Evaluation of Seminal Fructose and Citric Acid Levels in Men with Fertility Problem

Abstract

Context:
Male infertility is a medical problem, attributed to 50% of infertility. Seminal plasma can be an anticipating factor as it comprises secretions of accessory sex gland, thus offering novel and precise ways to understand potential roles of these biochemical markers in male infertility.

Aim:
The objective of this study was to assess the correlation between biochemical markers and sperm parameters in envisaging male infertility.

Subjects and design:
We enlisted 105 men with fertility issue as patients and 25 fertile men as controls to evaluate the sperm parameters and biochemical markers, namely fructose and citric acid in ascertaining male infertility.

Materials and methods:
The semen samples from patients were collected properly and analyzed according to the World Health Organization-2010 manual. Later samples were centrifuged, seminal plasma was collected, and biochemical markers assessment was carried out by standard protocols.

Statistics:
Descriptive statistics, independent t-test, one-way ANOVA, and Pearson correlation were used for statistical analysis of different variables using SPSS 20.0. The mean sperm count and motility by all infertile conditions displayed a significant difference when compared with the controls (P < 0.05).

Results:
The mean fructose levels of oligozoospermia showed a nonsignificance difference when compared with controls (P < 0.05). Asthenozoospermia, asthenoteratozoospermia, and azoospermia had a significance difference (P < 0.05) for citric acid levels. Pearson correlation coefficient showed significant negative correlation of sperm count (r = -0.564) and sperm motility (r = -0.574) with fructose levels. Whereas seminal citric acid concentration had a positive correlation with sperm count (r = 0.458) and sperm motility (r = 0.446).

Conclusion:
Therefore, evaluation of certain biochemical markers of seminal fluid may benefit in understanding the functionality of accessory glands which subsidizes significantly to the seminal volume.

Full text

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© 2019 Journal of Human Reproductive Sciences | Published by Wolters Kluwer - Medknow
 Male infertility is a medical problem, attributed to 50% of infertility.
Seminal plasma can be an anticipating factor as it comprises secretions of
accessorysexgland,thusofferingnovelandprecisewaystounderstandpotential
roles of these biochemical markers in male infertility.  The objective of
this study was to assess the correlation between biochemical markers and sperm
parameters in envisaging male infertility.    We enlisted 105
menwith fertility issue aspatients and 25 fertilemen as controls to evaluatethe
sperm parameters and biochemical markers, namely fructose and citric acid in
ascertaining male infertility.    The semen samples from
patients were collected properly and analyzed according to the World Health
Organization‑2010 manual. Later samples were centrifuged, seminal plasma
was collected, and biochemical markers assessment was carried out by standard
protocols.  Descriptive statistics, independent t‑test, one‑way ANOVA,
andPearsoncorrelationwereusedforstatisticalanalysisofdifferentvariablesusing
SPSS20.0.Themeanspermcountandmotilitybyallinfertileconditionsdisplayed
asignicantdifferencewhencomparedwiththecontrols(P<0.05). The
meanfructoselevelsofoligozoospermiashowedanonsignicancedifferencewhen
comparedwith controls (P < 0.05).Asthenozoospermia, asthenoteratozoospermia,
and azoospermia had a signicance difference (P < 0.05) for citric acid levels.
Pearson correlation coefcient showed signicant negative correlation of sperm
count(r=−0.564)and sperm motility (r=−0.574)withfructoselevels.Whereas
seminal citric acid concentration had a positive correlation with sperm count
(r = 0.458) and sperm motility (r = 0.446).  Therefore, evaluation
ofcertain biochemical markers ofseminal uid may benet inunderstanding the
functionality of accessory glands which subsidizes signicantly to the seminal
volume.
 Accessory glands, citric acid, fructose, male infertility, seminal
plasma

Fertility Problem
Makhadumsab M. Toragall, Sanat K. Satapathy1, Girish G. Kadadevaru2, Murigendra B. Hiremath
Access this article online
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Website:
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DOI:
10.4103/jhrs.JHRS_155_18
Address for correspondence: Dr. Murigendra B. Hiremath,
Department of Biotechnology and Microbiology, Karnatak
University, Pavate Nagar, Dharwad ‑ 580 003, Karnataka, India.
E‑mail: murigendra@gmail.com
importance.[4,5] Male infertility is multifactorial, such as
endocrineailment,testicularcatastrophe,testicularcancer,
testicular instabilities, genital tract infection, varicocele,
exposure to gonadotoxic substances,[6‑8] smoking,
advanced age, ejaculatory dysfunction, obstruction and

Procreation is one of the most essential aspects of
mankind, and both the genders must be robust and
normaltoexecute thisprocesscomfortably.Theinability
ofcouplestoreproducemayresultinsternpsychological,
social,andphysicalencumbrance;sometimes,thistrauma
ends in the loss of beloved ones. Today, 14%–30% of
couplesattheirprocreativeageareenduringinfertility,[1]
and male factors are instrumental in nearly 50%
of cases,[2,3] which is captivating global cumulative
Departmentsof
Biotechnologyand
Microbiologyand 2Zoology,
KarnatakUniversity,
Dharwad,1HubliAssisted
ConceptionCentre, Hubli,
Karnataka,India
Original Article

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given and the new creaons are licensed under the idencal terms.
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How to cite this article: Toragall MM, Satapathy SK, Kadadevaru GG,
Hiremath MB. Evaluation of seminal fructose and citric acid levels in men
with fertility problem. J Hum Reprod Sci 2019;12:199-203.
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Toragall, et al.: Biochemical indicators and male infertility
200 Journal of Human Reproductive Sciences ¦ Volume 12 ¦ Issue 3 ¦ July-September 2019
abnormalfunctioningof accessorysexorgans,prolonged
exposure to heat, obesity, environmental pollutants,[9‑11]
poor Zinc and Vitamin C in food, excessive stress, and
use of certain drugs.[12,13] The reproductive physiology
of men affected by such factors produces lower sperm
count,hasdeprivedspermmotility,andshowsanomalous
sperm morphology, which are the key attributes of
male infertility.[14]Semen is composed of concentrated
suspension of spermatozoa, which is diluted by seminal
uid predominantly secreted by the seminal vesicles
followed by prostate, with a slight contributions from
the bulbourethral (Cowper’s) glands and epididymis
for the normal functioning of spermatozoa.[15‑20]The
seminal plasma is composed of an intricate assortment
of organic and inorganic elements, that may not crucial
for fertilization, yet it optimizes the suitable atmosphere
forspermmotility,endurance andtransportinthefemale
reproductiveexpanse.[18,21]The rst portionofthehuman
ejaculateis principally composed of spermandprostatic
exudates i.e. citric acid, proteases, acid phosphatase and
thelaterportion hasfructose,prostaglandins,coagulating
elementsandbicarbonatesfordefendingtheacidicvaginal
zone secreted by seminal vesicles.[16,17,22] Consequently,
these biochemical secretions serve as a markers of
their respective glands.[23]The seminal plasma has an
excessive concentrations of fructose, which provides an
anaerobic and aerobic source of energy for the sperm[24]
and has been obliquely associated with progressive
sperm motility and viscosity.[25,26] Evaluating fructose
concentrationofseminalplasmacandisplaythestatusof
seminal vesicles, endocrine anomalies and also potential
ejaculatory duct obstruction, if any.[16,23,27] Citric acid
is an essential organic acid, and its principle role is to
maintain pH, convert protein, fat, and sugar into carbon
dioxide.[24,28]It is a vital biochemical constituent of
seminal plasma which not only rebounds the condition
of the prostate, but also allied with coagulation and
liquefaction of semen in humans.[29] Hence, it plays
a vital part in sperm motility and hyaluronidase
activity.[19,29] The importance of citric acid in altering
sperm attributes during abstinence has been underrated,
inspecting the levels of citric acid in seminal plasma
thus may benet to nd the probable causes of male
infertility.A proper counselling (brief medical history,
physicalinspectionand imaging), simple semen analysis
beside biochemical evaluation of seminal plasma is the
prerequisite step to identify potential cause affecting
viability, motility and morphology of spermatozoa[18,30]
which laterally provides activity status of accessory sex
glands.[31]Hence,assessingbiochemicalindicatorsforthe
identication of biological attributes of semen can help
in establishing novel benchmarks that are precise and
equitable in envisaging male infertility. Therefore, the
currentstudywascarriedouttore‑evaluatetheefciency
ofbiochemicalmarkersinassessing maleinfertility.

Study design
After gratifying the inclusion and exclusion standards
forthisstudy,atotalof105mendiagnosedwithfertility
issues as patients and 25 fertility‑proven men with
normozoospermia as controls were conscripted, who
visited a renowned in vitro fertilization center, during
the course of 2015–2018. The study was carried out
in accordance with hospital ethics and guidelines and
patients were aware of details of the study; written
consenttopartakeforthis studywasobtained.
Semen collection and examination
Afterejaculatoryabstinenceof3–5days,semensamples
from patients and controls were collected in a sterile
plastic container and examined after 30 min according
to World Health Organization ‑2010 criteria.[18] Infertile
groups were classied based on sperm concentration,
motility, and morphology. Later, samples were
centrifuged at 3000 rpm for 10 min and seminal
plasmawas stored at −20°C forfructoseand citric acid
estimation.
Estimation of fructose
Fructose is the source of energy for spermatozoa
and acts as marker of seminal vesicle functionality.
20 µl of seminal plasma was mixed thoroughly with
220 µl distilled water, later the deprotinized with
50 µl of ZnSO4 and 50 µl of NaOH. After 15 min of
incubation, it was centrifuged at 2500 rpm and 200 µl
of clear supernatant was mixed with Indole reagent
followed by 32% hydrochloric acid. The mixture was
incubatedat60°Cfor 20minandaftercooling readings
weretakenat470nm.[32]
Estimation of citric acid
Seminal citric acid is the marker of prostate gland
functionality. 100 µl of seminal plasma and 100 µl
of 50% trichloro acetic acid were mixed cooled in
icebath.After centrifugation at 2000 rpm for 15 min,
800 µl of anhydrous acetic anhydride was added to
100µlofsupernatantandincubatedat60°Cfor10min
inawaterbath.Later,dry reagent grade pyridine was
added and incubated at 60°C for 40 min. Cooled on
ice bath for 5 min and absorbance was measured at
400nm.[33]
Statistical analysis
The data obtained were statistically interpreted and
expressed in mean and standard error of the mean.
Independent t‑test was used to nd whether the
signicant mean difference exists between patients
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Toragall, et al.: Biochemical indicators and male infertility
201
Journal of Human Reproductive Sciences ¦ Volume 12 ¦ Issue 3 ¦ July-September 2019
and controls along with Pearson correlation using
statistical program IBM SPSS Statistics software Inc.,
version20.0(Armonk,NY,USA:IBMCorp.).Statistical
interpretation was based on two‑sided tests at a 0.05
signicance level and correlation signicant at the 0.01
level(two‑tailed).

In the current study, the mean age of patients and
controls was 33.78 ± 0.42 and 32.56 ± 0.85 years,
respectively, at the time of diagnosis. The men
diagnosed with infertility problem were segregated
into seven different infertile conditions [Table 1]. All
infertileconditionsexhibitedsignicant mean difference
for sperm count and motility with controls (P < 0.05).
The fructose concentration was found higher in
oligoasthenoteratozoospermia (139.83±0.19) and
lower amongst asthenoteratozoospermia (47.85±2.74),
when compared with rest other infertile conditions.
Oligozoospermia(OL)hadnosignicantdifferencewith
control for mean fructose concentration, although rest
other conditions showed a fair signicance (P < 0.05).
AS+Tdisplayedhigher citric acid concentration when
compared with controls, whereas rest other conditions
exhibited marginal levels of citric acid. There was
a signicant difference among asthenozoospermia,
AS + T, and azoospermia (AZ) with respect to control
forcitricacidconcentration(P<0.05).However,overall
one‑way ANOVA result showed a signicant difference
for sperm count, motility, and citric acid level when
compared with controls (P < 0.05) except for fructose
concentrations [Table 2]. Pearson correlation results
exhibitedsignicantnegativecorrelationbetweensperm
count (r = −0.564), sperm motility (r = −0.574), and
fructoselevels.Whereasseminalcitricacidconcentration
hada positive correlation withspermcount (r = 0.458)
andspermmotility(r= 0.446)[Table3].

The aim of this study was to ascertain the correlation
between biochemical parameters in the seminal plasma
and sperm parameters in controls and infertile patients.
Our ndings showed that fructose concentration
decreasesasthe sperm concentration increases and vice
versa.[34]Thisisbecausefructoseisanenergyreservoir,[35]
and it is exploited by sperm for its metabolism and
motility.[36] The elevated fructose concentration in our
studywithrespect toAZ,OL+AS+T,OL,and severe
oligoasthenoteratozoospermia could be either because
of abridged sperm count, abnormal sperm morphology,
and decreased sperm activity resulting in decreased
utilization of fructose.[37,38] In our ndings, low fructose
concentration in AS + T [39,40] could be due to better
motilityofsperm or inammation of seminal vesicle,[41]
low levels of testosterone secretion,[42,43] or also due to
anatomical anomalies.[30] Our ndings revealed that
fructose concentration is negatively correlated with
sperm count and motility;[39] this correlation shows
the utilization of fructose by sperm.[40] The increase in
fructose content in teratozoospermia could be described
t

Patients (n)







Infertile(105) 25.35±2.33 21.70±1.38 95.68±4.09 42.16±1.22
Fertile(25) 62.40±4.45 43.04±0.70 104.29±2.79 36.70±1.65
Siglevel0.05 <0.05* <0.05* 0.31 0.03*
*P<0.05denesthelevelofsignicance.Allvaluesarepresentedasmean±SE.SE=Standarderror

Patients (n) Age
(years)








AS 26.66 33.39±0.97 50.93±3.99* 32.54±1.24* 50.83±2.51* 42.18±1.62*
AS+T 17.14 34.06±0.91 31.61±3.27* 29.94±1.77* 47.85±2.74* 60.99±3.28*
AZ 15.23 32.63±0.84 0.00±0.00* 0.00±0.00* 127.98±0.67* 31.74±0.99*
OL+AS+T 3.8 35.50±1.76 10.75±0.25* 15.25±4.94* 139.83±0.19* 39.60±1.46
OL 3.8 34.50±2.50 9.75±1.11* 27.25±5.04* 115.18±1.30 36.58±1.35
SOL+AS+T 19.04 25.20±0.85 5.05±0.71* 9.45±1.67* 135.90±0.68* 36.05±0.64
T 14.28 32.87±1.23 32.27±4.28* 31.33±1.40* 131.77±1.19* 41.01±2.62
Control ‑ 32.56±0.85 62.40±4.45 43.04±0.70 104.29±2.79 36.70±1.65
*P<0.05Denesthelevelofsignicance.Allvaluesarepresentedasmean±SE.n=Number,AS=Asthenozoospermia,
AS+T=Asthenoteratozoospermia,AZ=Azoospermia,OL+AS+T=Oligoasthenoteratozoospermia,OL=Oligozoospermia,SOL+AS+
T=Severeoligoasthenoteratozoospermia,T=Teratozoospermia,SE=Standarderror
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Toragall, et al.: Biochemical indicators and male infertility
202 Journal of Human Reproductive Sciences ¦ Volume 12 ¦ Issue 3 ¦ July-September 2019
byitslowutilizationbyspermatozoawithmorphological
defects.[40] Earlier studies reported that sperm with
abnormalmorphologymayhavepoororlackofmotility
and hence utilizes lower fructose.[30] The low levels of
fructoseinsemendisturbscoagulation,spermmovement
which could be due to genital tract inammation.[37,44]
The concentration of citric acid in seminal plasma acts
as a dependable measure of prostate gland secretion;
it plays a vital part in balancing osmotic equilibrium
of semen which will affect the membrane activity
and morphology of the spermatozoa.[40,45,46] Reduced
concentration of citric acid have been found in severe
or chronic prostatitis.[47] As it acts as gelling agent and
helps in liquefaction of semen, indirectly benet the
sperm motility.[48] In our ndings, symphonious to this,
sperm count and motility showed positive correlation
with citric acid.[48,49] In the current study, the negligible
difference in the concentration of citric acid was found
amongallinfertilepatientsexceptAS+T,whichcould
beduetoanimproperactivityofprostatic glands.[49]

Biochemical markers such as fructose and citric
acid can be used for the recognition of biological
attributes of semen which may assist in ourishing
novel standards that are precise in anticipating and
enhancing male fertility.These markers may not be a
pertinentindexofmalereproductivedysfunctionbutin
combination with alternative seminal characters could
present effective manifestation of male reproductive
function. Fructose is an indispensable liveliness
resource for metabolism and motility of sperm; its
absence is the mark of irregularity of seminal vesicle
or ejaculatory duct impediment. The loss of citric
acid in semen could be disablement of ejaculatory
channels and could be a prior indication of prostate
cancer. Therefore, evaluation of certain biochemical
markers of seminal uid may benet in understanding
the functionality of accessory glands which subsidizes
signicantlytotheseminalvolume.
Financial support and sponsorship
Nil.
Conicts of interest
Therearenoconictsofinterest.
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Motility 0.749** −0.574** 0.446**
Count −0.564** 0.458**
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**CorrelationissignicantattheP<0.01level(2‑tailed)
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Toragall, et al.: Biochemical indicators and male infertility
203
Journal of Human Reproductive Sciences ¦ Volume 12 ¦ Issue 3 ¦ July-September 2019
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