J Samavat and others Male hypogonadism and 171:5 555–560

Clinical Study bariatric surgery

Hypogonadism as an additional indication for

bariatric surgery in male morbid obesity?
Jinous Samavat, Enrico Facchiano1, Marcello Lucchese1, Gianni Forti,
Edoardo Mannucci2, Mario Maggi3 and Michaela Luconi
Correspondence
Endocrinology Unit, Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence, should be addressed
Italy, 1Bariatric and Metabolic Surgery, Careggi Hospital, 2Diabetes Agency, Azienda Ospedaliera-Universitaria to M Maggi
Careggi, Florence, Italy and 3Sexual Medicine and Andrology Unit, Department of Experimental and Clinical Email
Biomedical Sciences, University of Florence, Viale Pieraccini 6, 50139 Florence, Italy [Link]@[Link]

Abstract
Objective: Male obesity is often associated with reduced levels of circulating total (TT) and calculated free testosterone (cFT),
with normal/reduced gonadotropins. Bariatric surgery often improves sex steroid and sex hormone-binding globulin (SHBG)
levels. The aim of this study was to assess the effects of bariatric surgery on waist circumference (WC) and BMI, and on TT levels,
in morbidly obese men, stratified, according to the gonadal state, in eugonadal and hypogonadal (TT!8 nmol/l) subjects.
European Journal of Endocrinology

Design: A cohort of morbidly obese patients (29 with hypogonadism (HG) and 26 without) undergoing bariatric surgery
(37, 10, 6, and 2, with Roux-en-Y gastric bypass, laparoscopic adjustable gastric banding, biliopancreatic diversion and gastric
sleeve, respectively) was studied at 6 and 12 months from the operation.
Methods: Anthropometric parameters (weight, BMI, WC) and sex hormones (gonadotropins, TT, cFT, estradiol (E2), SHBG)
were assessed.
Results: WC was the only parameter significantly correlated with androgens, but not with E2, SHBG, and gonadotropins, at
baseline. After surgery, a significant increase in TT, cFT, and SHBG, accompanied by a decrease in E2, was evident in the two
groups. However, both TT and cFT, but not E2, SHBG, and gonadotropin variations, were significantly higher in the
hypogonadal group at follow-up, with an overall 93% complete recovery from HG. Reduction in WC, but not BMI, was
significantly greater in hypogonadal men (DWCZK29.4G21.6 vs K14.4G17.4 at 12 months, PZ0.047).
Conclusions: Recovery from obesity-associated HG is one of the beneficial effects of bariatric surgery in morbidly obese men.
The present findings suggest that the gonadal state is a predictor of WC decrease after bariatric surgery.

European Journal of
Endocrinology
(2014) 171, 555–560

Introduction
Obesity and its associated comorbidities have been diabetes (T2DM), which are significantly ameliorated after
exponentially increasing during the last 40 years, repre- the intervention (2, 3, 4).
senting a medical and socio-economic burden, not only Alterations in sex steroid hormones are often associ-
in industrialized, but also in developing countries (1). ated with male obesity. In particular, low circulating levels
Treatments for obesity include a wide range of interven- of total (TT) and free (FT) testosterone in the presence of
tions, such as dietary prescriptions, structured exercise, reduced gonadotropins, characterizing central secondary
lifestyle modification programs, specific drugs, and bar- hypogonadism (HG), with elevated estrogens, have been
iatric surgery. The currently recognized indications of described in male metabolic syndrome (5, 6). Obesity and
bariatric surgery are limited to morbid obesity, i.e. BMIO HG are linked in a vicious cycle, in which low testosterone
40 kg/m2, or BMIR35 kg/m2 associated with risky comor- favors weight gain, and adiposity induces HG (6, 7).
bidities, such as cardiovascular (CV) diseases and type 2 Interestingly, both obesity and HG are associated with

[Link] Ñ 2014 European Society of Endocrinology Published by Bioscientifica Ltd.

DOI: 10.1530/EJE-14-0596 Printed in Great Britain
 Clinical Study J Samavat and others Male hypogonadism and 171:5 556
bariatric surgery

increased all-cause and CV mortality (6, 8). Several studies University Hospital in Florence, Italy, between July 1,
demonstrated that weight loss and reduction in waist 2009 and June 30, 2011, who gave their consent
circumference (WC) induce an increase in testosterone were enrolled in the study, provided that they had a
levels. A recent meta-analysis (9) comparing bariatric BMI O40 kg/m2 and no history of present or past
surgery with lifestyle modifications programs has shown treatment for HG. The choice of surgery and type of
a greater recovery in TT and FT with the surgical approach, surgery was made by a team composed of a surgeon, an
probably due to a greater effect on body weight. On the endocrinologist, and a dietitian, depending on the
other hand, it is possible that androgen levels, in men, overall evaluation of the patient’s history. Among the
contribute to the regulation of body weight. Hypogonadal 55 patients studied, 37, 10, 6, 2, underwent Roux-en-Y
subjects, who have reduced muscle mass and lower gastric bypass (67%), laparoscopic adjustable gastric
muscular strength, could also have a reduced energy banding (18%), biliopancreatic diversion (11%), and
expenditure as described for aging males (10); in addition, gastric sleeve (4%), respectively.
androgens could play a role in the regulation of adipose In the prospective observation, pre-surgery baseline
tissue metabolism (11). evaluation (T0) was performed at hospital admission for
The aim of this study was to verify whether hypogo- bariatric surgery. The follow-up evaluation was performed
nadism (TT!8 nmol/l) modulates the effects of bariatric 6 (T1) and 12 (T2) months after surgery.
surgery on abdominal adiposity, body weight, and TT.

Biochemical and anthropometric measurements

Subjects and methods
European Journal of Endocrinology

i) Anthropometric measures: height, weight, and WC

Patients were measured for each subject at the three time
The clinic-based survey was performed on a consecutive points, according to the cohort.
series of morbidly obese (BMIO40 kg/m2) patients who were ii) Sex hormones: serum TT, estradiol (E2) follicle-stimu-
undergoing bariatric surgery at Careggi University Hospital lating hormone (FSH), luteinizing hormone (LH), and
in Florence (nZ55). All patients were enrolled for a sex hormone-binding globulin (SHBG) were measured
subsequent 6- and 12-month follow-up, after intervention. by immunoassay (Immulite 2000, M-Medical System,
The study was approved by the Local Ethical Committee and Milan, Italy) on a sample of venous blood drawn in the
Institutional Review Board (protocol number 83/13). All morning. The analytical sensitivity of the assays was
patients enrolled gave signed informed consent after 0.5 nmol/l for TT, 55 pmol/l for E2, 0.1 mIU/ml for FSH,
receiving written and oral information on the study. 0.05 mIU/ml for LH, and 0.02 nmol/l for SHBG. TT
measurement by immunoassay has been validated by
isotopic dilution-liquid chromatography–tandem
Study design
mass spectrometry method for values higher than
All male patients in the list for bariatric surgery at the nanomolar (12). Calculated free testosterone (cFT)
Metabolic and Bariatric Surgery Unit of Careggi was calculated as demonstrated previously (13).

Table 1 Anthropometric and sex steroid parameters before bariatric surgery in the obese cohort enrolled (nZ55). MeanGS.D.
values at baseline before surgery (T0) and at 6 (T1) and 12 months (T2) from surgery are indicated, as well as P significance between
the indicated time points after Student’s t-test for paired data. Significant P values are indicated in bold.

T0 (nZ55) T1 (nZ50) PT1KT0 T2 (nZ42) PT2KT0

Age (years) 42.3G11.6

BMI (kg/m2) 46.6G7.4 37.5G6.7 0.000 32.2G6.8 0.000
Weight (kg) 148.4G26.1 120.7G26.3 0.000 101.8G24.1 0.000
WC (cm) 140.1G18.0 121.5G17.1 0.000 113.6G16.6 0.000
TT (nmol/l) 9.02G4.71 14.77G6.35 0.000 14.6G6.0 0.000
cFT (nmol/l) 0.224G0.132 0.263G0.111 0.038 0.265G0.097 0.339
E2 (pmol/l) 139.6G49.5 135.6G52.7 0.347 126.7G44.9 0.007
SHBG (nmol/l) 21.7G8.9 42.3G19.7 0.000 42.2G20.0 0.000
FSH (mIU/ml) 4.03G2.56 5.59G3.00 0.000 6.21G3.90 0.000
LH (mIU/ml) 3.09G1.96 4.34G2.14 0.000 4.47G2.60 0.001

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 Clinical Study J Samavat and others Male hypogonadism and 171:5 557
bariatric surgery

Statistical analysis

Variation in anthropometrical and sex hormone parameters after bariatric surgery in the cohort of obese men stratified in hypogonadal and eugonadal by a

within groups at T1 (PDT1) and T2 (PDT2) between hypogonadal and eugonadal subjects is indicated (P between groups) at both T1 and T2, with P significant values in bold.
basal TTZ8-nM cutoff. MeanGS.D. variation in all parameters at 6 (DT1) and 12 (DT2) months after surgery is indicated. Statistical significance in parameter variations

P between groups

0.276
0.305
0.047
0.001
0.001
0.184
0.425
0.993
0.796
PDT2
Patients were included in the analysis when evaluations at
baseline and at least one follow-up were available. Para-
metric distribution of data was evaluated by Kolmogorov–

0.650
0.297
0.200
0.037
0.009
0.413
0.697
0.759
0.187
PDT1
Smirnov test. Data have been expressed as meanGS.D.
Correlations were performed using Spearman’s analysis.
Student’s t-test was used for comparisons of two sets of
paired or independent data, as appropriate. A P!0.05 value

0.000
0.000
0.011
0.342
0.148
0.011
0.000
0.025
0.022
PDT2
was used for statistical significance. Stepwise multiple linear
regression was applied for multivariate analysis. All statisti-
cal analyses were performed on SPSS 20.0 for Windows

Eugonadal (nZ26)

K0.052G0.157
(Statistical Package for the Social Sciences).

K41.2G29.5
K14.4G17.4
1.51G7.11

K35.3G57.3
18.9G19.9
2.35G4.43
1.61G2.98
K12.5G8.6
DT2 (nZ21)
Results
Among the 58 morbidly obese patients initially enrolled,
55 were available for analysis (nZ55, 1.2% dropout),

0.000
0.000
0.000
0.020
0.719
0.255
0.000
0.000
0.002
PDT1
having clinical data and blood sampling before surgery
(T0, nZ55) and at 6 (T1, nZ50, 10% dropout) and/or 12
European Journal of Endocrinology

(T2, nZ42, 24% dropout) months. In the sample analyzed,

the mean age was 42.3G11.6 years, and mean BMI was

K0.013G0.174
K28.7G13.4

3.56G7.26

K14.1G59.1
19.2G15.9
1.55G1.69
1.78G2.49
K9.6G4.8

K16.6G8.8
46.6G7.4 kg/m2. Among those patients, 37, 10, 6, and 2,

DT1 (nZ24)
underwent Roux-en-Y gastric bypass (67%), laparoscopic
adjustable gastric banding (18%), biliopancreatic diver-
sion (11%), and gastric sleeve (4%), respectively. Six
months after bariatric surgery, the decrease in adiposity
(reduction in BMI, weight, and WC) was associated with 0.000
0.000
0.000
0.000
0.002
0.271
0.000
0.013
0.022
PDT2

a significant increase in TT and SHBG and decrease in

estradiol (E2) levels, which were further maintained at
Hypogonadal (nZ29)

12 months (Table 1). cFT significantly increased at 0.251G0.097

6 months, but the significance was lost at 12 months

K51.6G35.0
K29.4G21.6
9.11G6.69

K12.6G51.1
24.0G21.1
2.36G3.85
1.39G2.57
DT2 (nZ21)

K15.6G9.4

(Table 1). Gonadotropins (FSH and LH) increased,

although not significantly, at both time points. When
patients were stratified according to the gonadal status at
baseline, in hypogonadal (nZ29) and eugonadal (nZ26)
subjects (cutoff TTZ8 nmol/l), a significant increase vs
0.000
0.000
0.000
0.000
0.000
0.910
0.000
0.000
0.002
PDT1

baseline was observed in both TT and cFT (Table 2), but

not in E2 (Table 2), SHBG, and gonadotropins, only in the
hypogonadal group (Fig. 1). Differences between hypogo-
K22.6G19.8
K22.3G16.7
7.52G5.57
0.164G0.08
K1.1G50.9
21.0G16.1
1.40G1.72
0.99G1.48

nadal and eugonadal patients in variations from baseline

K8.8G6.7
DT1 (nZ26)

were significant only for DTT and DcFT. No significant

differences between the two groups were observed in
either BMI or weight changes, but the mean variation in
WC was significantly higher in hypogonadal men at
12 months (Table 2). Receiver operating characteristics
SHBG (nmol/l)
FSH (mIU/ml)
Weight (kg)
BMI (kg/m )

(ROC) curve analysis was used to confirm the ability of the

LH (mIU/ml)
cFT (nmol/l)
2

TT (nmol/l)

E2 (pmol/l)

hypogonadal state (TT!8 nmol/l) to predict the WC

WC (cm)
Table 2

reduction at 12 months (Fig. 2). Hypogonadal condition

(TT!8 nmol/l), in fact, identified a WC decrease R23 cm,

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 Clinical Study J Samavat and others Male hypogonadism and 171:5 558
bariatric surgery

A B 0.50 C 70
24 Hypogonadal (n=29) Hypogonadal (n=29)
65 Hypogonadal (n=29)
22 Eugonadal (n=25) 0.45 Eugonadal (n=25)
60 Eugonadal (n=25)
20 55
0.40
18 50 d d
0.35

SHBG (nmol/l)
16 45

cFT (nmol/l)
TT (nmol/l)

a 40
14 0.30 a
a 35
12 0.25 a
a 30
10 a 25
0.20
8 20
0.15 **
6 ** 15 *
4 10
0.10
2 5
0.05 0
T0 T1 T2 T0 T1 T2 T0 T1 T2

D 250 E 12 F 9
Hypogonadal (n=29) Hypogonadal (n=29) Hypogonadal (n=29)
Eugonadal (n=25)
11 Eugonadal (n=25) 8 Eugonadal (n=25)
225
10
200 9 7
8 6

FSH (mIU/ml)

LH (mIU/ml)
175 d f
E2 (pmol/l)

7 e 5
d
150 6
5 4
125 * e b c
4 3 a
a
100 3 2
2
75 1
1
50 0 0
T0 T1 T2 T0 T1 T2 T0 T1 T2

G 70 H 190 I 160
Hypogonadal (n=29) Hypogonadal (n=29) Hypogonadal (n=29)
65 Eugonadal (n=25)
180 Eugonadal (n=25) Eugonadal (n=25)
170 150
60 *
160
55 140
150
BMI (kg/m2)

Weight (kg)

a
European Journal of Endocrinology

Waist (cm)
50 a 140 a 130
45 130
40 a 120 120 f
a
110 d d
35 d 110 a
100
30 d d
90 100
25 80
20 70 90
T0 T1 T2 T0 T1 T2 T0 T1 T2

Figure 1
Variation in anthropometric and sex hormone parameters after surgery (T0) and at 6 (T1) and 12 (T2) months of follow-up.
bariatric surgery in the cohort of morbidly obese men stratified Statistical significance: *P!0.05 and **P!0.0001 between
a
in hypogonadal and eugonadal by a basal TTZ8 nmol/l cut-off. hypogonadal and eugonadal at T0; vs T0 in each group: and
d b e c f
MeanGS.D. values of all parameters (A: TT, B: cFT, C: SHBG, D: E2, P!0.0001, and P!0.01, and P!0.05, in hypogonadal
E: FSH, F: LH, G: BMI, H: weight, I: waist) at baseline before and eugonadal respectively.

with an accuracy (area under the ROC curve) of 71.2G A strong positive correlation was found at baseline
9.9% (P!0.05), with a 67% sensitivity and 71% specificity. between BMI and WC in hypogonadal subjects (rZ0.811,
E2 significantly decreased at 12 months, only in the P!0.0001, nZ29), which was still significant but weaker in
eugonadal group (Fig. 1 and Table 2). eugonadal subjects (rZ0.465, PZ0.045, nZ26). Conver-
Bariatric surgery resulted in a complete recovery from sely, the correlation was statistically significant between
HG (TT!8 nmol/l) in 93% of the hypogonadal subjects DBMI and DWC at 12 months from surgery in hypogona-
(27/29), already starting at 6 months from surgery (Fig. 1). dal (rZ0.864, R2Z0.747, P!0.0001, nZ21) subjects, but
No statistically significant differences were evident for not in eugonadal (rZ0.412, R2Z0.169, PZ0.144, nZ21)
baseline parameters between the two groups (BMI, weight, subjects. The relationship between 12-month DBMI (x) and
and gonadotropins) but for WC (P!0.05), TT and cFT DWC (y) was yZ2.132xC0.858 and yZ0.759xK4.556 in
(P!0.0001), SHBG, and E2 (P!0.05; Fig. 1 and Table 2). hypogonadal and eugonadal subjects respectively.
The distribution of the type of bariatric surgery was Among all parameters considered to define adiposity
similar between hypogonadal and eugonadal groups (BMI, weight, WC), only WC at baseline showed a
(data not shown), and the prevalence of T2DM was statistically significant correlation with androgens
5/29Z17% and 2/26Z8%, respectively, with no signifi- (rZK0.375, PZ0.013 and rZK0.411, PZ0.006 for TT and
cant differences. cFT respectively), but not with E2, SHBG, and gonadotropin

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 Clinical Study J Samavat and others Male hypogonadism and 171:5 559
bariatric surgery

1.0 Interestingly, baseline testosterone levels appear to

moderate the effect of bariatric surgery on sex hormone
∆WCT2 = –23 cm recovery. The previous works reported that BMI (9, 17) and
0.8 age (18) were among the best predictors of androgen
recovery after bariatric surgery. However, such cohorts of
morbidly obese patients included both hypogonadal and
0.6 eugonadal subjects. In this study, we show that HG is the
1-Sensitivity

best predictor of the decrease in WC after surgery. It can be

speculated that the rapid weight loss induced by bariatric
0.4 surgery eliminates disturbances in the regulation of
gonadotropin and androgen secretion determined by
excess adiposity, resulting in an improvement in testoster-
0.2 one levels in hypogonadal subjects. Conversely, in
patients who remain eugonadal despite morbid obesity,
feedback from appropriate levels of circulating testo-
0.0 sterone could prevent any further increase in androgen
0.0 0.2 0.4 0.6 0.8 1.0 secretion. It can also be observed that the role of E2 in
1-Specificity the determination of obesity-related hypogonadism could
be smaller than what has been previously hypothesized
(10, 21); in fact, E2 levels at baseline are lower in
European Journal of Endocrinology

Figure 2
Hypogonadal condition predicts WC reduction at 12 months
hypogonadal subjects compared with eugonadal subjects.
from surgery. The receiver operating characteristics (ROC) curve
In addition, in eugonadal subjects, the reduction in E2
shows that baseline hypogonadism (TT!8 nmol/l) identifies
determined by surgery does not produce an increase in
a reduction in waist circumference greater than K23 cm
testosterone, whereas recovery of hypogonadism occurs
(indicated by the arrow, DWCT2) at 12 months from surgery with
without any significant increase in E2 levels.
an accuracy (area under the ROC curve) of 71% (P!0.05), a 67%
At enrolment, WC was higher in hypogonadal than in
sensitivity, and 71% specificity. The ROC curve was constructed
eugonadal patients, despite a similar BMI. This confirms
by plotting the sensitivity (true positive) vs the false positive rate
that WC is one of the major predictors of obesity-
(1-specificity) for different DWC values at 12 months from surgery.
associated hypogonadism (6, 9), suggesting that abdomi-
nal fat has a greater impact on the regulation of sex
levels (not shown). Such negative correlations remained hormone secretion than peripheral fat.
statistically significant, even after adjustment for age as a Interestingly, the reduction in WC in patients with
further confounding factor (adj. rZ0.373, PZ0.013 and hypogonadism was more pronounced than that observed
adj. rZK0.400, PZ0.008 for TT and cFT respectively). for eugonadal subjects with a similar weight loss,
suggesting that bariatric surgery could have a specific
effect on abdominal adiposity in hypogonadal subjects.
Discussion
It can be speculated that the improvement in testosterone
Bariatric surgery has been extensively described to levels induced by bariatric surgery, which is greater in
ameliorate sex hormone and SHBG levels in morbidly hypogonadal patients, contributes, to a greater extent in
obese patients (9, 14, 15, 16, 17, 18, 19), with an effect that those subjects, to the preservation of lean mass, resulting
may exceed what is predictable on the basis of weight loss in a greater reduction in abdominal adiposity. Unfortu-
(17). In this study, we demonstrate that the increase in nately, no measures of body composition were available in
androgens (cFT and TT) occurs only in hypogonadal this study. Further limitations were the absence of insulin
patients (TT!8 nmol/l). Conversely, estrogen levels, sensitivity and glycemic parameters at baseline and
which were significantly lower before surgery in hypogo- follow-up, and the variety of surgery procedure used,
nadal individuals, significantly decreased in eugonadal which did not allow a subgroup analysis for type of
patients only. Remarkably, bariatric surgery resulted in an intervention. Moreover, 89% (49/55) of the patients
almost complete and rapid recovery of HG, even starting undergoing bariatric surgery had BMI R40 kg/m2. Further
at 6 months from surgery, similarly to what was found for studies carried out on subjects with BMI between
T2DM recovery (20). 35 and 40 kg/m2 are necessary to evaluate whether

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 Clinical Study J Samavat and others Male hypogonadism and 171:5 560
bariatric surgery

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Dr E Mannucci has received: consultancy fees from Novo Nordisk, Eli Lilly, 12 Huhtaniemi IT, Tajar A, Lee DM, O’Neill TW, Finn JD, Bartfai G,
AstraZeneca, and GSK; speaking fees from Novo Nordisk, Eli Lilly, Boonen S, Casanueva FF, Giwercman A, Han TS et al. Comparison of
AstraZeneca, and Sanofi; research grants from Novo Nordisk, Eli Lilly, and serum testosterone and estradiol measurements in 3174 European men
AstraZeneca. Prof. M Maggi has received consultancy fees or research using platform immunoassay and mass spectrometry; relevance for the
grants from Eli Lilly, Bayer, and Prostrakan. The other authors have no diagnostics in aging men. European Journal of Endocrinology 2012 66
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simple methods for the estimation of free testosterone in serum.
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Received 16 July 2014

Accepted 6 August 2014

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