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Paternal Exposure to Drugs and Environmental Chemicals: Effects on Progeny Outcome

2001; Wiley; Volume: 22; Issue: 6 Linguagem: Inglês

10.1002/j.1939-4640.2001.tb03431.x

2047-2927

Barbara F. Hales, Bernard Robaire,

Assisted Reproductive Technology and Twin Pregnancy

Journal of AndrologyVolume 22, Issue 6 p. 927-936 Free Access Paternal Exposure to Drugs and Environmental Chemicals: Effects on Progeny Outcome BARBARA F. HALES, Corresponding Author BARBARA F. HALES Pharmacology and Therapeutics, McGill University, Montréal, Québec, Canada. Departments, McGill University, Montréal, Québec, Canada.Department of Pharmacology and Therapeutics, McGill University, 3655 Promenade Sir-William-Osler, Montréal, Québec, Canada H3G 1Y6. (e-mail: bhales@pharma.mcgill.ca).Search for more papers by this authorBERNARD ROBAIRE, BERNARD ROBAIRE Pharmacology and Therapeutics, McGill University, Montréal, Québec, Canada. Obstetrics and Gynecology, McGill University, Montréal, Québec, Canada. Departments, McGill University, Montréal, Québec, Canada.Search for more papers by this author BARBARA F. HALES, Corresponding Author BARBARA F. HALES Pharmacology and Therapeutics, McGill University, Montréal, Québec, Canada. Departments, McGill University, Montréal, Québec, Canada.Department of Pharmacology and Therapeutics, McGill University, 3655 Promenade Sir-William-Osler, Montréal, Québec, Canada H3G 1Y6. (e-mail: bhales@pharma.mcgill.ca).Search for more papers by this authorBERNARD ROBAIRE, BERNARD ROBAIRE Pharmacology and Therapeutics, McGill University, Montréal, Québec, Canada. Obstetrics and Gynecology, McGill University, Montréal, Québec, Canada. Departments, McGill University, Montréal, Québec, Canada.Search for more papers by this author First published: 02 January 2013 https://doi.org/10.1002/j.1939-4640.2001.tb03431.xCitations: 39AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat References Ahmadi A., Ng S. C.. Fertilizing ability of DNA-damaged spermatozoa. J Exp Zool. 1999; 284: 696– 704. Allen JW, Collins BW, Cannon RE, McGregor PW, Afshari A., Fuscoe JC. Aneuploidy tests: cytogenetic analysis of mammalian germ cells. In: AF Olshan, DR Mattison eds., Male-Mediated Developmental Toxicity. Washington, NY: Plenun Press; 1994: 59– 69. Anderson D., Bishop JB, Garner RC, Ostrosky-Wegman P., Selby PB. Cyclophosphamide: review of its mutagenicity for an assessment of potential germ cell risks. Mutat Res. 1995; 330: 115– 181. Anderson LM, Kasprzak KS, Rice JM. Preconception exposure of males and neoplasia in their progeny: effects of metals and consideration of mechanisms. In: AF Olshan, DR Mattison eds., Male-Mediated Developmental Toxicity. Washington, NY: Plenum Press; 1994: 129– 140. Anttila A., Sallmén M. Effects of parental occupational exposure to lead and other metals on spontaneous abortion. J Occup Environ Med. 1995; 37: 915– 921. Arbuckle TE, Schrader SM, Cole D., Hall JC, Bancej CM, Turner LA, Claman P. 2,4-Dichlorophenoxyacetic acid residues in semen of Ontario farmers. Reprod Toxicol. 1999; 13: 421– 429. Arbuckle TE, Sever LE. Pesticide exposures and fetal death: a review of the epidemiologic literature. Crit Rev Toxicol. 1998; 28: 229– 270. Auroux M., Dulioust EJ, Nawar NN, Yacoub SG, Mayaux MJ, Schwartz D., David G. Antimitotic drugs in the male rat. Behavioral abnormalities in the second generation. J Androl. 1988; 9: 153– 159. Auroux M., Dulioust E., Selva J., Rince P. Cyclophosphamide in the F0 male rat: physical and behavioral changes in three successive adult generations. Mutat Res. 1990; 229: 189– 200. Austin SM, Robaire B., Hales BF, Kelly SM [Corrected to Austin SM Paternal cyclophosphamide exposure causes decreased cell proliferation in cleavage-stage embryos. Biol Reprod. 1994; 50: 55– 64. Backer LC, Gibson MJ, Moses MJ, Allen JW. Synaptonemal complex damage in relation to meiotic chromosome aberration after exposure of male mice to cyclophosphamide. Mutat Res. 1988; 203: 317– 330. Bartolomei MS, Zemel S., Tilghman SM. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev. 1993; 7: 1663– 1673. Barton SC, Surani MAH, Norris ML. Role of paternal and maternal genomes in mouse development. Nature. 1984; 311: 374– 376. Bonde JP. The risk of male subfecundity attributable to welding of metals. Studies of semen quality, infertility, fertility, adverse pregnancy outcome and childhood malignancy. Int J Androl. 1993; 16: 1– 29. Bonduelle M., Camus M., de Vos A., Staessen C., Tournaye H., Van Assche E., Verheyen G., Devroey P., Seven years of intracytoplasmic sperm injection and follow-up of 1987 subsequent children. Hum Reprod. 1999; 14: 243– 264. Bonduelle M., Joris H., Hofmans K., Liebaers I., Van Steirteghem A. Mental development of 201 ICSI children at two years of age. Lancet. 1998; 351: 1553. Bowen JR, Gibson FL, Leslie GI, Saunders DM. Medical and developmental outcome at 1 year for children conceived by intracytoplasmic sperm injection. Lancet. 1998; 351: 1529– 1534. Brinkworth MH. Paternal transmission of genetic damage: findings in animals and humans. Int J Androl. 2000; 23: 123– 135. Brinkworth MH, Nieschlag E. Association of cyclophosphamide-induced male-mediated, foetal abnormalities with reduced paternal germ cell apoptosis. Mutat Res. 2000; 447: 149– 154. Byrne J. Long-term genetic and reproductive effects of ionizing radiation and chemotherapeutic agents on cancer patients and their offspring. Teratology. 1999; 59: 210– 215. Byrne J., Mulvihill JJ, Myers MH, Connelly RR, Naughton MD, Krauss MR, Steinhorn SC, Hassinger DD et al., Effects of treatment on fertility in long-term survivors of childhood or adolescent cancer. N Engl J Med. 1987; 317: 1315– 1321. Byrne J., Rasmussen SA, Steinhorn SC, Connelly RR, Myers MH, Lynch CF, Flannery J., Austin DF et al., Genetic disease in offspring of long-term survivors of childhood and adolescent cancer. Am J Hum Genet. 1998; 62: 45– 52. Cai L., Hales BF, Robaire B. Induction of apoptosis in the germ cells of adult male rats after exposure to cyclophosphamide. Biol Reprod. 1997; 56: 1490– 1497. Chellman GJ, Bus JS, Working PK. Role of epididymal inflammation in the induction of dominant lethal mutations in Fischer 344 rat sperm by methyl chloride. Proc Natl Acad Sci USA. 1986a; 83: 8087– 8091. Chellman GJ, Morgan KT, Bus JS, Working PG. Inhibition of methyl chloride toxicity in male F-344 rats by the anti-inflammatory agent BW755C. Toxicol Appl Pharmacol. 1986b; 85: 367– 379. Clermont Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogenic renewal. Physiol Rev. 1972; 52: 198– 236. Correa A., Gray D., Cohen R., Rothman N., Saha F., Seacat H., Corn M. Ethylene glycol ethers and risk of spontaneous abortion and subfecundity. Am J Epidemiol. 1996; 143: 707– 717. Davis W. Jr., Schultz RM. Role of the first round of DNA replication in reprogramming gene expression in the preimplantation mouse embryo. Mol Reprod Dev. 1997; 47: 430– 434. Doerksen T., Trasler JM. Developmental exposure of male germ cells to 5-azacytidine results in abnormal preimplantation development in rats. Biol Reprod. 1996; 55: 1155– 1162. Doyle P., Maconochie N., Roman E., Davies G., Smith PG, Beral V. Fetal death and congenital malformation in babies born to nuclear industry employees: report from the nuclear industry family study. Lancet. 2000; 356: 1293– 1299. Edwards AJ, Anderson D., Brinkworth MH, Myers B., Parry JM. An investigation of male-mediated F1 effects in mice treated acutely and sub-chronically with urethane. Teratog Carcinog Mutagen. 1999; 19: 87– 103. Eskenazi B., Fenster L., Hudes M., Wyrobek AJ, Katz DF, Gerson J., Rempel DM. A study on the effect of perchloroethylene exposure on the reproductive outcomes of wives of dry cleaning workers. Am J Ind Med. 1991; 20: 593– 600. Fabricant JD, Legator MS, Adams PM. Post-meiotic cell mediation of behavior in progeny of male rats treated with cyclophosphamide. Mutat Res. 1983; 119: 185– 190. Fischbein A., Zabludovsky N., Eltes F., Grischenko V., Bartoov B. Ultramorphological sperm characteristics in the risk assessment of health effects after radiation exposure among salvage workers in Chernobyl. Environ Health Perspect. 1997; 105: 1445– 1449. Fraga CG, Motchnik PA, Wyrobek AJ, Rempel DM, Ames BN. Smoking and low anti-oxidant levels increase oxidative damage to sperm DNA. Mutat Res. 1996; 351: 199– 203. Gandley R., Anderson L., Silbergeld EK. Lead: male-mediated effects on reproduction and development in the rat. Environ Res. 1999; 80: 355– 363. Generoso WM, Cattanach B., Malashenko AM. Mutagenicity of selected chemicals in mammals; the heritable translocation test. In: FJ Serres, MD Shelby eds., Comparative Chemical Mutagenesis. Washington, NY: Plenum Press; 1981: 681– 707. Gray LE, Ostby S., Kelce WR. A dose-response analysis of the reproductive effects of a single gestational dose of 2,3,7,8-tetrachlorordibenzo-ρ-dioxin in male Long Evans hooded rat offspring. Toxicol Appl Pharmacol. 1997; 146: 11– 20. Green LM, Dodds L., Miller AB, Tomkins DJ, Li J., Escobar M. Risk of congenital anomalies in children of parents occupationally exposed to low level ionizing radiation. Occup Environ Med. 1997; 54: 629– 635. Guo YL, Hsu P. C., Hsu C. C., Lambert GH. Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. Lancet. 2000; 356: 1240– 1241. Hales BF, Crosman K., Robaire B. Increased postimplantation loss and malformations among the F2 progeny of male rats chronically treated with cyclophosphamide. Teratology. 1992; 45: 671– 678. Hales BF, Robaire B. Reversibility of the effects of chronic paternal exposure to cyclophosphamide on pregnancy outcome in rats. Mutat Res. 1990; 229: 129– 134. Hales BF, Smith S., Robaire B. Cyclophosphamide in the seminal fluid of treated males: transmission to females by mating and effects on progeny outcome. Toxicol Appl Pharmacol. 1986; 84: 423– 430. Harrouk W., Codrington A., Vinson R., Robaire B., Hales BF. Paternal exposure to cyclophosphamide induces DNA damage and alters the expression of DNA repair genes in the rat preimplantation embryo. Mutat Res. 2000a; 461: 229– 241. Harrouk W., Khatabaksh S., Robaire B., Hales BF. Paternal exposure to cyclophosphamide dysregulates the gene activation program in rat pre-implantation embryos. Mol Reprod Dev. 2000b; 57: 214– 223. Harrouk W., Robaire B., Hales BF. Paternal exposure to cyclophosphamide alters cell-cell contacts and activation of embryonic transcription in the pre-implantation rat embryo. Biol Reprod. 2000c; 63: 74– 81. Hjollund NHI, Bonde JPE, Jensen Kold T., Henriksen Brink T., Andersson A. M., Kolstad HA, Ernst E., Giwercman A. et al., Male-mediated spontaneous abortion among spouses of stainless steel welders. Scand J Work Environ Health. 2000; 26: 187– 192. Hooser SB, Van Dijk-Knijnenburg WCM, Waalkens-Berendsen IDH, Smits-van Prooije AE, Snoeij NJ, Baan RA, Fichtinger-Schepman AMJ. Cisplatin-DNA adduct formation in rat spermatozoa and its effect on fetal development. Cancer Lett. 2000; 151: 71– 80. Infante-Rivard C., Sinnett D. Preconceptional paternal exposure to pesticides and increased risk of childhood leukaemia. Lancet. 1999; 354: 1819. Irgens A., Krüger K., Ulstein M. The effect of male occupational exposure in infertile couples in Norway. J Occup Environ Med. 1999; 41: 1116– 1120. Kangasniemi M., Wilson G., Parchuri N., Huhtaniemi I., Meistrich ML. Rapid protection of rat spermatogenic stem cells against procarbazine by treatment with gonadotropin-releasing hormone antagonist (Nal-Glu) and an antiandrogen (flutamide). Endocrinology. 1995; 136: 2881– 2888. Kerjean A., Dupont J. M., Vasseur C., Le Tessier D., Cuisset L., Pàldi A., Jouannet P., Jeanpierre M. Establishment of the paternal methylation imprint of the human H19 and MEST/PEG1 genes during spermatogenesis. Hum Mol Genet. 2000; 9: 2183– 2187. Kolstad HA, Bisanti L., Roeleveld N., Bonde JPE, Joffe M. Time to pregnancy for men occupationally exposed to styrene in several European reinforced plastics companies. Asclepios. Scand J Work Environ Health. 1999a; 25 (suppl 1): 66– 69. Kolstad HA, Bonde JPE, Spano M., Giwercman A., Zschiesche W., Kaae D., Roeleveld N. Sperm chromatin structure and semen quality following occupational styrene exposure. Asclepios. Scand J Work Environ Health. 1999b; 25 (suppl 1): 70– 73. Li E., Beard C., Jaenisch R. Role for DNA methylation in genomic imprinting. Nature. 1993; 366: 362– 365. Andreu Lopez JA, Fernandez PJ, Ferris I., Tortajada J., Navarro I., Rodriguez-Ineba A., Antonio P., Muro MD, Romeu A. Persistent altered spermatogenesis in long-term childhood cancer survivors. Pediatr Hematol Oncol. 2000; 17: 21– 30. Lowe XR, de Stoppelaar JM, Bishop J., Cassel M., Hoebee B., Moore D. II, Wyrobek AJ. Epididymal sperm aneuploidies in three strains of rats detected by multicolor fluorescence in situ hybridization. Environ Mol Mutagen. 1998; 31: 125– 132. Luke GA, Ricches AC, Bryant PE. Genomic instability in haematopoietic cells of F1 generation mice of irradiated male parents. Mutagenesis. 1997; 12: 147– 152. Marchetti F., Lowe X., Bishop J., Wyrobek AJ. Induction of chromosomal aberrations in mouse zygotes by acrylamide treatment of male germ cells and their correlation with dominant lethality and heritable translocations. Environ Mol Mutagen. 1997; 30: 410– 417. Marchetti F., Lowe X., Bishop J., Wyrobek AJ. Absence of selection against aneuploid sperm at fertilization. Biol Reprod. 1999; 61: 948– 954. Martin RH. Human sperm chromosome complements in chemotherapy patients and infertile men. Chromosoma. 1998; 107: 523– 527. Martin RH, Rademaker AW, Hildebrand K., Barnes M., Arthur K., Ringrose T., Brown IS, Douglas G. A comparison of chromosomal aberrations induced by in vivo radiotherapy in human sperm and lymphocytes. Mutat Res. 1989; 226: 21– 30. Martin RH, Rademaker AW, Leonard NJ. Analysis of chromosomal abnormalities in human sperm after chemotherapy by karyotyping and fluorescence in situ hybridization (FISH). Cancer Genet Cytogenet. 1995; 80: 29– 32. Meistrich ML. Hormonal stimulation of the recovery of spermatogenesis following chemo- or radiotherapy. APMIS. 1998; 106: 37– 46. Mocarelli P., Gerthoux PM, Ferrari E., Patterson DG Jr, Kietszak SM, Brambilla P., Vincoli N., Signorini S. et al., Paternal concentrations of dioxin and sex ratio of offspring. Lancet. 2000; 355: 1858– 1863. Nagao T., Fujikawa K. Male-mediated teratogenesis: spectrum of congenital malformations in the offspring of A/J male mice treated with ethylnitrosourea. Teratog Carcinog Mutagen. 1996, 16: 301– 305. Neel JV, Schull WJ The effects of exposure to the atomic bombs on pregnancy termination in Hiroshima and Nagasaki. Washington, DC: National Academy of Sciences—National Research Council; 1956. Neuber E., Havari E., Sanchez Aquiles J., Powers RD, Wangh LJ. Efficient human sperm pronucleus formation and replication in Xenopus egg extracts. Biol Reprod. 1999; 61: 912– 920. Obata Y., Kaneko-Ishino T., Koide T., Takai Y., Ueda T., Domeki I., Shiroishi T., Ishino F., Kono T. Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development. 1998; 125: 1553– 1560. Olivennes F., Kerbrat V., Rufat P., Blanchet V., Fanchin R., Frydman R. Follow-up of a cohort of 422 children aged 6 to 13 years conceived by in vitro fertilization. Fertil Steril. 1997; 67: 284– 289. AF Olshan, DR Mattison eds., Male-Mediated Developmental Toxicity. Washington, NY: Plenum Press; 1994. Otake M., Schull WJ, Neel JV. Congenital malformations, stillbirths, and early mortality among the children of atomic bomb survivors: a reanalysis. Radiat Res. 1990; 122: 1– 11. Palermo GD, Colombero LT, Schattman GL, Davis OK, Rosenwaks Z. Evolution of pregnancies and initial follow-up of newborns delivered after intracytoplasmic sperm injection. JAMA. 1996; 276: 1893– 1897. Parker L., Pearce MS, Dickinson HO, Aitkin M., Craft AW. Stillbirths among offspring of male radiation workers at Sellafield nuclear reprocessing plant. Lancet. 1999; 354: 1407– 1414. Pichini S., Zuccaro P., Pacifici R. Drugs in semen. Clin Pharmacokinet. 1994; 26: 356– 373. Potashnik G., Yanai-Inbar I., Sacks MI, Israeli R. Effect of dibromochloropropane on human testicular function. Isr J Med Sci. 1979; 15: 438– 442. Qiu J., Hales BF, Robaire B. Adverse effects of cyclophosphamide on progeny outcome can be mediated through post-testicular mechanisms in the rat. Biol Reprod. 1992; 46: 926– 931. Qiu J., Hales BF, Robaire B. Damage to rat spermatozoal DNA after chronic cyclophosphamide exposure. Biol Reprod. 1995a; 53: 1465– 1473. Qiu J., Hales BF, Robaire B. Effects of chronic low dose cyclophosphamide exposure on the nuclei of rat spermatozoa. Biol Reprod. 1995b; 52: 33– 40. Quintanilla-Vega B., Hoover DJ, Bal W., Silbergeld EK, Waalkes MP, Anderson LD. Lead interaction with human protamine (HP2) as a mechanism of male reproductive toxicity. Chem Res Toxicol. 2000; 13: 594– 600. Robaire B., Hales BF. The male germ cell as a target for drug and toxicant action. In: C. Gagnon ed., The Male Gamete: From Basic Science to Clinical Applications. Washington, Fla: Cache River Press; 1999: 469– 474. Robbins WA, Meistrich ML, Moore D., Hagemeister FB, Weier HU, Cassel MJ, Wilson G., Eskenazi B., Wyrobek AJ. Chemotherapy induces transient sex chromosomal and autosomal aneuploidy in human sperm. Nat Genet. 1997; 16: 74– 78. Rubes J., Lowe X., Moore D. II, Perreault S., Slott V., Evenson D., Selevan SG, Wyrobek AJ. Smoking cigarettes is associated with increased sperm disomy in teenage men. Fertil Steril. 1998; 70: 715– 723. Russell LB. Effects of spermatogenic cell type on quantity and quality of mutations. In: DR Mattison, AF Olshan eds., Male-Mediated Developmental Toxicity. Washington, NY: Plenum Press; 1994: 37– 48. Sadowy S., Tomkin G., Munné S., Ferrara-Congedo T., Cohen J. Impaired development of zygotes with uneven pronuclear size. Zygote. 1998; 6: 137– 141. Sallmén M., Lindbohm M. L., Anttila A., Kyyrönen P., Taskinen H., Nykyri E., Hemminki K. Time to pregnancy among the wives of men exposed to organic solvents. Occup Environ Med. 1998; 55: 24– 30. Sallmén M., Lindbohm M. L., Anttila A., Taskinen H., Hemminki K. Time to pregnancy among the wives of men exposed to lead. Epidemiology. 2000a; 11: 141– 147. Sallmén M., Lindbohm M. L., Nurminen M. Paternal exposure to lead and infertility. Epidemiology. 2000b; 11: 148– 152. Sawyer DE, Brown DB. Diminished decondensation and DNA synthesis in activated sperm from rats treated with cyclophosphamide. Toxicol Lett. 2000; 14: 19– 26. Shibuya T., Horiya N., Matsuda H., Sakamoto K., Hara T. Dose-dependent induction of recessive mutations with N-ethyl-N-nitrosourea in primordial germ cells of male mice. Mutat Res. 1996, 357: 219– 224. Hikim Sinha AP, Swerdloff RS. Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod. 1999; 4: 38– 47. Sotomayor RE, Cumming RB. Induction of translocations by cyclophosphamide in different germ cell stages of male mice: cytological characterization and transmission. Mutat Res. 1975; 27: 375– 388. Soyka LF, Peterson JM, Joffe JM. Lethal and sublethal effects on the progeny of male rats treated with methadone. Toxicol Appl Pharmacol. 1978; 45: 797– 807. Stancheva I., Meehan RR. Transient depletion of xDnmt1 leads to premature gene activation in Xenopus embryos. Genes Dev. 2000; 14: 313– 327. Surani MAH, Barton SC, Norris ML. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature. 1984; 308: 548– 550. Sutcliffe AG, Taylor B., Li J., Thornton S., Grudzinskas JG, Lieberman BA. Children born after intracytoplasmic sperm injection: a population control study. BMJ. 1999; 318: 704– 705. Tielemans E., Van Kooij R., Velde ER, Burdorf A., Heederik D. Pesticide exposure and decreased fertilization rates in vitro. Lancet. 1999; 354: 484– 485. Tielemans E., Van Kooij R., Looman C., Burdof A., Velde E., Heederik D. Paternal occupational exposures and embryo implantation rates after IVF. Fertil Steril. 2000; 74: 690– 695. Thonneau P., Abell A., Larsen SB, Bonde JP, Joffe M., Clavert A., Ducot B., Multigner L., Danscher G. Effects of pesticide exposure on time to pregnancy. Results of a multicenter study in France and Denmark. Am J Epidemiol. 1999; 150: 157– 163. Trasler JM, Hales BF, Robaire B. Paternal cyclophosphamide treatment of rats causes fetal loss and malformations without affecting male fertility. Nature. 1985; 316: 144– 146. Trasler JM, Hales BF, Robaire B. Chronic low dose cyclophosphamide treatment of adult male rats: effect on fertility, pregnancy outcome and progeny. Biol Reprod. 1986; 34: 275– 283. Trasler JM, Hales BF, Robaire B. A time course study of chronic paternal cyclophosphamide treatment in rats: effects on pregnancy outcome and the male reproductive and hematologic systems. Biol Reprod. 1987; 37: 317– 326. Trasler J., Doerksen T. Teratogen update: paternal exposures—reproductive risks. Teratology. 1999; 60: 161– 172. Vine MF, Setzer RW Jr, Everson RB, Wyrobek AJ. Human sperm morphometry and smoking, caffeine, and alcohol consumption. Reprod Toxicol. 1997; 11: 179– 185. Whorton MD, Krauss RM, Marshall S., Milby TH. Infertility in male pesticide workers. Lancet. 1977; II: 1259– 1261. Wyrobek AJ, Robbins WA, Mehraein Y., Pinkel D., Weier H. U. Detection of sex-chromosomal aneuploidies X-X, Y-Y, and X-Y in human sperm using two-color chromosome fluorescence in situ hybridization. Am J Med Genet. 1994; 53: 1– 7. Citing Literature Volume22, Issue6November‐December 2001Pages 927-936 ReferencesRelatedInformation