{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,2]],"date-time":"2026-11-02T23:17:40Z","timestamp":1793661460620,"version":"4.5.1"},"reference-count":51,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2025,6,13]],"date-time":"2025-06-13T00:00:00Z","timestamp":1749772800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004837","name":"Spanish Ministry of Science and Innovation","doi-asserted-by":"publisher","award":["PID2019-106380RBI00\/AEI\/10.13039\/501100011033"],"award-info":[{"award-number":["PID2019-106380RBI00\/AEI\/10.13039\/501100011033"]}],"id":[{"id":"10.13039\/501100004837","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004837","name":"Spanish Ministry of Science and Innovation","doi-asserted-by":"publisher","award":["PDC2022-133589-I00"],"award-info":[{"award-number":["PDC2022-133589-I00"]}],"id":[{"id":"10.13039\/501100004837","id-type":"DOI","asserted-by":"publisher"}]},{"name":"European Union \u2018Next Generation\u2019 EU\/PRTR","award":["PID2019-106380RBI00\/AEI\/10.13039\/501100011033"],"award-info":[{"award-number":["PID2019-106380RBI00\/AEI\/10.13039\/501100011033"]}]},{"name":"European Union \u2018Next Generation\u2019 EU\/PRTR","award":["PDC2022-133589-I00"],"award-info":[{"award-number":["PDC2022-133589-I00"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Veterinary Sciences"],"abstract":"<jats:p>Artificial insemination (AI) is essential in intensive pig production, which significantly depends on semen quality from boars selected for health, genetics, and fertility. While AI aims to improve productivity, larger litters often result in smaller and less resistant piglets. Beyond fertility and genetic traits, boars also influence offspring health. This study investigated the relationship between sperm parameters of highly fertile boars and both reproductive outcomes and piglet physiological indicators. Multivariate analysis revealed significant paternal effects on blood markers reflecting organ function, including those of the pancreas, liver, and kidneys, as well as on glucose homeostasis, lipid metabolism, oxidative stress, protein and carbohydrate metabolism, muscle contraction, and neural signaling. Notably, sperm velocity was correlated with mitochondrial function, which is crucial for sperm motility, capacitation, DNA integrity, and embryo development\u2014factors likely linked to healthier, more resilient offspring. Boars transmitting superior sperm velocity, erythropoiesis efficiency, and oxygen transport capacities produced piglets with better glucose regulation, growth, and resistance to neonatal hypoglycemia. These findings underscore the broader impact of sperm quality on offspring vitality and suggest that advanced sperm analysis could improve boar selection and enable more effective, health-oriented breeding strategies.<\/jats:p>","DOI":"10.3390\/vetsci12060582","type":"journal-article","created":{"date-parts":[[2025,6,13]],"date-time":"2025-06-13T03:53:12Z","timestamp":1749786792000},"page":"582","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["The Individual Variations in Sperm Quality of High-Fertility Boars Impact the Offspring Production and Early Physiological Functions"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0009-0006-3035-2981","authenticated-orcid":false,"given":"Santa Mar\u00eda","family":"Toledo-Guardiola","sequence":"first","affiliation":[{"name":"Department of Physiology, Faculty of Veterinary Medicine, University of Murcia, Campus Espinardo, 30100 Murcia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Luongo","sequence":"additional","affiliation":[{"name":"Department of Physiology, Faculty of Veterinary Medicine, University of Murcia, Campus Espinardo, 30100 Murcia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Felipe","family":"Mart\u00ednez-Pastor","sequence":"additional","affiliation":[{"name":"Cell Biology, Department of Molecular Biology, University of Le\u00f3n, Campus Vegazana, 24071 Le\u00f3n, Spain"},{"name":"Institute of Animal Health and Livestock Development (INDEGSAL), University of Le\u00f3n, Campus Vegazana, 24071 Le\u00f3n, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2880-3342","authenticated-orcid":false,"given":"Cristina","family":"Soriano-\u00dabeda","sequence":"additional","affiliation":[{"name":"Institute of Animal Health and Livestock Development (INDEGSAL), University of Le\u00f3n, Campus Vegazana, 24071 Le\u00f3n, Spain"},{"name":"Animal Reproduction and Obstetrics, Department of Veterinary Medicine, Surgery, and Anatomy, University of Le\u00f3n, Campus Vegazana, 24071 Le\u00f3n, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carmen","family":"Mat\u00e1s","sequence":"additional","affiliation":[{"name":"Department of Physiology, Faculty of Veterinary Medicine, University of Murcia, Campus Espinardo, 30100 Murcia, Spain"},{"name":"Pascual Parrilla Murcian Biosanitary Research Institute (IMIB\u2014Arrixaca), 30120 Murcia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,6,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1439-0531.2011.01869.x","article-title":"Review on International Trade with Boar Semen","volume":"46","author":"Riesenbeck","year":"2011","journal-title":"Reprod. Domest. Anim."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1186\/s40813-017-0062-5","article-title":"Boar Management and Semen Handling Factors Affect the Quality of Boar Extended Semen","volume":"3","author":"Arsenakis","year":"2017","journal-title":"Porc. Health Manag."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40813-016-0049-7","article-title":"Factors for Improving Reproductive Performance of Sows and Herd Productivity in Commercial Breeding Herds","volume":"3","author":"Koketsu","year":"2017","journal-title":"Porc. Health Manag."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1842","DOI":"10.1016\/S0140-6736(18)30312-X","article-title":"Origins of Lifetime Health around the Time of Conception: Causes and Consequences","volume":"391","author":"Fleming","year":"2018","journal-title":"Lancet"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Costa-J\u00fanior, J.M., Ferreira, S.M., Kurauti, M.A., Bernstein, D.L., Ruano, E.G., Kameswaran, V., Schug, J., Freitas-Dias, R., Zoppi, C.C., and Boschero, A.C. (2022). Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23010001"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2200","DOI":"10.1073\/pnas.1305609111","article-title":"Maternal Tract Factors Contribute to Paternal Seminal Fluid Impact on Metabolic Phenotype in Offspring","volume":"111","author":"Bromfield","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"396","DOI":"10.2164\/jandrol.04155","article-title":"Cooling and Freezing of Boar Spermatozoa: Supplementation of the Freezing Media with Reduced Glutathione Preserves Sperm Function","volume":"26","author":"Gadea","year":"2005","journal-title":"J. Androl."},{"key":"ref_8","unstructured":"R Core Team (2024). R: A Language and Environment for Statistical Computing, Version 4.4.1, R Foundation for Statistical Computing."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1016\/j.theriogenology.2004.09.040","article-title":"Impact of Genetic Selection on Management of Boar Replacement","volume":"63","author":"Robinson","year":"2005","journal-title":"Theriogenology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"R109","DOI":"10.1530\/REP-18-0524","article-title":"Ejaculate-Mediated Paternal Effects: Evidence, Mechanisms and Evolutionary Implications","volume":"157","author":"Evans","year":"2019","journal-title":"Reproduction"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1432","DOI":"10.1017\/S1751731118002987","article-title":"Sow Environment during Gestation: Part I. Influence on Maternal Physiology and Lacteal Secretions in Relation with Neonatal Survival","volume":"13","author":"Merlot","year":"2019","journal-title":"Animal"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Luongo, C., Llamas-L\u00f3pez, P.J., Hern\u00e1ndez-Caravaca, I., Mat\u00e1s, C., and Garc\u00eda-V\u00e1zquez, F.A. (2022). Should All Fractions of the Boar Ejaculate Be Prepared for Insemination Rather Than Using the Sperm Rich Only?. Biology, 11.","DOI":"10.3390\/biology11020210"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.theriogenology.2024.02.017","article-title":"Artificial Insemination of All Ejaculated Sperm Fractions Accelerates Embryo Development and Increases the Uterine Vascularity in the Pig","volume":"219","author":"Seva","year":"2024","journal-title":"Theriogenology"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.theriogenology.2021.12.010","article-title":"Effects of Farrowing Induction with Prostaglandins on Farrowing Traits and Piglet Performance: A Systematic Review and Meta-Analysis","volume":"180","author":"Monteiro","year":"2022","journal-title":"Theriogenology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"100350","DOI":"10.1016\/j.animal.2021.100350","article-title":"Review: Improving the Performance of Neonatal Piglets","volume":"16","author":"Farmer","year":"2022","journal-title":"Animal"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"E105","DOI":"10.2527\/2006.8413_supplE105x","article-title":"The Biological Basis for Prenatal Programming of Postnatal Performance in Pigs","volume":"84","author":"Foxcroft","year":"2006","journal-title":"J. Anim. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1093\/humupd\/dmg027","article-title":"Role of Sperm Chromatin Abnormalities and DNA Damage in Male Infertility","volume":"9","author":"Agarwal","year":"2003","journal-title":"Hum. Reprod. Update"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2402","DOI":"10.1093\/humrep\/deu228","article-title":"Paternal Influence of Sperm DNA Integrity on Early Embryonic Development","volume":"29","author":"Simon","year":"2014","journal-title":"Hum. Reprod."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1953","DOI":"10.1007\/s10815-018-1304-4","article-title":"Paternal Factors Contributing to Embryo Quality","volume":"35","author":"Colaco","year":"2018","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Mateo-Otero, Y., Madrid-Gambin, F., Llavanera, M., Gomez-Gomez, A., Haro, N., Pozo, O.J., and Yeste, M. (2023). Sperm Physiology and in Vitro Fertilising Ability Rely on Basal Metabolic Activity: Insights from the Pig Model. Commun. Biol., 6.","DOI":"10.1038\/s42003-023-04715-3"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.semcdb.2019.06.008","article-title":"The Influence of Seminal Plasma on Offspring Development and Health","volume":"97","author":"Morgan","year":"2020","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"S138","DOI":"10.1016\/j.theriogenology.2007.03.018","article-title":"Role of the Oviduct in Sperm Capacitation","volume":"68","year":"2007","journal-title":"Theriogenology"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Fern\u00e1ndez-L\u00f3pez, P., Garriga, J., Casas, I., Yeste, M., and Bartumeus, F. (2022). Predicting Fertility from Sperm Motility Landscapes. Commun. Biol., 5.","DOI":"10.1038\/s42003-022-03954-0"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.anireprosci.2018.03.024","article-title":"The Sperm Mitochondrion: Organelle of Many Functions","volume":"194","author":"Moraes","year":"2018","journal-title":"Anim. Reprod. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1530\/REP-13-0178","article-title":"Mitochondria Functionality and Sperm Quality","volume":"146","author":"Amaral","year":"2013","journal-title":"Reproduction"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Mateo-Otero, Y., Llavanera, M., Torres-Garrido, M., and Yeste, M. (2024). Embryo Development Is Impaired by Sperm Mitochondrial-Derived ROS. Biol. Res., 57.","DOI":"10.1186\/s40659-024-00483-4"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1560","DOI":"10.1242\/jeb.02136","article-title":"Sperm Selection and Competition in Pigs May Be Mediated by the Differential Motility Activation and Suppression of Sperm Subpopulations within the Oviduct","volume":"209","author":"Satake","year":"2006","journal-title":"J. Exp. Biol."},{"key":"ref_28","first-page":"24","article-title":"Seminal Factors Influencing Return to Estrus in Female Pigs Following Artificial Insemination","volume":"11","author":"Mcpherson","year":"2014","journal-title":"Anim. Reprod."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Bhadsavle, S.S., and Golding, M.C. (2022). Paternal Epigenetic Influences on Placental Health and Their Impacts on Offspring Development and Disease. Front. Genet., 13.","DOI":"10.3389\/fgene.2022.1068408"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1152\/physrev.00013.2018","article-title":"The Female Response to Seminal Fluid","volume":"100","author":"Schjenken","year":"2020","journal-title":"Physiol. Rev."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Berger, T., Guerrero, V., Boeldt, R., Legacki, E., Roberts, M., and Conley, A.J. (2024). Development of Porcine Accessory Sex Glands. Animals, 14.","DOI":"10.3390\/ani14030462"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Rodriguez-Martinez, H., Martinez, E.A., Calvete, J.J., Pe\u00f1a Vega, F.J., and Roca, J. (2021). Seminal Plasma: Relevant for Fertility?. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22094368"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Mateo-Otero, Y., Llavanera, M., Recuero, S., Delgado-Berm\u00fadez, A., Barranco, I., Ribas-Maynou, J., and Yeste, M. (2022). Sperm DNA Damage Compromises Embryo Development, but Not Oocyte Fertilisation in Pigs. Biol. Res., 55.","DOI":"10.1186\/s40659-022-00386-2"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2541","DOI":"10.1098\/rspb.2010.0333","article-title":"Paternal Levels of DNA Damage in Spermatozoa and Maternal Parity Influence Offspring Mortality in an Endangered Ungulate","volume":"277","author":"Espeso","year":"2010","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Li, F., Duan, X., Li, M., and Ma, X. (2024). Sperm DNA Fragmentation Index Affect Pregnancy Outcomes and Offspring Safety in Assisted Reproductive Technology. Sci. Rep., 14.","DOI":"10.1038\/s41598-023-45091-6"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Opuwari, C.S., and Henkel, R.R. (2016). An Update on Oxidative Damage to Spermatozoa and Oocytes. BioMed Res. Int., 2016.","DOI":"10.1155\/2016\/9540142"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1071\/RD18159","article-title":"Tropical Summer Induces DNA Fragmentation in Boar Spermatozoa: Implications for Evaluating Seasonal Infertility","volume":"31","author":"Stone","year":"2019","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.theriogenology.2019.11.018","article-title":"Influence of the Age of the Individual on the Stability of Boar Sperm Genetic Material","volume":"147","author":"Czubaszek","year":"2020","journal-title":"Theriogenology"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Ausejo, R., Mart\u00ednez, J.M., Soler-llorens, P., Bolar\u00edn, A., Tejedor, T., and Falceto, M.V. (2021). Seasonal Changes of Nuclear DNA Fragmentation in Boar Spermatozoa in Spain. Animals, 11.","DOI":"10.3390\/ani11020465"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1038\/jhg.2012.2","article-title":"Common Genetic Factors for Hematological Traits in Humans","volume":"57","author":"Okada","year":"2012","journal-title":"J. Hum. Genet."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"248","DOI":"10.54846\/jshap\/1399","article-title":"Assessment of Hemoglobin Concentration in Sows and Their Offspring over Consecutive Reproductive Cycles","volume":"32","author":"McClellan","year":"2024","journal-title":"J. Swine Health Prod."},{"key":"ref_42","unstructured":"Bauer, A.E. (2000). Oxygen Supply and Consumption in Tissues. Sepsis and Organ Dysfunction, Springer."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Pittman, R.N. (2016). Regulation of Tissue Oxygenation, Morgan & Claypool.","DOI":"10.4199\/C00140ED2V01Y201606ISP065"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"\u00c1lvarez-Rodr\u00edguez, M., Mart\u00ednez, C., Wright, D., Barranco, I., Roca, J., and Rodr\u00edguez-Mart\u00ednez, H. (2020). The Transcriptome of Pig Spermatozoa, and Its Role in Fertility. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21051572"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/0165-0378(94)90036-1","article-title":"Inflammatory Response in the Pig Uterus Induced by Seminal Plasma","volume":"26","author":"Bischoft","year":"1994","journal-title":"J. Reprod. Immunol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1530\/rep.1.00160","article-title":"Seminal Plasma Regulates Endometrial Cytokine Expression, Leukocyte Recruitment and Embryo Development in the Pig","volume":"128","author":"Jasper","year":"2004","journal-title":"Reproduction"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1111\/rda.12383","article-title":"Seminal Fluid and Immune Adaptation for Pregnancy\u2014Comparative Biology in Mammalian Species","volume":"49","author":"Schjenken","year":"2014","journal-title":"Reprod. Domest. Anim."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Waberski, D., Sch\u00e4fer, J., B\u00f6lling, A., Scheld, M., Henning, H., Hambruch, N., Schuberth, H.J., Pfarrer, C., Wrenzycki, C., and Hunter, R.H.F. (2018). Seminal Plasma Modulates the Immune-Cytokine Network in the Porcine Uterine Tissue and Pre-Ovulatory Follicles. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0202654"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1177\/1040638716658928","article-title":"Age-Related Changes of Platelet and Plasma Coagulation Parameters in Young Pigs","volume":"28","author":"Gemra","year":"2016","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1046\/j.1439-0442.2003.00581.x","article-title":"Reference Intervals and Age-Related Changes for Platelet Count, Mean Platelet Volume and Plateletcrit in Healthy Pre-Weaning Piglets in Italy","volume":"50","author":"Faustini","year":"2003","journal-title":"J. Vet. Med. Ser. A Physiol. Pathol. Clin. Med."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Vahedi Raad, M., Firouzabadi, A.M., Tofighi Niaki, M., Henkel, R., and Fesahat, F. (2024). The Impact of Mitochondrial Impairments on Sperm Function and Male Fertility: A Systematic Review. Reprod. Biol. Endocrinol., 22.","DOI":"10.1186\/s12958-024-01252-4"}],"container-title":["Veterinary Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2306-7381\/12\/6\/582\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:51:10Z","timestamp":1760032270000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2306-7381\/12\/6\/582"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6,13]]},"references-count":51,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2025,6]]}},"alternative-id":["vetsci12060582"],"URL":"https:\/\/doi.org\/10.3390\/vetsci12060582","relation":{},"ISSN":["2306-7381"],"issn-type":[{"value":"2306-7381","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,13]]}}}