Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes
Open accessAbstract
OBJECTIVE—The aim of our study was to assess the prevalence of clinical hypogonadism, based on both symptoms and biochemical available measures of testosterone deficiency, in men with type 2 diabetes. RESEARCH DESIGN AND METHODS—In a cross-sectional study of 355 type 2 diabetic men aged >30 years, total and bioavailable testosterone, sex hormone–binding globulin, BMI, and waist circumference were measured and free testosterone was calculated. Overt hypogonadism was defined as the presence of clinical symptoms of hypogonadism and low testosterone level (total testosterone <8 nmol/l and/or bioavailable testosterone <2.5 nmol/l). Borderline hypogonadism was defined as the presence of symptoms and total testosterone of 8–12 nmol/l or bioavailable testosterone of 2.5–4 nmol/l. RESULTS—A low blood testosterone level was common in diabetic men, and a significant proportion of these men had symptoms of hypogonadism. Overt hypogonadism was seen in 17% of men with total testosterone <8 nmol/l and 14% with bioavailable testosterone <2.5 nmol/l. Borderline hypogonadism was found in 25% of men with total testosterone 8–12 nmol/l and bioavailable testosterone between 2.5 and 4 nmol/l; 42% of the men had free testosterone <0.255 nmol/l. BMI and waist circumference were both significantly negatively correlated with testosterone levels in men, with the association being stronger for waist circumference. CONCLUSIONS—Testosterone levels are frequently low in men with type 2 diabetes, and the majority of these men have symptoms of hypogonadism. Obesity is associated with low testosterone levels in diabetic men.
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Written from the paper’s full text.
TL;DR
In a cross-sectional study of 355 men with type 2 diabetes, low testosterone levels were common and frequently accompanied by hypogonadal symptoms, with overt hypogonadism in 17% by total testosterone and 14% by bioavailable testosterone. Testosterone levels were inversely associated with BMI and waist circumference, with the association stronger for waist circumference.
Key findings
- Low testosterone was common: 20% (71 men) had total testosterone <8 nmol/l, 31% (109) had total testosterone 8–12 nmol/l, 16% (58) had bioavailable testosterone <2.5 nmol/l, 36% (126) had bioavailable testosterone 2.5–4 nmol/l, and 50% (179) had free testosterone <0.255 nmol/l.
- Symptomatic hypogonadism was frequent: overt hypogonadism was found in 17% (61) with total testosterone <8 nmol/l and 14% (51) with bioavailable testosterone <2.5 nmol/l; borderline/possible hypogonadism was found in 25% (89) with total testosterone 8–12 nmol/l and 29% (104) with bioavailable testosterone 2.5–4 nmol/l; 42% (149) had free testosterone <0.255 nmol/l.
- Testosterone correlated negatively with adiposity: total testosterone with BMI (r = −0.247; P < 0.001) and waist circumference (r = −0.275; P < 0.001); bioavailable testosterone correlated more strongly with waist circumference (r = −0.210; P < 0.001) than BMI (r = −0.148; P = 0.006).
- Erectile dysfunction was the most common symptom, occurring in >70% of diabetic men with low testosterone; men with erectile dysfunction had lower bioavailable testosterone (3.92 ± 0.09 vs. 4.25 ± 0.13 nmol/l, P = 0.04) and free testosterone (0.265 ± 0.01 vs. 0.295 ± 0.01 nmol/l, P = 0.006), with no significant total testosterone difference (P = 0.1).
Methods
- Cross-sectional study of 355 type 2 diabetic men aged >30 years registered at the Centre for Diabetes and Endocrinology, Barnsley Hospital NHS Foundation Trust, U.K.; 70 were treated with diet alone, 95 with insulin, and 160 with oral hypoglycemic agents (Table 1 reports 190 oral hypoglycemics).
- Assessments included total testosterone, SHBG, bioavailable testosterone, calculated free testosterone, BMI, waist circumference, blood pressure, A1C, and the Androgen Deficiency in the Aging Male (ADAM) questionnaire; hypogonadism definitions combined symptoms with total testosterone <8 nmol/l or bioavailable testosterone <2.5 nmol/l for overt, and total testosterone 8–12 nmol/l or bioavailable testosterone 2.5–4 nmol/l for borderline.
- Analysis used SPSS with linear regression/correlation, chi-square tests, and Mann-Whitney U tests; significance set at P < 0.05.
Limitations
- The paper states that the ADAM questionnaire lacks specificity and is useful only in the presence of a low testosterone level; it also states there is no widely accepted consensus on the testosterone threshold for treatment and that diagnosis is difficult because symptoms are nonspecific, especially in diabetic men.
- The paper states that larger studies are required to establish the benefit of testosterone replacement therapy on quality of life and the diabetic state.
- Evident from the text: the cross-sectional design cannot establish causality between low testosterone and visceral adiposity or diabetes, and the study lacks an internal nondiabetic control group, relying on comparisons with other published cohorts.
Model-written summary. Check it against the paper before relying on it.
Integrity signals
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Cites
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Claims the paper makes
0 of 38 cited sources checked · 0 supported · 0 flagged
- Findingown data
Overt hypogonadism, defined as symptoms plus bioavailable testosterone <2.5 nmol/l, was present in 14% of type 2 diabetic men.
“14% with bioavailable testosterone Ͻ2.5 nmol/l”
- Also stated in: § Prevalence of symptoms and low testosterone levels (hypogonadism) · plain
“14% (51 men) had overt hypogonadism with bioavailable testosterone Ͻ2.5 nmol/l”
Quote in the paperSubstantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Also stated in: § Prevalence of symptoms and low testosterone levels (hypogonadism) · plain
- Findingown data
42% of type 2 diabetic men had free testosterone <0.255 nmol/l.
“42% of the men had free testosterone Ͻ0.255 nmol/l”
- Also stated in: § Prevalence of symptoms and low testosterone levels (hypogonadism) · plain
“42% (149 patients) had free testosterone Ͻ0.255 nmol/l”
Quote in the paperNot a substantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Also stated in: § Prevalence of symptoms and low testosterone levels (hypogonadism) · plain
- Findingown data
SHBG significantly negatively correlated with BMI (r=-0.309; P<0.001).
“SHBG also significantly correlated with both BMI (r ϭ Ϫ0.309; P Ͻ 0.001) and waist circumference (r ϭ Ϫ0.277; P Ͻ 0.001).”
Quote in the paperSubstantial claim - Findingown data
When both waist circumference and A1C were compared against total testosterone, only waist circumference was a significant predictor (P<0.001).
“Similarly, only waist circumference was a significant predictor of total testosterone (P Ͻ 0.001) when both waist circumference and A1C were compared against total testosterone.”
Quote in the paperSubstantial claim - Findingown data
Using criteria from the Baltimore longitudinal study, the prevalence of hypogonadism in diabetic men was higher across all age groups (42, 44, 39, and 56% in age groups 40-49, 50-59, 60-69, and 70-79 years, respectively).
“Using the cri-teria in that study, we found a higher prevalence of hypogonadism across all age-groups (42, 44, 39, and 56% in the age-groups 40 -49, 50 -59, 60 -69, and 70 -79 years, respectively).”
Quote in the paperSubstantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Findingown data
There was no significant association between history of smoking and bioavailable or total testosterone levels.
“There was no significant association between history of smoking and bioavailable or total testosterone levels (Table 3).”
Quote in the paperNot a substantial claim - Findingown data
Men with ED had significantly lower bioavailable testosterone than men without ED (3.92 ± 0.09 vs 4.25 ± 0.13 nmol/l, P=0.04).
“men with ED had significantly lower bioavailable and free testosterone levels than those without ED (bioavailable testosterone 3.92 Ϯ 0.09 vs. 4.25 Ϯ 0.13 nmol/l, P ϭ 0.04; free testosterone 0.265 Ϯ 0.01 vs. 0.295 Ϯ 0.01 nmol/l, P ϭ 0.006).”
Quote in the paperSubstantial claim - Findingown data
There was no significant association between testosterone levels and history of hypertension.
“There was no significant association between testosterone levels and history of hypertension (Table 3).”
Quote in the paperNot a substantial claim - Findingnone given
Frequencies of hypogonadal symptoms were similar in all defined groups of low testosterone.
“The frequencies of hypogonadal symptoms were similar in all defined groups of low testosterone.”
Quote in the paperNot a substantial claim - Findingown data
Total and bioavailable testosterone levels were significantly lower in men with BMI >30 kg/m2.
“Total and bioavailable testosterone levels were significantly lower in men with BMI Ͼ30 kg/m 2 or waist circumference Ͼ94 cm (Table 3).”
Quote in the paperSubstantial claim - Findingown data
31% of type 2 diabetic men had total testosterone between 8 and 12 nmol/l.
“31% (109 men) had total testosterone between 8 and 12 nmol/l”
Quote in the paperNot a substantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Findingown data
Total and bioavailable testosterone levels were significantly lower in men with waist circumference >94 cm.
“Total and bioavailable testosterone levels were significantly lower in men with BMI Ͼ30 kg/m 2 or waist circumference Ͼ94 cm (Table 3).”
Quote in the paperSubstantial claim - Findingown data
Low blood testosterone levels are common in men with type 2 diabetes.
“A low blood testosterone level was common in diabetic men”
- Also stated in: § Abstract · plain
“Testosterone levels are frequently low in men with type 2 diabetes”
Quote in the paperSubstantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Also stated in: § Abstract · plain
- Findingown data
There was no significant correlation between A1C and SHBG (P=0.16).
“or between A1C and SHBG (P ϭ 0.16).”
Quote in the paperNot a substantial claim - Findingown data
Borderline/possible hypogonadism, defined as symptoms plus total testosterone 8-12 nmol/l, was present in 25% of type 2 diabetic men.
“Borderline hypogonadism was found in 25% of men with total testosterone 8 -12 nmol/l”
- Also stated in: § Prevalence of symptoms and low testosterone levels (hypogonadism) · plain
“25% (89 men) had possible hypogonadism with total testosterone between 8 and 12 nmol/l”
Quote in the paperNot a substantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Also stated in: § Prevalence of symptoms and low testosterone levels (hypogonadism) · plain
- Findingown data
Primary hypogonadism (FSH or LH >10 IU/l) was seen in 26% of hypogonadal men.
“Primary hypogonadism (FSH or LH Ͼ10 IU/l) was seen in 26%”
Quote in the paperNot a substantial claim - Findingown data
50% of type 2 diabetic men had free testosterone <0.255 nmol/l.
“50% (179 men) had free testosterone Ͻ0.255 nmol/l”
Quote in the paperNot a substantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Findingown data
Possible hypogonadism, defined as symptoms plus bioavailable testosterone 2.5-4 nmol/l, was present in 29% of type 2 diabetic men.
“29% (104 men) had possible hypogonadism with bioavailable testosterone between 2.5 and 4 nmol/l”
Quote in the paperNot a substantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Findingown data
There is a strong association between bioavailable and free testosterone (r=0.821; P<0.001).
“There was a strong association between bioavailable and free testosterone (r ϭ 0.821; P Ͻ 0.001).”
Quote in the paperNot a substantial claim - Findingown data
SHBG significantly negatively correlated with waist circumference (r=-0.277; P<0.001).
“SHBG also significantly correlated with both BMI (r ϭ Ϫ0.309; P Ͻ 0.001) and waist circumference (r ϭ Ϫ0.277; P Ͻ 0.001).”
Quote in the paperSubstantial claim - Findingown data
20% of type 2 diabetic men had total testosterone <8 nmol/l.
“20% (71 men) had total testosterone Ͻ8 nmol/l”
Quote in the paperNot a substantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Findingown data
Approximately one-third of hypogonadal men had either primary or secondary hypogonadism.
“In our study, approximately onethird of the hypogonadal men had either primary or secondary hypogonadism.”
Quote in the paperNot a substantial claim - Findingown data
Among men with ED and hypogonadism, 23% had other symptoms of hypogonadism.
“and 23% had other symptoms of hypogonadism”
Quote in the paperNot a substantial claim - Findingown data
There were no significant differences in total testosterone levels between men with and without ED (12.5 ± 0.09 vs 12.7 ± 0.08 nmol/l, P=0.1).
“There were no significant differences in total testosterone levels in men with and without ED (total testosterone 12.5 Ϯ 0.09 vs. 12.7 Ϯ 0.08 nmol/l, P ϭ 0.1).”
Quote in the paperSubstantial claim - Findingown data
Secondary hypogonadism (FSH or LH <2 IU/l) was seen in 7% of hypogonadal men.
“and 7% had secondary hypogonadism (FSH or LH Ͻ2 IU/l”
Quote in the paperNot a substantial claim - Findingown data
16% of type 2 diabetic men had bioavailable testosterone <2.5 nmol/l.
“16% (58 men) had bioavailable testosterone Ͻ2.5 nmol/l”
Quote in the paperNot a substantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Findingown data
ED was the most common symptom, occurring in >70% of diabetic men with low testosterone levels.
“ED was the most common symptom occurring in Ͼ70% of the diabetic men with low testosterone levels (Table 2).”
Quote in the paperNot a substantial claim - Findingown data
36% of type 2 diabetic men had bioavailable testosterone between 2.5 and 4 nmol/l.
“36% (126 patients) had bioavailable testosterone between 2.5 and 4 nmol/l”
Quote in the paperNot a substantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Findingown data
There was no significant correlation between A1C and bioavailable or free testosterone (P=0.13).
“There was no significant correlation between A1C and bioavailable or free testosterone (P ϭ 0.13)”
Quote in the paperNot a substantial claim - Findingown data
A1C was associated with waist circumference (r=0.053; P=0.007).
“A1C was also associated with waist circumference (r ϭ 0.053; P ϭ 0.007)”
Quote in the paperNot a substantial claim - Findingown data
A1C was associated with BMI (r=0.126; P=0.018).
“and BMI (r ϭ 0.126; P ϭ 0.018).”
Quote in the paperNot a substantial claim - Findingown data
Among men with ED and hypogonadism, 63% had reduced libido.
“Of the men with ED and hypogonadism (total testosterone Ͻ12 nmol/l or bioavailable testosterone Ͻ4 nmol/l or free testosterone Ͻ0.255 nmol/l), 63% had reduced libido”
Quote in the paperNot a substantial claim - Findingown data
Total testosterone was significantly lower in men with A1C >6.5%.
“Total testosterone was significantly lower in men with A1C Ͼ6.5% (Table 3).”
Quote in the paperNot a substantial claim - Findingown data
Total testosterone was significantly associated with A1C (r=-0.16; P=0.04).
“Total testosterone was significantly associated with A1C (r ϭ Ϫ0.16; P ϭ 0.04).”
Quote in the paperNot a substantial claim - Findingown data
Obesity is associated with low testosterone levels in diabetic men.
“Obesity is associated with low testosterone levels in diabetic men.”
- Also stated in: § A1C, blood pressure, smoking, and testosterone levels · plain
“Our data also showed that obesity and visceral adiposity, as assessed by both BMI and waist circumference, were negatively associated with low levels of testosterone.”
Quote in the paperSubstantial claim- Rests on an assumption: BMI and waist circumference adequately assess visceral adiposity.
- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Also stated in: § A1C, blood pressure, smoking, and testosterone levels · plain
- Findingown data
Among hypogonadal men, 14% had ED without any other associated symptom.
“Only 14% of the hypogonadal men had ED without any other associated symptom.”
Quote in the paperNot a substantial claim - Findingown data
67% of hypogonadal men had normal levels of gonadotrophins.
“67% had hypogonadism with normal levels of gonadotrophins.”
Quote in the paperNot a substantial claim - Findingown data
The majority of men with type 2 diabetes and low testosterone have symptoms of hypogonadism.
“the majority of these men have symptoms of hypogonadism”
- Also stated in: § A1C, blood pressure, smoking, and testosterone levels · boosted
“This study has demonstrated that there is a high prevalence of symptomatic hypogonadism in men with type 2 diabetes.”
Quote in the paperSubstantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Also stated in: § A1C, blood pressure, smoking, and testosterone levels · boosted
- Findingown data
Men with ED had significantly lower free testosterone than men without ED (0.265 ± 0.01 vs 0.295 ± 0.01 nmol/l, P=0.006).
“men with ED had significantly lower bioavailable and free testosterone levels than those without ED (bioavailable testosterone 3.92 Ϯ 0.09 vs. 4.25 Ϯ 0.13 nmol/l, P ϭ 0.04; free testosterone 0.265 Ϯ 0.01 vs. 0.295 Ϯ 0.01 nmol/l, P ϭ 0.006).”
Quote in the paperSubstantial claim - Findingcitation
Mean total and bioavailable testosterone levels in diabetic men were lower in all age groups compared with data reported by Leifke et al. in healthy nonobese males and by Muller et al. in independently living men.
“The mean total and bioavailable testosterone levels in our diabetic men were also lower in all age-groups compared with data reported by Leifke et al. (11) in healthy nonobese males and by Muller et al. (33) in independently living men.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [11] Leifke E, Gorenoi V, Wichers C, Muhlen A, Buren E, Brabant G: Age-related changes of serum sex hormones, insulin-like growth factor-1 and sex-hormone binding globulin levels in men: cross-sectional data from a healthy male cohort. Clin Endocrinol (Oxf) 53:689–695, 2000 source
Not checked in the free run.
- cites [33] Muller M, Tonkelaar ID, Thijssen JHH, Grobbeee DE, Schouw YT: Endogenous sex hormones in men aged 40–80 years. Eur J Endocrinol 149:583–589, 2003 source
Not checked in the free run.
- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Findingown data
Overt hypogonadism, defined as symptoms plus total testosterone <8 nmol/l, was present in 17% of type 2 diabetic men.
“Overt hypogonadism was seen in 17% of men with total testosterone Ͻ8 nmol/l”
- Also stated in: § Prevalence of symptoms and low testosterone levels (hypogonadism) · plain
“17% (61 subjects) had overt hypogonadism with total testosterone Ͻ8 nmol/l”
- Also stated in: § A1C, blood pressure, smoking, and testosterone levels · plain
“17% of the diabetic men had overt hypogonadism with total testosterone Ͻ8 nmol/l”
Quote in the paperSubstantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Also stated in: § Prevalence of symptoms and low testosterone levels (hypogonadism) · plain
- Findingown data
A high proportion of diabetic men have low levels of bioavailable and free testosterone.
“In our study, we found that a high proportion of diabetic men have low levels of bioavailable and free testosterone.”
Quote in the paperSubstantial claim- Rests on an assumption: The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
- Interpretationown data
Low testosterone levels cannot be explained solely by the lower levels of SHBG associated with insulin resistance.
“the finding of a similar prevalence of hypogonadism using bioavailable testosterone and the wide range of SHBG levels (5.14 -129 nmol/l) suggests that this is not the case.”
Quote in the paperSubstantial claim - Premisecitation
An inverse relationship exists between testosterone levels and insulin concentrations in healthy men.
“An inverse relationship ex-ists between testosterone levels and insulin concentrations in healthy men (2).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [2] Simon D, Preziosi P, Barrett-Connor E, Roger M, Saint-Paul M, Nahoul K, Papoz L: Interrelation between plasma testosterone and plasma insulin in healthy adult men: the Telecom Study. Diabetologia 35:173–177, 1992 source
Not checked in the free run.
- Interpretationreasoning
The diagnosis of hypogonadism is difficult because symptoms are nonspecific, especially in diabetic men.
“It also illustrates that the diagnosis of hypogonadism is difficult in that the symptoms are nonspecific, especially in diabetic men.”
Quote in the paperSubstantial claim - Premisecitation
Low testosterone levels in men are associated with reduced insulin sensitivity and type 2 diabetes.
“It is being increasingly recognized that low testosterone levels in men are associated with reduced insulin sensitivity and type 2 diabetes (1).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [1] Kapoor D, Malkin CJ, Channer KS, Jones TH: Androgens, insulin resistance and vascular disease in men. Clin Endocrinol (Oxf ) 63: 239–250, 2005 source
Not checked in the free run.
- Premisecitation
A recent study demonstrated that free testosterone levels, which are independent of SHBG, are low in one-third of diabetic men.
“A recent study has demonstrated that free testosterone levels, which are independent of SHBG, are low in one-third of diabetic men (9).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [9] Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P: Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 89:5462–5468, 2004 source
Not checked in the free run.
- Premisecitation
Dhindsa et al. demonstrated that 33% of men with type 2 diabetes had significantly lower levels of free testosterone measured by equilibrium dialysis.
“Importantly, Dhindsa et al. (9) demonstrated that 33% of men with type 2 diabetes had significantly lower levels of free testosterone measured by equilibrium dialysis, which is the widely accepted most clinically relevant assay for free testosterone.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [9] Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P: Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 89:5462–5468, 2004 source
Not checked in the free run.
- Premisecitation
Most studies in diabetic men have defined hypogonadism solely on the basis of testosterone levels.
“Most of the studies in diabetic men have defined hypogonadism solely on the basis of testosterone levels (9).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [9] Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P: Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 89:5462–5468, 2004 source
Not checked in the free run.
- Premisecitation
Testosterone levels are lower in diabetic men compared with nondiabetic subjects.
“Furthermore, it has been reported that testosterone levels are lower in diabetic men compared with nondiabetic subjects (6 -9).”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [6] Barrett-Connor E, Khaw KT, Yen SS: Endogenous sex hormone levels in older men with diabetes mellitus. Am J Epidemiol 132:895–901, 1990 source
Not checked in the free run.
- cites [7] Barrett-Connor E: Lower endogenous androgen levels and dyslipidemia in men with non insulin-dependent diabetes mellitus. Ann Intern Med 117:807–811, 1992 source
Not checked in the free run.
- cites [8] Andersson B, Marin P, Lissner L, Vermeulen A, Bjorntorp P: Testosterone concentrations in women and men with NIDDM. Diabetes Care 17:405–411, 1994 source
Not checked in the free run.
- cites [9] Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P: Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 89:5462–5468, 2004 source
Not checked in the free run.
- Premisecitation
Testosterone replacement therapy in two studies converted sildenafil nonresponders to responders.
“Testosterone replacement therapy in two studies was found to convert sildenafil nonresponders to responders (18,19).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [18] Shabsigh R, Kaufman J, Steidle J, Padma-Nathan H: Randomized study of testosterone gel as adjunctive therapy to sildenafil in hypogonadal men with erectile dysfunction who do not respond to sildenafil alone. J Urol 172:658–663, 2004 source
Not checked in the free run.
- cites [19] Aversa A, Isidori AM, Spera G, Lenzi A, Fabbri A: Androgens improve cavernous vasodilation and response to sildenafil in patients with erectile dysfunction. Clin Endocrinol (Oxf ) 58:632–638, 2003 source
Not checked in the free run.
- Premisecitation
Men with ED who fail to respond to phosphodiesterase inhibitors have low testosterone levels.
“Men with ED who fail to respond to phosphodiesterase inhibitors have been shown to have low testosterone levels (17).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [17] Kalinchenko SY, Kozlov GI, Gontcharov NP, Katsiya GV: Oral testosterone undecanoate reverses erectile dysfunction associated with diabetes mellitus in patients failing on sildenafil citrate therapy alone. Aging Male 6:94–99, 2003 source
Not checked in the free run.
- Premisecitation
Two studies in type 2 diabetic men have shown an improvement in glycemic control with testosterone replacement therapy.
“Two studies in type 2 diabetic men have shown an improvement in glycemic control (26,27) with testosterone replacement therapy”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [26] Kapoor D, Goodwin E, Channer KS, Jones TH: Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholesterolaemia in hypogonadal men with type 2 diabetes. Eur J Endocrinol 154:899–906, 2006 source
Not checked in the free run.
- cites [27] Boyanov MA, Boneva Z, Christov VG: Testosterone supplementation in men with type 2 diabetes, visceral obesity and partial androgen deficiency. Aging Male 6:1–7, 2003 source
Not checked in the free run.
- May combine two claims. 12
- The quote only partly states this claim. 1
- Classified as probably not a substantial claim. 8
May combine two claims.
Findingown dataBMI and waist circumference are both significantly negatively correlated with testosterone levels in men with type 2 diabetes.
“BMI and waist circumference were both significantly negatively correlated with testosterone levels in men”
- Also stated in: § Sex hormones and body composition · plain
“Total testosterone significantly and negatively correlated with both BMI (r ϭ Ϫ0.247; P Ͻ 0.001) and waist circumference (r ϭ Ϫ0.275; P Ͻ 0.001).”
Quote in the paperSubstantial claim- Also stated in: § Sex hormones and body composition · plain
The quote only partly states this claim.
Findingown dataThe negative association between testosterone and waist circumference is stronger than that with BMI.
“with the association being stronger for waist circumference”
- Also stated in: § Sex hormones and body composition · plain
“Bioavailable testosterone correlated more strongly with waist circumference (r ϭ Ϫ0.210; P Ͻ 0.001) than with BMI (r ϭ Ϫ0.148; P ϭ 0.006).”
Quote in the paperNot a substantial claim- Also stated in: § Sex hormones and body composition · plain
May combine two claims.
Findingown dataWhen both A1C and BMI were adjusted for in regression analysis, BMI (P<0.001) and not A1C (P=0.153) was a significant predictor of total testosterone.
“However, when both A1C and BMI were adjusted for in regression analysis, BMI (P Ͻ 0.001) and not A1C (P ϭ 0.153) was a significant predictor of total testosterone.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataBioavailable testosterone measurement is an important adjunct to the assessment of borderline hypogonadism in diabetes, removing the confounding effect of variable SHBG levels.
“The data presented here also show that bioavailable testosterone measurement is an important adjunct to the assessment of borderline hypogonadism in diabetes, removing the confounding effect of variable SHBG levels.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationLow testosterone levels predict insulin resistance and the future development of type 2 diabetes.
“Low testosterone levels have also been found to predict insulin resistance and the future development of type 2 diabetes (3-5).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [3] Oh JY, Barrett-Connor E, Wedick NM, Wingard DL: Endogenous sex hormones and the development of type 2 diabetes in older men and women. Diabetes Care 25:55–60, 2002 source
Not checked in the free run.
- cites [4] Stellato RK, Feldman HA, Hamdy O, Horton ES, McKinlay JB: Testosterone, sex hormone binding globulin and the development of type 2 diabetes in middle aged men. Diabetes Care 23:490–494, 2000 source
Not checked in the free run.
- cites [5] Haffner SM, Shaten J, Stern MP, Smith GD, Kuller L: Low levels of sex hormone binding globulin and testosterone predict the development of non insulin dependent diabetes mellitus in men. Am J Epidemiol 143:889–897, 1996 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSerum testosterone levels have been reported to be lower in men with hypertension.
“Serum testosterone levels have been reported to be lower in men with hypertension (40).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [40] Phillips GB, Jing TY, Resnick LM, Barbagallo M, Laragh JH, Sealey JE: Sex hormones and hemostatic risk factors for coronary heart disease in men with hypertension. J Hypertens 11:699–702, 1993 source
Not checked in the free run.
May combine two claims.
PremisecitationTestosterone improves cardiac ischemia in men with chronic stable angina and symptoms in men with heart failure.
“These findings and the fact that testosterone improves cardiac ischemia in men with chronic sta-ble angina (43) and symptoms in men with heart failure (44) suggest that the diagnosis of hypogonadism in men with type 2 diabetes has important clinical consequences besides the benefits on libido and well-being associated with normalization of testosterone status.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [43] English KM, Steeds RP, Jones TH, Diver MJ, Channer KS: Low dose transdermal testosterone therapy improves angina threshold in men with chronic stable angina. Circulation 102:1906–1911, 2000 source
Not checked in the free run.
- cites [44] Malkin CJ, Pugh PJ, West JN, van Beek EJR, Jones TH, Channer KS: Testosterone therapy in men with moderate severity heart failure: a randomised double blind placebo controlled trial. Eur Heart J 27:57–64, 2006 source
Not checked in the free run.
Classified as probably not a substantial claim.
PremisecitationHypogonadism is a clinical condition comprising both symptoms and biochemical evidence of testosterone deficiency.
“Hypogonadism is a clinical condition comprising both symptoms and biochemical evidence of testosterone deficiency (10).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [10] Nieschlag E, Behre HM, Bouchard P, Corrales JJ, Jones TH, Stalla GK, Webb SM, Wu FCW: Testosterone replacement therapy: current trends and future directions. Hum Reprod Update 5:409–411, 2004 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationCorrales et al. reported a neutral effect of intramuscular testosterone treatment on glycemic control in a small study of 10 men.
“although in a small study of 10 men, Corrales et al. (28) reported a neutral effect using intramuscular testosterone treatment.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [28] Corrales JJ, Burgo RM, Garca-Berrocal B, Almeida M, Alberca I, Gonzalez-Buitrago JM, Orfa A, Miralles JM: Partial androgen deficiency in aging type 2 diabetic men and its relationship to glycemic control. Metabolism 53:666–672, 2004 source
Not checked in the free run.
May combine two claims.
PremisecitationTestosterone treatment reduces insulin resistance in obese men, men with heart failure, and type 2 diabetic subjects.
“Testosterone treatment has also been shown to reduce insulin resistance in obese men (23,24), men with heart failure (25), and type 2 diabetic subjects (26).”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [23] Marin P, Holmang S, Jonsson L, Sjostrom L, Kvist H, Holm G, Lindstedt G, Bjorntorp P: The effects of testosterone treatment on body composition and metabolism in middle-aged obese men. Int J Obes Relat Metab Disord 16:991–997, 1992
Not checked in the free run.
- cites [24] Marin P, Krotkiewski M, Bjorntorp P: Androgen treatment of middle-aged, obese men: effects on metabolism, muscle and adipose tissues. Eur J Med 1:329–336, 1992
Not checked in the free run.
- cites [25] Malkin CJ, Jones TH, Channer KS: The effect of testosterone on insulin sensitivity in men with heart failure. Eur J Heart Fail 9:40–50, 2007 source
Not checked in the free run.
- cites [26] Kapoor D, Goodwin E, Channer KS, Jones TH: Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholesterolaemia in hypogonadal men with type 2 diabetes. Eur J Endocrinol 154:899–906, 2006 source
Not checked in the free run.
Classified as probably not a substantial claim.
PremisecitationA free testosterone level <0.255 nmol/l was taken as low.
“A free testosterone level Ͻ0.255 nmol/l was taken as low (31).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [31] Morales A, Lunenfeld B: Investigation, treatment and monitoring of late-onset hypogonadism in males: Official Recommendations of ISSAM. Aging Male 5:74–86, 2002 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationThe ADAM questionnaire has 88% sensitivity and 60% specificity and should only be used in the presence of a low testosterone level.
“This questionnaire has 88% sensitivity and 60% specificity and should only be used in the presence of a low testosterone level.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [14] Morley JE, Charlton E, Patrick P, Kaiser FE, Cadeau P, McCready D, Perry HM 3rd: Validation of a screening questionnaire for androgen deficiency in aging males. Metabolism 49:1239–1242, 2000 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationNo significant differences have been reported in bioavailable testosterone levels between smokers and nonsmokers.
“However, no significant differences have been reported in bioavailable testosterone levels between smokers and nonsmokers (42).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [42] English KM, Pugh P, Parry H, Scutt N, Channer KS, Jones TH: Effect of cigarette smoking on levels of bioavailable testosterone in healthy men. Clin Sci 100:661–665, 2001 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenAssessments were always made between 8:00 and 10:00 A.M.
“Assessments were always made between 8:00 and 10:00 A.M.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationSHBG rises with age, and thus free testosterone decreases more rapidly than total testosterone in older men.
“A confounding factor is that SHBG rises with age, and thus free testosterone decreases more rapidly than total testosterone in older men (11).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [11] Leifke E, Gorenoi V, Wichers C, Muhlen A, Buren E, Brabant G: Age-related changes of serum sex hormones, insulin-like growth factor-1 and sex-hormone binding globulin levels in men: cross-sectional data from a healthy male cohort. Clin Endocrinol (Oxf) 53:689–695, 2000 source
Not checked in the free run.
May combine two claims.
PremisecitationTestosterone replacement therapy improves insulin resistance, glycemic control, cholesterol levels, and waist circumference in diabetic men with low testosterone levels.
“Furthermore, there is recent evidence that testosterone replacement therapy improves insulin resistance, glycemic control, cholesterol levels, and waist circumference in diabetic men with low testosterone levels (26).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [26] Kapoor D, Goodwin E, Channer KS, Jones TH: Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholesterolaemia in hypogonadal men with type 2 diabetes. Eur J Endocrinol 154:899–906, 2006 source
Not checked in the free run.
May combine two claims.
PremisecitationIn our laboratory, bioavailable testosterone below the normal range (<2.5 nmol/l) is consistent with overt hypogonadism in young healthy men, whereas a significant proportion of patients with bioavailable testosterone between 2.5 and 4 nmol/l are also hypogonadal as shown by Leifke et al.
“In our laboratory, bioavailable testosterone below the normal range (Ͻ2.5 nmol/l) is consistent with overt hypogonadism in young healthy men, whereas a significant proportion of patients with bioavailable testosterone between 2.5 and 4 nmol/l are also hypogonadal as shown in the study by Leifke et al. (11).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [11] Leifke E, Gorenoi V, Wichers C, Muhlen A, Buren E, Brabant G: Age-related changes of serum sex hormones, insulin-like growth factor-1 and sex-hormone binding globulin levels in men: cross-sectional data from a healthy male cohort. Clin Endocrinol (Oxf) 53:689–695, 2000 source
Not checked in the free run.
May combine two claims.
PremisecitationStudies have shown that free testosterone levels are low in obese men and inversely correlate with the degree of obesity.
“Studies have shown that free testosterone levels are low in obese men and inversely correlate with the degree of obesity (20,21).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [20] Zumoff B, Strain GW, Miller LK, Rosner W, Senie R, Seres DS, Rosenfeld RS: Plasma free and non sex-hormone-binding-globulin-bound testosterone are decreased in obese men in proportion to their degree of obesity. J Clin Endocrinol Metab 71:929–931, 1990 source
Not checked in the free run.
- cites [21] Haffner SM, Valdez RA, Stern MP, Katz MS: Obesity, body fat distribution and sex hormones in men. Int J Obes 17:643–649, 1993
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationVarious studies have shown significantly increased, decreased, and unchanged levels of total testosterone in male smokers.
“Various studies have shown significantly increased, decreased, and unchanged levels of total testosterone in male smokers (41).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [41] Kapoor D, Jones TH: Smoking and hormones in health and endocrine disorders. Eur J Endocrinol 152:491–499, 2005 source
Not checked in the free run.
May combine two claims.
PremisecitationThere is increased deposition of abdominal adipose tissue in hypogonadal subjects, which leads to a further decrease in testosterone concentrations through conversion to estradiol by aromatase.
“There is increased deposition of abdominal adipose tissue in hypogonadal subjects, which in turn leads to a further decrease in testosterone concentrations, through conversion to estradiol by aromatase.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [1] Kapoor D, Malkin CJ, Channer KS, Jones TH: Androgens, insulin resistance and vascular disease in men. Clin Endocrinol (Oxf ) 63: 239–250, 2005 source
Not checked in the free run.
The paper relies on this without support.
No prior study has compared symptoms of hypogonadism with biochemical testosterone deficiency in diabetic men.
“In no study have symptoms of hypogonadism been compared with biochemical testosterone deficiency.”
The paper relies on this without support.
Few diabetic men with testosterone deficiency are diagnosed and treated worldwide.
“Currently, few diabetic men with testosterone deficiency are diagnosed and treated worldwide.”
The paper relies on this without support.
There is no clear consensus for an accepted lower limit of normal testosterone.
“There is no clear consensus for an accepted lower limit of normal testosterone.”
The paper relies on this without support.
Visceral obesity is an important cause of insulin resistance.
“Visceral obesity is an important cause of insulin resistance.”
The paper relies on this without support.
BMI and waist circumference adequately assess visceral adiposity.
“obesity and visceral adiposity, as assessed by both BMI and waist circumference”
The paper relies on this without support.
The sample of 355 type 2 diabetic men from a single centre is representative of type 2 diabetic men generally.
“Testosterone levels are frequently low in men with type 2 diabetes”
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?
Multiple studies confirmed the association between low or inappropriate T levels in men and T2D and obesity.
“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 [167]
Age, BMI, fasting blood glucose, triglycerides, alcohol consumption and estradiol levels have all been reported to be associated with alteration in hormone levels.
“Age, 11,14-17 body mass index (BMI), 12 fasting blood glucose, 1,35 triglycerides, 36 alcohol consumption 13,14 and estradiol levels, 13 which have all been reported to be associated with alteration in hormone levels, were chosen as potential confounding factors in this study.”
From Cigarette smoking has a positive and independent effect on testosterone levels (2013) · cites this paper as [35]
Age and BMI were major factors influencing both total and calculated free testosterone levels in the cohort.
“In our cohort, age and BMI were major factors influencing both TT and cFT levels, consistent with reports from previous studies (2,7,25).”
From Low testosterone levels are common and associated with insulin resistance in men with diabetes (2008) · cites this paper as [2]
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.
Bioavailable-testosterone category counts disagree
MajorThe results report 58 men below 2.5 nmol/l and 126 between 2.5 and 4 nmol/l, while Table 3 lists 53 and 131, respectively. In particular, a category defined as ≤2.5 nmol/l cannot contain fewer men than one defined as <2.5 nmol/l.
“16% (58 men) had bioavailable testosterone Ͻ2.5 nmol/l and 36% (126 patients) had bioavailable testosterone between 2.5 and 4 nmol/l”
“TT Յ8 nmol/l TT 8-12 nmol/l TT Ͼ12 nmol/l BT Յ2.5 nmol/l BT 2.5-4 nmol/l BT Ͼ4 nmol/l n 71 109 175 53 131 171”
Oral hypoglycemic treatment count differs
MinorThe methods report 160 men treated with oral hypoglycemic agents, whereas Table 1 reports 190. The table's treatment counts sum to the stated study size of 355; the methods counts sum to 325.
“Seventy patients were treated with diet alone, 95 with insulin, and 160 with oral hypoglycemic agents.”
“Medications (n) Diet 70 Insulin 95 Oral hypoglycemics 190”
Oldest age group's percentage does not match its count
MinorOf 355 subjects, 46 are approximately 13%, not the reported 12%.
Reported 12 · recomputed 12.957746
“Ͼ69 years (46 men; 12%)”
Age-group free and bioavailable testosterone values are reversed
MinorThe stated order assigns values around 4 nmol/l to free testosterone and around 0.3 nmol/l to bioavailable testosterone. Table 1 identifies the approximately 4 nmol/l values as bioavailable testosterone and the approximately 0.3 nmol/l values as free testosterone.
“The age distribution and mean testosterone levels (total, free, and bioavailable, respectively) were Ͻ40 years (13 men; 4%): 11.1, 4.05, and 0.32 nmol/l; 40 -49 years (60 men; 17%): 12.3, 4.34, and 0.30 nmol/l;”
“Bioavailable testosterone (nmol/l) (NR 2.5-11.9nmol/l) 4.03 Ϯ 0.08 0.89-11.49Calculated free testosterone (nmol/l) (NR 0.26-0.71nmol/l) 0.274 Ϯ 0.01 0.05-1.02”
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“The reason for this is the presumption that testosterone levels are low because the level of sex hormone– binding globulin (SHBG), the major carrier protein of testosterone in circulation, is low as a consequence of insulin resistance (8).”
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Sex hormones and hemostatic risk factors for coronary heart disease in men with hypertension
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“Serum testosterone levels have been reported to be lower in men with hypertension (40).”
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Investigation, treatment and monitoring of late-onset hypogonadism in males
Wang, C., Nieschlag, E., Swerdloff, R., Behre, H. M., Hellstrom, W. J., Gooren, L. J., Kaufman, J. M., Legros, J.-J., Lunenfeld, B., Morales, A., et al. (2008) · European Journal of Endocrinology · doi:10.1530/eje-08-0601 · Cited by 867 · see citing works
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Self-citationLow testosterone levels are common and associated with insulin resistance in men with diabetes
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- Authors
- Kapoor, D., Aldred, H., Clark, S., Channer, K. S., & Jones, T. H.
- Affiliations
- Barnsley Hospital NHS Foundation Trust (GB)
- University of Sheffield (GB)
- Royal Hallamshire Hospital (GB)
- ORCID
- Jones, T. Hugh
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2007-04-01
- Volume
- 30
- Issue
- 4
- Pages
- 911-917
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- OpenAlex
- W2160140561
- Semantic Scholar
- 710e5986dbc5fce8b69e7c669578fe08065a25a8
- Cited by
- 493
- References
- 47
- Citations by year
- 2026: 15 · 2025: 11 · 2024: 12 · 2023: 15 · 2022: 17 · 2021: 28 · 2020: 23 · 2019: 29 · 2018: 27 · 2017: 32 · 2016: 35 · 2015: 35 · 2014: 36 · 2013: 35 · 2012: 25
- FWCI
- 23.19
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Diabetes Care (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- hypogonadism, type 2 diabetes, androgen deficiency, bioavailable testosterone, free testosterone, sex hormone-binding globulin, obesity, waist circumference, body mass index
- MeSH terms
- Adipose Tissue, Adult, Aged, Aged, 80 and over, Biological Availability, Cross-Sectional Studies, Diabetes Mellitus, Type 2, Humans, Hypogonadism, Erectile Dysfunction, Male, Middle Aged, Obesity, Sex Hormone-Binding Globulin, Testosterone, Viscera, Body Mass Index, Body Size
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.
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