Performing different kinds of physical exercise differentially attenuates the genetic effects on obesity measures: Evidence from 18,424 Taiwan Biobank participants

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Abstract

Obesity is a worldwide health problem that is closely linked to many metabolic disorders. Regular physical exercise has been found to attenuate the genetic predisposition to obesity. However, it remains unknown what kinds of exercise can modify the genetic risk of obesity. This study included 18,424 unrelated Han Chinese adults aged 30–70 years who participated in the Taiwan Biobank (TWB). A total of 5 obesity measures were investigated here, including body mass index (BMI), body fat percentage (BFP), waist circumference (WC), hip circumference (HC), and waist-to-hip ratio (WHR). Because there have been no large genome-wide association studies on obesity for Han Chinese, we used the TWB internal weights to construct genetic risk scores (GRSs) for each obesity measure, and then test the significance of GRS-by-exercise interactions. The significance level throughout this work was set at 0.05/550 = 9.1x10 ^-5 because a total of 550 tests were performed. Performing regular exercise was found to attenuate the genetic effects on 4 obesity measures, including BMI, BFP, WC, and HC. Among the 18 kinds of self-reported regular exercise, 6 mitigated the genetic effects on at least one obesity measure. Regular jogging blunted the genetic effects on BMI, BFP, and HC. Mountain climbing, walking, exercise walking, international standard dancing, and a longer practice of yoga also attenuated the genetic effects on BMI. Exercises such as cycling, stretching exercise, swimming, dance dance revolution, and qigong were not found to modify the genetic effects on any obesity measure. Across all 5 obesity measures, regular jogging consistently presented the most significant interactions with GRSs. Our findings show that the genetic effects on obesity measures can be decreased to various extents by performing different kinds of exercise. The benefits of regular physical exercise are more impactful in subjects who are more predisposed to obesity.

Author summary

The complex interplay of genetics and lifestyle makes obesity a challenging issue. Previous studies have found performing regular physical exercise could blunt the genetic effects on body mass index (BMI). However, BMI does not take into account lean body mass or identify central obesity. Moreover, it remains unclear what kinds of exercise could more effectively attenuate the genetic effects on obesity measures. With a sample of 18,424 unrelated Han Chinese adults, we comprehensively investigated gene-exercise interactions on 5 obesity measures: BMI, body fat percentage, waist circumference, hip circumference, and waist-to-hip ratio. Moreover, we tested whether the genetic effects on obesity measures could be modified by any of 18 kinds of self-reported regular exercise. Because no large genome-wide association studies on obesity have been done for Han Chinese, we constructed genetic risk scores with internal weights for analyses. Among these exercises, regular jogging consistently presented the strongest evidence to mitigate the genetic effects on all 5 obesity measures. Moreover, mountain climbing, walking, exercise walking, international standard dancing, and a longer practice of yoga attenuated the genetic effects on BMI. The benefits of regularly performing these 6 kinds of exercise are more impactful in subjects who are more predisposed to obesity.

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Independent filtering increases detection power for high-throughput experiments.

Richard Bourgon, Robert C Gentleman, Wolfgang Huber (2010)

With high-dimensional data, variable-by-variable statistical testing is often used to select variables whose behavior differs across conditions. Such an approach requires adjustment for multiple testing, which can result in low statistical power. A two-stage approach that first filters variables by a criterion independent of the test statistic, and then only tests variables which pass the filter, can provide higher power. We show that use of some filter/test statistics pairs presented in the literature may, however, lead to loss of type I error control. We describe other pairs which avoid this problem. In an application to microarray data, we found that gene-by-gene filtering by overall variance followed by a t-test increased the number of discoveries by 50%. We also show that this particular statistic pair induces a lower bound on fold-change among the set of discoveries. Independent filtering-using filter/test pairs that are independent under the null hypothesis but correlated under the alternative-is a general approach that can substantially increase the efficiency of experiments.

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Obesity and the metabolic syndrome in developing countries.

Anoop Misra, Lokesh Khurana (2008)

Prevalence of obesity and the metabolic syndrome is rapidly increasing in developing countries, leading to increased morbidity and mortality due to type 2 diabetes mellitus (T2DM) and cardiovascular disease. Literature search was carried out using the terms obesity, insulin resistance, the metabolic syndrome, diabetes, dyslipidemia, nutrition, physical activity, and developing countries, from PubMed from 1966 to June 2008 and from web sites and published documents of the World Health Organization and Food and Agricultural Organization. With improvement in economic situation in developing countries, increasing prevalence of obesity and the metabolic syndrome is seen in adults and particularly in children. The main causes are increasing urbanization, nutrition transition, and reduced physical activity. Furthermore, aggressive community nutrition intervention programs for undernourished children may increase obesity. Some evidence suggests that widely prevalent perinatal undernutrition and childhood catch-up obesity may play a role in adult-onset metabolic syndrome and T2DM. The economic cost of obesity and related diseases in developing countries, having meager health budgets is enormous. To prevent increasing morbidity and mortality due to obesity-related T2DM and cardiovascular disease in developing countries, there is an urgent need to initiate large-scale community intervention programs focusing on increased physical activity and healthier food options, particularly for children. International health agencies and respective government should intensively focus on primordial and primary prevention programs for obesity and the metabolic syndrome in developing countries.

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Variability in the Heritability of Body Mass Index: A Systematic Review and Meta-Regression

Cathy E Elks, Marcel den Hoed, Jing Hua Zhao … (2012)

Evidence for a major role of genetic factors in the determination of body mass index (BMI) comes from studies of related individuals. Despite consistent evidence for a heritable component of BMI, estimates of BMI heritability vary widely between studies and the reasons for this remain unclear. While some variation is natural due to differences between populations and settings, study design factors may also explain some of the heterogeneity. We performed a systematic review that identified 88 independent estimates of BMI heritability from twin studies (total 140,525 twins) and 27 estimates from family studies (42,968 family members). BMI heritability estimates from twin studies ranged from 0.47 to 0.90 (5th/50th/95th centiles: 0.58/0.75/0.87) and were generally higher than those from family studies (range: 0.24–0.81; 5th/50th/95th centiles: 0.25/0.46/0.68). Meta-regression of the results from twin studies showed that BMI heritability estimates were 0.07 (P = 0.001) higher in children than in adults; estimates increased with mean age among childhood studies (+0.012/year, P = 0.002), but decreased with mean age in adult studies (−0.002/year, P = 0.002). Heritability estimates derived from AE twin models (which assume no contribution of shared environment) were 0.12 higher than those from ACE models (P < 0.001), whilst lower estimates were associated with self reported versus DNA-based determination of zygosity (−0.04, P = 0.02), and with self reported versus measured BMI (−0.05, P = 0.03). Although the observed differences in heritability according to aspects of study design are relatively small, together, the above factors explained 47% of the heterogeneity in estimates of BMI heritability from twin studies. In summary, while some variation in BMI heritability is expected due to population-level differences, study design factors explained nearly half the heterogeneity reported in twin studies. The genetic contribution to BMI appears to vary with age and may have a greater influence during childhood than adult life.

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Author and article information

Contributors

Wan-Yu Lin:

ORCID: http://orcid.org/0000-0002-3385-4702

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing

Chang-Chuan Chan: Role: Writing – review & editing

Yu-Li Liu: Role: Data curationRole: Writing – review & editing

Albert C. Yang: Role: Data curationRole: Writing – review & editing

Shih-Jen Tsai: Role: Data curationRole: Writing – review & editing

Po-Hsiu Kuo:

ORCID: http://orcid.org/0000-0003-0365-3587

Role: Data curationRole: Funding acquisitionRole: Writing – review & editing

Tuomas Kilpeläinen: Role: Editor

Journal

Journal ID (nlm-ta): PLoS Genet

Journal ID (iso-abbrev): PLoS Genet

Journal ID (publisher-id): plos

Journal ID (pmc): plosgen

Title: PLoS Genetics

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Print): 1553-7390

ISSN (Electronic): 1553-7404

Publication date (Electronic): 1 August 2019

Publication date Collection: August 2019

Volume: 15

Issue: 8

Electronic Location Identifier: e1008277

Affiliations

[1 ] Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan

[2 ] Department of Public Health, College of Public Health, National Taiwan University, Taipei, Taiwan

[3 ] Institute of Occupational Medicine and Industrial Hygiene, College of Public Health, National Taiwan University, Taipei, Taiwan

[4 ] Center for Neuropsychiatric Research, National Health Research Institutes, Zhunan, Miaoli County, Taiwan

[5 ] Division of Psychiatry, National Yang-Ming University, Taipei, Taiwan

[6 ] Division of Interdisciplinary Medicine and Biotechnology, Beth Israel Deaconess Medical Center/Harvard Medical School, Boston, Massachusetts, United States of America

[7 ] Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan

[8 ] Department of Psychiatry, Taipei Veterans General Hospital, Beitou District, Taipei, Taiwan

University of Copenhagen, DENMARK

Author notes

The authors have declared that no competing interests exist.

* E-mail: linwy@ 123456ntu.edu.tw (WYL); phkuo@ 123456ntu.edu.tw (PHK)

Author information

Wan-Yu Lin http://orcid.org/0000-0002-3385-4702

Po-Hsiu Kuo http://orcid.org/0000-0003-0365-3587

Article

Publisher ID: PGENETICS-D-19-00266

DOI: 10.1371/journal.pgen.1008277

PMC ID: 6675047

PubMed ID: 31369549

SO-VID: eddaafea-9f2a-4980-9b18-9b0fd2d47681

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 15 February 2019

Date accepted : 26 June 2019

Page count

Figures: 3, Tables: 5, Pages: 21

Funding

Funded by: funder-id http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;

Award ID: 107-2314-B-002-195-MY3

Award Recipient :

ORCID: http://orcid.org/0000-0002-3385-4702

Wan-Yu Lin

Funded by: funder-id http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;

Award ID: 102-2314-B-002-117-MY3

Award Recipient :

ORCID: http://orcid.org/0000-0003-0365-3587

Po-Hsiu Kuo

Funded by: funder-id http://dx.doi.org/10.13039/501100005762, National Taiwan University Hospital;

Award ID: UN106-050

Award Recipient :

ORCID: http://orcid.org/0000-0003-0365-3587

Po-Hsiu Kuo

This study was supported by the Ministry of Science and Technology of Taiwan (grant number MOST 107-2314-B-002-195-MY3 to Wan-Yu Lin). The acquisition of TWB data was supported by a MOST grant (grant number MOST 102-2314-B-002-117-MY3 to Po-Hsiu Kuo) and a collaboration grant (National Taiwan University Hospital: grant number UN106-050 to Po-Hsiu Kuo). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Data Availability Individual-level Taiwan Biobank data are available upon application to Taiwan Biobank ( https://www.twbiobank.org.tw/new_web/).

ScienceOpen disciplines: Genetics

Data availability:

ScienceOpen disciplines: Genetics

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Performing different kinds of physical exercise differentially attenuates the genetic effects on obesity measures: Evidence from 18,424 Taiwan Biobank participants

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Most cited references 44

Independent filtering increases detection power for high-throughput experiments.

Obesity and the metabolic syndrome in developing countries.

Variability in the Heritability of Body Mass Index: A Systematic Review and Meta-Regression

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