{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,28]],"date-time":"2026-04-28T22:55:58Z","timestamp":1777416958808,"version":"3.51.4"},"reference-count":46,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2014,6,1]],"date-time":"2014-06-01T00:00:00Z","timestamp":1401580800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":["rep.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2014,6,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>We have applied the mitochondria-specific superoxide fluorescent probe MitoSOX Red (MitoSOX) to detect mitochondria-specific reactive oxygen species (mROS) production in human sperm samples using flow cytometry. We show that human ejaculates are heterogeneous in terms of mROS production, with three subpopulations clearly detectable, comprising sperm that produce increasing amounts of mROS (MitoSOX\u2212, MitoSOX+, and MitoSOX++). The sperm subpopulation producing the lowest amount of mROS represented the most functional subset of male gametes within the ejaculate, as it was correlated with the highest amount of live and non-apoptotic sperm and increased both in samples with better semen parameters and in samples processed by both density-gradient centrifugation and swim-up, both known to select for higher quality sperm. Importantly, the MitoSOX\u2212 subpopulation was clearly more prevalent in samples that gave rise to pregnancies following assisted reproduction. Our work, therefore, not only describe discreet human sperm heterogeneity at the mROS level but also suggests that mROS may represent a strategy to both evaluate sperm samples and isolate the most functional gametes for assisted reproduction.<\/jats:p>\n                  <jats:p>Free Portuguese abstract<\/jats:p>\n                  <jats:p>A Portuguese translation of this abstract is freely available at http:\/\/www.reproduction-online.org\/content\/147\/6\/817\/suppl\/DC1<\/jats:p>","DOI":"10.1530\/rep-13-0644","type":"journal-article","created":{"date-parts":[[2014,2,17]],"date-time":"2014-02-17T23:46:40Z","timestamp":1392680800000},"page":"817-824","update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-1","source":"Crossref","is-referenced-by-count":24,"title":["Low amounts of mitochondrial reactive oxygen species define human sperm quality"],"prefix":"10.1093","volume":"147","author":[{"given":"M\u00f3nica","family":"Marques","sequence":"first","affiliation":[{"name":"Biology of Reproduction and Stem Cell Group \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Human Reproduction Service \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Portuguese Institute for Blood and Transplantation \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Faculty of Medicine \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Department of Life Sciences \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"}]},{"given":"Ana Paula","family":"Sousa","sequence":"additional","affiliation":[{"name":"Biology of Reproduction and Stem Cell Group \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Human Reproduction Service \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Portuguese Institute for Blood and Transplantation \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Faculty of Medicine \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Department of Life Sciences \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"}]},{"given":"Artur","family":"Paiva","sequence":"additional","affiliation":[{"name":"Biology of Reproduction and Stem Cell Group \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Human Reproduction Service \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Portuguese Institute for Blood and Transplantation \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Faculty of Medicine \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Department of Life Sciences \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"}]},{"given":"Teresa","family":"Almeida-Santos","sequence":"additional","affiliation":[{"name":"Biology of Reproduction and Stem Cell Group \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Human Reproduction Service \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Portuguese Institute for Blood and Transplantation \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Faculty of Medicine \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Department of Life Sciences \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"}]},{"given":"Jo\u00e3o","family":"Ramalho-Santos","sequence":"additional","affiliation":[{"name":"Biology of Reproduction and Stem Cell Group \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Human Reproduction Service \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Portuguese Institute for Blood and Transplantation \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Faculty of Medicine \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"},{"name":"Department of Life Sciences \u00a0 CNC\u2013Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal 2 \u00a0 University Hospitals of Coimbra, Pr. Mota Pinto, Ed. S\u00e3o Jer\u00f3nimo, 3000-075 Coimbra, Portugal 3 \u00a0 Coimbra, Portugal 4 \u00a0 University of Coimbra, Coimbra, Portugal 5 \u00a0 University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal"}]}],"member":"286","published-online":{"date-parts":[[2014,6,1]]},"reference":[{"key":"2026010712273314900_bib1","doi-asserted-by":"crossref","first-page":"157","DOI":"10.3109\/01485019408987819","article-title":"Effect of sperm washing on levels of reactive oxygen species in semen","volume":"33","author":"Agarwal","year":"1994","journal-title":"Archives of Andrology"},{"key":"2026010712273314900_bib2","doi-asserted-by":"crossref","first-page":"169","DOI":"10.3109\/01485019408987783","article-title":"Levels of reactive oxygen species before and after sperm preparation \u2013 comparison of swim-up and L4 Filtration","volume":"32","author":"Agarwal","year":"1994","journal-title":"Archives of 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