Hypogonadism and Subnormal Total Testosterone Levels in Men with Type 2 Diabetes Mellitus

Abstract

To determine the frequency of testosterone deficiency syndrome (TDS) in men with type 2 diabetes mellitus (DM).
A cross-sectional study.
The Gbagada General Hospital, Gbagada Lagos, Nigeria, from December 2009 to May 2010.
A total of 203 men with type 2 DM aged 30-86 years were evaluated for TDS by a combination of positive ADAM (androgen deficiency in the ageing male) scores and subnormal total testosterone levels. Mild testosterone deficiency referred to total testosterone (TT) levels of 8-12 nmol/L with symptoms of hypogonadism and severe testosterone deficiency referred to TT levels < 8 nmol/L with or without hypogonadal symptoms.
Mild and severe TDS were present in 18.3% and 17% respectively of the study subjects. Commonly occurring clinical parameters of the TDS were erectile dysfunction and loss of libido, which were documented in 63% and 60% respectively in the study subjects. The majority of clinical features of the TDS were comparable in men with and without the TDS.
About a third of men with type 2 DM had the TDS. The majority of the symptoms of hypogonadism are largely non-specific and their occurrence is comparable in men with and without low testosterone levels; thus, underscoring the need to have testosterone levels determined in men presenting with such symptoms.

Full text

146 Journal of the College of Physicians and Surgeons Pakistan 2011, Vol. 21 (9): 0
INTRODUCTION
Diabetes mellitus (DM) is one of the most prevalent non-
communicable diseases in Nigeria with a reported
prevalence rate of 2.2%.1It is also one of the
commonest reasons for medical admissions and deaths
in Nigerian hospitals.2,3 Reports abound in literature on
the relationship between plasma testosterone and
type 2 DM. Testosterone levels are not only lower in men
with type 2 DM, but also that the risk of developing
type 2 DM is increased in men with low testosterone
levels.4-5 Testosterone deficiency syndrome (TDS) or
symptomatic hypogonadism is an entity characterized
by clinical symptoms and biochemical parameters of
testosterone deficiency.6The prevalence rate of
symptomatic hypogonadism in men with type 2 DM is
high and documented rates range from 20-64% with
higher prevalence rates reported in the elderly.7Some of
the clinical features of the TDS include diminished
sexual function, changes in mood, decreased
intellectual activity, fatigue, sleep disturbance, increased
abdominal fat, decreased body hair and bone mineral
density. The commonly documented feature of the TDS
in men with DM is erectile dysfunction (ED); it is reported
to be three times higher in men with DM than in those
without DM.8In a report from United Kingdom (UK),9
20% and 31% of men with type 2 DM had total
testosterone below 8 nmol/L and 12 nmol/L respectively.
In an Asian report,10 the prevalence of hypogonadism in
men with type 2 DM aged between 28 and 80 years was
reported to be 43%. In the same report, the prevalence
ABSTRACT
Objective: To determine the frequency of testosterone deficiency syndrome (TDS) in men with type 2 (DM).
Study Design: A cross-sectional study.
Place and Duration of Study: The Gbagada General Hospital, Gbagada Lagos, Nigeria, from December 2009 to May
2010.
Methodology: A total of 203 men with type 2 DM aged 30-86 years were evaluated for TDS by a combination of positive
ADAM (androgen deficiency in the ageing male) scores and subnormal total testosterone levels. Mild testosterone
deficiency referred to total testosterone (TT) levels of 8-12 nmol/L with symptoms of hypogonadism and severe
testosterone deficiency referred to TT levels < 8 nmol/L with or without hypogonadal symptoms.
Results: Mild and severe TDS were present in 18.3% and 17% respectively of the study subjects. Commonly occurring
clinical parameters of the TDS were erectile dysfunction and loss of libido which were documented in 63% and 60%
respectively in the study subjects. The majority of clinical features of the TDS were comparable in men with and without
the TDS.
Conclusion: About a third of men with type 2 DM had the TDS. The majority of the symptoms of hypogonadism are largely
non-specific and their occurrence is comparable in men with and without low testosterone levels; thus, underscoring the
need to have testosterone levels determined in men presenting with such symptoms.
Key words: Hypogonadism. Type 2 diabetes mellitus. Total testosterone levels. Prevalence.
1Department of Internal Medicine, Lagos State University
Teaching Hospital, Ikeja Lagos, Nigeria.
2Department of Medicine, University of Port-Harcourt Teaching
Hospital, Port-Harcourt, Nigeria.
3Department of Internal Medicine, Lagos University Teaching
Hospital, Idi-araba, Lagos, Nigeria.
4Department of Chemical Pathology, General Hospital, Lagos
Island, Lagos, Nigeria.
Correspondence: Dr. Ogbera Anthonia Okeoghene,
Department of Internal Medicine, Lagos State University
Teaching Hospital, Ikeja Lagos, Nigeria.
E-mail: oogbera@yahoo.co.uk
Received December 01, 2010; accepted July 30, 2011.
Hypogonadism and Subnormal Total Testosterone Levels in
Men with Type 2 Diabetes Mellitus
Ogbera Anthonia Okeoghene1, Chinenye Sonny2, Fasanmade Olufemi3and Ajala Wale4
ORIGINAL ARTICLE
7196/OA/10
Q3/21/10

of hypogonadism was noted to have increased from
63% among participants aged 30 through 39 years to
89% in participants aged 80 years and above.10
TDS is largely understudied in sub-Saharan Africa. It is
imperative to note that the most widely accepted
parameters to establish the presence of hypogonadism
are the measurements of total testosterone and free
testosterone calculated from measured total
testosterone and SHBG or measured by a reliable free
testosterone dialysis method. However, in a resource-
poor endocrine practice, the facilities for measuring
SHBG and free testosterone dialysis are unavailable.11
The aim of this study was the determination of the
pattern and the frequency of occurrence of hypogonadal
symptoms and sub-optimal testosterone levels in a clinic
population of men with type 2 DM.
METHODOLOGY
This was a descriptive study involving 203 men with type
2 DM aged 30-86 years receiving care at a DM Clinic in
Lagos, Nigeria. Ethical consent was obtained from the
Hospital authorities and the study subjects gave
informed written consent. This work was carried out
from December 2009 to May 2010 in accordance with
the ethical standards as stated by the Helsinki
Declaration of 1983.
Exclusion criteria were prior / present treatment for
hypogonadism with testosterone replacement or anti-
androgens, documented history of prostate or testicular
cancer, history of inflammatory diseases or acute
infections and illnesses warranting hospitalization.
Demographic data, data pertaining to DM and
hypertension, smoking and alcohol ingestion were
documented. The ADAM questionnaire was used for
obtaining information pertaining to features of
hypogonadism.12 Other findings documented from
clinical examination included body mass index (BMI)
and waist circumference measurements. The waist
circumference measurement was determined by
applying a measuring tape to the midpoint between the
inferior margin of the last rib and the crest of the ilium.
Biochemical data were obtained for blood glucose and
total testosterone (TT) determinations. Venous blood
samples were collected in a fasting state before 10 a.m.
in the morning for the analysis of the aforestated
biochemical parameters. Blood glucose analysis was
done using the glucose oxidase method. The intra and
inter-assay coefficient of variation for glucose were
3.45% and 1.33%. respectively. TT estimation was
carried out by an enzyme immunoassay technique
which is a one-step technique that utilized equal
molecular antigen-antibody on microplate wells.
Samples of blood were centrifuged and supernants
stored at 20°C to ensure pre-analytical uniformity of
assay. All assays were done in duplications. The
absorbance values of each calibrator controls and test
samples duplicate were calculated and concentration of
calibrations plotted against their respective absorbance
and the values of samples concentrations read off the
graph.
The mean detectable concentration (analytical
sensitivity) was 0.2 nmol/l; assay dynamic range
0-40 nmol/l; inter-assay precision CV 4.95%; intra assay
precision was 6.8%.
Testosterone deficiency syndrome or symptomatic
hypogonadism defined a combination of clinical
symptoms and biochemical evidence of testosterone
deficiency. Mild TDS referred to TT of 8-12 nmol/L with
symptoms of hypogonadism or levels of < 8 nmol/L with
or without symptoms of hypogonadism.11 The clinical
symptoms of hypogonadism were said to be present if
there was a positive answer to question 1, or 7 or more
than 3 other questions.12 Obesity referred to a BMI of
≥30 kg/m2.
Journal of the College of Physicians and Surgeons Pakistan 147
Hypogonadism and subnormal total testosterone in diabetes

Statistical analysis was carried out on SPSS 17.
Continuous variables were expressed as means and
standard deviation (SD). Testosterone levels were
expressed as quartiles. The baseline differences
between men with mild, severe and normal testosterone
levels were determined with analysis of variance
(ANOVA) and chi-square. Clinical and biochemical
parameters were compared between men with and
without ED using the Mann-Whitney U test. P-values of
< 0.05 were considered statistically significant.
RESULTS
The mean age of the study subjects was 61.4 years and
the majority of them were on oral hypoglycaemic agents.
These results are shown in Table I.
Smoking and alcohol consumption were documented in
51 (25%) and 78 (38%) of the study subjects
respectively. History of hypertension was recorded in
97 (47%).
The mean (SD) testosterone level was 17 + 9.2 nmol/L
and the range was 0.2-37.5 nmol/L. The quartiles of
testosterone levels showed the values of testosterone at
25, 50 and 75 percentiles are 10.6 nmol/L, 15.7 nmol/L
and 22.6 nmol/L respectively. The distribution of various
cadre of testosterone levels showed that 36% of the
study subjects had symptomatic hypogonadism of which
17.7% and 18.3% had severe and mild testosterone
deficiency respectively. All the subjects with subnormal
testosterone levels had diagnostic clinical parameters of
hypogonadism. The commonly documented features of
hypogonadism included erectile dysfunction and
reduced libido. Reduced bodily hair and increased
sweating were documented in 11 (5%) and 23 (11%)
respectively of the study subjects. The proportion of
subjects with reduced bodily hair was significantly
higher in those with testosterone deficiency compared
with those of normal testosterone levels {9 (12.3%)
vs. 2 (1.5%), p=0.0001}. Increased sweating was noted
more, in subjects with testosterone deficiency compared
with men without hypogonadism and this difference was
statistically significant {13 (18%) vs. 10 (8%), p=0.02}. A
comparison of the frequency of occurrence of the TDS
parameters using the ADAM questionnaire in the
148 Journal of the College of Physicians and Surgeons Pakistan
Ogbera Anthonia Okeoghene, Chinenye Sonny, Fasanmade Olufemi and Ajala Wale
Table I: Baseline characteristics of the study subjects.
Parameters Value Range
Age (years) 61.4 + 11.2 30-85
BMI (kg/m2) 26.1 + 5.7 15.3-42.9
Duration of DM (years) 7.2 + 6.9 0.1-30
WC (cm) 91.4 + 12.2 66-132
Marital status
Married 177 (95.7%)
Divorced 2 (1.1%)
Widowed 4 (3.2%)
Glucose lowering medications (n)
Oral hypoglycemics (OHA) 166 (82%)
Combination of insulin and OHA 22 (11%)
Insulin 15 (7%)
Table II: Comparison of the clinical features of TDS in subjects with
normal and subnormal testosterone levels.
TDS parameter All subjects TT deficiency Normal TT p-value
203 (%) 73 (%) 130 (%)
Reduced libido 122 (60%) 60 (82%) 62 (48%) < 0.001
Lack of energy 79 (39%) 36 (49%) 43 (33%) 0.02
Decreased stamina 75 (37%) 32 (44%) 43 (33%) 0.1
Loss of height 14 (7%) 7 (10%) 7 (5.4%) 0.2
Decreased “enjoyment of life” 21 (10%) 10 (14%) 11 (8.5%) 0.2
Feeling sad and grumpy 19 (9%) 10 (14%) 8 (6%) 0.07
Weak erection 128 (63%) 49 (67%) 79 (61%) 0.3
Reduced exercise 88 (43%) 35 (48%) 53 (41%) 0.3
Falling asleep after dinner 59 (29%) 25 (34%) 34 (26%) 0.223
Reduced work performance 30 (15%) 15 (21%) 15 (12%) 0.08
Table III:Comparison of some clinical and biochemical profile of
subjects with and without symptomatic hypogonadism.
Variables Normal status Mild hypogo- Severe hypo- p-value
(130) nadism (38) gonadism (35)
Age (years) 61 (10.7) 64.6 (12) 60 (10.7) 0.140
BMI (kg/m2) 26.1 (5) 26 (5.8) 27.6 (7.4) 0.347
WC (cm) 91.2 (11.8) 91.7 (11.2) 91.8 (14.9) 0.954
Testosterone (nmol/L) 22.1 (7.3) 10.6 ( 1) 5.1 (2) < 0.001
Table IV: Association of low testosterone levels with some clinical
parameters.
Clinical parameters TT > 12 nmol/L TT 8-12 nmol/L TT < 8 nmol/L p-value
Hypertension 59 (45%) 22 (60%) 13 (36%) 0.194
Obesity 22 (17%) 7 (19%) 13 (36%) 0.030
Central obesity 20 (15.4%) 7 (19%) 12 (33%) 0.041
Smoking history 24 (19%) 13 (35%) 14 (40%) 0.01
Alcohol history 41 (31.5%) 18 (49%) 19 (53%) 0.02
TT > 12 nmol/L (130) TT 8-12 nmol/L (38) TT < 8 nmol/L (35)

Journal of the College of Physicians and Surgeons Pakistan 149
subjects with normal testosterone and reduced
testosterone levels are shown 1 in Table II.
The highest frequency of occurrence of severe and mild
testosterone levels were noted in the eight and sixth
decades respectively. The stratification of the
prevalence of hypogonadism by age decades is shown
in Figure 1.
Using the one way ANOVA to compare continuous data
amongst the three cadre of testosterone levels, there
were no detected differences for the testosterone levels.
These results are shown in Table III.
Fasting plasma and 2 hours postprandial glucose levels
were checked for normality using the Kolmogorov-
Smirnov test and a p-value of < 0.0001 was obtained.
The Mann-Whiney U test was then used to compare the
medians of both parameters and the results showed that
both level were significant p=0.86 for FPG and p=0.94
for 2HPP both different in hypogonadal and non-
hypogonadal men.
However, a comparison of the presence of obesity,
central obesity, hypertension significant smoking and
alcohol histories by proportions showed some significant
associations. These results are shown in Table IV.
Thirty Nine (30%) of the subjects with ED had
subnormal testosterone levels and 25 (20%) of the
subjects with ED had discussed this problem with their
health care givers. Twelve (9%) subjects with ED
admitted this to be a source of problems between them
and their spouses/partners. Twelve (9%) subjects with
ED had used medications for their sexual dysfunction
and 5 (4%) had used phosphodiesterase 5 inhibitors.
Seven (5.5%) resorted to use of herbal therapies
provided by friends/neighbours.
TT levels were significantly lower in men with ED
compared with men without ED (37 vs. 138.5,
p=0.0001). All other studied clinical and biochemical
parameters (age, BMI, WC, duration of DM, FBS, 2HPP)
were comparable in both groups.
DISCUSSION
Male hypogonadism has been noted to occur frequently
in type 2 DM 12-13. This report demonstrated that a
third of Nigerian men with type 2 DM had TDS. The
frequency of occurrence of the TDS in this report is
comparable to that from a UK study9but lower than the
prevalence rates documented in an Asian report.11
The symptoms of TDS are often non-specific. Save for a
reduction in libido and reduction in strength, the
presence of other TDS symptoms assessed by the
ADAM questionnaire was comparable in the subjects
with normal and subnormal testosterone levels.
Therefore, we cannot conclude that the ADAM
questionnaire is completely valid for the assessment of
the clinical symptoms of hypogonadism in Nigerian men
with type 2 DM. As reported elsewhere,14 ED was a
common complaint in the study subjects and with
reduced libido, were the prevalent clinical features of the
TDS. Reported prevalence rates of ED in DM range
from to 30-90%.15,16 Some features of the TDS not
included in the ADAMS questionnaire, but which were
found to be of significance in this report was reduction in
bodily hair, the decreased need to shave and increased
sweating. The proportion of subjects with histories of
Hypogonadism and subnormal total testosterone in diabetes
Figure 1: The frequency of occurrence of hypogonadism by age decades.

reduced need to shave and increased sweating was
significantly higher in those with subnormal testosterone
levels when compared with those with normal
testosterone levels. In the Nigerian context, there might
be a need to incorporate these TDS defining parameters
in studies addressing male hypogonadism.
The findings support the role of testosterone in the
maintenance of male sexual functioning. There was a
significant difference in testosterone levels between
subjects with ED and those without ED and in a third of
the subjects with ED, testosterone deficiency was a
potential contributory factor. Bodie et al. found that 18%
of men with ED had subnormal testosterone levels.17
Studies have shown that circulating androgens are not
only important mediators of the erectile process,
regulating arterial flow and vasodilation, but also
stimulate the central mechanism of sexual activity.6,18
The median testosterone level in this report was
15.7 nmol/L and the prevalence rates of mild and severe
TDS was18.3% and 17.7% respectively. Kapoor et al.
reported the prevalence rates of mild and severe TDS to
be 17% and 25 % respectively when total testosterone
was estimated.9It is pertinent to note that sex hormone
binding globulin (SHBG) which accounts for 60-80% of
testosterone binding rises with age and may serve as a
confounding factor when total testosterone is used
solely in the evaluation of testosterone levels. Low
levels of SHBG on the other hand may occur in the
presence of insulin resistance; thus, resulting in low total
testosterone levels. In the absence of the assessment of
bioavailable testosterone levels, the degree to which
this confounder- SHBG- affected our results if at all is
difficult to speculate on. However in the above study, the
prevalence rates of mild and severe TDS using
bioavailable testosterone assessments were found to be
comparable to those obtained using total testosterone
levels.9
Although the increase in the frequency of occurrence of
the TDS from age 60 through 69 to 80 years and above,
there was no significant difference in the mean age of
the subjects with normal, mild and severe TDS.
Significant associations were found between obesity,
smoking and alcohol histories and subnormal
testosterone levels. Kapoor et al. had reported significant
associations of low testosterone levels with not only
obesity, but also with visceral adiposity.9
Testosterone replacement not surprisingly has been
shown to decrease visceral fat mass, increase lean
body mass as well as improve insulin sensitivity which is
negatively affected in the presence of visceral adiposity.
Hypertension, a frequently occurring co-morbidity in
Nigerians with DM3was noted in 47% of the study
subjects. We could not assess the influence of
hypertension on testosterone levels but we report
comparable mean levels of testosterone in subjects with
and those without hypertension. The presence of ED
was also comparable in subjects with and without
hypertension. Kapoor et al.9also reported a lack of
significant association between hypertension and
testosterone levels. Although we have not showed a
clear relationship between the presence of hypertension
and male sexual dysfunction, one may safely infer that
the presence of hypertension is unlikely to have a
bearing or strong influence on sexual functioning in men
with DM if at all. Conversely, a study in men with DM
found no effect of testosterone replacement of blood
pressure readings.19
Sexual dysfunction is not an often discussed problem in
our practice. From the present results it is observed that
only a fifth of people with ED discussed this problem
with their doctor. There results also show gross under
treatment of this disorder which is noted to cause friction
between partners in 9% of people who have the
problem.
Journal of the College of Physicians and Surgeons Pakistan 150
Ogbera Anthonia Okeoghene, Chinenye Sonny, Fasanmade Olufemi and Ajala Wale

In this report, even though we did not have a control
group of non-diabetic men, it is pertinent to note that the
TDS have been documented more frequently in men
with DM than in non-diabetic men.20 In the Rancho
Bernardo study which involved 985 men aged 40-79
years (an age group comparable with study subjects).
110 men with Diabetes had lower total testosterone
levels and lower SHBG levels than did the non-diabetic
men, even after adjustment for BMI and age.20 In the
same report, 21% of diabetic men compared with 13%
of non-diabetic men had suboptimal testosterone
levels.20
Limitations of this study need to be mentioned. The
sample size was relatively small; largely due to technical
and financial constraints. Testosterone was not
measured by mass spectrometer technology because
this technique is not available in Nigeria. Measuring
bioavailable testosterone would have been ideal, but
this is not available in this practice hence, the report was
limited to the determination of total testosterone levels.
CONCLUSION
The prominent features of the testosterone deficiency
syndrome in Nigerian men with type 2 DM are loss of
libido and erectile dysfunction. This study has
demonstrated the importance of assessing testosterone
levels in men with clinical features of hypogonadism
because of the non-specificity of these clinical
parameters.
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