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Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes
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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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.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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%”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Strength:plain· not yet calibratedn = 69Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes- Also stated in: § Prevalence of testosterone deficiency in men with type 1 diabetes · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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%”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Discussion · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 1 diabetes
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 1 diabetes
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIn the paper
“This frequency of low TT levels in men with type 1 diabetes was not significantly greater than observed in reproductively normal young men (21).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 1 diabetes
What the sources say
- Not checked yetcites [21] Sikaris, 2005, Reproductive hormone reference intervals for healthy fertile young men: evaluation of automated platform assays., J Clin Endocrinol Metab source
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As in men with type 2 diabetes, the major predictor of cFT levels in individuals with type 1 diabetes was age (Fig. 2B).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 1 diabetes
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, when SHBG was included in the model, this difference between type 1 and type 2 diabetes was eliminated (P ϭ 0.16).”
- Also stated in: § Discussion · plain
“When SHBG was included into the model, this difference between type 1 and type 2 diabetes was eliminated (P ϭ 0.16).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 1 diabetes
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Discussion · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“20.3% of men with type 1 diabetes had low calculated free testosterone”
- Also stated in: § Prevalence of testosterone deficiency in men with type 1 diabetes · plain
“one in five men with type 1 diabetes had low cFT levels (20.3%, Fig. 1)”
- Also stated in: § Statistical analysis · plain
“Low cFT (Ͻ0.23 nmol/liter) (%) 20% 57% 60%”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Prevalence of testosterone deficiency in men with type 1 diabetes · plain
In the paper
“insulin resistance (as estimated by the HOMA-IR equation) (23) was independently associated with low TT levels (odds ratio ϭ 1.2; 95% CI ϭ 1.0 -1.4), after adjusting for age, BMI, treatment regimens, and other potentially confounding variables.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Testosterone indices and insulin resistance
What the sources say
- Not checked yetcites [23] Wallace, 2004, Use and abuse of HOMA modeling., Diabetes Care source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The inverse association between cFT levels and age (Fig. 2B) was significantly stronger that that observed for TT (P Ͻ 0.01)”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 2 diabetes
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIn the paper
“a prevalence significantly higher than normally observed in healthy men (21).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 1 diabetes
What the sources say
- Not checked yetcites [21] Sikaris, 2005, Reproductive hormone reference intervals for healthy fertile young men: evaluation of automated platform assays., J Clin Endocrinol Metab source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Serial measurements also revealed an inverse relationship between changes in testosterone levels and insulin resistance.”
- Also stated in: § Changes in testosterone levels over time · boosted
“we were able to demonstrate a significant inverse relationship between the change in TT level and the change in HOMA-IR during the same follow-up period (P ϭ 0.01).”
- Also stated in: § Changes in testosterone levels over time · plain
“the change in cFT was inversely correlated with the change in HOMA-IR during the same follow-up period (P ϭ 0.03).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Changes in testosterone levels over time · boosted
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“For every decade increase in age, the prevalence of low cFT levels effectively doubled [adjusted odds ratio ϭ 2.0; 95% confidence interval (CI) ϭ 1.4 -2.4].”
- Also stated in: § Prevalence of testosterone deficiency in men with type 2 diabetes · plain
“The prevalence of low cFT levels was 13% in men with type 2 diabetes younger than 40 yr, 19% in men aged 40 -49 yr, 45% in men 50 -59 yr old, 60% in men 60 -69 yr old, 67% in men 70 -79 yr old, and 76% in men with type 2 diabetes aged 80 yr or older.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 2 diabetes
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes- Also stated in: § Prevalence of testosterone deficiency in men with type 2 diabetes · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In this cohort, TT levels were inversely related to age (Fig. 2A).”
- Also stated in: § Discussion · plain
“age and BMI were major factors influencing both TT and cFT levels”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 2 diabetes
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes- Also stated in: § Discussion · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Low testosterone levels were independently associated with insulin resistance in men with type 1 diabetes as well as type 2 diabetes.”
- Also stated in: § Discussion · boosted
“we show that free testosterone levels were independently correlated with indices of insulin resistance in men with type 2 diabetes as well as those with type 1 diabetes.”
- Also stated in: § Discussion · plain
“Moreover, cFT levels, a SHBG-independent testosterone parameter, were still reduced in individuals with both type 2 and type 1 diabetes and independently associated with insulin resistance.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Discussion · boosted
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“similar to that observed in type 2 diabetes (age-body mass index adjusted odds ratio ϭ 1.4; 95% confidence interval ϭ 0.7-2.9).”
- Also stated in: § Prevalence of testosterone deficiency in men with type 1 diabetes · plain
“This frequency was statistically similar to that observed in age-and BMI-matched men with type 2 diabetes (adjusted odds ratio ϭ 1.4; 95% CI ϭ 0.7-2.9)”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Prevalence of testosterone deficiency in men with type 1 diabetes · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Forty-three percent of men with type 2 diabetes had a reduced total testosterone”
- Also stated in: § Prevalence of testosterone deficiency in men with type 2 diabetes · plain
“Forty-three percent of all men (n ϭ 249) with type 2 diabetes in our clinic had low TT levels (Ͻ10 nmol/liter)”
- Also stated in: § Discussion · plain
“43% of men with type 2 diabetes had low TT levels”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Prevalence of testosterone deficiency in men with type 2 diabetes · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Levels of SHBG were not associated with insulin resistance in men with type 2 diabetes after adjusting for age and BMI (P ϭ 0.281).”
- Also stated in: § Discussion · plain
“there was no independent association of SHBG levels with the HOMA index of insulin resistance in men with type 2 diabetes.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Testosterone indices and insulin resistance
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Discussion · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In addition, the change in TT level was also independently correlated with the change in HbA 1c during the same follow-up period (P ϭ 0.02).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, after adjusting for each subject's baseline parameters, age, and the time between clinic visits, we were able to demonstrate a significant inverse relationship between the change in TT level and the change in HOMA-IR during the same follow-up period (P ϭ 0.01).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“At the second analysis, there was also a good correlation between cFT levels obtained at the two time points (r 2 ϭ 0.57, Fig. 3C).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesNone of the sources cited for this claim have been checked yet.
In the paper
“In our cohort, age and BMI were major factors influencing both TT and cFT levels, consistent with reports from previous studies (2,7,25).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [2] Kapoor, 2007, Clinical and biochemical assessment of hypogonadism in men with type 2 diabetes: correlations with bioavailable testosterone and visceral adiposity., Diabetes Care source
- Not checked yetcites [7] Selvin, 2007, Androgens and diabetes in men: results from the Third National Health and Nutrition Examination Survey (NHANES III)., Diabetes Care source
- Not checked yetcites [25] Tsai, 2004, Association of bioavailable, free, and total testosterone with insulin resistance: influence of sex hormone-binding globulin and body fat., Diabetes Care source
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Insulin sensitivity was also independently associated with cFT levels in individuals with type 2 diabetes, such that that men with low cFT levels also tended to be more insulin resistant after adjusting for age, obesity, treatment regimens, and other potentially confounding variables (partial correlation coefficient ϭ Ϫ0.10; P ϭ 0.02).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Testosterone indices and insulin resistance
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“There was no signif-icant relationship between the change in cFT level during follow-up and the change in HbA 1c .”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“TT levels were also correlated with the HOMA-estimated insulin resistance within the normal range of both parameters after adjusting for age and obesity (partial correlation coefficient ϭ Ϫ0.13; P ϭ 0.002).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Testosterone indices and insulin resistance
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, the frequency of testosterone deficiency defined by low cFT levels (Ͻ0.230 nmol/liter, 48%) at the second time point was significantly lower than obtained at the first estimation (60% difference, P Ͻ 0.001).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIn the paper
“In men with type 1 diabetes, cFT levels were also independently associated with eGDR, a marker of insulin sensitivity in individuals with type 1 diabetes (24), after adjusting for age (P ϭ 0.04).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Testosterone indices and insulin resistance
What the sources say
- Not checked yetcites [24] Williams, 2000, Can clinical factors estimate insulin resistance in type 1 diabetes?, Diabetes source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Two thirds (66%) of patients with low testosterone levels at the first estimation continued to have low levels at the second reading.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Seventy-three percent of individuals with low TT level on the first estimation had low TT levels on repeat testing.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Nonetheless, after adjusting for each subject's baseline measurements, the change in cFT was inversely correlated with the change in HOMA-IR during the same follow-up period (P ϭ 0.03).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
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In the paper
“However, low SHBG levels were independently associated with poorer glycemic control (HbA 1c ) after adjustment for age and BMI (P ϭ 0.04).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Testosterone indices and insulin resistance
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“There was no statistically significant association between eGDR and TT or SHBG levels.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Testosterone indices and insulin resistance
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Testosterone levels are partly influenced by insulin resistance, which may represent an important avenue for intervention”
- Also stated in: § Discussion · hedged
“These findings support the hypothesis that circulating testosterone levels in men with diabetes may be influenced by insulin sensitivity, and vice versa.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Discussion · hedged
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Testosterone deficiency is common in men with diabetes, regardless of the type.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The cohort of men attending a single tertiary referral clinic is representative of men with diabetes generally.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The 4-fold higher prevalence of reduced TT levels observed in men with type 2 diabetes when compared with those with type 1 diabetes was largely driven by reduced levels of SHBG (Fig. 2C), which was present at all ages and across all levels of BMI.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIn the paper
“However, this study is the first to demonstrate a similar prevalence of low cFT levels in individuals with type 1 diabetes, in contrast to previous findings (16), despite otherwise similar demographic and biochemical patient characteristics.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [16] Tomar, 2006, Contrasting testosterone concentrations in type 1 and type 2 diabetes., Diabetes Care source
Load-bearingStrength:boosted· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIn the paper
“Findings from the cross-sectional component of our study are also limited because a single low testosterone level is inadequate for making the diagnosis of hypogonadism, given the variability in serum testosterone levels that can result from circadian rhythms, the pulsatile nature of its secretion, use of concomitant medications, and measurement variations (22).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [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
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesNone of the sources cited for this claim have been checked yet.
In the paper
“The cFT levels (20) correlate well with measurements of free testosterone as determined by the gold standard of equilibrium dialysis (22).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Quantification of testosterone levels
What the sources say
- Not checked yetcites [20] Vermeulen, 1999, A critical evaluation of simple methods for the estimation of free testosterone in serum., J Clin Endocrinol Metab source
- Not checked yetcites [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
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesNone of the sources cited for this claim have been checked yet.
In the paper
“Insulin is known to inhibit hepatic production of SHBG (31), and SHBG levels fall acutely during hyperglycemic-euglycemic clamp studies (32).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [31] Plymate, 1988, Inhibition of sex hormone-binding globulin production in the human hepatoma (Hep G2) cell line by insulin and prolactin., J Clin Endocrinol Metab source
- Not checked yetcites [32] Katsuki, 1996, Acute and chronic regulation of serum sex hormone-binding globulin levels by plasma insulin concentrations in male noninsulin-dependent diabetes mellitus patients., J Clin Endocrinol Metab
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This was partly explained by the association between SHBG and HbA 1c (P Ͻ 0.01).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesWhat the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The clinical characteristics of this subgroup were not significantly different from those of the total cohort of men with type 2 diabetes (Table 1).”
- Also stated in: § Changes in testosterone levels over time · plain
“The clinical characteristics of this subgroup in which testosterone levels were retested were not significantly different from those of the total cohort of men with type 2 diabetes (Table 1).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Follow-up estimation of testosterone levels
Strength:plain· not yet calibratedn = 262Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes- Also stated in: § Changes in testosterone levels over time · plain
In the paper
“This is consistent with reports in nondiabetic men, where as many as 30% of men will have normal levels when repeated (34).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [34] Swerdloff, 2000, Long-term pharmacokinetics of transdermal testosterone gel in hypogonadal men., J Clin Endocrinol Metab
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes
- It may state two separate claims as one. 6
- Probably not a substantial claim. 10
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“finding that 27 and 33% of individuals with low TT and cFT levels respectively had levels in the normal range when retested.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Abstract
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
- Also stated in: § Discussion · hedged
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“possibly because of the age-associated rise in SHBG (Fig. 2C).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Prevalence of testosterone deficiency in men with type 2 diabetes
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“None of these men received testosterone therapy.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Changes in testosterone levels over time
Strength:plain· not yet calibratedn = 262Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Interpretation of our study is therefore limited because we did not obtain a detailed record of symptomatology history.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“All men gave written informed consent, and the study was approved by the Human Research Ethics Committee, Research Ethics Unit, Austin Health.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Cross-sectional survey
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“However, testosterone may have deleterious actions on prostate disease, sleep apnea, and possibly cardiovascular risk (35).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [35] Rhoden, 2004, Risks of testosterone-replacement therapy and recommendations for monitoring., N Engl J Med source
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Consequently, the appropriate clinical response to this emerging problem remains to be determined.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
Strength:plain· not yet calibratedTests✓ Asserted: passes✗ Checkable: fails✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. It may be too vague to check against evidence. The paper’s conclusions may not depend on it.
In the paper
“previous studies have reported an association of loss of weight in obese insulinresistant men with increased testosterone levels (30).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [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
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Certainly, testosterone replacement can improve performance, mood, and libido in men with hypogonadism (22) and augments insulin sensitivity (11,15).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [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 yetcites [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 yetcites [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
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✗ Based: failsProbably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds. It may state two separate claims as one.
In the paper
“Indeed, reduced SHBG has been suggested as a surrogate marker for insulin resistance (33).”
§ Low Testosterone Levels Are Common and Associated with Insulin Resistance in Men with Diabetes > Discussion
What the sources say
- Not checked yetcites [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
Strength:hedged· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
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”
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?
The cited source says what the claim attributes to it.
In the citing paper
“In fact, multiple studies confirmed the association between low or inappropriate T levels in men and T2D and obesity [167–170].”
From Role of sex hormone-binding globulin in the free hormone hypothesis and the relevance of free testosterone in androgen physiology (2022) · cites this paper as [168]
In the citing paper
“A longitudinal study in 265 men with a baseline hemoglobin A1c of 7.6% reported an inverse relationship between changes in glycemic control and testosterone levels.”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [35]
In the citing paper
“In those whose glycemic control improved over time, testosterone increased, whereas in those whose control worsened, testosterone decreased (35).”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [35]
In the citing paper
“Approximately, 50% of older (age >40 years) male patients with type 2 diabetes mellitus (DM2) have decreased testosterone (T) levels”
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
MajorThe 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.
“higher hs-CRP levels (median 7.7 vs. 4.5, P Ͻ 0.01)”
“hs-CRP (IU/ml) 1.5 (0.2-11.5) 3.0 (0.2-192) 2.9 (0.2-58)”
Macrovascular disease prevalence differs from Table 1
MinorThe results describe macrovascular disease in one third of men with type 2 diabetes, but Table 1 reports 42% for that group.
“One third of men with type 2 diabetes had documented macrovascular disease”
“Macrovascular disease (%) 16% 42% 40%”
Citations
Cites
Use and Abuse of HOMA Modeling
Wallace, T. M., Levy, J. C., & Matthews, D. R. (2004) · Diabetes Care · doi:10.2337/diacare.27.6.1487 · Cited by 5,114
A Critical Evaluation of Simple Methods for the Estimation of Free Testosterone in Serum
Vermeulen, A., Verdonck, L., & Kaufman, J. M. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.10.6079 · Cited by 3,824
Hyperinsulinemia as an independent risk factor for ischemic heart disease
Després, J.-P., Lamarche, B., Mauriège, P., Cantin, B., Dagenais, G. R., Moorjani, S., & Lupien, P.-J. (1996) · New England Journal of Medicine · doi:10.1056/nejm199604113341504 · Cited by 1,699
Ding, E. L., Song, Y., Malik, V. S., & Liu, S. (2006) · JAMA · doi:10.1001/jama.295.11.1288 · Cited by 1,354
Bhasin, S., Cunningham, G. R., Hayes, F. J., Matsumoto, A. M., Snyder, P. J., Swerdloff, R. S., & Montori, V. M. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2847 · Cited by 965
Kapoor, D., Goodwin, E., Channer, K. S., & Jones, T. H. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02166 · Cited by 791
Risks of testosterone-replacement therapy and recommendations for monitoring.
Rhoden, E. L., & Morgentaler, A. (2004) · New England Journal of Medicine · doi:10.1056/nejmra022251 · Cited by 705
Androgens and Cardiovascular Disease
Liu, P. Y., Death, A. K., & Handelsman, D. J. (2003) · Endocrine Reviews · doi:10.1210/er.2003-0005 · Cited by 695
PLYMATE, S. R., MATEJ, L. A., JONES, R. E., & FRIEDL, K. E. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-67-3-460 · Cited by 693
Can clinical factors estimate insulin resistance in type 1 diabetes?
Williams, K. V., Erbey, J. R., Becker, D., Arslanian, S., & Orchard, T. J. (2000) · Diabetes · doi:10.2337/diabetes.49.4.626 · Cited by 640
Flagged first, then by citations
Cited by
Sorted by citations
Skakkebæk, N. E., Meyts, E. R., Louis, G. M. B., Toppari, J., Andersson, A., Eisenberg, M. L., Jensen, T. K., Jørgensen, N., Swan, S. H., Sapra, K. J., et al. (2015) · Physiological Reviews · doi:10.1152/physrev.00017.2015 · Cited by 1,030
Physical activity and exercise: Strategies to manage frailty
Angulo, J., El Assar, M., Álvarez-Bustos, A., & Rodríguez-Mañas, L. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101513 · Cited by 771
Cancer risk in diabetic patients treated with metformin: a systematic review and meta-analysis
Noto, H., Goto, A., Tsujimoto, T., & Noda, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033411 · Cited by 566
Klinefelter Syndrome—A Clinical Update
Groth, K. A., Skakkebaek, A. H., Høst, C., Gravholt, C. H., & Bojesen, A. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2382 · Cited by 513
Nehra, A. X., Jackson, G., Miner, M. M., Billups, K. L., Burnett, A. L. “., Buvat, J., Carson, C. C., Cunningham, G. R., Ganz, P., Goldstein, I., et al. (2012) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2012.06.015 · Cited by 475
Metadata
- 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
- 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
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
A language model drew the claims from the paper on 2026-10-10, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-10 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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