Black Tea Aqueous Extracts Improve Human Sperm Functions: An <i>In Vitro</i> Study

Setumo, M. A.; Choma, S. S. R.; Henkel, R.; Opuwari, C. S.

doi:https://doi.org/10.1155/2023/4323458

Andrologia

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Abstract Introduction Materials and Methods Results Discussion Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 4323458 | https://doi.org/10.1155/2023/4323458

Black Tea Aqueous Extracts Improve Human Sperm Functions: An In Vitro Study

M. A. Setumo,¹S. S. R. Choma,¹R. Henkel,^2,3,4and C. S. Opuwari²

Academic Editor: Shuiqiao Yuan

Received23 Dec 2022

Revised27 Sept 2023

Accepted06 Dec 2023

Published22 Dec 2023

Abstract

Infertility affects about 25% of couples worldwide, and oxidative stress (OS) is linked to its idiopathic etiology. Green, black, white, and oolong teas are produced from Camellia sinensis, depending on their oxidation level, and contain antioxidant properties that may enhance male reproductive functions. The study aimed to investigate the effects of black tea aqueous extract on human sperm functions in vitro. Semen samples were collected from donors, liquefied, analyzed, and divided into normal (n = 40) and abnormal (n = 19) groups using the World Health Organization 2010 criteria. Samples were washed and incubated with black tea aqueous extracts (0, 0.4, 4, 40, 405 μg/ml) for 1 hr and analyzed. Along with a considerable decrease in intracellular reactive oxygen species (ROS) production, DNA-fragmented spermatozoa, and acrosome reaction, the percentage of sperm vitality and intact mitochondrial membrane potential (MMP) increased (). Furthermore, compared to the normal group, a substantial increase in the percentage of acrosome reaction, ROS production, and percentage of spermatozoa with fragmented DNA, while a reduction in the percentage of intact MMP and sperm vitality, was noted in the abnormal group (). Compared to the controls, there was no significant change in motility between the normal and abnormal groups (). Black tea’s antioxidant activity, caffeine concentration, or both may have contributed to its improvement in human sperm function in vitro.

1. Introduction

The inability to conceive after regular unprotected sexual intercourse for 12 months in a woman under age 35 or after 6 months in a woman over the age of 35 is described as infertility [1]. In addition, infertility may be characterized as primary infertility, where a couple never had a child or secondary infertility, where a couple fails to achieve pregnancy following a successful conception [2]. Approximately 25% of couples worldwide are affected by infertility, which affects one in six couples. Of these, 30%–50% are ascribed to the male factor [3, 4]. According to Agarwal et al. [5], infertility affects about 20%–30% of men globally, of which 10%–20% of male factors are idiopathic. Compared to their fertile counterparts, males with idiopathic infertility are commonly diagnosed with oxidative stress (OS) [6]. An imbalance between the capacity of the available antioxidants to scavenge reactive oxygen species (ROS) and the formation of ROS can lead to OS.

On the other hand, recent studies revealed that reductive stress, caused by an excessive buildup of reductants, may also increase ROS levels, contradicting the long-held belief that OS is the primary mediator of many disorders, including male infertility, which is brought on by elevated ROS [7]. Because of the induction of electron leakage, oxidized reductants such as nicotinamide adenine dinucleotide (NAD⁺), glutathione disulfide (GSSG), and oxidized thioredoxins may not be as readily available, leading to the formation of ROS [7]. An overdose of countertop antioxidants resulted in poor sperm function due to an imbalance in the oxidative–reductive potential [8, 9]. Disproportionate accumulation of reductants that can cause DNA breakage and guanidine oxidation may result from excessive dietary supplementation, overproduction of nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) through the pentose phosphate pathway, elevated levels of glutathione (GSH), and nicotinamide adenine nucleotide (NADH) accumulation [7].

Infertility may lead to psychological difficulties because of societal stigmatization and purposeless feelings in men [10]. Therefore, infertility treatment may be a significant need for people, and each cause of infertility may determine the type of treatment needed [11]. The most common type of treatment is assisted reproductive technology (ART) and is not limited to in vitro fertilization and intracytoplasmic sperm injection [11]. However, most health insurance schemes do not cover ART due to the expensive costs and lack of guarantee for a positive outcome [12]. ART is also not readily available to all social and economic classes, as it tends to be expensive and not accessible [13]. Therefore, lower cost infertility treatments are necessary [14].

Several studies have demonstrated the affordability and availability of diverse medicinal plants across social classes globally [15, 16]. These medicinal plants contain beneficial compounds, including antioxidants [17] that serve as the protective barrier for spermatozoa prevention of excessive ROS generation (prevention antioxidants such as metal chelators and metal-binding proteins) or to remove already existing ROS (scavenging ROS) [18]. Antioxidants may be classified as nonenzymatic (glutathione, ascorbic acid, and tocopherol) and enzymatic (superoxide dismutase, glutathione peroxidase, and catalase) [19]. The improvement of male fertility parameters is usually attributed to their antioxidant properties [20].

Tea is the second most popular beverage after water and is produced from the buds and young leaves of the Camellia sinensis plant in the family of Theaceae [21, 22]. Black tea is the highest-produced tea globally (76%–78%), followed by green tea (20%–22%) and oolong tea (2%) [23]. Freshly plucked leaves are processed to produce diverse types of tea, including green and white teas (unfermented), black tea (fermented), and oolong tea (semifermented) [22, 24]. Catechins, theaflavins, thearubigins, amino acids, and alkaloids are common constituents of tea, with theaflavins and thearubigins being the most important polyphenolic components in black tea [25, 26]. During the fermentation process of black tea, theaflavins and thearubigins result from the oxidation and polymerization of catechins [25].

Health benefits of C. sinensis include anticancer, hepato-protective, anti-inflammatory, analgesic, antipyretic, antiallergic, antimicrobial, antiviral, and antiparasitic activities; relieves asthma and allergy; and improves cardiovascular activities [27]. It is used traditionally to treat urinary inconsistency and common colds, as well as an anxiety suppressant and to prevent blister formation on a burn wound [28]. Additionally, because black tea elevates testosterone levels, traditional Sri Lankan practitioners utilize it to improve sexual performance and delay ejaculation [29]. In a different in vivo study, male Wistar rats given ad libitum access to black tea aqueous extracts (2% and 5%) did not significantly affect testosterone production, sperm concentration, or the weight of their reproductive organs; however, sperm motility and vitality improved significantly [30]. It was demonstrated after a 24-hr treatment in vitro that black tea aqueous extract (250 and 1,000 μg/ml) had an antiandrogenic effect on TM3 Leydig cells by significantly lowering testosterone synthesis [31]. The aim of the current work is to investigate the direct effects of aqueous black tea extract on the in vitro functions of human spermatozoa.

2. Materials and Methods

2.1. Materials

Unless otherwise indicated, all reagents were obtained from Sigma-Aldrich (St. Louis, MO, USA). In addition, commercial black tea was acquired locally (Five Roses™, Cape Town, South Africa).

2.2. Collection of Plant Extract and Preparation

As described by Setumo [32], an aqueous extract of black tea was prepared by infusing 2 g of the leaves in freshly boiled (100 ml) for 5 min, filtered using a vacuum filtration system, and cooled to room temperature [31]. The filtrate was freeze-dried (with an average yield of 3.60 g/l) and kept in a cool, dry place until use. The extracts were reconstituted in human tubular fluid containing bovine serum albumin (HTF-BSA) to final concentrations of 0.4, 4.0, 40, and 405 μg/ml, based on the recommended daily intake of six cups (a cup equivalent to 150 ml) for an average of 80 kg man [33].

2.3. Ethics Approval

Turfloop Research Ethics Committee of the University of Limpopo (UL), Sovenga, South Africa (TREC/393/2019: PG) and Biomedical Research Ethics Committee (BMREC) of the University of the Western Cape (UWC), Bellville, South Africa (BMI18/3/17).

2.4. Source and Preparation of Semen Samples

Healthy donors signed informed consent, abstained from sexual activity for 3–5 days, and masturbated to collect semen samples were obtained by masturbation, which was then placed in a sterile vial (n = 59; 18–45 years) at the comparative spermatology laboratory UWC and allowed to liquefy (30 min; 37°C). Using a Sperm Class Analyser (SCA) (Microptic, Barcelona, Spain), baseline sperm concentration and motility were determined. Afterwards, the World Health Organization (WHO) [34] guidelines classified the samples as normal or abnormal. A normal semen sample is defined as having sperm concentrations > 15 million/ml, progressive motility > 32%, and total motility > 40%; an abnormal semen sample is defined as having sperm concentrations < 15 × 10⁶/ml, progressive motility < 32%, and total motility < 40% [32]. For a semen sample to be classified as normal, it must meet all three criteria; otherwise, it is classified as an abnormal sample. The washed samples were incubated with black tea aqueous extract (0.4, 4.0, 40, and 405 μg/ml) for 1 hr at 37°C. Additional sperm parameters, sperm motility, vitality, mitochondrial membrane potential (MMP), ROS production, DNA fragmentation, capacitation, and acrosome reaction, were analyzed as previously described [32, 35–38]. The control contained only HTF-BSA.

2.5. Sperm Motility and Kinematic Parameters

The SCA was used to assess the motility of treated sperm suspension (2 μl) on Leja slides and incubated at 37°C. Moreover, analysis was done on the following: beat cross frequency (BCF), linearity (LIN), straightness (STR), amplitude of lateral head displacement (ALH), wobble (WOB), average velocity path (VAP), velocity curve line (VCL), velocity straight line (VSL), and total motility [32, 37].

2.6. Sperm Vitality

According to WHO [34] guidelines, sperm vitality was evaluated by one-step eosin–nigrosin (E&N) staining. After the incubation period, a smear was made on a glass slide by combining the sperm solution with E&N stain 1 : 1, allowing it to air dry, and then viewed under a 100x light microscope. Spermatozoa that were dead or alive appeared pink and white, respectively. The percentage of living spermatozoa was calculated after counting the 200 spermatozoa.

2.7. Mitochondrial Membrane Potential of Sperm

According to the manufacturer’s instructions, the MMP was determined (DePsipher™, Trevigen, Minneapolis, USA). The prepared slides were observed with a fluorescence microscope (Zeiss, Oberkochen, Germany) at 400x, using a 488 nm excitation filter. Spermatozoa with intact MMP fluoresced intense red/orange and fluoresced green for those with disrupted MMP. The spermatozoa (200) were counted, and the results represented the percentage of spermatozoa with intact MMP.

2.8. Reactive Oxygen Species Production

The ROS production was determined using dihydroethidium (DHE; Molecular Probes, Eugene, OR, USA) [39]. After the treatment, 100 μl of spermatozoa were centrifuged (10 min; 500 × g) and then resuspended in 100 μl of PBS and 20 μl of stock solution of DHE (20 μM DHE in PBS, pH = 7.4). The mixture was then incubated for a further 15 min at 37°C. After that, the sample was placed on a slide and viewed under oil immersion using an epifluorescence microscope (Zeiss, Oberkochen, Germany) with 488 nm excitation and 590 emission filters. Spermatozoa with excessive ROS production fluoresced bright orange (ROS-positive spermatozoa). Two hundred spermatozoa were analyzed, representing the result as the percentage of ROS-positive spermatozoa.

2.9. DNA Fragmentation

Sperm DNA fragmentation was evaluated using the terminal deoxynucleotidyl transferase-mediated dUTP-biotin nick end labeling (TUNEL) (Dead End™; Promega, Madison, USA), per the manufacturer’s instructions. The prepared slides were examined under a fluorescence microscope with an emission filter of 510–530 nm and an excitation filter of 488 nm. A total of 200 spermatozoa were evaluated. Spermatozoa that fluoresced bright green spermatozoa were, respectively, categorized as TUNEL-positive (fragmented DNA) or TUNEL-negative (intact DNA) if they fluoresced bright green or had light background staining. The percentage of TUNEL-positive spermatozoa was used to express the result.

2.10. Capacitation and Acrosome Reaction in Sperm

The chlortetracycline fluorescence assay protocol was utilized to evaluate the capacitation and acrosome reaction [40]. Using a fluorescence microscope with a 488 nm excitation filter (Zeiss, Oberkochen, Germany), 200 spermatozoa were assessed based on the presence or absence of fluorescence and classified as acrosome reacted, capacitated acrosome intact or noncapacitated, acrosome intact cell [32, 38].

2.11. Data Analysis

Data analysis was performed with the GraphPad Prism version. 5.01 (Graph Pad Software Inc., San Diego, CA, USA). D’Agostino & Pearson omnibus normality test was employed to determine normal distribution. One-way analysis of variance (ANOVA) and Tukey’s posttest were used for normally distributed data. In contrast, the Kruskal–Wallis and Dunnetts’ multiple posttests were used for data that was not normally distributed. A two-way ANOVA was used to compare the respective parameters between the normal and abnormal groups. Results were considered statistically significant with a p-value < 0.05.

3. Results

Sperm concentration () and progressive motility () were found to be considerably higher in the normal samples than in the abnormal samples, according to the baseline analysis of the semen samples obtained (Table 1). On the other hand, there was no statistically significant difference in semen volume or total motility between the abnormal and normal samples (, Table 1).

Figure 1(a)–1(c) shows how the aqueous extract of black tea affects sperm motility. Total motility did not significantly differ between the normal and abnormal samples () or between the normal and abnormal groups when compared to the corresponding controls (Figure 1(a)). However, a significant drop in total motility was seen for both groups at 405 μg/ml as opposed to 0.4 μg/ml (Figure 1(a); ). Moreover, Figure 1(b) shows no difference in the proportion of progressively motile spermatozoa between the normal and abnormal samples () or either group compared to their control. Conversely, 0.4 μg/ml showed a significant increase in progressive motility compared to 405 μg/ml (). Furthermore, the percentage of nonprogressive spermatozoa in both groups did not alter (). However, there was a significant drop in the percentage of nonprogressive spermatozoa at 405 μg/ml compared to 0.4 μg/ml (). Moreover, LIN, STR, VAP, VCL, VSL, and WOB did not significantly differ in either group (Table 2; ). On the other hand, the normal group’s BCF and ALH showed no change (), while the abnormal group’s showed a substantial difference ().

(a)

(b)

(c)

The percentage of viable spermatozoa in the normal group was substantially more significant than in the abnormal group (Figure 2; ). Furthermore, at 40 and 405 μg/ml, the proportion of viable spermatozoa increased significantly compared to the control of the normal group (Figure 2; ). Figure 2 shows a significant increase in the percentage of viable spermatozoa at 4, 40, and 405 μg/ml in the abnormal group ().

The proportion of spermatozoa with intact MMP significantly increased in the normal (40 and 405 μg/ml) and abnormal (4, 40, and 405 μg/ml) groups (), with the former having a much higher percentage of intact MMP () (Figure 3). Furthermore, the normal and abnormal groups showed a dose-dependent decrease in ROS generation (; Figure 4). Additionally, the abnormal group produced significantly higher ROS than the normal group (; Figure 4).

Both groups showed a dose-dependent decrease in the proportion of spermatozoa with fragmented DNA compared to the control (; Figure 5). Furthermore, a considerably lower percentage of spermatozoa with fragmented DNA was noted for the normal samples (4, 40, and 405 μg/ml) () as well as the abnormal samples (0.4 and 405 μg/ml) (). The abnormal group’s percentage of spermatozoa with fragmented DNA was substantially higher than that of the normal group, particularly between 0 and 40 μg/ml (; Figure 5).

There was a dose-dependent drop in the proportion of spermatozoa that underwent spontaneous acrosome reaction in both groups (Figure 6; ). On the other hand, the abnormal group exhibited a considerably higher percentage of spermatozoa that underwent spontaneous acrosome reaction () in comparison to the normal group (Figure 6). In both the normal and abnormal samples, the acrosome reaction significantly decreased at 4, 40, and 405 μg/ml compared to the control (Figure 6; ).

4. Discussion

The current study investigated the effect of black tea aqueous extract on human sperm functions in vitro, as per WHO [34] guidelines. Sperm parameters related to sperm motility: progressive motility, total motility, VCL, VSL, VAP, STR, LIN, ALH, BCF, WOB, as well as acrosome reaction, DNA fragmentation, MMP, ROS production, and sperm vitality were evaluated. The current study demonstrates that spermatozoa directly exposed to black tea aqueous extract did not influence sperm motility or most kinematic measures but increased sperm viability and MMP and decreased ROS generation and DNA fragmentation [32].

After an hour of incubation, the current investigation demonstrated that black tea aqueous extract (0.4, 4.0, 40, and 405 μg/ml) had no significant effect on sperm motility in both groups compared to their controls and between the two groups. Like this study, Ratnasooriya and Amarakoon [41] demonstrated that black tea aqueous extract did not affect total motility in vivo (500, 1,000, and 2,000 mg/ml). Total sperm motility seemed higher in the abnormal than normal samples, albeit this difference was not statistically significant. Ajayi et al. [42] demonstrated that antioxidant dietary supplementation notably improved sperm motility, sperm concentration, and sperm morphology in patients with poor semen quality while remaining unchanged in the normal samples, suggesting the beneficial role of antioxidants in abnormal semen samples compared to normal samples. Acrosome reaction, sperm vitality, and total motility increased significantly following ad libitum consumption of black tea aqueous extracts in male rats [30]. The varying results obtained could be due to the different concentrations of the extracts utilized as a dose-dependent increase in soluble solids, total polyphenols, flavonol, flavanol (mg catechin/ml), as well as the ferric reducing antioxidant power of black tea aqueous extract, was noted, indicating higher antioxidant activities with increasing concentrations [43].

Furthermore, sperm kinematic parameters predict sperm-fertilizing capabilities [44], which are essential as markers in sperm function. The current study investigated the effect of black tea extracts on sperm kinematic parameters (VAP, VCL, VSL, STR, BCF, WOB, LIN, and ALH), which showed that black tea aqueous extract had no significant effect on VCL, VSL, VAP, LIN, STR, and WOB, except for ALH and BCF. Similar to a previous study by Ratnasooriya and Amarakoon [41], black tea extracts (0.4, 4, and 40 μg/ml) caused a noticeable increase in the ALH. On the other hand, BCF declined significantly at 405 μg/ml in the current study. In other studies, supplementation with various polyphenolic compounds significantly decreased total motility, progressive motility, VAP, VCL, STR, and LIN dose-dependently [45, 46], and suggests that the obtained results in this study may be due to the synergistic activities of the combined compounds present in black tea extracts. A significant increase in sperm viability was noted following the exposure to black tea aqueous extract in both the normal and abnormal samples, with the former having a significantly higher amount. In line with the current study, an inverse relationship exists between sperm viability and DNA fragmentation [47]. Despite the increase in sperm viability and MMP, no effect was noted for sperm motility in both groups. Besides its polyphenol content (antioxidants), black tea contains a considerable amount of caffeine [48], which has been shown to stimulate motility. While the antioxidants could protect sperm from dying, the caffeine will stimulate motility in the presence of an energy source. However, this short-lived stimulation could decrease motility, especially if the caffeine concentration is high or the exposure time is extended. Also, if the energy source is insufficient, motility will drop again. For instance, a previous study demonstrates that 10 nM of caffeine significantly increased the progressive motility of spermatozoa in normozoospermic and asthenozoospermic groups [49]. Studies have also shown that the caffeine content in tea increases with increasing steep time and temperature [50–52]. The current study, however, did not analyze the caffeine content in the grade of tea used, and further study on the caffeine and polyphenolic contents at various infusion times of this grade of tea is therefore recommended.

Spermatozoa must be supplied with sufficient adenosine triphosphate (ATP) (a source of energy) to maintain their normal functioning [53]. Proton concentration gradients and electric potential gradients are stored in the mitochondria of spermatozoa and used to synthesize ATP [53, 54]. As a result, reduced mitochondrial function and an incapacity to store enough ATP for efficient sperm movement may cause low-sperm motility [55]. In addition, excessive ROS production has also been indicated to be harmful to the mitochondrial membrane [56, 57]. In the current study, the percentage of intact MMP in both the abnormal and normal samples increased significantly in response to black tea aqueous extract in a dose-dependent manner.

Furthermore, compared to the abnormal samples, the normal samples had a more significant percentage of intact MMP, which the polyphenols in the plant could explain. Ferramosca et al. [58] have demonstrated that plant polyphenols, depending on their concentration, have variable effects (either positively or adversely) on sperm mitochondria. The current study thus showed that the polyphenolic content of black tea extract (together with the concentration used) positively affects MMP in both sample groups.

Antioxidants have been shown in several studies in both animals and people to be crucial for proper sperm quality and reproductive function and are thought to counteract the adverse effects of OS on spermatozoa [59, 60]. An imbalance between cellular antioxidants and ROS generation may result in OS [8]. Furthermore, by supplying the required membrane fluidity, the physiological amount of ROS is essential for capacitation and fertilization [61]; this maintains the sperm acrosome reaction and permits fertilization of the egg [62]. The causes of excessive ROS production may be linked to lifestyle choices like smoking, drinking alcohol, poor diet, or deficiencies in antioxidants like vitamins A and E. These choices have the potential to harm biological molecules like DNA and proteins as well as sperm’s ability to undergo capacitation [62–65]. In vitro treatment of human sperm with antioxidants, ascorbate, and tocopherol inhibited ROS production [46].

The plant extract’s antioxidant property may be attributed to the current study’s dose-dependently substantial reduction in the proportion of ROS produced in both groups compared to their respective controls. Additionally, compared to normal samples, a more significant percentage of sperm that produced excessive amounts of ROS was noted in the abnormal samples. These suggest that black tea aqueous extract could enhance sperm quality by lowering excessive ROS generation in sperm cells [66].

The acrosome reacted spermatozoa proportion was significantly lower after black tea aqueous extract treatment. Also, the percentage of acrosome-reacted spermatozoa was markedly higher in the abnormal samples compared to the normal samples. The observed decrease in the number of acrosome-reacted spermatozoa shows that the number of spermatozoa with intact acrosome capable of interacting with the zona pellucida has increased, implying a possible improved fertilizing capability of the spermatozoa [67]. Spermatozoa must complete capacitation before undergoing an acrosome acrosome reaction [68]. This study did not investigate the mechanism by which black tea prevents the spontaneous acrosome reaction and requires further investigation. However, this may be mediated through decreased ROS production.

Furthermore, DNA fragmentation was significantly decreased by the black tea aqueous extract in vitro, with abnormal samples exhibiting a higher proportion of spermatozoa with fragmented DNA than normal samples. Research indicates a correlation between ROS and DNA strand breakage, especially in males diagnosed with infertility [69]; this could potentially account for the increased proportion of fragmented DNA and elevated levels of ROS found in the abnormal samples compared to the normal. This study observed that increased MMP was associated with reduced ROS levels and DNA fragmentation. In addition, the current study also showed an increased MMP level in the normal and abnormal samples. The increased MMP agrees with the reduced ROS production and DNA fragmentation, and in consonance with previous studies [70, 71], it was associated with reduced ROS levels and DNA fragmentation.

To conclude, the current study established that black tea aqueous extract has the potential to significantly improve some of the sperm functions such as vitality, DNA fragmentation, MMP, ROS, as well as acrosome reaction, which may be attributed to its antioxidant properties. However, no significant change in sperm motility was noted. More research is necessary to understand the mechanism of action of black tea extract further, its potential to aid in infertility, and its potential antioxidative and cytoprotective properties against OS.

Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no potential conflicts of interest.

Acknowledgments

The authors thank the donors and the Comparative Spermatology Laboratory of the Department of Medical Biosciences, University of the Western Cape. This study was supported by the National Research Foundation of South Africa (no. TTK170426228930).

References

S. A. Carson and A. N. Kallen, “Diagnosis and management of infertility: a review,” JAMA, vol. 326, no. 1, pp. 65–76, 2021.
View at: Publisher Site | Google Scholar
U. Larsen, “Primary and secondary infertility in sub-Saharan Africa,” International Journal of Epidemiology, vol. 29, no. 2, pp. 285–291, 2000.
View at: Publisher Site | Google Scholar
A. Agarwal, A. Mulgund, A. Hamada, and M. R. Chyatte, “A unique view on male infertility around the globe,” Reproductive Biology and Endocrinology, vol. 13, Article ID 37, 2015.
View at: Publisher Site | Google Scholar
M. L. Eisenberg, S. C. Esteves, D. J. Lamb et al., “Male infertility,” Nature Reviews Disease Primers, vol. 9, Article ID 49, 2023.
View at: Publisher Site | Google Scholar
A. Agarwal, S. Baskaran, N. Parekh et al., “Male infertility,” The Lancet, vol. 397, no. 10271, pp. 319–333, 2021.
View at: Publisher Site | Google Scholar
B. Ayad, T. S. Omolaoye, N. Louw et al., “Oxidative stress and male infertility: evidence from a research perspective,” Frontiers in Reproductive Health, vol. 4, Article ID 822257, 2022.
View at: Publisher Site | Google Scholar
N. Sadeghi, G. Boissonneault, M. Tavalaee, and M. H. Nasr-Esfahani, “Oxidative versus reductive stress: a delicate balance for sperm integrity,” Systems Biology in Reproductive Medicine, vol. 69, no. 1, pp. 20–31, 2023.
View at: Publisher Site | Google Scholar
S. Dutta, R. Henkel, P. Sengupta, and A. Agarwal, “Physiological role of ROS in sperm function,” in Male Infertility, S. Parekattil, S. Esteves, and A. Agarwal, Eds., pp. 337–345, Springer, Cham, 2nd edition, 2020.
View at: Publisher Site | Google Scholar
S. Kothari, A. Thompson, A. Agarwal, and S. S. du Plessis, “Free radicals: their beneficial and detrimental effects on sperm function,” Indian Journal of Experimental Biology, vol. 48, pp. 425–435, 2010.
View at: Google Scholar
V. Ravitsky and S. Kimmins, “The forgotten men: rising rates of male infertility urgently require new approaches for its prevention, diagnosis and treatment,” Biology of Reproduction, vol. 101, no. 5, pp. 872–874, 2019.
View at: Publisher Site | Google Scholar
K. A. Turner, A. Rambhatla, S. Schon et al., “Male infertility is a women’s health issue—research and clinical evaluation of male infertility is needed,” Cells, vol. 9, no. 4, Article ID 990, 2020.
View at: Publisher Site | Google Scholar
C. Massarotti, G. Gentile, C. Ferreccio, P. Scaruffi, V. Remorgida, and P. Anserini, “Impact of infertility and infertility treatments on quality of life and levels of anxiety and depression in women undergoing in vitro fertilization,” Gynecological Endocrinology, vol. 35, no. 6, pp. 485–489, 2019.
View at: Publisher Site | Google Scholar
P. Sengupta, A. Agarwal, M. Pogrebetskaya, S. Roychoudhury, D. Durairajanayagam, and R. Henkel, “Role of Withania somnifera (Ashwagandha) in the management of male infertility,” Reproductive Biomedicine Online, vol. 36, no. 3, pp. 311–326, 2018.
View at: Publisher Site | Google Scholar
A. Fleetwood and L. Campo-Engelstein, “The impact of infertility: why ART should be a higher priority for women in the global south,” in Oncofertility, T. Woodruff, L. Zoloth, L. Campo-Engelstein, and S. Rodriguez, Eds., vol. 156 of Cancer Treatment and Research, pp. 237–248, Springer, Boston, MA, 2010.
View at: Publisher Site | Google Scholar
E.-O. J. Ozioma and O. A. N. Chinwe, “Herbal medicines in African traditional medicine,” in Herbal Medicine, P. F. Builders, Ed., vol. 10, pp. 191–214, IntechOpen, 2019.
View at: Publisher Site | Google Scholar
U. Schippmann, D. J. Leaman, and A. B. Cunningham, “Impact of cultivation and gathering of medicinal plants on biodiversity: global trends and issues,” in Biodiversity and the Ecosystem Approach in Agriculture, Forestry and Fisheries, FAO, 2002.
View at: Google Scholar
K. Bastola, Y. Guragain, V. Bhadriraju, and P. Vadlani, “Evaluation of standards and interfering compounds in the determination of phenolics by folin-ciocalteu assay method for effective bioprocessing of biomass,” American Journal of Analytical Chemistry, vol. 8, no. 6, pp. 416–431, 2017.
View at: Publisher Site | Google Scholar
J. Zhang, D. Duan, Z.-L. Song, T. Liu, Y. Hou, and J. Fang, “Small molecules regulating reactive oxygen species homeostasis for cancer therapy,” Medicinal Research Reviews, vol. 41, no. 1, pp. 342–394, 2021.
View at: Publisher Site | Google Scholar
S. B. Nimse and D. Pal, “Free radicals, natural antioxidants, and their reaction mechanisms,” RSC Advances, vol. 5, pp. 27986–28006, 2015.
View at: Publisher Site | Google Scholar
A. Chikhoune, L. Stouvenel, M. Iguer-Ouada et al., “In-vitro effects of Thymus munbyanus essential oil and thymol on human sperm motility and function,” Reproductive BioMedicine Online, vol. 31, no. 3, pp. 411–420, 2015.
View at: Publisher Site | Google Scholar
M.-Y. Chang, Y.-Y. Lin, Y.-C. Chang et al., “Effects of infusion and storage on antioxidant activity and total phenolic content of black tea,” Applied Sciences, vol. 10, no. 8, Article ID 2685, 2020.
View at: Publisher Site | Google Scholar
Z.-T. Fang, C.-J. Song, H.-R. Xu, and J.-H. Ye, “Dynamic changes in flavonol glycosides during production of green, yellow, white, oolong and black teas from Camellia sinensis L. (cv. Fudingdabaicha),” International Journal of Food Science & Technology, vol. 54, no. 2, pp. 490–498, 2019.
View at: Publisher Site | Google Scholar
D. L. McKay and J. B. Blumberg, “The role of tea in human health: an update,” Journal of the American College of Nutrition, vol. 21, no. 1, pp. 1–13, 2002.
View at: Publisher Site | Google Scholar
P. Carloni, L. Tiano, L. Padella et al., “Antioxidant activity of white, green and black tea obtained from the same tea cultivar,” Food Research International, vol. 53, no. 2, pp. 900–908, 2013.
View at: Publisher Site | Google Scholar
B. Abudureheman, X. Yu, D. Fang, and H. Zhang, “Enzymatic oxidation of tea catechins and its mechanism,” Molecules, vol. 27, no. 3, Article ID 942, 2022.
View at: Publisher Site | Google Scholar
S. Li, C.-Y. Lo, M.-H. Pan, C.-S. Lai, and C.-T. Ho, “Black tea: chemical analysis and stability,” Food & Function, vol. 4, no. 1, pp. 10–18, 2013.
View at: Publisher Site | Google Scholar
S. Poddar, T. Sarkar, S. Choudhury, S. Chatterjee, and P. Ghosh, “Indian traditional medicinal plants: a concise review,” International Journal of Botany Studies, vol. 5, no. 5, pp. 174–190, 2020.
View at: Google Scholar
P. K. Srivastava and A. K. Pandey, “Natural products and derivatives: biological and pharmacological activities,” Biochemical and Cellular Archives, vol. 15, no. 1, pp. 1–38, 2015.
View at: Google Scholar
W. D. Ratnasooriya and T. S. P. Fernando, “Effect of black tea brew of Camellia sinensis on sexual competence of male rats,” Journal of Ethnopharmacology, vol. 118, no. 3, pp. 373–377, 2008.
View at: Publisher Site | Google Scholar
C. S. Opuwari and T. K. Monsees, “In vivo effects of black tea on the male rat reproductive system and functions of the kidney and liver,” Andrologia, vol. 52, no. 4, Article ID e13552, 2020.
View at: Publisher Site | Google Scholar
C. Opuwari and T. Monsees, “Reduced testosterone production in TM3 Leydig cells treated with Aspalathus linearis (Rooibos) or Camellia sinensis (tea),” Andrologia, vol. 47, no. 1, pp. 52–58, 2015.
View at: Publisher Site | Google Scholar
M. A. Setumo, Determination of in vitro effects of aqueous extract of camellia sinensis on human sperm functions, University of Limpopo, 2021, M. S. Thesis.
E. Saito, M. Inoue, N. Sawada et al., “Association of green tea consumption with mortality due to all causes and major causes of death in a Japanese population: the Japan Public Health Center-based prospective study (JPHC study),” Annals of Epidemiology, vol. 25, no. 7, pp. 512–518.e3, 2015.
View at: Publisher Site | Google Scholar
WHO, WHO Laboratory Manual for the Examination and Processing of Human Semen, WHO, 2010.
F. T. Moichela, G. A. Adefolaju, R. R. Henkel, and C. S. Opuwari, “Aqueous leaf extract of Moringa oleifera reduced intracellular ROS production, DNA fragmentation and acrosome reaction in Human spermatozoa in vitro,” Andrologia, vol. 53, no. 1, Article ID e13903, 2021.
View at: Publisher Site | Google Scholar
M. A. Setumo, S. S. Choma, R. Henkel, and C. S. Opuwari, “Green tea (Camellia sinensis) aqueous extract improved human spermatozoa functions in vitro,” Journal of Medicinal Plants for Economic Development, vol. 6, no. 1, Article ID a166, pp. 1–8, 2022.
View at: Publisher Site | Google Scholar
N. B. Takalani, In vitro effects of aqueous extract of Aspalathus linearis (rooibos) on human sperm cells, University of Limpopo, 2020, M. S. Thesis.
N. B. Takalani, G. A. Adefolaju, R. R. Henkel, and C. S. Opuwari, “In vitro effects of aqueous extract of unfermented rooibos on human spermatozoa,” Andrologia, vol. 54, no. 8, Article ID e14452, 2022.
View at: Publisher Site | Google Scholar
C. Mupfiga, D. Fisher, T. Kruger, and R. Henkel, “The relationship between seminal leukocytes, oxidative status in the ejaculate, and apoptotic markers in human spermatozoa,” Systems Biology in Reproductive Medicine, vol. 59, no. 6, pp. 304–311, 2013.
View at: Publisher Site | Google Scholar
C. M. Green, S. M. Cockle, P. F. Watson, and L. R. Fraser, “A possible mechanism of action for fertilization promoting peptide, a TRH-related tripeptide that promotes capacitation and fertilizing ability in mammalian spermatozoa,” Molecular Reproduction and Development, vol. 45, no. 2, pp. 244–252, 1996.
View at: Google Scholar
W. D. Ratnasooriya and A. M. T. Amarakoon, “Effect of Sri Lankan high grown black tea (Camellia sinensis L.O Kuntze) on motility of human spermatozoa in vitro,” Sri Lanka Journal of Tea Science, vol. 72, no. 1, pp. 16–22, 2007.
View at: Google Scholar
R. Ajayi, J. Okhowat, D. Spitzer, B. Schechinger, and N. H. Zech, “Impact of antioxidative supplementation on semen quality according to MSOME criteria,” JBRA Assisted Reproduction, vol. 17, no. 1, pp. 27–31, 2013.
View at: Publisher Site | Google Scholar
C. S. Opuwari, Effect of tea and herbal infusions on mammalian reproduction and fertility, University of the Western Cape, 2013, Ph.D. Thesis.
I. Robayo, V. Montenegro, C. Valdés, and J. F. Cox, “CASA assessment of kinematic parameters of ram spermatozoa and their relationship to migration efficiency in ruminant cervical mucus,” Reproduction in Domestic Animals, vol. 43, no. 4, pp. 393–399, 2008.
View at: Publisher Site | Google Scholar
R. J. Aitken, L. Muscio, S. Whiting et al., “Analysis of the effects of polyphenols on human spermatozoa reveals unexpected impacts on mitochondrial membrane potential, oxidative stress and DNA integrity; implications for assisted reproductive technology,” Biochemical Pharmacology, vol. 121, pp. 78–96, 2016.
View at: Publisher Site | Google Scholar
E. T. Donnelly, N. McClure, and S. E. M. Lewis, “Antioxidant supplementation in vitro does not improve human sperm motility,” Fertility and Sterility, vol. 72, no. 3, pp. 484–495, 1999.
View at: Publisher Site | Google Scholar
M. K. Samplaski, A. Dimitromanolakis, K. C. Lo et al., “The relationship between sperm viability and DNA fragmentation rates,” Reproductive Biology and Endocrinology, vol. 13, Article ID 42, 2015.
View at: Publisher Site | Google Scholar
C.-N. Zhao, G.-Y. Tang, S.-Y. Cao et al., “Phenolic profiles and antioxidant activities of 30 tea infusions from green, black, oolong, white, yellow and dark teas,” Antioxidants, vol. 8, no. 7, Article ID 215, 2019.
View at: Publisher Site | Google Scholar
S. A. Banihani and H. J. Khaled, “Caffeine increased progressive motility of human spermatozoa in normozoospermic and asthenozoospermic semen samples and enhanced activity of seminal creatine kinase,” Andrologia, vol. 53, no. 6, Article ID e14052, 2021.
View at: Publisher Site | Google Scholar
J. M. Chin, M. L. Merves, B. A. Goldberger, A. Sampson-Cone, and E. J. Cone, “Caffeine content of brewed teas,” Journal of Analytical Toxicology, vol. 32, no. 8, pp. 702–704, 2008.
View at: Publisher Site | Google Scholar
J. A. M. Kyle, P. C. Morrice, G. McNeill, and G. G. Duthie, “Effects of infusion time and addition of milk on content and absorption of polyphenols from black tea,” Journal of Agricultural and Food Chemistry, vol. 55, no. 12, pp. 4889–4894, 2007.
View at: Publisher Site | Google Scholar
S. A. Ramalho, N. Nigam, G. B. Oliveira et al., “Effect of infusion time on phenolic compounds and caffeine content in black tea,” Food Research International, vol. 51, no. 1, pp. 155–161, 2013.
View at: Publisher Site | Google Scholar
S. K. Agnihotri, A. K. Agrawal, B. A. Hakim et al., “Mitochondrial membrane potential (MMP) regulates sperm motility,” In Vitro Cellular & Developmental Biology—Animal, vol. 52, pp. 953–960, 2016.
View at: Publisher Site | Google Scholar
C. Marchetti, G. Obert, A. Deffosez, P. Formstecher, and P. Marchetti, “Study of mitochondrial membrane potential, reactive oxygen species, DNA fragmentation and cell viability by flow cytometry in human sperm,” Human Reproduction, vol. 17, no. 5, pp. 1257–1265, 2002.
View at: Publisher Site | Google Scholar
C. Marchetti, N. Jouy, B. Leroy-Martin, A. Defossez, P. Formstecher, and P. Marchetti, “Comparison of four fluorochromes for the detection of the inner mitochondrial membrane potential in human spermatozoa and their correlation with sperm motility,” Human Reproduction, vol. 19, no. 10, pp. 2267–2276, 2004.
View at: Publisher Site | Google Scholar
M. Darbandi, S. Darbandi, A. Agarwal et al., “Reactive oxygen species and male reproductive hormones,” Reproductive Biology and Endocrinology, vol. 16, Article ID 87, 2018.
View at: Publisher Site | Google Scholar
C. R. Darr, D. D. Varner, S. Teague, G. A. Cortopassi, S. Datta, and S. A. Meyers, “Lactate and pyruvate are major sources of energy for stallion sperm with dose effects on mitochondrial function, motility, and ROS production,” Biology of Reproduction, vol. 95, no. 2, Article ID 34, pp. 1–31, 2016.
View at: Publisher Site | Google Scholar
A. Ferramosca, S. Lorenzetti, M. Di Giacomo et al., “Modulation of human sperm mitochondrial respiration efficiency by plant polyphenols,” Antioxidants, vol. 10, no. 2, Article ID 217, 2021.
View at: Publisher Site | Google Scholar
B. Eskenazi, S. A. Kidd, A. R. Marks, E. Sloter, G. Block, and A. J. Wyrobek, “Antioxidant intake is associated with semen quality in healthy men,” Human Reproduction, vol. 20, no. 4, pp. 1006–1012, 2005.
View at: Publisher Site | Google Scholar
C. Ross, A. Morriss, M. Khairy et al., “A systematic review of the effect of oral antioxidants on male infertility,” Reproductive BioMedicine Online, vol. 20, no. 6, pp. 711–723, 2010.
View at: Publisher Site | Google Scholar
S. Baskaran, R. Finelli, A. Agarwal, and R. Henkel, “Reactive oxygen species in male reproduction: a boon or a bane?” Andrologia, vol. 53, no. 1, Article ID e13577, 2021.
View at: Publisher Site | Google Scholar
M. N. De Luca, M. Colone, R. Gambioli, A. Stringaro, and V. Unfer, “Oxidative stress and male fertility: role of antioxidants and inositols,” Antioxidants, vol. 10, no. 8, Article ID 1283, 2021.
View at: Publisher Site | Google Scholar
A. Akilah Amira, M. Kabel Ahmed, and A. Alharthi Huda, “New perspectives in male infertility,” GSC Biological and Pharmaceutical Sciences, vol. 1, no. 3, pp. 12–19, 2017.
View at: Publisher Site | Google Scholar
M. Ali, M. Martinez, and N. Parekh, “Are antioxidants a viable treatment option for male infertility?” Andrologia, vol. 53, no. 1, Article ID e13644, 2021.
View at: Publisher Site | Google Scholar
M. K. Panner Selvam, R. F. Ambar, A. Agarwal, and R. Henkel, “Etiologies of sperm DNA damage and its impact on male infertility,” Andrologia, vol. 53, no. 1, Article ID e13706, 2021.
View at: Publisher Site | Google Scholar
K. Nowicka-Bauer and B. Nixon, “Molecular changes induced by oxidative stress that impair human sperm motility,” Antioxidants, vol. 9, no. 2, Article ID 134, 2020.
View at: Publisher Site | Google Scholar
I. P. Oyeyipo, P. J. Maartens, and S. S. du Plessis, “In vitro effects of nicotine on human spermatozoa,” Andrologia, vol. 46, no. 8, pp. 887–892, 2014.
View at: Publisher Site | Google Scholar
E. de Lamirande and C. Gagnon, “Capacitation-associated production of superoxide anion by human spermatozoa,” Free Radical Biology and Medicine, vol. 18, no. 3, pp. 487–495, 1995.
View at: Publisher Site | Google Scholar
A. Agarwal and T. M. Said, “Role of sperm chromatin abnormalities and DNA damage in male infertility,” Human Reproduction Update, vol. 9, no. 4, pp. 331–345, 2003.
View at: Publisher Site | Google Scholar
Z. Li, Y. Zhou, R. Liu et al., “Effects of semen processing on the generation of reactive oxygen species and mitochondrial membrane potential of human spermatozoa,” Andrologia, vol. 44, no. 3, pp. 157–163, 2012.
View at: Publisher Site | Google Scholar
X. Wang, R. K. Sharma, A. Gupta et al., “Alterations in mitochondria membrane potential and oxidative stress in infertile men: a prospective observational study,” Fertility and Sterility, vol. 80, no. Suppl 2, pp. 844–850, 2003.
View at: Publisher Site | Google Scholar

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Copyright © 2023 M. A. Setumo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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