body weight is also achieved in this period of time [Citation18]. Other studies concluded that, compared with HDL-C, exercise with a higher intensity is required to reduce the level of LDL-C and TG [Citation19].
Despite many randomized controlled trials (RCTs) related to this topic, the investigated aerobic exercises were limited to walking, cycling, or jogging [Citation7, Citation9–Citation12, Citation20, Citation21]. Very few studies have evaluated the effects of other aerobic exercises such as dancing, mountain climbing, swimming, playing tennis, etc. Moreover, it remains unknown which exercises are more related to a lower risk of dyslipidemia.
To address this issue, we applied data of 95,247 Taiwan Biobank (TWB) participants to evaluate the associations of regular exercise with their TG, LDL-C, HDL-C, and TG/HDL-C levels. The 95,247 TWB subjects were genotyped by one of two single-nucleotide polymorphism arrays. Therefore, by nature, we separated them into a discovery cohort and a replication cohort according to their genotyping arrays.
In this study, we aim to identify exercises that are associated with a lower risk of dyslipidemia according to the discovery cohort, and then we seek replication from the replication cohort. While most previous studies were RCTs with limited sample sizes and exercise kinds [Citation7, Citation9–Citation12, Citation21], this work is an observational study with a much larger sample size and more than 20 kinds of exercise.
Methods
Taiwan biobank
From October 2012 to February 2020, TWB recruited 95,247 Taiwan residents aged 30 to 70 years. Among the 95,247 subjects, 27,735 and 67,512 subjects were whole-genome genotyped by the TWB1 and TWB2 genotyping arrays, separately. They were so-called the TWB1 and TWB2 cohorts, respectively [Citation22]. Although the current study includes no genetic analysis, the two cohorts formed a natural separation of a discovery set and a replication set. We here used the 27,735 subjects genotyped by the TWB1 array as the discovery cohort and the 67,512 subjects genotyped by the TWB2 array as the replication cohort. After signing informed consent, these 95,247 community-based volunteers provided blood and urine samples, took physical examinations, and reported lifestyle factors (regular exercise, alcohol drinking, and cigarette smoking) through a face-to-face interview with TWB researchers [Citation23].
TWB was approved by the Institutional Review Board on Biomedical Science Research/IRB-BM, Academia Sinica, and also by the Ethics and Governance Council of Taiwan Biobank, Taiwan. Written informed consent was obtained before data collection, from each participant in accordance with institutional requirements and the principles of the Declaration of Helsinki. Our use of the TWB research data was approved by TWB on February 18, 2020 (application number: TWBR10810–07). This study further received approval from the Research Ethics Committee of National Taiwan University Hospital (NTUH-REC no. 201805050RINB).
Dyslipidemia indices
We analyzed 3 indices that are related to dyslipidemia: TG, LDL-C, and HDL-C, all measured from serum. HDL-C is considered as “good cholesterol” in the sense that a higher level of HDL-C is linked to a lower risk of coronary heart disease [Citation24]. On the contrary, LDL-C is usually regarded as the “bad” type of cholesterol [Citation25]. A TG level < 150 mg/dL, an LDL-C level < 130 mg/dL, and a HDL-C level > 40 mg/dL for males or a HDL-C level > 50 mg/dL for females, are considered desirable [Citation26]. In addition to these 3 dyslipidemia indices, we also investigated TG/HDL-C ratio, which is a useful indicator of metabolic syndrome [Citation1]. An elevated TG/HDL-C ratio is strongly associated with an increased risk of adverse cardiac events [Citation27].
Covariates under adjustment
Sex, age, obesity, alcohol drinking, cigarette smoking, and education level are closely related to dyslipidemia [Citation28]. Therefore, our regression model adjusted sex, age (in years), body mass index (BMI), drinking status (yes vs. no), smoking status (yes vs. no), and educational attainment (a value ranging from 1 to 7). In TWB, drinking was defined as a subject having a weekly intake of more than 150 mL of alcohol for at least 6 months and having not stopped drinking at the time his/her phenotypes were measured. Smoking was defined as a subject who had smoked for at least 6 months and had not quit smoking at the time his/her phenotypes were measured.
Educational attainment was recorded according to a face-to-face interview with TWB researchers, ranging from 1 to 7: 1 “illiterate”, 2 “no formal education but literate”, 3 “primary school graduate”, 4 “junior high school graduate”, 5 “senior high school graduate”, 6 “college graduate”, and 7 “Master’s or higher degree”.
Regular exercise was defined as performing 30 min of “exercise” three times a week. “Exercise” includes leisure-time activities such as jogging, swimming, dancing, cycling, mountain climbing, weight training, etc. Individuals with regular exercise would then be asked what kinds of exercise they usually engaged in.
Statistical analysis
To investigate exercise effects on the 4 dyslipidemia indices, we considered the following regression model: 1 1 where Y k is dyslipidemia index k (k = 1, 2, 3, or 4), E j is an indicator variable taking a value of 1 or 0 (E j = 1 if the subject chose exercise j as the regular exercise, and j = 1, ⋯, 23), Covariate v is the v th covariate (v = 1, ⋯, 6), and ε is the random error term. Exercise j will be claimed to exhibit effects on index k if the p-value of vs. is less than , which is the Bonferroni-corrected significance level considering 30 regression coefficients () in model (1) and 4 dyslipidemia indices. All analyses were performed using R version 4.0.3.
Results
Basic characteristics of the TWB subjects
Among the 95,247 TWB subjects, 27,735 were classified into the discovery cohort whereas 67,512 the replication cohort. Table presents the basic characteristics of these two cohorts, stratified by sexes. The discovery (replication) cohort shows that 28.6% (29.6%) males and 13.8% (15.9%) females had TG > 150 mg/dL; 38.3% (36.4%) males and 33.6% (35.3%) females had LDL-C > 130 mg/dL; 22.7% (23.2%) males had HDL-C < 40 mg/dL and 27.6% (27.8%) females had HDL-C < 50 mg/dL. The replication cohort presents similar results (Table ).
To assess exercise effects while adjusting for covariates, we fitted model (1) for the 4 dyslipidemia indices, respectively. The results were presented in Tables and . We used the “car” package (https://cran.r-project.org/web/packages/car/) to compute variance inflation factor (VIF). The VIFs under 8 models (4 dyslipidemia indices in 2 cohorts) were all smaller than 2. This suggests that multicollinearity between variables in model (1) is acceptable.
Table shows the associations of 6 covariates with each dyslipidemia index, respectively. As mentioned above, a p-value less than 0.0004 is considered significant throughout this work. Female had a lower mean TG by 18.5 mg/dL (95% confidence interval [C.I.] = 16.2–20.8) and a higher mean HDL-C by 8.2 mg/dL (95% C.I. = 7.9–8.5) than males. Elder subjects had increased TG and LDL-C levels than younger subjects, but no significant association of age with HDL-C was observed (p = 0.13 and 0.04 in the discovery cohort and the replication cohort, respectively).
A strong association was found in BMI and all indices. A larger BMI was associated with increased TG, and LDL-C levels, and a decreased HDL-C level. Alcohol drinking was associated with elevated TG and HDL-C levels, and a decreased LDL-C level. The relationship between alcohol consumption and health outcomes remains controversial. On the contrary, cigarette smoking is consistently adverse to health by being associated with increased TG and LDL-C levels, and decreased HDL-C level. A higher education attainment was associated with a lower TG level.
Associations of performing exercises with dyslipidemia indices
Table shows the associations of performing each exercise with 4 dyslipidemia indices, respectively. We also presented the effect sizes () in Figs. , , and . Performing exercise was generally associated with a decreased level in TG (Fig. ) and an increased level in HDL-C (Fig. ). However, no significant associations were detected between any exercise and LDL-C (Table and Fig. ).
Subjects choosing jogging as their regular exercise had a lower TG level by 10.2 mg/dL (95% C.I. = 5.9–14.5), a higher HDL-C level by 2.7 mg/dL (95% C.I. = 2.1–3.3), and a decreased TG/HDL-C ratio by 0.36 (95% C.I. = 0.22–0.49). Moreover, swimming (95% C.I. = 1.6–3.3), dance dance revolution (DDR) (95% C.I. = 1.5–3.4), international standard dancing (95% C.I. = 1.0–2.7), and cycling (95% C.I. = 0.6–1.8) were associated with an increased level in HDL-C. These significant findings were well replicated in the TWB2 cohort, and the effect sizes () were similar across the TWB1 and TWB2 cohorts (Table ).
Discussion
This is a large-scale observational study evaluating the associations of regularly performing physical exercises with lipoprotein-lipid profiles. In line with the previous studies [Citation4, Citation19], we here also found that HDL-C is the most sensitive index to exercise among the 3 dyslipidemia measures. Performing regular exercise has been found to improve HDL-C functionality, including cholesterol efflux capacity, anti-oxidative, and anti-inflammatory properties [Citation17]. Cholesterol efflux capacity is a measure of the ability for a subject’s HDL-C to extract cholesterol from macrophages [Citation29]. Moreover, exercise elevates lipid peroxide transport function of HDL-C [Citation17, Citation30]. Finally, exercise training increased the ability of HDL-C to protect endothelial cells from injury [Citation31].
Existing evidence on LDL-C response to aerobic exercises remains contradictory and inconsistent [Citation9–Citation12]. A number of studies have concluded that exercise has little effect on LDL-C unless combined with dietary change and weight loss [Citation4, Citation32–Citation34]. In this work, we have not found any significant association between LDL-C and physical exercise (Fig. ).
Some RCTs have investigated exercise effects on dyslipidemia [Citation20]. RCTs are usually small to medium in sample sizes, say, from 12 to 111 subjects [Citation7, Citation9–Citation12, Citation21]. Moreover, the kinds of exercise examined in RCTs are typically limited [Citation7]. For example, LeMura et al. compared aerobic exercise with “resistance exercise” (or “strength training”) [Citation9]. In that study, aerobic exercise included cycling, walking, and jogging; resistance exercise indicated weight training [Citation9]. In a meta-analysis evaluating the efficacy of aerobic exercises on HDL-C [Citation7], 22 out of 25 RCTs investigated the effects of walking, jogging, or cycling. Among aerobic exercises, these three kinds of exercise were commonly studied.
In this study, all the 5 exercises found to be associated with a healthier lipoprotein-lipid profile (i.e., jogging, swimming, DDR, international standard dancing, and cycling, as shown in Fig. ) were examples of aerobic exercise. Another type of exercise, resistance exercise such as weight training, has not been found to improve people’s lipoprotein-lipid profile [Citation9]. In line with this previous finding [Citation9], we here did not observe any significant association between weight training and the 4 dyslipidemia indices.
While resistance exercise aims at increasing strength of muscles, aerobic exercise increases oxygen consumption without significantly changing strength [Citation35, Citation36]. Aerobic exercise increases the activity of lipoprotein lipase (LPL) [Citation37, Citation38], an enzyme produced by skeletal muscles and adipose tissues [Citation39]. LPL can reduce circulating TG in the bloodstream [Citation40]. Among aerobic exercises, jogging is especially a full-body exercise involving many body parts. To jog, one’s arms swing, legs and feet run, shoulders and abdomen are also involved in this continuous movement. As an aerobic endurance exercise, jogging can more effectively boost oxygen consumption and blood circulation [Citation41]. A jogging training lasting for 12 weeks has been shown to increase serum LPL concentrations [Citation42], which further facilitates the clearance of circulating TG and elevation of HDL-C level [Citation43].
A limitation of this work is that exercise intensity (usually monitored by the percentage of one’s maximum heart rate) could not be monitored as what was done in RCTs. Although this is an observational study and all signals were explained as associations, many of our results were consistent with the results from previous RCTs [Citation9–Citation12]. Moreover, this is the first large-scale observational study linking various kinds of physical exercise to people’s lipoprotein-lipid profile.
Conclusion
Our significant findings here were identified by the discovery cohort of 27,735 subjects and further well replicated by the replication cohort of 67,512 subjects. Through our analysis, we showed that regular jogging was not only associated with an increased level of HDL-C, but also the only one exercise associated with a decreased level of TG and TG/HDL-C ratio. Nonetheless, jogging may be difficult to engage in for subjects with limited exercise capacity. We here found that swimming, dancing (including DDR and international standard dancing), and cycling are also significantly associated with an increased level of HDL-C. People who are seeking exercise to improve their lipoprotein-lipid profiles can have other choices now.
Author’s contributions
W.-Y.L. conceived the study design, applied for the Taiwan Biobank (TWB) data, developed the analysis tool, analyzed the TWB data, and wrote the manuscript. The author read and approved the final manuscript.
Declarations
Ethics approval and consent to participate
Taiwan Biobank (TWB) was approved by the Institutional Review Board on Biomedical Science Research/IRB-BM, Academia Sinica, and also by the Ethics and Governance Council of Taiwan Biobank, Taiwan. Written informed consent was obtained before data collection, from each participant in accordance with institutional requirements and the principles of the Declaration of Helsinki. Our use of the TWB research data was approved by TWB on February 18, 2020 (application number: TWBR10810–07). This study further received approval from the Research Ethics Committee of National Taiwan University Hospital (NTUH-REC no. 201805050RINB).
Consent for publication
Not applicable. This manuscript does not contain any individual details, images or videos. Only aggregate data were used in this work.
Competing interests
The authors declare that they have no competing interests.
Abbreviations
DDR | = | Dance dance revolution |
HDL-C | = | High-density lipoprotein cholesterol |
LDL-C | = | Low-density lipoprotein cholesterol |
RCT | = | Randomized controlled trial |
TWB | = | Taiwan Biobank |
TG | = | Triglyceride |
Acknowledgments
The author would like to thank the three anonymous reviewers for their insightful and constructive comments, and the Taiwan Biobank for approving our application to access the data.
Funding
This study was supported by the Ministry of Science and Technology of Taiwan (grant number MOST 107–2314-B-002-195-MY3 to W.-Y.L.).
Availability of data and materials
The datasets analyzed during the current study are available from the Taiwan Biobank, https://www.twbiobank.org.tw/new_web_en/index.php
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- BorrayoGBasurtoLGonzalez-EscuderoEDiazAVazquezASanchezLHernandez-GonzalezGOBarreraSDegolladoJACordovaN et al Tg/Hdl-C ratio as cardio-metabolic biomarker even in Normal weight womenActa Endocrinol-Buch201814 2 261 267 1:STN:280:DC%2BB3M3hsl2ntQ%3D%3D
- BackesJAnzaloneDHillemanDCatiniJThe clinical relevance of omega-3 fatty acids in the management of hypertriglyceridemiaLipids Health Dis201615 1 118 1:CAS:528:DC%2BC2sXhvVGktrzL https://doi.org/10.1186/s12944-016-0286-4 27444154 4957330
- GrandjeanPWCrouseSFRohackJJInfluence of cholesterol status on blood lipid and lipoprotein enzyme responses to aerobic exerciseJ Appl Physiol (1985)200089 2 472 480 1:CAS:528:DC%2BD3cXmtleltro%3D https://doi.org/10.1152/jappl.2000.89.2.472
- WangYXuDEffects of aerobic exercise on lipids and lipoproteinsLipids Health Dis201716 1 132 1:CAS:528:DC%2BC1cXitVOqtrnN https://doi.org/10.1186/s12944-017-0515-5 28679436 5498979
- SarzynskiMARuiz-RamieJJBarberJLSlentzCAApolzanJWMcGarrahRWHarrisMNChurchTSBorjaMSHeY et al Effects of increasing exercise intensity and dose on multiple measures of HDL (high-density lipoprotein) functionArterioscler Thromb Vasc Biol201838 4 943 952 1:CAS:528:DC%2BC1cXltFentbg%3D https://doi.org/10.1161/ATVBAHA.117.310307
- DurstineJLGrandjeanPWDavisPGFergusonMAAldersonNLDuBoseKDBlood lipid and lipoprotein adaptations to exercise: a quantitative analysisSports Med200131 15 1033 1062 1:STN:280:DC%2BD3Mnptlyjuw%3D%3D https://doi.org/10.2165/00007256-200131150-00002 11735685
- KodamaSTanakaSSaitoKShuMSoneYOnitakeFSuzukiEShimanoHYamamotoSKondoKOhashiYYamadaNSoneHEffect of aerobic exercise training on serum levels of high-density lipoprotein cholesterol: a meta-analysisArch Intern Med2007167 10 999 1008 1:CAS:528:DC%2BD2sXmvVGrtLk%3D https://doi.org/10.1001/archinte.167.10.999 17533202
- KokkinosPFHollandJCNarayanPColleranJADotsonCOPapademetriouVMiles run per week and high-density lipoprotein cholesterol levels in healthy, middle-aged men. A dose-response relationshipArch Intern Med1995155 4 415 420 1:CAS:528:DyaK2MXkvVWnsbw%3D https://doi.org/10.1001/archinte.1995.00430040091011
- LeMuraLMvon DuvillardSPAndreacciJKlebezJMChellandSARussoJLipid and lipoprotein profiles, cardiovascular fitness, body composition, and diet during and after resistance, aerobic and combination training in young womenEur J Appl Physiol200082 5–6 451 458 1:CAS:528:DC%2BD3cXlsF2murg%3D https://doi.org/10.1007/s004210000234 10985600
- NyboLSundstrupEJakobsenMDMohrMHornstrupTSimonsenLBulowJRandersMBNielsenJJAagaardP et al High-intensity training versus traditional exercise interventions for promoting healthMed Sci Sports Exerc201042 10 1951 1958 https://doi.org/10.1249/MSS.0b013e3181d99203 20195181
- KrausWEHoumardJADuschaBDKnetzgerKJWhartonMBMcCartneyJSBalesCWHenesSSamsaGPOtvosJDKulkarniKRSlentzCAEffects of the amount and intensity of exercise on plasma lipoproteinsN Engl J Med2002347 19 1483 1492 1:CAS:528:DC%2BD38XosVOnsL8%3D https://doi.org/10.1056/NEJMoa020194 12421890
- O'DonovanGOwenABirdSRKearneyEMNevillAMJonesDWWoolf-MayKChanges in cardiorespiratory fitness and coronary heart disease risk factors following 24 wk of moderate- or high-intensity exercise of equal energy costJ Appl Physiol (1985)200598 5 1619 1625 https://doi.org/10.1152/japplphysiol.01310.2004
- HsuCSChangSTNforONLeeKJLeeSSLiawYPEffects of regular aerobic exercise and resistance training on high-density lipoprotein cholesterol levels in Taiwanese adultsInt J Environ Res Public Health201916 11 2003 1:CAS:528:DC%2BC1MXitFyju7rN https://doi.org/10.3390/ijerph16112003 6603984
- KazeminasabFMarandiMGhaediKEsfarjaniFMoshtaghianJEndurance training enhances LXRalpha gene expression in Wistar male ratsEur J Appl Physiol2013113 9 2285 2290 1:CAS:528:DC%2BC3sXht1Ons7vO https://doi.org/10.1007/s00421-013-2658-z 23674092
- Ghanbari-NiakiAKhabazianBMHossaini-KakhakSARahbarizadehFHedayatiMTreadmill exercise enhances ABCA1 expression in rat liverBiochem Biophys Res Commun2007361 4 841 846 1:CAS:528:DC%2BD2sXpt1KgsLk%3D https://doi.org/10.1016/j.bbrc.2007.07.100 17689492
- KazeminasabFMarandiMGhaediKEsfarjaniFMoshtaghianJEffects of a 4-week aerobic exercise on lipid profile and expression of LXRalpha in rat liverCell J201719 1 45 49 https://doi.org/10.22074/cellj.2016.4871 28367416
- Ruiz-RamieJJBarberJLSarzynskiMAEffects of exercise on HDL functionalityCurr Opin Lipidol201930 1 16 23 1:CAS:528:DC%2BC1cXisFyks77F https://doi.org/10.1097/MOL.0000000000000568 30480581 6492243
- GoldbergACHopkinsPNTothPPBallantyneCMRaderDJRobinsonJGDanielsSRGiddingSSde FerrantiSDItoMKMcGowanMPMoriartyPMCromwellWCRossJLZiajkaPEFamilial hypercholesterolemia: screening, diagnosis and management of pediatric and adult patients: clinical guidance from the National Lipid Association Expert Panel on familial hypercholesterolemiaJ Clin Lipidol20115 3 Suppl S1 S8 https://doi.org/10.1016/j.jacl.2011.04.003 21600525
- MannSBeedieCJimenezADifferential effects of aerobic exercise, resistance training and combined exercise modalities on cholesterol and the lipid profile: review, synthesis and recommendationsSports Med201444 2 211 221 https://doi.org/10.1007/s40279-013-0110-5 24174305
- KelleyGAKelleyKSAerobic exercise and HDL2-C: a meta-analysis of randomized controlled trialsAtherosclerosis2006184 1 207 215 1:CAS:528:DC%2BD2MXht1Olu7jL https://doi.org/10.1016/j.atherosclerosis.2005.04.005 15907854 2447856
- SugiuraHSugiuraHKajimaKMirbodSMIwataHMatsuokaTEffects of long-term moderate exercise and increase in number of daily steps on serum lipids in women: randomised controlled trial [ISRCTN21921919]BMC Womens Health20022 1 3 https://doi.org/10.1186/1472-6874-2-3 11846892 65683
- LinWYLiuYLYangACTsaiSJKuoPHActive cigarette smoking is associated with an exacerbation of genetic susceptibility to diabetesDiabetes202069 12 2819 2829 1:CAS:528:DC%2BB3MXitVegur0%3D https://doi.org/10.2337/db20-0156
- ChenCHYangJHChiangCWKHsiungCNWuPEChangLCChuHWChangJSongIWYangSLChenYTLiuFTShenCYPopulation structure of Han Chinese in the modern Taiwanese population based on 10,000 participants in the Taiwan biobank projectHum Mol Genet201625 24 5321 5331 1:CAS:528:DC%2BC2sXhtV2gur7O https://doi.org/10.1093/hmg/ddw346 27798100 6078601
- MarzWKleberMEScharnaglHSpeerTZewingerSRitschAParhoferKGvon EckardsteinALandmesserULaufsUHDL cholesterol: reappraisal of its clinical relevanceClin Res Cardiol2017106 9 663 675 1:CAS:528:DC%2BC2sXltl2htb4%3D https://doi.org/10.1007/s00392-017-1106-1 28342064 5565659
- ElshourbagyNAMeyersHVAbdel-MeguidSSCholesterol: the good, the bad, and the ugly - therapeutic targets for the treatment of dyslipidemiaMed Princ Pract201423 2 99 111 https://doi.org/10.1159/000356856 24334831
- LeeJSChangPYZhangYKizerJRBestLGHowardBVTriglyceride and HDL-C dyslipidemia and risks of coronary heart disease and ischemic stroke by glycemic Dysregulation status: the strong heart studyDiabetes Care201740 4 529 537 https://doi.org/10.2337/dc16-1958 28122840 5360283
- SultaniRTongDCPeverelleMLeeYSBaradiAWilsonAMElevated triglycerides to high-density lipoprotein cholesterol (TG/HDL-C) ratio predicts long-term mortality in high-risk patientsHeart Lung Circ202029 3 414 421 https://doi.org/10.1016/j.hlc.2019.03.019 31014557
- QiLDingXTangWLiQMaoDWangYPrevalence and risk factors associated with dyslipidemia in Chongqing, ChinaInt J Environ Res Public Health201512 10 13455 13465 1:CAS:528:DC%2BC28XhtVOlsbjO https://doi.org/10.3390/ijerph121013455 26516874 4627042
- KheraAVDemlerOVAdelmanSJCollinsHLGlynnRJRidkerPMRaderDJMoraSCholesterol efflux capacity, high-density lipoprotein particle number, and incident cardiovascular events: an analysis from the JUPITER trial (justification for the use of statins in prevention: an intervention trial evaluating Rosuvastatin)Circulation2017135 25 2494 2504 1:CAS:528:DC%2BC2sXhtVSqurjP https://doi.org/10.1161/CIRCULATIONAHA.116.025678 28450350 5490983
- TiainenSLuotoRAhotupaMRaitanenJVasankariT6-mo aerobic exercise intervention enhances the lipid peroxide transport function of HDLFree Radic Res201650 11 1279 1285 1:CAS:528:DC%2BC28XhvFCgu7vJ https://doi.org/10.1080/10715762.2016.1252040 27776442
- SangHYaoSZhangLLiXYangNZhaoJZhaoLSiYZhangYLvXXueYQinSWalk-run training improves the anti-inflammation properties of high-density lipoprotein in patients with metabolic syndromeJ Clin Endocrinol Metab2015100 3 870 879 1:CAS:528:DC%2BC2MXlvVGitr8%3D https://doi.org/10.1210/jc.2014-2979 25514103
- NiemanDCBrockDWButterworthDUtterACNiemanCCReducing diet and/or exercise training decreases the lipid and lipoprotein risk factors of moderately obese womenJ Am Coll Nutr200221 4 344 350 1:CAS:528:DC%2BD38XmsFejsrw%3D https://doi.org/10.1080/07315724.2002.10719233 12166532
- KatzelLIBleeckerERColmanEGRogusEMSorkinJDGoldbergAPEffects of weight loss vs aerobic exercise training on risk factors for coronary disease in healthy, obese, middle-aged and older men. A randomized controlled trialJAMA1995274 24 1915 1921 1:STN:280:DyaK287gvFSrsg%3D%3D https://doi.org/10.1001/jama.1995.03530240025035 8568984
- WoodPDPhysical activity, diet, and health: independent and interactive effectsMed Sci Sports Exerc199426 7 838 843 1:STN:280:DyaK2M%2FitVCmuw%3D%3D https://doi.org/10.1249/00005768-199407000-00005
- LambertCPEvansWJAdaptations to aerobic and resistance exercise in the elderlyRev Endocr Metab Disord20056 2 137 143 https://doi.org/10.1007/s11154-005-6726-5 15843885
- VillarealDTAguirreLGurneyABWatersDLSinacoreDRColomboEArmamento-VillarealRQuallsCAerobic or resistance exercise, or both, in dieting obese older adultsNew Engl J Med2017376 20 1943 1955 https://doi.org/10.1056/NEJMoa1616338 28514618
- MarandiSMAbadiNGEsfarjaniFMojtahediHGhasemiGEffects of intensity of aerobics on body composition and blood lipid profile in obese/overweight femalesInt J Prev Med20134 Suppl 1 S118 S125 23717761 3665017
- FenkciSSarsanARotaSArdicFEffects of resistance or aerobic exercises on metabolic parameters in obese women who are not on a dietAdv Ther200623 3 404 413 1:CAS:528:DC%2BD28XhtVGisbbE https://doi.org/10.1007/BF02850161 16912022
- WangHEckelRHLipoprotein lipase: from gene to obesityAm J Physiol Endocrinol Metab2009297 2 E271 E288 1:CAS:528:DC%2BD1MXhtVahsbnN https://doi.org/10.1152/ajpendo.90920.2008 19318514
- Pirahanchi Y, Anoruo MD, Sharma S. Biochemistry, Lipoprotein Lipase. In: StatPearls: Treasure Island (FL); 2021. https://www.ncbi.nlm.nih.gov/books/NBK537040/.
- RadakZZhaoZKoltaiEOhnoHAtalayMOxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signalingAntioxid Redox Signal201318 10 1208 1246 1:CAS:528:DC%2BC3sXis1WlsLg%3D https://doi.org/10.1089/ars.2011.4498 22978553 3579386
- MiyashitaMEtoMSasaiHTsujimotoTNomataYTanakaKTwelve-week jogging training increases pre-heparin serum lipoprotein lipase concentrations in overweight/obese middle-aged menJ Atheroscler Thromb201017 1 21 29 1:CAS:528:DC%2BC3MXhvVertbc%3D https://doi.org/10.5551/jat.2337 20075597
- PillarisettiSSaxenaULipoprotein lipase as a therapeutic target for dyslipidemiaFront Biosci-Landmrk20038 D237 D241