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Population variation in age-related decline in male salivary testosterone

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Abstract

Age-related declines in free and bioavailable testosterone are frequently reported for Western populations, but interpopulation variation in this pattern has not previously been investigated. Salivary testosterone was measured using a consistently applied protocol on morning samples collected from men in four populations (USA, Congo, Nepal, and Paraguay) representing different geographical, ecological, and cultural settings. Mean testosterone levels varied significantly between the four populations. The mean testosterone differences between populations were greatest for young men (aged 15-30 years) and insignificant for older men (aged 45-60 years). The slope of age-related decline in testosterone was significant in the USA and Congolese participants, but not in the Nepalese or Paraguayan participants. Age patterns of testosterone decline vary between populations primarily as a result of variation in the peak levels attained in young adulthood. The potential consequences of this variation for other aspects of male health deserve investigation.
Human Reproduction Vol.17, No.12 pp. 3251–3253, 2002
Population variation in age-related decline in male salivary
testosterone
Peter T.Ellison
1,7
, Richard G.Bribiescas
2
, Gillian R.Bentley
3
, Benjamin C.Campbell
4
,
Susan F.Lipson
1
, Catherine Panter-Brick
5
and Kim Hill
6
1
Department of Anthropology, Harvard University, Cambridge, MA,
2
Department of Anthropology, Yale University, New Haven, CT,
USA,
3
Department of Anthropology, University College London, London, UK,
4
Department of Anthropology, Boston University,
Boston, MA, USA,
5
Department of Anthropology, Durham University, Durham, UK and
6
Department of Anthropology, University of
New Mexico, Albuquerque, NM, USA
7
To whom correspondence should be addressed at: Department of Anthropology, Peabody Museum, Harvard University,
11 Divinity Avenue, Cambridge, MA 02138 USA. E-mail: pellison@fas.harvard.edu
BACKGROUND: Age-related declines in free and bioavailable testosterone are frequently reported for Western
populations, but interpopulation variation in this pattern has not previously been investigated. METHODS: Salivary
testosterone was measured using a consistently applied protocol on morning samples collected from men in four
populations (USA, Congo, Nepal, and Paraguay) representing different geographical, ecological, and cultural
settings. RESULTS: Mean testosterone levels varied significantly between the four populations. The mean testosterone
differences between populations were greatest for young men (aged 15–30 years) and insignificant for older men
(aged 45–60 years). The slope of age-related decline in testosterone was significant in the USA and Congolese
participants, but not in the Nepalese or Paraguayan participants. CONCLUSIONS: Age patterns of testosterone
decline vary between populations primarily as a result of variation in the peak levels attained in young adulthood.
The potential consequences of this variation for other aspects of male health deserve investigation.
Key words: ageing/population variation/salivary testosterone/testosterone
Introduction
Although formerly controversial, an age-related decline in free
and bioavailable testosterone in healthy males is now a
frequently reported pattern in Western populations (Ferrini and
Barrett-Connor, 1998; Vermeulen et al., 1999; Harman et al.,
2001). Age-related declines in testosterone levels in males
have been associated with changes in body composition,
including increases in fat mass, decreases in muscle mass,
and decreases in bone mineral density (Denti et al., 1999;
Vermeulen et al., 1999; Kenny et al., 2000; van den Beld
et al., 2000). Reflecting these linkages to body composition,
age-related declines in male testosterone are also associated
with elevated risk of type II diabetes (Stellato et al., 2000;
Haffner et al., 1996), coronary heart disease (Simon et al.,
1997; De Pergola et al., 1997), ischemic stroke (Jeppesen
et al., 1996) and osteoporosis (Francis, 1999; Snyder et al.,
1999a). Low testosterone levels in older men are also
associated with low libido, erectile dysfunction, and depression
(Barrett-Connor et al., 1999; Schweiger et al., 1999; Wang
et al., 2000). On the other hand, high testosterone levels have
been associated with elevated risk and progress of prostate
cancer (Crawford, 1992; van Tinteren and Dasio, 1993).
Testosterone supplementation of older men has been shown to
result in increases in lean-body mass, decreases in fat mass,
© European Society of Human Reproduction and Embryology 3251
increases in bone mineral density, and improvements in mood
and sexual function (Bhasin and Tenover, 1997; Snyder et al.,
1999a,b; Winters, 1999).
Despite evidence of its clinical importance, relatively little
is known about population variation in age patterns of
testosterone. This contrasts strikingly with the increasing
awareness of population variation in female ovarian steroid
profiles and its relationship to disease risk (Ellison et al., 1993;
O’Rourke and Ellison, 1993; Ellison, 1999; Jasienska et al.,
2000; Jasienska and Thune, 2001). There are scattered reports
of male testosterone levels from non-Western, non-clinical
populations, but the comparability of these data is limited
by differences in sample collection, handling, and assay
procedures (Guerra-Garcia et al., 1969; Smith et al., 1975;
Christiansen, 1991a,b; Beall et al., 1992; Campbell, 1994).
This report presents data on age variation in male salivary
testosterone values from four populations spanning broad
genetic, ecological, and life style differences. All the samples
were collected using the same protocols and were assayed in
the same laboratory using consistent methods. The data are
used for a preliminary test of the hypothesis that significant
population variation exists in the pattern of age-related decline
in male testosterone. By analogy with findings for women
(Ellison et al., 1993), we expect that non-Western males will
P.T.Ellison et al.
Table I. Mean (pmol/l) salivary testosterone levels (T) from men in four populations, for total sample and for three age groups.
Population All ages 15 to 30 years 30 to 45 years 4560 years
T (pmol) SEM n T (pmol) SEM n T (pmol) SEM n T (pmol/l) SE n
USA 259 10 106 335 20 24 288 17 31 238 14 26
Congo 268 12 33 286 15 17 250 19 11 247 34 5
Nepal 240 13 37 251 18 22 224 19 14 225 0 1
Paraguay 192 12 45 197 25 15 187 14 21 192 36 8
P-value 0.0002 0.0001 0.0004 NS
P-value is given for one-way ANOVA; NS not signicant.
have lower levels of testosterone in adulthood and slower rates
of decline in testosterone with increasing age.
Materials and methods
Participants in this study represent males from four populations that
are geographically, genetically, ecologically, and culturally distinct:
Lese horticulturalists from the Ituri Forest, Democratic Republic of
the Congo (formerly Zaı
¨
re), (Bentley et al., 1993; n 33); Tamang
agropastoralists from central Nepal (n 39; Ellison and Panter-
Brick, 1996); Ache foragers from southern Paraguay (Bribiescas,
1996; n 45) and residents of Massachusetts, USA (n 106). Lese,
Tamang, and Ache participants represent all available willing males
in the corresponding study areas. The USA participants were recruited
by public advertisement, thus the potential for self-selection bias
should be noted. Age data were derived from detailed demographic
interviews in the Congo, Nepal, and Paraguay and from self-report
in the USA.
In all cases participants provided between one and ve morning
saliva samples collected within 2 h of waking from 15 days according
to established collection protocols which minimize the risk of contam-
ination with serum or gingival uid (Lipson and Ellison, 1989). The
samples were preserved with sodium azide until they could be
transferred to the laboratory and frozen at 20°C. Testosterone levels
have been found to be stable under these collection and handling
procedures for up to 6 months (Lipson and Ellison, 1989). Testosterone
values were determined for each sample by a tritium-based radio-
immunoassay according to published protocols (Ellison et al., 1989).
The sample values for individual participants were averaged to
provide mean values for each subject.
The age pattern of testosterone within each population was analysed
using simple linear regression. Sample sizes were too small to justify
higher order curve tting. Population variation in average testosterone
values is assessed by analysis of variance and by multiple linear
regression with age, population, and age multiplied by population
interaction as independent variables. For the purposes of the multiple
regression population was re-coded as a binary variable, USA and
non-USA.
Results
The mean salivary testosterone values for men in the four
populations were signicantly different (ANOVA, P 0.0002,
Table I) although they fall within the broad normal range
(1001000 pmol/l) for adult males in all cases. However, the
differences are not consistent across age groups and show
convergence with age. Population differences are greatest
3252
among men under the age of 30 years (ANOVA, P 0.0001)
and are non-signicant for men 4560 years.
A linear regression of testosterone on age for the combined
data from all four populations indicates a highly signicant
negative relationship (y 332 2.0x, P 0.0001). The
individual population regressions of testosterone against age
are signicant in the USA (y 418 3.4x, P 0.0001) and
Congo (y 346 2.3x, P 0.03), but not in Nepal (y
286 1.5x, P 0.39) or Paraguay (y 218 0.7x, P
0.50). A multiple linear regression model with age, population
(recoded as USA and non-USA), and agepopulation inter-
action as independent variables indicates signicant effects of
all three variables (y 549 5.2Age 131.5Population
1.7AgePopulation, multiple R 0.47, P 0.0001.
Signicance of individual variables: Age, P 0.0001; Popula-
tion, P 0.0002; AgePopulation, P 0.05).
Discussion
The data presented here provide the rst opportunity to consider
population variation in the relationship of male testosterone to
age. All the data were collected according to the same protocols
and analysed with the same assay methods in the same
laboratory. This common methodology helps to control for
many of the sources of variation that may confound the
comparison of results from different studies. The most import-
ant general observation from these data is that age-related
decline in free testosterone, as represented by salivary levels,
is not a uniform characteristic of all populations. In particular,
the rate of decline with age varies signicantly between
populations and in some populations (i.e. Nepal and Paraguay)
does not achieve statistical signicance, although this may be
due to the sample size limitations in this study.
The testosterone levels of older men (45 years) tend to
converge for all the populations studied while the levels of
younger men (30 years) vary signicantly. This suggests
that variability in the pattern of testosterone decline with age,
results from population variation in the reproductive physiology
of young males rather than in population differences in the
rate of reproductive senescence among older males. If so,
research into the mechanisms underlying age patterns of male
testosterone should focus on the determinants of young adult
levels as well as the causes of age-related decline.
Because population differences in age patterns of testoster-
one have not previously been appreciated, the implications of
Interpopulation salivary testosterone variation in males
such variation for patterns of health risk have not been
considered. If, for example, set-points for muscle anabolism
and bone mineral density are established relative to testosterone
levels in young adulthood, a steeper decline in testosterone
from higher young-adult levels might result in more rapid age-
related changes in male body composition, bone mineral
density, and related health risks. Higher testosterone exposure
throughout adulthood in populations with high young-adult
levels may also lead to greater prostate cancer risk. These
possibilities provide additional motivation for increased efforts
to study global variation in male gonadal function to comple-
ment studies of Western populations.
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Submitted on March 7, 2002; resubmitted on June 11, 2002; accepted on July
31, 2002
... The platelet samples were not washed and were grouped accordingly: 18-53-year-old premenopausal females, younger females (YF), ≥54-year-old, postmenopausal females, older females (OF), 18-44-year-old males, younger males (YM), ≥45-year-old males, older males (OM) using their sex as assigned at birth. [22][23][24][25][26][27][28][29][30] The subdivision of females was based on the average age of menopause of ≥54 years and the gradual fall in total testosterone levels which begins around 45 years of age after peaking at 19 years and was verified by sex hormone levels. [22][23][24][25][26][27][28][29] The median and range of the numbers of donations for each group are summarized and 2/5 YF, 3/5 OF, 3/5 YM, and 2/4 OM donated >6 times/year. ...
... [22][23][24][25][26][27][28][29][30] The subdivision of females was based on the average age of menopause of ≥54 years and the gradual fall in total testosterone levels which begins around 45 years of age after peaking at 19 years and was verified by sex hormone levels. [22][23][24][25][26][27][28][29] The median and range of the numbers of donations for each group are summarized and 2/5 YF, 3/5 OF, 3/5 YM, and 2/4 OM donated >6 times/year. All platelet samples were normalized to 300 × 10 6 platelets/ml before control/hormone incubation so that identical numbers of platelets were used. ...
... Apheresis platelets were collected from healthy donors, who were stratified into four groups on the basis of sex or age: younger females (YF) <54 years of age (21-51, n = 5), the average age of menopause, older females (OF) ≥54 years of age (59-66 years, n = 5), younger males (YM) <45 years of age (31-41, n = 5), and older males (OM) ≥45 years (52-76, n = 5) ( Figure 1A), the age when testosterone levels began to decrease. 22,23,[25][26][27][28][29][30][31][32] Metabolites were measured for these patients (Table S1), and unsupervised analyses were performed to determine the impact of sex, age, and in vitro incubation with testosterone or estradiol on platelet metabolism. Hierarchical clustering analysis ( Figure 1B) and principal component analysis ( Figure 1C) showed a significant effect of sex and age on platelet metabolism, with platelets from OM showing the strongest differential phenotype across all groups. ...
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Wide-ranging and inclusive, this text provides an invaluable review of an expansive selection of topics in human evolution, variation and adaptability for professionals and students in biological anthropology, evolutionary biology, medical sciences and psychology. The chapters are organized around four broad themes, with sections devoted to phenotypic and genetic variation within and between human populations, reproductive physiology and behavior, growth and development, and human health from evolutionary and ecological perspectives. An introductory section provides readers with the historical, theoretical and methodological foundations needed to understand the more complex ideas presented later. Two hundred discussion questions provide starting points for class debate and assignments to test student understanding.
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In the space of one generation major changes have begun to take place in the field of human reproduction. A rapid increase in the control of fertility and the understanding and treatment of sexual health issues have been accompanied by an emerging threat to reproductive function linked to increasing environmental pollution and dramatic changes in lifestyle. Organised around four key themes, this book provides a valuable review of some of the most important recent findings in human reproductive ecology. Major topics include the impact of the environment on reproduction, the role of physical activity and energetics in regulating reproduction, sexual maturation and ovulation assessment and demographic, health and family planning issues. Both theoretical and practical issues are covered, including the evolution and importance of the menopause and the various statistical methods by which researchers can analyse characteristics of the menstrual cycle in field studies.
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In the space of one generation major changes have begun to take place in the field of human reproduction. A rapid increase in the control of fertility and the understanding and treatment of sexual health issues have been accompanied by an emerging threat to reproductive function linked to increasing environmental pollution and dramatic changes in lifestyle. Organised around four key themes, this book provides a valuable review of some of the most important recent findings in human reproductive ecology. Major topics include the impact of the environment on reproduction, the role of physical activity and energetics in regulating reproduction, sexual maturation and ovulation assessment and demographic, health and family planning issues. Both theoretical and practical issues are covered, including the evolution and importance of the menopause and the various statistical methods by which researchers can analyse characteristics of the menstrual cycle in field studies.
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Salivary testosterone levels were measured in a population of New World indigenous adult hunter-gatherer males in order to compare circulating levels of free unbound bioactive steroid with those previously reported among Boston and nonwestern males. The study population consisted of adult Aché hunter-gatherer males (n=45) living in eastern Paraguay. Morning and evening salivary testosterone levels (TsalA.M.; TsalP.M.) among the Aché were considerably lower than western values (Boston) and even lower than other previously reported nonwestern populations (Efe, Lese, Nepalese). No association was observed between height, weight, or age and salivary testosterone levels within the Aché group, although older men (ages>40) were poorly represented in the study sample. Nevertheless, a mild correlation was observed between Aché TsalA.M. levels and BMI (r=0.133,p=0.0725). Comparison of Aché values with those for other populations confirms the prevalence of significant interpopulational variation in testosterone levels among adult males. Interpopulational variation in male testosterone is not as great, however, as has been documented for ovarian steroids among females, nor is it likely that such variation reflects differences in male fecundity. Nevertheless, such interpopulational variation in salivary testosterone levels may have a functional significance in the regulation of protein anabolism in skeletal muscle, thereby affecting the overall energy budget of the organism. It is suggested that relative suppression of average testosterone may be adaptive under conditions of chronic energy shortage.
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