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Cited by 403Diabetes, Cardiovascular Risks, and LipoproteinsLiver Disease Diagnosis and TreatmentDiet, Metabolism, and Disease

Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

Open access
Petersen, Kitt Falk, Dufour, Sylvie, Feng, Jing, Befroy, Douglas, Dziura, James, Man, Chiara Dalla, Cobelli, Claudio, Shulman, Gerald I.·2006·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.0608537103PMC PMC1693873
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Abstract

Type 2 diabetes mellitus (T2DM) is strongly associated with obesity in most, but not all, ethnic groups, suggesting important ethnic differences in disease susceptibility. Although it is clear that insulin resistance plays a major role in the pathogenesis of T2DM and that insulin resistance is strongly associated with increases in hepatic (HTG) and/or intramyocellular lipid content, little is known about the prevalence of insulin resistance and potential differences in intracellular lipid distribution among healthy, young, lean individuals of different ethnic groups. To examine this question, 482 young, lean, healthy, sedentary, nonsmoking Eastern Asians ( n = 49), Asian-Indians ( n = 59), Blacks ( n = 48), Caucasians ( n = 292), and Hispanics ( n = 34) underwent an oral glucose tolerance test to assess whole-body insulin sensitivity by an insulin sensitivity index. In addition, intramyocellular lipid and HTG contents were measured by using proton magnetic resonance spectroscopy. The prevalence of insulin resistance, defined as the lower quartile of insulin sensitivity index, was ≈2- to 3-fold higher in the Asian-Indians compared with all other ethnic groups, and this could entirely be attributed to a 3- to 4-fold increased prevalence of insulin resistance in Asian-Indian men. This increased prevalence of insulin resistance in the Asian-Indian men was associated with an ≈2-fold increase in HTG content and plasma IL-6 concentrations compared with Caucasian men. These data demonstrate important ethnic and gender differences in the pathogenesis of insulin resistance in Asian-Indian men and have important therapeutic implications for treatment of T2DM and for the development of steatosis-related liver disease in this ethnic group.

AI snapshot

Written from the paper’s full text.

TL;DR

In a cross-sectional study of 482 young, lean, healthy, sedentary, nonsmoking adults, insulin resistance prevalence was 2- to 3-fold higher in Asian-Indians than in other ethnic groups, entirely attributable to a 3- to 4-fold increase in Asian-Indian men. This increased insulin resistance in Asian-Indian men was associated with approximately 2-fold higher hepatic triglyceride content and plasma IL-6 concentrations compared with Caucasian men.

Key findings

  • Insulin resistance, defined as the lowest quartile of the insulin sensitivity index (ISI), was present in 59% of Asian-Indians versus 20% of Caucasians, 30% of Eastern-Asians, 33% of Blacks, and 18% of Hispanics. This 2- to 3-fold higher prevalence was entirely accounted for by Asian-Indian men, in whom prevalence was 81% (3- to 4-fold higher than other men).
  • In Asian-Indian men compared with Caucasian men, after adjustment for ISI, hepatic triglyceride content was >2-fold higher (1.54% vs. 0.77%, adjusted P = 0.007) and plasma IL-6 was approximately 2-fold higher (1.48 vs. 0.79 pg/ml, adjusted P = 0.001); the intramyocellular lipid difference did not persist after ISI adjustment (0.90% vs. 0.76%, adjusted P = 0.12).
  • Asian-Indian men had increased basal β-cell responsivity (Phib 7.98 ± 2.1 vs. 6.21 ± 2.32, P < 0.04) but a lower disposition index (994 ± 1,012 vs. 2,517 ± 2,518, P < 0.01), indicating inadequate β-cell compensation for their degree of insulin resistance.
  • There were no differences in ISI or HOMA among the other ethnic or gender groups, and Asian-Indian women did not show the increased prevalence of insulin resistance seen in Asian-Indian men.

Methods

  • Cross-sectional study of 482 young, lean, healthy, sedentary, nonsmoking volunteers recruited from the New Haven community from 1998 to 2006: Caucasian n = 292, Eastern-Asian n = 59, Asian-Indian n = 49, Black n = 48, and Hispanic n = 34 (Table 1 and Experimental Procedures; the abstract lists Eastern-Asian n = 49 and Asian-Indian n = 59).
  • Whole-body insulin sensitivity was assessed by a 2-h, 75-g oral glucose tolerance test with HOMA and ISI; β-cell responsiveness was estimated from OGTT glucose and C-peptide concentrations using the oral C-peptide minimal model; hepatic triglyceride and intramyocellular lipid contents were measured by proton magnetic resonance spectroscopy in subgroups.
  • Differences across racial groups were evaluated by analysis of covariance adjusted for BMI and age with Tukey’s HSD pairwise comparisons; analyses were stratified by gender after gender significantly modified the effect of race on insulin sensitivity (P < 0.001), and some comparisons were further adjusted for ISI.

Limitations

  • The paper states that the MRS subgroup differed slightly from subjects who did not undergo MRS (fasting plasma glucose 94.2 vs. 90.1 mg/dl; ISI median 3.5 vs. 4.8; HOMA median 2.64 vs. 1.93), and that the higher proportion of Asian-Indian men who underwent MRS compared with Caucasian men (74% vs. 59%) suggests the estimates of differences may be conservative.
  • The paper states that whether increased plasma IL-6 plays a causative role or is secondary to hepatic steatosis and insulin resistance remains to be determined, and that the molecular mechanism of fat-induced hepatic insulin resistance is unclear.
  • Evident from the text: the cross-sectional design cannot establish temporal or causal relationships; MRS and adipocytokine analyses were restricted to subsets of Caucasian and Asian-Indian men; and findings may not generalize beyond young, lean, sedentary, nonsmoking volunteers.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1073/pnas.0608537103

Cites

43 of 43 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 34 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    The increased prevalence of insulin resistance in Asian-Indian men is associated with an approximately 2-fold increase in hepatic triglyceride (HTG) content compared with Caucasian men.

    “This increased prevalence of insulin resistance in the Asian-Indian men was associated with an ≈ 2-fold increase in HTG content and plasma IL-6 concentrations compared with Caucasian men.”
    • Also stated in: § Results · plain
      “when adjusted for by the ISI, the Asian-Indian men had a > 2-fold increase in HTG content compared with the Caucasian men”
    • Also stated in: § Discussion · plain
      “when adjusted for the ISI, this increased prevalence of insulin resistance in Asian-Indian men was associated with an ≈ 2-fold increase in HTG content and plasma IL-6 concentrations compared with Caucasian men.”
    Quote in the paperSubstantial claim
  • Findingown data
    § Results

    When adjusted for the insulin sensitivity index, the difference in intramyocellular lipid content between Asian-Indian and Caucasian men did not persist.

    “whereas the differences in the amount of IMCL between the two groups did not persist (Table 4).”
    Quote in the paperSubstantial claim
  • Findingown data
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    The increased prevalence of insulin resistance in Asian-Indian men is associated with an approximately 2-fold increase in plasma IL-6 concentrations compared with Caucasian men.

    “This increased prevalence of insulin resistance in the Asian-Indian men was associated with an ≈ 2-fold increase in HTG content and plasma IL-6 concentrations compared with Caucasian men.”
    • Also stated in: § Results · plain
      “Plasma concentrations of IL-6 and leptin were both increased in Asian-Indian men compared with Caucasian men both adjusted and unadjusted for by the ISI (Table 4).”
    • Also stated in: § Discussion · plain
      “In contrast, we did observe an ≈ 2-fold increase in plasma IL-6 concentrations in the Asian-Indian men that persisted even after adjustment for the ISI.”
    Quote in the paperSubstantial claim
  • Findingown data
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    The prevalence of insulin resistance, defined as the lower quartile of the insulin sensitivity index, is approximately 2- to 3-fold higher in Asian-Indians compared with all other ethnic groups.

    “The prevalence of insulin resistance, defined as the lower quartile of insulin sensitivity index, was ≈ 2- to 3-fold higher in the AsianIndians compared with all other ethnic groups”
    • Also stated in: § Results · plain
      “the prevalence of insulin resistance, as defined by the lower ISI quartile, was 2- to 3-fold higher in the Asian-Indian group (59%) compared with other ethnic groups [Caucasian (20%), Eastern-Asian (30%), Black (33%), and Hispanic (18%)].”
    Quote in the paperSubstantial claim
  • Findingown data
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    The increased prevalence of insulin resistance in Asian-Indians can entirely be attributed to a 3- to 4-fold increased prevalence of insulin resistance in Asian-Indian men.

    “and this could entirely be attributed to a 3- to 4-fold increased prevalence of insulin resistance in Asian-Indian men.”
    • Also stated in: § Discussion · boosted
      “These studies demonstrate that the prevalence of insulin resistance in healthy, young, lean Asian-Indian men is 3- to 4-fold greater than lean men of other ethnic groups.”
    Quote in the paperSubstantial claim
  • May combine two claims. 9
  • Classified as probably not a substantial claim. 9

  • May combine two claims.

    Findingown data
    § Results

    Both intrahepatic triglyceride and intramyocellular lipid (IMCL) content were increased in Asian-Indian men compared with Caucasian men.

    “Both intrahepatic triglyceride and IMCL content were increased in the Asian-Indian men compared with the Caucasian men (Table 4).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    Eastern-Asians and Asian-Indians tend to develop type 2 diabetes mellitus without the same degree of generalized adiposity and with a greater tendency to develop central obesity.

    “In contrast to other ethnic groups, Eastern-Asians and Asian-Indians tend to develop T2DM without the same degree of generalized adiposity (2) and with a greater tendency to develop central obesity (3).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [2] source

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  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductreasoning
    § Results

    Only nonsmoking and sedentary subjects were selected to participate because smoking and physical activity can affect insulin sensitivity.

    “Because smoking and physical activity can affect insulin sensitivity, only subjects who were nonsmoking and sedentary were selected to participate in these studies.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Smoking and physical activity can affect insulin sensitivity.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Discussion

    Recent studies suggest that visceral adiposity may play an important role in causing hepatic insulin resistance through release of fatty acids and adipocytokines to the liver via the portal vein.

    “Recent studies have also suggested that visceral adiposity may play an important role in causing hepatic insulin resistance through its release of fatty acids and adipocytokines to the liver via the portal vein (28-31).”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [28] Goldstein BJ (2002) Am J Cardiol 90:3G-10G. source

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    • cites [29] Wellen KE, Hotamisligil GS (2005) J Clin Invest 115:1111-1119. source

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    • cites [30] Bjorntorp P (1992) Ann Med 24:465-468. source

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    • cites [31] Kabir M, Catalano KJ, Ananthnarayan S, Kim SP, Van Citters GW, Dea MK, Bergman RN (2005) Am J Physiol 288:E454-E461. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    Insulin resistance plays a major role in the pathogenesis of type 2 diabetes mellitus.

    “Although it is clear that insulin resistance plays a major role in the pathogenesis of T2DM”
    • Also stated in: § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men · boosted
      “Although the primary cause of T2DM is unknown, insulin resistance plays a major role in the pathogenesis of this disease and is strongly associated with increases in intracellular fat content in liver and skeletal muscle (9-13).”
    Quote in the paperNot a substantial claim0 of 5 sources checked
    • cites [9] source

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  • May combine two claims.

    Study design and conductown data
    § Results

    All subjects were weight-stable, and there were no significant differences in dietary composition among the ethnic groups as assessed by dietary questionnaire.

    “Furthermore, all subjects were weight-stable, and there were no significant differences in dietary composition among the ethnic groups as assessed by dietary questionnaire (data not shown).”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation
    § Discussion

    Recent studies in rodents have demonstrated that acute infusions of IL-6 cause insulin resistance in both liver and skeletal muscle.

    “Recent studies in rodents have demonstrated that acute infusions of IL-6 caused insulin resistance in both liver and skeletal muscle (32).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [32] Kim HJ, Higashimori T, Park SY, Choi H, Dong J, Kim YJ, Noh HL, Cho YR, Cline G, Kim YB, Kim JK (2004) Diabetes 53:1060-1067. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data
    § Results

    Data were adjusted for age and BMI.

    “*Data were adjusted for age and BMI.”
    • Also stated in: § Experimental Procedures · plain
      “Differences across racial groups were evaluated by analysis of covariance with adjustment for BMI and age with pairwise comparisons corrected by Tukey's HSD test.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    Type 2 diabetes mellitus is strongly associated with obesity in most, but not all, ethnic groups, suggesting important ethnic differences in disease susceptibility.

    “Type 2 diabetes mellitus (T2DM) is strongly associated with obesity in most, but not all, ethnic groups, suggesting important ethnic differences in disease susceptibility.”
    • Also stated in: § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men · hedged
      “These data suggest important ethnic differences in T2DM susceptibility (5-8).”
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    Premisecitation
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    The prevalence of diabetes is higher in Hispanics and Blacks compared with Caucasians.

    “In addition, the prevalence of diabetes has been found to be much higher in Hispanics and Blacks compared with Caucasians (4).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [4] source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data
    § Results

    All subjects were young, lean, healthy, and similar in age, weight, and BMI among the different ethnic groups, although Eastern-Asian subjects tended to be slightly smaller and leaner.

    “All subjects were young, lean, healthy, and similar in age, weight, and BMI among the different ethnic groups, although the Eastern-Asian subjects tended to be on average slightly smaller and leaner than the other ethnic groups (Table 1).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given
    § Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men

    Increases in intracellular lipid metabolism have been implicated in the pathogenesis of insulin resistance in liver and muscle.

    “Because increases in intracellular lipid metabolism have been implicated in the pathogenesis of insulin resistance in liver and muscle, these studies were complemented by proton magnetic resonance spectroscopy (MRS) measurements of hepatic triglyceride (HTG) and intramyocellular lipid (IMCL) content.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductown data
    § Results

    Physical activity questionnaires demonstrated that all ethnic groups were sedentary and had similar daily activity levels.

    “Physical activity questionnaires demonstrated that all groups were indeed sedentary and had similar daily activity levels (Table 1).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § Experimental Procedures

    The RIA for leptin did not cross-react with human proinsulin, insulin, or glucagon.

    “The RIA for leptin did not cross-react with human proinsulin, insulin, or glucagon.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductown data
    § Results

    The proportion of Asian-Indian subjects who underwent MRS was higher than the proportion of Caucasian men who underwent MRS (74% vs. 59%), suggesting that estimates of differences between Asian-Indian and Caucasian men may be conservative.

    “Nevertheless, the proportion of Asian-Indian subjects who underwent MRS was higher than the proportion of the Caucasian men who underwent MRS (74% vs. 59%), suggesting that our estimates of differences between Asian-Indian and Caucasian men may be conservative.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Discussion

    There is increasing evidence for a causal relationship between hepatic steatosis and hepatic insulin resistance in rodent models and in patients with nonalcoholic fatty liver disease.

    “There is increasing evidence for a causal relationship between hepatic steatosis and hepatic insulin resistance both in rodent models with hepatic steatosis and in patients with nonalcoholic fatty liver disease (4, 18-25).”
    Quote in the paperNot a substantial claim0 of 9 sources checked
    • cites [4] source

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    • cites [23] Kim JK, Fillmore JJ, Chen Y, Yu C, Moore IK, Pypaert M, Lutz EP, Kako Y, Velez-Carrasco W, Goldberg IJ, et al. (2001) Proc Natl Acad Sci USA 98:7522-7527. source

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    • cites [24] Kim JK, Gavrilova O, Chen Y, Reitman ML, Shulman GI (2000) J Biol Chem 275:8456-8460. source

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    • cites [25] Savage DB, Choi CS, Samuel VT, Liu ZX, Zhang D, Wang A, Zhang XM, Cline GW, Yu XX, Geisler JG, et al. (2006) J Clin Invest 116:817-824. source

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  • May combine two claims.

    Interpretationreasoning
    § Discussion

    The increased prevalence of nonalcoholic fatty liver disease in Asian-Indian men has important implications for future health risks because this condition is associated with steatohepatitis, which may progress to cirrhosis and end-stage liver disease.

    “Furthermore, increased prevalence of nonalcoholic fatty liver disease in the Asian-Indian men has important implications for future health risks in these individuals because this condition is associated with steatohepatitis, which may progress to cirrhosis and end-stage liver disease.”
    Quote in the paperSubstantial claim
17 of 17

  • The paper relies on this without support.

    Smoking and physical activity can affect insulin sensitivity.

    “Because smoking and physical activity can affect insulin sensitivity, only subjects who were nonsmoking and sedentary were selected to participate in these studies.”
1 of 1

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Recent studies by our group demonstrate a relatively low prevalence of hepatic steatosis in young, lean, healthy subjects of different ethnic backgrounds, with the important exception of Asian Indian males who have a marked increase in the prevalence of hepatic steatosis.

    “is consistent with recent studies by our group demonstrating the relatively low prevalence of hepatic steatosis in young, lean, healthy subjects of different ethnic backgrounds with the important exception of Asian Indian males who have a marked increase in the prevalence of hepatic steatosis (13).”

    From The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome (2007) · cites this paper as [13]

  • Asian Indian men have a high prevalence of nonalcoholic fatty liver disease and insulin resistance.

    “We began by studying a cohort of healthy Asian Indian men, a group that has been shown to have a high prevalence of nonalcoholic fatty liver disease and insulin resistance.9”

    From Apolipoprotein C3 gene variants in nonalcoholic fatty liver disease (2010) · cites this paper as [9]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Insulin resistance is defined using both a quartile and a tertile

    Major

    The Results section defines insulin resistance using the lowest ISI quartile, but the Calculations section specifies the lowest tertile. These thresholds classify different proportions of the study population and affect the reported prevalence comparison.

  • Eastern-Asian and Asian-Indian sample sizes are reversed

    Minor

    The opening summary assigns 49 participants to the Eastern-Asian group and 59 to the Asian-Indian group, while the Methods section assigns 59 and 49, respectively. The Methods counts agree with the tables.

2 of 2

Cites

Flagged first, then by citations

Research works printed but not linked: 2

  1. D Galipeau, S Verma, JH McNeill Am J Physiol 283, H2478–H2484 (2002).
  2. H Vasudevan, H Xiang, JH McNeill Am J Physiol 289, H1335–H1342 (2005).

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Related

Authors
Petersen, K. F., Dufour, S., Feng, J., Befroy, D., Dziura, J., Man, C. D., Cobelli, C., & Shulman, G. I.
Affiliations
  • Yale University (US)
  • Howard Hughes Medical Institute (US)
  • University of Padua (IT)
Corresponding author
  • Man, Chiara Dalla
  • Shulman, Gerald I.
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2006-11-28
Volume
103
Issue
48
Pages
18273-18277
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.0608537103
PMC
PMC1693873
OpenAlex
W1989653265
Semantic Scholar
c5640cad2608a91448722cb4861d7daa2600a2e0
Cited by
403
References
43
Citations by year
2026: 9 · 2025: 21 · 2024: 7 · 2023: 15 · 2022: 22 · 2021: 18 · 2020: 21 · 2019: 29 · 2018: 22 · 2017: 16 · 2016: 25 · 2015: 35 · 2014: 28 · 2013: 27 · 2012: 19
FWCI
9.96
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Padua Research Archive (University of Padova) (submittedVersion, other-oa)
Funders
  • American Diabetes Association (DK-49230)
  • Yale University
  • National Institute on Aging (R01-AG-23686, R01AG023686)
  • National Institute of Diabetes and Digestive and Kidney Diseases (P30DK45735, R01DK049230, R01 DK-49230, P30DK045735, P01DK068229)
  • National Center for Research Resources (M01RR000125, M01 RR-00125)
Topics
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
  • Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
Keywords
insulin resistance, non-alcoholic fatty liver disease, type 2 diabetes, hepatic triglyceride content, intramyocellular lipid, insulin sensitivity index, interleukin-6, ethnic differences, sex differences, 1H NMR
MeSH terms
Adipose Tissue, Adult, Fatty Liver, Female, Humans, India, Insulin Resistance, Male, Sex Characteristics, Triglycerides, Prevalence, Cytokines, Insulin-Secreting Cells

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