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Year : 2019  |  Volume : 12  |  Issue : 1  |  Page : 4-18

Role of oxidative stress in male infertility: An updated review

Department of Pathological Analysis, College of Science, University of Sumer, Thi-Qar, Iraq

Date of Web Publication10-Apr-2019

Correspondence Address:
Dr. Ahmed T Alahmar
College of Science, University of Sumer, Al-Rifa'i
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jhrs.JHRS_150_18

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Current evidence links oxidative stress (OS) to male infertility, reduced sperm motility, sperm DNA damage and increased risk of recurrent abortions and genetic diseases. A review of PubMed, Medline, Google Scholar, and Cochrane review databases of published articles from years 2000–2018 was performed focusing on physiological and pathological consequences of reactive oxygen species (ROS), sperm DNA damage, OS tests, and the association between OS and male infertility, pregnancy and assisted reproductive techniques outcomes. Generation of ROS is essential for reproductive function, but OS is detrimental to fertility, pregnancy, and genetic status of the newborns. Further, there is a lack of consensus on selecting OS test, type, and duration of antioxidants treatment as well as on the target patients group. Developing advanced diagnostic and therapeutic options for OS is essential to improve fertility potential and limit genetic diseases transmitted to offspring.

Keywords: Antioxidants, male infertility, oxidative stress, sperm DNA damage

How to cite this article:
Alahmar AT. Role of oxidative stress in male infertility: An updated review. J Hum Reprod Sci 2019;12:4-18

How to cite this URL:
Alahmar AT. Role of oxidative stress in male infertility: An updated review. J Hum Reprod Sci [serial online] 2019 [cited 2023 Feb 3];12:4-18. Available from:

   Introduction Top

Infertility is defined as the inability to achieve pregnancy after 1 year of regular unprotected sexual intercourse.[1] The global prevalence of infertility varies between 2.5%–15%, correlating to at least 30 million infertile men worldwide.[2] Infertility has been linked to several emotional, physical, and sociocultural problems.[3] One of the mechanisms proposed for idiopathic male infertility is oxidative stress (OS). Male infertility accounts for about 40% of all cases and it is known that some conditions such as varicocele, cryptorchidism, hypogonadism, and genetic factors can cause infertility. However, no underlying cause can be identified for primary or secondary infertility in approximately 25% of couples which is termed idiopathic infertility.[4] One of the proposed mechanisms for idiopathic infertility is OS and reactive oxygen species (ROS).

Increased ROS along with decreased antioxidant defense result in redox imbalance, reduced sperm motility and sperm DNA damage. Spermatozoa are highly susceptible to the deleterious effects of ROS due to the large amounts of unsaturated fatty acids found in their cell membranes. Reactive oxygen species promote peroxidation of lipids, resulting in intracellular oxidative burden. The sequence of events involves lipid peroxidation, loss of membrane integrity with increased permeability, reduced sperm motility, structural DNA damage, and apoptosis.[5],[6],[7] Several intrinsic and extrinsic factors have been associated with increased OS in the male reproductive system.

The World Health Organization (WHO) has published references values for seminal fluid analysis parameters.[8] Decreased sperm concentration – defined as < 15 ×106 sperm/ml – is termed oligozoospermia; whereas asthenozoospermia corresponds to progressive sperm motility of <32% or total sperm mobility under 40%. Teratospermia is defined as normal sperm motility of <4% using Kruger's strict criteria.[9] The combination of all these abnormalities is termed oligoasthenoteratozoospermia.

Currently, there is a lack of agreement on which patients should be tested for OS, as well as which test to perform. There are also controversies on types, dose, and duration of antioxidants treatment of in patients with excessive ROS levels.[10] Therefore, the aim of this review is to provide an update on current evidence regarding ROS production, tests and the association between OS and male infertility as well as pregnancy and assisted reproductive techniques (ART) outcomes.

   Methods Top

This review of literature included a systematic search strategy performed in electronic scientific databases PUBMED, Medline, Google Scholar, and Cochrane review to include published articles from years 2000 to 2018. The search involved keywords including combinations of search terms “oxidative stress,” “reactive oxygen species,” “semen parameters,” “male infertility,” “sperm function,” “antioxidants,” “semen analysis,” “oxidative stress tests,” “pregnancy outcomes,” and “assisted reproductive techniques.” Articles were perused, and their reference lists were checked for relevant publications. We included articles published in English only.

   Oxidative Stress Definition Top

OS is defined as an imbalance between the production of reactive oxygen species (ROS) and the scavenging capacity of available antioxidants resulting in redox paradox.[11] Sperm cells are vulnerable to ROS because of the abundance of polyunsaturated fatty acids in their plasma membrane and cytoplasm [12] and limited antioxidant capacity and DNA repair system.[13] Certain levels of ROS are required for maturation of spermatozoa, acrosome reaction, capacitation, hyperactivation, and sperm-oocyte fusion.[14] Excessive ROS production, however, overwhelms the neutralizing capability of antioxidants (enzymatic and nonenzymatic) in the seminal plasma. ROS are formed as natural byproducts of oxygen during metabolism and have important roles in cell signaling and homeostasis.[15] Sources of ROS can be endogenous or exogenous [Figure 1] and body antioxidant defense mechanism aims to neutralize the harmful effects of these pro-oxidants molecules.
Figure 1: Sources of reactive oxygen species in the body and their pathological consequences on semen, fertility and health. ROS = Reactive oxygen species, OS = Oxidative stress

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   Sources of Reactive Oxygen Species Top


Redox reactions in aerobic metabolism yield ROS as byproducts. In mitochondria, these reactions require nicotinamide adenine dinucleotide (NADH) as an electron donor and acceptor in the electron transport chain, which allows synthesis of adenosine triphosphate (ATP)[16] [Figure 1]. Seminal fluid ROS can also originate from cytoplasmic glucose-6-phosphate dehydrogenase.[17] Varicocele, the most common etiology of male infertility, has been linked with the increased oxidative burden and ROS-induced sperm DNA damage;[14] as well as with increased scrotal temperature.[18] These findings have been corroborated with evidence describing reduced levels of seminal lipid peroxidation and sperm DNA damage after varicocelectomy.[18] Moreover, increased temperature has also been related to increased ROS production and negative effects on other seminal fluid parameters.[19],[20] In particular, elevated ROS have been associated with male accessory gland infection, including the urethra, prostate, deferent ducts, seminal vesicles, epididymis, or testes.[21] This has been attributed to the capacity of seminal leukocytes to produce 1000-fold more ROS and free radicals than any other cell with aerobic metabolism.[22] Infections have also been independently associated with increased ROS.[23],[24] Furthermore, hyperglycemia is another important factor for male infertility, as strong correlations have been identified between prediabetes and diabetes mellitus with increased OS and altered sperm parameters.[25]


Extrinsic factors such as smoking, alcohol intake, and exposure to radiation and industrial heavy metals have been associated with increased ROS and male infertility [Figure 1]. Smoking has been associated with reduced sperm concentration, motility, and altered morphology.[26] Smoking also elicits a chronic inflammatory response which recruits leukocytes to the genital tract and causes a substantial increase in seminal ROS levels,[27] as well as increased sperm DNA damage.[13]

Seminal fluid abnormalities have been associated with excessive alcohol intake, including decreased spermatogenesis, abnormal sperm morphology, decreased seminal fluid volume, low levels of testosterone, and increased OS.[28] Indeed, alcohol abuse results in increased production of acetaldehyde which promotes the generation of ROS due to its interactions with proteins and lipids.[11]

Altered sperm function and increased DNA damage have been associated with industrial exposure to heavy metals such as lead, cadmium, iron, and copper, as well as exposure to phthalates, pesticides, and pollution.[20],[29] Malignancies are another important extrinsic source of ROS, along with the accompanying exposure to radiation and chemotherapy. Men treated with chemotherapy medications such as cisplatin, doxorubicin, or cyclophosphamide have been linked to increased OS.[30] Radiotherapy has also been associated with increased OS, while low-level radiation therapy appears to modulate NADH oxidase activity promoting sperm death.[31],[32]

   Antioxidants in Semen Top

Both enzymatic and nonenzymatic antioxidant protective systems have been identified in semen, which positively interact with each other to counteract the adverse effects of ROS.

Enzymatic antioxidants

Superoxide dismutase, catalase, and glutathione (GSH) peroxidase form the main antioxidant system in semen.[33] These metalloenzymes are present in both the intracellular and extracellular space. Superoxide dismutase catalyzes the dismutation of the superoxide anion, utilizing the copper and zinc molecules in its active center.[34] There are two main isoforms of superoxide dismutase (SOD) enzyme: SOD-1, with about 75% of the antioxidant, and SOD-3, with the remaining 25%.[35] Seminal SOD activity has been positively correlated with sperm concentration and motility.[36]

Catalase acts on hydrogen peroxide, resulting in its decomposition to water and molecular oxygen. The heme system with an iron atom in the center is the prominent characteristic of this enzyme, which can be found in the cytoplasm, endoplasmic reticulum, and various other organelles.[37] This enzyme is synthesized in the prostrate and catalase activity involves capacitation of nitric oxide and involvement of hydrogen peroxide.[33],[38] Catalase level has been positively correlated with progressive sperm motility in normospermic individuals.[39] GSH peroxidase is responsible for the catalytic reduction of hydrogen peroxide and organic peroxides, including the peroxides of phospholipids.[34] This enzyme contains selenium in its active site and is primarily located in the mitochondrial matrix of spermatozoa. A specific isoform protects sperm DNA from oxidative damage and chromatin condensation.[40] GSH peroxidase activity was reduced in individuals diagnosed with severe asthenozoospermia, oligozoospermia, and teratozoospermia.[41]

Nonenzymatic antioxidants

Numerous nonenzymatic antioxidants are present in semen, including Vitamins A, E, C, and B complex, GSH, coenzyme Q10, carnitine, and minerals such as zinc, copper, selenium, and chromium.[42] GSH is a tripeptide thiol with a wide array of biological functions, including the preservation of the intracellular redox status and detoxification of exogenous and endogenous compounds. Structurally, it stems from a combination of three amino acids; cysteine, glycine, and glutamine. GSH possesses an innate reducing power that protects cells against OS, in particular, due to its sulfhydryl group (SH). GSH is found in both its oxidized and reduced forms. The antioxidant mechanisms of GSH are mediated by associated enzymes such as GSH peroxidase and GSH reductase.[43]

Vitamin E or alpha-tocopherol is a fat-soluble molecule found in almonds, avocados, spinach, and sweet potatoes. It has potent antioxidant properties, by neutralizing free radicals and inhibiting ROS damage to cell membranes; resulting in prevention of lipid peroxidation and enhancement of other antioxidants. According to the European Commission Directive 2008/100/EC, the recommended daily intake of Vitamin E is 12 mg.[44] In an interventional placebo-controlled trial on infertile men conducted by Greco et al.,[45] minimal sperm DNA damage was observed after 2-month supplementation of Vitamin E (1 g/day) and Vitamin C (1 g/day).

Vitamin C is a water-soluble vitamin with antioxidant properties found in citric fruits and fresh berries. Numerous studies have evaluated the effect of Vitamin C supplementation on sperm function. A study performed on male rats showed ascorbic acid could revert testicular OS induced by cyclophosphamide.[46] In another study, reduced levels of Vitamin C and increased ROS levels were detected in the seminal fluid of men with asthenozoospermia.[47] Carotenoids are a group of organic compounds found in orange, red, yellow, and pink vegetable dyes, which act as precursors for Vitamin A, whose integral component is retinol. These are naturally occurring antioxidants, necessary for maintaining the integrity of cell membranes. They are also involved in the regulation of spermatogenesis. Carotenoid deficiency can lead to decreased sperm motility and male infertility.[48]

Zinc is the second-most abundant metal in the human body and a cofactor for various enzymes involved in DNA transcription and protein synthesis, playing a pivotal role in reproduction. Zinc participates in various reproductive processes such as steroidogenesis, testicular development, gonadal differentiation, production of luteinizing hormone and follicle stimulating hormone, formation and maturation of spermatozoa, acrosome reaction, and fertilization.[49],[50] The WHO currently estimates zinc deficiency to affect one-third of the population worldwide. Zinc, along with various antioxidant enzymes, may improve sperm parameters and increase the likelihood of pregnancy for men with oligoasthenoteratozoospermia.[51] Selenium is another essential trace element, which intervenes in sperm formation and testosterone synthesis.[52] At least 25 selenoproteins have been identified in humans and animals, involved in the maintenance of sperm structural integrity. Several randomized clinical trials have tried selenium in combination with other antioxidants with promising results.[53],[54]

   Physiological Role of Reactive Oxygen Species in Male Fertility Top

The development of male germ cells yields significant amounts of ROS which constitutes a principal source of OS in spermatozoa.[55] Reactive oxygen species modulate sperm chromatin condensation by adjusting the number of germ cells and inducing apoptosis or proliferation of spermatozoa.[56] ROS are also involved in the processes of capacitation, acrosome reaction, mitochondrial stability, and sperm motility in mature sperm. ROS can function as messengers, by modulating the NADPH oxidase enzyme complex in the cell membrane, and intervening in the respiratory chain within mitochondria. In spermatozoa, superoxide anion metabolism is regulated by the NADH oxidoreductase enzyme, which works in close conjunction with the mitochondrial respiratory chain and xanthine oxidase found in sperm and seminal plasma.[33] Immature spermatozoa with cytoplasmic residues show increased production of ROS when compared to sperm with normal morphology.[17],[57]

Seminal leukocytes are another source of ROS, producing 1000 times more of these molecules than sperm cells under physiological conditions. This is because seminal leukocytes represent the first line of defense against offending infectious agents, using primarily oxidative and inflammatory mechanisms.[22] However, this can become a double-edged sword, as an imbalance between oxidants and antioxidants could result in cellular injury. Indeed, ROS generated to counteract infectious agents can also damage host cells, which can result in the disintegration of the cell membrane or sperm DNA damage.

   Pathological Effects of Reactive Oxygen Species on Male Fertility Top

The rationale behind the use of antioxidants for the treatment of male infertility relies on excessive levels of ROS and free radicals cause altered sperm function and sperm DNA damage. A study Desai et al. found that sperm characteristics were significantly lower in infertile men with high levels of ROS in semen as assessed through chemiluminescence.[32] Reactive oxygen species alter DNA integrity in the sperm nucleus by inducing breakage of DNA strands, base modifications, and chromatin cross-linking [Figure 1].[58] Moreover, spermatozoa have limited defense mechanisms against ROS-induced DNA damage.

Human ejaculate contains sperm cells with various degrees of maturity, along with leukocytes, epithelial cells and round cells from different stages spermatogenesis. Among these cells, peroxidase-positive leukocytes and immature spermatozoa produce significant amount of free radicals.[59] Spermatozoa are especially susceptible to oxidative damage due to the presence of abundant polyunsaturated fatty acids in their plasma membrane. These fatty acids are important as they provide membrane fluidity, a key feature for several membrane fusion events such as acrosome reaction and sperm-egg interactions. However, these unsaturated fatty acids render them vulnerable to free radical attacks and ongoing lipid peroxidation.[60]

Nevertheless, in around 85% of cases, the sperm genome is protected from free radical damage as it is bound to central nucleoprotamines.[13] Deficient protamination has been observed in infertile men, representing yet another source of ROS-induced DNA damage [61] which is compounded by the limited capacity for sperm DNA repair seen during spermatogenesis.[62] ROS-mediate disruption of mitochondrial membranes leads to caspase activation, resulting in apoptosis. The apoptotic pathways involve cytochrome c release, which augments the levels of ROS, DNA damage, and apoptosis.[63]

DNA bases are also prone to OS-induced damage with base modifications, strand-breaks, and chromatin cross-linking. Indeed, OS and apoptosis are key events involved in causing DNA damage in the germ line.[64] The major role of ROS in the etiology of sperm DNA damage in infertile men has been corroborated in multiple studies.[65],[66],[67],[68]

Spermatozoa carry a complete haploid genome to the ovum to form a new individual. Condensation of the nuclear material in the sperm nucleus is essential for this process to be successful. This condensation is promoted by the unique process of protamination, which involves the replacement of histones by positively charged protamines, which in turn form tight toroidal complexes. This is essential, as chromatin organization is necessary for fertilization and early embryonic development.[69] However, normal sperm appears to possess varying degrees of fragmented DNA; although, infertile men appear to have larger proportions of fragmented DNA.[70]

Both extrinsic and intrinsic factors are involved in the pathogenesis of fragmented DNA. The latter include poor chromatin structure and limited repair capacity. Intrinsic factors include abortive apoptosis and defective maturation.[71],[72] Accumulating evidence suggests extrinsic factors are responsible for the increased DNA fragmentation found in the epididymis and ejaculated sperm in comparison to testicular sperm.[73] Recent research posits OS as another extrinsic cause of sperm DNA fragmentation (SDF),[74] as ROS can surpass the limited antioxidant mechanisms of sperm and damage polyunsaturated fatty acids in membranes, resulting in SDF.[75],[76]

   Sperm DNA Damage Induced by Reactive Oxygen Species Top

Although ROS seem to play a physiological role in the acrosome reaction, normal sperm function, activation, motility, and capacitation;[77] their potentially deleterious effects cannot be overlooked. Spermatozoa are especially vulnerable to ROS as they contain large amounts of polyunsaturated fatty acids in their plasma membrane and cytoplasm. OS could induce a rapid loss of intracellular ATP, resulting in axonemal damage with decreased sperm viability and mobility and increased mid-piece structural defects, with deleterious effects on sperm capacitation and the acrosome reaction. Lipid peroxidation of the sperm membrane is a key mediator of ROS-induced sperm damage, leading to infertility [Figure 1].[78],[79]

Hydrogen peroxide is the principal ROS in human spermatozoa, while excessive production of ROS by abnormal spermatozoa or leukocytes appears to be associated with male infertility.[75] Moderately elevated concentrations of hydrogen peroxide cause sperm immobilization, mostly through depletion of intracellular ATP and reduced phosphorylation of axonemal proteins, with no impact on viability. In contrast, higher concentrations of hydrogen peroxide promote lipid peroxidation and cell death.[80],[81]

In a study by Pasqualotto et al.,[82] the levels of antioxidants in seminal plasma from infertile men were significantly lower than in fertile controls, and the levels of ROS produced by spermatozoa were negatively correlated with sperm quality. In semen of infertile men, pathological levels of ROS are likely to be the result of increased ROS production and impaired antioxidant capacity.[83]

Exogenous or endogenous sources of ROS can induce sperm DNA damage that in turn may cause childhood diseases such as autosomal dominant disorders, neuropsychiatric disorders, and childhood cancers like retinoblastoma.[84],[85] OS tends to target on telomeres, which are key genome protectors. Telomeres erode faster when exposed to OS, resulting in telomere dysfunction, chromosome instability, and apoptosis; all of which have been related to aging and carcinogenesis.[86]

This form of DNA damage could be particularly important in recurrent spontaneous abortion (RSA). Various paternal factors have been linked to RSA, including ROS-induced sperm DNA damage. In a study on 25 couples with idiopathic RSA and 25 proven fertile controls, ROS levels and DNA damage were significantly higher among the men in the RSA group.[87] Mitochondrial dysfunction and OS have been associated with cancer, cellular senescence, apoptosis and aging; as well as with isolated cases of asthenozoospermia.[88] Antioxidants may prevent telomere loss and promote genomic stability in cells with mitochondrial dysfunction, corroborating the association with OS. Furthermore, nuclear transfer protected the genomes from telomere dysfunction and reconstitution of the mitochondria, thereby promoting cell survival.[89]

Lipid peroxidation cascade contributes to the production of free radicals and induces the production of lipid aldehydes such as acrolein, 4-hydorxynonenal (4-HNE), and malondialdehyde (MDA).[12] These have been linked with OS and damage to nuclear and mitochondrial DNA, with shorter telomeres, formation of the base product 8-hydroxy-deoxyguanine (8-OHdG), and fragmentation of mitochondrial DNA. They can also affect sperm plasma membranes, thus affecting their motility and ability to fuse with the oocyte. Production of 8-OHdG facilitates DNA damage by limiting the repairing capacity of spermatozoa.[90] Because fragmented DNA carries a high mutagenic potential, the oocyte may skip the base-excision repair and correction of 8-OHdG-associated changes, resulting in genomic hypermutability and instability, as well as infertility.[91] A high incidence of genetic aberrations in embryos have been attributed to ROS-induced OS in the male germ line; in association with conditions such as childhood cancers, neuropsychiatric disorders such as autism and schizophrenia, and dominant gene mutations such as Apert syndrome and achondroplasia.[13]

   Antioxidant Therapy in Male Infertility Top

The rationale for oral antioxidant therapy is because seminal OS is due to increased ROS production and/or decreased levels of seminal antioxidants.[60] The different oral antioxidants available belong to the exogenous antioxidant category and they include Vitamin C, Vitamin E, coenzyme Q10, N-acetyl cysteine, carnitines, trace elements such as zinc, selenium, pentoxifylline, and a combination of these oral antioxidants. Numerous studies have been conducted to assess the effectiveness of oral antioxidant supplementation for the treatment of male infertility. Most of the studies showed an improvement in one or more of seminal fluid parameters,[92],[93] whereas some studies reported no positive effect [Table 1].[94],[95],[96]
Table 1: Antioxidant therapy in male infertility

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   Tests to Measure Reactive Oxygen Species in Semen Top

Assessment of sperm ROS levels among infertile men can aid in determining which individuals who may benefit from antioxidant therapy. Various tests have been developed to detect seminal ROS levels which can be classified into direct and indirect assays [Table 2] and [Table 3]. Currently, there are no infertility guidelines that recommend routine ROS measurement and there is still an ongoing debate on which type of patients have to be tested for the oxidative burden. Asthenozoospermia in a semen sample is probably a marker of ROS.[11] Hyperviscosity has also been suggestive of increased OS because it is attributed to increased malondialdehyde levels. Increased leukocytes or round cells which is one of the principal sources of ROS may suggest further testing for OS. Abnormal sperm morphology due to cytoplasmic residues also correlates with high levels of ROS.[10] The hypo-osmotic swelling test suggests membrane damage in the sperm due to lipid peroxidation and this might imply higher levels of ROS in semen. Besides, some studies recommend ROS testing in individuals with idiopathic infertility.[110]
Table 2: Direct assays of oxidative stress

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Table 3: Indirect assays of oxidative stress

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   Reactive Oxygen Species Effects on Pregnancy Loss and Outcomes Top

The effects of SDF on natural pregnancy and pregnancy outcome have been recognized.[111] The Danish First Pregnancy Planner study illustrated a correlation between infertility and an SDF index of >30%. There was a significant association between a high sperm SDF and increased time to conceive naturally and lower fertility potential.[112] Similarly, in 500 couples with no infertility history who discontinued contraception for the purpose of pregnancy and they were enrolled in the Longitudinal Investigation of Fertility and the Environment study, SDF was associated with low fecundity.[113] A meta-analysis included 616 couples demonstrated that three studies showed an odds ratio of 7.01 suggestive of an association between high SDF and failure to achieve natural pregnancy.[114]

OS has become a growing concern for researchers and clinicians because of association with decreased fertilization, poor embryonic development, pregnancy loss, potential birth defects such as autism and cancers.[11] The chromatin in the sperm DNA is vulnerable to OS and there are base-pair modifications along with DNA fragmentation. Sperm and oocyte DNA damage may interfere with implantation and ultimately result in abortion. Evidence suggests that about 80% of the chromosomal aberrations are of paternal origin in humans.[115] Further, sperm DNA damage has been implicated in apoptosis, poor fertilization rate, higher frequency of miscarriage, and morbidity in offspring.[11]

Emerging evidence suggests that in ART, there is a correlation between high SDF and an increased risk of miscarriage. In a systematic review reported by Rilcheva et al., it was found that after in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI), there were increased chances of pregnancy loss due to high SDF with a combined odds ratio of 2.48.[116] Another systematic review with 16 individual cohorts and 2969 couples corroborated the above results and it observed a 2.16-fold increase in the risk of pregnancy loss after IVF and ICSI with semen specimens with high SDF.[117] Both systematic reviews stated that the significant correlations between miscarriage rates and high SDF were independent of the method of fertilization used. A study involving 25 fertile sperm donors and 20 recurrent pregnancy loss (RPL) couples showed double-stranded DNA breaks analyzed by Comet assay among RPL sperm donors without any female factor.[118] A more recent study showed that there was a positive association between RSA and high SDF.[119]

   Reactive Oxygen Species, Fertility Capacity and Assisted Reproduction Techniques Outcomes Top

Reactive oxygen species and oxidation-reduction potential (ORP) play significant roles in the fertility process and in the outcome of ART. In a prospective case-control study carried out in 1168 infertile and 100 fertile men, semen analysis parameters, the ORP and SDF were compared. The study concluded that infertile men had significant lower semen parameters and higher ORP and SDF levels, and that a significant positive correlation exists between ORP, SDF, and sperm head defects.[120] In a meta-analysis by Van Waart et al., pregnancy rates achieved with intrauterine insemination (IUI) were correlated with normal sperm morphology and it was found a significant improvement in the pregnancy rate associated with >4% sperm morphology, and hence, they concluded that sperm morphology assessment by strict criteria is a good predictor of IUI outcome.[121] However, more recent studies failed to show an association of ART outcomes in groups with or without isolated teratozoospermia is semen.[122] Hotaling et al., reported that in four retrospective studies, isolated teratozoospermia was not associated with lower pregnancy rates following IVF or ICSI. Hence, the predictive power of sperm morphology on ART outcomes is still debatable.[123],[124]

The existing literature about the consequences of sperm DNA damage on ART outcomes is still controversial. Li et al. performed a meta-analysis and found that sperm DNA damage had a negative impact on IVF clinical pregnancy rates but did not affect the IVF and ICSI fertilization and the ICSI clinical pregnancy.[125] Another meta-analysis by Zini et al., evaluating the influence of sperm DNA damage on spontaneous pregnancy loss after IVF and ICSI, showed the detrimental effect of sperm DNA damage on ART outcomes and suggested a clinical test to evaluate the DNA damage before IVF or ICSI procedures.[126] However, the Practice Committee of the American Society for Reproductive Medicine concluded that the data in the existing literature does not support the adverse consequences of sperm DNA damage on ART and natural pregnancy outcomes, but recommends future research to validate the clinical utility of sperm integrity tests.[127] A more recent meta-analysis by Simon et al. including 41 studies showed that DNA damage in the sperm significantly correlated with adverse ART outcomes with IVF or ICSI techniques. The sperm DNA damage was evaluated using various tests such as Comet assay, sperm chromatin structure assay, terminal deoxyuridine nick end labeling assay, and sperm chromatin dispersion assay.[128] Therefore, despite that studies demonstrated correlation between sperm DNA damage and adverse ART events, the evidence is inconclusive as there is no standardization of the tests that has been used to detect sperm DNA damage.

   Conclusion Top

Although reactive oxygen species are essential for some reproductive processes such as capacitation and acrosome reaction, increased ROS along with decreased antioxidant defense result in OS status which ultimately leads to sperm membrane lipid peroxidation, reduced motility, sperm DNA damage, poor pregnancy, and ART outcomes and increased risk of genetic diseases in offspring. Various diagnostic and therapeutic options have been developed for OS. However, there is lack of agreement on selecting OS test, type, and duration of antioxidants treatment as well as on defining the target patients group. Further studies are warranted to overcome these limitations, improve fertility potential and reduce the risk of genetic diseases and malignant tumors in newborns.


The author would like to show sincere gratitude for anonymous reviewers for their valuable help and support to accomplish this work.

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Conflicts of interest

There are no conflicts of interest.

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Plants. 2022; 11(13): 1624
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13 Effect of Giving Traditional Drinks Kameko and Pongasih from Southeast Sulawesi on Sperm Quality of Mice (Mus musculus)
Indria Hafizah, Tien ., Dewi Akka, Satrio Wicaksono, Ida Afrini, Mubarak .
Pakistan Journal of Biological Sciences. 2022; 25(10): 892
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14 Oxidative stress and female reproductive disorder: A review
Kalaivani Manokaran, Pavithra Bhat, Deepak Nayak, Ravisankar Baskaran, Prabu Paramasivam, ShiekFareeth Ahmed, Keerthi Priya, KarkalaSreedhara Ranganath Pai, VigneshE Balaji
Asian Pacific Journal of Reproduction. 2022; 11(3): 107
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15 A correlative interaction between thyroid dysfunction and semen parameters in male infertility: A prospective case control study
M. Venkateswara Rao, K. V. N. Geetha Devi, D. Rajarajeswari, K. Ashalatha
Acta Medica Martiniana. 2022; 22(3): 129
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16 Influence of Single Layer Centrifugation with Canicoll on Semen Freezability in Dogs
Guillaume Domain, Hiba Ali Hassan, Eline Wydooghe, Osvaldo Bogado Pascottini, Anders Johannisson, Jane M. Morrell, Wojciech Nizanski, Ann Van Soom
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17 Measuring Reactive Oxygen Species in Semen for Male Preconception Care: A Scientist Perspective
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18 The Synergetic Effect of Egyptian Portulaca oleracea L. (Purslane) and Cichorium intybus L. (Chicory) Extracts against Glucocorticoid-Induced Testicular Toxicity in Rats through Attenuation of Oxidative Reactions and Autophagy
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19 Infertility in Men: Advances towards a Comprehensive and Integrative Strategy for Precision Theranostics
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20 Are There Associations between Seminal Plasma Advanced Oxidation Protein Products and Selected Redox-Associated Biochemical Parameters in Infertile Male Patients? A Preliminary Report
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21 Effects of BPA, BPS, and BPF on Oxidative Stress and Antioxidant Enzyme Expression in Bovine Oocytes and Spermatozoa
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22 Reprotoxic Impact of Environment, Diet, and Behavior
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International Journal of Environmental Research and Public Health. 2022; 19(3): 1303
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23 Costus root extract improves testicular toxicity of Bisphenol A in adult male albino rats: histopathological, ultrastructural and biochemical studies
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Beni-Suef University Journal of Basic and Applied Sciences. 2022; 11(1)
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24 Loss of Prm1 leads to defective chromatin protamination, impaired PRM2 processing, reduced sperm motility and subfertility in male mice
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25 What is known so far about bull sperm protamination: a review
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26 Indicators of antioxidant protection of the body of dairy cows depending on the phase of lactation and physiological state
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27 Mitochondrial metabolism determines the functional status of human sperm and correlates with semen parameters
Pilar Irigoyen, Paula Pintos-Polasky, Lucia Rosa-Villagran, Maria Fernanda Skowronek, Adriana Cassina, Rossana Sapiro
Frontiers in Cell and Developmental Biology. 2022; 10
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28 Systematic Review and Critical Analysis on Dietary Supplements for Male Infertility: From a Blend of Ingredients to a Rationale Strategy
Andrea Garolla, Gabriel Cosmin Petre, Francesco Francini-Pesenti, Luca De Toni, Amerigo Vitagliano, Andrea Di Nisio, Giuseppe Grande, Carlo Foresta
Frontiers in Endocrinology. 2022; 12
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29 Is oxidative stress evaluated in viable human spermatozoa a marker of good semen quality?
Giulia Traini, Lara Tamburrino, Linda Vignozzi, Elisabetta Baldi, Sara Marchiani
Frontiers in Endocrinology. 2022; 13
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30 Is a Ketogenic Diet Superior to a High-Fat, High-Cholesterol Diet Regarding Testicular Function and Spermatogenesis?
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31 The Impact of Non-caloric Sweeteners on Male Fertility: A Systematic Review and Narrative Synthesis in Rodent Models
Michelle L. Kearns, Fionn MacAindriu, Clare M. Reynolds
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32 Oxidative Stress and Male Infertility: Evidence From a Research Perspective
Bashir Ayad, Temidayo S. Omolaoye, Nicola Louw, Yashthi Ramsunder, Bongekile T. Skosana, Peter I. Oyeipo, Stefan S. Du Plessis
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33 Single injection of very mild dose botulinum toxin in the vastus lateralis improves testicular spermatogenesis and sperm motility in ageing experimental mice
Risna Kanjirassery Radhakrishnan, Sowbarnika Ravichandran, Aishwarya Sukesh, Balamuthu Kadalmani, Mahesh Kandasamy
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34 Sperm concentration and semen volume increase after smoking cessation in infertile men
Deniz Kulaksiz, Tuncay Toprak, Eda Tokat, Mehmet Yilmaz, Mehmet Akif Ramazanoglu, Asgar Garayev, Muhammed Sulukaya, Recep Burak Degirmentepe, Elnur Allahverdiyev, Murat Gul, Ayhan Verit
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35 Antioxidants (selenium and garlic) alleviated the adverse effects of tramadol on the reproductive system and oxidative stress markers in male rabbits
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36 Persea americana seed extract restores defective sperm quality and biochemical parameters relevant to reproduction in male wistar rats treated with cyclosporine A
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37 Autophagy and mitochondrial damage in the testis of high-fat diet fed rats
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38 The effect of testosterone and antioxidants nanoliposomes on gene expressions and sperm parameters in asthenospermic individuals
Masoomeh mohammadzadeh, Hamed Hamishehkar, Mahboubeh Vatanparast, ZHima Akhavan sales, Ali Nabi, Fahimeh Mazaheri, Fatemeh Mohseni, Ali Reza Talebi
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39 Trifolium pratense extract increases testosterone and improves sperm characteristics and antioxidant status in diabetic rats
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40 An overview of the role of metallic and nonmetallic nanoparticles and their salts during sperm cryopreservation and in vitro embryo manipulation
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41 Sperm motility in asthenozoospermic semen samples can be improved by incubation in a continuous single culture medium (CSCM®)
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42 Predictors of pregnancy and time to pregnancy in infertile men with idiopathic oligoasthenospermia pre- and post-coenzyme Q10 therapy
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43 Beneficial effect of L- Proline supplementation on the quality of human spermatozoa
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44 Therapeutic efficacy of N -acetylcysteine and zinc sulphate against di-(2-ethylhexyl) phthalate-induced testicular oxido-nitrergic stress in male Wistar rat
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45 The effect of Fumaria parviflora on the expression of sexual hormones along with their receptors in testicles of adult rats induced by varicocele
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46 A review on applications and toxicities of metallic nanoparticles in mammalian semen biology
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47 Long-term sperm storage in eusocial H ymenoptera
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48 The therapeutic effect of co-administration of pentoxifylline and zinc in men with idiopathic infertility
Zeynab Dadgar, Seyed Mohammad Ali Shariatzadeh, Malek Soleimani Mehranjani, Abdolreza Kheirolahi
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49 Sperm oxidative status varies with the level of sperm competition and affects male reproductive success
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50 Motility and oxidative stress of common carp Cyprinus carpio sperm during short-term storage
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51 The influence of salinity on the toxicity of chemical UV-filters to sperms of the free-spawning mussel Mytilus galloprovincialis (Lamark, 1819)
Alessia Cuccaro, Lucia De Marchi, Matteo Oliva, Gianfranca Monni, Vincenzo Miragliotta, Giorgia Fumagalli, Rosa Freitas, Carlo Pretti
Aquatic Toxicology. 2022; 250: 106263
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52 Reduction of SLC7A11 and GPX4 Contributing to Ferroptosis in Sperm from Asthenozoospermia Individuals
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53 Exercise training amplifies SIRT1/Nrf2/antioxidant/testosterone pathway after long-time tramadol toxicity in rat testicles; insights into miR-126-3p and miR-181a induced roles
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54 d -ribose- l -cysteine abrogates testicular maladaptive responses induced by polychlorinated bisphenol intoxication in rats via activation of the mTOR signaling pathway mediating inhibition of apoptosis, in
Oyovwi O. Mega, Tesi P. Edesiri, Emojevwe Victor, Nwangwan E. Kingsley, Rotu A. Rume, Falajiki Y. Faith, Ovuakporaye I. Simon, Bright O. Oghenetega, Ejime Agbonifo-Chijiokwu
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55 In vitro testicular toxicity of environmentally relevant endocrine-disrupting chemicals: 2D vs. 3D models of prepubertal Leydig TM3 cells
Eliška Sychrová, Affiefa Yawer, Petra Labohá, Amrita Basu, Aneta Dydowiczová, Ishita Virmani, Pavel Babica, Iva Sovadinová
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56 A microplate-based DCFH-DA assay for the evaluation of oxidative stress in whole semen
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57 Quercetin-loaded on whey protein improves male fertility parameters and atherogenic indices of rats on a western-style diet
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58 Altered sperm fate in the reproductive tract milieu due to oxidative stress leads to sub-fertility in type 1 diabetes females: A Drosophila-based study
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59 Preliminary investigation on impact of intergenerational treatment of resveratrol endorses the development of ‘super-pups’
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60 Comparison of polymorphism 139C?>?A ( (rs737008) of protamine 1 gene in infertile men with diagnosis of oligospermia and asthenospermia
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61 Dietary supplementation with canthaxanthin and 25-hydroxycholecalciferol on the incubation performance and fertility of European quail breeders
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62 Sperm flow cytometric parameters, antioxidant status, and testicular histomorphology in roosters fed diets supplemented with camphor
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63 Sperm DNA fragmentation in reproductive medicine: A review
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64 Comparison of the effects of coenzyme Q10 and Centrum multivitamins on semen parameters, oxidative stress markers, and sperm DNA fragmentation in infertile men with idiopathic oligoasthenospermia
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65 Semen evaluation: methodological advancements in sperm quality-specific fertility assessment — A review
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66 Evaluation of Serum Selenium Status by Age and Gender: A Retrospective Observational Cohort Study in Western Romania
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67 Determination of Semen Quality and Antibacterial Susceptibility Pattern of Bacteria Isolated from Semen of Iraqi Subjects
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68 Spermatogenic and Leydig Cells Induced Hyperlipidemia: A Review
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69 Coenzyme Q10 Improves Sperm Parameters, Oxidative Stress Markers and Sperm DNA Fragmentation in Infertile Patients with Idiopathic Oligoasthenozoospermia
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70 Highly Cited Articles in the Field of Male Infertility and Antioxidants: A Scientometric Analysis
Ashok Agarwal, Manesh Kumar Panner Selvam, Saradha Baskaran, Renata Finelli, Kristian Leisegang, Catalina Barbaro?ie, Peter Natesan Pushparaj, Kathy Amy Robert, Rafael F. Ambar, Concetta Iovine, Damayanthi Durairajanayagam, Ralf Henkel
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71 A Global Survey of Reproductive Specialists to Determine the Clinical Utility of Oxidative Stress Testing and Antioxidant Use in Male Infertility
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72 Coenzyme Q10, oxidative stress markers, and sperm DNA damage in men with idiopathic oligoasthenoteratospermia
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73 Coenzyme Q10, oxidative stress, and male infertility: A review
Ahmed T. Alahmar, Aldo E. Calogero, Rajender Singh, Rossella Cannarella, Pallav Sengupta, Sulagna Dutta
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74 Male subfertility and oxidative stress
Emily P.P. Evans, Jorien T.M. Scholten, Aldona Mzyk, Claudia Reyes-San-Martin, Arturo E. Llumbet, Thamir Hamoh, Eus G.J.M. Arts, Romana Schirhagl, Astrid E.P. Cantineau
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75 Toxicity associated with long term use of aluminum cookware in mice: A systemic, genetic and reproductive perspective
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76 Ellagic acid Nanoparticles Attenuate Oxidative Stress and Testicular Damage in High Fat Diet/Streptozotocin-Induced Diabetic Rats
Steve Harakeh, Mohammed Qari, Nisreen Rajeh, Soad Ali, Nagla El-Shitany, Saber Hassan, Elham A. Abd-Allah, Hanaa Tashkandi, Muhammad Faraz Arshad Malik, Feras Khaled Aljabri, Leena Azhar, Najiah Azhar, Soad Al-Jaouni, Yousef Almehmadi, Turki Al Amri, Shaker Mousa
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77 Soursop juice enhanced seminal antioxidant defence and semen quality of rabbit bucks in extremely dry climatic condition of Southwestern Nigeria
Olatunji Abubakar Jimoh, Bolaji Fatai Oyeyemi, Wahab Adekunle Oyeyemi
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78 Combining in vivo pathohistological and redox status analysis with in silico toxicogenomic study to explore the phthalates and bisphenol A mixture-induced testicular toxicity
Katarina Baralic, Dragica Jorgovanovic, Katarina Živancevic, Aleksandra Buha Djordjevic, Evica Antonijevic Miljakovic, Milica Miljkovic, Jelena Kotur-Stevuljevic, Biljana Antonijevic, Danijela Đukic-Cosic
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79 Mangiferin mitigates di-(2-ethylhexyl) phthalate-induced testicular injury in rats by modulating oxidative stress-mediated signals, inflammatory cascades, apoptotic pathways, and steroidogenesis
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80 Influences of the polymorphisms of the Sod2 gene (rs4880) on the motility and vigor of X- and Y-bearing sperm at different pH values
Francis Jackson de Oliveira Paludo, Matheus Augusto de Bittencourt Pasquali, Amanda Rodrigues de Vargas, Iara Bezerra de Oliveira, Luzia Valberligia Batista Gonçalves, Daniel Pens Gelain, José Cláudio Fonseca Moreira
Biomedicine & Pharmacotherapy. 2021; 142: 111993
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81 Impact of Coenzyme Q10 and Selenium on Seminal Fluid Parameters and Antioxidant Status in Men with Idiopathic Infertility
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82 Ethnobotanical knowledge of medicinal plants used in the treatment of male infertility in southern Benin
Eric Agbodjento, Jean Robert Klotoé, Téniola Isabelle Sacramento, Victorien Dougnon, Frontenel Lopez Tchabi, Esther Déguénon, Jean-Marc Atčgbo
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83 Waterpipe Tobacco Smoke Exposure during Lactation—Susceptibility of Reproductive Hormones and Oxidative Stress Parameters in Male Progeny Rats
Nour A. Al-Sawalha, Indira D. Pokkunuri, Karem H. Alzoubi, Omar F. Khabour, Bashar N. Almomani
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84 Diet Supplemented with Chrysophyllum albidum G. Don (Sapotaceae) Fruit Pulp Improves Reproductive Function in Hypertensive Male Rats
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85 Vitamin D3 Supplementation Effects on Spermatogram and Oxidative Stress Biomarkers in Asthenozoospermia Infertile Men: a Randomized, Triple-Blind, Placebo-Controlled Clinical Trial
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86 Antioxidant enzymes and association of CAT SNP-21 A/T (rs7943316) with male infertility
Khulah Sadia, Sikandar Sultan, Kifayatullah Khan, Leonel M. Javeres, Baseerat Rumman, Syed T. A. Shah, Sajida Batool, Syed M. Nurulain
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87 Potential of total-reflection X-ray spectrometry for multielement analysis of biological samples using dilution or suspension sample preparation techniques
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88 Indicators of the Lipid Peroxidation—Antioxidant Protection System as Important Metabolic Markers of Reproductive Potential in Men
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89 Lack of trusted diagnostic tools for undetermined male infertility
Swati Pandruvada, Rachel Royfman, Tariq A. Shah, Puneet Sindhwani, James M. Dupree, Samantha Schon, Tomer Avidor-Reiss
Journal of Assisted Reproduction and Genetics. 2021; 38(2): 265
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90 Organopesticides and fertility: where does the link lead to?
Baskar Venkidasamy, Umadevi Subramanian, Ramkumar Samynathan, Govindasamy Rajakumar, Mohammad Ali Shariati, Ill-Min Chung, Muthu Thiruvengadam
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91 Quercetin improves the apoptotic index and oxidative stress in post-thaw dog sperm
Seonggyu Bang, Ahmad Yar Qamar, Bereket Molla Tanga, Xun Fang, Gyeonghwan Seong, Abdelbagi Hamad Talha Nabeel, Il-Jeoung Yu, Islam M. Saadeldin, Jongki Cho
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92 Effects of hazelnut supplemented diet on doxorubicin-induced damage of reproductive system in male rats
Hanife Kara, Asim Orem, Esin Yulug, Fulya Balaban Yucesan, Gokcen Kerimoglu, Birgul Vanizor Kural, Serap Ozer Yaman, Akin Bodur, Sibel Turedi, Cesarettin Alasalvar
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118 Effectiveness of Exercise Training on Male Factor Infertility: A Systematic Review and Network Meta-analysis
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119 Multiparametric Study of Antioxidant Effect on Ram Sperm Cryopreservation—From Field Trials to Research Bench
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130 Comparative analysis of the subjective perception of oneself as a future parent among married couples with different reproductive history
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153 Impact of Oxidative stress on Infertility, with emphasis on infertility management strategies
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154 Antioxidant Effects of Marigold (Calendula officinalis) Flower Extract on the Oxidative Balance of Bovine Spermatozoa
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