{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T22:53:24Z","timestamp":1789772004127,"version":"4.0.1"},"reference-count":72,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,11,12]],"date-time":"2021-11-12T00:00:00Z","timestamp":1636675200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,11,12]],"date-time":"2021-11-12T00:00:00Z","timestamp":1636675200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100014440","name":"Ministerio de Ciencia, Innovaci\u00f3n y Universidades","doi-asserted-by":"publisher","award":["AGL2017-88329-R"],"award-info":[{"award-number":["AGL2017-88329-R"]}],"id":[{"id":"10.13039\/100014440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014440","name":"Ministerio de Ciencia, Innovaci\u00f3n y Universidades","doi-asserted-by":"publisher","award":["FJCI-2017-31689"],"award-info":[{"award-number":["FJCI-2017-31689"]}],"id":[{"id":"10.13039\/100014440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014440","name":"Ministerio de Ciencia, Innovaci\u00f3n y Universidades","doi-asserted-by":"publisher","award":["RYC-2014-15581"],"award-info":[{"award-number":["RYC-2014-15581"]}],"id":[{"id":"10.13039\/100014440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007801","name":"Fundaci\u00f3n S\u00e9neca","doi-asserted-by":"publisher","award":["19892\/GERM-15"],"award-info":[{"award-number":["19892\/GERM-15"]}],"id":[{"id":"10.13039\/100007801","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003030","name":"Ag\u00e8ncia de Gesti\u00f3 d\u2019Ajuts Universitaris i de Recerca","doi-asserted-by":"publisher","award":["2017-SGR-1229"],"award-info":[{"award-number":["2017-SGR-1229"]}],"id":[{"id":"10.13039\/501100003030","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003030","name":"Ag\u00e8ncia de Gesti\u00f3 d\u2019Ajuts Universitaris i de Recerca","doi-asserted-by":"publisher","award":["2020-FI-B-00412"],"award-info":[{"award-number":["2020-FI-B-00412"]}],"id":[{"id":"10.13039\/501100003030","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Animal Sci Biotechnol"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      Metabolomic approaches, which include the study of low molecular weight molecules, are an emerging -omics technology useful for identification of biomarkers. In this field, nuclear magnetic resonance (NMR) spectroscopy has already been used to uncover (in) fertility biomarkers in the seminal plasma (SP) of several mammalian species. However, NMR studies profiling the porcine SP metabolome to uncover\n                      <jats:italic>in vivo<\/jats:italic>\n                      fertility biomarkers are yet to be carried out. Thus, this study aimed to evaluate the putative relationship between SP-metabolites and\n                      <jats:italic>in vivo<\/jats:italic>\n                      fertility outcomes. To this end, 24 entire ejaculates (three ejaculates per boar) were collected from artificial insemination (AI)-boars throughout a year (one ejaculate every 4 months). Immediately after collection, ejaculates were centrifuged to obtain SP-samples, which were stored for subsequent metabolomic analysis by NMR spectroscopy. Fertility outcomes from 1525 inseminations were recorded over a year, including farrowing rate, litter size, stillbirths per litter and the duration of pregnancy.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>A total of 24 metabolites were identified and quantified in all SP-samples. Receiver operating characteristic (ROC) curve analysis showed that lactate levels in SP had discriminative capacity for farrowing rate (area under the curve [AUC]\u2009=\u20090.764) while carnitine (AUC\u2009=\u20090.847), hypotaurine (AUC\u2009=\u20090.819), sn-glycero-3-phosphocholine (AUC\u2009=\u20090.833), glutamate (AUC\u2009=\u20090.799) and glucose (AUC\u2009=\u20090.750) showed it for litter size. Similarly, citrate (AUC\u2009=\u20090.743), creatine (AUC\u2009=\u20090.812), phenylalanine (AUC\u2009=\u20090.750), tyrosine (AUC\u2009=\u20090.753) and malonate (AUC\u2009=\u20090.868) levels had discriminative capacity for stillbirths per litter; and malonate (AUC\u2009=\u20090.767) and fumarate (AUC\u2009=\u20090.868) levels for gestation length.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>\n                      The assessment of selected SP-metabolites in ejaculates through NMR spectroscopy could be considered as a promising non-invasive tool to predict\n                      <jats:italic>in vivo<\/jats:italic>\n                      fertility outcomes in pigs. Moreover, supplementing AI-doses with specific metabolites should also be envisaged as a way to improve their fertility potential.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s40104-021-00636-5","type":"journal-article","created":{"date-parts":[[2021,11,12]],"date-time":"2021-11-12T07:02:55Z","timestamp":1636700575000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["Metabolomic fingerprinting of pig seminal plasma identifies in vivo fertility biomarkers"],"prefix":"10.1186","volume":"12","author":[{"given":"Yentel","family":"Mateo-Otero","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pol","family":"Fern\u00e1ndez-L\u00f3pez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ariadna","family":"Delgado-Berm\u00fadez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pau","family":"Nolis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jordi","family":"Roca","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jordi","family":"Mir\u00f3","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabel","family":"Barranco","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2209-340X","authenticated-orcid":false,"given":"Marc","family":"Yeste","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,11,12]]},"reference":[{"key":"636_CR1","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1016\/j.theriogenology.2019.05.030","volume":"137","author":"D Waberski","year":"2019","unstructured":"Waberski D, Riesenbeck A, Schulze M, Weitze KF, Johnson L. Application of preserved boar semen for artificial insemination: past, present and future challenges. Theriogenology. 2019;137:2\u20137. https:\/\/doi.org\/10.1016\/j.theriogenology.2019.05.030.","journal-title":"Theriogenology."},{"issue":"1","key":"636_CR2","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/j.theriogenology.2015.11.026","volume":"86","author":"J Roca","year":"2016","unstructured":"Roca J, Parrilla I, Bolarin A, Martinez EA, Rodriguez-Martinez H. Will AI in pigs become more efficient? Theriogenology Elsevier Ltd. 2016;86(1):187\u201393. https:\/\/doi.org\/10.1016\/j.theriogenology.2015.11.026.","journal-title":"Theriogenology Elsevier Ltd"},{"issue":"Suppl 2","key":"636_CR3","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1111\/j.1439-0531.2011.01861.x","volume":"46","author":"MLWJ Broekhuijse","year":"2011","unstructured":"Broekhuijse MLWJ, Feitsma H, Gadella BM. Field data analysis of boar semen quality. Reprod Domest Anim. 2011;46(Suppl 2):59\u201363. https:\/\/doi.org\/10.1111\/j.1439-0531.2011.01861.x.","journal-title":"Reprod Domest Anim"},{"issue":"Suppl 2","key":"636_CR4","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1111\/rda.12530","volume":"50","author":"J Roca","year":"2015","unstructured":"Roca J, Broekhuijse MLWJ, Parrilla I, Rodriguez-Martinez H, Martinez EA, Bolarin A. Boar differences in artificial insemination outcomes: can they be minimized? Reprod Domest Anim. 2015;50(Suppl 2):48\u201355. https:\/\/doi.org\/10.1111\/rda.12530.","journal-title":"Reprod Domest Anim"},{"key":"636_CR5","first-page":"1","volume":"66","author":"H Rodriguez-Martinez","year":"2009","unstructured":"Rodriguez-Martinez H, Kvist U, Saravia F, Wallgren M, Johannisson A, Sanz L, et al. The physiological roles of the boar ejaculate. Soc Reprod Fertil Suppl. 2009;66:1\u201321.","journal-title":"Soc Reprod Fertil Suppl"},{"key":"636_CR6","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1111\/j.1600-0897.2011.01033.x","volume":"66","author":"H Rodr\u00edguez-Mart\u00ednez","year":"2011","unstructured":"Rodr\u00edguez-Mart\u00ednez H, Kvist U, Ernerudh J, Sanz L, Calvete JJ. Seminal plasma proteins: what role do they play? Am J Reprod Immunol. 2011;66:11\u201322. https:\/\/doi.org\/10.1111\/j.1600-0897.2011.01033.x.","journal-title":"Am J Reprod Immunol"},{"key":"636_CR7","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.theriogenology.2019.05.035","volume":"137","author":"S Recuero","year":"2019","unstructured":"Recuero S, Fernandez-Fuertes B, Bonet S, Barranco I, Yeste M. Potential of seminal plasma to improve the fertility of frozen-thawed boar spermatozoa. Theriogenology. 2019;137:36\u201342. https:\/\/doi.org\/10.1016\/j.theriogenology.2019.05.035.","journal-title":"Theriogenology."},{"key":"636_CR8","doi-asserted-by":"crossref","unstructured":"Morgan HL, Watkins AJ. The influence of seminal plasma on offspring development and health. Semin. Cell Dev. Biol. 2020;97:131\u20137.","DOI":"10.1016\/j.semcdb.2019.06.008"},{"issue":"4","key":"636_CR9","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1586\/14737159.7.4.351","volume":"7","author":"F Deepinder","year":"2007","unstructured":"Deepinder F, Chowdary HT, Agarwal A. Role of metabolomic analysis of biomarkers in the management of male infertility. Expert Rev Mol Diagn. 2007;7(4):351\u20138. https:\/\/doi.org\/10.1586\/14737159.7.4.351.","journal-title":"Expert Rev Mol Diagn"},{"issue":"4","key":"636_CR10","doi-asserted-by":"publisher","first-page":"998","DOI":"10.1016\/j.fertnstert.2013.01.111","volume":"99","author":"JR Kovac","year":"2013","unstructured":"Kovac JR, Pastuszak AW, Lamb DJ. The use of genomics, proteomics, and metabolomics in identifying biomarkers of male infertility. Fertil Steril. 2013;99(4):998\u20131007. https:\/\/doi.org\/10.1016\/j.fertnstert.2013.01.111.","journal-title":"Fertil Steril"},{"issue":"2","key":"636_CR11","first-page":"64","volume":"20","author":"B Mehrparavar","year":"2019","unstructured":"Mehrparavar B, Minai-Tehrani A, Arjmand B, Gilany K. Metabolomics of male infertility: a new tool for diagnostic tests. J Reprod Infertil. 2019;20(2):64\u20139.","journal-title":"J Reprod Infertil"},{"key":"636_CR12","doi-asserted-by":"publisher","first-page":"106354","DOI":"10.1016\/j.anireprosci.2020.106354","volume":"220","author":"JA Long","year":"2020","unstructured":"Long JA. The \u201comics\u201d revolution: use of genomic, transcriptomic, proteomic and metabolomic tools to predict male reproductive traits that impact fertility in livestock and poultry. Anim Reprod Sci. 2020;220:106354. https:\/\/doi.org\/10.1016\/j.anireprosci.2020.106354.","journal-title":"Anim Reprod Sci"},{"issue":"2","key":"636_CR13","doi-asserted-by":"publisher","DOI":"10.1111\/and.13711","volume":"53","author":"MK Panner Selvam","year":"2021","unstructured":"Panner Selvam MK, Finelli R, Agarwal A, Henkel R. Proteomics and metabolomics - current and future perspectives in clinical andrology. Andrologia. 2021;53(2):e13711. https:\/\/doi.org\/10.1111\/and.13711.","journal-title":"Andrologia"},{"issue":"6","key":"636_CR14","doi-asserted-by":"publisher","first-page":"609","DOI":"10.1111\/and.12496","volume":"48","author":"A Minai-Tehrani","year":"2016","unstructured":"Minai-Tehrani A, Jafarzadeh N, Gilany K. Metabolomics: a state-of-the-art technology for better understanding of male infertility. Andrologia. 2016;48(6):609\u201316. https:\/\/doi.org\/10.1111\/and.12496.","journal-title":"Andrologia"},{"issue":"2","key":"636_CR15","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1093\/bib\/bbl012","volume":"7","author":"V Shulaev","year":"2006","unstructured":"Shulaev V. Metabolomics technology and bioinformatics. Brief Bioinform. 2006;7(2):128\u201339. https:\/\/doi.org\/10.1093\/bib\/bbl012.","journal-title":"Brief Bioinform"},{"issue":"1","key":"636_CR16","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1530\/jrf.0.0970051","volume":"97","author":"S Hamamah","year":"1993","unstructured":"Hamamah S, Seguin F, Barthelemy C, Akoka S, Le Pape A, Lansac J, et al. 1H nuclear magnetic resonance studies of seminal plasma from fertile and infertile men. J Reprod Fertil. 1993;97(1):51\u20135. https:\/\/doi.org\/10.1530\/jrf.0.0970051.","journal-title":"J Reprod Fertil"},{"issue":"8","key":"636_CR17","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0181115","volume":"12","author":"S Qiao","year":"2017","unstructured":"Qiao S, Wu W, Chen M, Tang Q, Xia Y, Jia W, et al. Seminal plasma metabolomics approach for the diagnosis of unexplained male infertility. PLoS One. 2017;12(8):1\u201313. https:\/\/doi.org\/10.1371\/journal.pone.0181115.","journal-title":"PLoS One"},{"issue":"2","key":"636_CR18","doi-asserted-by":"publisher","first-page":"450","DOI":"10.1111\/andr.12707","volume":"8","author":"A Mumcu","year":"2020","unstructured":"Mumcu A, Karaer A, Dogan B, Tuncay G. Metabolomics analysis of seminal plasma in patients with idiopathic Oligoasthenoteratozoospermia using high-resolution NMR spectroscopy. Andrology. 2020;8(2):450\u20136. https:\/\/doi.org\/10.1111\/andr.12707.","journal-title":"Andrology"},{"key":"636_CR19","doi-asserted-by":"publisher","first-page":"112888","DOI":"10.1016\/j.jpba.2019.112888","volume":"177","author":"Y Xu","year":"2020","unstructured":"Xu Y, Lu H, Wang Y, Zhang Z, Wu Q. Comprehensive metabolic profiles of seminal plasma with different forms of male infertility and their correlation with sperm parameters. J Pharm Biomed Anal. 2020;177:112888. https:\/\/doi.org\/10.1016\/j.jpba.2019.112888.","journal-title":"J Pharm Biomed Anal"},{"issue":"1","key":"636_CR20","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1111\/rda.13861","volume":"56","author":"ZY Ting","year":"2021","unstructured":"Ting ZY, Liu Y, Lin LH, Qian XQ, Hua LZ, Gang WX. Metabolomic differences of seminal plasma between boars with high and low average conception rates after artificial insemination. Reprod Domest Anim. 2021;56(1):161\u201371. https:\/\/doi.org\/10.1111\/rda.13861.","journal-title":"Reprod Domest Anim"},{"issue":"2","key":"636_CR21","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1002\/mrd.22450","volume":"82","author":"A Kumar","year":"2015","unstructured":"Kumar A, Kroetsch T, Blondin P, Anzar M. Fertility-associated metabolites in bull seminal plasma and blood serum: 1H nuclear magnetic resonance analysis. Mol Reprod Dev. 2015;82(2):123\u201331. https:\/\/doi.org\/10.1002\/mrd.22450.","journal-title":"Mol Reprod Dev"},{"issue":"4","key":"636_CR22","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0195279","volume":"13","author":"ALC Velho","year":"2018","unstructured":"Velho ALC, Menezes E, Dinh T, Kaya A, Topper E, Moura AA, et al. Metabolomic markers of fertility in bull seminal plasma. PLoS One. 2018;13(4):e0195279. https:\/\/doi.org\/10.1371\/journal.pone.0195279.","journal-title":"PLoS One"},{"issue":"12","key":"636_CR23","doi-asserted-by":"publisher","first-page":"4327","DOI":"10.2527\/jas.2012-5040","volume":"90","author":"MLWJ Broekhuijse","year":"2012","unstructured":"Broekhuijse MLWJ, \u0160o\u0161tari\u0107 E, Feitsma H, Gadella BM. Relationship of flow cytometric sperm integrity assessments with boar fertility performance under optimized field conditions. J Anim Sci. 2012;90(12):4327\u201336. https:\/\/doi.org\/10.2527\/jas.2012-5040.","journal-title":"J Anim Sci"},{"key":"636_CR24","volume-title":"Rstanarm: Bayesian applied regression modeling via Stan","author":"B Goodrich","year":"2020","unstructured":"Goodrich B, Gabry J, Ali I, Brilleman S. Rstanarm: Bayesian applied regression modeling via Stan. 2020. Available from: https:\/\/mc-stan.org\/rstanarm\/"},{"key":"636_CR25","doi-asserted-by":"publisher","first-page":"e1005752","DOI":"10.1371\/journal.pcbi.1005752","volume":"13","author":"F Rohart","year":"2017","unstructured":"Rohart F, Gautier B, Singh A, L\u00ea Cao K-A. mixOmics: An R package for \u2018omics feature selection and multiple data integration. PLOS Comput Biol. 2017;13:e1005752.","journal-title":"PLOS Comput Biol"},{"issue":"1","key":"636_CR26","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1186\/1471-2105-12-77","volume":"12","author":"X Robin","year":"2011","unstructured":"Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, et al. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics. 2011;12(1):77. https:\/\/doi.org\/10.1186\/1471-2105-12-77.","journal-title":"BMC Bioinformatics"},{"issue":"1","key":"636_CR27","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1186\/1471-2105-12-253","volume":"12","author":"KA L\u00ea Cao","year":"2011","unstructured":"L\u00ea Cao KA, Boitard S, Besse P. Sparse PLS discriminant analysis: biologically relevant feature selection and graphical displays for multiclass problems. BMC Bioinformatics. 2011;12(1):253. https:\/\/doi.org\/10.1186\/1471-2105-12-253.","journal-title":"BMC Bioinformatics."},{"key":"636_CR28","doi-asserted-by":"crossref","unstructured":"Emwas AH, Roy R, McKay RT, Tenori L, Saccenti E, Nagana Gowda GA, et al. NMR spectroscopy for metabolomics research. Metabolites. 2019;9(7):123.","DOI":"10.3390\/metabo9070123"},{"key":"636_CR29","doi-asserted-by":"publisher","unstructured":"Mateo-Otero Y, Fern\u00e1ndez-L\u00f3pez P, Ribas-Maynou J, Roca J, Mir\u00f3 J, Yeste M, et al. Metabolite profiling of pig seminal plasma identifies potential biomarkers for sperm resilience to liquid preservation. Front cell Dev Biol. 2021;9:669974. https:\/\/doi.org\/10.3389\/fcell.2021.669974.","DOI":"10.3389\/fcell.2021.669974"},{"issue":"1","key":"636_CR30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12864-019-6074-6","volume":"20","author":"EB Menezes","year":"2019","unstructured":"Menezes EB, Velho ALC, Santos F, Dinh T, Kaya A, Topper E, et al. Uncovering sperm metabolome to discover biomarkers for bull fertility. BMC Genomics. 2019;20(1):1\u201316. https:\/\/doi.org\/10.1186\/s12864-019-6074-6.","journal-title":"BMC Genomics"},{"issue":"2","key":"636_CR31","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1095\/biolreprod.116.140707","volume":"95","author":"CR Darr","year":"2016","unstructured":"Darr CR, Varner DD, Teague S, Cortopassi GA, Datta S, Meyers SA. Lactate and pyruvate are major sources of energy for stallion sperm with dose effects on mitochondrial function, motility, and ROS production. Biol Reprod. 2016;95(2):34. https:\/\/doi.org\/10.1095\/biolreprod.116.140707.","journal-title":"Biol Reprod"},{"issue":"s2","key":"636_CR32","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1111\/j.1439-0531.2006.00765.x","volume":"41","author":"J Rodriguez-Gil","year":"2006","unstructured":"Rodriguez-Gil J. Mammalian sperm energy resources management and survival during conservation in refrigeration. Reprod Domest Anim. 2006;41(s2):11\u201320. https:\/\/doi.org\/10.1111\/j.1439-0531.2006.00765.x.","journal-title":"Reprod Domest Anim"},{"issue":"3","key":"636_CR33","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1016\/j.bbrc.2015.04.128","volume":"462","author":"G Paventi","year":"2015","unstructured":"Paventi G, Lessard C, Bailey JL, Passarella S. In boar sperm capacitation L-lactate and succinate, but not pyruvate and citrate, contribute to the mitochondrial membrane potential increase as monitored via safranine O fluorescence. Biochem Biophys Res Commun. 2015;462(3):257\u201362. https:\/\/doi.org\/10.1016\/j.bbrc.2015.04.128.","journal-title":"Biochem Biophys Res Commun"},{"issue":"1","key":"636_CR34","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1530\/jrf.0.0020042","volume":"2","author":"JG Aalbers","year":"1961","unstructured":"Aalbers JG, Mann T, Polge C. Metabolism of boar semen in relation to sperm motility and survival. J Reprod Fertil. 1961;2(1):42\u201353. https:\/\/doi.org\/10.1530\/jrf.0.0020042.","journal-title":"J Reprod Fertil"},{"issue":"3","key":"636_CR35","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1002\/mrd.20414","volume":"73","author":"A Medrano","year":"2006","unstructured":"Medrano A, Fern\u00e1ndez-Novell JM, Rami\u00f3 L, Alvarez J, Goldberg E, Rivera MM, et al. Utilization of citrate and lactate through a lactate dehydrogenase and ATP-regulated pathway in boar spermatozoa. Mol Reprod Dev. 2006;73(3):369\u201378. https:\/\/doi.org\/10.1002\/mrd.20414.","journal-title":"Mol Reprod Dev"},{"issue":"1","key":"636_CR36","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1016\/j.jpba.2010.07.021","volume":"54","author":"A Gupta","year":"2011","unstructured":"Gupta A, Mahdi AA, Ahmad MK, Shukla KK, Jaiswer SP, Shankhwar SN. 1H NMR spectroscopic studies on human seminal plasma: a probative discriminant function analysis classification model. J Pharm Biomed Anal. 2011;54(1):106\u201313. https:\/\/doi.org\/10.1016\/j.jpba.2010.07.021.","journal-title":"J Pharm Biomed Anal"},{"issue":"1","key":"636_CR37","doi-asserted-by":"publisher","first-page":"208","DOI":"10.1016\/j.jep.2013.06.024","volume":"149","author":"A Gupta","year":"2013","unstructured":"Gupta A, Mahdi AA, Shukla KK, Ahmad MK, Bansal N, Sankhwar P, et al. Efficacy of Withania somnifera on seminal plasma metabolites of infertile males: a proton NMR study at 800 MHz. J Ethnopharmacol. 2013;149(1):208\u201314. https:\/\/doi.org\/10.1016\/j.jep.2013.06.024.","journal-title":"J Ethnopharmacol"},{"issue":"5-6","key":"636_CR38","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1387\/ijdb.072522bs","volume":"52","author":"BT Storey","year":"2008","unstructured":"Storey BT. Mammalian sperm metabolism: Oxygen and sugar, friend and foe. Int J Dev Biol. 2008;52(5-6):427\u201337. https:\/\/doi.org\/10.1387\/ijdb.072522bs.","journal-title":"Int J Dev Biol"},{"issue":"1","key":"636_CR39","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1530\/jrf.0.0630109","volume":"63","author":"RHF Hunter","year":"1981","unstructured":"Hunter RHF. Sperm transport and reservoirs in the pig oviduct in relation to the time of ovulation. J Reprod Fertil. 1981;63(1):109\u201317. https:\/\/doi.org\/10.1530\/jrf.0.0630109.","journal-title":"J Reprod Fertil"},{"key":"636_CR40","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/j.jprot.2013.05.029","volume":"91","author":"X Druart","year":"2013","unstructured":"Druart X, Rickard JP, Mactier S, Kohnke PL, Kershaw-Young CM, Bathgate R, et al. Proteomic characterization and cross species comparison of mammalian seminal plasma. J Proteome. 2013;91:13\u201322. https:\/\/doi.org\/10.1016\/j.jprot.2013.05.029.","journal-title":"J Proteome"},{"issue":"5","key":"636_CR41","doi-asserted-by":"publisher","first-page":"1437","DOI":"10.1095\/biolreprod.104.029041","volume":"71","author":"JL Albarrac\u00edn","year":"2004","unstructured":"Albarrac\u00edn JL, Fern\u00e1ndez-Novell JM, Ballester J, Rauch MC, Quintero-Moreno A, Pe\u00f1a A, et al. Gluconeogenesis-linked glycogen metabolism is important in the achievement of in vitro capacitation of dog spermatozoa in a medium without glucose. Biol Reprod. 2004;71(5):1437\u201345. https:\/\/doi.org\/10.1095\/biolreprod.104.029041.","journal-title":"Biol Reprod"},{"issue":"4","key":"636_CR42","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1002\/j.1939-4640.2001.tb02229.x","volume":"22","author":"AC Williams","year":"2001","unstructured":"Williams AC, Ford WCL. The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl. 2001;22(4):680\u201395.","journal-title":"J Androl"},{"issue":"2","key":"636_CR43","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1093\/humupd\/2.2.87","volume":"2","author":"C Jeulin","year":"1996","unstructured":"Jeulin C, Lewin LM. Role of free L-carnitine and acetyl-L-carnitine in post-gonadal maturation of mammalian spermatozoa. Hum Reprod Update. 1996;2(2):87\u2013102. https:\/\/doi.org\/10.1093\/humupd\/2.2.87.","journal-title":"Hum Reprod Update"},{"key":"636_CR44","unstructured":"Chavoshi Nezhad N, Vahabzadeh Z, Allahveisie A, Rahmani K, Raoofi A, Rezaie MJ, et al. The effect of L-carnitine and coenzyme Q10 on the sperm motility, DNA fragmentation, chromatin structure and oxygen free radicals during, before and after freezing in Oligospermia men. Urol J. 2021;18(3):330\u20136."},{"key":"636_CR45","doi-asserted-by":"publisher","unstructured":"Naderi Noreini S, Malmir M, Ghafarizadeh A, Faraji T, Bayat R. Protective effect of L-carnitine on apoptosis, DNA fragmentation, membrane integrity and lipid peroxidation of spermatozoa in the asthenoteratospermic men. Andrologia. 2020;53(2):e13932. https:\/\/doi.org\/10.1111\/and.13932.","DOI":"10.1111\/and.13932"},{"issue":"11","key":"636_CR46","doi-asserted-by":"publisher","first-page":"1763","DOI":"10.5713\/ajas.19.0455","volume":"33","author":"K Yang","year":"2020","unstructured":"Yang K, Wang N, Guo HT, Wang JR, Sun HH, Sun LZ, et al. Effect of L-carnitine on sperm quality during liquid storage of boar semen. Asian-Australasian J Anim Sci. 2020;33(11):1763\u20139. https:\/\/doi.org\/10.5713\/ajas.19.0455.","journal-title":"Asian-Australasian J Anim Sci"},{"issue":"5","key":"636_CR47","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1016\/j.theriogenology.2009.10.013","volume":"73","author":"M Yeste","year":"2010","unstructured":"Yeste M, Sancho S, Briz M, Pinart E, Bussalleu E, Bonet S. A diet supplemented with l-carnitine improves the sperm quality of Pi\u00e9train but not of Duroc and large white boars when photoperiod and temperature increase. Theriogenology. 2010;73(5):577\u201386. https:\/\/doi.org\/10.1016\/j.theriogenology.2009.10.013.","journal-title":"Theriogenology."},{"issue":"7-8","key":"636_CR48","doi-asserted-by":"publisher","first-page":"1247","DOI":"10.1016\/j.theriogenology.2003.07.022","volume":"61","author":"DM Kozink","year":"2004","unstructured":"Kozink DM, Estienne MJ, Harper AF, Knight JW. Effects of dietary L-carnitine supplementation on semen characteristics in boars. Theriogenology. 2004;61(7-8):1247\u201358. https:\/\/doi.org\/10.1016\/j.theriogenology.2003.07.022.","journal-title":"Theriogenology."},{"issue":"4","key":"636_CR49","doi-asserted-by":"publisher","first-page":"840","DOI":"10.1093\/humrep\/15.4.840","volume":"15","author":"A Z\u00f6pfgen","year":"2000","unstructured":"Z\u00f6pfgen A, Priem F, Sudhoff F, Jung K, Lenk S, Loening SA, et al. Relationship between semen quality and the seminal plasma components carnitine, alpha-glucosidase, fructose, citrate and granulocyte elastase in infertile men compared with a normal population. Hum Reprod. 2000;15(4):840\u20135. https:\/\/doi.org\/10.1093\/humrep\/15.4.840.","journal-title":"Hum Reprod"},{"issue":"3","key":"636_CR50","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1002\/j.1939-4640.1992.tb00317.x","volume":"13","author":"RP Holmes","year":"1992","unstructured":"Holmes RP, Goodman HO, Shihabi ZK, Jarow JP. The taurine and Hypotaurine content of human semen. J Androl. 1992;13(3):289\u201392.","journal-title":"J Androl"},{"key":"636_CR51","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.cryobiol.2019.07.004","volume":"90","author":"M Seify","year":"2019","unstructured":"Seify M, Zarabadipour M, Ghaleno LR, Alizadeh AR, Rezazadeh VM. The anti-oxidant roles of taurine and Hypotaurine on acrosome integrity, HBA and HSPA2 of the human sperm during vitrification and post warming in two different temperature. Cryobiology. 2019;90:89\u201395. https:\/\/doi.org\/10.1016\/j.cryobiol.2019.07.004.","journal-title":"Cryobiology"},{"issue":"5","key":"636_CR52","doi-asserted-by":"publisher","first-page":"1060","DOI":"10.1016\/j.theriogenology.2006.12.004","volume":"67","author":"MN Bucak","year":"2007","unstructured":"Bucak MN, Ate\u015f\u015fahin A, Vari\u015fli \u00d6, Y\u00fcce A, Tekin N, Ak\u00e7ay A. The influence of trehalose, taurine, cysteamine and hyaluronan on ram semen. Microscopic and oxidative stress parameters after freeze-thawing process. Theriogenology. 2007;67(5):1060\u20137. https:\/\/doi.org\/10.1016\/j.theriogenology.2006.12.004.","journal-title":"Theriogenology"},{"issue":"8","key":"636_CR53","doi-asserted-by":"publisher","first-page":"2045","DOI":"10.1093\/humrep\/det253","volume":"28","author":"F Brugnon","year":"2013","unstructured":"Brugnon F, Ouchchane L, Pons-Rejraji H, Artonne C, Farigoule M, Janny L. Density gradient centrifugation prior to cryopreservation and hypotaurine supplementation improve post-thaw quality of sperm from infertile men with oligoasthenoteratozoospermia. Hum Reprod. 2013;28(8):2045\u201357. https:\/\/doi.org\/10.1093\/humrep\/det253.","journal-title":"Hum Reprod"},{"issue":"6","key":"636_CR54","doi-asserted-by":"publisher","first-page":"692","DOI":"10.1002\/mrd.23354","volume":"87","author":"KK Saraf","year":"2020","unstructured":"Saraf KK, Kumaresan A, Dasgupta M, Karthikkeyan G, Prasad TSK, Modi PK, et al. Metabolomic fingerprinting of bull spermatozoa for identification of fertility signature metabolites. Mol Reprod Dev. 2020;87(6):692\u2013703. https:\/\/doi.org\/10.1002\/mrd.23354.","journal-title":"Mol Reprod Dev"},{"issue":"3","key":"636_CR55","doi-asserted-by":"publisher","first-page":"689","DOI":"10.1016\/0093-691X(94)90178-L","volume":"41","author":"GF Miller","year":"1994","unstructured":"Miller GF, Gliedt DW, Rakes JM, Rorie RW. Addition of penicillamine, hypotaurine and epinephrine (PHE) or bovine oviductal epithelial cells (BOEC) alone or in combination to bovine in vitro fertilization medium increases the subsequent embryo cleavage rate. Theriogenology. 1994;41(3):689\u201396. https:\/\/doi.org\/10.1016\/0093-691X(94)90178-L.","journal-title":"Theriogenology."},{"issue":"4","key":"636_CR56","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1017\/S0967199407004273","volume":"15","author":"C Suzuki","year":"2007","unstructured":"Suzuki C, Yoshioka K, Sakatani M, Takahashi M. Glutamine and hypotaurine improves intracellular oxidative status and in vitro development of porcine preimplantation embryos. Zygote. 2007;15(4):317\u201324. https:\/\/doi.org\/10.1017\/S0967199407004273.","journal-title":"Zygote"},{"issue":"6","key":"636_CR57","doi-asserted-by":"publisher","first-page":"803","DOI":"10.1530\/REP-20-0181","volume":"160","author":"JM Ortiz-Rodr\u00edguez","year":"2020","unstructured":"Ortiz-Rodr\u00edguez JM, Mart\u00edn-Cano FE, Gaitskell-Phillips G, Silva A, Tapia JA, Gil MC, et al. The SLC7A11: sperm mitochondrial function and non-canonical glutamate metabolism. Reproduction. 2020;160(6):803\u201318. https:\/\/doi.org\/10.1530\/REP-20-0181.","journal-title":"Reproduction."},{"issue":"12","key":"636_CR58","doi-asserted-by":"publisher","first-page":"1886","DOI":"10.1016\/j.biochi.2010.08.015","volume":"28","author":"SR Zanetti","year":"2010","unstructured":"Zanetti SR, Monclus MDL\u00c1, Rensetti DE, Forn\u00e9s MW, Avelda\u00f1o MI. Differential involvement of rat sperm choline glycerophospholipids and sphingomyelin in capacitation and the acrosomal reaction. Enferm Infecc Microbiol Clin. 2010;28(12):1886\u201394. https:\/\/doi.org\/10.1016\/j.biochi.2010.08.015.","journal-title":"Enferm Infecc Microbiol Clin"},{"key":"636_CR59","doi-asserted-by":"publisher","unstructured":"Mieusset R, Bujan L, Mansat AFP, Grandjean H, chap H. Glycerophosphocholine in seminal plasma of fertile and infertile men. Int J Androl. 1988;11(5):405\u201313. https:\/\/doi.org\/10.1111\/j.1365-2605.1988.tb01013.x.","DOI":"10.1111\/j.1365-2605.1988.tb01013.x"},{"key":"636_CR60","doi-asserted-by":"crossref","unstructured":"Akram M. Citric acid cycle and role of its Intermediates in metabolism. Cell Biochem Biophys. 2014;68:475\u20138.","DOI":"10.1007\/s12013-013-9750-1"},{"issue":"1","key":"636_CR61","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1093\/humrep\/13.1.132","volume":"13","author":"S Hamamah","year":"1998","unstructured":"Hamamah S, Seguin F, Bujan L, Barthelemy C, Mieusset R, Lansac J. Quantification by magnetic resonance spectroscopy of metabolites in seminal plasma able to differentiate different forms of azoospermia. Hum Reprod. 1998;13(1):132\u20135. https:\/\/doi.org\/10.1093\/humrep\/13.1.132.","journal-title":"Hum Reprod"},{"issue":"6","key":"636_CR62","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1093\/humrep\/dey081","volume":"33","author":"T Umehara","year":"2018","unstructured":"Umehara T, Kawai T, Goto M, Richards JS, Shimada M. Creatine enhances the duration of sperm capacitation: a novel factor for improving in vitro fertilization with small numbers of sperm. Hum Reprod. 2018;33(6):1117\u201329. https:\/\/doi.org\/10.1093\/humrep\/dey081.","journal-title":"Hum Reprod"},{"issue":"09\/2020","key":"636_CR63","doi-asserted-by":"publisher","first-page":"1751","DOI":"10.7754\/Clin.Lab.2020.191248","volume":"66","author":"F Nasrallah","year":"2020","unstructured":"Nasrallah F, Hammami MB, Omar S, Aribia H, Sanhaji H, Feki M. Semen creatine and creatine kinase activity as an indicator of sperm quality. Clin Lab. 2020;66(09\/2020):1751\u20137. https:\/\/doi.org\/10.7754\/Clin.Lab.2020.191248.","journal-title":"Clin Lab"},{"issue":"6","key":"636_CR64","doi-asserted-by":"publisher","first-page":"1549S","DOI":"10.1093\/jn\/137.6.1549S","volume":"137","author":"DE Matthews","year":"2007","unstructured":"Matthews DE. An overview of phenylalanine and tyrosine kinetics in humans. J Nutr. 2007;137(6):1549S\u201355S. https:\/\/doi.org\/10.1093\/jn\/137.6.1549S.","journal-title":"J Nutr"},{"issue":"6","key":"636_CR65","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1530\/REP-14-0621","volume":"149","author":"B Houston","year":"2015","unstructured":"Houston B, Curry B, Aitken RJ. Human spermatozoa possess an IL4I1 L-amino acid oxidase with a potential role in sperm function. Reproduction. 2015;149(6):587\u201396. https:\/\/doi.org\/10.1530\/REP-14-0621.","journal-title":"Reproduction."},{"key":"636_CR66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fcell.2019.00347","volume":"7","author":"MR Ugur","year":"2020","unstructured":"Ugur MR, Dinh T, Hitit M, Kaya A, Topper E, Didion B, et al. Amino acids of seminal plasma associated with freezability of bull sperm. Front Cell Dev Biol. 2020;7:1\u201314. https:\/\/doi.org\/10.3389\/fcell.2019.00347.","journal-title":"Front Cell Dev Biol"},{"issue":"2","key":"636_CR67","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/S0009-2797(00)00179-4","volume":"127","author":"FWPC Van Overveld","year":"2000","unstructured":"Van Overveld FWPC, Haenen GRMM, Rhemrev J, Vermeiden JPW, Bast A. Tyrosine as important contributor to the antioxidant capacity of seminal plasma. Chem Biol Interact. 2000;127(2):151\u201361. https:\/\/doi.org\/10.1016\/S0009-2797(00)00179-4.","journal-title":"Chem Biol Interact"},{"issue":"8","key":"636_CR68","doi-asserted-by":"publisher","first-page":"1086","DOI":"10.1016\/j.bbabio.2016.03.012","volume":"2016","author":"L Tretter","year":"1857","unstructured":"Tretter L, Patocs A, Chinopoulos C. Succinate, an intermediate in metabolism, signal transduction, ROS, hypoxia, and tumorigenesis. Biochim Biophys Acta Bioenerg. 1857;2016(8):1086\u2013101. https:\/\/doi.org\/10.1016\/j.bbabio.2016.03.012.","journal-title":"Biochim Biophys Acta Bioenerg"},{"key":"636_CR69","doi-asserted-by":"crossref","unstructured":"Bowman CE, Wolfgang MJ. Role of the malonyl-CoA synthetase ACSF3 in mitochondrial metabolism. Adv. Biol. Regul. 2019;71:34\u201340.","DOI":"10.1016\/j.jbior.2018.09.002"},{"issue":"9","key":"636_CR70","doi-asserted-by":"publisher","first-page":"1195","DOI":"10.1007\/s10815-014-0282-4","volume":"31","author":"V Jayaraman","year":"2014","unstructured":"Jayaraman V, Ghosh S, Sengupta A, Srivastava S, Sonawat HM, Narayan PK. Identification of biochemical differences between different forms of male infertility by nuclear magnetic resonance (NMR) spectroscopy. J Assist Reprod Genet. 2014;31(9):1195\u2013204. https:\/\/doi.org\/10.1007\/s10815-014-0282-4.","journal-title":"J Assist Reprod Genet"},{"issue":"12","key":"636_CR71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1074\/mcp.M111.012658","volume":"10","author":"C Peng","year":"2011","unstructured":"Peng C, Lu Z, Xie Z, Cheng Z, Chen Y, Tan M, et al. The first identification of lysine malonylation substrates and its regulatory enzyme. Mol Cell Proteomics. 2011;10(12):1\u201312. https:\/\/doi.org\/10.1074\/mcp.M111.012658.","journal-title":"Mol Cell Proteomics"},{"issue":"5","key":"636_CR72","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1016\/j.tibtech.2004.03.007","volume":"22","author":"R Goodacre","year":"2004","unstructured":"Goodacre R, Vaidyanathan S, Dunn WB, Harrigan GG, Kell DB. Metabolomics by numbers: acquiring and understanding global metabolite data. Trends Biotechnol. 2004;22(5):245\u201352. https:\/\/doi.org\/10.1016\/j.tibtech.2004.03.007.","journal-title":"Trends Biotechnol"}],"container-title":["Journal of Animal Science and Biotechnology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40104-021-00636-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s40104-021-00636-5\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40104-021-00636-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,11]],"date-time":"2024-09-11T21:00:15Z","timestamp":1726088415000},"score":1,"resource":{"primary":{"URL":"https:\/\/jasbsci.biomedcentral.com\/articles\/10.1186\/s40104-021-00636-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,12]]},"references-count":72,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["636"],"URL":"https:\/\/doi.org\/10.1186\/s40104-021-00636-5","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-510687\/v1","asserted-by":"object"}]},"ISSN":["2049-1891"],"issn-type":[{"value":"2049-1891","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,12]]},"assertion":[{"value":"9 May 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 September 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 November 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Ethical review and approval for animal participants was not required as samples were provided by the AI-Centre and authors did not manipulate any animals.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"113"}}