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 Table of Contents  
ORIGINAL ARTICLE
Year : 2014  |  Volume : 27  |  Issue : 4  |  Page : 793-800

Effect of monosodium glutamate on the ovaries of adult female albino rats and the possible protective role of green tea


Department of Histology, Faculty of Medicine, Menofyia University, Menoufiya, Egypt

Date of Submission26-Jan-2014
Date of Acceptance03-Mar-2014
Date of Web Publication22-Jan-2015

Correspondence Address:
Mona Abd El Mawla Mohammed Soliman
Department of Histology, Faculty of Medicine, Menofyia University, Sheibin El Kom, Menoufiya
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.149773

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  Abstract 

Objective
The aim of this study was to determine the histological, histochemical, and immunohistochemical effects of monosodium glutamate (MSG) on the ovaries of adult female albino rats and the possible protective role of green tea.
Background
MSG is a commonly used food additive. It plays an important role in the pathogenesis of anovulatory infertility.
Materials and methods
A total of 35 female adult albino rats were used in this study. The rats were divided into four groups: groups I-IV. Group I was the control group. In group II (MSG treated) 10 rats were treated with MSG at a dose of 4 mg/g body weight by subcutaneous injection daily for 14 days. The rats were killed 24 h after MSG treatment. In group III [combined green tea extract (GTE) and MSG treated] 10 rats were treated with GTE and MSG for 14 days. MSG was given at the same dose as that in group II and GTE was given at 300 mg/kg body weight orally daily. The rats were killed 24 h after MSG and GTE treatment. In group IV (GTE treated) five adult rats were treated with GTE only for 14 days and then killed.
Results
MSG-treated rats showed degenerative changes of the ovary with many atretic follicles. The stroma appeared vacuolated. The medulla showed multiple vacuoles with congested blood vessels. However, combined treatment of GTE and MSG in group III showed amelioration of the histological changes in the ovary.
Conclusion
It has been concluded that GTE improves the histological changes caused by MSG in the ovary.

Keywords: Anovulatory infertility, atretic follicles, green tea extract, monosodium glutamate, ovary


How to cite this article:
Ali AA, El-Seify GH, El Haroun HM, Mohammed Soliman MA. Effect of monosodium glutamate on the ovaries of adult female albino rats and the possible protective role of green tea. Menoufia Med J 2014;27:793-800

How to cite this URL:
Ali AA, El-Seify GH, El Haroun HM, Mohammed Soliman MA. Effect of monosodium glutamate on the ovaries of adult female albino rats and the possible protective role of green tea. Menoufia Med J [serial online] 2014 [cited 2020 Feb 27];27:793-800. Available from: http://www.mmj.eg.net/text.asp?2014/27/4/793/149773


  Introduction Top


Female infertility is a very real medical problem. The female reproductive system is very sensitive to different harmful environmental factors [1]. A variety of environmental chemicals, industrial pollutants and food additives have been implicated as causing harmful effects. Most food additives act either as preservatives or as enhancers of palatability [2]. One such food additive is monosodium glutamate (MSG) [3].

MSG, also known as sodium glutamate, is a sodium salt of glutamic acid, a naturally occurring nonessential amino acid [4]. It is widely used not only in the food industry but also at homes and restaurants. This taste enhancer is present in flavored chips and snacks, soups or sauces (canned, packed), prepared meals, frozen foods and meals, fresh sausages, marinated meats and stuffed chicken, bottled soya or oriental sauces, manufactured meats, some hams, luncheon chicken, flavored tuna, vegetarian burgers and sausages [1].

The ovary is a paired, egg-producing reproductive organ found in female organisms. The ovaries also function in the production of various steroid and peptide hormones like estrogen and progesterone, which subserve many functions in the reproductive system. Abnormality in ovarian function usually leads to anovulatory infertility, which constitutes a major problem [5].

The effect of MSG on the female reproductive system has been studied by many investigators. They found that MSG plays a critical role in the pathogenesis of anovulatory infertility [5].

Natural herbs and its compounds present in the human diet have attracted extensive attention as chemopreventive and protective agents. In this study, selective green tea extract (GTE) will be used, made from leaves of the Theaceae family. Green tea contains good medical properties, associated with health benefits against multiple diseases including cancer, inflammation, atherosclerosis and cardiovascular disorders as it acts as an antioxidant [6].

However, its protective effect on MSG-induced ovarian damage has not been well studied.


  Materials and methods Top


Materials

Animals

Thirty-five adult female albino rats were used in this study. They were kept at the same environmental condition with free access to food and water ad libitum.

Drugs

  1. MSG was obtained from Sigma Company in the form of salt. It is given at a dose of 4 mg/g body weight by subcutaneous injection [1].
  2. GTE was obtained from the Technomade Group in the form of tablets. Each tablet contained 200 mg of GTE. It was given at a dose of 300 mg/kg body weight orally [7].


The rats were divided into four groups as follows:

Group I (control): This group comprised 10 adult rats that were left untreated. They were killed at the end of the experiment.

Group II (MSG treated): This group comprised 10 adult rats treated with MSG for 14 days. They were killed 24 h after MSG treatment.

Group III (combined MSG and green tea treated): This group comprised 10 adult rats treated with MSG and GTE daily for 14 days. They were killed 24 h after MSG and GTE treatment.

Group IV (green tea only treated): This group comprised five adult rats treated only with GTE daily for 14 days and then killed.

Methods

At the end of each determined period, the animals were killed, and both ovaries of each animal were excised. The weight of the ovaries was measured and they were fixed in 10% formol saline and processed for paraffin blocks. Sections of 5-6 mm were cut and stained with hematoxilin and eosin for routine histological examination [8], with Periodic Acid Schiff's reaction (PAS) and Masson's trichrome (MT) stain for histochemical study [8], and with estrogen receptor-b (ERb) and progesterone receptors (PR) for immunohistochemical study [9]. Morphometric study was carried out on H&E sections of different experimental groups (control and treated groups) by counting the number of different types of ovarian follicles. Primordial follicles were counted at a total magnification of 400, whereas other types of follicles were counted at a total magnification of 100. Ten readings were obtained for each specimen of all subgroups and the mean values were obtained.

Statistical analysis

The ovarian weight and the number of different types of follicles of the control and treated groups were recorded in the tables. The data were statistically analyzed using statistical package for social science, expressed as mean ± SE, and compared between two groups using Student's t-test. P values greater than 0.05 were considered nonsignificant; values less than 0.01 were considered highly significant; and values less than 0.05 were considered significant.


  Results Top


Histological results

Sections of control and GTE-only-treated rats had the same histological picture. The surface of their ovaries showed an irregular appearance. The ovary consisted of two distinct regions: an outer cortex full of growing follicles and an inner central medulla consisting of loose connective tissue containing blood vessels. The surface of the ovary was covered with germinal epithelium with tunica albugina beneath the epithelium. Primordial, primary, secondary, mature graafian follicles consisting of an enlarged oocyte surrounded by clear zona pellucida present at one side of the follicle surrounded by corona radiate with cumulus oophorus connecting it to the wall of the follicle, having wide cavity lined by cells of zona granulosa full of liquor folliculi appeared within the follicle appeared within the cortex. Corpous luteum formed of granulosa lutein cells and theca lutein cells could be seen.

Sections from MSG-treated rats showed multiple degenerated follicles within the cortex. These degenerated follicles had degenerated oocytes with pyknotic nuclei and vacuolated cytoplasm, which had a foamy appearance. The cells of the zona granulosa of the degenerated follicles appeared vacuolated. Some of these cells were exfoliated within the center of the follicles. The medulla appeared degenerated, having multiple vacuoles with congested blood vessels. Some blood vessels were full of hyaline material. Sections of MSG-treated and GTE-treated rats showed amelioration of the previous findings. The histological findings of this group were more or less similar to those of the control group [Figure 1]a-d.
Figure 1: (a) Photomicrograph of a control adult rat ovary showing secondary antral follicles. It consists of an enlarged oocyte (O) surrounded by clear zona pellucida (↓↓). Zona granulosa cells (ZG) formed of multilayers of cubical cells surround the follicle. Two cavities (A) full of liquor folliculi appear within the follicle. Flattened cells of the theca externa (TE) surround the follicle (H&E, ×400). (b) Photomicrograph of an adult rat ovary treated with green tea only for 14 days showing two ovarian follicles. The multilayered primary follicle consists of an oocyte surrounded by clear zona pellucida (↓↓). Multilayers of cubical cells forming the ZG surround the oocyte. The antral (secondary) follicle consists of an oocyte surrounded by clear zona pellucid (↓↓). Multilayers of cubical cells resting on clear basement membrane forming the ZG surround the oocyte. The cavity (A) appears at one side of the follicle (H&E, ×400). (c) Photomicrograph of an adult rat ovary treated with MSG for 14 days showing normal germinal epithelium covering the surface of the ovary (↓) consisting of a single layer of cubical epithelium. Degenerated follicles (DF) with degenerated oocyte appear within the cortex. Multiple vacuoles (V) appear in between cells of the ZG, which have pyknotic nuclei. Some cells appear exfoliated within the center of the follicle (arrow heads) (H&E, ×400). (d) Photomicrograph of an adult rat ovary treated with MSG and green tea for 14 days during the prepubertal period and left until puberty showing relatively normal mature Graafian follicle. It consists of a normal oocyte surrounded by clear zona pellucida. A single layer of columnar cells surround the oocyte forming corona radiate (arrow heads). Relatively normal cells of the ZG resting on a clear basement membrane (↓) surround the follicle. The oocyte is attached to the wall of the follicle by cumulus oophorus (CO). The cavity within the follicle is full of liquor folliculi (LF). Relatively normal TE surround the follicle (H&E, ×400).

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Histochemical results

PAS stain

PAS-stained sections of the control and GTE-treated group revealed moderate PAS-positive reaction in oocytes and strong reaction in the zona pellucida surrounding the oocyte.

Sections from the MSG-treated group showed weak reaction within the oocytes and their surrounding zona pellucid, which appeared interrupted in some follicles. Other degenerated follicles showed moderate PAS-positive reaction within their degenerated oocytes and their surrounding zona pellucida. Sections from the MSG-treated and GTE-treated group showed a histological picture more or less similar to that of the control group [Figure 2]a-d.
Figure 2: (a) Photomicrograph of a control adult rat ovary showing intense PAS-positive (magenta red) reaction in the surface epithelium (↓), in the zona granulosa (ZG) surrounding the follicles, and within the ovarian stroma (ST). There is a moderate reaction in oocytes (O).There is a strong reaction in the zona pellucida (↓↓) surrounding the oocyte (PAS, ×400). (b) Photomicrograph of an adult rat ovary treated with green tea only for 14 days showing intense PAS-positive reaction in the surface epithelium (↓), in the ZG surrounding the follicles, and within the ST. There is a strong reaction in the zona pellucida (↓↓) surrounding the oocyte. There is a moderate reaction in oocytes (PAS, ×400). (c) Photomicrograph of an adult rat ovary treated with MSG for 14 days showing moderate PAS-positive reaction in the ZG surrounding the follicles. There is a mild PAS-positive reaction within the ST. There is a weak reaction in the zona pellucida (↓↓) surrounding the oocyte that appear interrupted and within the oocyte in some follicles. Other degenerated follicles showed moderate PAS-positive reaction within their degenerated oocyte (DO) and their surrounding zona pelluicida (PAS, ×400). (d) Photomicrograph of an adult rat ovary treated with MSG and green tea for 14 days showing intense PAS-positive reaction in the surface epithelium (↓), in the ZG surrounding the follicles, and within the ST. There is a strong reaction in the zona pellucida (↓↓) surrounding the oocyte. There is a moderate reaction in oocytes. The cells forming the corpus luteum (CL) show moderate to strong PAS reaction (PAS, ×400). MSG, monosodium glutamate.

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Masson trichrome stain

MT-stained sections of the control and GTE-treated group showed collagen fibers around the follicles and within the ovarian stroma. Sections from the MSG-treated group showed mild increase in the amount of collagen fibers surrounding the ovarian follicles and within the ovarian stroma. The collagen fibers around the follicles were separated by wide spaces. Multiple vacuoles were present between the collagen fibers of the stroma, whereas sections from the combined MSG-treated and GTE-treated group showed collagen fibers around the follicles and within the ovarian stroma [Figure 3]a-d.
Figure 3: (a) Photomicrograph of a control adult rat ovary showing collagen fibers (arrows) appearing blue in color surrounding the ovarian follicles. Also, there are collagen fibers (C) within the ovarian stroma in between the follicles (MT, ×400). (b) Photomicrograph of an adult rat ovary treated with green tea only for 14 days showing collagen fibers (arrow) surrounding ovarian follicle. Others appear (C) within the ovarian stroma (MT, ×400). (c) Photomicrograph of an adult rat ovary treated with MSG for 14 days showing mild increase in the amount of collagen fibers surrounding the ovarian follicles and within the ovarian stroma. There are wide spaces (S) in between the collagen fibers (arrow) surrounding the degenerated ovarian follicles. Multiple vacuoles (V) appear separating collagen fibers within the ovarian stroma (MT, ×400). (d) Photomicrograph of an adult rat ovary treated with MSG and green tea for 14 days showing collagen fibers (arrow) surrounding the ovarian follicle (MT, ×400). MSG, monosodium glutamate.

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Immunohistochemical results

Sections from the control and GTE-treated group showed strong positive immunoreactivity for ERb and PR within the cells of the zona granulosa. Sections from the MSG-treated group showed negative immunoreactivity for ERb and PR within the cells of the zona granulosa. Sections from the combined MSG-treated and GTE-treated group showed strong positive immunoreactivity for ERb and PR within the cells of the zona granulosa [Figure 4]a-d and [Figure 5]a-d.
Figure 4: (a) Photomicrograph of an control adult rat ovary showing strong positive immunoreactivity for β-estrogen receptors within zona granulosa cells (PAP, ×1000). (b) Photomicrograph of an adult rat ovary treated with green tea only for 14 days showing strong positive immunoreactivity for β-estrogen receptors within zona granulosa cells (PAP, ×1000). (c) Photomicrograph of an adult rat ovary treated with MSG for 14 days showing negative immunoreactivity for β-estrogen receptors within zona granulosa cells (PAP, ×1000). (d) Photomicrograph of an adult rat ovary treated with MSG and green tea for 14 days showing strong positive immunoreactivity for beta estrogen receptors within zona granulosa cells (PAP, ×1000). MSG, monosodium glutamate.

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Figure 5: (a) Photomicrograph of a control adult rat ovary showing strong positive immunoreactivity for progestrone receptors within zona granulosa cells (PAP, ×1000). (b) Photomicrograph of an adult rat ovary treated with green tea only for 14 days showing strong positive immunoreactivity for progestrone receptors within zona granulosa cells (PAP, ×1000). (c) Photomicrograph of an adult rat ovary treated with MSG for 14 days showing negative immunoreactivity for progestrone receptors within zona granulosa cells (PAP, ×1000). (d) Photomicrograph of an adult rat ovary treated with MSG and green tea for 14 days showing strong positive immunoreactivity for progestrone receptors within zona granulosa cells (PAP, ×1000). MSG, monosodium glutamate.

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Quantitative and statistical results

Ovarian weight

The mean ovarian weight of adult rats treated with MSG for 14 days showed significant decrease as compared with adult control rats. The mean ovarian weight of adult rats treated with MSG and green tea for 14 days and that of adult rats treated with green tea only for 14 days showed a nonsignificant decrease as compared with adult control rats [Table 1].
Table 1: Descriptive statistics for mean and SD of ovarian weight in adult groups

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Morphometrical results

Rats treated with MSG for 14 days showed highly significant decrease in the number of primordial, primary, secondary, and mature graafian follicles with no corpus luteum but a highly significant increase in the number of atretic follicles as compared with control rats. Rats treated with MSG and green tea for 14 days and rats treated only with GTE for 14 days showed a nonsignificant decrease in the number of primordial, primary, and secondary follicles but a nonsignificant increase in the number of atretic follicles compared with control rats [Table 2] and [Table 3].
Table 2: Descriptive statistics for mean (X) and SD of the count of primordial, primary, secondary, mature Graafian, corpus luteum, and atretic follicles in different groups

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Table 3: Comparison between the control group and other studied groups as regards follicular counts

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  Discussion Top


MSG is a widely used flavor-enhancing food additive that may be present in packaged foods without appearing on the label [10]. Previous studies have indicated that MSG could exhibit harmful effects on the human body, including retinal degeneration, endocrine disorders, obesity, urticaria, addiction, stroke, epilepsy, brain trauma, neuropathic pain, schizophrenia, anxiety, depression, Parkinson's disease, Alzheimer's disease, Huntington's disease, and amyotrophic lateral sclerosis [11].

The effect of MSG on the female reproductive system has been studied by many investigators. They found that MSG plays a critical role in the pathogenesis of anovulatory infertility (1,5), but the mechanism of MSG action has not been explained well yet.

Natural herbs and its compounds that are present in the human diet have attracted extensive attention as chemopreventive and protective agents. In this study, we investigated the protective effects of green tea, which is a beverage that is second only to water in terms of consumption worldwide, made from leaves from the Theaceae family. Green tea contains good medical properties, is associated with health benefits against multiple diseases including cancer, inflammation, atherosclerosis and cardiovascular disorders, and acts as an antioxidant [6]. However, its protective effect on MSG-induced ovarian damage has not been well studied.

In this study, ovarian sections of rats treated with MSG for 14 days showed considerable structural changes, including multiple degenerated follicles with degenerated oocytes. The cells of the zona granulosa of degenerated follicles appeared vacuolated. Some of these cells were exfoliated within the center of the follicles. Stroma of the ovary showed multiple vacuoles with congested blood vessels. The medulla appeared degenerated, having multiple vacuoles with congested blood vessels. Some blood vessels were full of hyaline material. These histological results were confirmed by quantitative study, image analysis, and statistical analysis. These findings were in agreement with those of Bojanic and colleagues [1, 5, 12], who reported cystic degeneration of the ovary and degenerative and atrophic changes within the oocytes in rat ovaries after MSG treatment. The ovaries contained many atretic follicles with no corpora lutea. The stroma of ovaries showed multiple vacuoles with hyalinosis of arteriola.

The degeneration of ovarian follicles and their oocytes detected in this study might be due to oxidative stress caused by MSG. This agreed with the results of Ismail and colleagues [10],[13], who attributed ovarian pathologies after MSG treatment to oxidative damage. This could be explained by the fact that MSG leads to generation of oxygen-derived free radicals and related reactive oxygen species (ROS). These substances are dangerous for biological systems as they react with DNA, proteins, and lipids, leading to cellular damage as previously shown by Singh and Ahluwalia [14].

Recent studies have shown that glutamate receptors play a very important role in the pathogenesis of disorders induced by MSG. Glutamate is a predominant excitatory neurotransmitter in the mammalian central nervous system [15],[16]. There are two basic types of glutamate receptors: ionotropic (NMDA, kainite, and AMPA) and metabotropic (mGluR). Neurotoxicity of MSG is related to glutamate receptor activation [17],[18].

Congestion of blood vessels and hyalinosis of arteriola within the ovarian medulla may be due to the inhibition of prostaglandin synthesis, as these compounds are known to be involved in the regulation of blood flow. This is commensurate with the results of Ismail [10], who demonstrated congestion of testicular blood vessels following MSG treatment of male rats.

Vacuolation within the zona granulosa cells of the ovarian follicles, exfoliation of some of these cells within the follicular cavity, and vacuolation within the ovarian stroma and ovarian medulla might be signs of ovarian toxicity and cell degeneration. Also, these may be considered as a type of cellular defensive mechanism against injurious substances. These vacuoles could be responsible for collecting the injurious elements and preventing them from interfering with the biological activities of these cells as previously reported by El-Deeb and colleagues [19],[20].

PAS-stained ovarian sections of rats treated with MSG for 14 days showed moderate PAS-positive reaction within some oocytes with complete absence of zona pellucida, whereas other oocytes showed weak reaction with mild reaction in the zona pellucida surrounding them, which appeared interrupted. These results indicated reduction or even depletion of carbohydrates within the oocytes and their surrounding zona pellucida. These results were in accordance with those of Abd El-Mawla and colleagues [21],[22], who demonstrated marked depletion in carbohydrate content in the cortex and medulla of kidneys of MSG-treated rats.

Disturbances in carbohydrate metabolism could be suggested to be achieved by modifying the activities of the enzymes of the glycolytic pathways that lead to metabolic degradation and inhibition of carbohydrate synthesis in the ovarian follicles, as previously reported by El-Sherbiny et al. [23], who found marked decrease in glycogen content within the ovarian follicles after using certain insecticides.

MT-stained ovarian sections of rats treated with MSG for 14 days showed a mild increase in the amount of collagen fibers surrounding the degenerated ovarian follicles and within the ovarian stroma. Also, collagen fibers were separated from each other by wide spaces in between collagen fibers. This result was in agreement with those of Waer and Edress [24], who reported an increase in the amount of collagen fibers in liver cells after MSG treatment.

Immunohistochemical results of rats treated with MSG for 14 days showed negative immunoreactivity of zona granulosa cells for ERb and PR. This could be attributed to degeneration of granulosa cells of degenerated ovarian follicles due to toxicity of MSG. These cells were positive for ERb and PR, as previously reported by Salvetti et al. [25], who stated that ERb and PR were detected mainly in granulosa cells.

Ovarian sections of adult rats treated with MSG and GTE for 14 days and killed 24 h after treatment revealed two distinct regions within the ovary. An outer cortex showed multiple relatively normal primordial, growing follicles, mature Graafian follicles, and corpus luteum. The medulla occupied the central zone of the sections consisting of loose connective tissue containing blood vessels. These results were confirmed histochemically, immunohistochemically, and by quantitative and morphometrical studies. These findings were in agreement with those of Yousef [4], who stated that administration of green tea provided significant protection to kidney from the oxidative stress of MSG.

Green tea can protect against ovarian damage caused by MSG, as green tea consumed within a balanced controlled diet improves the overall antioxidative status and protects against oxidative damage, as previously reported by Erba et al. [26].

Ali et al. [27] demonstrated that the strong antioxidant properties of green tea are mainly attributed to the catechins EGCG and EGC. Catechins are characterized by their chemical structures that contribute to their effective antioxidant activity. These chemical structures include the vicinal dihydroxy or trihydroxy structure, which can chelate metal ions and prevent the generation of free radicals.

Kondo et al. [28] explained that this structure also allows electron delocalization, conferring high reactivity to quench free radicals. Under certain conditions, however, catechins may undergo auto-oxidation and behave like pro-oxidants. During the reactions of tea polyphenols with free radicals, several oxidation products are formed. Reactions of EGCG and other catechins with peroxyl radicals lead to the formation of anthocyanin-like compounds as well as seven-membered B ring anhydride dimers and ring-fission compounds. The B ring appears to be the principal site of antioxidant reactions.

Green tea preparations have been shown to trap ROS, such as superoxide radical, singlet oxygen, hydroxyl radical, peroxyl radical, nitric oxide, nitrogen dioxide, and peroxynitrite, reducing their damage to lipid membranes, proteins, and nucleic acids in cell-free systems. The radical quenching ability of green tea is usually higher than that of black tea, as previously reported by Khan et al. [29].

Mckady and Blumberg [30] demonstrated that green tea contains many compounds other than polyphenols (catechins and gallic acid, particularly) - for example, carotenoids, tocophenols, ascorbic acid (vitamin C), minerals such as Cr, Mn, Se, and Zn, and certain phytochemical compounds. These compounds could increase the antioxidant potential of green tea polyphenols.

It was found that green tea intake increases the activity of liver antioxidant enzymes such as glutathione peroxidase and oxidized glutathione, as well as reduce glutathione activity and improve the total antioxidant activity, as previously reported by Kiernan [8].

Consequently, trapping of ROS by green tea would contribute to the protection of the ovarian structure from the effect of MSG.

From the foregoing results, it is clear that MSG can induce many histological, histochemical, and immunohistochemical changes in the ovary. These changes can be ameliorated with the use of green tea. Thus, green tea can be recommended as a protective agent against MSG-induced ovarian damage, especially with the increasing use of MSG in restaurants (particularly mixed in noodles, soups, etc.), packaged food industries (e.g. instant meals), and household kitchens. It may be present in packaged foods without appearing on the label. Green tea is cheap, available, and has several health-promoting properties. These advantages could render it a protective agent.


  Acknowledgements Top


Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]


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