The Relationship between Sperm Oxidative Stress Alterations and IVF/ICSI Outcomes: A Systematic Review from Nonhuman Mammals
Abstract
:1. Introduction
2. Methods
2.1. Systematic Review Execution and Registration
2.2. Data Sources and Systematic Search Strategy
2.3. Study Eligibility
2.4. Study Selection Procedure
2.5. Data Extraction for Systematic Review and Statistics
3. Results
3.1. Identification and Selection of Articles for Qualitative Analysis
3.2. Systematic Review: Qualitative Analysis
3.2.1. Effect of Different Treatments on Spermatozoa
3.2.2. Effect of the Different Treatments on IVF/ICSI Outcomes
4. Discussion
4.1. Strengths and Limitations
4.2. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Appendix A
References
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Animal | Total Studies | Fertilization Method | Oocyte Origin | |||
---|---|---|---|---|---|---|
IVF Studies | ICSI Studies | IVM | Superovulated | Nonspecified | ||
Pig | 3 | 3 | 0 | 3 | - | - |
Cattle | 9 | 8 | 1 | 7 | 1 | 1 |
Mice | 13 | 7 | 6 | - | 12 | 1 |
Mouse and Hamster | 1 | 0 | 1 | - | 1 | - |
Sheep | 1 | 0 | 1 | 1 | - | - |
Rat | 1 | 1 | 0 | - | 1 | - |
Macaque | 1 | 0 | 1 | - | 1 | - |
Horse | 1 | 0 | 1 | - | 1 (only ovulation induction) | - |
ID | Reference | Aim | Animal | Treatment | Sperm Parameter Measured | Effects of Treatment on Sperm | Oocyte Origin | IVF or ICSI | Effects on IVF/ICSI | Conclusion |
---|---|---|---|---|---|---|---|---|---|---|
1 | Ahmadi et al. 1999 [40] | To study the developmental capacity of spermatozoa at various levels of disintegration. | MouseHamster | Frozen twice without cryoprotectant plus DTT and gamma radiation | DNA damage: TUNEL | Increased DNA damage. | Super-ovulated | ICSI | - Similar fertilization rates - Lower blastocyst development - Lower live birth rate | Impairment of sperm cells causes a reduction in ICSI outcomes. |
2 | Arias et al. 2014 [41] | To evaluate the effects of pretreatment of bovine spermatozoa with NaOH and DTT on in vitro developmental potential. | Cattle | Incubation of sperm with 5 mM DTT for 20 min and 1 mM NaOH for 60 min | DNA fragmentation: TUNEL | Highest concentrations of NaOH led to high DNA damage. | Super-ovulated | ICSI | - High concentration of NaOH blocked blastocyst development | NaOH has a detrimental effect on embryo development after ICSI. |
3 | Bittner et al. 2018 [42] | To elucidate whether sperm oxidative stress results in increased DNA damage in the embryo. | Cattle | Incubation of sperm with H2O2 | DNA damage: SCSA | Exposure of sperm to H2O2 led to an increase of DNA damage in the embryo. | IVM | IVF | - Embryo development was delayed when sperm were incubated with H2O2 treatment - Reduced cleavage and blastocyst rates | Oxidative stress in spermatozoa induces developmental abnormalities in the embryo. |
4 | Burruel et al. 2013 [38] | To determine whether sperm oxidative damage induced by ROS affects embryo development. | Rhesus Macaque | Oxidation of sperm cells with xanthine oxidase. | - Lipid peroxidation | Treatment with xanthine oxidase led to an increase of lipid peroxidation. | Super-ovulated | ICSI | - Exposure to high levels of ROS leads to arrest of embryo development before eight-cell stage. Additionally, all stages were affected in the treated group. | Paternal oxidative stress influences early embryo development. |
5 | Castro et al. 2016 [43] | To assess the impact of sperm oxidative stress on embryo development. | Cattle | Incubation of sperm with increasing doses of H2O2 | - Oxidative status: CellROX green - DNA damage: SCSA | Incubation causes an increase of oxidative stress and alterations in chromatin integrity. | IVM | IVF | - Cleavage rates, development to 8 cells and percentages of blastocysts are inversely related to H2O2 concentration | Oxidative environment can impair bull sperm quality, affecting embryo development. |
6 | Castro et al. 2018 [44] | To predict in vitro bull fertility with the assessment of DNA integrity. | Cattle | High vs. low fertility bulls based on embryo development rate | - DNA damage: SCSA and Comet - DNA condensation: CMA3 | None. | Not specified | IVF | - SCSA and Comet did not show differences between high and low fertility groups - DNA condensation (CMA3 test) was lower in the high fertility group. | The differences found in DNA condensation through CMA3 were not sufficient to explain differences in fertility rates. |
7 | Cho et al. 2003 [45] | To determine whether a reduction in protamine content results in failure to transmit the male genome to next generation. | Mouse | Chimeric, Prm2−/>− mice | - DNA damage: Comet assay | DNA damage was observed in chimeras, affecting more than 70% spermatozoa. | Not specified | ICSI | - Arrested embryos at metaphase. - Less embryos developed to later stages. | Protamine 2 is essential to maintain sperm DNA integrity and to promote embryo development. |
8 | Ebadi Manas et al. 2013 [46] | To elucidate how pyridaben can affect sperm quality and in vitro fertilizing ability. | Mouse | Oral administration of pyridaben for 45 days at two different doses | - Chromatin integrity: Aniline blue and acridine orange | Increase of sperm DNA damage. | Super-ovulated | IVF | - Lower fertilization rates - Lower development to blastocyst rates | Pyridaben induces DNA damage, which decreases fertilization and blastocyst rates. |
9 | Fatehi et al. 2006 [47] | To investigate whether and at what level the paternal DNA damage influences fertilization and embryo development. | Cattle | Irradiation with X or Gamma rays | - DNA damage: TUNEL and Acridin Orange | Sperm DNA damage increased in a dose dependent manner. | IVM | IVF | - Similar rates of embryo cleavage at day 4 - Embryo development to blastocyst was severely impaired | DNA damage induced by radiations impair embryo development to blastocyst. |
10 | Gawecka et al. 2013 [19] | To test how zygotes respond to DNA damage during the first cell cycle. | Mouse | Induction of DNA damage with manganese and calcium | - DNA damage: Pulsed Field Gel Electrophoresis | Double strand DNA damage detected by Pulsed Field Gel Electrophoresis (PFGE). | Super-ovulated | ICSI | - Chromosomal alterations at first paternal pronucleus - No fertilization impairment - Embryo development was delayed after fertilization and arrested before reaching the blastocyst stage | DNA damage is important for proper embryo development at initial stages. |
11 | Gonçalves et al. 2010 [48] | To investigate the effects of antioxidants and a pro-oxidant on the quality and fertilizing ability of bull spermatozoa. | Cattle | Sperm were co-incubated with antioxidants (β-mercaptoethanol and Cysteamine) or pro-oxidant (buthionine sulfoximine) molecules | - DNA damage: Acridine Orange | No effect on sperm DNA damage, but reduction of plasma membrane integrity. | IVM | IVF | - Antioxidants and pro-oxidants reduced fertilization and blastocyst rates | Supplementation with antioxidants and with pro-oxidants during IVF procedures impaired sperm quality, normal pronuclear formation and development to blastocyst. |
12 | Gonzalez-Castro et al. 2018 [49] | To determine which sperm population characteristics are predictive of ICSI outcome. | Horse | Evaluation of DNA damage and plasma membrane integrity | - Membrane integrity: HOS test - DNA damage: SCD test | None. | Ovulation induction and follicle aspiration | ICSI | - DNA damage was not associated to any fertilization, embryo development or pregnancy | Plasma membrane integrity was the parameter with higher association to ICSI outcome |
13 | Hourcade et al. 2010 [50] | To investigate if female tract is able to select nonaffected sperm cells. | Mouse | Heat stress and Gamma radiation to animals. | - DNA damage: Comet assay | The extent of DNA damage in sperm obtained from female tract was higher following heat stress than after gamma radiation. | Super-ovulated | IVF and ICSI | - Heat stress reduced fertilization rates in both IVF and ICSI - Gamma radiation decreased blastocyst rates in gamma radiation in both IVF and ICSI | - Sperm DNA fragmentation affects IVF and ICSI. - ICSI should be performed with highly motile sperm. |
14 | Izquierdo-Vega et al. 2008 [51] | To evaluate the effects of fluoride on in vitro sperm fertilizing ability. | Rat | Rats administered with 5 mg fluoride/kg/body mass/24 h for eight weeks | - SOD activity - Intracellular superoxide anion levels - Lipid peroxidation | Fluoride increases oxidative stress, decreases the antioxidant activity of SOD, and increases lipid peroxidation. | Super-ovulated | IVF | - Lower ability to fertilize oocytes | Fluoride exposure causes a decrease in sperm fertilization capacity. |
15 | Jang et al. 2010 [52] | To examine the developmental rates of semen treated with and without melatonin in the presence of H2O2. | Pig | Treatment of semen with H2O2 with and without melatonin. | - Lipid peroxidation: Malondialdehyde levels | Exposure to H2O2 augmented lipid peroxidation, but this increase was mitigated by melatonin. | IVM | IVF | - Fertilization was not impaired by exposure of sperm to H2O2 - Exposing sperm to H2O2 arrested the development to blastocyst, but melatonin prevented that negative effect. | Supplementation with melatonin could improve sperm quality, increasing the developmental capacity of porcine embryos. |
16 | Li et al. 2009 [53] | To evaluate whether normal offspring can be generated after exposing sperm to high NaOH concentrations. | Mouse | High alkaline treatment of sperm cells | - DNA damage: Acridine Orange | Increase of DNA damage. | Super-ovulated | ICSI | - Decrease of fertilization rates - Reduction of implantation and live pups born - Increase of chromosomal damage in embryos | Sperm treated with NaOH retain their ability to activate the oocyte, but embryo development is lower as NaOH concentration increases. |
17 | Li et al. 2020 [54] | To assess the extent to which the measurement of DNA fragmentation index in sperm can predict their fertilizing ability. | Mouse | Freeze-thawing | - DNA damage: TUNEL | Cryopreservation increased DNA damage. | Super-ovulated | IVF and ICSI | - Sperm DNA damage reduced fertilization rates following both IVF and ICSI. - Samples with higher DNA damage resulted in a reduction of viable offspring. | DNA fragmentation index is an accurate parameter to determine sperm quality and fertility potential. |
18 | Llamas Luceño et al. 2020 [55] | To address the impact of natural heat stress on bull fertility. | Cattle | Comparison of different bulls exposed to separate levels of heat stress | - ROS production - Lipid peroxidation - DNA fragmentation: TUNEL | No differences in H2O2 production, lipid peroxidation and DNA damage. A tendency to significance in total ROS production was observed. | IVM | IVF | - No impact of exposing sperm to heat stress upon cleavage rates - A reduction of day 7 and 8 blastocyst rate and a delay of blastocyst hatching were observed. | Sperm fertilizing ability decreases due to male exposure to heat stress. |
19 | Makvan-di et al. 2019 [56] | To show the potential benefits of alpha lipoic acid as antioxidant in lipopolysaccharide- treated sperm cells. | Mouse | Sperm cells were incubated with lipopolysaccharide and alpha lipoic acid at different concentrations | - ROS production: DCFH-DA test - DNA damage: Acridine orange | Lipopolysaccharide augmented ROS and DNA damage, but the addition of alpha lipoic acid mitigated those increases. | Super-ovulated | IVF | While lipopolysaccharide led to lower fertilization, cleavage, compaction and blastocyst rates, this effect was reverted by alpha lipoic acid. | Alpha lipoic acid is a strong antioxidant and protective sperm factor. |
20 | Matini Behzad et al. 2014 [57] | To evaluate the effects of fish oil feeding on sperm parameters and its incidence in IVF. | Sheep | Fish oil diet for 70 days | Intracellular ROS | Superoxide anion was lower in the treated than in the control group. | IVM | IVF | - Cleavage rates were higher in the treated group. | Addition of fish oil to ram diet improves sperm quality and in vitro fertilization ability. |
21 | Mehraban et al. 2019 [58] | To evaluate the antioxidant effects of Gallic Acid on apoptotic-like changes in sperm. | Mouse | Cyclophosphamide and gallic acid | Apoptotic-like changes: Annexin V staining | Cyclophosphamide induces apoptotic-like changes compared to controls. Gallic Acid mitigates that increase. | Super-ovulated | IVF | - Cyclophosphamide reduces fertilization rates and proportions of cleaved embryos. | Gallic Acid suppresses ROS induced by Cyclophosphamide and help rescue fertility. |
22 | Paul et al. 2008 [59] | To explore the link between heat stress, DNA damage and the impact on cell function. | Mouse | Acute testicular heat stress at different temperatures | - Sperm DNA damage: SCSA - Spermatocyte DNA damage | Increase of DNA damage in spermatocytes and spermatozoa when heat stress was 40 °C/42 °C. | Super-ovulated | IVF | - Fertilization was similar between groups. - Development to 2-4 cells was similar to controls. - Development to blastocyst was severely reduced. | Spermatogenesis is impaired when scrotal temperatures increase, showing that exposing male to high temperatures reduces embryo development and pregnancy of the oocytes fertilized with those sperm. |
23 | Perez-Crespo et al. 2008 [60] | To evaluate whether factors released from membrane-damaged spermatozoa have a role in DNA damage and ICSI outcomes. | Mouse | Incubation of sperm in media containing factors released by damaged sperm | - DNA damage: TUNEL | Increase of sperm DNA damage. | Super-ovulated | ICSI | - Cleavage and blastocyst rates were not impaired by treatment - Implantation was reduced, regardless of whether embryos were transferred at 2-cell stage or at blastocyst stage. | Factors released from membrane-damaged sperm are capable of inducing DNA fragmentation in viable spermatozoa, and decrease implantation rates. |
24 | Sanchez-Gutierrez et al. 2008 [61] | To evaluate the effect of selenium deficiency on in vitro fertilizing ability. | Mouse | Selenium deficient diet for 4 months | - Glutathione peroxidase activity - Lipid peroxidation | Glutathione peroxidase activity was reduced and lipid peroxidation was increased in selenium free diet. | Super-ovulated | IVF | - Fertilization rates were reduced | Selenium deficiency leads to a reduction of sperm quality and fertilizing ability. |
25 | Silva et al. 2007 [62] | To describe the effects of exposing bull sperm to mild and intense ROS generation conditions. | Cattle | Sperm were incubated with pro-oxidant molecules | - Sperm DNA oxidation - Lipid peroxidation - Cytosol and mitochondrial oxidation | Increased intracellular and mitochondrial ROS, while no significant increase of DNA oxidation was observed. | IVM | IVF | - Reduced cleavage rates and blastocyst rates when high oxidation was applied. | Oxidative stress can result in damaged sperm cell structures, affecting embryo development. |
26 | Simoes et al. 2013 [63] | To evaluate the influence of sperm oxidative stress susceptibility on DNA fragmentation and IVF outcomes. | Cattle | Division in four groups according to oxidative stress susceptibility | - DNA damage: Comet assay, Acridine Orange and TUNEL | Sperm DNA was compromised in response to increased oxidative stress susceptibility. | IVM | IVF | - Embryo cleavage decreased as oxidative stress increased - No significant differences in blastocyst rates or number of blastocysts were observed | Increased sperm oxidative stress leads to a reduction of embryo quality. |
27 | Yamauchi et al. 2007 [37] | To test if embryo DNA synthesis is related to paternal DNA degradation in zygotes, which is induced by sperm DNA damage. | Mouse | Sperm DNA damage induction through manganese and calcium incubations | - DNA damage: Pulsed Field Gel Electrohporesis (PFGE) | Treatment caused DNA damage detected through PFGE. | Super-ovulated | ICSI | - Fertilization with vas deferens damaged sperm led to DNA degradation in paternal pronucleous. - Intiation of male and female pronucleus DNA replication was delayed. - Blastocyst development was arrested | Impairment of DNA synthesis in the embryo is related to DNA damage in sperm. |
28 | Yamauchi et al. 2007 [64] | To test embryo development from sperm cells to which DNA damage was induced. | Mouse | DNA damage induction through manganese and calcium incubations | - DNA damage: Pulsed Field Gel Electrohporesis | Treatment caused DNA damage detected through PFGE. | Super-ovulated | ICSI | - DNA damage caused a reduction in the percentage of embryos reaching two-cell stage - Development to blastocyst was impaired when sperm DNA was damaged | Embryo development is impaired when the fertilizing sperm presents chromatin fragmentation. |
29 | Yi et al. 2016 [65] | To examine the effects of Davallialactone (DAVA) on in vitro sperm fertilizing ability. | Pig | Spermatozoa were incubated with DAVA | - ROS production: intracellular H2O2 | DAVA reduced intracellular H2O2 in sperm cells. | IVM | IVF | - Fertilization was enhanced by DAVA | Addition of DAVA to fertilization medium reduces ROS and increases fertilization rates |
30 | Yi et al. 2017 [66] | To determine the impact of difructose dianhydride IV (DFA-IV) on in vitro sperm fertilizing ability. | Pig | Spermatozoa were incubated in DFA-IV at different concentrations for two hours | - Total oxidative stress. | Total intracellular ROS levels were decreased in samples incubated with DFA-IV. | IVM | IVF | - Higher fertilization rates - Higher cleavage and blastocyst rates | Addition of DFA-IV to sperm increases fertilization and blastocyst rates. |
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Ribas-Maynou, J.; Yeste, M.; Salas-Huetos, A. The Relationship between Sperm Oxidative Stress Alterations and IVF/ICSI Outcomes: A Systematic Review from Nonhuman Mammals. Biology 2020, 9, 178. https://doi.org/10.3390/biology9070178
Ribas-Maynou J, Yeste M, Salas-Huetos A. The Relationship between Sperm Oxidative Stress Alterations and IVF/ICSI Outcomes: A Systematic Review from Nonhuman Mammals. Biology. 2020; 9(7):178. https://doi.org/10.3390/biology9070178
Chicago/Turabian StyleRibas-Maynou, Jordi, Marc Yeste, and Albert Salas-Huetos. 2020. "The Relationship between Sperm Oxidative Stress Alterations and IVF/ICSI Outcomes: A Systematic Review from Nonhuman Mammals" Biology 9, no. 7: 178. https://doi.org/10.3390/biology9070178