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Low testosterone levels are common and associated with insulin resistance in men with diabetes

Grossmann, Mathis, Thomas, Merlin C., Panagiotopoulos, Sianna, Sharpe, Ken, MacIsaac, Richard J., Clarke, Sophie, Zajac, Jeffrey D., Jerums, George·2008·The Journal of Clinical Endocrinology & Metabolism
DOI 10.1210/jc.2007-2177
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Abstract

Context: Low testosterone levels are common in men with type 2 diabetes and may be associated with insulin resistance. Objective: We investigated prevalence of testosterone deficiency and the relationship between testosterone and insulin resistance in a large cohort of men with type 2 and type 1 diabetes. Design: The study was a cross-sectional survey of 580 men with type 2 diabetes and 69 men with type 1 diabetes. A subgroup of 262 men with type 2 diabetes was then reassessed after a median of 6 months. Results: Forty-three percent of men with type 2 diabetes had a reduced total testosterone, and 57% had a reduced calculated free testosterone. Only 7% of men with type 1 diabetes had low total testosterone. By contrast, 20.3% of men with type 1 diabetes had low calculated free testosterone, similar to that observed in type 2 diabetes (age-body mass index adjusted odds ratio = 1.4; 95% confidence interval = 0.7–2.9). Low testosterone levels were independently associated with insulin resistance in men with type 1 diabetes as well as type 2 diabetes. Serial measurements also revealed an inverse relationship between changes in testosterone levels and insulin resistance. Conclusions: Testosterone deficiency is common in men with diabetes, regardless of the type. Testosterone levels are partly influenced by insulin resistance, which may represent an important avenue for intervention, whereas the utility of testosterone replacement remains to be established in prospective trials.

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Written from the paper’s full text.

TL;DR

In a single-center cross-sectional survey, testosterone deficiency was common in men with diabetes: 43% of men with type 2 diabetes had low total testosterone and 57% had low calculated free testosterone, while 20.3% of men with type 1 diabetes had low calculated free testosterone. Low testosterone indices were independently associated with insulin resistance in both diabetes types, and longitudinal changes in testosterone were inversely related to changes in insulin resistance in a type 2 diabetes subgroup.

Key findings

  • Among men with type 2 diabetes, 43% had low total testosterone (<10 nmol/L) and 57% had low calculated free testosterone (<0.23 nmol/L); among men with type 1 diabetes, 7% had low total testosterone but 20.3% had low calculated free testosterone, similar to age- and BMI-adjusted men with type 2 diabetes (adjusted odds ratio 1.4; 95% CI 0.7–2.9).
  • Low total testosterone in type 2 diabetes was independently associated with insulin resistance by HOMA-IR (odds ratio 1.2; 95% CI 1.0–1.4), and calculated free testosterone was independently associated with insulin sensitivity in type 2 diabetes (partial correlation coefficient −0.10; P = 0.02) and with eGDR in type 1 diabetes (P = 0.04).
  • In 262 men with type 2 diabetes reassessed after a median of 6 months, the change in total testosterone was inversely related to the change in HOMA-IR (P = 0.01), and the change in calculated free testosterone was inversely correlated with the change in HOMA-IR (P = 0.03).
  • The prevalence of low calculated free testosterone approximately doubled per decade of age in type 2 diabetes (adjusted odds ratio 2.0; 95% CI 1.4–2.4) and in type 1 diabetes (adjusted odds ratio 2.4; 95% CI 1.4–3.9).

Methods

  • Cross-sectional survey of 580 men with type 2 diabetes and 69 men with type 1 diabetes at a single clinic; 6 men with type 2 diabetes were excluded from statistical analysis, and a randomly selected subgroup of 262 men with type 2 diabetes was reassessed after a median of 6 months (range 1–15 months).
  • Fasting blood samples were drawn between 0800 and 1000 h; total testosterone was measured by Access assay, SHBG by Immulite, and calculated free testosterone was derived using Vermeulen’s formula. Low total testosterone was defined as <10 nmol/L and low calculated free testosterone as <0.23 nmol/L.
  • Insulin resistance was estimated by HOMA-IR in type 2 diabetes and by eGDR in type 1 diabetes; analyses used logistic regression, multiple regression, ANOVA, analysis of covariance, and nonparametric tests as appropriate.

Limitations

  • The paper states that it did not obtain a detailed symptomatology history, so the biochemical testosterone deficiency may not represent a true hypogonadal state; it also states that a single low testosterone level is inadequate for diagnosing hypogonadism because of variability, and on repeat testing 27% of men with low total testosterone and 33% with low calculated free testosterone had normal levels.
  • The paper states that longitudinal changes in testosterone in type 1 diabetes remain to be explored and that the utility of testosterone replacement remains to be established in prospective trials.
  • Evident from the text: the study was observational and single-center, with a tertiary referral cohort that had longstanding diabetes and high complication prevalence, which may limit generalizability and cannot establish causality.

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

Integrity signals

Registry

Crossref · 10.1210/jc.2007-2177

Cites

37 of 37 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 20 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    In men with type 1 diabetes, 7% had low total testosterone.

    “Only 7% of men with type 1 diabetes had low total testosterone.”
    • Also stated in: § Prevalence of testosterone deficiency in men with type 1 diabetes · plain
      “Few men with type 1 diabetes had low TT (7.2%, P Ͻ 0.001, vs. type 2 diabetes, Fig. 1).”
    • Also stated in: § Statistical analysis · plain
      “Low TT (Ͻ10 nmol/liter) (%) 7% 43% 42%”
    Quote in the paperNot a substantial claim
  • Findingown data

    In men with type 2 diabetes, 57% had low calculated free testosterone (<0.23 nmol/L).

    “57% had a reduced calculated free testosterone”
    • Also stated in: § Discussion · plain
      “57% had low cFT levels”
    • Also stated in: § Statistical analysis · plain
      “Low cFT (Ͻ0.23 nmol/liter) (%) 20% 57% 60%”
    Quote in the paperSubstantial claim
  • Findingown data

    After adjusting for age, BMI, and other confounders, the frequency of low total testosterone remained significantly higher in men with type 2 diabetes compared with type 1 diabetes (adjusted OR 4.0; 95% CI 1.5-10.7; P=0.005).

    “After adjusting for age, body mass index (BMI), and other confounding factors, the frequency of low TT levels remained significantly higher in men with type 2 diabetes when compared with those with type 1 diabetes (adjusted odds ratio ϭ 4.0; 95% CI ϭ 1.5-10.7;P ϭ 0.005).”
    Quote in the paperSubstantial claim
  • Findingown data

    In men with type 1 diabetes, for each decade of life, the prevalence of low calculated free testosterone effectively doubled (adjusted OR 2.4; 95% CI 1.4-3.9).

    “For each decade of life, the prevalence of low cFT levels effectively doubled (adjusted odds ratio for low cFT levels ϭ 2.4; 95% CI ϭ 1.4 -3.9).”
    Quote in the paperNot a substantial claim
  • Findingcitation

    The frequency of low total testosterone in men with type 1 diabetes was not significantly greater than that observed in reproductively normal young men.

    “This frequency of low TT levels in men with type 1 diabetes was not significantly greater than observed in reproductively normal young men (21).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [21] Sikaris, 2005, Reproductive hormone reference intervals for healthy fertile young men: evaluation of automated platform assays., J Clin Endocrinol Metab source

      Not checked in the free run.

  • May combine two claims. 6
  • Classified as probably not a substantial claim. 10

  • May combine two claims.

    Findingown data

    In the follow-up subgroup, 27% of individuals with low total testosterone and 33% with low calculated free testosterone had levels in the normal range when retested.

    “finding that 27 and 33% of individuals with low TT and cFT levels respectively had levels in the normal range when retested.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the follow-up subgroup of men with type 2 diabetes, the prevalence of low total testosterone at second analysis was not significantly different from first (39 vs 42%, P=0.2), and there was a strong correlation between estimations (r2=0.73).

    “At the second analysis, the prevalence of testosterone deficiency defined by low TT levels (Ͻ10 nmol/liter) was not significantly different from obtained at the first estimation (39 vs. 42%, P ϭ 0.2), and there was a strong correlation between estimations (r 2 ϭ 0.73, Fig. 3A).”
    Quote in the paperNot a substantial claim

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

    Interpretationreasoning

    The utility of testosterone replacement remains to be established in prospective trials.

    “whereas the utility of testosterone replacement remains to be established in prospective trials.”
    • Also stated in: § Discussion · hedged
      “Although there is a strong rationale for testosterone replacement, the balance of benefits and risks is currently unknown and still to be defined by large and long-term clinical trials.”
    Quote in the paperNot a substantial claim

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

    Interpretationreasoning

    The stronger age association for calculated free testosterone may be due to the age-associated rise in SHBG.

    “possibly because of the age-associated rise in SHBG (Fig. 2C).”
    Quote in the paperNot a substantial claim

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

    Study design and conductown data

    None of the men in the follow-up subgroup received testosterone therapy.

    “None of these men received testosterone therapy.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    Interpretation of the study is limited because the authors did not obtain a detailed record of symptomatology history.

    “Interpretation of our study is therefore limited because we did not obtain a detailed record of symptomatology history.”
    Quote in the paperSubstantial claim

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

    Study design and conductnone given

    All men gave written informed consent, and the study was approved by the Human Research Ethics Committee.

    “All men gave written informed consent, and the study was approved by the Human Research Ethics Committee, Research Ethics Unit, Austin Health.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Testosterone may have deleterious actions on prostate disease, sleep apnea, and possibly cardiovascular risk.

    “However, testosterone may have deleterious actions on prostate disease, sleep apnea, and possibly cardiovascular risk (35).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [35] Rhoden, 2004, Risks of testosterone-replacement therapy and recommendations for monitoring., N Engl J Med source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning

    The appropriate clinical response to this emerging problem remains to be determined.

    “Consequently, the appropriate clinical response to this emerging problem remains to be determined.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Weight loss in obese insulin-resistant men is associated with increased testosterone levels.

    “previous studies have reported an association of loss of weight in obese insulinresistant men with increased testosterone levels (30).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [30] Niskanen, 2004, Changes in sex hormone-binding globulin and testosterone during weight loss and weight maintenance in abdominally obese men with the metabolic syndrome., Diabetes Obes Metab source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Testosterone replacement can improve performance, mood, and libido in men with hypogonadism and augments insulin sensitivity.

    “Certainly, testosterone replacement can improve performance, mood, and libido in men with hypogonadism (22) and augments insulin sensitivity (11,15).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [22] Bhasin, 2006, Testosterone therapy in adult men with androgen deficiency syndromes: an endocrine society clinical practice guideline., J Clin Endocrinol Metab [Erratum (2006) 91:1995–2010] source

      Not checked in the free run.

    • cites [11] Kapoor, 2006, Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholesterolaemia in hypogonadal men with type 2 diabetes., Eur J Endocrinol source

      Not checked in the free run.

    • cites [15] Simon, 2001, Androgen therapy improves insulin sensitivity and decreases leptin level in healthy adult men with low plasma total testosterone: a 3-month randomized placebo-controlled trial., Diabetes Care source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Study design and conductnone given

    The strengths of this study include the large number of subjects, inclusion of a large cohort of patients with type 1 diabetes, measurement of serum testosterone levels at the appropriate time of day (early morning), accurate assays for total and free testosterone levels, and longitudinal follow-up in a substantial number of men with type 2 diabetes.

    “The strengths of this study include the large number subjects, inclusion of a large cohort of patients with type 1 diabetes, measurement of serum testosterone levels at the appropriate time of day (early morning), accurate assays for total and free testosterone levels, and longitudinal follow-up in a substantial number of men with type 2 diabetes.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Reduced SHBG has been suggested as a surrogate marker for insulin resistance.

    “Indeed, reduced SHBG has been suggested as a surrogate marker for insulin resistance (33).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [33] Jayagopal, 2003, The biological variation of testosterone and sex hormone-binding globulin (SHBG) in polycystic ovarian syndrome: implications for SHBG as a surrogate marker of insulin resistance., J Clin Endocrinol Metab source

      Not checked in the free run.

13 of 13

  • The paper relies on this without support.

    The cohort of men attending a single tertiary referral clinic is representative of men with diabetes generally.

    “in a large, unselected cohort of men with type 1 or type 2 diabetes presenting at a single center”
    “large unselected cohort of men presenting to a single tertiary referral center”
1 of 1

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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.

  • Overall hs-CRP median is below both reported subgroup medians

    Major

    The reported hs-CRP medians for men with and without low TT are 7.7 and 4.5, respectively. The overall type 2 diabetes median in Table 1 is 3.0, which cannot be below both subgroup medians if these are the same cohort.

  • Macrovascular disease prevalence differs from Table 1

    Minor

    The results describe macrovascular disease in one third of men with type 2 diabetes, but Table 1 reports 42% for that group.

2 of 2

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Related

Authors
Grossmann, M., Thomas, M. C., Panagiotopoulos, S., Sharpe, K., MacIsaac, R. J., Clarke, S., Zajac, J. D., & Jerums, G.
Affiliations
  • The University of Melbourne (AU)
  • Baker Heart and Diabetes Institute (AU)
Corresponding author
Grossmann, Mathis
ORCID
Venue
The Journal of Clinical Endocrinology & Metabolism
Publisher
The Endocrine Society
Published
2008-05-01
Volume
93
Issue
5
Pages
1834-1840
ISSN
  • 0021-972X (ISSN-L)
  • 1945-7197
DOI
10.1210/jc.2007-2177
OpenAlex
W1975633687
Semantic Scholar
02f5d7f00e960755b4687b5424387d4da02771b3
Cited by
468
References
37
Citations by year
2026: 22 · 2025: 22 · 2024: 22 · 2023: 23 · 2022: 28 · 2021: 24 · 2020: 23 · 2019: 15 · 2018: 24 · 2017: 33 · 2016: 34 · 2015: 30 · 2014: 41 · 2013: 31 · 2012: 30
FWCI
15.97
Type
journal article
Language
en
Open access
closed
Locations
  • The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Medical Research Council
  • National Health and Medical Research Council
Topics
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
  • Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
Keywords
androgen deficiency, insulin resistance, type 2 diabetes, type 1 diabetes, men, free testosterone, total testosterone, testosterone replacement therapy, prevalence
MeSH terms
Adult, Aged, Cross-Sectional Studies, Diabetes Mellitus, Diabetes Mellitus, Type 1, Diabetes Mellitus, Type 2, Humans, Insulin Resistance, Male, Middle Aged, Sex Hormone-Binding Globulin, Testosterone

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