The Aging Male

ISSN: 1368-5538 (Print) 1473-0790 (Online) Journal homepage: http://www.tandfonline.com/loi/itam20

The relationship between serum total

testosterone and free testosterone levels with
serum hemoglobin and hematocrit levels: a study
in 1221 men

Yu Seob Shin, Jae Hyung You, Jai Seong Cha & Jong Kwan Park

To cite this article: Yu Seob Shin, Jae Hyung You, Jai Seong Cha & Jong Kwan Park (2016):
The relationship between serum total testosterone and free testosterone levels with
serum hemoglobin and hematocrit levels: a study in 1221 men, The Aging Male, DOI:
10.1080/13685538.2016.1229764

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Published online: 18 Oct 2016.

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ISSN: 1368-5538 (print), 1473-0790 (electronic)

The Aging Male, Early Online: 1–6

! 2016 Informa UK Limited, trading as Taylor & Francis Group. DOI: 10.1080/13685538.2016.1229764

ORIGINAL ARTICLE

The relationship between serum total testosterone and free

testosterone levels with serum hemoglobin and hematocrit levels:
a study in 1221 men
Yu Seob Shin1,2,3, Jae Hyung You1,2,3, Jai Seong Cha1,2,3, and Jong Kwan Park1,2,3
1
Department of Urology, Chonbuk National University, Jeonju, Republic of Korea, 2Research Institute of Clinical Medicine of Chonbuk National
University, Jeonju, Republic of Korea, and 3Biomedical Research Institute of Chonbuk National University, Jeonju, Republic of Korea

Abstract Keywords
Objective: To investigate the relationship between serum total testosterone (TT) and free Anemia, free testosterone, hemoglobin,
testosterone (FT) levels in men with anemia. hematocrit, testosterone
Methods: We reviewed the records of 1221 subjects between March 2009 and December 2014.
All the subjects’ blood samples were drawn for TT and FT assays. Their serum hemoglobin (Hb) History
and serum hematocrit (Hct) levels were measured. The primary objective of our study was to
investigate the association between TT and FT levels with Hb and Hct levels. Received 1 August 2016
Results: The mean age was 59.82 ± 12.71 years. The mean TT and FT levels were 4.54 ± 2.02 ng/ Revised 19 August 2016
mL and 10.63 ± 3.69 pg/mL, respectively. The mean Hb and Hct levels were 14.72 ± 1.34 g/dL Accepted 24 August 2016
and 43.11 ± 3.75%, respectively. Subjects with low TT (52.35 ng/mL) had low Hb and Hct levels Published online 7 October 2016
(p50.001, p50.001, respectively). TT was positively associated with FT, Hb, and Hct. TT and FT
levels were significantly lower in older men.
Conclusions: Subjects with low TT and FT levels had low Hb and Hct levels. This suggests that TT
and FT play a significant role in erythropoiesis. Testosterone replacement therapy may be
effective in men with hypogonadism to reduce the incidence of anemia.

Introduction
Anemia is associated with increased morbidity and mortality,
and can lead to cardiovascular and neurological events [1].
Furthermore, correlations have been shown between anemia
and limited physical performance and weakness [2]. Recent
data from the National Health and Nutrition Examination
Survey III demonstrated an anemia prevalence of 11.0% in
men aged 65 years and older [3]. They classified anemia into
four categories according to its underlying cause, i.e., anemia
from nutrient deficiencies, renal anemia, anemia of chronic
inflammation and, in the absence of other identifiable causes,
unexplained anemia [3]. The listed categories, however, are
not mutually exclusive and several pathologies may coexist in
an individual patient.
Earlier studies have found that low testosterone levels have
an independent influence on the development of anemia in
older adults [4]. Testosterone stimulates the production of
erythropoietin-responsive cells and burst-forming units in
the bone marrow, which boosts iron absorption and
Address for correspondence: Jong Kwan Park, MD, PhD, Department of
Urology, Medical School, Chonbuk National University, Geonji-Ro 20,
Deokjin-Gu, Jeonju 54907, Korea. Tel: +82-63-250-1510. Fax: +82-63-
250-1564. E-mail: rain@chonbuk.ac.kr
erythropoiesis [5]. The effects of testosterone on the bone
marrow affecting the hematopoietic growth factors and iron
absorption have shown associations between testosterone and
erythropoiesis [4,5]. Also, our previous study noted that the
prevalence of anemia decreased and patients with anemia
showed increased erythropoietin after testosterone replace-
ment therapy (TRT) [6]. Considering that testosterone has an
independent influence on erythropoiesis and iron absorption,
it is reasonable to assume that patients with hypogonadism
might experience an increased frequency of anemia. Based on
this theory, we hypothesized that there is a relationship
between serum total testosterone (TT) and free testosterone
(FT) levels, and serum hemoglobin (Hb) and hematocrit
(Hct) levels. There are very few reports that have evaluated
the relationship between TT, FT with Hb, and Hct levels,
and their subjects were usually limited to older age groups
[4,7,8].
Considering the limitations of existing studies, more
research is necessary to determine the relationship between
TT with Hb levels and clarify the treatment in the general
male population. To our knowledge, the present study is the
first investigation targeting all age groups to investigate the
relationship between TT and FT levels with the Hb and Hct
levels.
2 Y. S. Shin et al.
Methods
Study objectives
The primary objective was to investigate the relationship
between TT and FT with Hb and Hct levels. The secondary
objective of our study was to investigate the correlation
between age, TT, FT, Hb, Hct, total cholesterol (TC),
triglyceride (TG), high-density lipoprotein cholesterol
(HDL), low-density lipoprotein cholesterol (LDL), and pros-
tate-specific antigen (PSA) levels.
Study subjects and measures
The 1221 subjects who had visited our institutions to undergo
evaluation for the urologic diseases were prospectively/
retrospectively enrolled in this study. We reviewed the
medical records of patients between March 2009 and March
2011. Subsequently, prospective study was started in April
2011 and it was finished in December 2014. The study was
approved by the Institutional Review Board at our hospital
and conducted in accordance with the Declaration of
Helsinki. All the patients had a blood samples for hormonal
tests, including TT (Testosterone ELISA kit, Cat. No. ADI-
901–065; Enzo Life Science, Farmingdale NY), FT (Free
Testosterone ELISA kit, Cat. No. 1885; Alpha Diagnostic
International, San Antonio TX). All the subjects’ blood
samples for TT and FT assays were drawn between 8:00 and
10:00 AM. Serum TT levels of 52.35 (2.365TT59.96 ng/
mL, and FT58.7 (8.85FT527) pg/mL were considered to
be low. Using serum samples obtained at the same time as the
full blood count determination, the levels of Hb, Hct, TC, TG,
HDL, LDL and PSA were measured. All assays were
conducted at the Laboratory of Analytical Biochemistry at
the Chonbuk National University Hospital. The Hb was
determined using an auto-analyzer (Sysmex XE-2100, Kobe,
Japan). All measurements were performed within 2 h of blood
being drawn. Men using testosterone or other androgenic
anabolic steroids either at, or six months prior to, the time
of the survey were excluded. Those with a PSA level of
44.0 ng/mL, a current or previous diagnosis of prostate
cancer, an untreated prolactinoma, uncontrolled diabetes
mellitus (HbA1c above 10%), liver and kidney disease,
known diseases of the testis or the pituitary were excluded.
We also excluded men who had presented with a primary
diagnosis of infertility, Klinefelter syndrome, or secondary
hypogonadism after appropriate assessment of history and
endocrine evaluation with gonadotropins.
Statistical analysis
The association between nine factors including age, TT, FT,
Hb, Hct, TC, TG, HDL, LDL, and PSA levels were analyzed
using the Pearson correlation coefficient. Comparisons across
subgroups according to TT and FT levels with Hb and Hct
levels were analyzed by ANOVA. The TT and FT levels were
divided into three (52.35, 2.3 5–9.96, 9.965ng/mL and58.7,
8.8–27, 275pg/mL, respectively)). Normal TT and FT levels
were set based on the reference values of the Endocrine
Society Clinical Practice Guidelines, and upon observational
studies [9–12]. The comparisons across subgroups according
to level of Hb levels with TT and FT levels were analyzed by
The Aging Male, Early Online: 1–6
an independent t-test. The comparisons across subgroups
according to age with TT and FT levels were analyzed by the
independent t-test. The subjects were divided into two age
groups (565 and 65 years). The statistical software package
SPSS 18.0 (SPSS Inc., Chicago, IL) was used for all statistical
analyses. Values of p50.05 were considered statistically
significant.
Results
Primary objective outcomes
Table 1 shows the mean baseline values of the variables
measured among all age groups. The mean age was
59.82 ± 12.71 years. The mean TT and FT levels were
4.54 ± 2.02 ng/mL and 10.63 ± 3.69 pg/mL, respectively. The
mean Hb and Hct levels were 14.72 ± 1.34 g/dL and
43.11 ± 3.75%, respectively. The subjects with low TT
(52.35 ng/mL) levels had low Hb and Hct levels (p50.001,
p50.001, respectively) (Figure 1). The low FT levels (58.7 pg/mL)
had low Hb and Hct levels (p50.001, p50.001, respectively)
(Figure 1). The low Hb levels had low TT and FT levels
(p50.001, p50.001, respectively) (Figure 2). The TT and FT
levels were significantly low in men with older than 65 years
(p50.001, p50.001, respectively) (Figure 2).
Secondary objective outcomes
A total of 106 subjects (8.68%) had a TT level of52.35 ng/dL,
and 123 subjects (10.07%) had a Hb level of 513 g/dL.
Subject age was positively correlated with TC, TG, LDL, PSA
and negatively correlated with TT, FT, and HDL levels
(Table 2). The TT levels were positively correlated with FT,
Hb, Hct, and HDL levels. The TT levels were negatively
correlated with age and TG levels (Table 2). Also, FT levels
were positively correlated with TT, Hb, Hct, and HDL levels,
and FT levels were negatively correlated with age and TC and
LDL levels (Table 2).
Discussion
The studies on the stimulating effects of testosterone on bone
marrow affecting the hematopoietic growth factors and iron
absorption have shown associations between testosterone and
Table 1. Mean levels of variables of the
general study population.
Age (years) 59.82 ± 12.71
TT (ng/mL) 4.54 ± 2.02
FT (pg/mL) 10.63 ± 3.69
Hb (g/dL) 14.72 ± 1.34
Hct (%) 43.11 ± 3.75
TC (mg/dL) 180.12 ± 36.38
TG (mg/dL) 145.97 ± 95.53
HDL (mg/dL) 47.21 ± 11.93
LDL (mg/dL) 99.01 ± 30.02
PSA (ng/mL) 3.23 ± 21.14
TT: serum total testosterone; FT: serum free
testosterone; Hb: serum hemoglobin; Hct:
serum hematocrit; TC: total cholesterol;
TG: triglyceride; HDL: high-density lipo-
protein cholesterol: LDL: low-density lipo-
protein cholesterol; PSA: serum prostate-
specific antigen.
DOI: 10.1080/13685538.2016.1229764
erythropoiesis [13,14]. The production of erythropoietin-
responsive cells and burst-forming units increase in the bone
marrow by enhancing nuclear receptors. Since testosterone
stimulates erythropoiesis, TRT is used to help increase Hb
levels in hypogonadal patients. According to the results of our
previous study, Hb and Hct levels significantly increased after
TRT by an average of 2.46 gm/dL (p50.001) and 3.03%
(p50.001), respectively [6]. While higher levels of testoster-
one in boys after puberty (generally after the age of 13 years)
mark the difference in Hb levels between male and female
adults, patients with delayed male puberty show similar Hb
levels with prepubertal boys and girls [15,16]. Those patients
can be treated with testosterone to normalize Hb levels by
stimulating erythropoiesis.
Considering that testosterone has an independent influence
on erythropoiesis, it is reasonable to assume that patients
suffering from hypogonadism or taking antiandrogenic drugs
might experience anemia more frequently [17]. In fact, studies
by Grossmann et al. [8] and Bhatia et al. [18] have revealed
the relationship between low serum testosterone levels and
anemia. However, their research was confined to men with
type-2 diabetes mellitus. The results of our study are similar
Figure 1. Levels of serum hemoglobin and
hematocrit with serum total testosterone and
free testosterone. *p50.001. TT: serum total
testosterone; FT: serum free testosterone; Hb:
serum hemoglobin; Hct: serum hematocrit.
Relationship between testosterone with anemia 3
to the existing findings of worsening anemia in men with low
TT levels. The difference is that our study population was not
composed of patients with chronic disease. Importantly, we
investigated the influence of testosterone on anemia in a
general male population.
In men, 1–3% of testosterone is unbound and known as FT.
The FT and albumin-bound testosterone, which possess
biological activity, make up the bioavailable testosterone
[19]. Cabral et al. reported that androgen deficiency of the
aging male and Massachusetts Male Aging Study question-
naires showed adequate sensitivity in diagnosing male patients
with low levels of FT [20]. The analysis of our study is similar
to the existing findings that FT was positively correlated with
TT levels. And, measuring FT with TT may provide a more
accurate picture than measuring TT alone when it comes to
diagnosing androgen deficiency of the aging male.
It is also noticeable that testosterone is related to metabolic
syndrome (MS), which is recently causing great concern in
the medical field as a main factor of lowering quality of life.
MS is a group of health conditions, including central obesity,
insulin resistance, and dyslipidemia, associated with an
increased risk of heart disease and other disorders [21].
4 Y. S. Shin et al. The Aging Male, Early Online: 1–6

Figure 2. Levels of serum total testosterone

and free testosterone with serum hemoglobin
and age. *p50.001. TT: serum total testos-
terone; FT: serum free testosterone; Hb:
serum hemoglobin; Hct: serum hematocrit.

Table 2. Pearson correlation coefficient showing correlation between age, TT, FT, Hb, Hct, TC, TG, HDL, LDL, and PSA.

Age TT FT Hb Hct TC TG HDL LDL PSA

Age 1 0.164** 0.296** 0.351** 0.339** 0.066* 0.107** 0.029 0.086** 0.096**
TT 0.164** 1 0.547** 0.122** 0.138** 0.002 0.220** 0.168** 0.017 0.012
FT 0.296** 0.547** 1 0.324** 0.348** 0.083** 0.011 0.102** 0.062* 0.042
Hb 0.351** 0.122** 0.324** 1 0.957** 0.218** 0.176** 0.04 0.193** 0.063*
Hct 0.339** 0.138** 0.348** 0.957** 1 0.248** 0.143** 0.066* 0.231** 0.049
TC 0.066* 0.002 0.083** 0.218** 0.248** 1 0.253** 0.238** 0.783** 0.018
TG 0.107** 0.220** 0.011 0.176** 0.143** 0.253** 1 0.286** 0.036 0.003
HDL 0.029 0.168** 0.102** 0.04 0.066* 0.238** 0.286** 1 0.039 0.046
LDL 0.086** 0.017 0.062* 0.193** 0.231** 0.783** 0.036 0.039 1 0.018
PSA 0.096** 0.012 0.042 0.063* 0.049 0.018 0.003 0.046 0.018 1

TT: total testosterone; FT: free testosterone; Hb: hemoglobin; Hct: hematocrit; TC: total cholesterol; TG: triglyceride; HDL: high-density lipoprotein
cholesterol: LDL: low-density lipoprotein cholesterol; PSA: prostate-specific antigen.
*p50.05.
**p50.01.

While various factors can lead to MS, central obesity is
considered to be fundamental because of its linkage to other
diseases, such as hypertension, increased LDL, decreased
HDL, and hyperglycemia [21,22]. The key here is that central
obesity has an inverse relationship with TT levels [23–26].
The evidence of the relationship has been found not only in
the existing studies but also in the present study. The analysis
of our study has reported that TT negatively correlated with
TG and positively correlated with HDL levels. FT was also
positively correlated with Hb, Hct, HDL and negatively
correlated with TC and LDL levels.
Many researchers have put their efforts towards explaining
the relationships between testosterone and serum PSA levels,
but most of their studies were conducted not in healthy men
but in hypogonadal men undergoing TRT [27,28]. Some of
them have shown that the PSA level significantly increased
after TRT. The relationship between PSA and TT levels is still
controversial. To our knowledge, the relationship between TT
levels with PSA values in healthy patients was first analyzed
by Mustafa et al. [29]. In their reports, no impact of
testosterone was found on healthy men with PSA levels of
54 ng/mL. The results of our study are similar to the existing
findings that TT and FT are not correlated with PSA.
However, Rastrelli et al. reported that PSA was negatively
correlated with the TT level [30]. Furthermore, low PSA was
associated with hypogonadism-related features [31]. Thus,
more large-cohort studies are needed to completely explain
the relationship between TT and PSA levels.
Testosterone deficiency was observed in 12.3% of aging
men in Massachusetts Male Aging Study [32]. A study
reported that from the age of 40, TT levels of men decline at a
rate of 1–2% per year [33]. Normal aging could be one of the
causes of this deficiency. In our study, we noted that TT and
FT levels decreased significantly with age.
DOI: 10.1080/13685538.2016.1229764
Hb and Hct are more frequently measured than testoster-
one in a routine laboratory assessment, it would be even more
useful to predict hypogonadism. It is also known that Hb and
Hct show a very consistent response to TRT [6]. Therefore,
Hb and Hct could potentially be a qualifying marker for
hypogonadism and trigger measurement of testosterone.
Strengths of this study include the large number subjects,
measurement of testosterone levels at the appropriate time of
day (early morning), and accurate assays for TT and FT
levels. A limitation of our study is that TT levels were
measured only once. Also, the medication status of 5a-
reductase inhibitors in study subjects was not considered.
Dihydrotestosterone (DHT) is produced from the reduction of
testosterone by the enzymes 5a-reductase and 5a-reductase
inhibitors decrease serum DHT concentrations. However,
according to previous studies, there is no influence of
receiving 5a-reductase inhibitors on Hb levels [33,34].
Amory et al. reported that Hb and Hct levels increased
significantly in the TRT only and TRT plus finasteride
groups, but having no difference in Hb and Hct levels between
the two groups [34]. Also, Shigehara et al. reported that
patients with low TT levels had insignificant changes in Hb
levels after 12 months of treatment with dutasteride [35].
Conclusions
Our data demonstrated that subjects with low TT and FT
levels had low Hb and Hct levels. This result suggests that TT
and FT may play a significant role in erythropoiesis. Although
men with hypogonadism were not always anemic, the
association between low testosterone and low Hb levels was
statistically significant. TRT may be effective in men with
hypogonadism to reduce the incidence of anemia.
Acknowledgments
The authors thank the members of the Laboratory of
Experimental Urology for helpful discussions.
Declaration of interest
This study was supported by grants from the Korea
Healthcare Technology R&D Project, Ministry for
Health, Welfare & Family Affairs, Republic of Korea
(HI14C0018).
The Korea Healthcare Technology R&D Project, Ministry
for Health, Welfare & Family Affairs, Republic of Korea had
no role in the design or conduct of the study; collection,
management, analysis, and interpretation of the data; or
preparation, review, or approval of the manuscript. The
content of this article is solely the responsibility of the authors
and does not necessarily represent the official views of the
Korea Healthcare Technology R&D Project, Ministry for
Health, Welfare & Family Affairs, Republic of Korea.
The authors report no conflict of interest.
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