Phenotypic characteristics associated with insulin resistance in metabolically obese but normal-weight young women.
Abstract
Metabolically obese, normal-weight (MONW) individuals are a hypothesized subgroup of the general population. These normal-weight individuals potentially display a cluster of obesity-related features, although this has not been systematically tested in young women. We hypothesized that MONW young women would display higher levels of total and visceral fat and lower levels of physical activity than normal women. In a cohort of 71 healthy nonobese women (21-35 years old), we identified MONW women based on cut points for insulin sensitivity (normal = glucose disposal >8 mg x min(-1) x kg(-1) of fat-free mass [FFM], n = 58; impaired = glucose disposal <8 ml x min(-1) x kg(-1) of FFM, n = 13). Thereafter, we measured body composition (dual energy X-ray absorptiometry) and body fat distribution (computed tomography), cardiorespiratory fitness (VO2max on a treadmill), physical activity energy expenditure (doubly labeled water and indirect calorimetry), glucose tolerance (oral glucose tolerance test), serum lipid profile, and dietary intake. We found a higher body fat percentage (32 +/- 6 vs. 27 +/- 6%, P = 0.01) and higher subcutaneous (213 +/- 61 vs. 160 +/- 78 cm2, P = 0.03) and visceral (44 +/- 16 vs. 35 +/- 14 cm2, P < 0.05) abdominal adiposity in the MONW group versus the normal group. The MONW group showed a lower physical activity energy expenditure (2.66 +/- 0.92 vs. 4.39 +/- 1.50 MJ/day, P = 0.01), but no difference in cardiorespiratory fitness was noted between groups. In conclusion, despite a normal body weight, a subset of young, apparently healthy women displayed a cluster of risky phenotypic characteristics that, if left untreated, may eventually predispose them to type 2 diabetes and cardiovascular disease.
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Some individuals have the metabolic syndrome with only a moderate degree of total body obesity.
“Indeed, as mentioned before, some individuals exhibit the metabolic syndrome with only a moderate degree of total body obesity.43,44”
From Diagnosis and Management of the Metabolic Syndrome: An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement (2005) · cites this paper as [44]
The US population varies considerably in degree of insulin resistance; those with more inherent insulin resistance can develop the metabolic syndrome with only moderate excess abdominal fat, while even people with little or no inherent insulin resistance can develop it if they accumulate marked abdominal obesity.
“Moreover, the population of the United States varies considerably in degree of insulin resistance 46 ; those having more inherent insulin resistance can develop the metabolic syndrome with only moderate excess in abdominal fat, 43,44 but even people with little or no inherent insulin resistance can develop the metabolic syndrome if they accumulate marked abdominal obesity.3,8”
From Diagnosis and Management of the Metabolic Syndrome: An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement (2005) · cites this paper as [44]
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The Concept of Normal Weight Obesity
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BackgroundWeight Loss Reduces C-Reactive Protein Levels in Obese Postmenopausal Women
Tchernof, A., Nolan, A., Sites, C. K., Ades, P. A., & Poehlman, E. T. (2002) · Circulation · doi:10.1161/hc0502.103331 · Cited by 541 · see citing works
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LORENZO, A. D. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i2.681 · Cited by 312 · see citing works
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Schöttl, T., Kapser-Fischer, I., & Ussar, S. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.162958 · Cited by 215 · see citing works
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BackgroundMetabolic and Behavioral Characteristics of Metabolically Obese but Normal-Weight Women
Conus, F., Allison, D. B., Rabasa-Lhoret, R., St-Onge, M., St-Pierre, D. H., Tremblay-Lebeau, A., & Poehlman, E. T. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0265 · Cited by 215 · see citing works
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Characteristics of metabolically obese normal-weight (MONW) subjects
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BackgroundResultIncident Cardiovascular Disease Events in Metabolically Benign Obese Individuals
Ogorodnikova, A. D., Kim, M., McGinn, A. P., Muntner, P., Khan, U. I., & Wildman, R. P. (2011) · Obesity · doi:10.1038/oby.2011.243 · Cited by 146 · see citing works
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MethodDoes Metabolically Healthy Obesity Exist?
Muñoz‐Garach, A., Cornejo-Pareja, I. M., & Tinahones, F. J. (2016) · Nutrients · doi:10.3390/nu8060320 · Cited by 145 · see citing works
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Brandão, I., Martins, M. J., & Monteiro, R. (2020) · Metabolites · doi:10.3390/metabo10020048 · Cited by 115 · see citing works
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“sidering that subcutaneous fat stores tend to be increased in individuals who have increased visceral fat mass, even when all of the subjects studied are of normal weight (28).”
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Obesity, metabolic health, and mortality in adults: a nationwide population-based study in Korea
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ResultDeterminants of Insulin‐resistant Phenotypes in Normal‐weight and Obese Black African Women
Jennings, C., Lambert, E. V., Collins, M., Joffe, Y. T., Levitt, N. S., & Goedecke, J. H. (2008) · Obesity · doi:10.1038/oby.2008.233 · Cited by 90 · see citing works
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MethodPhysical Activity, Obesity Status, and Glycemic Control
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“reported that physical activity energy expenditure was significantly lower (412 kcal lower) in the MANW group compared to the MHNW group [33].”
ResultIs Visceral Adiposity the “Enemy Within”?
Tracy, R. P. (2001) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.21.6.881 · Cited by 81 · see citing works
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Ferrannini, E. (2006) · Annals of Medicine · doi:10.1080/07853890500415358 · Cited by 74 · see citing works
“Physical activity, on the other hand, is a strong determinant of insulin sensitivity (46) and cardiorespiratory fitness is a potent predictor of metabolic and cardiovascular risk (47,48).”
BackgroundPrevalence and Clinical Profile of Metabolic Obesity and Phenotypic Obesity in Asian Indians
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Life Years Lost Associated with Obesity-Related Diseases for U.S. Non-Smoking Adults
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“5, 25); overweight if BMI M [25, 30); class I obese if BMI M [30, 35), class II obese if BMI M [35, 40), and class III obese if BMI is at least 40 kg/m(2).”
BackgroundFactors that may impede the weight loss response to exercise‐based interventions
Boutcher, S. H., & Dunn, S. L. (2009) · Obesity Reviews · doi:10.1111/j.1467-789x.2009.00621.x · Cited by 67 · see citing works
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BackgroundSleep deprivation and energy metabolism: to sleep, perchance to eat?
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Excess accumulation of body fat is related to dyslipidemia in normal-weight subjects
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Changes in Metabolic Health Status Over Time and Risk of Developing Type 2 Diabetes
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Severe Periodontitis Is Associated with Insulin Resistance in Non-abdominal Obese Adults
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Main characteristics of metabolically obese normal weight and metabolically healthy obese phenotypes
Teixeira, T. F., Alves, R. D. M., Moreira, A. P. B., & Pelúzio, M. D. C. G. (2015) · Nutrition Reviews · doi:10.1093/nutrit/nuu007 · Cited by 58 · see citing works
Peppa, Μ., Koliaki, C. C., Papaefstathiou, A., Garoflos, E., Katsilambros, N. L., Raptis, S., Hadjidakis, D. I., & Dimitriadis, G. (2013) · Obesity · doi:10.1002/oby.20227 · Cited by 58 · see citing works
“Our findings add to the existing strong evidence that central adiposity is a prominent body composition factor, which is associated with ‘‘metabolically obese’’ phenotypes, irrespective of BMI (4-6,12,34).”
BackgroundResultBåvenholm, P., Kuhl, J., Pigon, J., Saha, A. K., Ruderman, N. B., & Efendić, S. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020330 · Cited by 58 · see citing works
“(32) recently reported that young normalweight and insulin-resistant women have increased total and visceral fat, compared with control women of similar weight and BMI but normal insulin sensitivity.”
BackgroundPrevalence of metabolic syndrome in normal weight individuals
Suliga, E., Kozieł, D., & Głuszek, S. (2016) · Annals of Agricultural and Environmental Medicine · doi:10.5604/12321966.1226858 · Cited by 58 · see citing works
Shaharyar, S., Roberson, L. L., Jamal, O. S., Younus, A., Blaha, M. J., Ali, S. S., Zide, K., Agatston, A. A., Blumenthal, R. S., Conceição, R., et al. (2015) · Journal of Obesity · doi:10.1155/2015/178526 · Cited by 57 · see citing works
“The aim of this study was to explore the association amongMHO, MUNW, and markers of subclinical CVD burden as assessed by high sensitivity C-reactive protein (CRP) and hepatic steatosis (HS) in individuals without overt CVD.”
InfluentialChoi, J., Se-Young, O., Lee, D., Tak, S. K., Hong, M., Park, S., Cho, B., & Park, M. (2010) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2010.09.001 · Cited by 57 · see citing works
“[6] reported that MONW women had a similar proportion of fat-free mass, but had a higher proportion of total fat mass and body fat percentage compared to metabolically healthy, normal weight (MHNW) women.”
Insulin resistance and metabolic syndrome in normal-weight individuals
Chen, S., Chen, Y., Liu, X., Li, M., Wu, B., Li, Y., Liang, Y., Shao, X., Holthöfer, H., & Zou, H. (2013) · Endocrine · doi:10.1007/s12020-013-0079-8 · Cited by 56 · see citing works
The ESHRE/ASRM consensus on polycystic ovary syndrome (PCOS) – an extended critical analysis
Geisthövel, F., & Rabe, T. (2007) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60902-9 · Cited by 56 · see citing works
“but normal weight (MONW)’ individuals (Ruderman et al., 1998; Dvorak et al., 1999; St-Onge et al., 2004; Meigs et al., 2006) and ‘metabolically normal but obese (MNO)’”
BackgroundBo, S., Musso, G., Gambino, R., Villois, P., Gentile, L., Durazzo, M., Cavallo‐Perin, P., & Cassader, M. (2012) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.040006 · Cited by 52 · see citing works
“The following effects have been reported as putative contributors to insulin resistance in NW subjects: reduced physical activity, lower peak oxygen uptake, less dietary restraint (4, 39), increased accumulation of visceral adipose tissue (2, 16, 39, 40), low fiber intake (41), high concentrations of free fatty acids…”
BackgroundAgius, R., Pace, N. P., & Fava, S. (2023) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3725 · Cited by 62 · see citing works
“14,22,30,51,52 Again, the use of consensus criteria to define MH should help to remove definition ‐ related variability.”
BackgroundIs adiposity at normal body weight relevant for cardiovascular disease risk?
Tanaka, S., Togashi, K., Rankinen, T., Përusse, L., Leon, A. S., Rao, D. C., Skinner, J. S., Wilmore, J. H., & Bouchard, C. (2002) · International Journal of Obesity · doi:10.1038/sj.ijo.0801880 · Cited by 54 · see citing works
Normal weight dyslipidemia: Is it all about the liver?
Ipsen, D. H., Tveden‐Nyborg, P., & Lykkesfeldt, J. (2016) · Obesity · doi:10.1002/oby.21443 · Cited by 51 · see citing works
“However, generally applied features of NWD include dyslipidemia and increased blood glucose, waist circumference, and BMI when compared with controls (42-51).”
BackgroundInfluentialLee, J., Lee, H. C., Shim, J., Im, J., Kim, S., Choi, H.-A., & Lee, D. (2007) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2007.02780.x · Cited by 49 · see citing works
Catov, J. M., Newman, A. B., Roberts, J. M., Sutton‐Tyrrell, K., Kelsey, S. F., Harris, T. B., Jackson, R., Colbert, L. H., Satterfield, S., Ayonayon, H. N., et al. (2006) · Annals of Epidemiology · doi:10.1016/j.annepidem.2006.02.007 · Cited by 49 · see citing works
Bervoets, L., & Massa, G. (2016) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem-2015-0395 · Cited by 47 · see citing works
“However, it has previously been shown that the MUO phenotype also occurs in normalweight individuals and that a higher degree of obesity in children and adolescents is not always associated with a higher prevalence of prediabetes and/or the metabolic syndrome [19, 27].”
BackgroundCho, Y. G., Song, H. J., Kim, J. M., Park, K., Paek, Y., Cho, J. J., Caterson, I. D., & Kang, J. G. (2009) · Metabolism · doi:10.1016/j.metabol.2009.01.004 · Cited by 47 · see citing works
Tanrıkulu-Kılıç, F., Bekpınar, S., Ünlüçerçi, Y., & Orhan, Y. (2006) · Physiological Research · doi:10.33549/physiolres.930745 · Cited by 45 · see citing works
Chen, S., Chen, Y., Liu, X., Li, M., Wu, B., Li, Y., Liang, Y., Shao, X., Holthöfer, H., & Zou, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074058 · Cited by 44 · see citing works
“Apart from fat mass and fat distribution, dietary, physical inactivity, genetic factors are associated with IR in non-obese individuals [1,18].”
BackgroundTanaka, S., Togashi, K., Rankinen, T., Përusse, L., Leon, A. S., Rao, D. C., Skinner, J. S., Wilmore, J. H., Després, J., & Bouchard, C. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802545 · Cited by 43 · see citing works
Kim, D., Nam, S.-Y., Ahn, C. W., Kim, K., Yoon, S., Kim, J., Cha, B., Lim, S., Kim, K.-R., Lee, H., et al. (2003) · Diabetes Care · doi:10.2337/diacare.26.6.1825 · Cited by 42 · see citing works
“Moreover, visceral adipose tissue is well recognized to be significantly related to insulin resistance of obese type 2 diabetic patients and even patients with normal weight (4,5).”
BackgroundJeor, S. T. S., Hayman, L. L., Daniels, S. R., Gillman, M. W., Howard, G., Law, C., Lewis, C. E., & Poehlman, É. T. (2004) · Circulation · doi:10.1161/01.cir.0000140092.48032.d2 · Cited by 44 · see citing works
Avolio, E., Gualtieri, P., Romano, L., Pecorella, C., Ferraro, S., Palma, G., Di Renzo, L., & De Lorenzo, A. (2020) · Current Medicinal Chemistry · doi:10.2174/0929867326666190326113607 · Cited by 43 · see citing works
Metabolic Syndrome Pathophysiology
Das, U. N. (2010) · Wiley eBooks · doi:10.1002/9780813820637 · Cited by 44 · see citing works
- Authors
- Dvorak, R. V., DeNino, W. F., Ades, P. A., & Poehlman, E. T.
- Affiliations
- Department of Medicine, College of Medicine, University of Vermont, Burlington 05405, USA.
- University of Vermont (US)
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 1999-11-01
- Volume
- 48
- Issue
- 11
- Pages
- 2210-2214
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2155025864
- Cited by
- 243
- References
- 0
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 4 · 2023: 6 · 2022: 9 · 2021: 7 · 2020: 4 · 2019: 10 · 2018: 15 · 2017: 8 · 2016: 16 · 2015: 11 · 2014: 12 · 2013: 12 · 2012: 17
- FWCI
- 3.86
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ag015114-03)
- National Institute on Aging (R01-AG15114)
- National Institute of Dental and Craniofacial Research (DE 950226)
- National Center for Research Resources (RR-00109)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Obesity, Physical Activity, Diet
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- insulin resistance, visceral fat, subcutaneous abdominal fat, physical activity energy expenditure, cardiorespiratory fitness, body composition, glucose tolerance, type 2 diabetes risk, cardiovascular risk, young women
- MeSH terms
- Adipose Tissue, Adult, Blood Glucose, Blood Pressure, Body Constitution, Body Weight, Contraceptives, Oral, Diabetes Mellitus, Female, Glucose, Humans, Obesity, Phenotype, Reference Values, Body Mass Index
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