THE EFFECT OF PINEAPPLE (Ananas comosus) ON SEX HORMONES OF ADULT MALE RATS

THE EFFECT OF PINEAPPLE (Ananas comosus) ON
SEX HORMONES OF ADULT MALE RATS
Shrouk A. Showky ; Naeem M. Rabeh* and Hany G. EL-Masry
Nutrition and Food Science Department, Faculty of Home Economics, Helwan
University, Cairo, Egypt
*E-mail - naeemrabeh@gmail.com
Key Words: Pineapple (Ananas comosus), rats, sex hormones, lipid
profile, liver functions
ABSTRACT
Pineapple (Ananas comosus) has stimulatory effects on sex hormone
and semen production as well as sperm motility. The aim of the present
study was to investigate the effect of Pineapple (leaves, pulp and husk)
supplementation on sex hormones of adult male rats. Thirty adult male
albino rats, weighing about (180±5g) were divided randomly into two main
groups as follow: the first main group kept as negative control group (6 rats)
was fed on basal diet. The second main group (24 rats) were fed on basal
diet and given orally lead acetate, then divided into 4 subgroups as follow,
subgroup 2 (+ve control) fed on basal diet. Groups (3, 4 and 5) were fed on
basal diet supplemented with leaves, pulp and husk of dried Pineapple
at10% each, respectively. At the end of the experimental period (8 weeks),
semen was collected from each rat then, rats were scarified to obtain blood
then serum was collected for biochemical analyses. Results indicated that
Pineapple supplementation either leaves, pulp, or husk significantly
(P<0.05) improved the serum concentrations of (testosterone; FSH), total
antioxidant, CAT and significantly decreased MDA, as well as improving
liver functions and lipid profile. Moreover, significant improvement in
semen analysis were observed as Pineapple supplementation. It could be
recommended that incorporating pineapple (leaves, pulp and husk) in a
healthy normal diet is essential to boost fertility in adult male rats.
INTRODUCTION
Infertility is a prevalent condition affecting an estimated 70 million
people globally. The World Health Organization estimates that 9% of
couples worldwide struggle with fertility issues and that male factor
contributed to 50% of the issues. Male infertility has different causes,
ranging from genetic mutations to lifestyle choices to medical illnesses or
medications (Fainberg and Kashanian, 2019).
Pineapple (Ananas comosus) is the third most essential fruit crop in
the tropical and subtropical regions of the world, only preceded by banana
and citrus. Pineapple is an essential source of sugars, organic acids and
some important minerals for human nutrition and its quality of good flavor,
aroma, juiciness and sweetness is well known and appreciated by
consumers. Moreover, pineapple is also rich in health-promoting
Egypt. J. of Appl. Sci., 36 (7-8) 2021 60-72
antioxidants, such as ascorbic acid, flavonoids, and other phenolic
compounds related to antioxidant activities (Lu et al., 2014).
Pineapple has stimulatory effects on sex hormone and semen
production (Siddiq et al., 2012) as well as sperm motility. It also exerts
protective effects on the semen during the freezing process for storage. The
July-August 2009 issue of "Oxidative Medicine and Cellular Longevity"
features a study from Indian researchers, which correlates manganese
consumption in pineapple juice and other foods with increased sperm
movement. It also protected sperm during freezing for storage, which can
raise conception chances (Debnath et al., 2012).
One hundred grams of this fruit allows covering about 80% of the
daily demand for vitamin C. Other substances present in the pineapple that
are worth mentioning involve folate (18 μg) and beta-carotene (35 μg)
(Zdrojewicz et al., 2018). Pineapple also is a good source of vitamin B1,
vitamin B6 (Hossain et al., 2015). It was recorded that vitamin B
deficiencies, involving vitamin B6, are linked with gonadal abnormalities in
males, such as altered spermatogenesis (Forges et al., 2007and Vujkovic et
al., 2009). Throughout the pineapple production and consumption chain,
several tons of by-products are produced, which, in most cases, are
discarded as waste (Sznida, 2018).
Therefore, this study was conducted to evaluate the effect of dried
Pineapple (leaves, pulp and husk) supplementation on sex hormones of adult
male rats.
MATERIALS AND METHODS
Materials:
Pineapple with its leaves was purchased from local market in
Cairo, Egypt. Casein, cellulose, choline bitartrate, D-L methionine,
vitamins and minerals were obtained from El-Gomhoriya Pharmaceutical
Company. Chemical kits were purchased from Gama Trade Company for
Chemical, Cairo, Egypt. Starch, corn oil and sucrose were obtained from
the Egyptian local market. Thirty adult male albino rats (Sprague-Dawley
strain), weighing about (180±5 g) were obtained from Helwan
Experimental Animals Station., Egypt.
Methods:
1- Botany of Pineapple (Ananas comosus): Pineapple belongs to the
order Bromeliales, Family: Bromeliaceae, Genus: Ananas, Species:
A. comosus. This classification was carried out at the Agricultural
Research Center, Giza, Egypt.
2. Preparation of Dried Pineapple: Pineapple leaves, pulp, and flesh
(husk) were dried by solar energy At the National Research Center,
Dokki, Egypt.
3. Induction of impaired fertility: lead acetate was dissolved in 5 ml
of distilled water and were administered orally (once daily at 9.00
61 Egypt. J. of Appl. Sci., 36 (7-8) 2021
am) to male rats at 100 mg/kg BW of rats for 4 weeks (Nkechi et al.,
2015).
4. Diet Composition and Experimental Animal Design: The basal
diet was formulated according to AIN-93M diet (Reeves et al.,
1993). Animals (30 rats) were housed in well conditions in
biological studies lab of Faculty of Home Economics. They were left
for seven days as adaptation period, and they were allowed to feed
standard laboratory food and water. After the period of adaptation,
animals were divided into 2 main groups, as follows: - the first main
group (6 rats) was fed on basal diet and served as a negative control
group (-ve), the second main group (24 rats) was fed on basal diet
and given orally lead acetate then was divided into 4 subgroups,
subgroup 2 (+ve control) fed on basal diet. Groups (3, 4 and 5) were
fed on basal diet supplemented with leaves, pulp and husk of dried
Pineapple at10% each, respectively.
At the end of the experimental period (8 weeks), rats were fasted
overnight before scarifying and blood samples were collected from
each rat and were centrifuged at 3000 rpm for 15 min to obtain the
serum for biochemical analysis.
5. Biological Evaluation: Feed intake (FI), body weight gain percent
(BWG%) and feed efficiency ratio (FER) were determined
according to Chapman et al., (1959) using the following equation:
BWG% = Error! × 100
FER = Weight gain / Feed intake.
6. Biochemical Analysis of Serum:
Follicular stimulating hormone (FSH) and testosterone level were
determined according to Loraine and Bell (1976) and Wilke and
Utley (1987), respectively. Aspartate aminotransaminase (AST) and
Alanine aminotransaminases (ALT) were determined according to the
method described by Bergmeyer et al., (1978), and Alkaline
phosphates (ALP) was determined according to Belfield and
Goldberg (1971). Total antioxidant and Malondialdehyde (MDA)
were determined according to Benzie and Strain, (1998) and Placer
et al., (1966), respectively. Serum total cholesterol (TC), triglyceride
(TG), high density lipoprotein cholesterol (HDL-C) were determined
according to Richmond, (1973); Wahlefeld, (1974) and Albers et
al., (1983), respectively. Regarding to serum low density lipoprotein
cholesterol (LDL-C) and very low-density lipoprotein cholesterol
(VLDL-C) were calculated according to Fridewald et al., (1972).
7. Semen Analysis: Semen analysis was determined according to
Adamkovicova et al., (2016).
Egypt. J. of Appl. Sci., 36 (7-8) 2021 62
8. Statistical Analysis: The obtained results were analyzed according
to SPSS program (The statistical package for social sciences,
version 20.0, Inc., Chicago, Illinois, USA). ANOVA test were used
to compare results among groups and Psignificant (Snedecor and Cochron, 1989).
RESULTS AND DISCUSSION
Herbal medicine is commonly used to treat male infertility, and it
has been demonstrated in vivo (Kim et al., 2013). It’s a good idea to look
for any alternative measures that use dietary components with the fewest
side effects as a supplement to reduce treatment costs and other unwanted
effects. So that, this study was conducted to investigate the effect of dried
Pineapple (leaves, pulp and husk) supplementation on sex hormones of
adult male rats. Pineapple is high in minerals and vitamins. In addition,
pineapple has been shown to have anti-inflammatory and antioxidant
properties (Mohd et al., 2020).
Results of Table (1) showed a significant increase in the IBW for
all groups as compared to the negative control group. Statistically
significant increase(P<0.05) in the mean value of FBW (gm), for the rats
that fed basal diet and supplemented with various derivatives of
pineapple, as compare to +ve group. On the other hand, there was
statistically significant increase (P<0.05) in the mean value of BWG% as
compared to +ve group. As regard to FER, there was statistically
significant difference (P<0.05) in the mean value of FER for the treated
rats as compared to +ve control group. Pulp pineapple gave the best
improvement in BWG% and FER as compared to other derivatives of
pineapple.
Table (1): Effect of pineapple leaves, pulp and husk supplementation
on body weight status in adult male rats
FER
FI
(g/d/rat)
IBW (g) FBW(g) BWG%
Parameters
Groups
0.054±0.03a 21.19±1.45 15.3 a 209.3±2.60 a 172.33±2.33 b Control (-ve)
0.011±0.05d 3.41±1.70 12.0 d 186.1±1.98 c 180.00±1.73 a Control (+ve)
0.032±0.03bc 11.62±1.41 14.5 bc 198.6±2.02 b 178.00±1.52 a Leaves
0.042±0.04ab 15.55±1.59 15.0 b 206.7±3.52 ab 178.83±1.09 a Pulp
0.027±0.03c 9.36±1.29 14.2 c 198.5±2.18 b 181.66±1.45 a Husk
Results are expressed as mean ± SE.
Values in each column which have different letters are significantly different at
(P<0.05).
The current results Table (2) showed statistically significant
(P<0.05) improvement in serum sex hormones of adult male rats
(testosterone and FSH) that fed basal diet and supplemented with various
derivatives of Pineapple. It was observed that there was no significant
difference in serum testosterone between pineapple leaves and pineapple
husk, while there was a significant increase (P<0.05) in the mean value
of testosterone for the rats fed pulp pineapple as compared to the
63 Egypt. J. of Appl. Sci., 36 (7-8) 2021
pineapple leaves or husk group. On other hand, there was a significant
difference in the mean of FSH among the treated groups. The best
improvement in the concentration of testosterone and FSH was recorded
at the group that fed pulp of pineapple.
Table (2): Effect of pineapple leaves, pulp and husk supplementation
on serum sex hormones of adult male rats
Testosterone (ng/ml) FSH (ng/ml)
Parameters
Groups
16.43±0.33a 2.02±0.03 c Control (-ve)
9.86±0.22d 1.38±0.08 d Control (+ve)
13.61±0.32b 4.40±0.20 b Leaves
17.03±0.15a 5.08±0.22 a Pulp
11.88±0.35c 4.08±0.20 b Husk
Results are expressed as mean ± SE.
Values in each column which have different letters are significantly different at
(P<0.05).
Maintaining a sufficient intra-testicular testosterone concentration
is critical for testicular function, particularly spermatogenesis
(Woolveridge et al., 1998). When comparing the control and treated
groups in Leko et al., (2021) study, there was a statistically significant
difference in testosterone hormone levels; the rats that received
aluminium chloride and a high dose of pineapple juices had the highest
value and the negative control group that received aluminium alone had
the lowest. Pineapple juices boosted testosterone in a dose-dependent
way, implying that they improved male fertility. One cup of pineapple
juice contains 1.3 mg of manganese (Debnath et al., 2012), which is
enough to meet up to 73 percent of daily needs (Hossain et al., 2015). At
55 days of age, the rats given the 25 mg/kg dose had higher levels of LH,
FSH, and testosterone. Furthermore, there was a concurrent rise in both
daily sperm production and spermatogenesis efficiency (P<0.05),
indicating a Mn-induced spermatogenesis acceleration (Lee et al., 2006).
Results of Table (3) showed statistically significant
increase(P<0.05) in antioxidant status regarding total antioxidant and
CAT and a significant decrease (P<0.05) in MDA in adult male rats that
fed with various derivatives of Pineapple. As regard T. Antioxidant,
CAT, MDA there was statistically significant difference (P<0.05) for the
rats that fed with various derivatives of pineapple. The most
improvement of antioxidant status was observed at the rats fed on pulp
pineapple as compared to the treatments.
Because large amounts of reactive oxygen species and poor
antioxidant status have been linked to infertility, treatment focused on
ways to improve the reproductive microenvironment's exhausted
antioxidant defense is logical (Adeoye et al., 2018).
Egypt. J. of Appl. Sci., 36 (7-8) 2021 64
Table (3): Effect of Pineapple Leaves, Pulp and Husk on T.
antioxidant, CAT and MDA in Adult Male Rats
CAT ( MDA (nmol/ml)
T. Antioxidant (n
mol/ml)
Parameters
Groups
2.92±0.04d 130.96±2.21 a 1.02±0.03 c Control (-ve)
6.33±0.38a 76.43±3.03 d 0.57±0.05 d Control (+ve)
3.93±0.12c 107.50±1.09 b 1.65±0.05 b Leaves
3.16±0.13d 123.33±3.33 a 2.04±0.10 a Pulp
4.75±0.20b 91.16±3.76 c 1.03±0.08 c Husk
Results are expressed as mean ± SE.
Values in each column which have different letters are significantly different at
(P<0.05).
The MDA level was reduced by 60.16 % after treatment with
pineapple peel extract at 2.5 mL/kg bw. This was found to be more
efficacious than a double-dose treatment (5.0 mL/kg bw). Treatment with
2.5 mL/kg bw pineapple peel extract increased catalase activity by 87.46
%, but treatment with a twofold dose (5.0 mL/kg bw) lowered activity by
32.67 % (Okafor et al., 2011). Pineapple manganese content also is a
cofactor for several enzymes involved in energy synthesis and
antioxidant activities (Siddiq et al., 2012).
Bromelain found in the pineapple, is a proteolytic enzyme that
can act as an antioxidant (Saptarini et al., 2019). Effects of bromelain on
oxidative stress indicators in dichlorvos-intoxicated mice’s serum were
studied by Agarwal et al., (2016).
Results of Table (4) showed statistically significant improvement
in liver function parameters regarding ALT, AST and ALP levels in adult
male rats that fed with various derivatives of Pineapple as compared to
+ve control group.
It was clear that, there was no significant difference in serum
AST, ALT and ALP between the groups fed either dried pineapple leaves
or pulp. Also, no changes in the mean of AST and ALT between the
groups fed either dried leaves or pulp of pineapple. pineapple Pulp gave
the most improvement of liver functions.
Aminotransferase readings can be used to assess seminal quality,
with the AST/ALT ratio being used to differentiate between different
kinds of azoospermia according to (Buitrago et al., (1981). A
considerable reduction in AST (99.8%) and ALP (56.53 %) levels was
seen after treatment with pineapple peel extract at 2.5 mL/kg bw. While;
Treatment with 2.5 mL/kg bw pineapple peel extract resulted in a rise in
ALT levels. However, a double dose (5.0 mL/kg bw) resulted in a 10.06
% reduction (Okafor et al., 2011).
65 Egypt. J. of Appl. Sci., 36 (7-8) 2021
Table (4): Effect of pineapple leaves, pulp and husk supplementation
on liver functions in adult male rats
Parameters AST ALT ALP
Groups (μ/L)
79.90±4.93c 26.53±0.64 c 64.82±3.24 d Control (-ve)
104.33±1.65a 37.83±0.99 a 93.46±1.99 a Control (+ve)
83.13±1.60c 31.96±0.96 b 80.07±1.15 bc Leaves
80.63±3.67c 28.36±0.84 c 74.53±1.81 c Pulp
93.47±1.84b 34.40±0.55 b 84.62±2.47 b Husk
Results are expressed as mean ± SE.
Values in each column which have different letters are significantly different at
(P<0.05).
A significant improvement (P<0.05) in lipid profile as shown in
Table (5) in adult male rats that fed basal diet supplemented with various
derivatives of Pineapple by reducing the mean value of TC, TG, LDL-C
and increasing the level of HDL-C as compared to +ve group. Moreover,
there was a significant difference (P<0.05) among the three treated
groups for lipid profile. The lowest value TG, LDL-C and VLDL-C and the
highest value of HDL-C; were found in Group that fed on Pineapple Pulp
followed by Pineapple husk,
Many animal studies have shown that hypercholesterolemia,
steroidogenesis, and male fertility are linked (Xu et al., 2007 and
Whitfield et al., 2015). Serum VLDL, total triglyceride, and testosterone
levels were all found to be strongly linked to sperm motility (Ergün et
al., 2007).
Table (5): Effect of pineapple leaves, pulp and husk supplementation
on lipid profile of adult male rats
Parameters TC TG VLDL-C HDL-C LDL-C
Groups (mg/dl)
15.77±4.31de 48.00±1.61 a 50.53±0.74 10.10±0.14e e 73.88±3.17 c Control (-ve)
54.39±1.72a 23.30±0.52 d 15.00±0.42 a 75.04±2.14 a 92.70±1.68 a Control (+ve)
20.72±0.86c 37.63±1.28 b 12.71±0.42 c 63.56±2.10 c 71.06±0.63 cb Leaves
9.60±2.22d 44.86±1.48 a 11.49±0.23 d 57.46±1.16 d 65.96±0.92 d Pulp
34.72±1.51b 32.43±1.14 c 13.09±0.15 b 69.53±0.75 b 81.06±1.59 b Husk
Results are expressed as mean ± SE.
Values in each column which have different letters are significantly different at
(P<0.05).
Gallic acid, gentisic acid, syringic acid, vanillin, ferulic acid,
sinapic acid, isoferulic acid, and o-coumaric acid are among the eight
phenolic chemicals found in pineapple fruits (Yapo et al., 2011). In
obese mice, gallic acid lowered body weight and serum triacylglycerol
(McGarry and Brown, 1997). Pineapple has a high fat binding capacity
(FBC), which is significant for detecting anti-obesity properties in diet.
Bromelain has been shown to be beneficial in the treatment of stoutness
Egypt. J. of Appl. Sci., 36 (7-8) 2021 66
in a few clinical studies (Mohamed et al., 2014). When compared to the
obese group, pineapple extract was found to enhance HDL levels,
indicating that pineapple may be able to reduce the risk of lipid-related
disorders (Emmanuel et al., 2016). The reduction in blood cholesterol in
the pineapple juice groups in the study of El-Shazly et al., (2018) was
accompanied by a reduction in the LDL percentage. As a result, it lowers
the atherogenic index, presumably through improving LDL catabolism
via hepatic receptors (Xie et al., 2005).
Regarding to Semen analysis, Results of Table (6) showed
statistically significant (P<0.05) improvement in semen analysis (normal
count as well as abnormal count) in adult male rats that fed with various
derivatives of Pineapple as compared to +ve control group. There was no
significant difference in the mean value of normal and abnormal semen
analysis, for the rats that fed either dried pineapple leaves or husk. The
highest normal semen count was observed at the group fed on pineapple
pulp as compared to the other treatments
Table (6): Effect of pineapple leaves, pulp and husk supplementation
on semen of adult male rats
Normal (%) Abnormal (%)
Parameters
Groups
12.38±4.01d 87.62±4.01 a Control (-ve)
46.90±2.46a 53.10±2.46 d Control (+ve)
34.26±1.46b 65.73±1.46 c Leaves
24.06±2.70c 75.93±2.70 b Pulp
36.01±2.02b 63.99±2.02 c Husk
Results are expressed as mean ± SE.
Values in each column which have different letters are significantly different at
(P<0.05).
Because of its stimulatory effects on sex hormone and semen
production (Siddiq et al., 2012), as well as sperm motility, pineapple
juice may be utilized to promote fertility by improving semen quality
(Hossain et al., 2015). It also protects the sperm throughout the freezing
process so that it may be stored (Debnath et al., 2012). In agreement
with these results recently, Leko et al., (2021) found that the rats fed
with pineapple juice had significantly higher concentration counts, motile
counts, progressive assessments, and morphology, indicating good
spermatogenesis and testicular steroidogenesis.
One hundred gram of fresh pineapple ripe contains 11 mcg of
folic acid and 5 mcg of folic acid present in syrup. One ripe pineapple
fruit can supply about 16.2% of daily requirement for vitamin C in an
adult. Furthermore, half a glass of pineapple juice provides up to 28 mg
of vitamin C (Debnath et al., 2012). Pineapple also is a good source of
vitamin B1, vitamin B6 (Hossain et al., 2015). Because they both operate
together in the process of DNA creation and the creation of S-adenosyl
methionine, vitamin B and folate are effective markers of male fertility
67 Egypt. J. of Appl. Sci., 36 (7-8) 2021
(Froese et al., 2019). Vitamin C supplementation in infertile men
improved sperm count, motility, and morphology, suggesting that it
could be used as a supplement to increase sperm quality in the lead up to
conception according to Akmal et al., (2006).
From the above-mentioned results it could be conducted that,
Pineapple (Ananas comosus) supplementations have raising sex
hormones productions also shown possible capacity to positively
influence male fertility directly and indirectly by affecting lipid profile
lowering cholesterol, triglycerides, LDL while raising HDL beside
enhancing antioxidant effects against free radicals through beneficial
effects of its contents of bromelain and other vitamins and minerals.
To boost fertility in adult male rats, incorporate pineapple
derivatives in a healthy normal diet as a rich source of antioxidant
compounds. People with infertility should have to eat pineapple;
pineapple is a wonderful fertility super food because it is inexpensive and
readily available in most shops.
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تأثير الأناناس عمى الهرمونات الجنسية لذکور الفئ ا رن البالغة
شروق أحمد شوقي ، نعيم محمد ا ربح ، هاني جابر المصري
قسم التغذية وعموم الأطعمة .کمية الاقتصاد المنزلي. جامعة حموان
الأناناس لديو تأثي ا رت تحفيزية عمى اليرمونات الجنسية وانتاج السائل المنوي وکذلک عمي
حرکة الحيوانات المنوية. لذلک کان اليدف من ىذه الد ا رسة ىو معرفة تأثير التدعيم بفاکية
الأناناس )قشور، وأو ا رق ، المب( عمى اليرمونات الجنسية لذکور الفئ ا رن البالغة. تم تقسيم ثلاثين
5 جم( بشکل ± وزنيا حوالي ) 081 ، )Sprague-Dawley من ذکور الفئ ا رن البالغة )سلالة
عشوائي إلى مجموعتين رئيسيتين عمى النحو التالي: المجموعة الأولى )المجموعة الضابطة
السالبة وتحتوي 6 فئ ا رن( تم تغذيتيا عمى النظام الغذائي الأساسي. تم تغذية المجموعة الثانية
42 فأ ا ر( عمى نظام غذائي أساسي يحتوي عمى أسيتات الرصاص ، ثم قسمت إلى 2 (
5(. المجموعة الفرعية ) 4( تم تغذيتيا عمى النظام الغذائي الأساسي - مجموعات فرعية من ) 4
فقط. المجموعة الفرعية الثالثة وال ا ربعة والخامسة تغذت عمى الغذاء الاساسي المدعم بمسحوق
أو ا رق ، قشر ، المب الاناناس بنسبة 01 ٪ عمى التوالي. في نياية فترة التجربة ) 8 أسابيع( تم
جمع عينة من الحيوانات المنوية من کل فأر ، وتم الحصول عمي الدم وطرده مرکزيا لمحصول
عمي السيرم لاستخدامو في التحاليل البيوکيميائية.
أشارت النتائج إلى أن التدعيم بالأناناس سواء ) الاو ا رق، القشر او المب( ادي الي
نسبة مضادات الأکسدة ،)FSH تحسن معنوي في ترکي ا زت )ىرمون التستوستيرون ، ىرمون
الکمية، الکاتاليز و ادت الي حدوث انخفاض معنوي في المالونداىايد، کما ادت الي تحسن في
وظائف الکبد وصورة الدىون . علاوة عمي ذلک تم ملاحظة تحسين معنوي في تحميل السائل
المنوي. وبذلک يمکن التوصية بأن ادخال فاکية الأناناس ) المب، الاو ا رق، المب( في نظام
غذائي صحي طبيعي ضروري لزيادة الخصوبة لدى ذکور الفئ ا رن البالغة.
Egypt. J. of Appl. Sci., 36 (7-8) 2021 72