Cited by 414Hormonal and reproductive studiesBariatric Surgery and OutcomesHypothalamic control of reproductive hormones

Body weight loss reverts obesity-associated hypogonadotropic hypogonadism: a systematic review and meta-analysis

Open access
Corona, Giovanni, Rastrelli, Giulia, Monami, Matteo, Saad, Farid, Luconi, Michaela, Lucchese, Marcello, Facchiano, Enrico, Sforza, Alessandra +3 more·2013·European Journal of Endocrinology

Abstract

OBJECTIVE: Few randomized clinical studies have evaluated the impact of diet and physical activity on testosterone levels in obese men with conflicting results. Conversely, studies on bariatric surgery in men generally have shown an increase in testosterone levels. The aim of this study is to perform a systematic review and meta-analysis of available trials on the effect of body weight loss on sex hormones levels. DESIGN: Meta-analysis. METHODS: An extensive Medline search was performed including the following words: 'testosterone', 'diet', 'weight loss', 'bariatric surgery', and 'males'. The search was restricted to data from January 1, 1969 up to August 31, 2012. RESULTS: Out of 266 retrieved articles, 24 were included in the study. Of the latter, 22 evaluated the effect of diet or bariatric surgery, whereas two compared diet and bariatric surgery. Overall, both a low-calorie diet and bariatric surgery are associated with a significant (P<0.0001) increase in plasma sex hormone-binding globulin-bound and -unbound testosterone levels (total testosterone (TT)), with bariatric surgery being more effective in comparison with the low-calorie diet (TT increase: 8.73 (6.51-10.95) vs 2.87 (1.68-4.07) for bariatric surgery and the low-calorie diet, respectively; both P<0.0001 vs baseline). Androgen rise is greater in those patients who lose more weight as well as in younger, non-diabetic subjects with a greater degree of obesity. Body weight loss is also associated with a decrease in estradiol and an increase in gonadotropins levels. Multiple regression analysis shows that the degree of body weight loss is the best determinant of TT rise (B=2.50±0.98, P=0.029). CONCLUSIONS: These data show that weight loss is associated with an increase in both bound and unbound testosterone levels. The normalization of sex hormones induced by body weight loss is a possible mechanism contributing to the beneficial effects of surgery in morbid obesity.

Integrity signals

Registry

Crossref · 10.1530/eje-12-0955

Cites

71 of 72 references verified0 citation errors · 1 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

9 of 34 cited sources checked · 3 supported · 0 flagged · accuracy not yet measured

  • Premisecitation

    Increased BMI is associated with low measured or calculated free and bioavailable testosterone.

    “However, it is important to note that an increased BMI was associated with a low measured, or calculated, free and bioavailable testosterone (24).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [24] 24. Saad F, Aversa A, Isidori AM & Gooren LJ. Testosterone as potential effective therapy in treatment of obesity in men with testosterone deficiency: a review. Current Diabetes Reviews 2012 8 131-143. (doi:10.2174/157339912799424573) source

      The 'Relationship Between Testosterone and Obesity' section reports an inverse relationship between BMI and testosterone levels in men. It does not specify that this BMI association holds for measured or calculated free and bioavailable testosterone; its separate discussion of free and bioavailable testosterone concerns diabetes risk, not BMI. Page numbers were not available in our copy. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
  • Premisecitation

    Patients with T2DM and insulin resistance show a higher prevalence of hypogonadotropic hypogonadism.

    “Accordingly, patients with T2DM and insulin resistance show a higher prevalence of hypogonadotropic hypogonadism (54,55,60)”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites [54] 54. Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A & Dandona P. Frequent occurrence of hypogonadotropic hypogo- nadism in type 2 diabetes. Journal of Clinical Endocrinology and Metabolism 2004 89 5462-5468. (doi:10.1210/jc.2004- 0804) source
    • cites [55] 55. Dandona P & Dhindsa S. Update: hypogonadotropic hypogonadism in type 2 diabetes and obesity. Journal of Clinical Endocrinology and Metabolism 2011 96 2643-2651. (doi:10.1210/jc.2010- 2724) source
    • cites [60] 60. Corona G, Mannucci M, Petrone L, Ricca V, Balercia G, Mansani R, Chiarini V, Giommi R, Forti G & Maggi M. Association of hypogonadism and type 2 diabetes in men attending an outpatient erectile dysfunction clinic. International Journal of Impotence Research 2006 18 190-197. (doi:10.1038/sj.ijir.3901391) source
  • Premisecitation

    An obesity-associated decline in SHBG might partially explain the observed fall in testosterone levels.

    “An obesityassociated decline in SHBG might partially explain the observed fall in testosterone levels (19,20,21,22,23).”
    Quote in the paperNot a substantial claim1 of 5 sources checked
    • cites [19] 19. Corona G, Rastrelli G, Vignozzi L & Maggi M. Emerging medication for the treatment of male hypogonadism. Expert Opinion on Emerging Drugs 2012 17 239-592. (doi:10.1517/14728214. 2012.683411) source
    • cites [20] 20. Corona G, Rastrelli G, Vignozzi L, Mannucci E & Maggi M. How to recognize late-onset hypogonadism in men with sexual dysfunc- tion. Asian Journal of Andrology 2012 14 251-259. (doi:10.1038/ aja.2011.138) source

      The classification section says SHBG can be decreased in obesity and recommends considering free testosterone measurement in that setting. The Abstract reports that waist circumference helps detect low testosterone, but the paper does not explicitly say that reduced SHBG explains the fall in testosterone levels. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites [21] 21. Corona G, Rastrelli G, Morelli A, Vignozzi L, Mannucci E & Maggi M. Hypogonadism and metabolic syndrome. Journal of Endocrinological Investigation 2011 34 557-567. source
    • cites [22] 22. Corona G, Mannucci E, Forti G & Maggi M. Following the common association between testosterone deficiency and diabetes mellitus, can testosterone be regarded as a new therapy for diabetes? International Journal of Andrology 2009 32 431-441. (doi:10.1111/j.1365-2605.2009.00965.x) source
    • cites [23] 23. Wu FC, Tajar A, Pye SR, Silman AJ, Finn JD, O'Neill TW, Bartfai G, Casanueva F, Forti G, Giwercman A et al. Hypothalamic-pituitary- testicular axis disruptions in older men are differentially linked to age and modifiable risk factors: the European Male Aging Study. Journal of Clinical Endocrinology and Metabolism 2008 93 2737-2745. (doi:10.1210/jc.2007-1972) source
  • Premisecitation

    Obesity-related male hypogonadism is considered a form of hypogonadotropic hypogonadism.

    “Based on these and other studies (53,54), obesity-related male hypogonadism is now considered as a form of hypogonadotropic hypogonadism (see for a review, references (55,56)).”
    Quote in the paperSubstantial claim2 of 4 sources checked
    • cites [53] 53. Corona G, Mannucci E, Fisher AD, Lotti F, Petrone L, Balercia G, Bandini E, Forti G & Maggi M. Low levels of androgens in men with erectile dysfunction and obesity. Journal of Sexual Medicine 2008 5 2454-2463. source
    • cites [54] 54. Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A & Dandona P. Frequent occurrence of hypogonadotropic hypogo- nadism in type 2 diabetes. Journal of Clinical Endocrinology and Metabolism 2004 89 5462-5468. (doi:10.1210/jc.2004- 0804) source
    • cites [55] 55. Dandona P & Dhindsa S. Update: hypogonadotropic hypogonadism in type 2 diabetes and obesity. Journal of Clinical Endocrinology and Metabolism 2011 96 2643-2651. (doi:10.1210/jc.2010- 2724) source
    • cites [56] 56. Saad F, Aversa A, Isidori AM, Zafalon L, Zitzmann M & Gooren L. Onset of effects of testosterone treatment and time span until maximum effects are achieved. European Journal of Endocrinology 2011 165 675-685. (doi:10.1530/EJE-11-0221) source

      The Discussion addresses testosterone treatment, visceral obesity and metabolic syndrome, but does not classify obesity-related male hypogonadism as hypogonadotropic. Searches for that classification and for “hypogonadotropic” found the term only in titles in the References, not a passage making the claimed connection; page numbers were unavailable in our copy. (LLM, conf=0.74)

      Experimental — accuracy not yet measured
  • Premisecitation

    Increased estrogen levels might play a negative feedback on both the hypothalamus and the pituitary, leading to decreased LH secretion.

    “The increased amount of estrogen levels might, in turn, play a negative feedback on both the hypothalamus and the pituitary, leading to decreased LH secretion (22,55).”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [22] 22. Corona G, Mannucci E, Forti G & Maggi M. Following the common association between testosterone deficiency and diabetes mellitus, can testosterone be regarded as a new therapy for diabetes? International Journal of Andrology 2009 32 431-441. (doi:10.1111/j.1365-2605.2009.00965.x) source
    • cites [55] 55. Dandona P & Dhindsa S. Update: hypogonadotropic hypogonadism in type 2 diabetes and obesity. Journal of Clinical Endocrinology and Metabolism 2011 96 2643-2651. (doi:10.1210/jc.2010- 2724) source

      The Abstract describes a hypothesis that excess estrogen in obesity may suppress hypothalamic GnRH secretion, which could account for reduced LH. It does not attribute estrogen feedback to the pituitary, and it reports that lower estradiol in men with diabetic hypogonadotropic hypogonadism argues against this mechanism as their explanation. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
  • May combine two claims. 14
  • Classified as probably not a substantial claim. 10
  • May combine two claims.

    Premisecitation

    Obesity in men is associated with low testosterone and reduced sex hormone-binding globulin levels.

    “It is known that obesity in men is associated with low testosterone and reduced sex hormone-binding globulin (SHBG) levels (19,20,21,22,23).”
    Quote in the paperSubstantial claim1 of 5 sources checked
    • cites [19] 19. Corona G, Rastrelli G, Vignozzi L & Maggi M. Emerging medication for the treatment of male hypogonadism. Expert Opinion on Emerging Drugs 2012 17 239-592. (doi:10.1517/14728214. 2012.683411) source
    • cites [20] 20. Corona G, Rastrelli G, Vignozzi L, Mannucci E & Maggi M. How to recognize late-onset hypogonadism in men with sexual dysfunc- tion. Asian Journal of Andrology 2012 14 251-259. (doi:10.1038/ aja.2011.138) source
    • cites [21] 21. Corona G, Rastrelli G, Morelli A, Vignozzi L, Mannucci E & Maggi M. Hypogonadism and metabolic syndrome. Journal of Endocrinological Investigation 2011 34 557-567. source
    • cites [22] 22. Corona G, Mannucci E, Forti G & Maggi M. Following the common association between testosterone deficiency and diabetes mellitus, can testosterone be regarded as a new therapy for diabetes? International Journal of Andrology 2009 32 431-441. (doi:10.1111/j.1365-2605.2009.00965.x) source
    • cites [23] 23. Wu FC, Tajar A, Pye SR, Silman AJ, Finn JD, O'Neill TW, Bartfai G, Casanueva F, Forti G, Giwercman A et al. Hypothalamic-pituitary- testicular axis disruptions in older men are differentially linked to age and modifiable risk factors: the European Male Aging Study. Journal of Clinical Endocrinology and Metabolism 2008 93 2737-2745. (doi:10.1210/jc.2007-1972) source
  • May combine two claims.

    Premisecitation

    Bariatric surgery has a relevant beneficial effect on body weight loss, survival, and obesity-related comorbidities.

    “These studies showed a relevant beneficial effect of surgery on body weight loss, survival, and obesity-related comorbidities (64, 65).”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [64] 64. Sjo ¨stro ¨m L, Narbro K, Sjo ¨stro ¨m CD, Karason K, Larsson B, Wedel H, Lystig T, Sullivan M, Bouchard C, Carlsson B et al. Effects of bariatric surgery on mortality in Swedish obese subjects. New England Journal of Medicine 2007 357 741-752. (doi:10.1056/ NEJMoa066254) source
    • cites [65] 65. Sjo ¨stro ¨m L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B, Dahlgren S, Larsson B, Narbro K, Sjo ¨stro ¨m CD et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. New England Journal of Medicine 2004 351 2683-2693. (doi:10.1056/NEJMoa035622) source

      The Abstract reports substantial long-term weight loss and improvements in several obesity-related risk factors after surgery, though not all risk factors improved. The “death and other adverse events” section says mortality analyses were still ongoing, so this paper does not establish a survival benefit. (LLM, conf=0.91)

      Experimental — accuracy not yet measured
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    Out of 266 retrieved articles, 24 were included in the study.

    “Out of 266 retrieved articles, 24 were included in the study.”
    • Also stated in: § Results · plain
      “Out of 266 retrieved articles, 24 were included in the study.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Mean total testosterone increase was 8.73 nmol/l (95% CI 6.51-10.95) for bariatric surgery and 2.87 nmol/l (95% CI 1.68-4.07) for low-calorie diet.

    “with bariatric surgery being more effective in comparison with the low-calorie diet (TT increase: 8.73 (6.51-10.95)vs 2.87 (1.68-4.07)for bariatric surgery and the low-calorie diet, respectively; both P!0.0001 vs baseline).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    Of the 24 included studies, 22 evaluated the effect of diet or bariatric surgery, whereas two compared diet and bariatric surgery.

    “Of the latter, 22 evaluated the effect of diet or bariatric surgery, whereas two compared diet and bariatric surgery.”
    • Also stated in: § Results · plain
      “Of the included studies (see the trial flow summary in Fig. 1), 22 evaluated the effect of diet or bariatric surgery, whereas two compared diet and bariatric surgery.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Baseline total testosterone, BMI, and change in BMI as well as percent increase in SHBG were all significantly associated with percent increase in total testosterone after weight loss.

    “Baseline TT, BMI, and D-BMI as well as the percent increase in SHBG (D-SHBG) were all significantly associated with D-TT (BZ5.16G2.13,PZ0.022; BZ2.51G0.84,PZ0.007; BZ2.76G0.71,PZ0.001; and BZ0.70G 0.24, PZ0.013 respectively), whereas no association between D-TT and D-E 2 or DM at baseline was observed after adjusting for age (data not shown).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingnone given

    Body weight loss is associated with an increase in SHBG, calculated free testosterone, LH, and FSH, and a reduction in estradiol.

    “Furthermore, a reduction in body weight is associated with an increase in SHBG, cFT, LH, and FSH and a reduction in E 2 .”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In the included studies, body weight loss was 9.8% with diet versus 32% with surgery.

    “However, the testosterone rise induced by lifestyle interventions was only modest, probably reflecting the relatively modest results of the targeted diet and physical activity on body weight loss (9.8% with diet vs 32% with surgery in the studies included in this meta-analysis).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    The diabetic condition has a negative effect on testosterone rise after the intervention.

    “Interestingly, we now report that the diabetic condition has a negative effect on testosterone rise after the intervention; however, this difference does not retain statistical significance after adjusting for D-BMI, suggesting that it could be due to a greater body weight loss in non-diabetic patients.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The quality of studies was assessed using the Cochrane criteria.

    “The quality of studies was assessed using the Cochrane criteria (49).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [49] 49. The Cochrane Collaboration, 2008. (Available from www. cochrane-handbook.org).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

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

    Study design and conductnone given

    Identification of relevant abstracts, selection of studies, and data extraction were performed independently by two authors, with conflicts resolved by a third investigator.

    “The identification of relevant abstracts, the selection of studies based on the criteria described above, and the subsequent data extraction were performed independently by two of the authors (G Corona and G Rastrelli), and conflicts resolved by the third investigator (M Monami).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    Completed but unpublished trials were identified through clinicaltrials.gov and results obtained through formal request to authors when not available.

    “Completed but still unpublished trials were identified through a search of the www.clinicaltrials.govwebsite and the results, when not already available on the website, were obtained through a formal request to the authors.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    The beneficial effects of body weight loss are more apparent in younger, nondiabetic subjects with a greater degree of obesity; however, this could be due to a greater body weight loss.

    “The beneficial effects of body weight loss are more apparent in younger, nondiabetic subjects with a greater degree of obesity; however, this could be due to a greater body weight loss.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The Endocrine Society Guidelines and the Third International Consultation on Sexual Medicine emphasize that lifestyle modifications should be strongly encouraged in hypogonadal subjects with obesity, T2DM, and MetS.

    “In line with this data, the Endocrine Society Guidelines (62) and the Third International Consultation on Sexual Medicine (63) emphasized that lifestyle modifications should be strongly encouraged in hypogonadal subjects with obesity, T2DM, and the MetS.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [62] 62. Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, Montori VM, Task Force & Endocrine Society. Testosterone therapy in men with androgen deficiency syndromes: an Endocrine Society Clinical Practice Guideline. Journal of Clinical Endocrinology and Metabolism 2010 95 2536-2559. (doi:10.1210/jc.2009-2354) source
    • cites [63] 63. Buvat J, Maggi M, Gooren L, Guay AT, Kaufman J, Morgentaler A, Schulman C, Tan HM, Torres LO, Yassin A et al. Endocrine aspects of male sexual dysfunctions. Journal of Sexual Medicine 2010 7 (4 Pt 2) 1627-1656. (doi:10.1111/j.1743-6109.2010.01780.x) source
  • May combine two claims.

    Premisecitation

    In an 18-week placebo-controlled RCT in obese patients with obstructive sleep apnea, the combination of TRT and lifestyle modifications improved insulin sensitivity, reduced liver fat, and increased muscle mass compared with placebo and lifestyle modifications alone.

    “Similarly, an 18-week, placebocontrolled RCT in obese patients with obstructive sleep apnea demonstrated that the combination of TRT and lifestyle modifications improved insulin sensitivity, reduced liver fat, and increased muscle mass in comparison with placebo and lifestyle modifications alone (69).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [69] 69. Hoyos CM, Yee BJ, Phillips CL, Machan EA, Grunstein RR & Liu PY. Body compositional and cardiometabolic effects of testosterone therapy in obese men with severe obstructive sleep apnea: a randomised placebo-controlled trial. European Journal of Endo- crinology 2012 167 531-541. (doi:10.1530/EJE-12-0525) source
  • May combine two claims.

    Premisecitation

    Testosterone deficiency induces increased adiposity while increased adiposity induces hypogonadism.

    “Evidence indicates that testosterone deficiency induces increased adiposity while increased adiposity induces hypogonadism (22,25).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [22] 22. Corona G, Mannucci E, Forti G & Maggi M. Following the common association between testosterone deficiency and diabetes mellitus, can testosterone be regarded as a new therapy for diabetes? International Journal of Andrology 2009 32 431-441. (doi:10.1111/j.1365-2605.2009.00965.x) source
    • cites [25] 25. Stanik S, Dornfeld LP, Maxwell MH, Viosca SP & Korenman SG. The effect of weight loss on reproductive hormones in obese men. Journal of Clinical Endocrinology and Metabolism 1981 53 828-832. (doi:10.1210/jcem-53-4-828) source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    A weekly low dose (2.5 mg) of the aromatase inhibitor letrozole can restore testosterone levels and increase LH levels in severely obese hypogonadal men.

    “Accordingly, it has been reported that a weekly low dose (2.5 mg) of the aromatase inhibitor letrozole can restore testosterone levels and increase LH levels in severely obese hypogonadal men (57).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [57] 57. Loves S, Ruinemans-Koerts J & de Boer H. Letrozole once a week normalizes serum testosterone in obesity-related male hypogonad- ism. European Journal of Endocrinology 2008 158 741-747. (doi:10.1530/EJE-07-0663) source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Hormonal assays and reference values were not often comparable across studies.

    “First, hormonal assays and reference values were not often comparable.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Weight reduction is associated with increased insulin sensitivity, with insulin having a permissive role on GnRH neuron activity.

    “An alternative possibility is that weight reduction is associated with increased insulin sensitivity, with insulin having a permissive role on GnRH neuron activity (59).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [59] 59. Burcelin R, Thorens B, Glauser M, Gaillard RC & Pralong FP. Gonadotropin-releasing hormone secretion from hypothalamic neurons: stimulation by insulin and potentiation by leptin. Endocrinology 2003 144 4484-4491. (doi:10.1210/en.2003-0457) source
19 of 19
  • The paper relies on this without support.

    Most studies that did not describe P values reported a non-significant difference across groups.

    “Given that most of the studies that did not describe P values reported a non-significant difference across groups, the mean (paired) analysis, which excludes these data, is likely to overestimate the effect of treatments.”
  • The paper relies on this without support.

    Obesity is characterized by a relative abundance of estrogens because P450 aromatase is highly expressed by fat tissue.

    “Obesity is characterized by a relative abundance of estrogens since P450 aromatase is highly expressed by fat tissue.”
  • The paper relies on this without support.

    Male hypogonadism is one of the many adverse consequences of overweight and obesity.

    “Male hypogonadism can be considered as one of the many adverse consequences of overweight and obesity.”
3 of 3

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?

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.

  • Estradiol result differs from its figure

    Major

    The text reports a pooled estradiol change of −8.87 pmol/l, whereas the final estimate in Figure 4A is −6.54 pg/ml. The estimates and confidence intervals cannot be reconciled by a single change of units.

  • BMI-regression intercept is not centered in its confidence interval

    Minor

    The BMI plot prints an intercept of −12.58 with confidence limits of −14.76 and +10.39. Those limits have a midpoint of −2.185, suggesting that a minus sign is missing from the upper limit.

    Reported -12.58 · recomputed -2.185

  • LH pooled estimate differs from Figure 5A

    Minor

    The text gives the LH increase as 1.31 U/l with a 0.80-1.82 interval. Figure 5A's final LH estimate is 1.33 U/l with a 0.75-1.91 interval.

3 of 3

Cites

Flagged first, then by citations

Research works printed but not linked: 6

  1. 2010, JOURNAL OF SEXUAL MEDICINE, 1, 1362
  2. 2007, BMJ, 334, 29912
  3. Corona, 2011, Journal of endocrinological investigation, 34, 557
  4. 2011, JOURNAL OF SEXUAL MEDICINE, 10, 2868
  5. 2009, Journal of the American College of Surgeons, 35, S22
  6. 2012, Obesity surgery : the official journal of the American Society for Bariatric Surgery and of the Obesity Surgery Society of Australia and New Zealand, 23, 167

Cited by

Sorted by citations

Authors
Corona, G., Rastrelli, G., Monami, M., Saad, F., Luconi, M., Lucchese, M., Facchiano, E., Sforza, A., Forti, G., Mannucci, E., & Maggi, M.
Affiliations
  • Azienda USL di Bologna (IT)
  • University of Florence (IT)
  • Azienda Ospedaliero-Universitaria Careggi (IT)
Corresponding author
Maggi, Mario
Venue
European Journal of Endocrinology
Published
2013-06
Volume
168
Issue
6
Pages
829-843
ISSN
  • 0804-4643 (ISSN-L)
  • 1479-683X
OpenAlex
W2102933102
Cited by
414
References
72
Citations by year
2026: 19 · 2025: 29 · 2024: 22 · 2023: 33 · 2022: 40 · 2021: 34 · 2020: 30 · 2019: 33 · 2018: 38 · 2017: 29 · 2016: 20 · 2015: 37 · 2014: 35 · 2013: 14
FWCI
5.18
Type
journal article
Language
en
Open access
Locations
  • European Journal of Endocrinology (publishedVersion)
  • PubMed (publishedVersion)
  • Florence Research (University of Florence) (submittedVersion)
Topics
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
  • Health Sciences › Medicine › Surgery › Bariatric Surgery and Outcomes
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords
obesity, hypogonadotropic hypogonadism, testosterone, weight loss, bariatric surgery, hypocaloric diet, sex hormone-binding globulin, estradiol, gonadotropins, morbid obesity, men
MeSH terms
Body Weight, Humans, Hypogonadism, Obesity, Weight Loss

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