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Sperm Chromatin Structure Assay: Its Clinical Use for Detecting Sperm DNA Fragmentation in Male Infertility and Comparisons With Other Techniques
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The Sperm Chromatin Structure Assay (SCSA) was first described in the December 5, 1980 issue of Science (Evenson et al, 1980a).The data described in that article showed a significant difference between proven fertile and subfertility or infertility in men and bulls and the susceptibility to denaturation of their sperm nuclear DNA.A subsequent study (Evenson et al, 1984) described SCSA data obtained from men with testicular cancer.The data were heterogeneous, and begged the question, what was SCSA measuring?Great effort has been spent over the past 15 years on animal model systems, mostly related to dose-response toxicology experiments and large animal fertility trials.The results from these studies showed that SCSA was highly dose-responsive to toxicants, highly repeatable, and provided meaningful biological information on sperm nuclear DNA defects.The extensive data from nonhumans (Evenson et al, 1985(Evenson et al, , 1986(Evenson et al, , 1989a(Evenson et al, ,b, 1993a(Evenson et al, ,b,c, 1994(Evenson et al, , 1995b;; Ballachey et
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“DNA fragmentation assessment using the Sperm Chromatin Structure Analysis (SCSA) test”
From The effect of antioxidants on male factor infertility: the Males, Antioxidants, and Infertility (MOXI) randomized clinical trial (2020) · cites this paper as [14]
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“Sperm chromatin structure is a significant determinant of sperm quality [55].”
BackgroundIntracytoplasmic Sperm Injection (ICSI) in Extreme Cases of Male Infertility
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“This is supported by the clear relationship of a low DFI and pregnancy outcome when natural intercourse and IUI are used [49, 52, 53].”
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“Interestingly, when TUNEL outcomes were evaluated by fl ow cytometry, the threshold value of TUNEL-positive spermatozoa with regard to ICSI outcome was calculated to be 30% (Hazout et al., 2006), which was much higher than for TUNEL evaluated by microscopic observation (Table 1).716 With the use of SCSA and fl ow cyto…”
BackgroundSpecht, I. O., Hougaard, K. S., Spanò, M., Bizzaro, D., Manicardi, G. C., Lindh, C. H., Toft, G. V., Jönsson, B., Giwercman, A., & Bonde, J. P. (2012) · Reproductive Toxicology · doi:10.1016/j.reprotox.2012.02.008 · Cited by 77
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“Sperm chromatin structure protects genetic integrity during transport of the paternal genome through the male and female reproductive tracts [2, 3].”
BackgroundDifferences in SCSA outcome among boars with different sperm freezability.
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“We have to take into account that the degree of packaging is different between species, being looser in human than in other mammals [5].”
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“…diluted 1:5 in buffer containing fixative and stored at 4°C and 100 ul aliquots of semen were frozen at -80°C. Sperm chromatin structure assay (SCSA) was performed at Reproductive Medicine Center, Skåne University Hospital, Malmö, Sweden and details of the method are described elsewhere [34 – 36].”
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“The analysis by flow cytometer allows evaluation of 10.000 spermatozoa within a minute or two resulting in a more robust analysis (Evenson et al., 2002; Evenson & Wixon, 2006; Zini et al., 2009; Evenson, 2013).”
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“If over 30% of the spermatozoa are DNA damaged, then the potential for natural fertility is reduced (Evenson et al., 2002).”
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Lusignan, M., Li, X., Herrero, B., Delbes, G., & Chan, P. T. (2018) · Andrology · doi:10.1111/andr.12529 · Cited by 70
“Sperm chromatin structure assay (SCSA ) To measure the susceptibility of the sperm nuclear DNA to low pH induced denaturation in situ, the SCSA method was used as previously described (Evenson et al., 2002; Delbes et al., 2013).”
MethodSellami, H., Znazen, A., Sellami, A., Mnif, H., Louati, N., Zarrouk, S. B., Keskes, L., Rebai, T., Gdoura, R., & Hammami, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098903 · Cited by 70
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“Multiple studies have focused on the correlation between DNA fragmentation (as tested by SCSA) and the three conventional sperm parameters resulting in variable and conflicting outcomes for pregnancy planners, infertile patients with and without an assisted reproductive treatment (Zini et al., 2001; Evenson et al., 20…”
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“…samples frozen at 2808C. Flow cytometry sperm chromatin structure assay To measure the Cy-induced DNA damage to sperm, we assayed the susceptibility of sperm nuclear DNA to low pH-induced denaturation in situ (sperm chromatin structure assay (SCSA)) as previously described (Evenson et al., 2002).”
BackgroundMethodInfluentialOumaima, A., Tesnim, A., Zohra, H., Amira, S., Ines, Z., Sana, C., Intissar, G., Lobna, E., Ali, J., & Meriem, M. (2018) · Environmental Science and Pollution Research · doi:10.1007/s11356-018-1417-4 · Cited by 69
“…the final addition of protamines to transform spermatogonia to spermatozoa with highly organized chromatin structure (Marcon and Boissonneault 2004), which protects the integrity of the paternal genome during transportation of sperm in the male and female reproductive tracts (Evenson et al. 2002).”
BackgroundMild induced testicular and epididymal hyperthermia alters sperm chromatin integrity in men.
Ahmad, G., Moinard, N., Esquerré-Lamare, C., Mieusset, R., & Bujan, L. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.12.025 · Cited by 68
Human Male infertility: A Complex Multifactorial Phenotype
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“Mutations of the sex chromosomal and autosomal genes regulating spermatogenesis may affect specific testicular cell types and reproductive function, resulting in male infertility or subfertility.(1,2)Genomic research offers a new opportunity for determining how diseases occur and research tools enables to identify the…”
BackgroundSperm DNA integrity in cancer patients: the effect of disease and treatment.
Ståhl, O., Eberhard, J., Cavallin-ståhl, E., Jepson, K., Friberg, B., Tingsmark, C., Spanô, M., & Giwercman, A. (2009) · International Journal of Andrology · doi:10.1111/j.1365-2605.2008.00933.x · Cited by 68
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“These results are of concern as sperm DNA integrity is essential for the accurate transmission of genetic information (Evenson et al. 2002, Agarwal & Said 2003, Perreault et al. 2003, Sakkas et al. 2003a).”
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HEALTH SURVEILLANCE OF GULF WAR I VETERANS EXPOSED TO DEPLETED URANIUM: UPDATING THE COHORT
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“Duplicate analyses were performed on the semen from each participant by previously published methods (Evenson et al. 1980, 2002) and all samples were analyzed in the same assay.”
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“Sperm DNA fragmentation includes both single- and double-strand DNA breaks [7].”
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“Pregnancy rates are significantly lower in men with a DFI of > 30% (Evenson et al., 2002).”
BackgroundMethodInfluentialRe-visiting the Protamine-2 locus: deletion, but not haploinsufficiency, renders male mice infertile
Schneider, S., Balbach, M., Jikeli, J. F., Fietz, D., Nettersheim, D., Jostes, S., Schmidt, R., Kressin, M., Bergmann, M., Wachten, D., et al. (2016) · Scientific Reports · doi:10.1038/srep36764 · Cited by 78
Effect of semen extenders on sperm parameters of ram semen during liquid storage at 4 °C
Kasimanickam, R., Kasimanickam, V., Tibary, A., & Pelzer, K. (2011) · doi:10.1016/j.smallrumres.2011.03.057 · Cited by 66
Genetic and epigenetic factors: Role in male infertility
Shamsi, M. B., Kumar, K., & Dada, R. (2011) · Indian Journal of Urology · doi:10.4103/0970-1591.78436 · Cited by 66
“The chances of live birth and conception decreases drastically when DNA fragmentation index is >30.[73] Infertile men may have sperm with normal sperm parameters, but the germ cells may harbor DNA damage, which cannot be predicted by routine semen analysis.”
BackgroundSmarr, M. M., Kannan, K., Sun, L., Honda, M., Wang, W., Karthikraj, R., Chen, Z., Weck, J., & Buck Louis, G. M. (2018) · Environmental Research · doi:10.1016/j.envres.2018.07.004 · Cited by 66
Pulse Doppler ultrasound as a tool for the diagnosis of chronic testicular dysfunction in stallions
Ortiz-Rodríguez, J., Anel-López, L., Martín-Muñoz, P., Alvarez, M., Gaitskell-Phillips, G., Anel, L., Rodríguez-Medina, P., Peña, F., & Ferrusola, C. O. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175878 · Cited by 65
“Increased susceptibility of DNA to denaturation (% DFI) has been associated with reduced fertility in the equine [18, 32].”
Özkösem, B., Feinstein, S. I., Fisher, A. B., & O’Flaherty, C. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.115.137646 · Cited by 69
“Altered chromatin structure measured by the susceptibility of sperm DNA to acid-induced denaturation at sites of existing DNA strand breaks [66] was assessed with the Sperm Chromatin Structure Assay (SCSA) [56;67-69].”
MethodBronet, F., Martínez, E., Gaytán, M., Liñán, A., Cernuda, D., Ariza, M., Nogales, M., Pacheco, A., Celestino, M., & García-Velasco, J. (2012) · Human Reproduction · doi:10.1093/humrep/des148 · Cited by 65
“…that could be affected by the integrity of the DNA in ejaculated spermatozoa include fertilization, blastocyst development and pregnancy rates; a correlation between DNA integrity and fertilization rates has been described (Evenson et al., 1999, 2002; Virro et al., 2004; Borini et al., 2006).”
BackgroundAarabi, M., Bałakier, H., Bashar, S., Moskovtsev, S. I., Šutovský, P., Librach, C. L., & Oko, R. J. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.05.003 · Cited by 72
Hammoud, I., Boitrelle, F., Ferfouri, F., Vialard, F., Bergère, M., Wainer, B., Bailly, M., Albert, M., & Selva, J. (2012) · Andrologia · doi:10.1111/j.1439-0272.2012.01328.x · Cited by 67
Kasimanickam, R., Kasimanickam, V., Pelzer, K., & Dascanio, J. (2007) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2006.09.001 · Cited by 64
Núñez-Martínez, I., Morán, J., & Peña, F. (2005) · Reproduction in domestic animals = Zuchthygiene · doi:10.1111/j.1439-0531.2005.00628.x · Cited by 64
No association between body mass index and sperm DNA integrity.
Bandel, I., Bungum, M., Richtoff, J., Malm, J., Axelsson, J., Pedersen, H., Ludwicki, J., Czaja, K., Hernik, A., Toft, G., et al. (2015) · Human Reproduction · doi:10.1093/humrep/dev111 · Cited by 63
“SCSA is a flow cytometric technique (Evenson et al., 2002), which measures the susceptibility of sperm DNA to acid induced DNA denaturation in situ, followed by staining with the fluorescent dye acridine orange (AO).”
MethodVarum, S., Bento, C. F., Sousa, A., Gomes-Santos, C. S., Henriques, P., Almeida-Santos, T., Teodosio, C., Paiva, A., & Ramalho-Santos, J. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.07.1528 · Cited by 63
Ernest, S. R., Wade, M. G., Lalancette, C., Ma, Y., Berger, R. G., Robaire, B., & Hales, B. (2012) · Toxicological Sciences · doi:10.1093/toxsci/kfs098 · Cited by 62
“To assess the susceptibility of sperm nuclear DNA to acid-induced denaturation, the acridine orange (AO) assay, also known as the sperm chromatin structure assay (SCSA) (Evenson et al., 2002), was applied, as previously described (Delbes et al.”
BackgroundMethodInfluentialAgarwal, A., Bragais, F. M., & Sabanegh, E. (2008) · Urologic clinics of North America · doi:10.1016/j.ucl.2008.01.012 · Cited by 62
“A cut off rate of greater than 30% was associated with a significant decrease in in vivo fertilization rates [71,75].”
BackgroundFraser, L., & Strzeżek, J. (2007) · Theriogenology · doi:10.1016/j.theriogenology.2007.05.001 · Cited by 62
“The sperm chromatin structure assay (SCSA) determines the sensitivity of sperm DNA to acid-induced DNA denaturation, providing a measure of chromatin condensation status and DNA damage [5,7].”
BackgroundLuben, T. J., Olshan, A. F., Herring, A. H., Jeffay, S., Strader, L., Buus, R. M., Chan, R. L., Savitz, D. A., Singer, P. C., Weinberg, H. S., et al. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.10120 · Cited by 61
“For the SCSA, aliquots were shipped on liquid nitrogen to SCSA Diagnostics (Brookings, SD) for analysis according to established methods (Evenson et al. 2002).”
MethodVončina, S. M., Golob, B., Ihan, A., Kopitar, A. N., Kolbezen, M., & Zorn, B. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.11.037 · Cited by 75
Villani, P., Eleuteri, P., Grollino, M., Rescia, M., Altavista, P., Spanô, M., Pacchierotti, F., & Cordelli, E. (2010) · Reproduction · doi:10.1530/rep-10-0176 · Cited by 61
Muratori, M., Tamburrino, L., Tocci, V., Costantino, A., Marchiani, S., Giachini, C., Laface, I., Krausz, C., Meriggiola, M., Forti, G., et al. (2010) · Journal of Andrology · doi:10.2164/jandrol.109.008508 · Cited by 61
“On the contrary, SCSA is a long established and standardized technique used in combination with flow cytometry (Evenson et al, 2002; Virro et al, 2004).”
MethodHigher sperm DNA damage in semen from men with spinal cord injuries compared with controls.
Brackett, N., Ibrahim, E., Grotas, J. A., Aballa, T., & Lynne, C. (2008) · Journal of Andrology · doi:10.2164/jandrol.107.003574 · Cited by 61
Fleming, C., Maldjian, A., da Costa, D., Rullay, A. K., Haddleton, D., John, J. S. S., Penny, P., Noble, R., Cameron, N., & Davis, B. (2005) · Nature Chemical Biology · doi:10.1038/nchembio730 · Cited by 61
Variability and laboratory factors affecting the sperm chromatin structure assay in human semen.
Boe-Hansen, G., Ersbøll, A., & Christensen, P. (2005) · Journal of Andrology · doi:10.2164/jandrol.04056 · Cited by 61
The value of home-based collection of biospecimens in reproductive epidemiology.
Rockett, J., Buck, G., Lynch, C., & Perreault, S. (2004) · Environmental Health Perspectives · doi:10.1289/ehp.6264 · Cited by 61
“Fink et al. (2002) used this approach successfully in carrying out microarray analysis of RNA extracted from laser capture microdissection samples.”
Relationship between sperm morphology and sperm DNA dispersion
Jakubik-Uljasz, J., Gill, K., Rosiak-Gill, A., & Piasecka, M. (2020) · Translational Andrology and Urology · doi:10.21037/tau.2020.01.31 · Cited by 60
Sperm quality variables as indicators of bull fertility may be breed dependent.
Morrell, J., Nongbua, T., Valeanu, S., Lima-Verde, I., Lundstedt-Enkel, K., Edman, A., & Johannisson, A. (2017) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2017.08.001 · Cited by 60
Abdelbaki, S. A., Sabry, J., Al-Adl, A. M., & Sabry, H. (2017) · Arab Journal of Urology · doi:10.1016/j.aju.2017.03.002 · Cited by 60
“[24], who first described the SCSA, suggested that a threshold of 0–15% DFI% correlated to a high fertility potential, whilst 16–29% and a >30% DFI%, correlated to moderate, and low fertility potential, respectively.”
BackgroundMethodPersistent organic pollutants and semen quality: The LIFE Study
Mumford, S. L., Kim, S., Chen, Z., Gore‐Langton, R. E., Barr, D. B., & Louis, G. M. B. (2014) · Chemosphere · doi:10.1016/j.chemosphere.2014.11.015 · Cited by 67
Maselli, J., Hales, B., Chan, P., & Robaire, B. (2012) · Biology of Reproduction · doi:10.1095/biolreprod.111.098616 · Cited by 60
“The susceptibility of sperm nuclear DNA to acid-induced denaturation was determined by the SCSA/acridine orange (AO) assay, as previously described [19].”
MethodZubkova, E., & Robaire, B. (2006) · Human Reproduction · doi:10.1093/humrep/del193 · Cited by 60
The Effects of Low‐Level Laser Light Exposure on Sperm Motion Characteristics and DNA Damage
Firestone, R., Esfandiari, N., Moskovtsev, S. I., Burstein, E., Videna, G. T., Librach, C. L., Bentov, Y., & Casper, R. F. (2012) · Journal of Andrology · doi:10.2164/jandrol.111.013458 · Cited by 64
Moskovtsev, S., Willis, J., White, J., & Mullen, J. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.11.132 · Cited by 59
Leopardi, P., Villani, P., Cordelli, E., Siniscalchi, E., Veschetti, E., & Crebelli, R. (2005) · Toxicology Letters · doi:10.1016/j.toxlet.2005.02.009 · Cited by 59
Jamal, F., Haque, Q. S., Singh, S., & Rastogi, S. (2016) · Toxicology and industrial health · doi:10.1177/0748233714568175 · Cited by 58
“The integrity of sperm DNA was analyzed with ethanol-fixed specimens by flow cytometry using the sperm chromatin structure assay (SCSA) (Evenson et al., 2002).”
BackgroundMethodInfluentialRetractedde Jager, C., Aneck-Hahn, N., Bornman, M., Farías, P., Leter, G., Eleuteri, P., Rescia, M., & Spanô, M. (2009) · Human Reproduction · doi:10.1093/humrep/dep249 · Cited by 58
“In the present study, we have applied the SCSA method (Evenson et al., 2002; Perreault et al., 2003), which measures by flow cytometry (FCM) the susceptibility of sperm nuclear DNA to denaturation in situ followed by Acridine Orange (AO) staining (Evenson et al.”
BackgroundMethodInfluentialA novel approach for the selection of human sperm using annexin V-binding and flow cytometry.
Hoogendijk, C., Kruger, T. F., Bouic, P., & Henkel, R. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.01.042 · Cited by 58
Chromatin-unstable boar spermatozoa have little chance of reaching oocytes in vivo.
Ardón, F., Helms, D., Şahin, E., Bollwein, H., Topfer-Petersen, E., & Waberski, D. (2008) · Reproduction · doi:10.1530/rep-07-0333 · Cited by 58
“Chromatin instability as detected with the SCSA may only show the ‘tip of the iceberg’ of a population of immature spermatozoa (Evenson et al. 2002).”
BackgroundInfluentialOmrani, B. A., Aleisa, N. A., Javed, M., Ghedan, M. A., Al-Matrafi, H., & Sufyan, H. A. (2018) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-018-0369-3 · Cited by 57
Huang, L.-P., Lee, C.-C., Fan, J.-P., Kuo, P., Shih, T., & Hsu, P. (2013) · International Archives of Occupational and Environmental Health · doi:10.1007/s00420-013-0905-6 · Cited by 54
“The most frequently used test systems are the terminal deoxynucleotidyl transferase (TdT)-mediated nick end labeling (TUNEL) assay (Gorczyca et al. 1993) and the sperm chromatin DNA structure assay (SCSA) (Evenson et al. 2002).”
MethodInfluentialSperm DNA Fragmentation: Consequences for Reproduction
Simon, L., Emery, B. R., & Carrell, D. T. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-21664-1_6 · Cited by 81
Tsarev, I., Bungum, M., Giwercman, A., Erenpreisa, J., Ebessen, T., Ernst, E., & Ērenpreiss, J. (2009) · Human Reproduction · doi:10.1093/humrep/dep068 · Cited by 56
“Sperm chromatin structure assay The SCSA was applied following the procedure described elsewhere (Evenson et al., 2002; Erenpreiss et al., 2004).”
BackgroundMethodEvenson, D., & Wixon, R. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.08.009 · Cited by 56
Self-citationThe impact of testicular carcinoma and its treatment on sperm DNA integrity
Ståhl, O., Eberhard, J., Jepson, K., Spanô, M., Cwikiel, M., Cavallin-ståhl, E., & Giwercman, A. (2004) · Cancer · doi:10.1002/cncr.20068 · Cited by 56
“DFI expresses the percentage of cells containing denatured DNA.19 Five thousand cells were analyzed by FACSort (Becton Dickinson, San Jose, CA).”
MethodInfluentialLifestyle and demographic factors associated with human semen quality and sperm function
Shi, X., Chan, C. P. S., Waters, T. H. B., Chi, L., Chan, D. Y., & Li, T. C. (2018) · Systems Biology in Reproductive Medicine · doi:10.1080/19396368.2018.1491074 · Cited by 55
“Sperm DNA fragmentation was measured according to conventional sperm chromatin structure assay (SCSA) as described by Evenson et al. (2002).”
MethodAmbient air pollution and semen quality
Nobles, C., Schisterman, E., Ha, S., Kim, K., Mumford, S., Louis, G. B. B., Chen, Z., Liu, D.-P., Sherman, S., & Mendola, P. (2018) · Environmental Research · doi:10.1016/j.envres.2018.02.004 · Cited by 55
“%) and high DNA stainability (%), were assessed using the sperm chromatin stability assay following methods of Evenson et al. (Evenson et al., 2002).”
Kennedy, C., Ahlering, P., Rodriguez, H., Levy, S., & Sutovsky, P. (2011) · Reproductive Biomedicine Online · doi:10.1016/j.rbmo.2010.11.020 · Cited by 55
“The DFI and HDS parameters are more repeatable than conventional, subjectively evaluated semen parameters such as sperm count, morphology and motility (Evenson and Wixon, 2006; Evenson et al., 2002; Virro et al., 2004).”
BackgroundDiagnostic Methods for Evaluation of Stallion Subfertility: A Review
Ball, B. (2008) · doi:10.1016/j.jevs.2008.10.003 · Cited by 55
Giwercman, A., Rylander, L., Rignell-Hydbom, A., Jönsson, B., Pedersen, H., Ludwicki, J., Lesovoy, V., Zvyezday, V., Spanô, M., Manicardi, G., et al. (2007) · Pharmacogenetics & Genomics · doi:10.1097/01.fpc.0000236329.26551.78 · Cited by 55
Viability and DNA fragmentation in differently sorted boar spermatozoa.
de Ambrogi, M., Spinaci, M., Galeati, G., & Tamanini, C. (2006) · Theriogenology · doi:10.1016/j.theriogenology.2006.05.017 · Cited by 55
“Differences among species are rather evident: the threshold for considering human sperm quality low or unsuitable for assisted reproduction is 30% of DFI using SCSA [18].”
BackgroundCordelli, E., Eleuteri, P., Leter, G., Rescia, M., & Spanô, M. (2005) · Contraception · doi:10.1016/j.contraception.2005.03.004 · Cited by 55
Oehninger, S., & Gosden, R. (2002) · Human Reproduction · doi:10.1093/humrep/17.9.2237 · Cited by 55
Swayne, B. G., Kawata, A., Behan, N. A., Williams, A., Wade, M. G., MacFarlane, A. J., & Yauk, C. L. (2012) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2012.07.002 · Cited by 56
Detection of DNA fragmentation in human spermatozoa: correlation with semen parameters
Mehdi, M., Khantouche, L., Ajina, M., & Saad, A. (2009) · Andrologia · doi:10.1111/j.1439-0272.2009.00953.x · Cited by 54
“The chances of conception decrease drastically when DNA fragmentation index (DFI) is >30 per cent (Evenson et al., 2002).”
BackgroundSeminal plasma albumin: origin and relation to the male reproductive parameters
Elzanaty, S., Erenpreiss, J., & Becker, C. (2007) · Andrologia · doi:10.1111/j.1439-0272.2007.00764.x · Cited by 54
“The sperm chromatin structure assay (SCSA) was applied following the procedure described earlier, using staining with acridine orange (AO) (Evenson et al., 2002; Erenpreiss et al., 2004).”
MethodMakhlouf, A., & Niederberger, C. (2006) · Journal of Andrology · doi:10.2164/jandrol.05217 · Cited by 54
Waterhouse, K., Gjeldnes, A., Tverdal, A., de Angelis, P., Farstad, W., Håård, M., & Kommisrud, E. (2010) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2009.04.011 · Cited by 54
“A detailed description of the procedure was given previously (Evenson et al., 2002).”
BackgroundMethodInfluentialInter‐ and intra‐laboratory standardization of TUNEL assay for assessment of sperm DNA fragmentation
Ribeiro, S. C., Sharma, R. K., Gupta, S., Çakar, Z., de Geyter, C., & Agarwal, A. (2017) · Andrology · doi:10.1111/andr.12334 · Cited by 53
“It measures all existing single-strand and double-strand DNA breaks including those with 3-OH breaks (Evenson et al., 2002; Virro et al., 2004; Bungum et al., 2007; Ribas-Maynou et al., 2013; Evenson, 2016).”
BackgroundSperm DNA damage—the effect of stress and everyday life factors
Radwan, M., Jurewicz, J., Merecz‐Kot, D., Sobala, W., Radwan, P., Bochenek, M., & Hanke, W. (2016) · International Journal of Impotence Research · doi:10.1038/ijir.2016.15 · Cited by 57
Rybář, R., Přinosilová, P., Kopecká, V., Hlavicová, J., Veznik, Z., Zajĩcovã, A., & Rubes, J. (2012) · Andrologia · doi:10.1111/j.1439-0272.2011.01198.x · Cited by 53
“However, the latter fails to objectively evaluate the functional integrity of the highly specialised sperm cells (Zini et al., 2001; Evenson et al., 2002).”
BackgroundOleszczuk, K., Giwercman, A., & Bungum, M. (2011) · Human Reproduction · doi:10.1093/humrep/der328 · Cited by 53
“In contrast, previous studies on men who had a DFI of 10% have shown a high level of repeatability (Evenson et al., 1991, 2002).”
ResultGosálvez, J., Nuñez, R., Fernández, J., López-Fernández, C., & Caballero, P. (2011) · Andrologia · doi:10.1111/j.1439-0272.2010.01022.x · Cited by 53
“However, the relationship between the frequency of sperm cells with fragmented DNA and these parameters is not so obvious and varies among the different studies (Evenson et al., 2002; Payne et al., 2005; Makhlouf & Niederberger, 2006; Muriel et al., 2006; Collins et al., 2008; Velez de la Calle et al., 2008).”
BackgroundResultDemir, B., Dilbaz, B., Cinar, O., Karadağ, B., Taşçı, Y., Koçak, M., Dilbaz, S., & Goktolga, U. (2011) · Journal of Obstetrics and Gynaecology Research · doi:10.3109/01443615.2011.569780 · Cited by 53
“Sperm DNA fragmentation increased with age including the potential effects of oxidative stress and aberrant apoptosis (Evenson and Wixon 2006; Evenson et al. 2002; Duran et al. 2002).”
Background
Metadata
- Authors
- EVENSON, D. P., LARSON, K. L., & JOST, L. K.
- Affiliations
- South Dakota State University (US)
- Corresponding author
- EVENSON, DONALD P.
- ORCID
- EVENSON, DONALD P.
- Venue
- Journal of Andrology
- Publisher
- Wiley
- Published
- 2002-01-02
- Volume
- 23
- Issue
- 1
- Pages
- 25-43
- ISSN
- 0196-3635 (ISSN-L)
- 1939-4640
- OpenAlex
- W1532901402
- Cited by
- 1,072
- References
- 158
- Citations by year
- 2026: 15 · 2025: 21 · 2024: 18 · 2023: 25 · 2022: 36 · 2021: 59 · 2020: 35 · 2019: 50 · 2018: 49 · 2017: 51 · 2016: 42 · 2015: 53 · 2014: 53 · 2013: 68 · 2012: 61
- FWCI
- 38.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Andrology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (9452894, 9720642)
- U.S. Environmental Protection Agency
- South Dakota Agricultural Experiment Station
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
- Health Sciences › Medicine › Urology › Male Reproductive Health Studies
- Keywords
- sperm chromatin structure assay, sperm DNA fragmentation, male infertility, testicular cancer
- MeSH terms
- Chromatin, Humans, Infertility, Male, Male, Spermatozoa, DNA Fragmentation
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