DR SONG XIN (Orcid ID : 0000-0002-3602-7593)

Accepted Article
Article type : Original article

Chronic epididymitis and leptin and their associations with semen

characteristics in men with infertility

Song Xin1, Ye Hao1, Ma ZhiPeng2,Lin Nanhe1, Chen Bin1＃

1Department of Urology, Shanghai Institute of Andrology, Renji Hospital, Shanghai
Jiaotong University School of Medicine, Shanghai (200001), China
2 Department of Urology, Weifang Yi Du Center Hospital, Weifang, Shandong, China

＃
Corresponding author：Chen Bin, E-mail:dr_binchen@126.com

Running title
Epididymitis and leptin affect semen characteristics

Abstract
Objective: The aim of this study was to ascertain the associations between serum leptin
levels and chronic epididymitis and semen parameters in patients with infertility.
Methods: 846 patients who were diagnosed as primary infertility were enrolled and
divided into four groups. The general information, blood lipids, reproductive hormones
and semen parameters were collected. ROC curves of leptin was plotted for diagnosis of
the poor sperm quality. We used the Student’s t-test, the Chi-square test to analyze their
relationships, and used logistic regression analysis to evaluate potential confounding
factors. Results: ROC curve revealed that leptin had better sensitivity and specificity at
the concentration of 6.02 (0.565 and 0.917). Isolated epididymitis or elevated leptin had
no effect on sperm concentration and sperm membrane function, but the combination
of these conditions would reduce the concentration and normal morphology rate both
(p=0.002, p=0.005). Epididymitis or elevated leptin can affect the motility of sperms, the

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lead to differences between this version and the Version of Record. Please cite this article as
doi: 10.1111/aji.13126

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 former presented more significance (p=0.000), and the co-existence would further
reduce the sperm motility (p=0.001). Conclusions: Low sperm motility and sperm
normal morphology were found to be associated with chronic epididymitis and high
Accepted Article
leptin. Simultaneously suffering from chronic epididymitis and high leptin could
produce a more serious effect on sperm quality.

Keywords: leptin；chronic epididymitis；semen characteristics；infertility

Introduction
Infertility is always proposed to be one of the important health issues in spite of
cultures and races1. Defined as one year of unprotected intercourse without
pregnancy, infertility is estimated to affect nearly 50 million couples worldwide2.
Approximately half of overall infertility rates are due to males, and prevalence of
such kind of infertility presents the tendency of increasing3.
Considered to be the breakthrough in the diagnosis of male infertility, semen
analysis contains rich information about the fertility status of men in spite of its
limited role in distinguishing the underlying cause4. Since pinpointing the lesion
is supposed to be the first step in identifying and classifying the disorders, it is
meaningful to find relationships between seminal parameters and the disorders.
So it will make a difference in figuring out the pathophysiology and guiding
patients appropriately.
About up to 15% of male fertility disorders are attributable to infection and
inflammatory conditions5. In reality, chronic epididymitis is thought to be a
common consequence of previous events, bacterial or viral colonization or scrotal
injuries included6,7. Although there are a few studies based on limited samples
suggesting the association between these conditions and seminal parameters,
such as sperm density, motility, or morphology, it calls for further research6,8.
Leptin, mainly synthesized and secreted by the differentiated white adipose
tissue, is a 16-kDa peptide hormone coded by the obese gene9. Leptin exerts
various effects on glucose metabolism, bone marrow, vessels, bones, wounds, and
reproduction10. Studies on both experimental animals and humans have pointed
out leptin’s potential role in the regulation of reproduction functioning as a
metabolic junction of nutritional status and fertility11-13. Despite leptin’s well
proven effects on fertility in female, it remains debatable how it plays a part in
the complicated regulatory network affecting male reproduction14.
In addition to the above mentioned role, leptin is supposed to involve in the
chronic pro-inflammatory status commonly seen in obesity, metabolic syndrome
and subsequent atherosclerosis15. Leptin triggers inflammatory processes once
bound to the isoform of the leptin receptor (ObR) for various immune cells express
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 such kind of ObR. Some inflammatory and infectious stimuli like IL-1,
lipopolysaccharide (LPS), and TNF-a can stimulate the secretion of leptin in turn.
And this process is correlated with the degree of inflammation16. Hence the
Accepted Article
mutual links between leptin and inflammation participate in the circus of chronic
inflammation in obesity: pro-inflammatory cytokines promotes production and
secretion of leptin while leptin assists remaining the extent of inflammation.
So far, serum leptin levels of infertile patients with chronic epididymitis hasn’t
been demonstrated by any data in literature. Therefore, exploring leptin levels in
infertile men may be relevant in the light of reported association of serum leptin
with chronic epididymitis and infertility.
This study aimed at ascertaining the associations between semen characteristics
and serum leptin levels as well as chronic epididymitis in Chinese patients with
infertility.

Materials and methods

Patients
A total of 846 eligible patients aged 24-43 diagnosed with male infertility were
enrolled between January 2016 and January 2018. Patients were excluded for
lack of intact profiles about semen and blood tests, or being diagnosed with
obstructive or non-obstructive azoospermia, or any evidence of comorbidity
considered to affect fertility except for chronic epididymitis such as abnormal
karyotype, Y chromosome microdeletion, cryptorchidism, primary or secondary
hypogonadism or varicocele. Patients having a history of fever or receiving any
anti-inflammation or fertility-related medication within 3 months before study
were excluded as well.
Study design
Patients with an abnormal epididymis or vas deferens confrmed by palpation or
direct echography, or presented pain or discomfort located at unilateral or
bilateral scrotum, testicle or epididymis for previous 3 months or longer, were
considered to have chronic epididymitis 17. Those chronic epididymitis patients
usually presented indurations, irregularities, or thickening in the physical
examination, and reported a past event of scrotal pain episode related to genital
infection or trauma. Direct ultrasound can detect any abnormal modifcations in
diameter, texture, vascularization, cysts, and calcifcations. ROC curve was
applied to figure out the cut point of the leptin concentration to diagnose
oligoathenoteratospermia as the basis of grouping. We found that some patients
simultaneously developed chronic epididymitis and elevated leptin. Thus, we
finally divided these infertile patients into four groups: isolated chronic

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 epididymitis group, isolated elevated leptin group, combined chronic epididymitis
and elevated leptin group, and a control group without chronic epididymitis and
with a normal leptin concentration.
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We collected basic information including age, height, weight, and history of
smoking. Testicular volume was obtained through scrotal ultrasound. Blood tests
were performed before 10 a.m. Leptin was detected by ELISA using the kit
provided by Shanghai Hu Feng Biological Technology Co., Ltd. Patients
masturbated to get semen samples after 4-7 days of abstinence in the sampling
room. Semen routines and morphology detections were analyzed by
computer-assisted sperm quality and morphology analysis system. Sperm
hypoosmotic swelling test (HOS) is used to evaluate the sperm function. An
abnormal sample was defined as one with amount<2ml, sperm concentration<20
×106/mL, Grade (A+B) sperms<50% or normal morphology rate≤4%, HOS<70%.
Statistical analysis
The results are exhibited as mean and Standard deviation(Mean±s.d). The
receiver operating characteristic (ROC) curves of leptin was plotted for diagnosis
of the poor sperm quality. Comparisons between groups were achieved by
Chi-squared test for analysis of categorized variables and the Student’s t-test for
continuous variables. We utilize logistic regression analysis to to evaluate
potential confounding factors (age, BMI,smoking, and type of infertility). Data
analyses were accomplished by the SPSS for Windows version 24.0 (SPSS Inc.
Chicago, IL). P<0.05 was defined to be statistically significant.

Results
Among all the 846 patients screened for this study, 20 were excluded for lack of
intact profiles about semen and blood tests, 42 for azoospermia, 13 for abnormal
karyotype or Y chromosome microdeletion, 8 for cryptorchidism, 155 for primary
or secondary hypogonadism or varicocele and 82 for having a history of fever or
receiving any anti-inflammation or fertility-related medication within 3 months
before study. In total, 526 patients completed the study. Analysis of ROC curve
revealed that leptin had better sensitivity and specificity at the concentration of
6.02 (0.565 and 0.917, respectively). And the area under curve was 0.783 (95% CI
0.709~0.857) (Figure 1).
There were 65 patients in isolated chronic epididymitis group, 86 in isolated
elevated leptin group, 55 in combined chronic epididymitis and elevated leptin
group, and 320 in contrlol group. No significant difference was found among
groups in age. BMI was significantly higher in isolated elevated leptin group
compared to control group (p=0.000). On the other hand, more smokers were
observed in combined chronic epididymitis and elevated leptin group than control

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 group (p=0.014). Primary infertile patients made up 92.5% of control group while
secondary infertile patients predominated in the other 3 groups, especially the
isolated chronic epididymitis group (the proportion reached 36.9%,
Accepted Article
p=0.000)(Table 1).
Table 2 listed the semen characteristics of patients. The semen volume, sperm
concentration and HOS was similar among groups. However, isolated chronic
epididymitis group had a lower motility rate and normal morphology rate than
control group (p=0.003). Such phenomenon was observed in isolated elevated
leptin group as well (p=0.008, p=0.001, respectively). Meanwhile concentration of
a-glucosidase was lower in either isolated chronic epididymitis group or isolated
elevated leptin group (p=0.000, p=0.002, respectively).
Table 3 further analyzed influences of chronic epididymitis and leptin on semen.
Isolated epididymitis or elevated leptin had no effect on sperm concentration or
sperm membrane function, but the combination of these conditions would reduce
the concentration and normal morphology rate both (p=0.032, p=0.005,
respectively). Although epididymitis or elevated leptin affected the motility of
sperms, the former presented more significance (p=0.000). What’s worse, the
co-existence would further reduce the sperm motility (p=0.001).
Logistic regression analysis was applied to evaluate the influences of potential
confounding factors (BMI, smoking, types of infertility)(Table 4). As a result,
chronic epididymitis affected the normal morphology of sperms alone (p=0.000)
while elevated leptin affected sperm concentration and normal morphology alone
(p=0.008, p=0.000). The combination of both would exert negative effects on
sperm concentration, motility and normal morphology (p=0.012, p=0.023,
p=0.000, respectively).

Discussion
In this study, we investigated the semen profile, and ascertained the associations
between semen characteristics and serum leptin levels as well as chronic
epididymitis of patients having their first infertility consultation in China.
We found that isolated chronic epididymitis was correlated with impaired
seminal characteristics.Sperm motility, normal morphology rate as well as
a-glucosidase was all depressed. Alejandro et al. reported suppressed motility and
increased morphology abnormality in semen from men diagnosed with chronic
epididymitis alone18, which is similar to our results. Some studies also suggested
that chronic epididymitis might cause reduced sperm numbers 6,8. However, we
failed to proved the negative correlation between sperm concentration and
chronic epididymitis, this may be due to racial differences.

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 Inflammation can produce pro-inflammatory cytokines such as IL-6, IL-8 and
TNF-a, and the concentration of ROS will also increase. All these factors may
count for the damage of spermatogenesis, causing the eventual alterations in
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semen parameters19,20. Furthermore, accumulated ROS produce oxidative
alterations in DNA of spermatozoa and disturb the integrity. It is well known
that a-glucosidase in semen is mainly secreted by epididymal epithelial cells. It is
a specific enzyme and marker enzyme of the epididymis. It can catalyze the
decomposition of carbohydrate components or oligosaccharides of proteins and
provide suitable energy for sperm maturation. The enzyme can be used as a
functional index of the epididymis. Seminal plasma alpha-glucosidase levels in
infertile patients with epididymitis were lower than those without epididymitis,
which may be another reason for the decreased sperm viability.
Known to be a hormonal product of the obese gene in adipose tissue, leptin gets
involved in both of energy homeostasis and reproductive system. Humans or rats
with deficiency in leptin genes developed a variety of abnormalities in genital
system. They presented lighter ventral prostate gland and testes, fewer sperm in
the seminiferous tubules and smaller size of Leydig cells21. It proved that all
levels of the hypothalamus–pituitary–gonadal (HPG) axis in males were the
target of leptin. Nevertheless, nearly all obese patients turn to be insensitive to
the elevated leptin level, which is called as functional leptin resistance. Such kind
of suppression of leptin signaling may lead to dysfunctions of endocrine and
reproductive systems. Also, male infertility may result from the dysregulation of
leptin levels and following hypogonadism. So hypothalamic resistance or
insufficiency to leptin together with its modulation of testicular physiology may
be the underlying mechanisms22.
Several studies provided evidence for the association between elevated leptin
synthesis and regulation of reproduction. It is reported that azoospermic patients
had higher leptin levels than fertile ones. What’s more, the plasma leptin levels
were not associated with FSH and LH, indicating that testis could be a direct
target organ of leptin.23,24. Ahima et al. and Glander et al. described a negative
signification between leptin and sperm motility, respectively25,26. In the
population we studied, an elevated leptin level was related to depressed sperm
mortality, impaired morphology as well as reduced a-glucosidase.
There were a group of chronic epididymitis patients showing high leptin. With the
background of high frequency of each conditions in infertile men, we were not
surprised that they coexisted. However, the specific relationship hasn’t been
studied thoroughly until now.
Leptin regulates multiple systems. Besides hypothalamic-pituitary-adrenal axis,
leptin participates in energy homeostasis, insulin secretion, and reproduction27-30.
Recently, leptin’s role in the regulation of immune response has been a new

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 project. There are several studies revealing leptin’s function in the pathogenesis
of chronic inflammation. Moreover, obese patients’ high circulating leptin
concentrations seemed to help establish the low-grade inflammatory
Accepted Article
background31. Due to the pro-inflammatory effects, leptin shared similar
functions with acute phase substances, thus stimulating the level of
inflammatory cytokines like TNF-α, IL-6, and IL-1232,33. TNF-α and IL-1β will in
turn upregulate the expression of leptin mRNA in the adipose tissue34, forming a
positive feedback loop to prompt inflammation. This explains why patients who
simultaneously presented chronic epididymitis and high leptin had worse semen
quality than those in isolated chronic epididymitis group or isolated high leptin
group.
Based on the above evidence, we could theorize that chronic epididymitis and
leptin can not only affect semen quality alone, but also can interact with each
other, aggravating the impact on semen quality.
The main limitation of our study was the relatively small number of the patients
with chronic epididymitis, which could cause difficulties in making definite
conclusions. In addition, there is evidence of an association between MetS and
chronic inflammation or proinflammation state, but we did not detect
inflammation indicator such as pro-inflammatory cytokines. Studies showed that
excessive oxidative stress or WBC in seminal plasma is one of the potential
mechanisms leading to poor sperm quality in patients with chronic epididymitis,
but it is a pity that it is we did not detect these levels in the study. Sperm function
such as sperm DNA fragment index was not included in our study, it is also a
pity.
In conclusion, low sperm motility and sperm normal morphology were found to be
associated with chronic epididymitis and high leptin. Simultaneously suffering
from chronic epididymitis and high leptin could produce a more serious effect on
sperm quality, including sperm motility, sperm morphology, and sperm
concentration. Therefore, the comprehensive treatment of high leptin or obesity
and chronic epididymitis may be beneficial to improve semen qualities in infertile
patients.

Funding
This study was funded by the National Natural Science Foundation of China (No.
81471496).
Competing Interests
These authors declared that they have no competing financial interests.

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Accepted Article
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Accepted Article
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Figure 1 ROC curves of leptin for diagnosis of the poor sperm quality.

Table 1: General characteristics of the study population

Table 2: Semen characteristics of the study population

Table 3: Semen characteristics of the study population

Table 4: Adjusted odds ratios and 95% confdence intervals for the relationship between
genital disorders and semen characteristics

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 Table 1: General characteristics of the study population
Accepted Article
Controls Epididymitis( P1 Leptin(+) P2 Leptin(+) and P3
(n=320) +) (n=65) Epididymitis(+)
(n=86)
(n=55)

Age (year) 29.6±3.21 31.1±4.38 0.586 30.4±3.34 0.73 30.89±3.12 0.78

4 5

Type of 0.000 0.37 0.38

sterility, n (%) 2 9

Primary 296（92.5 41（63.1） 77（89.5） 49（89.1）

）

Secondary 24（7.5） 24（36.9） 9（10.5） 6（10.1）

BMI (kg/ m2), 0.865 0.00 0.88

n (%) 0 8

＜28 283（88.4 57（87.7） 43（50） 49（89.1）

）

＞28 37（11.6） 8（12.3） 43（50） 6（10.9）

Smoking, n 0.085 0.11 0.01

(%) 7 4

Never 222（69.4 52（80） 52（60.5） 47（85.5）

）

Ever 98（30.6） 13（20） 34（39.5） 8（14.5）

Total 31.46±5.65 30.34±5.11 0.879 32.42±6.98 0.78 31.01±4.13 0.89

testicular 4 8
volume (ml)

Notes: P1: Controls vs Epididymitis(+) ; P2: Controls vs Leptin(+); P3 Controls vs Leptin(+) and
Epididymitis(+)

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 Table 2: Semen characteristics of the study population
Accepted Article
Controls Only Only Leptin(+) P1 P2
Epididymitis(+)
(n=320) (n=86)
(n=65)

Semen volume 3.38±1.61 3.48±2.21 3.87±1.97 0.365 0.418

(ml)

Sperm 14.19±7.78 14.44±7.52 13.89±8.1 0.976 0.324

concentration
(×106 /ml)

Sperm motility (%) 37.35±17.47 15.43±10.61 26.34±19.40 0.003 0.008

Sperm morphology 9.98±5.02 5.76±3.39 4.82±3.1 0.003 0.001

(%)

a-glucosidase 43.79±11.25 26.13±10.12 33.13±9.12 0.000 0.002

HOS(%) 82.12±9.22 79.45±8.58 80.32±8.17 0.136 0.328

Notes: P1: Controls vs Only Epididymitis(+) ; P2: Controls vs Only Leptin(+)

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 Table 3: Semen characteristics of the study population

Only Only Leptin(+) and P1 P2 P3

Leptin(+) Epididymitis(+) Epididymitis(+)
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(n=86) (n=65) (n=55)

Semen volume 3.87±1.97 3.48±2.21 4.21±2.45 0.823 0.447 0.459

(ml)

Sperm 13.89±8.1 14.44±7.52 12.58±3.36 0.484 0.121 0.032

concentration
(×106 /ml)

Sperm motility (%) 26.34±19.40 15.43±10.61 8.96±2.66 0.000 0.001 0.001

Sperm 4.82±3.1 5.76±3.39 3.53±1.73 0.196 0.165 0.005

morphology (%)

a-glucosidase 33.13±9.12 26.13±10.12 19.35±6.87 0.012 0.000 0.003

HOS(%) 80.32±8.17 79.45±8.58 78.46±9.24 0.412 0.236 0.434

Notes: P1: Only Leptin(+) vs Only Epididymitis(+) ; P2: Only Leptin(+) vs Leptin(+) and
Epididymitis(+); P3 Only Epididymitis(+) vs Leptin(+) and Epididymitis(+)

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 Table 4: Adjusted odds ratios and 95% confdence intervals for the relationship between genital
disorders and semen characteristics
Accepted Article
Characteristics Leptin(+) Epididymitis(+) Leptin(+) and
Epididymitis(+)

P OR (95% CI) P OR (95% CI) P OR (95% CI)

Semen 0.437 1.626（0.477,5.547 0.605 1.402（0.39,5.041 0.833 1.181（0.25,5.58）

volume<2.0 ml ） ）

Sperm 0.008 0.172（0.047,0.63） 0.531 0.728（0.27,1.964 0.012 0.214（0,051,0.76）

concentration<2 ）
0 × 106 /ml

Sperm 0.395 0.644（0.233,1.777 0.198 0.534（0.145,1.523 0.023 0.043（0.078,0.584

motility<50% ） ） ）

Sperm 0.000 0.164（0.069,0.393 0.000 0.03(0.01，0.091) 0.000 0.012（0.001,0.093

morphology ） ）
<4%

HOS<70% 0.285 0.751 (0.502–1.121) 0.291 0.774 (0.457–1.246) 0.328 0.692 (0.433–1.151)

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Accepted Article

Figure 1 ROC curves of leptin for diagnosis of the poor sperm quality.

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