{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T13:25:46Z","timestamp":1787318746154,"version":"build-2736575974"},"reference-count":107,"publisher":"IMR Press","issue":"12","license":[{"start":{"date-parts":[[2024,12,17]],"date-time":"2024-12-17T00:00:00Z","timestamp":1734393600000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Front. Biosci. (Landmark Ed)"],"abstract":"<jats:p>The prevalence of sperm DNA fragmentation (SDF) is significantly higher in males with infertility, which is often associated with oligozoospermia and hypospermia. It can also occur in patients with infertility who have normal conventional semen indicators. The etiologies involve aberrations in sperm maturation, dysregulated apoptotic processes, and heightened levels of oxidative stress. In this article, we retrieved PubMed, China National Knowledge Infrastructure (CNKI) and Web of Science databases for articles and reviews published before February 28, 2024. Using \u201csperm DNA fragments; assisted reproductive technology, mechanism, clinical pregnancy outcome\u201d as keywords, and comprehensively reviewed on their basis. Numerous literature sources have reported an increased utilization of SDF testing in the context of male infertility, as there is a negative correlation between SDF levels and the success of natural conception as well as assisted reproductive technologies. To enhance the clinical outcome for individuals experiencing infertility, investigating the prevalence and underlying mechanisms of sperm DNA damage is beneficial. This review article delves into the mechanisms that lead to sperm DNA damage and assesses the impact of DNA fragmentation index (DFI) on pregnancy outcomes in the context of assisted reproductive technologies.<\/jats:p>","DOI":"10.31083\/j.fbl2912416","type":"journal-article","created":{"date-parts":[[2024,12,30]],"date-time":"2024-12-30T11:37:01Z","timestamp":1735558621000},"source":"Crossref","is-referenced-by-count":4,"title":["The Mechanism and Clinical Significance of Sperm DNA Damage in Assisted Reproductive"],"prefix":"10.31083","volume":"29","author":[{"given":"Kangsheng","family":"Liu","sequence":"first","affiliation":[{"name":"Department of Obstetrics and Gynecology, the First Affiliated Hospital of Xi'an Jiaotong University, 710061 Xi'an, Shaanxi, China"},{"name":"Department of Clinical Laboratory, Women's Hospital of Nanjing Medical University, Nanjing Women and Children's Health Care Hospital, 210029 Nanjing, Jiangsu, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yajun","family":"Chen","sequence":"first","affiliation":[{"name":"Department of Clinical Laboratory, Women's Hospital of Nanjing Medical University, Nanjing Women and Children's Health Care Hospital, 210029 Nanjing, Jiangsu, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruifang","family":"An","sequence":"first","affiliation":[{"name":"Department of Obstetrics and Gynecology, the First Affiliated Hospital of Xi'an Jiaotong University, 710061 Xi'an, Shaanxi, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"16242","published-online":{"date-parts":[[2024,12,17]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","unstructured":"Heidary Z, Zaki-Dizaji M, Saliminejad K, Khorram Khorshid HR. MicroRNA profiling in spermatozoa of men with unexplained asthenozoospermia. Andrologia. 2019; 51: e13284.","DOI":"10.1111\/and.13284"},{"key":"ref2","doi-asserted-by":"crossref","unstructured":"Agarwal A, Allamaneni SSR. Sperm DNA damage assessment: a test whose time has come. Fertility and Sterility. 2005; 84: 850\u2013853.","DOI":"10.1016\/j.fertnstert.2005.03.080"},{"key":"ref3","doi-asserted-by":"crossref","unstructured":"Li F, Duan X, Li M, Ma X. Sperm DNA fragmentation index affect pregnancy outcomes and offspring safety in assisted reproductive technology. Scientific Reports. 2024; 14: 356.","DOI":"10.1038\/s41598-023-45091-6"},{"key":"ref4","unstructured":"Yang J. Effect and Mechanism of Sperm DNA Damage on Embryonic Development Potential. [master\u2019s thesis] Zhengzhou University. 2020."},{"key":"ref5","doi-asserted-by":"crossref","unstructured":"Yifu P, Lei Y, Shaoming L, Yujin G, Xingwang Z. Sperm DNA fragmentation index with unexplained recurrent spontaneous abortion: A systematic review and meta-analysis. Journal of Gynecology Obstetrics and Human Reproduction. 2020; 101740.","DOI":"10.1016\/j.jogoh.2020.101740"},{"key":"ref6","doi-asserted-by":"crossref","unstructured":"Du C, Tuo Y. Correlation of DNA fragments with routine semen parameters and lifestyle and their impact on assisted reproductive outcomes. Revista Internacional De Andrologia. 2023; 21: 100337.","DOI":"10.1016\/j.androl.2022.03.001"},{"key":"ref7","doi-asserted-by":"crossref","unstructured":"Farkouh A, Salvio G, Kuroda S, Saleh R, Vogiatzi P, Agarwal A. Sperm DNA integrity and male infertility: a narrative review and guide for the reproductive physicians. Translational Andrology and Urology. 2022; 11: 1023\u20131044.","DOI":"10.21037\/tau-22-149"},{"key":"ref8","doi-asserted-by":"crossref","unstructured":"Bibi R, Jahan S, Razak S, Hammadeh ME, Almajwal A, Amor H. Protamines and DNA integrity as a biomarkers of sperm quality and assisted conception outcome. Andrologia. 2022; 54: e14418.","DOI":"10.1111\/and.14418"},{"key":"ref9","doi-asserted-by":"crossref","unstructured":"Alahmar AT, Singh R, Palani A. Sperm DNA Fragmentation in Reproductive Medicine: A Review. Journal of Human Reproductive Sciences. 2022; 15: 206\u2013218.","DOI":"10.4103\/jhrs.jhrs_82_22"},{"key":"ref10","doi-asserted-by":"crossref","unstructured":"Agarwal A, Majzoub A, Baskaran S, Panner Selvam MK, Cho CL, Henkel R, et al. Sperm DNA Fragmentation: A New Guideline for Clinicians. The World Journal of Men\u2019s Health. 2020; 38: 412\u2013471.","DOI":"10.5534\/wjmh.200128"},{"key":"ref11","unstructured":"Chen RL, Zhang YS. Mechanisms and Clinical Relevance of Sperm DNA Damage. Journal of International Reproductive Health\/Family Planning. 2023; 42: 130\u2013134."},{"key":"ref12","doi-asserted-by":"crossref","unstructured":"Zhu Y, Gao G, Xia L, Li X, Wu X, Her C, et al. The polymorphic hMSH5 C85T allele augments radiotherapy-induced spermatogenic impairment. Andrology. 2016; 4: 873\u2013879.","DOI":"10.1111\/andr.12203"},{"key":"ref13","doi-asserted-by":"crossref","unstructured":"Gunes S, Al-Sadaan M, Agarwal A. Spermatogenesis, DNA damage and DNA repair mechanisms in male infertility. Reproductive Biomedicine Online. 2015; 31: 309\u2013319.","DOI":"10.1016\/j.rbmo.2015.06.010"},{"key":"ref14","doi-asserted-by":"crossref","unstructured":"Santi D, De Vincentis S, Magnani E, Spaggiari G. Impairment of sperm DNA methylation in male infertility: a meta-analytic study. Andrology. 2017; 5: 695-703.","DOI":"10.1111\/andr.12379"},{"key":"ref15","doi-asserted-by":"crossref","unstructured":"Zhu CH, Wei Y, Chen F, Li F, Zhang SM, Dong NJ, et al. Investigation on the mechanisms of human sperm DNA damage based on the proteomics analysis by SWATH-MS. Clinical Proteomics. 2023; 20: 2.","DOI":"10.1186\/s12014-022-09391-9"},{"key":"ref16","doi-asserted-by":"crossref","unstructured":"Fraczek M, Lewandowska A, Budzinska M, Kamieniczna M, Wojnar L, Gill K, et al. The Role of Seminal Oxidative Stress Scavenging System in the Pathogenesis of Sperm DNA Damage in Men Exposed and Not Exposed to Genital Heat Stress. International Journal of Environmental Research and Public Health. 2022; 19: 2713.","DOI":"10.3390\/ijerph19052713"},{"key":"ref17","doi-asserted-by":"crossref","unstructured":"Sharma R, Harlev A, Agarwal A, Esteves SC. Cigarette Smoking and Semen Quality: A New Meta-analysis Examining the Effect of the 2010 World Health Organization Laboratory Methods for the Examination of Human Semen. European Urology. 2016; 70: 635\u2013645.","DOI":"10.1016\/j.eururo.2016.04.010"},{"key":"ref18","doi-asserted-by":"crossref","unstructured":"Catal\u00e1n J, Y\u00e1nez-Ortiz I, Torres-Garrido M, Ribas-Maynou J, Llavanera M, Barranco I, et al. Impact of Seminal Plasma Antioxidants on DNA Fragmentation and Lipid Peroxidation of Frozen-Thawed Horse Sperm. Antioxidants (Basel, Switzerland). 2024; 13: 322.","DOI":"10.3390\/antiox13030322"},{"key":"ref19","doi-asserted-by":"crossref","unstructured":"Martin-Hidalgo D, Bragado MJ, Batista AR, Oliveira PF, Alves MG. Antioxidants and Male Fertility: from Molecular Studies to Clinical Evidence. Antioxidants (Basel, Switzerland). 2019; 8: 89.","DOI":"10.3390\/antiox8040089"},{"key":"ref20","doi-asserted-by":"crossref","unstructured":"Li J, Barranco I, Tvarijonaviciute A, Molina MF, Martinez EA, Rodriguez-Martinez H, et al. Seminal plasma antioxidants are directly involved in boar sperm cryotolerance. Theriogenology. 2018; 107: 27\u201335.","DOI":"10.1016\/j.theriogenology.2017.10.035"},{"key":"ref21","doi-asserted-by":"crossref","unstructured":"Murat F, Mbengue N, Winge SB, Trefzer T, Leushkin E, Sepp M, et al. The molecular evolution of spermatogenesis across mammals. Nature. 2023; 613: 308\u2013316.","DOI":"10.1038\/s41586-022-05547-7"},{"key":"ref22","doi-asserted-by":"crossref","unstructured":"Zakariah M, Molele RA, Mahdy MAA, Ibrahim MIA, McGaw LJ. Regulation of spermatogenic cell apoptosis by the pro-apoptotic proteins in the testicular tissues of mammalian and avian species. Animal Reproduction Science. 2022; 247: 107158.","DOI":"10.1016\/j.anireprosci.2022.107158"},{"key":"ref23","unstructured":"Chen R, Yu S, Chen XX, Du J, Zhu ZD, Pan CY, et al. Regulatory Role of Noncoding RNAs During Spermatogenesis. Scientia Acricultura Sinica. 2017; 50: 380\u2013390."},{"key":"ref24","doi-asserted-by":"crossref","unstructured":"Guo H, Chen L, Cui H, Peng X, Fang J, Zuo Z, et al. Research Advances on Pathways of Nickel-Induced Apoptosis. International Journal of Molecular Sciences. 2015; 17: 10.","DOI":"10.3390\/ijms17010010"},{"key":"ref25","doi-asserted-by":"crossref","unstructured":"Meyer-Ficca ML, Lonchar J, Credidio C, Ihara M, Li Y, Wang ZQ, et al. Disruption of poly(ADP-ribose) homeostasis affects spermiogenesis and sperm chromatin integrity in mice. Biology of Reproduction. 2009; 81: 46\u201355.","DOI":"10.1095\/biolreprod.108.075390"},{"key":"ref26","doi-asserted-by":"crossref","unstructured":"Stobezki R, Titus S, Halicka D, Darzynkiewicz Z, Oktay K. Declining BRCA-Mediated DNA Repair in Sperm Aging and its Prevention by Sphingosine-1-Phosphate. Reproductive Sciences (Thousand Oaks, Calif.). 2020; 27: 940\u2013953.","DOI":"10.1007\/s43032-019-00098-1"},{"key":"ref27","doi-asserted-by":"crossref","unstructured":"Bibi R, Jahan S, Kafeel Qureshi S, Razak S, Afsar T, Almajwal A, et al. Analysis of sperm chromatin packaging and reproductive biomarker to evaluate the consequence of advanced male age. Frontiers in Endocrinology. 2023; 14: 1092603.","DOI":"10.3389\/fendo.2023.1092603"},{"key":"ref28","doi-asserted-by":"crossref","unstructured":"Horta F, Catt S, Ramachandran P, Vollenhoven B, Temple-Smith P. Female ageing affects the DNA repair capacity of oocytes in IVF using a controlled model of sperm DNA damage in mice. Human Reproduction (Oxford, England). 2020; 35: 529\u2013544.","DOI":"10.1093\/humrep\/dez308"},{"key":"ref29","doi-asserted-by":"crossref","unstructured":"Salehi M, Afarinesh MR, Haghpanah T, Ghaffari Novin M, Farifteh F. Impact of sperm DNA fragmentation on ICSI outcome and incidence of apoptosis of human pre-implantation embryos obtained from in vitro matured MII oocytes. Biochemical and Biophysical Research Communications. 2019; 510: 110\u2013115.","DOI":"10.1016\/j.bbrc.2019.01.056"},{"key":"ref30","doi-asserted-by":"crossref","unstructured":"Panner Selvam MK, Ambar RF, Agarwal A, Henkel R. Etiologies of sperm DNA damage and its impact on male infertility. Andrologia. 2021; 53: e13706.","DOI":"10.1111\/and.13706"},{"key":"ref31","doi-asserted-by":"crossref","unstructured":"Omar SS, Mahfouz W, Dawood W, Abo El-Wafa RAH, Ghazala RA, Zahran ARM. Relation of nitric oxide synthase gene (NOS3) polymorphisms to varicocele risk and post-varicocelectomy seminal oxidative stress reduction. Andrologia. 2020; 52: e13525.","DOI":"10.1111\/and.13525"},{"key":"ref32","doi-asserted-by":"crossref","unstructured":"Esteves SC, Agarwal A. Afterword to varicocele and male infertility: current concepts and future perspectives. Asian Journal of Andrology. 2016; 18: 319\u2013322.","DOI":"10.4103\/1008-682X.172820"},{"key":"ref33","doi-asserted-by":"crossref","unstructured":"Esteves SC, Gos\u00e1lvez J, L\u00f3pez-Fern\u00e1ndez C, N\u00fa\u00f1ez-Calonge R, Caballero P, Agarwal A, et al. Diagnostic accuracy of sperm DNA degradation index (DDSi) as a potential noninvasive biomarker to identify men with varicocele-associated infertility. International Urology and Nephrology. 2015; 47: 1471\u20131477.","DOI":"10.1007\/s11255-015-1053-6"},{"key":"ref34","doi-asserted-by":"crossref","unstructured":"Berg E, Houska P, Nesheim N, Schuppe HC, Pilatz A, Fijak M, et al. Chronic Prostatitis\/Chronic Pelvic Pain Syndrome Leads to Impaired Semen Parameters, Increased Sperm DNA Fragmentation and Unfavorable Changes of Sperm Protamine mRNA Ratio. International Journal of Molecular Sciences. 2021; 22: 7854.","DOI":"10.3390\/ijms22157854"},{"key":"ref35","doi-asserted-by":"crossref","unstructured":"Hologlu D, Gunes S, Asci R, Henkel R, Guvenc T. Association among sperm chromatin condensation, sperm DNA fragmentation and 8-OHdG in seminal plasma and semen parameters in infertile men with oligoasthenoteratozoospermia. Andrologia. 2022; 54: e14268.","DOI":"10.1111\/and.14268"},{"key":"ref36","doi-asserted-by":"crossref","unstructured":"Majzoub A, Arafa M, Mahdi M, Agarwal A, Al Said S, Al-Emadi I, et al. Oxidation-reduction potential and sperm DNA fragmentation, and their associations with sperm morphological anomalies amongst fertile and infertile men. Arab Journal of Urology. 2018; 16: 87\u201395.","DOI":"10.1016\/j.aju.2017.11.014"},{"key":"ref37","doi-asserted-by":"crossref","unstructured":"Tanaka T, Kobori Y, Terai K, Inoue Y, Osaka A, Yoshikawa N, et al. Seminal oxidation-reduction potential and sperm DNA fragmentation index increase among infertile men with varicocele. Human Fertility (Cambridge, England). 2022; 25: 142\u2013146.","DOI":"10.1080\/14647273.2020.1712747"},{"key":"ref38","doi-asserted-by":"crossref","unstructured":"Rubes J, Sipek J, Kopecka V, Musilova P, Vozdova M, Prinosilova P, et al. The effects of age on DNA fragmentation, the condensation of chromatin and conventional semen parameters in healthy nonsmoking men exposed to traffic air pollution. Health Science Reports. 2021; 4: e260.","DOI":"10.1002\/hsr2.260"},{"key":"ref39","doi-asserted-by":"crossref","unstructured":"Gao J, Yuan R, Yang S, Wang Y, Huang Y, Yan L, et al. Age-related changes in human conventional semen parameters and sperm chromatin structure assay-defined sperm DNA\/chromatin integrity. Reproductive Biomedicine Online. 2021; 42: 973\u2013982.","DOI":"10.1016\/j.rbmo.2021.02.006"},{"key":"ref40","unstructured":"Li ML, Zhou Q, Ge YF, Shao Y, Zeng R, Yao B. Effects of sperm DNA fragmentation index on semen parameters and pregnancy outcomes in intrauterine insemination. Zhonghua Nan Ke Xue. 2021; 27: 904\u2013908. (In Chinese)"},{"key":"ref41","doi-asserted-by":"crossref","unstructured":"Lu R, Chen X, Yu W, Jiang F, Zhou X, Xu Y, et al. Analysis of age-associated alternation of SCSA sperm DNA fragmentation index and semen characteristics of 1790 subfertile males in China. Journal of Clinical Laboratory Analysis. 2020; 34: e23548.","DOI":"10.1002\/jcla.23548"},{"key":"ref42","doi-asserted-by":"crossref","unstructured":"Halvaei I, Litzky J, Esfandiari N. Advanced paternal age: effects on sperm parameters, assisted reproduction outcomes and offspring health. Reproductive Biology and Endocrinology. 2020; 18: 110.","DOI":"10.1186\/s12958-020-00668-y"},{"key":"ref43","doi-asserted-by":"crossref","unstructured":"Vaughan DA, Tirado E, Garcia D, Datta V, Sakkas D. DNA fragmentation of sperm: a radical examination of the contribution of oxidative stress and age in 16 945 semen samples. Human Reproduction (Oxford, England). 2020; 35: 2188\u20132196.","DOI":"10.1093\/humrep\/deaa159"},{"key":"ref44","doi-asserted-by":"crossref","unstructured":"Comar VA, Petersen CG, Mauri AL, Mattila M, Vagnini LD, Renzi A, et al. Influence of the abstinence period on human sperm quality: analysis of 2,458 semen samples. JBRA Assisted Reproduction. 2017; 21: 306\u2013312.","DOI":"10.5935\/1518-0557.20170052"},{"key":"ref45","doi-asserted-by":"crossref","unstructured":"Haidl F, Haidl G, Oltermann I, Allam JP. Seminal parameters of chronic male genital inflammation are associated with disturbed sperm DNA integrity. Andrologia. 2015; 47: 464\u2013469.","DOI":"10.1111\/and.12408"},{"key":"ref46","doi-asserted-by":"crossref","unstructured":"Oghbaei H, Rastgar Rezaei Y, Nikanfar S, Zarezadeh R, Sadegi M, Latifi Z, et al. Effects of bacteria on male fertility: Spermatogenesis and sperm function. Life Sciences. 2020; 256: 117891.","DOI":"10.1016\/j.lfs.2020.117891"},{"key":"ref47","doi-asserted-by":"crossref","unstructured":"Pratap H, Hottigoudar SY, Nichanahalli KS, Rajendran S, Bheemanathi HS. Sperm DNA Integrity in Leukocytospermia and Its Association with Seminal Adenosine Deaminase. Journal of Human Reproductive Sciences. 2019; 12: 182\u2013188.","DOI":"10.4103\/jhrs.JHRS_1_19"},{"key":"ref48","doi-asserted-by":"crossref","unstructured":"Lundy SD, Vij SC, Rezk AH, Cohen JA, Bajic P, Ramasamy R. The microbiome of the infertile male. Current Opinion in Urology. 2020; 30: 355\u2013362.","DOI":"10.1097\/MOU.0000000000000742"},{"key":"ref49","unstructured":"Ling YH. Correlation of ureaplasma urealyticum and chlamydia trachomatis infection in reproductive tract with oligopermia or asthenospermia, chronic salpingitis and adverse pregnancy [master\u2019s thesis]. Wannan Medical College. 2016."},{"key":"ref50","doi-asserted-by":"crossref","unstructured":"Fraczek M, Wiland E, Piasecka M, Boksa M, Gaczarzewicz D, Szumala-Kakol A, et al. Fertilizing potential of ejaculated human spermatozoa during in\u2002vitro semen bacterial infection. Fertility and Sterility. 2014; 102: 711\u2013719.e1.","DOI":"10.1016\/j.fertnstert.2014.06.002"},{"key":"ref51","doi-asserted-by":"crossref","unstructured":"Zeyad A, Hamad MF, Hammadeh ME. The effects of bacterial infection on human sperm nuclear protamine P1\/P2 ratio and DNA integrity. Andrologia. 2018; 50.","DOI":"10.1111\/and.12841"},{"key":"ref52","doi-asserted-by":"crossref","unstructured":"Farahani L, Tharakan T, Yap T, Ramsay JW, Jayasena CN, Minhas S. The semen microbiome and its impact on sperm function and male fertility: A systematic review and meta-analysis. Andrology. 2021; 9: 115\u2013144.","DOI":"10.1111\/andr.12886"},{"key":"ref53","doi-asserted-by":"crossref","unstructured":"Dabizzi S, Maggi M, Torcia MG. Update on known and emergent viruses affecting human male genital tract and fertility. Basic Clin Androl. 2024; 34: 6.","DOI":"10.1186\/s12610-024-00222-5"},{"key":"ref54","doi-asserted-by":"crossref","unstructured":"Guiton R, Drevet JR. Viruses, bacteria and parasites: infection of the male genital tract and fertility. Basic and Clinical Andrology. 2023; 33: 19.","DOI":"10.1186\/s12610-023-00193-z"},{"key":"ref55","doi-asserted-by":"crossref","unstructured":"Tangal S, Ta\u015f\u00e7\u0131 Y, Pabu\u00e7cu EG, \u00c7a\u011flar GS, Halilo\u011flu AH, Yararba\u015f K. DNA fragmentation index and human papilloma virus in males with previous assisted reproductive technology failures. Turkish Journal of Urology. 2018; 45: 12\u201316.","DOI":"10.5152\/tud.2018.96393"},{"key":"ref56","unstructured":"Deng TQ, Huang YH, Zhen JY, Lu JT, Li YC, Tan XY, et al. Sperm DNA integrity of infertile males with hepatitis B virus infection. National Journal of Andrology. 2013; 19: 72\u201376."},{"key":"ref57","doi-asserted-by":"crossref","unstructured":"Muciaccia B, Corallini S, Vicini E, Padula F, Gandini L, Liuzzi G, et al. HIV-1 viral DNA is present in ejaculated abnormal spermatozoa of seropositive subjects. Human Reproduction (Oxford, England). 2007; 22: 2868\u20132878.","DOI":"10.1093\/humrep\/dem288"},{"key":"ref58","unstructured":"Jing J, Miao Y, Shaoguo R. Research progress on the mechanisms of sperm damage caused by environmental pollutants. Asian Journal of Ecotoxicology. 2019; 14: 11\u201322."},{"key":"ref59","doi-asserted-by":"crossref","unstructured":"Kwack SJ, Lee BM. Comparative Cytotoxicity and Sperm Motility Using a Computer-Aided Sperm Analysis System (CASA) for Isomers of Phthalic Acid, a Common Final Metabolite of Phthalates. Journal of Toxicology and Environmental Health. Part a. 2015; 78: 1038\u20131050.","DOI":"10.1080\/15287394.2015.1067503"},{"key":"ref60","doi-asserted-by":"crossref","unstructured":"Wong EWP, Cheng CY. Impacts of environmental toxicants on male reproductive dysfunction. Trends in Pharmacological Sciences. 2011; 32: 290\u2013299.","DOI":"10.1016\/j.tips.2011.01.001"},{"key":"ref61","doi-asserted-by":"crossref","unstructured":"Ranganathan P, Rao KA, Thalaivarasai Balasundaram S. Deterioration of semen quality and sperm-DNA integrity as influenced by cigarette smoking in fertile and infertile human male smokers-A prospective study. Journal of Cellular Biochemistry. 2019; 120: 11784\u201311793.","DOI":"10.1002\/jcb.28458"},{"key":"ref62","doi-asserted-by":"crossref","unstructured":"Corona G, Sansone A, Pallotti F, Ferlin A, Pivonello R, Isidori AM, et al. People smoke for nicotine, but lose sexual and reproductive health for tar: a narrative review on the effect of cigarette smoking on male sexuality and reproduction. Journal of Endocrinological Investigation. 2020; 43: 1391\u20131408.","DOI":"10.1007\/s40618-020-01257-x"},{"key":"ref63","doi-asserted-by":"crossref","unstructured":"Cui X, Jing X, Wu X, Wang Z, Li Q. Potential effect of smoking on semen quality through DNA damage and the downregulation of Chk1 in sperm. Molecular Medicine Reports. 2016; 14: 753\u2013761.","DOI":"10.3892\/mmr.2016.5318"},{"key":"ref64","doi-asserted-by":"crossref","unstructured":"Monteiro BS, Freire-Brito L, Carrageta DF, Oliveira PF, Alves MG. Mitochondrial Uncoupling Proteins (UCPs) as Key Modulators of ROS Homeostasis: A Crosstalk between Diabesity and Male Infertility? Antioxidants (Basel, Switzerland). 2021; 10: 1746.","DOI":"10.3390\/antiox10111746"},{"key":"ref65","doi-asserted-by":"crossref","unstructured":"Sharma V, Collins LB, Chen TH, Herr N, Takeda S, Sun W, et al. Oxidative stress at low levels can induce clustered DNA lesions leading to NHEJ mediated mutations. Oncotarget. 2016; 7: 25377\u201325390.","DOI":"10.18632\/oncotarget.8298"},{"key":"ref66","doi-asserted-by":"crossref","unstructured":"Morris ID. Sperm DNA damage and cancer treatment. International Journal of Andrology. 2002; 25: 255\u2013261.","DOI":"10.1046\/j.1365-2605.2002.00372.x"},{"key":"ref67","doi-asserted-by":"crossref","unstructured":"Stukenborg JB, Wyns C. Fertility sparing strategies for pre- and peripubertal male cancer patients. Ecancermedicalscience. 2020; 14: 1016.","DOI":"10.3332\/ecancer.2020.1016"},{"key":"ref68","doi-asserted-by":"crossref","unstructured":"Martinez M, Majzoub A. Best laboratory practices and therapeutic interventions to reduce sperm DNA damage. Andrologia. 2021; 53: e13736.","DOI":"10.1111\/and.13736"},{"key":"ref69","doi-asserted-by":"crossref","unstructured":"Liffner S, Pehrson I, Garc\u00eda-Calvo L, Nedstrand E, Zalavary S, Hammar M, et al. Diagnostics of DNA fragmentation in human spermatozoa: Are sperm chromatin structure analysis and sperm chromatin dispersion tests (SCD-HaloSpermG2\u00ae) comparable? Andrologia. 2019; 51: e13316.","DOI":"10.1111\/and.13316"},{"key":"ref70","doi-asserted-by":"crossref","unstructured":"Lusignan MF, Li X, Herrero B, Delbes G, Chan PTK. Effects of different cryopreservation methods on DNA integrity and sperm chromatin quality in men. Andrology. 2018; 6: 829\u2013835.","DOI":"10.1111\/andr.12529"},{"key":"ref71","doi-asserted-by":"crossref","unstructured":"Qiu Y, Yang H, Li C, Xu C. Progress in Research on Sperm DNA Fragmentation. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research. 2020; 26: e918746.","DOI":"10.12659\/MSM.918746"},{"key":"ref72","doi-asserted-by":"crossref","unstructured":"Santi D, Spaggiari G, Simoni M. Sperm DNA fragmentation index as a promising predictive tool for male infertility diagnosis and treatment management - meta-analyses. Reproductive Biomedicine Online. 2018; 37: 315\u2013326.","DOI":"10.1016\/j.rbmo.2018.06.023"},{"key":"ref73","doi-asserted-by":"crossref","unstructured":"Bungum M, Humaidan P, Spano M, Jepson K, Bungum L, Giwercman A. The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Human Reproduction (Oxford, England). 2004; 19: 1401\u20131408.","DOI":"10.1093\/humrep\/deh280"},{"key":"ref74","unstructured":"Ni WH, Ashok Agarwal, Sun YP, Sun HX, Deng CY, Liu P, et al. Clinical expert consensus on sperm DNA fragmentation detection. Journal of Reproductive Medicine. 2023; 32: 170\u2013180."},{"key":"ref75","doi-asserted-by":"crossref","unstructured":"Rex AS, Aagaard J, Fedder J. DNA fragmentation in spermatozoa: a historical review. Andrology. 2017; 5: 622\u2013630.","DOI":"10.1111\/andr.12381"},{"key":"ref76","doi-asserted-by":"crossref","unstructured":"Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Human Reproduction (Oxford, England). 2007; 22: 174\u2013179.","DOI":"10.1093\/humrep\/del326"},{"key":"ref77","doi-asserted-by":"crossref","unstructured":"Sugihara A, Van Avermaete F, Roelant E, Punjabi U, De Neubourg D. The role of sperm DNA fragmentation testing in predicting intra-uterine insemination outcome: A systematic review and meta-analysis. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2020; 244: 8\u201315.","DOI":"10.1016\/j.ejogrb.2019.10.005"},{"key":"ref78","unstructured":"Liu HH. Effects of Sperm DNA Integrity on Pregnancy Outcome for AIH. Medical Innovation of China. 2014; 11: 45\u201346."},{"key":"ref79","unstructured":"Yang HY, Li G, Song WY, Xu ZY, Su YC, Sun YP. Relationship of sperm DNA fragments index to semen routine parameters and lifestyle and its effect on the pregnancy outcome of artificial insemination. Chinese Journal of Reproduction and Contraception. 2020; 40: 19\u201323."},{"key":"ref80","unstructured":"Liang JY, Li ZT, Zhang J, Yan XH, Huan ZC, Wang LH, et al. Relation between sperm DNA integrity and induced sperm acrosome reaction with intrauterine insemination pregnancy rate. International Journal of Laboratory Medicine. 2015; 36: 1250\u20131252."},{"key":"ref81","doi-asserted-by":"crossref","unstructured":"Chen Y, Li W, Chen X. The Association of Sperm DNA Fragment and Assisted Reproductive Outcomes: A Meta-Analysis. Computational and Mathematical Methods in Medicine. 2022; 2022: 1126616.","DOI":"10.1155\/2022\/1126616"},{"key":"ref82","doi-asserted-by":"crossref","unstructured":"Cissen M, Wely MV, Scholten I, Mansell S, Bruin JPD, Mol BW, et al. Measuring Sperm DNA Fragmentation and Clinical Outcomes of Medically Assisted Reproduction: A Systematic Review and Meta-Analysis. PloS One. 2016; 11: e0165125.","DOI":"10.1371\/journal.pone.0165125"},{"key":"ref83","doi-asserted-by":"crossref","unstructured":"Dar S, Grover SA, Moskovtsev SI, Swanson S, Baratz A, Librach CL. In vitro fertilization-intracytoplasmic sperm injection outcome in patients with a markedly high DNA fragmentation index (>50%). Fertility and Sterility. 2013; 100: 75\u201380.","DOI":"10.1016\/j.fertnstert.2013.03.011"},{"key":"ref84","doi-asserted-by":"crossref","unstructured":"Boe-Hansen GB, Fedder J, Ersb\u00f8ll AK, Christensen P. The sperm chromatin structure assay as a diagnostic tool in the human fertility clinic. Human Reproduction (Oxford, England). 2006; 21: 1576\u20131582.","DOI":"10.1093\/humrep\/del019"},{"key":"ref85","unstructured":"Wang XB, Xu WM, Long W, Xu L. Association of sperm DNA integrity with semen parameters and clinical outcomes of assisted reproductive technology. Medical Journal of Wuhan University. 2015; 36: 944\u2013947. (In Chinese)"},{"key":"ref86","unstructured":"Zha XM, Zhu FX, Zhang JJ, Xu YH. Correlation analysis of sperm DFI, semen routine and sperm morphology and the effect of sperm DFI on IVF-ET\/ICSI outcome. Tianjin Medical Journal. 2021; 49: 45\u201349. (In Chinese)"},{"key":"ref87","doi-asserted-by":"crossref","unstructured":"Sun TC, Zhang Y, Li HT, Liu XM, Yi DX, Tian L, et al. Sperm DNA fragmentation index, as measured by sperm chromatin dispersion, might not predict assisted reproductive outcome. Taiwanese Journal of Obstetrics & Gynecology. 2018; 57: 493\u2013498.","DOI":"10.1016\/j.tjog.2018.06.003"},{"key":"ref88","doi-asserted-by":"crossref","unstructured":"Simon L, Zini A, Dyachenko A, Ciampi A, Carrell DT. A systematic review and meta-analysis to determine the effect of sperm DNA damage on in vitro fertilization and intracytoplasmic sperm injection outcome. Asian Journal of Andrology. 2017; 19: 80\u201390.","DOI":"10.4103\/1008-682X.182822"},{"key":"ref89","doi-asserted-by":"crossref","unstructured":"Deng C, Li T, Xie Y, Guo Y, Yang QY, Liang X, et al. Sperm DNA fragmentation index influences assisted reproductive technology outcome: A systematic review and meta-analysis combined with a retrospective cohort study. Andrologia. 2019; 51: e13263.","DOI":"10.1111\/and.13263"},{"key":"ref90","doi-asserted-by":"crossref","unstructured":"Ribas-Maynou J, Yeste M, Becerra-Tom\u00e1s N, Aston KI, James ER, Salas-Huetos A. Clinical implications of sperm DNA damage in IVF and ICSI: updated systematic review and meta-analysis. Biological Reviews of the Cambridge Philosophical Society. 2021; 96: 1284\u20131300.","DOI":"10.1111\/brv.12700"},{"key":"ref91","doi-asserted-by":"crossref","unstructured":"Oleszczuk K, Giwercman A, Bungum M. Sperm chromatin structure assay in prediction of in Vitrofertilization outcome. Andrology. 2016; 4: 290\u2013296.","DOI":"10.1111\/andr.12153"},{"key":"ref92","unstructured":"Yuan WN. Sperm DNA Damage and the Outcomes of Assisted Reproductive technolog. Journal of International Reproductive Health\/Family Planning. 2010; 29: 285\u2013287."},{"key":"ref93","doi-asserted-by":"crossref","unstructured":"Giwercman A, Lindstedt L, Larsson M, Bungum M, Spano M, Levine RJ, et al. Sperm chromatin structure assay as an independent predictor of fertility in vivo: a case-control study. International Journal of Andrology. 2010; 33: e221\u2013e227.","DOI":"10.1111\/j.1365-2605.2009.00995.x"},{"key":"ref94","doi-asserted-by":"crossref","unstructured":"Kamkar N, Ramezanali F, Sabbaghian M. The relationship between sperm DNA fragmentation, free radicals and antioxidant capacity with idiopathic repeated pregnancy loss. Reproductive Biology. 2018; 18: 330\u2013335.","DOI":"10.1016\/j.repbio.2018.11.002"},{"key":"ref95","doi-asserted-by":"crossref","unstructured":"Marchetti F, Essers J, Kanaar R, Wyrobek AJ. Disruption of maternal DNA repair increases sperm-derived chromosomal aberrations. National Academy of Sciences of the United States of America. 2007; 104: 17725\u20139.","DOI":"10.1073\/pnas.0705257104"},{"key":"ref96","doi-asserted-by":"crossref","unstructured":"Olszewska M, Barciszewska MZ, Fraczek M, Huleyuk N, Chernykh VB, Zastavna D, et al. Global methylation status of sperm DNA in carriers of chromosome structural aberrations. Asian Journal of Andrology. 2017; 19: 117\u2013124.","DOI":"10.4103\/1008-682X.168684"},{"key":"ref97","doi-asserted-by":"crossref","unstructured":"Chen Q, Zhao JY, Xue X, Zhu GX. The association between sperm DNA fragmentation and reproductive outcomes following intrauterine insemination, a meta analysis. Reproductive Toxicology (Elmsford, N.Y.). 2019; 86: 50\u201355.","DOI":"10.1016\/j.reprotox.2019.03.004"},{"key":"ref98","doi-asserted-by":"crossref","unstructured":"Wang S, Tan W, Huang Y, Mao X, Li Z, Zhang X, et al. Sperm DNA fragmentation measured by sperm chromatin dispersion impacts morphokinetic parameters, fertilization rate and blastocyst quality in ICSI treatments. Zygote (Cambridge, England). 2022; 30: 72\u201379.","DOI":"10.1017\/S0967199421000332"},{"key":"ref99","doi-asserted-by":"crossref","unstructured":"Chen L, Li D, Ni X, Zhu L, Zhang N, Fang J, et al. Effects of the normal sperm morphology rate on the clinical and neonatal outcomes of conventional IVF cycles. Andrologia. 2020; 52: e13568.","DOI":"10.1111\/and.13568"},{"key":"ref100","doi-asserted-by":"crossref","unstructured":"Zini A, Jamal W, Cowan L, Al-Hathal N. Is sperm DNA damage associated with IVF embryo quality? A systematic review. Journal of Assisted Reproduction and Genetics. 2011; 28: 391\u2013397.","DOI":"10.1007\/s10815-011-9544-6"},{"key":"ref101","doi-asserted-by":"crossref","unstructured":"Simon L, Emery B, Carrell DT. Sperm DNA Fragmentation: Consequences for Reproduction. Advances in Experimental Medicine and Biology. 2019; 1166: 87\u2013105.","DOI":"10.1007\/978-3-030-21664-1_6"},{"key":"ref102","doi-asserted-by":"crossref","unstructured":"Sakkas D, Alvarez JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertility and Sterility. 2010; 93: 1027\u20131036.","DOI":"10.1016\/j.fertnstert.2009.10.046"},{"key":"ref103","doi-asserted-by":"crossref","unstructured":"Yang H, Li G, Jin H, Guo Y, Sun Y. The effect of sperm DNA fragmentation index on assisted reproductive technology outcomes and its relationship with semen parameters and lifestyle. Translational Andrology and Urology. 2019; 8: 356\u2013365.","DOI":"10.21037\/tau.2019.06.22"},{"key":"ref104","unstructured":"Lin ZS. Clincal study on Effect of Guiyao Shengjing Capsule on Expression of DIF and Apoptosis Factors FAS and Fasl in Patients with Asthenospermia of Kidney Yang Deficiency Type [master\u2019s thesis]. Guangxi University of Chinese Medicine. 2020."},{"key":"ref105","unstructured":"Deng XY. Clinical Observation of Chaijuqiangjing decoction Combined with Lipoic Acid in Treating Sperm DNA Damage [master\u2019s thesis]. Guangxi University of Chinese Medicine. 2022."},{"key":"ref106","doi-asserted-by":"crossref","unstructured":"Alahmar AT, Singh R, Palani A. Sperm DNA Fragmentation in Reproductive Medicine: A Review. Journal of Human Reproductive Sciences. 2022; 15: 206\u2013218.","DOI":"10.4103\/jhrs.jhrs_82_22"},{"key":"ref107","doi-asserted-by":"crossref","unstructured":"Evgeni E, Sabbaghian M, Saleh R, G\u00fcl M, Vogiatzi P, Durairajanayagam D, et al. Sperm DNA fragmentation test: usefulness in assessing male fertility and assisted reproductive technology outcomes. Panminerva Medica. 2023; 65: 135\u2013147.","DOI":"10.23736\/S0031-0808.23.04836-X"}],"container-title":["Frontiers in Bioscience-Landmark"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.imrpress.com\/journal\/FBL\/29\/12\/10.31083\/j.fbl2912416","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,30]],"date-time":"2024-12-30T11:48:12Z","timestamp":1735559292000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.imrpress.com\/journal\/FBL\/29\/12\/10.31083\/j.fbl2912416"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,17]]},"references-count":107,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2024]]}},"alternative-id":["S2768-6701(24)01485-0"],"URL":"https:\/\/doi.org\/10.31083\/j.fbl2912416","relation":{},"ISSN":["2768-6701","2768-6698"],"issn-type":[{"value":"2768-6701","type":"print"},{"value":"2768-6698","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,17]]},"article-number":"416"}}