Analyze Diet
BMC veterinary research2025; 21(1); 204; doi: 10.1186/s12917-025-04652-9

Association between sperm DNA fragmentation and fertility parameters in farm animals: a systematic review and meta-analysis.

Abstract: Accurately predicting male fertility is crucial for the animal breeding industry due to its significant economic implications. Existing literature suggests that mammalian fertility is partially dependent on sperm DNA integrity. However, routine semen analysis often fails to detect DNA damage and does not consistently correlate with field fertility outcomes. While assessing sperm DNA integrity provides valuable biological insights, its role in diagnosing animal infertility remains uncertain. Results: This meta-analysis evaluated the association between sperm DNA fragmentation (SDF) and fertility in farm animals. Comprehensive searches were conducted using PubMed, Google Scholar, and Springer Link Library, with results stratified by animal species and SDF detection methods. Across 30 studies, the overall correlation coefficient (COR) between SDF and male fertility was -0.46 (95% confidence interval [CI]: -0.54 to -0.37; Z = -8.97; p < 0.001). A significant association was observed in bulls (COR = -0.47; 95% CI: -0.54 to -0.40; Z = -11.13; p < 0.001) and stallions (COR = -0.54; 95% CI: -0.72 to -0.29; Z = -3.83; p < 0.001), whereas no significant relationship was found in boars (COR = -0.19; 95% CI: -0.37 to 0.01; Z = -1.84; p = 0.07). The effect of SDF on male fertility was analyzed in 15 studies, demonstrating significantly higher SDF values in low-fertility animals compared to high-fertility groups (SMD = 0.85; 95% CI: 0.68 to 1.01; Z = 10.07; p < 0.001). This pattern was observed in both bulls (SMD = 1.21; 95% CI: 0.85 to 1.57; Z = 6.59; p < 0.001) and stallions (SMD = 0.64; 95% CI: 0.44 to 0.85; Z = 6.14; p < 0.001) subgroups. Conclusions: These findings suggest that incorporating SDF assays into breeding soundness evaluations could enhance the accuracy of selecting high-quality breeding males for artificial breeding programs. However, further research with adequately powered studies, standardized methodologies, and appropriate sample sizes is necessary to fully elucidate the impact of elevated SDF on fertility in farm animals.
Publication Date: 2025-03-26 PubMed ID: 40133892PubMed Central: PMC11938742DOI: 10.1186/s12917-025-04652-9Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Meta-Analysis
  • Systematic Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article presents a systematic review and meta-analysis of various studies that explore the relationship between sperm DNA fragmentation (SDF) and fertility in farm animal males. The study indicates that evaluating SDF can improve the prediction of animal fertility but further research is needed to completely understand the implications.

Research Background

  • The importance of accurate prediction of male fertility for the animal breeding industry due to practical economic impacts is highlighted.
  • The role of sperm DNA integrity in mammalian fertility is acknowledged but indicates limitations with current semen analysis in detecting DNA damage and in consistent correlation with fertility outcomes.
  • The authors express the uncertainty around the usefulness of assessing sperm DNA integrity in diagnosing animal infertility.

Research Methods

  • The authors conducted an extensive meta-analysis, analyzing the correlation between sperm DNA fragmentation and fertility across multiple farm animals.
  • The systematic review involved gathering data from several platforms like PubMed, Google Scholar, and Springer Link Library.
  • The data were then categorized based on animal species and the methods used for detecting SDF.

Main Findings

  • In a total of 30 studies, the overall correlation between SDF and male fertility was negative, suggesting that increased SDF is associated with reduced male fertility.
  • Significant negative associations between SDF and fertility were observed in bulls and stallions specifically.
  • In contrast, there was no significant correlation found in boars.
  • The studies also included an analysis of the impact of SDF on male fertility, with higher SDF values associated with lower fertility animals as compared to high fertility groups.

Conclusion and Impacts

  • The study concludes that integrating SDF assessments into breeding evaluations might improve the selection of high-quality breeding males for artificial breeding programs.
  • Despite these results, the study also emphasizes that further research is needed. Specifically, future studies need to have adequate power, standardized methodologies, and appropriate sample sizes to fully understand the influence of increased SDF on farm animal fertility.

Cite This Article

APA
Abah KO, Ligocka-Kowalczyk Z, Itodo JI, Ameh G, Partyka A, Nizanski W. (2025). Association between sperm DNA fragmentation and fertility parameters in farm animals: a systematic review and meta-analysis. BMC Vet Res, 21(1), 204. https://doi.org/10.1186/s12917-025-04652-9

Publication

ISSN: 1746-6148
NlmUniqueID: 101249759
Country: England
Language: English
Volume: 21
Issue: 1
Pages: 204
PII: 204

Researcher Affiliations

Abah, Kenneth Owoicho
  • Department of Reproduction and Clinic of Farm Animals, Faculty of Veterinary Medicine, Wroclaw University of Environmental and Life Sciences, Plac Grunwaldzki 49, 50‑366, Wroclaw, Poland. kenneth.abah@upwr.edu.pl.
Ligocka-Kowalczyk, Zuzanna
  • Department of Reproduction and Clinic of Farm Animals, Faculty of Veterinary Medicine, Wroclaw University of Environmental and Life Sciences, Plac Grunwaldzki 49, 50‑366, Wroclaw, Poland.
Itodo, Joy Iyojo
  • Department of Animal Science, Faculty of Agriculture, Federal University Lafia, Lafia, Nasarawa, 950101, Nigeria.
Ameh, Grace
  • Department of Microbiology, Faculty of Veterinary Medicine, University of Abuja, Airport Road FCT - Abuja P.M.B 117, Abuja, Nigeria.
Partyka, Agnieszka
  • Department of Reproduction and Clinic of Farm Animals, Faculty of Veterinary Medicine, Wroclaw University of Environmental and Life Sciences, Plac Grunwaldzki 49, 50‑366, Wroclaw, Poland.
Nizanski, Wojciech
  • Department of Reproduction and Clinic of Farm Animals, Faculty of Veterinary Medicine, Wroclaw University of Environmental and Life Sciences, Plac Grunwaldzki 49, 50‑366, Wroclaw, Poland.

MeSH Terms

  • Animals
  • Male
  • DNA Fragmentation
  • Spermatozoa / physiology
  • Fertility / genetics
  • Fertility / physiology
  • Horses
  • Semen Analysis / veterinary
  • Animals, Domestic

Conflict of Interest Statement

Declarations. Ethics approval and consent to participate: Not applicable. Consent for publication: Not applicable. Competing interests: The authors declare no competing interests.

References

This article includes 87 references
  1. Kumaresan A, Johannisson A, Al-Essawe EM, Morrell JM. Sperm viability, reactive oxygen species, and DNA fragmentation index combined can discriminate between above- and below-average fertility bulls.. J Dairy Sci 2017;100(7):5824–36.
    pubmed: 28478003
  2. Al-Kass Z, Ntallaris T, Morrell JM, Johannisson A. Deciphering sperm chromatin properties to predict stallion sperm fertility.. Anim Reprod Sci 2023;250: 107200.
    pubmed: 36801727
  3. Rota A, Furzi C, Panzani D, Camillo F. Studies on motility and fertility of cooled stallion spermatozoa.. Reprod Domest Anim Zuchthyg 2004;39(2):103–9.
    pubmed: 15065992
  4. Haadem CS, Nødtvedt A, Farstad W, Thomassen R. A retrospective cohort study on fertility in the Norwegian Coldblooded trotter after artificial insemination with cooled, shipped versus fresh extended semen.. Acta Vet Scand 2015;14(57):77.
    pmc: PMC4650285pubmed: 26578337
  5. Dobson H, Walker SL, Morris MJ, Routly JE, Smith RF. Why is it getting more difficult to successfully artificially inseminate dairy cows?. Anim Int J Anim Biosci 2008;2(8):1104–11.
    pmc: PMC2854809pubmed: 20396609
  6. Kumaresan A, Das Gupta M, Datta TK, Morrell JM. Sperm DNA Integrity and Male Fertility in Farm Animals: A Review.. Front Vet Sci 2020;7:321.
    pmc: PMC7317013pubmed: 32637425
  7. Robinson L, Gallos ID, Conner SJ, Rajkhowa M, Miller D, Lewis S. The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis.. Hum Reprod Oxf Engl 2012;27(10):2908–17.
    pubmed: 22791753
  8. Morrell JM, Johannisson A, Dalin AM, Hammar L, Sandebert T, Rodriguez-Martinez H. Sperm morphology and chromatin integrity in Swedish warmblood stallions and their relationship to pregnancy rates.. Acta Vet Scand 2008;50(1):2.
    pmc: PMC2246141pubmed: 18179691
  9. Narud B, Klinkenberg G, Khezri A, Zeremichael TT, Stenseth EB, Nordborg A. Differences in sperm functionality and intracellular metabolites in Norwegian Red bulls of contrasting fertility.. Theriogenology 2020;157:24–32.
    pubmed: 32777668
  10. Ausejo R, Martínez JM, Mendoza N, Bolarin A, Tejedor MT, Falceto MV. Nuclear DNA Fragmentation in Boar Spermatozoa: Measurement Methods and Reproductive Performance Implications.. Front Vet Sci 2022;9:929858.
    pmc: PMC9281558pubmed: 35847654
  11. Zhao J, Zhang Q, Wang Y, Li Y. Whether sperm deoxyribonucleic acid fragmentation has an effect on pregnancy and miscarriage after in vitro fertilization/intracytoplasmic sperm injection: a systematic review and meta-analysis.. Fertil Steril 2014;102(4):998–1005.
    pubmed: 25190048
  12. Didion BA, Kasperson KM, Wixon RL, Evenson DP. Boar fertility and sperm chromatin structure status: a retrospective report.. J Androl 2009;30(6):655–60.
    pubmed: 19478334
  13. Osman A, Alsomait H, Seshadri S, El-Toukhy T, Khalaf Y. The effect of sperm DNA fragmentation on live birth rate after IVF or ICSI: a systematic review and meta-analysis.. Reprod Biomed Online 2015;30(2):120–7.
    pubmed: 25530036
  14. Roca J, Parrilla I, Bolarin A, Martinez EA, Rodriguez-Martinez H. Will AI in pigs become more efficient?. Theriogenology 2016;86(1):187–93.
    pubmed: 26723133
  15. Sudano MJ, Crespilho AM, Fernandes CB, Junior AM, Papa FO, Rodrigues J. Use of bayesian inference to correlate in vitro embryo production and in vivo fertility in zebu bulls.. Vet Med Int 2011;2011:436381.
    pmc: PMC3087428pubmed: 21547211
  16. Oliveira L, Arruda R, De Andrade A, Carvalho Celeghini EC, Santos R, Beletti M. Assessment of field fertility and several in vitro sperm characteristics following the use of different Angus sires in a timed-AI program with suckled Nelore cows.. Livest Sci 2012;146:38–46.
  17. Morrell JM, Nongbua T, Valeanu S, Lima Verde I, Lundstedt-Enkel K, Edman A. Sperm quality variables as indicators of bull fertility may be breed dependent.. Anim Reprod Sci 2017;185:42–52.
    pubmed: 28811063
  18. Evenson DP, Darzynkiewicz Z, Melamed MR. Relation of mammalian sperm chromatin heterogeneity to fertility.. Science 1980;210(4474):1131–3.
    pubmed: 7444440
  19. Itodo JI, Rekwot PI, Aluwong T, Allam L, Olutimilehin Jolayemi K, Kyari S. Azanza garckeana ameliorates Bisphenol A-induced reproductive toxicities in rabbit bucks.. Theriogenology 2022;192:150–65.
    pubmed: 36099805
  20. Benchaib M, Lornage J, Mazoyer C, Lejeune H, Salle B, François GJ. Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome.. Fertil Steril 2007;87(1):93–100.
    pubmed: 17074327
  21. Morris ID, Ilott S, Dixon L, Brison DR. The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development.. Hum Reprod Oxf Engl 2002;17(4):990–8.
    pubmed: 11925396
  22. Seli E, Gardner DK, Schoolcraft WB, Moffatt O, Sakkas D. Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization.. Fertil Steril 2004;82(2):378–83.
    pubmed: 15302287
  23. Henkel R, Kierspel E, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C. DNA fragmentation of spermatozoa and assisted reproduction technology.. Reprod Biomed Online 2003;7(4):477–84.
    pubmed: 14656411
  24. Høst E, Lindenberg S, Smidt-Jensen S. The role of DNA strand breaks in human spermatozoa used for IVF and ICSI.. Acta Obstet Gynecol Scand 2000;79(7):559–63.
    pubmed: 10929955
  25. Frydman N, Prisant N, Hesters L, Frydman R, Tachdjian G, Cohen-Bacrie P. Adequate ovarian follicular status does not prevent the decrease in pregnancy rates associated with high sperm DNA fragmentation.. Fertil Steril 2008;89(1):92–7.
    pubmed: 17482180
  26. Love CC, Kenney RM. The relationship of increased susceptibility of sperm DNA to denaturation and fertility in the stallion.. Theriogenology 1998;50(6):955–72.
    pubmed: 10734467
  27. Vicente-Fiel S, Palacín I, Santolaria P, Fantova E, Quintín-Casorrán FJ, Sevilla-Mur E. In vitro assessment of sperm quality from rams of high and low field fertility.. Anim Reprod Sci 2014;146(1–2):15–20.
    pubmed: 24602507
  28. Puglisi R, Gaspa G, Balduzzi D, Severgnini A, Vanni R, Macciotta N. Genomewide analysis of bull sperm quality and fertility traits.. Reprod Domest Anim 2016;51(5):840–3.
    pubmed: 27550832
  29. Dogan S, Mason MC, Govindaraju A, Belser L, Kaya A, Stokes J. Interrelationships Between Apoptosis and Fertility in Bull Sperm.. J Reprod Dev 2013;59(1):18–26.
    pmc: PMC3943226pubmed: 22986927
  30. Paradowska-Dogan A, Fernandez A, Bergmann M, Kretzer K, Mallidis C, Vieweg M. Protamine mRNA ratio in stallion spermatozoa correlates with mare fecundity.. Andrology 2014;2(4):521–30.
    pubmed: 24711287
  31. Zoca MS, Shafii B, Price W, Utt M, Harstine B, McDonald K. Angus sire field fertility and in vitro sperm characteristics following use of different sperm insemination doses in Brazilian beef cattle.. Theriogenology 2020;147:146–53.
    pubmed: 31785860
  32. Holden SA, Fernandez-Fuertes B, Murphy C, Whelan H, O’Gorman A, Brennan L. Relationship between in vitro sperm functional assessments, seminal plasma composition, and field fertility after AI with either non-sorted or sex-sorted bull semen.. Theriogenology 2017;87:221–8.
    pubmed: 27678515
  33. Kutchy NA, Menezes ESB, Ugur MR, Ul Husna A, ElDebaky H, Evans HC. Sperm cellular and nuclear dynamics associated with bull fertility.. Anim Reprod Sci 2019;211:106203.
    pubmed: 31785643
  34. Rosyada ZNA, Pardede BP, Kaiin EM, Tumbelaka LITA, Solihin DD, Purwantara B. Identification of heat shock protein70-2 and protamine-1 mRNA, proteins, and analyses of their association with fertility using frozen-thawed sperm in Madura bulls.. Anim Biosci 2023;36(12):1796–805.
    pmc: PMC10623020pubmed: 37402446
  35. Donnellan EM, Perrier JP, Keogh K, Štiavnická M, Collins CM, Dunleavy EM. Identification of differentially expressed mRNAs and miRNAs in spermatozoa of bulls of varying fertility.. Front Vet Sci 2022;9:993561.
    pmc: PMC9581129pubmed: 36277068
  36. Rybar R, Kopecka V, Prinosilova P, Kubickova S, Veznik Z, Rubes J. Fertile bull sperm aneuploidy and chromatin integrity in relationship to fertility.. Int J Androl 2010;33(4):613–22.
    pubmed: 19751362
  37. Christensen P, Labouriau R, Birck A, Boe-Hansen GB, Pedersen J, Borchersen S. Relationship among seminal quality measures and field fertility of young dairy bulls using low-dose inseminations.. J Dairy Sci 2011;94(4):1744–54.
    pubmed: 21426963
  38. Waterhouse KE, Haugan T, Kommisrud E, Tverdal A, Flatberg G, Farstad W. Sperm DNA damage is related to field fertility of semen from young Norwegian Red bulls.. Reprod Fertil Dev 2006;18(7):781–8.
    pubmed: 17032587
  39. Myromslien FD, Tremoen NH, Andersen-Ranberg I, Fransplass R, Stenseth EB, Zeremichael TT. Sperm DNA integrity in Landrace and Duroc boar semen and its relationship to litter size.. Reprod Domest Anim 2019;54(2):160–6.
    pubmed: 30168871
  40. Michos I, Tsantarliotou M, Boscos CM, Tsousis G, Basioura A, Tzika ED. Effect of Boar Sperm Proteins and Quality Changes on Field Fertility.. Animal 2021;11(6):1813.
    pmc: PMC8234339pubmed: 34204554
  41. Boe-Hansen GB, Christensen P, Vibjerg D, Nielsen MBF, Hedeboe AM. Sperm chromatin structure integrity in liquid stored boar semen and its relationships with field fertility.. Theriogenology 2008;69(6):728–36.
    pubmed: 18242673
  42. Broekhuijse MLWJ, Šoštarić E, Feitsma H, Gadella BM. Relationship of flow cytometric sperm integrity assessments with boar fertility performance under optimized field conditions1.. J Anim Sci 2012;90(12):4327–36.
    pubmed: 23255815
  43. Waberski D, Schapmann E, Henning H, Riesenbeck A, Brandt H. Sperm chromatin structural integrity in normospermic boars is not related to semen storage and fertility after routine AI.. Theriogenology 2011;75(2):337–45.
    pubmed: 20961609
  44. García-Alvarez O, Maroto-Morales A, Ramón M, del Olmo E, Montoro V, Dominguez-Rebolledo AE. Analysis of selected sperm by density gradient centrifugation might aid in the estimation of in vivo fertility of thawed ram spermatozoa.. Theriogenology 2010;74(6):979–88.
    pubmed: 20580077
  45. Santolaria P, Vicente-Fiel S, Palacín I, Fantova E, Blasco ME, Silvestre MA. Predictive capacity of sperm quality parameters and sperm subpopulations on field fertility after artificial insemination in sheep.. Anim Reprod Sci 2015;163:82–8.
    pubmed: 26507945
  46. Serafini R, Love CC, Coletta A, Mari G, Mislei B, Caso C. Sperm DNA integrity in frozen-thawed semen from Italian Mediterranean Buffalo bulls and its relationship to in vivo fertility.. Anim Reprod Sci 2016;172:26–31.
    pubmed: 27421229
  47. Ahmed H, Andrabi SMH, Jahan S. Semen quality parameters as fertility predictors of water buffalo bull spermatozoa during low-breeding season.. Theriogenology 2016;86(6):1516–22.
    pubmed: 27321805
  48. Simões R, Feitosa WB, Siqueira AFP, Nichi M, Paula-Lopes FF, Marques MG. Influence of bovine sperm DNA fragmentation and oxidative stress on early embryo in vitro development outcome.. Reprod Camb Engl 2013;146(5):433–41.
    pubmed: 23940385
  49. Eid LN, Shamiah SM, El-Regalaty HAM, El-Keraby FE. Sperm DNA damage and embryonic development as related to fertility potential of buffalo bulls.. J Anim Poult Prod 2011;2(5):65–74.
  50. Zăhan M, Pall E, Cenariu M, Miclea I. Relationship between in vitro semen parameters and bull fertility.. Anim Bio Anim Hus 2018;10(2):156–63.
  51. Dogan S, Vargovic P, Oliveira R, Belser LE, Kaya A, Moura A. Sperm protamine-status correlates to the fertility of breeding bulls.. Biol Reprod 2015;92(4):92.
    pubmed: 25673563
  52. Anzar M, He L, Buhr MM, Kroetsch TG, Pauls KP. Sperm Apoptosis in Fresh and Cryopreserved Bull Semen Detected by Flow Cytometry and Its Relationship with Fertility1.. Biol Reprod 2002;66(2):354–60.
    pubmed: 11804948
  53. Ballachey BE, Hohenboken WD, Evenson DP. Heterogeneity of sperm nuclear chromatin structure and its relationship to bull fertility.. Biol Reprod 1987;36(4):915–25.
    pubmed: 3593856
  54. Bollwein H, Fuchs I, Koess C. Interrelationship between plasma membrane integrity, mitochondrial membrane potential and DNA fragmentation in cryopreserved bovine spermatozoa.. Reprod Domest Anim Zuchthyg 2008;43(2):189–95.
    pubmed: 17986172
  55. Erickson L, Kroetsch T, Anzar M. Relationship between sperm apoptosis and bull fertility: in vivo and in vitro studies.. Reprod Fertil Dev 2016;28(9):1369–75.
    pubmed: 25764086
  56. Gliozzi TM, Turri F, Manes S, Cassinelli C, Pizzi F. The combination of kinetic and flow cytometric semen parameters as a tool to predict fertility in cryopreserved bull semen.. Animal 2017;11(11):1975–82.
    pubmed: 28397643
  57. García-Macías V, de Paz P, Martinez-Pastor F, Alvarez M, Gomes-Alves S, Bernardo J. DNA fragmentation assessment by flow cytometry and Sperm-Bos-Halomax (bright-field microscopy and fluorescence microscopy) in bull sperm.. Int J Androl 2007;30(2):88–98.
    pubmed: 17166172
  58. Januskauskas A, Johannisson A, Rodriguez-Martinez H. Assessment of sperm quality through fluorometry and sperm chromatin structure assay in relation to field fertility of frozen-thawed semen from Swedish AI bulls.. Theriogenology 2001;55(4):947–61.
    pubmed: 11291917
  59. Januskauskas A, Johannisson A, Rodriguez-Martinez H. Subtle membrane changes in cryopreserved bull semen in relation with sperm viability, chromatin structure, and field fertility.. Theriogenology 2003;60(4):743–58.
    pubmed: 12832022
  60. Ballachey BE, Evenson DP, Saacke RG. The sperm chromatin structure assay. Relationship with alternate tests of semen quality and heterospermic performance of bulls.. J Androl 1988;9(2):109–15.
    pubmed: 3384741
  61. Karoui S, Díaz C, González-Marín C, Amenabar ME, Serrano M, Ugarte E. Is sperm DNA fragmentation a good marker for field AI bull fertility?. J Anim Sci 2012;90(8):2437–49.
    pubmed: 22367070
  62. Nagy S, Johannisson A, Wahlsten T, Ijäs R, Andersson M, Rodriguez-Martinez H. Sperm chromatin structure and sperm morphology: their association with fertility in AI-dairy Ayrshire sires.. Theriogenology 2013;79(8):1153–61.
    pubmed: 23523176
  63. Pardede BP, Agil M, Karja NWK, Sumantri C, Supriatna I, Purwantara B. PRM1 Gene Expression and Its Protein Abundance in Frozen-Thawed Spermatozoa as Potential Fertility Markers in Breeding Bulls.. Vet Sci 2022;9(3):111.
    pmc: PMC8951773pubmed: 35324839
  64. Atroshchenko MM, Arkhangelskaya E, Isaev DA, Stavitsky SB, Zaitsev AM, Kalaschnikov VV. Reproductive Characteristics of Thawed Stallion Sperm.. Animals 2019;9(12):1099.
    pmc: PMC6940853pubmed: 31818047
  65. Crespo F, Quiñones-Pérez C, Ortiz I, Diaz-Jimenez M, Consuegra C, Pereira B. Seasonal variations in sperm DNA fragmentation and pregnancy rates obtained after artificial insemination with cooled-stored stallion sperm throughout the breeding season (spring and summer).. Theriogenology 2020;148:89–94.
    pubmed: 32169626
  66. Kenney RM, Evenson DP, Garcia MC, Love CC. Relationships between Sperm Chromatin Structure, Motility, and Morphology of Ejaculated Sperm, and Seasonal Pregnancy Rate1.. Biol Reprod 1995;52:647–53.
  67. Estrada E, Rodriguese-Gil JE, Rocha LG, Balasch S, Bonet S, Yeste M. Supplementing cryopreservation media with reduced glutathione increases fertility and prolificacy of sows inseminated with frozen-thawed boar semen.. Andrology 2014;2:88–99.
    pubmed: 24123940
  68. Batista C, van Lier E, Petrocelli H. Dynamics of sperm DNA fragmentation in raw boar semen and fertility.. Reprod Domest Anim Zuchthyg 2016;51(5):774–80.
    pubmed: 27546051
  69. Tsakmakidis IA, Lymberopoulos AG, Khalifa TA. Relationship between sperm quality traits and field-fertility of porcine semen.. J Vet Sci 2010;11(2):151–4.
    pmc: PMC2873815pubmed: 20458156
  70. Serafini R, Varner DD, Blanchard TL, Teague SR, LaCaze K, Love CC. Effects of seminal plasma and flash-freezing on DNA structure of stallion epididymal sperm exposed to different potentiators of DNA damage.. Theriogenology 2018;117:34–9.
    pubmed: 29807256
  71. Evenson DP. The Sperm Chromatin Structure Assay (SCSA(®)) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility.. Anim Reprod Sci 2016;169:56–75.
    pubmed: 26919909
  72. Robertson MJ, Chambers C, Spanner EA, de Graaf SP, Rickard JP. The Assessment of Sperm DNA Integrity: Implications for Assisted Reproductive Technology Fertility Outcomes across Livestock Species.. Biology 2024;13(7):539.
    pmc: PMC11273975pubmed: 39056730
  73. Sailer BL, Jost LK, Evenson DP. Mammalian sperm DNA susceptibility to in situ denaturation associated with the presence of DNA strand breaks as measured by the terminal deoxynucleotidyl transferase assay.. J Androl 1995;16(1):80–7.
    pubmed: 7768756
  74. Martínez-Pastor F, Fernández-Santos MR, Domínguez-Rebolledo AE, Esteso MC, Garde JJ, Biology of Reproduction Group. DNA status on thawed semen from fighting bull: a comparison between the SCD and the SCSA tests.. Reprod Domest Anim 2009;44(3):424–31.
    pubmed: 18992075
  75. Barratt CLR, Aitken RJ, Björndahl L, Carrell DT, de Boer P, Kvist U. Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications-a position report.. Hum Reprod Oxf Engl 2010;25(4):824–38.
    pubmed: 20139429
  76. Krausz C, Escamilla AR, Chianese C. Genetics of male infertility: from research to clinic.. Reprod Camb Engl 2015;150(5):159–74.
    pubmed: 26447148
  77. Urdinguio RG, Bayón GF, Dmitrijeva M, Toraño EG, Bravo C, Fraga MF. Aberrant DNA methylation patterns of spermatozoa in men with unexplained infertility.. Hum Reprod Oxf Engl 2015;30(5):1014–28.
    pubmed: 25753583
  78. Rodríguez-Martínez H. Laboratory semen assessment and prediction of fertility: still utopia?. Reprod Domest Anim 2003;38(4):312–8.
    pubmed: 12887570
  79. Nagy Á, Polichronopoulos T, Gáspárdy A, Solti L, Cseh S. Correlation between bull fertility and sperm cell velocity parameters generated by computer-assisted semen analysis.. Acta Vet Hung 2015;63(3):370–81.
    pubmed: 26551427
  80. Bailey JL, Buhr MM, Robertson L. Relationships among in vivo fertility, computer-analysed motility and in vitro Ca2+ flux in bovine spermatozoa.. Can J Anim Sci 1994;74(1):53–8.
  81. Thundathil J, Gil J, Januskauskas A, Larsson B, Soderquist L, Mapletoft R. Relationship between the proportion of capacitated spermatozoa present in frozen-thawed bull semen and fertility with artificial insemination.. Int J Androl 1999;22(6):366–73.
    pubmed: 10624605
  82. Grippo AA, Way AL, Killian GJ. Effect of bovine ampullary and isthmic oviductal fluid on motility, acrosome reaction and fertility of bull spermatozoa.. J Reprod Fertil 1995;105(1):57–64.
    pubmed: 7490715
  83. Kumaresan A, Johannisson A, Bergqvist AS. Sperm function during incubation with oestrus oviductal fluid differs in bulls with different fertility.. Reprod Fertil Dev 2017;29(6):1096–106.
    pubmed: 27112984
  84. Singh RK, Kumaresan A, Chhillar S, Rajak SK, Tripathi UK, Nayak S. Identification of suitable combinations of in vitro sperm-function test for the prediction of fertility in buffalo bull.. Theriogenology 2016;86(9):2263–71.
    pubmed: 27555524
  85. Oliveira BM, Arruda RP, Thomé HE, Maturana Filho M, Oliveira G, Guimarães C. Fertility and uterine hemodynamic in cows after artificial insemination with semen assessed by fluorescent probes.. Theriogenology 2014;82(5):767–72.
    pubmed: 25023296
  86. Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis.. Stat Med 2002;21(11):1539–58.
    pubmed: 12111919
  87. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias.. Biometrics 1994;50(4):1088–101.
    pubmed: 7786990

Citations

This article has been cited 0 times.