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Macedonian Journal of Medical Sciences. 2011 Dec
15;
4(4):380-387.
http://dx.doi.org/10.3889/MJMS.1957-5773.2011.0198
Basic Science
Telfairia Occidentalis, a Prophylactic Medicine for Alcohol‘s Damaging Effect on the Testis
Edidiong Akang, Ademola Oremosu, Olufunke Dosumu, Adedayo Ejiwunmi
Department of Anatomy, College of Medicine, University of Lagos, P.M.B.
12003, Lagos, Nigeria
Background: Concerns have been expressed about rising cases of male
infertility. Studies have shown that alcohol impairs sexual performance and
desire in men. It also affects sperm count lowering it and contributing to
fertility problems.
Aim: This study investigated the role of Telfairia occidentals
in the protection of the testis against alcohol induced damage.
Material and Methods: 30 male Sprague-Dawley rats were divided into
five groups of 6 each. They were administered distilled water, 30% v/v of
ethanol at 2g/kg body weight, 200 mg/kg, 400 mg/kg and 600 mg/kg of
Telfairia occidentalis, for 8 weeks after which their blood samples were
collected for hormonal assay. The testis and cauda epididymis were also
excised for histology and semen analysis.
Results: Alcohol depleted the germinal epithelium of the testis but
animals that received Telfairia occidentalis showed a better germinal
epithelial lining and a significant increase in semen parameters and hormone
levels.
Conclusion: Telfairia occidentalis demonstrated a prophylactic
effect on alcohol induced testicular damage and has improved semen quality.
In addition, it also improved serum testosterone and luteinizing hormone
levels.
...................
Citation: Akang E, Oremosu A, Dosumu O, Ejiwunmi A. Telfairia
Occidentalis, a Prophylactic Medicine for Alcohol‘S Damaging Effect on the
Testis. Maced J Med Sci. 2011 Dec 15; 4(4):380-387.
http://dx.doi.org/10.3889/MJMS.1957-5773.2011.0198.
Key words: Infertility; Ethanol; Serum testosterone; Luteinizing
hormone; seminiferous epithelium; sperm count; sperm motility.
Correspondence: Mr. Edidiong Nnamso Akang. Department of Anatomy,
College of Medicine, University of Lagos, P.M.B. 12003, Lagos, Nigeria.
Phone: +2348065299278. E-Mail: eltyeddy@yahoo.com
Received: 11-May-2011; Revised: 28-Oct-2011; Accepted: 29-Oct-2011; Online
first: 29-Nov-2011
Copyright: © 2011 Akang E. This is an open access article distributed
under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited.
Competing Interests: The authors have declared that no competing
interests exist.
‘Infertility is the inability of a sexually active, non-contracepting couple
to achieve pregnancy in one year’ [1]. It has been reported that about 25%
of couples fail to achieve conception within 1 year, 15% seek medical
treatment for infertility and less than 5% remain unwillingly childless [2].
Infertility affects both men and women. Literature suggests that disorders
in males and females account for an equal proportion of infertility [1].
Concerns have been expressed about rising cases of male infertility [3].
This can be as a result of congenital and acquired urogenital abnormalities,
infections of the genital tract, increased scrotal temperature (varicocele),
endocrine disturbances, genetic abnormalities and immunological factors [4].
Studies have shown that alcohol impairs sexual performance and desire. It
also affects sperm count lowering it and contributing to fertility problems
[5, 6]. Studies on human beings have even shown that alcohol intoxication
will at least temporarily reduce sperm count [7, 8]. In addition, there is
evidence suggesting that long term use of alcohol will lead to more
permanent damage, including a permanent reduction in sperm count [9,10].
Van-Thiel [9] reports that alcohol atrophies the cytoplasmic mass of Leydig
cells responsible for the secretion of the male sex hormone testosterone.
Wright et al. [10] reports low doses of alcohol to cause a 44% reduction in
testosterone levels.
Researchers have shown that when testosterone is decreased, Luteinizing
hormone [LH] levels do not increase but sometimes decrease [7, 11]. Alcohol
has also been reported to decrease the functioning of luteinizing hormone
releasing hormone (LHRH) receptors, resulting in diminished LH release.
Researchers have also reported that alcohol impairs the function of protein
kinase C, a key enzyme in LH production. Alcohol also impairs steps critical
to LH synthesis and secretion [7]. This affects sperm maturation which
depends on the level of testosterone available [12]. Alcohol has been
demonstrated to reduce synthesis of luteinizing hormone by its effect on the
pituitary-gonadonal axis [9]. Also, studies have shown that alcohol causes
most of its damage on the male reproductive system by inducing oxidative
stress caused by abundance of free radicals [7].
Telfairia occidentalis commonly known as fluted pumpkin has the
following chemical composition and functional properties: crude protein
(17.50 ± 0.12%), carbohydrate (17.96 ± 0.35%), ash (5.67 ± 0.10%) and high
percentage of crude fat (42.17 ± 0.27%) but low moisture content (6.67 ±
0.01%) [13]. Mineral composition revealed that the seed flour contains
mostly potassium (1824 mg/100 g wet sample) followed by magnesium (535
mg/100 g wet sample) and sodium (280 mg/100 g wet sample) phosphorus (21000
µg/g), calcium (280 µg/g), iron (69 µg/g) and manganese (1.80 µg/g). The
physicochemical analysis of the oil revealed an acid value of 3.56 ± 0.45,
saponification value of 188.24 ± 2.12, iodine value of 78.26 ± 1.24, free
fatty acid 4.50 ± 0.15, refractive index of 1.471 and tannins [14,15]. Fatty
acids were detected in the oil. The unsaturated fatty acids were composed
mainly of oleic (61.83%) and linoleic (16.44%) while the saturated fatty
acids mainly of palmitic acid (21.20%). It can be considered as a good
protein ingredient since it has a low gelation capacity of 14% (w/v),
foaming capacity 12.8 ± 1.10%, water and oil absorption capacities of 90.2 ±
0.2% and 183.4 ± 2.5%, respectively [13]. The seed proteins have minimum
solubility at pH 5.0 and is also rich in antioxidants like vitamin C and
vitamin A [16].
Telfairia occidentalis leaves have been reported by Nwangwa et al.
[17] to attenuate the testicular damage induced by quinine. It was also
found to reduce lipid peroxidation there by improving spermatogenesis [18].
This however disagrees with the findings of Oyeyemi et al. [19], who
reported that Telfairia occidentalis leaves have a destructive effect
on the testis. The aqueous extract of Telfairia occidentalis has been
shown to be hepatoprotective against garlic-induced oxidative stress [20].
The administration of Telfairia occidentalis seed oil decreased
plasma cholesterol levels, arteriosclerosis and other degenerative changes
in several organs including the heart, liver and kidney [21]. In an earlier
study, administration of Telfairia occidentalis increased sperm count
in Sprague-Dawley rats [22].
This study is therefore designed to investigate the protective ability of
Telfairia occidentalis seed oil over alcohol induced testicular damage.
Extract preparation
Healthy fruits of Telfairia occidentalis (fluted pumpkin) were
obtained from Mushin market, Lagos, Nigeria during the month of June, 2009.
It was authenticated in Lagos University herbarium (Voucher no - LUH 2763),
University of Lagos, Lagos. The naked seeds were dried in an oven in the
laboratory at 30°C for one week. The seeds were blended to a fine powder
using Maurine electric blender. The powder was preserved for extraction of
the oil samples. The oil extract of the plant samples was obtained using
petroleum ether in continuous extraction in a Soxhlet reflux apparatus [23,
24]. At the completion of extraction, the petroleum ether was completely
evaporated using a rotary evaporator at 35oC (Heidolph Laborota 4010
digital). The concentrated oil was the desired sample.
Administration of alcohol & extract
The animals received a daily administration of 30% v/v of alcohol at a dose
of 2 g/kg body weight via oral ingestion while Telfairia occidentalis
seed oil was administered intraperitoneally at 3 different doses: 200 mg/kg,
400 mg/kg and 600 mg/kg body weight daily.
The experimental animals
30 male Sprague-Dawley rats weighing 170-200 g (12-13 weeks old) were
randomly selected from the Laboratory Animal Center of the College of
Medicine, University of Lagos. The rats were fed on standard diet (Bendel
Feed and Flour Mills Ltd), water was given ad libitum and maintained under
standard conditions. The animal room was well ventilated with a temperature
range of 25 - 27oC under day/night 12-12 h photoperiodicity. The rats were
grouped into five groups (6 rats each) A, B, C, D and E. The use of the
animals was approved by the Experimental Ethics Committee on Animals Use of
College of Medicine, University of Lagos, Nigeria.
Experimental procedure
Group A (control) received distilled water, Group B received 30% v/v of
ethanol at 2 g/kg body weight while groups C, D and E received 30% v/v of
ethanol at 2 g/kg body weight with 200 mg/kg, 400 mg/kg and 600 mg/kg bw of
Telfairia occidentalis respectively for 8 weeks with ethanol
administered once every other day while Telfairia occidentalis was
administered once daily (6 days/week). At the end of administration, blood
was collected through the medial canthus of the eye into plain sample
bottles and centrifuged for 5000 rpm for 10 minutes to obtain clear sera for
hormonal assay. The rats were sacrificed by cervical dislocation and placed
on dorsal recumbence. The testicles were surgically removed through a lower
abdominal incision. It was freed of fats, weighed and histologically
examined. The epididymis was trimmed off the testis and semen sample was
collected from the cauda epididymis.
Routine histological preparation
The histology of the testes was done by modification of method described by
Kayode et al. [25]. The organs were harvested and fixed in 10% buffered
formalin [26, 27] for 24 hours after which it was transferred to 70% alcohol
for dehydration. The tissues were passed through 90% and absolute alcohol
and xylene for different durations before they were transferred into two
changes of molten paraffin wax for 1 hour each in an oven at 65 o C for
infiltration. They were subsequently embedded and serial sections cut using
rotary microtome at 5 microns. The tissues were picked up with albumenised
slides and allowed to dry on hot plate for 2 min. The slides were dewaxed
with xylene and passed through absolute alcohol (2 changes); 70% alcohol,
50% alcohol and then to water for 5 min. The slides were then stained with
haematoxylin and eosin. The slides were mounted in Canada balsam.
Photomicrographs were at magnifications of ×100.
Testicular weight
Weights of testes were taken before immersion in formalin using Scout (tm)
Pro SPU 2001, electronic weighing balance, manufactured by Ohaus
Corporation, Pine Brook, NJ USA.
Hormonal assay
The blood specimens from the subjects were collected into plain sample
bottles and were immediately centrifuged to separate the sera from the
cells. The sera were labelled and analysed. Testosterone and luteinizing
hormones were assayed using the enzyme immunoassay methods of DIAGNOSTIC
AUTOMATION, INC (2008) [28].
Sperm Motility Analysis
The slides on which the sperm cells were counted were warmed to 37°C until
the time of the analysis. The analysis was carried out at room temperature
using one epididymis of each rat. The percentage of sperm motility was
calculated using the number of live sperm cells over the total number of
sperm cells (both motile and non - motile], from two samples from one
epididymis of each rat. All sperm cells that were not moving at all were
considered to be non - motile, while the rest, which displayed some
movement, were considered to be motile [29].
Sperm count
This was achieved using the new improved Neubauer‘s counting chamber
(Heamatcytometer). The epididymal fluid from both epididymides was diluted
with physiological solution by adding 0.9 ml to 0.1 ml of the crushed
epididymides. The counting chamber was next charged with a cover slip until
a rainbow picture was seen at the edges. This chamber was then filled with
sperm fluid and placed under a binocular light microscope using an
adjustable light source. The ruled part was then focused and the number of
spermatozoa counted in five 16-celled squares. The total sperm cells were
added, divided by two and multiplied by 106 and expressed as (X) × 106/ml,
where X is the total number of sperm cells in the five 16-celled square
after dividing by two [30]
Statistics
The data obtained from all the groups were compiled and statistically
analyzed and expressed as mean ± standard deviation. Differences between
groups were compared using one way ANOVA, with p< 0.05 considered
significant. This was done using the SPSS software.
Hormonal Assay
There was a significant decrease in serum testosterone levels with animals
that received 8 weeks of ethanol (B) compared to those that received distil
water only (A) (Table 1). Animals that received 200 mg/kg of Telfairia
occidentalis and ethanol for 8 weeks (C) showed a decrease in serum
testosterone (p>0.05) but those that received 8 weeks of 600 mg/kg
Telfairia occidentalis and ethanol (E) showed a significant decrease
compared to control (A) p<0.05. The animals that received 200 mg/kg (C)
showed an increase in serum testosterone but those that received 400 mg/kg
(D) of Telfairia occidentalis with ethanol for 8 weeks showed a
significant increase compared to the group that received 30% v/v of ethanol
(B) p<0.05 (Table 1).
Table 1: Effect of Telfairia occidentalis on serum testosterone and
luteinizing hormones.
T.O.- Telfairia occidentalis; Values are mean ± standard deviation, * p<0.05
vs. control group; ** p<0.05 vs. Group B.
There was no significant difference in the LH of all experimental animals
compared to control except the animals that received 8 weeks of ethanol (B)
p<0.05. Groups that received 200 mg/kg, 400 mg/kg and 600 mg/kg of
Telfairia occidentalis with ethanol for 8 weeks showed significant
increases in LH when compared with those that received ethanol only (B)
p<0.05 (Table 1).
Testicular weight
There was a significant increase in the group that received 400 mg/kg of
Telfairia occidentalis and ethanol for 8 weeks (D), compared to those
that received only ethanol (B) p<0.05. There was a non significant increase
in the group that received 200 mg/kg of Telfairia occidentalis with
ethanol and there was also a reduction in the group that received 600 mg/kg
of Telfairia occidentalis and ethanol (E) compared to those that
received ethanol (B).
When the experimental animals were compared to control (A), there was no
statistically significant difference p>0.05 (Table 2).
Semen parameters
The animals that received 200 mg/kg and 400 mg/kg of Telfairia
occidentalis and ethanol (C and D respectively) showed a significant
increase in sperm motility compared to those that received just ethanol (B)
p< 0.05 (Table 2). Those that received 600 mg/kg of Telfairia
occidentalis with ethanol (E) showed a non significant decrease in
motility compared to those that received only ethanol (B) p> 0.05 (Table 2).
Table 2: Effect of Telfairia occidentalis on sperm motility, sperm count,
testicular weight.
T.O =Telfairia occidentalis; Values are mean ± standard deviation, * p<0.05
vs. control group; ** p<0.05 vs. Group B.
Animals that received ethanol for 8 weeks (B) showed a significant decrease
in sperm count compared to control (A) p <0.05 (Table 2). Also, those that
received 200 mg/kg and 600 mg/kg (C and E) of Telfairia occidentalis
and ethanol for 8 weeks showed a statistically significant decrease compared
to control (A) but the animals that received 400 mg/kg of Telfairia
occidentalis and ethanol showed statistically significant increase
compared to those that received ethanol (B) p<0.05. At 200 mg/kg of
Telfairia occidentalis, sperm count increased but decreased at 600 mg/kg
p>0.05 (Table 2).
Testicular Histology
The testicular histology of control animals (group A) reflects a well
arranged spermatogenic cell series with a normal interstitium (Figure 1).
Figure 1: Section through the testis of group A (control) at magnification
×100, showing interstitial cells of Leydig (I) with a well developed
spermatogenic series (S.S) and mature spermatozoa in the lumen (L) of
seminiferous tubule (S.T).
Animals that received 8 weeks of ethanol only (B) showed distortion in the
seminiferous tubules and necrosis of the seminiferous epithelium (Figure 2).
Figure 2: Section through the testis of group B (30% v/v of ethanol) at
magnification ×100, showing hypocellularity leading to an enlarged lumen
(L), a distorted epithelium (D.E) and a distorted interstitium (D.I).
There was however an improvement in animals that received 200 mg/kg and 400
mg/kg of Telfairia occidentalis, with ethanol as depicted in Figure 3
and 4 respectively compared to those that received ethanol only (Figure 2).
Figure 3: section of testis of group B (200 mg/kg bw of Telfairia
occidentalis. with ethanol) at magnification ×100, showing sperm sell in
Lumen (L)slight distortion of spermatogenic cell series (S.S) and
interstitial cells of Leydig (I) .
At 200 mg/kg of Telfairia occidentalis, the testis showed a normal
interstitium and a normal seminiferous epithelium in most of the tubules
(Figure 3).
Figure 4: Section of testis of group C (400 mg/kg bw of Telfairia
occidentalis. with ethanol) at magnification ×100, showing a good
spermatogenic cell series (S.S) with mature sperm cell in the lumen (L) and
a well differentiated seminiferous tubule (S.T) with interstitial cells of
Leydig in between them.
At 400 mg/kg of Telfairia occidentalis, the testis showed a normal
interstitium, normal seminiferous tubules and a well differentiated
seminiferous epithelium (Figure 4) but at 600 mg/kg of Telfairia
occidentalis, it showed a distorted seminiferous epithelium and lumen
(Figure.5)
Figure 5: Section of testis of group D (600 mg/kg bw of Telfairia
occidentalis with ethanol) at magnification ×100, showing a distorted
spermatogenic cell series (S.S), a distorted interstium (I) and a reduced
seminiferous tubule (S.T).
From the present study, chronic administration
of alcohol suppressed testosterone significantly with a concomitant decrease
in luteinizing hormone levels. This suggests that alcohol affected the
testosterone feedback system and the hypothalamic cells which produce
Luteinizing hormone releasing hormone (LHRH). Research with young (i.e.,
pubertal) male rats indicate that both acute and chronic alcohol exposure
result in profound testosterone suppression accompanied by lower or normal
luteinizing hormone (LH) and follicle stimulating hormone (FSH) levels, when
elevated levels are expected [7, 31]. This suggests that the hypothalamic
cells which produce LHRH do not function correctly when the feedback
normally provided by testosterone is removed (i.e., when testosterone levels
decrease). Thus, it appears that alcohol’s damaging effects on reproduction
are mediated at all three levels of the male reproductive unit: the
hypothalamus, pituitary, and testes.
Spermatogenic cells occupy 95 percent of
testicular volume. Therefore, failure ofspermatogenesis may be characterized
by testicular atrophy associated with oligospermia or azoospermia [10]. In
this study, it was observed that suppressed testosterone levels showed
simultaneous reduction in seminiferous epithelial growth and caused
oligospermia and athenospermia on chronic administration of 30% v/v of
ethanol. This is assumed to have led to testicular atrophy and hence the
loss of testicular weight. This agrees with Willis [32], Anderson [33] and
El-Ashmawy [34] who worked on 6%, 5% and 25% v/v of ethanol respectively and
showed that it had adverse effects on sperm motility, sperm count,
histological architecture and testicular weight. It however disagrees with
Wright et al. [10]. According to him, decreased production of steroid sex
hormones principally testosterone is characterized by loss of male secondary
sex characteristics, impotence, diminished libido and many other symptoms
but usually not a reduction in testicular size. It was also observed that
Telfairia occidentalis ameliorated the deleterious effects of alcohol on
the histology of the testis and sperm production. It proves to work
optimally at a dose of 400 mg/kg. This finding supports the report by
Nwangwu et al. [35], who reported that Telfairia occidentalis leaves
had regenerative effects on the testes and improves sperm production. This
could have been due to the presence of tocopherol (vitamin E), an
antioxidant [14]. Antioxidants like vitamin A, C and E have been said to
have good protective effects on the testis and hence improve male fertility
[36,37]. It is believed that this antioxidant property must have protected
the testis against lipid peroxidation caused by alcohol [34].
Linoleic acid, a polyunsaturated fatty acid
present in this oil is known to increase membrane fluidity and allows for
osmosis, intracellular and extracellular gaseous exchange [38].
Though they are easily susceptible to lipid
peroxidation, the presence of vitamin A prevents it [39]. Also, the presence
of oleic acid, a monounsaturated fatty acid also reduces the susceptibility
of the testis to lipid peroxidation [38,40]. This further explains the
results obtained at 200 mg/kg and 400 mg/kg body weight.
This study further revealed that at higher doses
(600 mg/kg), Telfairia occidentalis had adverse effects on testis and
sperm parameters compared to the lower doses. This could be due to the
presence of iron (Fe) in the oil. Iron, which though maintains proper cell
function, could also be a pro-oxidant when administered at high doses [15,
41]. Therefore, when combined with alcohol, it had a deleterious effect and
subjected the testis to more oxidative stress.
Tannins, though they are classified as
antioxidants, at a high dose, they could become pro-oxidant, increasing
lipid peroxidation [15, 42]. This explains for the drop in sperm count and
motility including the decline in hormone levels at a dose of 600mg/kg body
weight.
In conclusion, the present study demonstrates
the potential benefits of Fluted pumpkin (Telfairia occidentalis)
seed oil in ameliorating the deleterious effects of alcohol on the testes.
These benefits can be attributed to the antioxidant potentials of
Telfairia occidentalis which if developed can be added to the repertoire
of antioxidant supplements available today. Even though, animal studies
cannot be directly extrapolated to humans, the result from this present
investigation gives a clue to the possible outcomes in humans with ethanol
induced testicular damage.
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