Role of Physical Activity and Fitness in the Characterization and Prognosis of the Metabolically Healthy Obesity Phenotype: A Systematic Review and Meta-analysis

https://doi.org/10.1016/j.pcad.2018.07.008Get rights and content

Abstract

The aims of the present article are to systematically review and meta-analyze the existing evidence on: 1) differences in physical activity (PA), sedentary behavior (SB), cardiorespiratory fitness (CRF) and muscular strength (MST) between metabolically healthy obesity (MHO) and metabolically unhealthy obesity (MUO); and 2) the prognosis of all-cause mortality and cardiovascular disease (CVD) mortality/morbidity in MHO individuals, compared with the best scenario possible, i.e., metabolically healthy normal-weight (MHNW), after adjusting for PA, SB, CRF or MST. Our systematic review identified 67 cross-sectional studies to address aim 1, and 11 longitudinal studies to address aim 2. The major findings and conclusions from the current meta-analysis are: 1) MHO individuals are more active, spend less time in SB, and have a higher level of CRF (yet no differences in MST) than MUO individuals, suggesting that their healthier metabolic profile could be at least partially due to these healthier lifestyle factors and attributes. 2) The meta-analysis of cohort studies which accounted for PA (N = 10 unique cohorts, 100% scored as high-quality) support the notion that MHO individuals have a 24–33% higher risk of all-cause mortality and CVD mortality/morbidity compared to MHNW individuals. This risk was borderline significant/non-significant, independent of the length of the follow-up and lower than that reported in previous meta-analyses in this topic including all type of studies, which could be indicating a modest reduction in the risk estimates as a consequence of accounting for PA. 3) Only one study has examined the role of CRF in the prognosis of MHO individuals. This study suggests that the differences in the risk of all-cause mortality and CVD mortality/morbidity between MHO and MHNW are largely explained by differences in CRF between these two phenotypes.

Section snippets

Protocol and registration

The present systematic review and meta-analysis was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) statement.43 The study protocol was registered in the International Prospective Register of Systematic Reviews (PROSPERO reference number: CRD42018093955).

Data sources and search strategies

The search was conducted for studies published from inception to March 21, 2018 in two major electronic databases: PubMed and Web of Science. The keywords used in search strategy were related

Literature search

In total, 70 unique studies were included in the systematic review; 67 of them were included for the systematic review for aim 1. Among them, 55 studies51., 52., 53., 54., 55., 56., 57., 58., 59., 60., 61., 62., 63., 64., 65., 66., 67., 68., 69., 70., 71., 72., 73., 74., 75., 76., 77., 78., 79., 80., 81., 82., 83., 84., 85., 86., 87., 88., 89., 90., 91., 92., 93., 94., 95., 96., 97., 98., 99., 100., 101., 102., 103., 104., 105. were focused on the differences between MHO and MUO in PA (N = 53)

Main findings

In the present systematic review and meta-analysis, we focused on two relevant topics related to the MHO phenotype, its characterization (aim 1) and prognosis (aim 2). The studies included in this review were mostly (80–100%) scored as high-quality studies indicating a low risk of bias in the findings obtained. We found 67 studies examining differences between MHO and MUO in PA, SB, CRF and MST. Our meta-analysis showed that MHO individuals have significantly higher levels of PA and CRF and

Conclusions

Our systematic review and meta-analysis provides novel insights in the characterization and prognosis of the MHO phenotype. First, the meta-analysis on cross-sectional studies supports that MHO individuals are more active, spent less time in SB, and have a higher level of CRF (yet no differences in MST) than MUO individuals, suggesting that their healthier metabolic profile could be, at least partially, due to these healthier lifestyle factors and attributes. Second, the findings from the

Funding

Current research activities of Dr. Ortega and Dr. Ruiz are supported by the Spanish Ministry of Economy and Competitiveness – MINECO/FEDER (DEP2016-79512-R); the University of Granada, Plan Propio de Investigación 2016, Excellence actions: Units of Excellence, Unit of Excellence on Exercise and Health (UCEES); the European Union's Horizon 2020 research and innovation programme under grant agreement No 667302; the SAMID III network, RETICS, funded by the PN I+D+I 2017-2021 (Spain), ISCIII -

Statement of Conflict of Interest

The authors declare no conflict of interest related to this work. Prof. Blair has served as consultants for weight loss and fitness companies and for The Coca-Cola Company, which has also provided them unrestricted research grants.

References (123)

  • N. Stefan et al.

    Metabolically healthy obesity: epidemiology, mechanisms, and clinical implications

    Lancet Diabetes Endocrinol

    (2013)
  • P. Deedwania et al.

    Dangers and long-term outcomes in metabolically healthy obesity: the impact of the missing fitness component

    J Am Coll Cardiol

    (2018)
  • C.J. Lavie et al.

    Impact of physical activity and fitness in metabolically healthy obesity

    J Am Coll Cardiol

    (2018)
  • J. Fan et al.

    Combined effect of obesity and cardio-metabolic abnormality on the risk of cardiovascular disease: a meta-analysis of prospective cohort studies

    Int J Cardiol

    (2013)
  • R. Caleyachetty et al.

    Metabolically healthy obese and incident cardiovascular disease events among 3.5 million men and women

    PLoS One

    (2017)
  • D. Moher et al.

    Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement

    J Clin Epidemiol

    (2009)
  • V.A. Aparicio et al.

    The role of sex and domestic physical activity on the metabolically healthy and unhealthy obesity. The HERMEX Study

    Rev Esp Cardiol (Engl Ed)

    (2016)
  • J.A. Bell et al.

    Healthy obesity and objective physical activity

    Am J Clin Nutr

    (2015)
  • C. Cadenas-Sanchez et al.

    Prevalence of metabolically healthy but overweight/obese phenotype and its association with sedentary time, physical activity, and fitness

    J Adolesc Health

    (2017)
  • S. Doustmohamadian et al.

    Risk of all-cause mortality in abdominal obesity phenotypes: Tehran Lipid and Glucose Study

    Nutr Metab Cardiovasc Dis

    (2017)
  • C. Gutierrez-Repiso et al.

    Variable patterns of obesity and cardiometabolic phenotypes and their association with lifestyle factors in the [email protected] study

    Nutr Metab Cardiovasc Dis

    (2014)
  • F. Hosseinpanah et al.

    Effect of different obesity phenotypes on cardiovascular events in Tehran Lipid and Glucose Study (TLGS)

    Am J Cardiol

    (2011)
  • L. Ingle et al.

    Characterization of the metabolically healthy phenotype in overweight and obese British men

    Prev Med

    (2017)
  • P.E. Korhonen et al.

    Lifestyle of metabolically healthy obese individuals

    Prim Care Diabetes

    (2015)
  • H.H. Lim

    Sleep duration independently influences metabolic body size phenotype in children and adolescents: a population-based study

    J Diabetes Res

    (2018)
  • J.A. McElroy et al.

    Obese but fit: the relationship of fitness to metabolically healthy but obese status among sexual minority women

    Womens Health Issues

    (2016)
  • Y. Song et al.

    Comparison of usefulness of body mass index versus metabolic risk factors in predicting 10-year risk of cardiovascular events in women

    Am J Cardiol

    (2007)
  • K.C. Sung et al.

    All-cause and cardiovascular mortality among Koreans: effects of obesity and metabolic health

    Am J Prev Med

    (2015)
  • N. Zhang et al.

    Metabolic abnormalities, but not metabolically healthy obesity, are associated with left ventricular hypertrophy

    Heart Lung Circ

    (2017)
  • Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants

    Lancet

    (2016)
  • Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults

    Lancet

    (2017)
  • S.N. Bhupathiraju et al.

    Epidemiology of obesity and diabetes and their cardiovascular complications

    Circ Res

    (2016)
  • M. Brochu et al.

    What are the physical characteristics associated with a normal metabolic profile despite a high level of obesity in postmenopausal women?

    J Clin Endocrinol Metab

    (2001)
  • H. Lin et al.

    The prevalence, metabolic risk and effects of lifestyle intervention for metabolically healthy obesity: a systematic review and meta-analysis: a PRISMA-compliant article

    Medicine (Baltimore)

    (2017)
  • F.B. Ortega et al.

    Obesity and cardiovascular disease

    Circ Res

    (2016)
  • R.S. Paffenbarger et al.

    Physical activity, all-cause mortality, and longevity of college alumni

    N Engl J Med

    (1986)
  • R.S. Paffenbarger et al.

    Physical activity as an index of heart attack risk in college alumni

    Am J Epidemiol

    (1978)
  • S.N. Blair et al.

    Physical fitness and all-cause mortality. A prospective study of healthy men and women

    JAMA

    (1989)
  • S. Kodama et al.

    Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis

    JAMA

    (2009)
  • J.R. Ruiz et al.

    Association between muscular strength and mortality in men: prospective cohort study

    BMJ

    (2008)
  • F.B. Ortega et al.

    Muscular strength in male adolescents and premature death: cohort study of one million participants

    BMJ

    (2012)
  • R. Ross et al.

    Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the American Heart Association

    Circulation

    (2016)
  • H. Henriksson et al.

    Muscular strength in adolescence and later disability: a population based cohort study of one million men

    Br J Sports Med

    (2018)
  • A. Garcia-Hermoso et al.

    Muscular strength as a predictor of all-cause mortality in an apparently healthy population: a systematic review and meta-analysis of data from approximately 2 million men and women

    Arch Phys Med Rehabil

    (2018)
  • F.B. Ortega et al.

    Fitness and fatness as health markers through the lifespan: an overview of current knowledge

    Prog Prev Med

    (2018)
  • V. Primeau et al.

    Characterizing the profile of obese patients who are metabolically healthy

    Int J Obes (Lond)

    (2011)
  • F.B. Ortega et al.

    The intriguing metabolically healthy but obese phenotype: cardiovascular prognosis and role of fitness

    Eur Heart J

    (2013)
  • A.B. Kennedy et al.

    Fitness or fatness: which is more important?

    JAMA

    (2018)
  • C.J. Lavie et al.

    Obesity is rarely healthy

    Lancet Diabetes Endocrinol

    (2018)
  • L.L. Roberson et al.

    Beyond BMI: the “metabolically healthy obese” phenotype & its association with clinical/subclinical cardiovascular disease and all-cause mortality — a systematic review

    BMC Public Health

    (2014)
  • Cited by (95)

    • Trends in Metabolic Phenotypes According to Body Mass Index Among US Adults, 1999-2018

      2022, Mayo Clinic Proceedings
      Citation Excerpt :

      Third, the NHANES with measured metabolic parameters is limited by small sample sizes for subgroups, which restricts the ability to provide estimates of metabolic phenotypes within underweight or MUO within obese participants in the secondary analysis. Finally, our study did not stratify individuals by levels of physical activity, much less cardiorespiratory fitness, which may be needed to fully assess prognosis along with MetS and metabolic healthiness.55,56 From 1999 to 2018, US adults experienced substantial increases in the prevalence of both metabolically healthy and unhealthy obesity, largely due to decreases in metabolically healthy normal weight.

    View all citing articles on Scopus

    Statement of Conflict of Interest: see page 203.

    1

    Co-first authors.

    View full text