Treatment of Functional Hypogonadism Besides Pharmacological Substitution
Open accessAbstract
A dichotomic distinction between "organic" and "functional" hypogonadism is emerging. The former is an irreversible condition due to congenital or "acquired" "organic" damage of the brain centers or of the testis. Conversely, the latter is a potentially reversible form, characterized by borderline low testosterone (T) levels mainly secondary to age-related comorbidities and metabolic derangements, including metabolic syndrome (MetS). Life-style modifications, - here reviewed and, when possible, meta-analyzed -, have documented that weight-loss and physical exercise are able to improve obesity-associated functional hypogonadism and its related sexual symptoms. A rabbit experimental model, of MetS originally obtained in our lab, showed that endurance training (PhyEx) completely reverted MetS-induced hypogonadotropic hypogonadism by reducing hypothalamus inflammation and testis fibrosis eventually allowing for a better corpora cavernosa relaxation and response to sildenafil. Physicians should strongly adapt all the reasonable strategies to remove/mitigate the known conditions underlying functional hypogonadism, including MetS and obesity. Physical limitations, including reduced muscle mass and increased fat mass, along with low self-confidence, also due to the sexual problems, might limit a subject's propensity to increase physical activity and dieting. A short term T treatment trial, by improving muscle mass and sexual function, might help hypogonadal obese patients to overcome the overfed, inactive state and to become physically and psychologically ready for changing their lifestyle.
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Written from the paper’s full text.
TL;DR
Functional hypogonadism is a potentially reversible form of testosterone deficiency, most often linked to obesity, metabolic syndrome, and related comorbidities. This review finds that diet-induced weight loss, bariatric surgery, and physical exercise can improve testosterone levels and sexual symptoms, while a short-term testosterone trial may help obese hypogonadal men become ready for lifestyle change.
Key findings
- In a meta-analysis of 22 low-calorie diet studies (567 patients; mean age 44.9 years; mean BMI 36.0 kg/m²; mean follow-up 23 weeks), diet significantly increased total testosterone; an earlier meta-analysis found an average diet-induced weight loss of 9.8% was associated with a total testosterone increase of 2.8 nmol/L (1.68–4.07 nmol/L) in paired models and 2.05 nmol/L (0.93–3.16 nmol/L) in non-paired models. Each 5 kg of weight reduction corresponded to about a 1 nmol/L increase in testosterone.
- Five meta-analyses of bariatric surgery consistently found sustained increases in total testosterone (8–10 nmol/L) and free testosterone (75–90 pmol/L), along with increased SHBG and gonadotropins; total estradiol decreased by about 20 pmol/L in most meta-analyses.
- In 8 exercise studies (202 patients; mean age 51.8 years; mean BMI 28.5 kg/m²; mean follow-up 15 weeks), physical exercise significantly increased total testosterone; greater weight loss and longer trial duration were independently associated with larger increases, and older men showed greater testosterone improvement for equal weight change. Regular physical activity reduced the odds ratio for erectile dysfunction by 50%, and physical activity increased IIEF-EFD by almost 4 points, close to the 5-point increase reported for avanafil.
- In a rabbit model of high-fat-diet-induced metabolic syndrome, endurance training completely restored testosterone and LH levels, prostate weight, and GnRH immunostaining, doubled GnRH gene expression in the preoptic area, reduced hypothalamic inflammation and testis fibrosis, and improved corpora cavernosa relaxation and response to sildenafil.
Methods
- Narrative review with meta-analyses of lifestyle interventions for functional hypogonadism, including low-calorie diet, bariatric surgery, drug-induced weight loss (liraglutide), and physical exercise.
- Human data included 22 diet studies (567 patients), 8 exercise studies (202 patients), five bariatric surgery meta-analyses, and one 16-week liraglutide trial with 15 subjects per arm.
- Preclinical data came from a rabbit model of high-fat-diet-induced metabolic syndrome and hypogonadotropic hypogonadism, with 12 weeks of treadmill endurance training.
Limitations
- The paper states that changing lifestyle is not easy in everyday clinical practice; therapeutic diets and behavioral modifications are reasonable but often not successful, and physical limitations, reduced muscle mass, increased fat mass, and low self-confidence may limit patients’ propensity to increase physical activity and dieting. It also notes that human data do not offer insights into how lifestyle change ameliorates testosterone deficiency and its symptoms.
- The text makes evident that the included human trials differ in basal testosterone levels and in diet or exercise protocols, and that some analyses used non-paired endpoint comparisons for a more conservative approach. The review is not described as a systematic review with formal risk-of-bias assessment.
- The mechanistic conclusions rely heavily on a rabbit model, which the text presents as supporting preclinical evidence; translation to human functional hypogonadism is not established in the paper. The suggestion that a short-term testosterone treatment trial may help obese hypogonadal patients become ready for lifestyle change is presented as an opinion, not as an outcome tested in the reviewed studies.
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- Findingown data
Low-calorie diet results in significant increases in sex hormone binding globulin and calculated free testosterone at endpoint.
“We observed similar results when hormone binding globulin (SHBG) and calculated free T were considered (Fig. 1B, 1C, respectively).”
Quote in the paperSubstantial claim - Findingcitation
A low-calorie diet-induced average weight loss of 9.8% was associated with a significant increase in total testosterone of 2.8 nmol/L (1.68-4.07 nmol/L) in paired t-test models and 2.05 nmol/L (0.93-3.16 nmol/L) in non-paired t-test models.
“We found that an average diet-induced weight loss of 9.8% was associated with a significant increase in total T (TT) of 2.8 nmol/L (1.68–4.07 nmol/L) and 2.05 (0.93–3.16 nmol/L), when paired and non-paired t-test models were applied.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [23] Corona, 2013, Eur J Endocrinol source
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- Findingown data
Combining 21 studies, low-calorie diet results in a significant increase in total testosterone levels at endpoint.
“Combining the results of those trials, low calorie diet results in a significant increase in TT levels at endpoint (Fig. 1A).”
Quote in the paperSubstantial claim - Findingown data
The association between weight reduction and testosterone increase was confirmed in a multivariate regression analysis after adjustment for age and trial duration (adjusted r = −1.21; p < 0.0001).
“The latter finding was confirmed in a multivariate regression analysis, after the adjustment for age and trial duration (adjusted r =−1.21; p<0.0001).”
Quote in the paperSubstantial claim - Findingown data
A higher weight reduction is associated with a higher testosterone increase, such that each 5 kg of weight reduction results in a 1 nmol/L increase.
“Meta-regression analysis showed that a higher Δ-weight is associated with a higher T increase, meaning that each 5 kg of weight reduction results in one nmol/L increases (Fig. 1D).”
Quote in the paperSubstantial claim
- Findingcitation
Combining diet and bariatric surgery data, weight loss induced a significant increase in luteinizing hormone (1.31 mU/L [0.80-1.82 mU/L]) and follicle stimulating hormone (1.79 mU/L [1.28-2.30 mU/L]).
“However, when data from diet were combined with those from bariatric surgery (see below), we reported a significant weight loss-induced increase in luteinizing hormone (LH) (1.31 mU/L [0.80–1.82 mU/L]) and follicle stimulating hormone (1.79 mU/L [1.28–2.30 mU/L]) [23].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [23] Corona, 2013, Eur J Endocrinol source
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- Findingown data
For equal weight change, a greater improvement in total testosterone levels is obtained in older men after physical exercise.
“Interestingly, the analysis also shows that for equal weight change, a greater improvement in TT levels is obtained in older men.”
Quote in the paperNot a substantial claim - Findingown data
Greater weight loss and longer trial duration are significantly associated with an increase in total testosterone levels after physical exercise, independently of age.
“The standardized coefficients are shown in Fig. 3B and suggest that a greater weight loss and a longer trial duration are significantly associated with an increase in TT levels, independently of age.”
Quote in the paperSubstantial claim - Findingown data
Combining 8 studies, physical exercise resulted in a significant increase in total testosterone levels at endpoint.
“Combining the results of those trials, physical exercise resulted in a significant increase in TT levels at endpoint (Fig. 3A).”
Quote in the paperSubstantial claim - Findingown data
Endurance training allowed for better corpora cavernosa relaxation and response to sildenafil in the MetS rabbit model.
“A rabbit experimental model, of MetS originally obtained in our lab, showed that endurance training (PhyEx) completely reverted MetS-induced hypogonadotropic hypogonadism by reducing hypothalamus inflammation and testis fibrosis eventually allowing for a better corpora cavernosa relaxation and response to sildenafil.”
Quote in the paperSubstantial claim - Findingown data
Endurance training completely reverted MetS-induced hypogonadotropic hypogonadism in the rabbit model.
“A rabbit experimental model, of MetS originally obtained in our lab, showed that endurance training (PhyEx) completely reverted MetS-induced hypogonadotropic hypogonadism by reducing hypothalamus inflammation and testis fibrosis eventually allowing for a better corpora cavernosa relaxation and response to sildenafil.”
Quote in the paperSubstantial claim - Findingown data
Endurance training reduced hypothalamus inflammation and testis fibrosis in the MetS rabbit model.
“A rabbit experimental model, of MetS originally obtained in our lab, showed that endurance training (PhyEx) completely reverted MetS-induced hypogonadotropic hypogonadism by reducing hypothalamus inflammation and testis fibrosis eventually allowing for a better corpora cavernosa relaxation and response to sildenafil.”
Quote in the paperSubstantial claim - Findingown data
High-fat diet induces a decline in circulating testosterone in rabbits.
“Fig. 4A, shows the HFD-dependent decline in circulating T in a large number of rabbits.”
Quote in the paperSubstantial claim - Premisecitation
All five systematic meta-analyses found a significant, sustained increase in total and free testosterone after bariatric surgery compared with pre-surgical values.
“Despite differences in the number of studies analyzed and in the inclusion criteria for the study selection (Table 2), all the meta-analyses found a significant, sustained increase in TT and free T after bariatric surgery, as compared with the pre-surgical values (Fig. 2A).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [1123464748]
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- Premisecitation
A significant increase in sex hormone binding globulin and gonadotropins was consistently found after bariatric surgery in all meta-analyses.
“A significant increase in SHBG and gonadotropins was also consistently found in all these meta-analyses (Fig. 2C–2E).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [1123464748]
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- Premisecitation
In a 16-week trial in obese hypogonadal men with sexual symptoms and poor responses to lifestyle measures, liraglutide but not testosterone therapy induced a 6% reduction in weight.
“Liraglutide, but not TTh, induced a 6% reduction in weight.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [49] Jensterle, 2019, Endocr Connect source
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- Premisecitation
The large majority of secondary functional hypogonadism is associated with unhealthy metabolic conditions such as metabolic syndrome, diabetes, and obesity.
“In particular, the large majority of secondary functional HG is associated with unhealthy metabolic conditions, such as MetS, diabetes, and obesity [17].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [17] Corona, 2015, J Sex Med source
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- Premisecitation
The most recent phosphodiesterase type 5 inhibitor on the market, avanafil, increases IIEF-EFD by 5 points in meta-analysis.
“They found that on average physical activity increased IIEF-EFD by almost 4 points, an effect that is not very far from the 5 point increase - as evaluated in the meta-analysis - by the most recent phosphodiesterase type 5 inhibitor (PDE5i) on the market, avanafil [59].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [59] Corona, 2016, Expert Opin Drug Saf source
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- Premisecitation
A recent meta-analysis indicates that consistent aerobic endurance exercise is the most effective strategy for preventing erectile dysfunction, besides increasing testosterone levels.
“In particular, a recent meta-analysis indicates that consistent aerobic endurance exercise is the most effective strategy for preventing ED [58], beside increasing T levels.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [58] Allen, 2018, J Sex Med source
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- Premisecitation
Regular physical activity reduced the odds ratio for erectile dysfunction by 50%.
“However, the most impressive results were observed for regular physical activity, which reduced the odds ratio for ED by 50% [58].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [58] Allen, 2018, J Sex Med source
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- Premisecitation
The effect of regular physical activity on erectile dysfunction was apparent in almost all individual studies scrutinized.
“In addition, this effect was apparent in almost all the individual studies scrutinized [58].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [58] Allen, 2018, J Sex Med source
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- Premisecitation
The rabbit model of metabolic syndrome shares with the human phenotype several basic characteristics of MetS: hypertension, glucose intolerance, dyslipidemia, and increased visceral fat.
“This animal model shares with the human phenotype several basic characteristics of MetS, i.e., hypertension, glucose intolerance, dyslipidemia, and increased visceral fat [60].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [60] Filippi, 2009, J Sex Med source
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- Premisecitation
On average, physical activity increased IIEF-EFD by almost 4 points in randomized controlled trials of ED patients.
“They found that on average physical activity increased IIEF-EFD by almost 4 points, an effect that is not very far from the 5 point increase - as evaluated in the meta-analysis - by the most recent phosphodiesterase type 5 inhibitor (PDE5i) on the market, avanafil [59].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [59] Corona, 2016, Expert Opin Drug Saf source
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- Premisecitation
MetS-associated hypogonadism was associated with symptoms and signs of testosterone deficiency, such as decreased prostate weight and erectile dysfunction.
“MetS-associated HG was also associated with symptoms and signs of TD, as decreased prostate weight and ED [6162].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [6162]
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- Premisecitation
In MetS animals, erectile dysfunction was characterized by impaired responsiveness to acetylcholine and PDE5 inhibitors, due to an impairment in nitric oxide formation and action.
“In MetS animals, ED was characterized by impaired responsiveness to acetylcholine (Ach) and PDE5i, due to an impairment in nitric oxide formation and action [6062].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [6062]
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- Premisecitation
In the medial preoptic area of MetS rabbits, several genes related to glucose transporters GLUT1-4 and metabolism (insulin receptor substrate 1) were up-regulated.
“Finally, in MPO of MetS rabbits several genes related to glucose transporter (GLUT) #1–4 and metabolism (insulin receptor substrate 1) were up-regulated [6162].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [6162]
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- Premisecitation
The MetS-induced hypogonadotropic hypogonadism was associated with inflammation of the medial preoptic area of the hypothalamus, characterized by increased expression of cyclooxygenase-2 and macrophage markers.
“We have previously demonstrated that the MetS-induced hypogonadotropic HP was associated with a peculiar inflammation of the medial preoptic area (MPO) of the hypothalamus, where GnRH neurons are located, characterized by an increased expression of cyclooxygenase-2 and macrophage markers [6162].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [6162]
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- Premisecitation
Testosterone administration was able to restore sensitivity to acetylcholine and PDE5 inhibitors in MetS animals.
“Interestingly, we previously reported that T administration was able to restore sensitivity to Ach and PDE5i [60].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [60] Filippi, 2009, J Sex Med source
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- Interpretationreasoning
High-fat diet induced a genuine hypogonadotropic hypogonadism in the rabbit model.
“Hence, HFD induced a genuine hypogonadotropic HP.”
Quote in the paperSubstantial claim - Premisecitation
Physical exercise restored Kiss1 receptor immunostaining, which was decreased by HFD.
“PhyEx restored Kiss1 receptor immunostaining, which resulted decreased by HFD (Fig. 6B).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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- Premisecitation
In corpora cavernosa extracts, several genes related to NO formation (DDAH1) and signaling (GCSa1, GCSb1, PDE5, PKG) were up-regulated by physical exercise, along with those involved in smooth muscle differentiation (SM22, αSMA) and androgen action (AR, STAMP2).
“In CC extracts, several genes related to NO formation (DDAH1) and signaling (GCSa1, GCSb1, PDE5, PKG) were up-regulated by PhyEx, along with those involved in smooth muscle differentiation (SM22, αSMA) and androgen action (AR, STAMP2).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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- Premisecitation
HFD-induced increases in genes related to inflammation, estrogen signaling, and glucose metabolism in the hypothalamus were significantly reduced in HFD rabbits given physical exercise.
“All the aforementioned HFD-induced increase in genes related to inflammation, estrogen signaling, and glucose metabolism in the hypothalamus were significantly reduced in HFD+PhyEx.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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- Premisecitation
Physical exercise reverted all these alterations in corpora cavernosa.
“PhyEx reverted all these alterations.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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- Interpretationcitation
The distinction between a functional and an organic form of hypogonadism is captious because even diet-induced hypogonadotropic hypogonadism is associated with distinct organic alterations within the hypothalamus, the testis and the penis.
“The distinction between a functional and an organic form of HG is, in some ways, captious because, as demonstrated in our preclinical model, even diet-induced hypogonadotropic HG is associated with distinct, organic alterations within the hypothalamus, the testis and the penis [606162].”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationreasoning
The main advantage of considering a functional form of hypogonadism is that it is essentially a reversible form of hypogonadism.
“However, the main advantage of considering a functional form of HG is that this is essentially a reversible form of HG.”
Quote in the paperSubstantial claim
- May combine two claims. 27
- Classified as probably not a substantial claim. 1
May combine two claims.
Findingown dataIn MetS rabbits, not only are testosterone levels reduced but luteinizing hormone levels are also reduced to levels not statistically different from those induced by GnRH analog administration.
“The same Fig. 4B shows that in MetS rabbits not only T levels were reduced but also LH levels are, at levels not statistically different from those induced by impairing LH secretion through gonadotropin-releasing hormone (GnRH) analog administration.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataPhysical exercise is able to increase testosterone levels, in particular in older individuals, with a benefit proportional to the amount and duration of the activity.
“We reported here, by meta-analyzing available studies, that physical exercise is able to increase T levels, in particular in older individuals, with a benefit that is proportional to the amount and duration of the activity.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim. May combine two claims.
PremisecitationFunctional hypogonadism is a reversible form with borderline low testosterone levels, sexual symptoms only partially ameliorated by testosterone therapy, and unknown therapy risk.
“In contrast, “functional” HG is a reversible form, with borderline low T levels, characterized by sexual symptoms that are only partially ameliorated by TTh, and, more importantly, with an unknown therapy risk.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [16] Grossmann, 2017, J Clin Endocrinol Metab source
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PremisecitationThe large majority of subjects consulting for sexual dysfunction and having low testosterone can be categorized as functional hypogonadism (85%), with secondary hypogonadism prevalent over primary at a ratio of 5.5:1.
“In addition, it should be emphasized that the large majority of subjects consulting for sexual dysfunction and having low T can be categorized as functional HG (85%), with secondary HG the prevalent form, with a ratio of 5.5:1 vs. primary HG [17].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [17] Corona, 2015, J Sex Med source
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PremisecitationThe mean increase in testosterone after bariatric surgery ranged from 8 to 10 nmol/L for total testosterone and from 75 to 90 pmol/L for free testosterone across meta-analyses.
“The mean increase in T was comparable in all the available meta-analyses ranging from 8 to 10 nmol/L for TT and from 75 to 90 pmol/L for free T (Fig. 2B).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [1123464748]
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PremisecitationTotal estradiol was significantly decreased after bariatric surgery, with a mean reduction of about 20 pmol/L as documented by most meta-analyses, except the earliest one which found a decline of around a half.
“Total estradiol was significantly decreased after bariatric surgery, with a mean reduction of about 20 pmol/L, as documented by most meta-analyses, except for the earliest one [11] which found a decline of around a half (Fig. 2F).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [11] Corona, 2015, Mol Cell Endocrinol source
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PremisecitationMetabolic syndrome is deeply underpinned with secondary hypogonadism and erectile dysfunction.
“Actually, MetS is also deeply underpinned with secondary HG and erectile dysfunction (ED) [1220].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [1220]
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PremisecitationOnly 50% of primary hypogonadism and 10% of secondary hypogonadism show an organic origin for testosterone deficiency.
“Only 50% and 10% of primary and secondary HG, respectively, show an organic origin for the TD.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [17] Corona, 2015, J Sex Med source
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PremisecitationIn the same trial, testosterone therapy further reduced luteinizing hormone levels, whereas liraglutide marginally improved it (0.7 mU/L).
“As expected, TTh further reduced LH levels, whereas liraglutide marginally improved it (0.7 mU/L).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [49] Jensterle, 2019, Endocr Connect source
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PremisecitationCigarette smoking, high alcohol intake, and lack of physical activity all have deleterious effects on erectile function.
“Cigarette smoking, high alcohol intake, and lack of physical activity all have deleterious effects on erectile function [58].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [58] Allen, 2018, J Sex Med source
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PremisecitationIn the same trial, both liraglutide and testosterone therapy ameliorated sexual symptoms and significantly increased total testosterone, although the increase was greater with testosterone gel (5.9 vs. 2.6 nmol/L with liraglutide).
“Both treatments ameliorated sexual symptoms and increased significantly TT, although the increase was more evident with T gel (5.9 vs. 2.6 nmol/L with liraglutide).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [49] Jensterle, 2019, Endocr Connect source
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InterpretationreasoningThe data summarized above suggest that reducing caloric intake or increasing physical activity are efficacious in restoring an altered HPT axis, as often observed in several metabolic conditions, including obesity and MetS.
“Overall, the data summarized above suggest that they are efficacious in restoring an altered HPT axis, as often observed in several metabolic conditions, including obesity and MetS.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataHuman data from intervention trials indicate that reducing caloric intake (diet or bariatric surgery) or increasing caloric expenditure (physical activity) improve testosterone deficiency in functional hypogonadism.
“Human data derived from intervention trials aimed at investigating the effect of changing lifestyle on functional HG indicate that reducing caloric intake (diet or bariatric surgery) or increasing caloric expenditure (physical activity) improve TD.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationIn the testis of MetS rabbits, all steroidogenic enzymes leading to testosterone synthesis were downregulated in a stepwise fashion, and fibronectin expression was increased.
“Within the testis, the MetS condition down regulated, in a stepwise fashion, all the steroidogenic enzymes leading to T synthesis, along with an increase in fibronectin expression.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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PremisecitationHFD rabbits showed typical metabolic and cardiovascular features of metabolic syndrome along with hypogonadotropic hypogonadism.
“As mentioned before, HFD rabbits showed typical metabolic and cardiovascular features of MetS along with hypogonadotropic HG.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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PremisecitationUpon high-fat diet, genes coding inhibitory factors for GnRH were increased, as well as neuropeptide Y and prodynorphin, along with their cognate receptors.
“We previously reported that, upon HFD, genes coding inhibitory factors for GnRH were increased, as well as neuropetide Y and prodynorphin, along with their cognate receptors [62].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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PremisecitationIn the medial preoptic area of MetS rabbits, expression of estrogen receptor ERβ and GPR30 was increased; in the male hypothalamus, these receptors mediate negative feedback on GnRH.
“In addition, we also reported an increased expression in MPO of estrogen receptor (ERβ and GPR30), which - in the male hypothalamus - mediates a negative feedback on GnRH [6162].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [6162]
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PremisecitationIn the medial preoptic area of MetS rabbits, immunopositivity for GnRH was decreased, along with altered expression of Kiss1 and its receptor (Kiss1R).
“Interestingly, in MPO of MetS rabbits, immunopositivity for GnRH was decreased, along with an altered expression of the main neurotransmitters regulating GnRH secretion, as Kiss1 and its receptor (Kiss1R) [606162].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [606162]
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PremisecitationThe rabbit model shows a MetS factor-dependent hypogonadotropic hypogonadism and erectile dysfunction.
“In addition, these rabbits show a MetS factor-dependent hypogonadotropic HP and ED [60].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [60] Filippi, 2009, J Sex Med source
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InterpretationreasoningIn this experimental model, endurance training (physical exercise) completely reverted metabolic syndrome-induced hypogonadotropic hypogonadism and erectile dysfunction, having beneficial effects on the HPT axis and on the penis.
“In conclusion, in this experimental model, endurance training (PhyEx) completely reverted MetS-induced hypogonadotropic HP and ED, having beneficial effects on the HPT axis and on the penis.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationPhysical exercise increased the ratio of androstenedione to testosterone concentration within the testis, which was downregulated by HFD.
“Accordingly, PhyEx increased the ratio of androstenedione to T concentration within the testis, which resulted downregulated by HFD [62].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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PremisecitationCorpora cavernosa strips from HFD rabbits showed hypo-responsiveness to acetylcholine and electrical field stimulation, and sildenafil action on electrical field- or sodium nitroprusside-induced relaxation was impaired in HFD corpora cavernosa.
“Corpora cavernosa (CC) strips from HFD rabbits showed a hypo-responsiveness to Ach and electrical field (EF) stimulation.”
- Also stated in: § 2. Effect of physical exercise in a rabbit with metabolic syndrome-associated hypogonadotropic hypogonadism · plain
“In addition, sildenafil action on EF- or sodium nitroprusside-induced relaxation was also impaired in HFD CC.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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- Also stated in: § 2. Effect of physical exercise in a rabbit with metabolic syndrome-associated hypogonadotropic hypogonadism · plain
May combine two claims.
PremisecitationWithin the testis, physical exercise normalized fibronectin expression and increased genes related to testosterone formation (17βHSD3) and metabolism (5α-reductase 1).
“Within the testis, PhyEx normalized fibronectin expression and increased genes related to T formation (17βHSD3) and metabolism (5α-reductase 1) [62].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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PremisecitationPhysical exercise completely restored testosterone and LH plasma levels, prostate weight and GnRH immunostaining in HFD rabbits, and doubled GnRH gene expression in the preoptic area.
“PhyEx completely restored T and LH plasma levels, prostate weight and GnRH immunostaining (Fig. 5), doubling its gene expression in the preoptic area [62].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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PremisecitationIn the hypothalamus, physical exercise increased Kiss1 and decreased orexigenic and GnRH-inhibiting factors (dynorphin and its receptors OPRD1 and OPRK1), whereas it increased anorexigenic factors (proopiomelanocortin).
“In particular, in the hypothalamus, PhyEx increased Kiss 1 and decreased orexigenic and GnRH-inhibiting factors (dynorphin and its receptors OPRD1 and OPRK1), whereas it increased anorexigenic ones (proopiomelanocortin).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [62] Morelli, 2019, Am J Physiol Endocrinol Metab source
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May combine two claims.
Interpretationown dataIn the hypothalamus, physical exercise reduced HFD-induced inflammation; in the testis, it reduced fibrosis; and in the penis, it allows a better relaxation and response to sildenafil.
“In the hypothalamus, PhyEx reduced HFD-induced inflammation, in the testis, it reduced fibrosis and, in the penis, it allows a better relaxation and response to sildenafil.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataTherapeutic diets and behavioral modifications are reasonable but not often successful clinical strategies for protecting against obesity-associated hypogonadism.
“Therapeutic diets and behavioral modifications are reasonable (but not often successful) clinical strategies, even for protecting against obesity-associated HG, as demonstrated by the meta-analyses also reported here.”
Quote in the paperSubstantial claim
The paper relies on this without support.
Human data does not offer insights on how changing lifestyle acts in ameliorating testosterone deficiency and its associated symptoms.
“However, human data does not offer insights on how changing lifestyle acts in ameliorating TD and its associated symptoms.”
The paper relies on this without support.
Physical limitations, including reduced muscle mass and increased fat mass, along with low self-confidence due to sexual problems, limit a subject's propensity to increase physical activity and dieting.
“Physical limitations, including reduced muscle mass and increased fat mass, along with low self-confidence, also due to the sexual problems, might limit a subject's propensity to increase physical activity and dieting.”
The paper relies on this without support.
Functional hypogonadism is by far the most common condition determining testosterone deficiency in adult males, with sexual complaints and erectile dysfunction as the most characteristic symptoms.
“Functional HG is by far the most common condition determining, in the adult male, a TD that can be also symptomatic, having sexual complains - and in particular ED - as the most characteristic symptoms.”
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?
Obesity is a very common cause of functional hypogonadism.
“Functional hypogonadism is usually due to hypothalamic–pituitary suppression by extragonadal disease, and obesity is a very common cause.”
From The role of the androgen receptor in the pathogenesis of obesity and its utility as a target for obesity treatments (2022) · cites this paper as [54]
Functional hypogonadism can be reversible by treating the disease causing hypothalamic-pituitary suppression, such as weight loss in obesity.
“Functional hypogonadism occurs in the absence of recognizable disease of the HPT and can be reversible by treating the disease causing hypothalamic–pituitary suppression, such as weight loss in obesity. 50 , 54”
From The role of the androgen receptor in the pathogenesis of obesity and its utility as a target for obesity treatments (2022) · cites this paper as [54]
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Advances in the treatment of functional male hypogonadism
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Self-citationObesity Surgery Improves Hypogonadism and Sexual Function in Men without Effects in Sperm Quality
Miñambres, I., Sardà, H., Urgell, E., Genua, I., Ramos, A., Fernández–Ananín, S., Balagué, C., Sánchez‐Quesada, J. L., Bassas, L., & Pérez, A. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11175126 · Cited by 19 · see citing works
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Self-citationPharmacological management of testosterone deficiency in men current advances and future directions
Corona, G., Rastrelli, G., Sparano, C., Vignozzi, L., Sforza, A., & Maggi, M. (2024) · Expert Review of Clinical Pharmacology · doi:10.1080/17512433.2024.2366505 · Cited by 16 · see citing works
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Pharmacotherapy of male hypogonadism
Rastrelli, G., Vignozzi, L., Corona, G., & Maggi, M. (2022) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2022.102323 · Cited by 11 · see citing works
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Managing antipsychotic-related sexual dysfunction in patients with schizophrenia
Silva, C. M., Rebelo, M., & Chendo, I. (2023) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2023.2281399 · Cited by 8 · see citing works
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Dietary patterns and testosterone balance: a review of clinical data and perspectives
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Functional hypogonadism in men: key causes and neuroendocrine mechanisms of its development
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Testosterone Therapy in Adult Males with Hypogonadism
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Self-citationHypogonadotropic hypogonadism as a cause of NOA and its treatment
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Rethinking Low Testosterone in Older Men: Association With Obesity Rather Than Aging
Tiraboschi, T. L. N., Miranda, E., Novaes, M. T., Silva, C. S., Contreras, J. C. Z., Filho, J. D. S. R., Reggio, E., Suartz, C. V., Gomes, C. M., & de Bessa, J. (2025) · Urology · doi:10.1016/j.urology.2024.12.036 · Cited by 4 · see citing works
Developments and challenges for new and emergent preparations for male hypogonadism treatment
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Self-citationEffect of Androgen Deficiency on the Condition of Carbohydrate Metabolism in Men
Mkrtumyan, A. M., Yegshatyan, L. V., & Shishkova, Y. A. (2020) · Effective Pharmacotherapy · doi:10.33978/2307-3586-2020-16-12-56-66 · Cited by 4 · see citing works
Male Hypogonadism (According to the Materials of the European Association of Urology)
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Varicocele and low testosterone
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Testosterone Therapy with a Man with Equivocal Testosterone Levels
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Self-citationThe Prevalence of Late-Onset Hypogonadism in Middle-Aged Men and Cardiovascular Risk Factors
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Hypogonadisme en een kinderwens, hebben we opties om te behandelen?
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Examining the Efficacy of Clomiphene Citrate as a Treatment for Male Infertility
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Benefits and Risks of Testosterone Replacement in the Older Man with Hypogonadism
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Trattare o non trattare con testosterone l’ipogonadismo funzionale?
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Erkrankungen der männlichen Gonaden
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Inflammation factors mediate association of muscle mass and erectile dysfunction: NHANES 2001–2004
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- Authors
- Corona, G., Rastrelli, G., Morelli, A., Sarchielli, E., Cipriani, S., Vignozzi, L., & Maggi, M.
- Affiliations
- Azienda USL di Bologna (IT)
- University of Florence (IT)
- Corresponding author
- Maggi, Mario
- ORCID
- Venue
- The World Journal of Men's Health
- Publisher
- XMLink
- Published
- 2020
- Volume
- 38
- Issue
- 3
- Pages
- 256
- ISSN
- 2287-4208 (ISSN-L)
- 2287-4690
- PMC
- PMC7308235
- OpenAlex
- W2971649306
- Semantic Scholar
- 86f807a114a6968f0c5b356365d11fd202d74759
- Cited by
- 87
- References
- 66
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 10 · 2023: 16 · 2022: 20 · 2021: 9 · 2020: 12 · 2019: 1
- FWCI
- 1.61
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Licence
- Locations
- The World Journal of Men s Health (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Florence Research (University of Florence) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- 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 › Psychiatry and Mental health › Sexual function and dysfunction studies
- Keywords
- functional hypogonadism, hypogonadotropic hypogonadism, metabolic syndrome, obesity, testosterone replacement therapy, lifestyle modification, weight loss, physical activity, endurance training, hypothalamic inflammation, testicular fibrosis, erectile function, sexual dysfunction, male sexual health
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