Tropical summer induces DNA fragmentation in boar spermatozoa: implications for evaluating seasonal infertility
Santiago T. Peña
A B C , Felicity Stone A , Bruce Gummow B D , Anthony J. Parker E and Damien B. B. P. Paris A F G
+ Author Affiliations
- Author Affiliations
A Discipline of Biomedical Science, College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Qld 4811, Australia.
B Discipline of Veterinary Science, College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Qld 4811, Australia.
C College of Veterinary Medicine, Visayas State University, Baybay City, Leyte, Philippines.
D Faculty of Veterinary Science, University of Pretoria, Onderstepoort, 0110, South Africa.
E College of Food, Agricultural and Environmental Sciences, Ohio State University, Wooster, OH 44691, USA.
F Centre for Tropical Environmental and Sustainability Science, James Cook University, Townsville, Qld 4811, Australia.
G Corresponding author. Email: damien.paris@jcu.edu.au
Reproduction, Fertility and Development 31(3) 590-601 https://doi.org/10.1071/RD18159
Journal Compilation © CSIRO 2018 Open Access CC BY-NC-ND
Abstract
Summer infertility continues to undermine pig productivity, costing the pig industry millions in annual losses. The boar’s inefficient capacity to sweat, non-pendulous scrotum and the extensive use of European breeds in tropical conditions, can make the boar particularly vulnerable to the effects of heat stress; however, the link between summer heat stress and boar sperm DNA damage has not yet been demonstrated. Semen from five Large White boars was collected and evaluated during the early dry, late dry and peak wet seasons to determine the effect of seasonal heat stress on the quality and DNA integrity of boar spermatozoa. DNA damage in spermatozoa during the peak wet was 16-fold greater than during the early dry and nearly 9-fold greater than during the late dry season. Sperm concentration was 1.6-fold lower in the peak wet than early dry whereas no difference was found across several motility parameters as determined by computer-assisted sperm analysis. These results demonstrate that tropical summer (peak wet season) induces DNA damage and reduces concentration without depressing motility in boar spermatozoa, suggesting that traditional methods of evaluating sperm motility may not detect inherently compromised spermatozoa. Boar management strategies (such as antioxidant supplementation) need to be developed to specifically mitigate this problem.
Additional keywords: DNA damage, heat stress, oxidative stress, pig, summer infertility, TUNEL.
References
Ahmadi, A., and Ng, S. C. (1999). Fertilizing ability of DNA-damaged spermatozoa. J. Exp. Zool. 284, 696–704.| Fertilizing ability of DNA-damaged spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Alexandratos, N., and Bruinsma, J. (2012) ‘World Agriculture Towards 2030/2050: The 2012 Revision’. (Food and Agriculture Organization of the United Nations: Rome.)
Alkmin, D. V., Martinez-Alborcia, M. J., Parrilla, I., Vazquez, J. M., Martinez, E. A., and Roca, J. (2013). The nuclear DNA longevity in cryopreserved boar spermatozoa assessed using the sperm-sus-halomax. Theriogenology 79, 1294–1300.
| The nuclear DNA longevity in cryopreserved boar spermatozoa assessed using the sperm-sus-halomax.Crossref | GoogleScholarGoogle Scholar |
Argenti, L. E., Parmeggiani, B. S., Leipnitz, G., Weber, A., Pereira, G. R., and Bustamante-Filho, I. C. (2018). Effects of season on boar semen parameters and antioxidant enzymes in the south subtropical region in Brazil. Andrologia , .
| Effects of season on boar semen parameters and antioxidant enzymes in the south subtropical region in Brazil.Crossref | GoogleScholarGoogle Scholar |
Auvigne, V., Leneveu, P., Jehannin, C., Peltoniemi, O., and Sallé, E. (2010). Seasonal infertility in sows: A five year field study to analyze the relative roles of heat stress and photoperiod. Theriogenology 74, 60–66.
| Seasonal infertility in sows: A five year field study to analyze the relative roles of heat stress and photoperiod.Crossref | GoogleScholarGoogle Scholar |
Barranco, I., Ortega, M. D., Martinez-Alborcia, M. J., Vazquez, J. M., Martinez, E. A., and Roca, J. (2013). Season of ejaculate collection influences the freezability of boar spermatozoa. Cryobiology 67, 299–304.
| Season of ejaculate collection influences the freezability of boar spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Boe-Hansen, G. B., Ersbøll, A. K., Greve, T., and Christensen, P. (2005). Increasing storage time of extended boar semen reduces sperm DNA integrity. Theriogenology 63, 2006–2019.
| Increasing storage time of extended boar semen reduces sperm DNA integrity.Crossref | GoogleScholarGoogle Scholar |
Boe-Hansen, G. B., Christensen, P., Vibjerg, D., Nielsen, M. B., and Hedeboe, A. M. (2008). Sperm chromatin structure integrity in liquid stored boar semen and its relationships with field fertility. Theriogenology 69, 728–736.
| Sperm chromatin structure integrity in liquid stored boar semen and its relationships with field fertility.Crossref | GoogleScholarGoogle Scholar |
Boma, M. H., and Bilkei, G. (2006). Seasonal infertility in Kenyan pig breeding units. Onderstepoort J. Vet. Res. 73, 229–232.
| Seasonal infertility in Kenyan pig breeding units.Crossref | GoogleScholarGoogle Scholar |
Brahem, S., Mehdi, M., Landolsi, H., Mougou, S., Elghezal, H., and Saad, A. (2011). Semen parameters and sperm DNA fragmentation as causes of recurrent pregnancy loss. Urology 78, 792–796.
| Semen parameters and sperm DNA fragmentation as causes of recurrent pregnancy loss.Crossref | GoogleScholarGoogle Scholar |
Broekhuijse, M. L. W. J., Šoštarić, E., Feitsma, H., and Gadella, B. M. (2012a). Application of computer-assisted semen analysis to explain variations in pig fertility. J. Anim. Sci. 90, 779–789.
| Application of computer-assisted semen analysis to explain variations in pig fertility.Crossref | GoogleScholarGoogle Scholar |
Broekhuijse, M. L. W. J., Šoštarić, E., Feitsma, H., and Gadella, B. M. (2012b). The value of microscopic semen motility assessment at collection for a commercial artificial insemination center, a retrospective study on factors explaining variation in pig fertility. Theriogenology 77, 1466–1479.e3.
| The value of microscopic semen motility assessment at collection for a commercial artificial insemination center, a retrospective study on factors explaining variation in pig fertility.Crossref | GoogleScholarGoogle Scholar |
Brzezińska-Ślebodzińska, E., Ślebodziński, A., Pietras, B., and Wieczorek, G. (1995). Antioxidant effect of vitamin E and glutathione on lipid peroxidation in boar semen plasma. Biol. Trace Elem. Res. 47, 69–74.
| Antioxidant effect of vitamin E and glutathione on lipid peroxidation in boar semen plasma.Crossref | GoogleScholarGoogle Scholar |
Bureau of Meteorology (2011a) Climate of Townsville, http://www.bom.gov.au/qld/townsville/climate_Townsville.shtml [Verified 12 October 2018].
Bureau of Meteorology (2011b) About air temperature data, http://www.bom.gov.au/climate/cdo/about/about-airtemp-data.shtml [Verified 12 October 2018].
Cameron, R. D., and Blackshaw, A. W. (1980). The effect of elevated ambient temperature on spermatogenesis in the boar. J. Reprod. Fertil. 59, 173–179.
| The effect of elevated ambient temperature on spermatogenesis in the boar.Crossref | GoogleScholarGoogle Scholar |
Carrell, D. T., Liu, L., Peterson, C. M., Jones, K. P., Hatasaka, H. H., Erickson, L., and Campbell, B. (2003). Sperm DNA fragmentation is increased in couples with unexplained recurrent pregnancy loss. Arch. Androl. 49, 49–55.
| Sperm DNA fragmentation is increased in couples with unexplained recurrent pregnancy loss.Crossref | GoogleScholarGoogle Scholar |
Cerolini, S., Maldjian, A., Pizzi, F., and Gliozzi, T. (2001). Changes in sperm quality and lipid composition during cryopreservation of boar semen. Reproduction 121, 395–401.
| Changes in sperm quality and lipid composition during cryopreservation of boar semen.Crossref | GoogleScholarGoogle Scholar |
Deshmukh, R. S., Østrup, O., Østrup, E., Vejlsted, M., Niemann, H., Lucas-Hahn, A., Petersen, B., Li, J., Callesen, H., and Hyttel, P. (2011). DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer. Epigenetics 6, 177–187.
| DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar |
Didion, B. A., Kasperson, K. M., Wixon, R. L., and Evenson, D. P. (2009). Boar fertility and sperm chromatin structure status: a retrospective report. J. Androl. 30, 655–660.
| Boar fertility and sperm chromatin structure status: a retrospective report.Crossref | GoogleScholarGoogle Scholar |
Dobrinski, I., Hughes, H. P., and Barth, A. D. (1994). Flow cytometric and microscopic evaluation and effect on fertility of abnormal chromatin condensation in bovine sperm nuclei. J. Reprod. Fertil. 101, 531–538.
| Flow cytometric and microscopic evaluation and effect on fertility of abnormal chromatin condensation in bovine sperm nuclei.Crossref | GoogleScholarGoogle Scholar |
Dubé, C., Beaulieu, M., Reyes-Moreno, C., Guillemette, C., and Bailey, J. L. (2004). Boar sperm storage capacity of BTS and Androhep Plus: viability, motility, capacitation, and tyrosine phosphorylation. Theriogenology 62, 874–886.
| Boar sperm storage capacity of BTS and Androhep Plus: viability, motility, capacitation, and tyrosine phosphorylation.Crossref | GoogleScholarGoogle Scholar |
Egbunike, G. N., and Dede, T. I. (1980). The influence of short-term exposure to tropical sunlight on boar seminal characteristics. Int. J. Biometeorol. 24, 129–135.
| The influence of short-term exposure to tropical sunlight on boar seminal characteristics.Crossref | GoogleScholarGoogle Scholar |
Einarsson, S., Brandt, Y., Lundeheim, N., and Madej, A. (2008). Stress and its influence on reproduction in pigs: a review. Acta Vet. Scand. 50, 48.
| Stress and its influence on reproduction in pigs: a review.Crossref | GoogleScholarGoogle Scholar |
Eriksson, B. M., and Rodriguez-Martinez, H. (2000). Effect of freezing and thawing rates on the post-thaw viability of boar spermatozoa frozen in flatpacks and maxi-straws. Anim. Reprod. Sci. 63, 205–220.
| Effect of freezing and thawing rates on the post-thaw viability of boar spermatozoa frozen in flatpacks and maxi-straws.Crossref | GoogleScholarGoogle Scholar |
Evenson, D. P. (1999). Loss of livestock breeding efficiency due to uncompensable sperm nuclear defects. Reprod. Fertil. Dev. 11, 1–15.
| Loss of livestock breeding efficiency due to uncompensable sperm nuclear defects.Crossref | GoogleScholarGoogle Scholar |
Evenson, D. P. (2016). 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. 169, 56–75.
| The sperm chromatin structure assay (scsa®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility.Crossref | GoogleScholarGoogle Scholar |
Evenson, D. P., and Wixon, R. (2006). Clinical aspects of sperm DNA fragmentation detection and male infertility. Theriogenology 65, 979–991.
| Clinical aspects of sperm DNA fragmentation detection and male infertility.Crossref | GoogleScholarGoogle Scholar |
Evenson, D. P., Kasperson, K., Wixon, R. L., and Didion, B. A. (2009). Boar fertility and sperm chromatin structure assay defined sperm DNA fragmentation. Reprod. Fertil. Dev. 21, 212.
| Boar fertility and sperm chromatin structure assay defined sperm DNA fragmentation.Crossref | GoogleScholarGoogle Scholar |
Fernandes, C. E., Dode, M. A., Pereira, D., and Silva, A. E. (2008). Effects of scrotal insulation in Nellore bulls (Bos taurus indicus) on seminal quality and its relationship with in vitro fertilizing ability. Theriogenology 70, 1560–1568.
| Effects of scrotal insulation in Nellore bulls (Bos taurus indicus) on seminal quality and its relationship with in vitro fertilizing ability.Crossref | GoogleScholarGoogle Scholar |
Flowers, W. L. (1997). Management of boars for efficient semen production. J. Reprod. Fertil. Suppl. 52, 67–78.
França, L. R., and Cardoso, F. M. (1998). Duration of spermatogenesis and sperm transit time through the epididymis in the Piau boar. Tissue Cell 30, 573–582.
| Duration of spermatogenesis and sperm transit time through the epididymis in the Piau boar.Crossref | GoogleScholarGoogle Scholar |
França, L. R., Avelar, G. F., and Almeida, F. F. L. (2005). Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 63, 300–318.
| Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs.Crossref | GoogleScholarGoogle Scholar |
Gadea, J., Selles, E., and Marco, M. A. (2004). The predictive value of porcine seminal parameters on fertility outcome under commercial conditions. Reprod. Domest. Anim. 39, 303–308.
| The predictive value of porcine seminal parameters on fertility outcome under commercial conditions.Crossref | GoogleScholarGoogle Scholar |
García-Macías, V., de Paz, P., Martinez-Pastor, F., Álvarez, M., Gomes-Alves, S., Bernardo, J., Anel, E., and Anel, L. (2007). DNA fragmentation assessment by flow cytometry and sperm-bos-halomax (bright-field microscopy and fluorescence microscopy) in bull sperm. Int. J. Androl. 30, 88–98.
| DNA fragmentation assessment by flow cytometry and sperm-bos-halomax (bright-field microscopy and fluorescence microscopy) in bull sperm.Crossref | GoogleScholarGoogle Scholar |
Gorczyca, W., Traganos, F., Jesionowska, H., and Darzynkiewicz, Z. (1993). Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells. Exp. Cell Res. 207, 202–205.
| Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells.Crossref | GoogleScholarGoogle Scholar |
Gosálvez, J., López‐Fernández, C., Fernández, J. L., Gouraud, A., and Holt, W. V. (2011). Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species. Mol. Reprod. Dev. 78, 951–961.
| Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species.Crossref | GoogleScholarGoogle Scholar |
Grant, S. A., Long, S. E., and Parkinson, T. J. (1994). Fertilizability and structural properties of boar spermatozoa prepared by Percoll gradient centrifugation. J. Reprod. Fertil. 100, 477–483.
| Fertilizability and structural properties of boar spermatozoa prepared by Percoll gradient centrifugation.Crossref | GoogleScholarGoogle Scholar |
Hahn, G. L., Gaughan, J. B., Mader, T. L., and Eigenberg, R. A. (2009) Thermal indices and their applications for livestock environments. In ‘Livestock Energetics and Thermal Environment Management’. (Ed James A. DeShazer.) pp. 113–130. (American Society of Agricultural and Biological Engineers: St. Joseph, MI.)
Hancock, J., and Hovell, G. (1959). The collection of boar semen. Vet. Rec. 71, e665.
Heitman, H., Cockrell, J. R., and Morrison, S. R. (1984). Cycling ambient temperature effect on boar semen. Anim. Sci. 38, 129–132.
Henkel, R., Hajimohammad, M., Stalf, T., Hoogendijk, C., Mehnert, C., Menkveld, R., Gips, H., Schill, W. B., and Kruger, T. F. (2004). Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil. Steril. 81, 965–972.
| Influence of deoxyribonucleic acid damage on fertilization and pregnancy.Crossref | GoogleScholarGoogle Scholar |
Henkel, R., Hoogendijk, C. F., Bouic, P. J., and Kruger, T. F. (2010). TUNEL assay and SCSA determine different aspects of sperm DNA damage. Andrologia 42, 305–313.
| TUNEL assay and SCSA determine different aspects of sperm DNA damage.Crossref | GoogleScholarGoogle Scholar |
Hennessy, D. P., and Williamson, P. E. (1984). Stress and summer infertility in pigs. Aust. Vet. J. 61, 212–215.
| Stress and summer infertility in pigs.Crossref | GoogleScholarGoogle Scholar |
Holt, C., Holt, W. V., Moore, H. D., Reed, H. C., and Curnock, R. M. (1997). Objectively measured boar sperm motility parameters correlate with the outcomes of on-farm inseminations: results of two fertility trials. J. Androl. 18, 312–323.
Hughes, P., and van Wettere, W. (2010) ‘Seasonal Infertility in Pigs’. (Pork Cooperative Research Centre Ltd.: Willaston, SA, Australia.) Available at: http://www.porkcrc.com.au/101217_SI.pdf [Verified 12 October 2018].
Huynh, T., Aarnink, A., Drucker, A., and Verstegen, M. (2007). Pig production in Cambodia, Laos, Philippines, and Vietnam: a review. Asian J. Agric. Dev. 4, 69–90.
Ingram, D. L. (1965). Evaporative cooling in the pig. Nature 207, 415–416.
| Evaporative cooling in the pig.Crossref | GoogleScholarGoogle Scholar |
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., and Altman, D. G. (2010). Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 8, e1000412.
| Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research.Crossref | GoogleScholarGoogle Scholar |
Kishikawa, H., Tateno, H., and Yanagimachi, R. (1999). Chromosome analysis of balb/c mouse spermatozoa with normal and abnormal head morphology. Biol. Reprod. 61, 809–812.
| Chromosome analysis of balb/c mouse spermatozoa with normal and abnormal head morphology.Crossref | GoogleScholarGoogle Scholar |
Knox, R. 2003. ‘The Anatomy and Physiology of Sperm Production in Boars’. (Department of Animal Sciences, University of Illinois: Urbana, IL.) Available at http://www.ansci.wisc.edu/jjp1/pig_case/html/library/boara&p.pdf [Verified 12 October 2018].
Love, R. J. (1981). Seasonal infertility in pigs. Vet. Rec. 109, 407–409.
| Seasonal infertility in pigs.Crossref | GoogleScholarGoogle Scholar |
Love, C. C., and Kenney, R. M. (1998). The relationship of increased susceptibility of sperm DNA to denaturation and fertility in the stallion. Theriogenology 50, 955–972.
| The relationship of increased susceptibility of sperm DNA to denaturation and fertility in the stallion.Crossref | GoogleScholarGoogle Scholar |
McNitt, J. I., and First, N. L. (1970). Effects of 72-hour heat stress on semen quality in boars. Int. J. Biometeorol. 14, 373–380.
| Effects of 72-hour heat stress on semen quality in boars.Crossref | GoogleScholarGoogle Scholar |
Mortimer, S. T. (2000). CASA-practical aspects. J. Androl. 21, 515–524.
Mount, L. E. (1968). The climatic physiology of the pig. In ‘Monographs. Physiological Society’. (Ed. E. Arnold.) pp. 1–271. (University of Michigan: Ann Arbor, MI.)
National Pork Board (2014) ‘Pork Quick Facts 2014’. (Pork Check Off, National Pork Board: Des Moines, IA.) Available at http://www.pork.org/pork-quick-facts/ [Verified 12 October 2018].
National Pork Board (2017) ‘World Per Capita Pork Consumption’. (Pork Check Off, National Pork Board: Des Moines, IA.) Available at http://www.pork.org/pork-quick-facts/home/stats/u-s-pork-exports/world-per-capita-pork-consumption-2/ [Verified 12 October 2018].
National Weather Service (NWS) (2016a) ‘Meteorological Conversions and Calculations. Heat Index Calculator’. Available at http://www.wpc.ncep.noaa.gov/html/heatindex.shtml [Verified 12 October 2018].
National Weather Service (NWS) (2016b) ‘Heat Index Chart’. Available at https://www.weather.gov/ffc/hichart [Verified 12 October 2018].
Oestrup, O., Hall, V., Petkov, S. G., Wolf, X. A., Hyldig, S., and Hyttel, P. (2009). From zygote to implantation: morphological and molecular dynamics during embryo development in the pig. Reprod. Domest. Anim. 44, 39–49.
| From zygote to implantation: morphological and molecular dynamics during embryo development in the pig.Crossref | GoogleScholarGoogle Scholar |
O’Leary, S. (2010) ‘Final Report to Pork CRC’. (Pork Cooperative Research Centre Ltd.: Willaston, SA, Australia.)
Pacey, A. A. (2010). Environmental and lifestyle factors associated with sperm DNA damage. Hum. Fertil. 13, 189–193.
| Environmental and lifestyle factors associated with sperm DNA damage.Crossref | GoogleScholarGoogle Scholar |
Parrish, J. J., Willenburg, K. L., Gibbs, K. M., Yagoda, K. B., Krautkramer, M. M., Loether, T. M., and Melo, F. C. S. A. (2017). Scrotal insulation and sperm production in the boar. Mol. Reprod. Dev. 84, 969–978.
| Scrotal insulation and sperm production in the boar.Crossref | GoogleScholarGoogle Scholar |
Paterson, A., Barker, I., and Lindsay, D. (1978). Summer infertility in pigs: its incidence and characteristics in an Australian commercial piggery. Aust. J. Exp. Agric. 18, 698–701.
| Summer infertility in pigs: its incidence and characteristics in an Australian commercial piggery.Crossref | GoogleScholarGoogle Scholar |
Paul, C., Murray, A. A., Spears, N., and Saunders, P. T. (2008). A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 136, 73–84.
| A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice.Crossref | GoogleScholarGoogle Scholar |
Peña, S., Summers, P., Gummow, B., and Paris, D. B. B. P. (2015). Oviduct binding ability of porcine spermatozoa develops in the epididymis and can be advanced by incubation with caudal fluid. Theriogenology 83, 1502–1513.
| Oviduct binding ability of porcine spermatozoa develops in the epididymis and can be advanced by incubation with caudal fluid.Crossref | GoogleScholarGoogle Scholar |
Peña, S. T., Gummow, B., Parker, A. J., and Paris, D. B. (2017). Revisiting summer infertility in the pig: could heat stress-induced sperm DNA damage negatively affect early embryo development? Anim. Prod. Sci. 57, 1975–1983.
| Revisiting summer infertility in the pig: could heat stress-induced sperm DNA damage negatively affect early embryo development?Crossref | GoogleScholarGoogle Scholar |
Pérez-Crespo, M., Pintado, B., and Gutiérrez-Adán, A. (2008). Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol. Reprod. Dev. 75, 40–47.
| Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice.Crossref | GoogleScholarGoogle Scholar |
Petrocelli, H., Batista, C., and Gosálvez, J. (2015). Seasonal variation in sperm characteristics of boars in southern Uruguay. Rev. Bras. Zootec. 44, 1–7.
| Seasonal variation in sperm characteristics of boars in southern Uruguay.Crossref | GoogleScholarGoogle Scholar |
Pingali, P. (2007). Westernization of Asian diets and the transformation of food systems: implications for research and policy. Food Policy 32, 281–298.
| Westernization of Asian diets and the transformation of food systems: implications for research and policy.Crossref | GoogleScholarGoogle Scholar |
Prunier, A., de Bragança, M. M., and Le Dividich, J. (1997). Influence of high ambient temperature on performance of reproductive sows. Livest. Prod. Sci. 52, 123–133.
| Influence of high ambient temperature on performance of reproductive sows.Crossref | GoogleScholarGoogle Scholar |
Pursel, V. G., and Johnson, L. A. (1975). Freezing of boar spermatozoa: fertilizing capacity with concentrated semen and a new thawing procedure. J. Anim. Sci. 40, 99–102.
| Freezing of boar spermatozoa: fertilizing capacity with concentrated semen and a new thawing procedure.Crossref | GoogleScholarGoogle Scholar |
Qiu, Y., Wang, L.-G., Zhang, L.-H., Li, J., Zhang, A.-D., and Zhang, M.-H. (2012). Sperm chromosomal aneuploidy and DNA integrity of infertile men with anejaculation. J. Assist. Reprod. Genet. 29, 185–194.
| Sperm chromosomal aneuploidy and DNA integrity of infertile men with anejaculation.Crossref | GoogleScholarGoogle Scholar |
Roca, J., Broekhuijse, M., Parrilla, I., Rodriguez‐Martinez, H., Martinez, E., and Bolarin, A. (2015). Boar differences in artificial insemination outcomes: can they be minimized? Reprod. Domest. Anim. 50, 48–55.
| Boar differences in artificial insemination outcomes: can they be minimized?Crossref | GoogleScholarGoogle Scholar |
Rockett, J. C., Mapp, F. L., Garges, J. B., Luft, J. C., Mori, C., and Dix, D. J. (2001). Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol. Reprod. 65, 229–239.
| Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice.Crossref | GoogleScholarGoogle Scholar |
Rybar, R., Faldikova, L., Faldyna, M., Machatkova, M., and Rubes, J. (2004). Bull and boar sperm DNA integrity evaluated by sperm chromatin structure assay in the Czech Republic. Vet. Med. (Praha) 49, 1–8.
Sailer, B. L., Sarkar, L. J., Bjordahl, J. A., Jost, L. K., and Evenson, D. P. (1997). Effects of heat stress on mouse testicular cells and sperm chromatin structure. J. Androl. 18, 294–301.
Sarlós, P., Egerszegi, I., Nagy, S., Fébel, H., and Rátky, J. (2011). Reproductive function of Hungarian Mangalica boars: effect of seasons. Acta Vet. Hung. 59, 257–267.
| Reproductive function of Hungarian Mangalica boars: effect of seasons.Crossref | GoogleScholarGoogle Scholar |
Satake, N., Elliott, R. M., Watson, P. F., and Holt, W. V. (2006). Sperm selection and competition in pigs may be mediated by the differential motility activation and suppression of sperm subpopulations within the oviduct. J. Exp. Biol. 209, 1560–1572.
| Sperm selection and competition in pigs may be mediated by the differential motility activation and suppression of sperm subpopulations within the oviduct.Crossref | GoogleScholarGoogle Scholar |
Serafini, R., McPhail, R. E., Varner, D. D., Blanchard, T. L., Teague, S. R., and Love, C. C. (2016). The relationship between sperm DNA structure and sexual rest in stallions. J. Equine Vet. Sci. 43, S65–S66.
| The relationship between sperm DNA structure and sexual rest in stallions.Crossref | GoogleScholarGoogle Scholar |
Simon, L., and Lewis, S. E. M. (2011). Sperm DNA damage or progressive motility: which one is the better predictor of fertilization in vitro? Syst Biol Reprod Med 57, 133–138.
| Sperm DNA damage or progressive motility: which one is the better predictor of fertilization in vitro?Crossref | GoogleScholarGoogle Scholar |
Simon, L., Proutski, I., Stevenson, M., Jennings, D., McManus, J., Lutton, D., and Lewis, S. E. M. (2013). Sperm DNA damage has a negative association with live-birth rates after IVF. Reprod. Biomed. Online 26, 68–78.
| Sperm DNA damage has a negative association with live-birth rates after IVF.Crossref | GoogleScholarGoogle Scholar |
Sonderman, J. P., and Luebbe, J. J. (2008). Semen production and fertility issues related to differences in genetic lines of boars. Theriogenology 70, 1380–1383.
| Semen production and fertility issues related to differences in genetic lines of boars.Crossref | GoogleScholarGoogle Scholar |
Stone, B. A. (1982). Heat induced infertility of boars: the inter-relationship between depressed sperm output and fertility and an estimation of the critical air temperature above which sperm output is impaired. Anim. Reprod. Sci. 4, 283–299.
| Heat induced infertility of boars: the inter-relationship between depressed sperm output and fertility and an estimation of the critical air temperature above which sperm output is impaired.Crossref | GoogleScholarGoogle Scholar |
Stone, B., and Seamark, R. (1984). Effects of acute and chronic testicular hyperthermia on levels of testosterone and corticosteroids in plasma of boars. Anim. Reprod. Sci. 7, 391–403.
| Effects of acute and chronic testicular hyperthermia on levels of testosterone and corticosteroids in plasma of boars.Crossref | GoogleScholarGoogle Scholar |
St-Pierre, N. R., Cobanov, B., and Schnitkey, G. (2003). Economic losses from heat stress by US livestock industries. J. Dairy Sci. 86, E52–E77.
| Economic losses from heat stress by US livestock industries.Crossref | GoogleScholarGoogle Scholar |
Sumena, K., Lucy, K., Chungath, J., Ashok, N., and Harshan, K. (2010). Regional histology of the subcutaneous tissue and the sweat glands of Large White Yorkshire pigs, Tamilnadu. J. Vet. Anim. Sci. (Lahore) 6, 128–135.
Sutovsky, P. (2015). New approaches to boar semen evaluation, processing and improvement. Reprod. Domest. Anim. 50, 11–19.
| New approaches to boar semen evaluation, processing and improvement.Crossref | GoogleScholarGoogle Scholar |
Tantasuparuk, W., and Kunavongkrit, A. (2014) ‘Pig Production in Thailand, Country Report’. Available at https://www.angrin.tlri.gov.tw/English/2014Swine/p136-144.pdf
Thom, E. C. (1959). The discomfort index. Weatherwise 12, 57–61.
| The discomfort index.Crossref | GoogleScholarGoogle Scholar |
Tramontano, F., Malanga, M., Farina, B., Jones, R., and Quesada, P. (2000). Heat stress reduces poly(adpr)polymerase expression in rat testis. Mol. Hum. Reprod. 6, 575–581.
| Heat stress reduces poly(adpr)polymerase expression in rat testis.Crossref | GoogleScholarGoogle Scholar |
Tsakmakidis, I. A., Lymberopoulos, A. G., and Khalifa, T. A. A. (2010). Relationship between sperm quality traits and field-fertility of porcine semen. J. Vet. Sci. 11, 151–154.
| Relationship between sperm quality traits and field-fertility of porcine semen.Crossref | GoogleScholarGoogle Scholar |
van Zelst, S. J., Zupp, J. L., Hayman, D. L., and Setchell, B. P. (1995). X-Y chromosome dissociation in mice and rats exposed to increased testicular or environmental temperatures. Reprod. Fertil. Dev. 7, 1117–1121.
| X-Y chromosome dissociation in mice and rats exposed to increased testicular or environmental temperatures.Crossref | GoogleScholarGoogle Scholar |
Vega, R., and Agbisit, E., Jr (2009) ‘Analysis and Utilization of Farm Performance Data as a Tool in Enhancing Swine Farm Productivity and Efficiency’. (Philippine Swine Industry Research and Development Foundation: Los Baños.) Available at: http://agris.fao.org/agris-search/search.do?recordID=PH2010000360 [Verified 12 October 2018].
Vega, R. S., Garcia, B. R., Agbisit, E., Calud, A. T., and Villar, E. C. (2010). Performance of commercial piggery farms affected by the third quarter reproduction syndrome. Philipp. J. Vet. Anim. Sci. 36, 63–72.
Venkatesh, S., Singh, A., Shamsi, M. B., Thilagavathi, J., Kumar, R. K., Mitra, D., and Dada, R. (2011). Clinical significance of sperm DNA damage threshold value in the assessment of male infertility. Reprod. Sci. 18, 1005–1013.
| Clinical significance of sperm DNA damage threshold value in the assessment of male infertility.Crossref | GoogleScholarGoogle Scholar |
Vyt, P., Maes, D., Quinten, C., Rijsselaere, T., Deley, W., Aarts, M., de Kruif, A., and Soom, A. (2008). Detailed motility evaluation of boar semen and its predictive value for reproductive performance in sows. Vlaams Diergeneeskundig Tijdschrift 77, 291–298.
Waberski, D., Schapmann, E., Henning, H., Riesenbeck, A., and Brandt, H. (2011). Sperm chromatin structural integrity in normospermic boars is not related to semen storage and fertility after routine AI. Theriogenology 75, 337–345.
| Sperm chromatin structural integrity in normospermic boars is not related to semen storage and fertility after routine AI.Crossref | GoogleScholarGoogle Scholar |
Wettemann, R. P., Wells, M. E., Omtvedt, I. T., Pope, C. E., and Turman, E. J. (1976). Influence of elevated ambient temperature on reproductive performance of boars. J. Anim. Sci. 42, 664–669.
| Influence of elevated ambient temperature on reproductive performance of boars.Crossref | GoogleScholarGoogle Scholar |
Wettemann, R. P., Wells, M. E., and Johnson, R. K. (1979). Reproductive characteristics of boars during and after exposure to increased ambient temperature. J. Anim. Sci. 49, 1501–1505.
| Reproductive characteristics of boars during and after exposure to increased ambient temperature.Crossref | GoogleScholarGoogle Scholar |
World Health Organization (WHO) (2010). ‘WHO Laboratory Manual for the Examination and Processing of Human Semen’. 5th edn. (World Health Organization: Geneva.). Available at http://apps.who.int/iris/bitstream/10665/44261/1/9789241547789_eng.pdf [Verified 12 October 2018].
Zasiadczyk, L., Fraser, L., Kordan, W., and Wasilewska, K. (2015). Individual and seasonal variations in the quality of fractionated boar ejaculates. Theriogenology 83, 1287–1303.
| Individual and seasonal variations in the quality of fractionated boar ejaculates.Crossref | GoogleScholarGoogle Scholar |
