International Journal of Impotence Research (2002) 14, Suppl 1, S93S98

2002 Nature Publishing Group All rights reserved 0955-9930/02 $25.00

www.nature.com/ijir

Male andropause: myth, reality, and treatment

E Wespes1* and CC Schulman2
1

Department of Urology, C.H.U. de Charleroi, Charleroi, Belgium; and 2Erasme Hospital, Brussels, Belgium
A progressive decrease in androgen production is common in aging men. The physiological causes
for this phenomenon seem to be multifactorial. The magnitude of the decline in testosterone with
age and the prevalence of older men with low testosterone levels have not been well established.
The extent to which an age-dependent decline in androgen levels leads to health problems that
might affect or alter the quality of life remains under debate. In men older than middle age, total
testosterone levels may be misleading because of an increase in sex hormone-binding globulin
levels. The mechanism of the age-associated decrease of the endocrine testicular function is also
essentially due to primary testicular failure, but important changes occur at the hypothalamopituitary level. The most prominent endocrinological alterations with aging are related to the sex
steroids, but others, such as growth hormone, melatonin cortisol, and thyroxine, are also affected.
The clinical picture of andropause syndrome is characterized by diminished sexual desire and
erectile capacity, decrease in intellectual activity, fatigue, depression, decrease in lean body mass,
skin alterations, decrease in body hair, decrease in bone mineral density that results in
osteoporosis, and increase in visceral fat and obesity. Current medical treatments for androgen
supplementation include oral tablets, intramuscular injections, and scrotal and nonscrotal
patches. Unfortunately, none of these preparations mimic the circadian rhythm, even if some of
them may approximate the circadian rhythm by dose adjustments. Moreover, the androgen
supplementation could have adverse effects on different organs, namely, the liver, lipid profile,
cardiovascular disease, prostate, sleep disorders, and emotional behavior. Clinical response is a
better guide to dose requirements, regardless of serum testosterone levels. This important field
must be actively investigated by the medical, behavioral, and social sciences.
International Journal of Impotence Research (2002) 14, Suppl 1, S93S98. DOI: 10.1038=
sj=ijir=3900798
Keywords: erectile dysfunction; male andropause; androgen; testosterone

Introduction
Many investigations suggest that aging men experience reductions in androgen levels, virility, and
fertility, along with related metabolic changes.
Nonetheless, the question of andropause remains
controversial, in part because of the difficulty in
discriminating the effects of age-related confounding variables, such as stress, nonendocrine illnesses,
malnutrition, obesity, and drug or medication use,
from aging per se, on the other hand.
The reproductive changes that occur in the aging
male are more subtle than the profound modifications in gonadal function that occur in women.
The term male menopause or andropause should
not be used.

*Correspondence: E Wespes, Department of Urology, C.H.U.

de Charleroi, Bld Paul Janson 92, 6000 Charleroi, Belgium.
E-mail: dr.wespes@skynet.be

Modifications of testosterone levels in diseases and

lifestyle
Acute critical illness1,2 or surgical injury3 cause a
profound, generally transient, decrease of free
testosterone ([F]T) levels.
As far as chronic diseases are concerned, decreased testosterone and sex hormone-binding globulin (SHBG) levels are observed in elderly men
with diabetes mellitus, with an inverse correlation
between testosterone and plasma glucose.4
Coronary atherosclerosis has been reported to be
associated with low testosterone levels.5
Chronic renal failure generally induces a hypogonadotropic hypogonadism with impaired pulsatile release of pituitary luteinizing hormone (LH).6
Chronic liver disease is accompanied by decreased (F)T levels and increased SHBG.7
Sleep apnea syndrome, with its hypoxia, is accompanied by lowered testosterone levels, secondary to
a hypogonadotropism; these patients are often
obese, which may aggravate the hypogonadism.8

Male andropause
E Wespes and CC Schulman

S94

Among drugs that may adversely affect Leydig

cell function in the elderly, the frequently used
glucocorticoids, as long-term therapy, often induce a
marked suppression of (F)T levels as the result of
both testicular and central actions of the drug, as
well as a decrease of SHBG levels.9
Smokers have higher testosterone levels than
nonsmokers.10
Alcohol intake, even without cirrhosis of the
liver, may accentuate the age-associated decline of
testosterone levels.10
The influence of diet can influence testosterone
levels. Fasting may affect testosterone production through diminished gonadotropic testicular
control.10

ing growth hormone or insulin-like growth factor

level.16
The best parameter to determine hypogonadism is
measurement of bioavailable testosterone, which
includes free and albumin-bound fractions. In the
aging male, total testosterone may be misleading
due to alterations in SHBG and flattening of the
circadian rhythm. Serum testosterone assessment
should be done between 8 and 11 am. If the
testosterone level is below or at the lower limit, it
is prudent to confirm the results with a second
determination with assessment of LH and folliclestimulating hormone (FSH).

Aging effects on androgen target tissues

Androgen changes with normal male aging
The causes for a decline in testosterone production
with age are multifactorial. The most important
change appears in the testes, where there is a
decline and an alteration of Leydig cell number.11
Moreover, young adult men exhibit a circadian
rhythm in their serum levels of total testosterone,
with peak levels in the morning and falling slowly
by about 35% during the day. This daily fluctuation in serum testosterone is attenuated in older
men.12,13
The ability of the testes to increase testosterone
secretion in response to increased gonadotropin
stimulation is also attenuated in older men.14 There
is evidence that age-related alterations in hypothalamopituitary function also contribute to the decline
in testosterone production. Elderly men fail to
demonstrate an appropriate increase in LH secretion
in response to a hypoandrogenic state. Most older
men with low testosterone levels have gonadotropin
levels (especially LH levels) that are within the
normal range for young adult men, resulting in a
relative hypogonadotropic hypogonadism. It has
been also clearly demonstrated that the hypothalamopituitary compartment of the gonadal axis is
more sensitive to the negative feedback effects of sex
hormones than is the case in young adults.15
A third aspect of the physiopathological mechanisms responsible for the age-related changes in
circulating testosterone levels, in addition to primary testicular factors and deficient neuroendocrine
feedback regulation, consists of a progressive increase of plasma SHBG binding capacity.16 The
cause of this increase with age remains unclear. The
decreased testosterone levels per se are probably not
responsible for the increased SHBG levels; at the
latter, increase is observed at an earlier age than the
decrease of testosterone, whereas estradiol levels are
similar in young and elderly men. A plausible
hypothesis is that the increase in SHBG levels is
related to the age-dependent decline in circulatInternational Journal of Impotence Research

Aging might also reduce androgen effect by causing

a loss of sensitivity of target tissues to testosterone or
dihydrotestosterone (DHT). Both decreased and
increased sensitivity of pituitary gonadotropin secretion to feedback regulation by androgens has
been reported in older men. Binding of DHT to exhormone responsive skin is also decreased with age,
suggesting than an age-related reduction in responsivity to androgens may result from alterations in
receptor number or affinity.17

Clinical manifestations
Aging in men is generally accompanied by a
decrease in general wellbeing; changes in mood
with concomitant decrease in intellectual activity;
spatial orientation ability fatigue; depression and
anger; decrease in virility, sexual desire and erectile
quality; decrease in skin thickness; decrease in
energy; decrease in muscular mass and in strength;
an increase in upper- and central-body fat; decrease
in bone mineral density resulting in osteoporosis;
and decrease in body hair.18 20

Androgen supplementation in aging men

With the paucity of data both on the consequences
of the relative hypogonadism of the elderly and on
the effects of androgen replacement therapy, it
would certainly not be justified to propose a strategy
of systematic androgen supplementation in elderly
men presenting with only moderately decreased
plasma testosterone levels. Meanwhile, there are
probably also no reasons to withhold treatment for
selected patients with clinical and biochemical manifestation of hypogonadism, after careful
screening.

Male andropause
E Wespes and CC Schulman

Available preparation for testosterone substitution

Testosterone is not suited for oral treatment since it
undergoes near-total first-passage metabolization in
the liver and there is a considerable interindividual
variation in the testosterone plasma levels achieved
with relatively high plasma levels for dihydrotestosterone; moreover, adequate substitution requires
the intake of a dose of 40 80 mg two or three times
per day.21
Preparations of intramuscular injection have been
the most widely available preparations for testosterone substitution. Injection of 200 mg of testosterone
every 2 3 weeks results in supraphysiological
testosterone levels during the first days following
administration with thereafter a progressive decline
to subphysiological testosterone levels during the
days preceding the next injection.22
A gel formulation for percutaneous administration of dihydrotestosterone has been available for
many years; adequate substitution requires the
application of large doses to the skin.23
Patches for transdermal testosterone administration have been developed, aimed at achieving more
physiological profiles of plasma testosterone concentration.24 Daily patches applied to the shaved
scrotal skin can produce plasma testosterone levels
around mid-normal values 4 to 8 h following
application, with progressive decline of the testosterone levels in the subsequent hours. The more
recently introduced permeation-enhanced nonscrotal patch produces mid to normal range testosterone
levels 8 12 h following nightly application.
Unfortunately, because of the lack of relevant
controlled clinical trials of sufficient duration, it is
not possible to propose an ideal therapeutic regimen
for androgen substitution in aging men.

group may not uniformly lead to problems with

polycythemia.27
Testosterone administration has been reported to
exacerbate pre-existing sleep apnea, but none of the
reports of testosterone therapy in older men have
noted the development of sleep apnea.28 Since these
apneic events and the ensuing oxygen desaturation
may lead to cardiovascular complications, it is
pertinent to ask older men about this symptom and
to measure and follow up hematocrit values before
and during androgen administration. Care must be
exercised in men who are overweight, heavy
smokers or who have chronic obstructive airway
disease.

S95

Androgens and gynecomastia

Administration of aromatizable androgens may lead
to gynecomastia in the aging male, in all likelihood
when the subsequent increases of estrogens and
androgens tip the balance in favor of a higher
estrogen=androgen ratio.29 Patients with liver or
renal disease may be particularly predisposed to the
development of gynecomastia.

Androgens and body composition

Adverse effects of androgen substitution

Although testosterone replacement studies in older

men have varied in design, mode, duration of
therapy, the data consistently demonstrate changes
in body composition with testosterone a decrease
in body fat, increase in lean body mass, and a
change in some aspects of muscle strength.30
Testosterone therapy inhibits triglyceride uptake
and lipoprotein lipase activity and causes a more
rapid turnover of triglycerides only in the abdominal
adipose tissue region.31

Androgen and hematopoiesis and sleep apnea

Androgens and bone

The stimulatory effects of androgen on erythropoiesis are well known. Both testosterone and 5adihydrotestosterone stimulate renal production of
erythropoietin. There is evidence for a direct
effect of androgens on erythropoietic stem cells.25
Androgen receptors have been found in cultured
erythroblasts.26
Studies in which young hypogonadal or eugonadal men have been supplemented with testosterone
have shown an increase in hemoglobin and hematocrit levels with treatment. Because healthy older
men tend to have slightly lower hematocrit values
and hemoglobin levels than do young adult men, the
erythropoietic effects of testosterone in the older age

Several studies have evaluated the effect of testosterone on parameters of bone turnover and=or bone
density in older men.30 A significant decline in
urinary excretion of hydroxyproline, or an increase
in serum osteocalcin, was reported in men after 3
months of testosterone therapy. After 18 months of
testosterone therapy in older men, a 5 13% increase
is noted in trabecular bone density, depending on
modality of measurement used. Bone density may be
increased and bone turnover slows in elderly men
undergoing testosterone therapy, although additional longer-term data are needed to confirm that
androgen replacement can sustain a stabilization or
reversal of bone loss in this age group.
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Androgens and mood, cognition, and sexual

behavior
In elderly men, the effects of testosterone therapy on
mood, aspects of cognition, and sexual behavior
have been evaluated. Several studies have shown
improvement in spatial cognition with androgen
therapy. Others have reported improvement in sense
of wellbeing and=or an increase in libido with
testosterone. Impotence in older men is usually
multifactioral and testosterone therapy often has not
been beneficial.32,33
Effect on body fluid and glucose metabolism
The administration of testosterone can produce fluid
retention, aggravating hypertension, peripheral
edema, and compulsive heart failures.34 Men
treated with testosterone produce a decrease in
fasting glucose in blood and a decrease in insulin
resistance.35

the possible promotional role of androgens in this

disease. The possibility cannot be excluded that
promotion of precursor lesions is stimulated by
androgens; therefore, androgen substitution should
not lead no superphysiological plasma levels of
androgenic steroids. PSA monitoring, which is a
solid marker for prostate cancer, can be used to
assess the androgen action on neoplastic cells in the
prostate. The problem is to define the cut-off since
we know that we will miss about 14% of cancer with
a PSA below 4 mg=ml with normal rectal examination and about 29% of cancer when the patients are
older than 60 y.38
Is it justified to do a biopsy before testosterone
treatment? The controversy exists; several investigators believe that it is mandatory to do biopsies in
everybody who is going to have supplemental
androgen therapy,39 whereas others not.40
Effects on sexual function

Androgens have a profound effect on the skin.

Androgens regulate, by means of receptors, the
sebaceous glands and hair growth function, and
remarkably they do so on two different types of
target cells in the skin: the epithelial sebocyte of the
sebaceous gland and the mesenchymal cells of
the hair follicle dermal papilla.17

In humans, testosterone seems to have an effect on

central events rather than on erectile tissues.
Exogenous testosterone significantly increases frequency of masturbation and sexual activity and
enhances the rigidity of nocturnal penile erections
in normal men and in hypogonadal men.41 It also
increases the number of nocturnal penile erections
but does not modify the responses to audiovisual
sexual stimulation.42,43
Recent studies have shown that testosterone
could have a control of cavernous tissue in animals
but not in men (see Smooth muscle pathology and
erectile dysfunction by E Wespes in this issue44).

Androgens and prostate

The potential risks of androgen therapy

Androgens and skin effects

The development of benign prostatic hyperplasia is

mediated by intracellular events resulting from the
action of 5a-dihydrotestosterone. Prostate size and
prostate-specific antigen (PSA) are shown to increase in hypogonadal men treated with testosterone
substitution.36 However, the prostate still remains
within the normal size range for eugonadal men of
the same age and within normal levels of PSA for
controlled population. There is only a mild reduction in urine flow.
Metastatic or local prostate cancer is usually
dependent on androgens in its growth.37 Based on
epidemiological and autopsy studies in the pathogenesis of human prostate cancer, a phase of
initiation and promotion can be differentiated.
Incidental prostatic carcinoma is present in
approximately 10% of patients undergoing transurethral resection of prostatic hyperplasia.37
Is focal prostate cancer stimulated by androgens?
This is a crucial question for the understanding of
International Journal of Impotence Research

Androgen supplementation could carry some potential risks, especially in the older man who may
have certain coexistent medical problems. Water
retention, development of polycythemia, hepatotoxicity, exacerbation of sleep apnea, development
of detrimental effects on the cardiovascular system,
and exacerbation of pre-existent benign or malignant
prostate disease can be observed.
Water retention could lead to hypertension,
peripheral edema, or exacerbation of congestive
heart failure.

Conclusions
Several studies suggest that aging men with low
serum testosterone levels could benefit from
testosterone replacement therapy for bone, muscle,
and psychosexual functions. However, in short-term
follow-up, significant adverse effects can be observed, and for long-term follow-up, larger clinical

Male andropause
E Wespes and CC Schulman

studies are needed before a risk-benefit profile for

testosterone therapy in hypogonadal aging men can
be assessed.

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Appendix
Open discussion following Dr Wespes presentation
Dr Montorsi: I dont know whether this is a semantic
problem or a conceptual problem. You said that at
least 25% of men in the aging population may
benefit from testosterone supplementation because
their testosterone level would be low. I believe that
you mean that, potentially, testosterone could give
some positive effect. If we only look at erectile
function, there is no evidence that testosterone
given to a 56-y-old man who has a testosterone level
at the lower border or below the normal limit will
improve his erectile function.
Dr Wespes: In humans we dont have any scientific
data showing that testosterone has an influence on
erectile physiology. Maybe on nocturnal erection it
can have a central effect, but it doesnt seem to have
a peripheral effect. We know that when you are
castrated after puberty you can still have a normal
erection. So what is the role of testosterone in
erectile dysfunction in humans? I cannot give you
the answer.
Dr Nehra: To carry that a step further, in our clinics,
we all see patients who have read the effects of
testosterone replacement who are either borderline
or even above the borderline of normal range. They
say, Ive read all of these effects of testosterone; can
you possibly supplement me with testosterone so I
will not go through the changes that occur in a
normal male? How do you respond to that?
Dr Pryor: With these patients with minimally
subnormal levels, if you give them testosterone,
they will feel better in a general sense. They will feel
more active.
Dr Carson: They also have higher levels of sexual
thoughts and fantasies.
Dr Wespes: Yes, of course. Its the same with another
drug thats prescribed in the United States that you
cannot find in the pharmacy, DHEA.
Dr Hatzichristou: So are you going to prescribe to
this man?

International Journal of Impotence Research

Dr Wespes: Up to now, I dont do that. But when we

discuss with a patient taking DHEA or testosterone,
they say that they are better with DHEA.
Dr Porst: We have a general dilemma with androgen
supplementation. Morgentaler once more has seen
that hypogonadal men with low free testosterone
levels have a much higher likelihood to have
prostate cancer. In the University of Mannheim
study, Juenemann et al have investigated all the men
who were referred for prostate cancer for surgery,
and it turned out that between 60% and 70% of
these men were hypogonadal. So the general question is what are the requests for checking hypogonadal patients for prostate cancer, because we know
that these males have a low PSA and a high
likelihood of prostate cancer. Are we forced to do
biopsies in all or any of these men before we are
supplementing this, because we know now from
several studies that we have a higher likelihood of
prostate cancer in hypogonadal men.
Dr Wespes: Because we know that we have
undifferentiated prostate cancer with low testosterone levels and because the cells are undifferentiated, these patients dont secrete PSA. Then you
have a lower level of PSA also.
Dr Althof: Twice a year I see a man with a perfectly
normal testosterone level and a lifelong history of
no sexual interest in anything whatsoever. Is there
work on testosterone receptors that suggests that
people who may have normal levels of free and
bound testosterone may have more difficulty utilizing whats in their system, thereby producing effects
like in this man, which is quite unusual?
Dr Wespes: There is one study, published 20 y ago in
1980, that shows that we have a very, very small
number of androgen receptors in the penis.
Dr Pryor: Possibly these fit into androgen insensitivity.
Dr Meuleman: Im aware of a lot of studies on
androgen receptors in infertile men, and it didnt
turn out that there was lesser receptivity in these
men or there were mutations in the androgen
receptor gene.