Abstract

Introduction: Robertsonian translocation (RobT) is the central fusion of the long arms of two acrocentric chromosomes, leading to 45 chromosomes in humans. The most common ones are rob(13;14) and rob(14;21) (91%). Other types of RobT are so-called rare cases. In the general population RobTs occur with a frequency of approximately 0.123%, but among men with reproductive failure this value rises 9-fold. Infertility in RobT carriers is associated with the formation of unbalanced spermatozoa resulting from segregation of the chromosomes involved in trivalent during the meiotic prophase. In spermatozoa of many RobT carriers an increased level of chromosomal aneuploidy is observed. Materials and Methods: We examined the hyperhaploidy level of chromosomes 7, 9, 18, 21, 22, X and Y in spermatozoa of 6 RobT unrelated carriers: two carriers with rare rob(13;15), one with rare rob(13;22), and three of the common rob(13;14). Results were compared with the control data from a group of 7 fertile men with a normal karyotype. Fluorescent in situ hybridization (FISH) was applied. Results: We found an increased level of sperm aneuploidy regarding at least one of the analyzed chromosomes in each of the carriers, while in rare RobTs interchromosomal effect (ICE) was observed. Meiotic segregation pattern of a rare rob(13;15) carrier revealed the 76% of normal /balanced spermatozoa. Disucussion: Due to the relatively high population frequency of RobTs, their influence on reproductive failure, hight risk of imbalancement in prenatal diagnosis (7%), and small amount of data for rare RobTs, each newly characterized case is valuable in genetic counseling.

References

• 1. Acar H., Yildirim M.S., Cora T., Ceylaner S.: Evaluation of segregationpatterns of 21;21 Robertsonian translocation along with sex chromosomesand interchromosomal effects in sperm nuclei of carrier by FISHtechnique. Mol. Reprod. Dev., 2002; 63: 232–236
  Google Scholar
• 2. Agarwal A., Mulgund A., Hamada A., Chyatte M.R.: A unique view onmale infertility around the globe. Reprod. Biol. Endocrinol., 2015; 13: 37
  Google Scholar
• 3. Anahory T., Hamamah S., Andréo B., Hédon B., Claustres M., SardaP., Pellestor F.: Sperm segregation analysis of a (13;22) Robertsoniantranslocation carrier by FISH: A comparison of locus-specific probeand whole chromosome painting. Hum. Reprod., 2005; 20: 1850–1854
  Google Scholar
• 4. Anton E., Blanco J., Egozcue J., Vidal F.: Sperm FISH studies in sevenmale carriers of Robertsonian translocation t(13;14)(q10;q10). Hum.Reprod., 2004; 19: 1345–1351
  Google Scholar
• 5. Anton E., Blanco J., Vidal F.: Meiotic behavior of three D;G Robertsoniantranslocations: Segregation and interchromosomal effect. J.Hum. Genet., 2010; 55: 541–545
  Google Scholar
• 6. Anton E., Vidal F., Blanco J.: Interchromosomal effect analyses bysperm FISH: Incidence and distribution among reorganization carriers.Syst. Biol. Reprod. Med., 2011; 57: 268–278
  Google Scholar
• 7. Aurias A., Prieur M., Dutrillaux B., Lejeune J.: Systematic analysisof 95 translocations of autosomes. Hum. Genet., 1978; 45: 259–282
  Google Scholar
• 8. Baccetti B., Collodel G., Marzella R., Moretti E., Piomboni P., ScapigliatiG., Serafini F.: Ultrastructural studies of spermatozoa from infertilemales with Robertsonian translocations and 18, X, Y aneuploidies.Hum. Reprod., 2005; 20: 2295–2300
  Google Scholar
• 9. Balasar Ö., Acar H.: Investigation of the interchromosomal effects inmale carriers with structural chromosomal abnormalities using FISH.Turk. J. Urol., 2020; 46: 178–185
  Google Scholar
• 10. Bernicot I., Schneider A., Mace A., Hamamah S., Hedon B., PellestorF., Anahory T.: Analysis using fish of sperm and embryos from two carriersof rare rob(13;21) and rob(15;22) robertsonian translocation undergoingPGD. Eur. J. Med. Genet., 2012; 55: 245–251
  Google Scholar
• 11. Blanco J., Egozcue J., Vidal F.: Interchromosomal effects for chromosome 21 in carriers of structural chromosome reorganizations determinedby fluorescencein in situ hybridization on sperm nuclei. Hum.Genet., 2000; 106: 500–505
  Google Scholar
• 12. Brugnon F., Janny L., Communal Y., Darcha C., Szczepaniak C.,Pellestor F., Vago P., Pons-Rejraji H., Artonne C., Grizard G.: Apoptosisand meiotic segregation in ejaculated sperm from Robertsonian translocationcarrier patients. Hum. Reprod., 2010; 25: 1631–1642
  Google Scholar
• 13. Brugnon F., Van Assche E., Verheyen G., Sion B., Boucher D., PoulyJ.L., Janny L., Devroey P., Liebaers I., Van Steirteghem A.: Study of twomarkers of apoptosis and meiotic segregation in ejaculated sperm ofchromosomal translocation carrier patients. Hum. Reprod., 2006; 21:685–693
  Google Scholar
• 14. Cassuto N.G., Le Foll N., Chantot-Bastaraud S., Balet R., Bouret D.,Rouen A., Bhouri R., Hyon C., Siffroi J.P.: Sperm fluorescence in situhybridization study in nine men carrying a Robertsonian or a reciprocaltranslocation: Relationship between segregation modes and highmagnificationsperm morphology examination. Fertil. Steril., 2011;96: 826–832
  Google Scholar
• 15. Chandley A.C., Maclean N., Edmond P., Fletcher J., Watson G.S.: Cytogeneticsand infertility in man. II. Testicular histology and meiosis.Ann. Hum. Genet., 1976; 40: 165–176
  Google Scholar
• 16. Chantot-Bastaraud S., Ravel C., Siffroi J.P.: Underlying karyotypeabnormalities in IVF/ICSI patients. Reprod. Biomed. Online, 2008; 16:514–522
  Google Scholar
• 17. Chen Y., Huang J., Liu P., Qiao J.: Analysis of meiotic segregationpatterns and interchromosomal effects in sperm from six males withRobertsonian translocations. J. Assist. Reprod. Genet., 2007; 24: 406–411
  Google Scholar
• 18. Choo K.H., Vissel B., Brown R., Filby R.G., Earle E.: Homologous alphasatellite sequences on human acrocentric chromosomes with selectivityfor chromosomes 13, 14 and 21: Implications for recombination betweennonhomologues and Robertsonian translocations. Nucleic AcidsRes., 1988; 16: 1273–1284
  Google Scholar
• 19. Douet-Guilbert N., Bris M.J., Amice V., Marchetti C., Delobel B., AmiceJ., Braekeleer M.D., Morel F.: Interchromosomal effect in sperm of maleswith translocations: Report of 6 cases and review of the literature. Int.J. Androl., 2005; 28: 372–379
  Google Scholar
• 20. Dutrillaux B., Lejeune J.: Study of progeny of individuals bearing at(DqDq) translocation. Ann. Genet., 1970; 13: 11–18
  Google Scholar
• 21. Egozcue S., Blanco J., Vendrell J.M, García F., Veiga A., Aran B., BarriP.N, Vidal F., Egozcue J.: Human male infertility: Chromosome anomalies,meiotic disorders, abnormal spermatozoa and recurrent abortion.Hum. Reprod. Update, 2000; 6: 93–105
  Google Scholar
• 22. Escudero T., Lee M., Carrel D., Blanco J., Munné S.: Analysis of chromosomeabnormalities in sperm and embryos from two 45,XY,t(13;14)(q10;q10) carriers. Prenat. Diagn., 2000; 20: 599–602
  Google Scholar
• 23. Ferfouri F., Selva J., Boitrelle F., Gomes D.M., Torre A., Albert M., BaillyM., Clement P., Vialard F.: The chromosomal risk in sperm from heterozygousRobertsonian translocation carriers is related to the spermcount and the translocation type. Fertil. Steril., 2011; 96: 1337–1343
  Google Scholar
• 24. Ferlin A., Arredi B., Foresta C.: Genetic causes of male infertility.Reprod. Toxicol., 2006; 22: 133–141
  Google Scholar
• 25. Frydman N., Romana S., Le Lorc’h M., Vekemans M., Frydman R.,Tachdjian G.: Assisting reproduction of infertile men carrying a Robertsoniantranslocation. Hum. Reprod., 2001; 16: 2274–2277
  Google Scholar
• 26. Godo A., Blanco J., Vidal F., Sandalinas M., Garcia-Guixé E., Anton E.:Altered segregation pattern and numerical chromosome abnormalitiesinterrelate in spermatozoa from Robertsonian translocation carriers.Reprod. Biomed. Online, 2015; 31: 79–88
  Google Scholar
• 27. Haidich A.B.: Meta-analysis in medical research. Hippokratia, 2010;14: 29–37
  Google Scholar
• 28. Hajlaoui A., Slimani W., Kammoun M., Sallem A., Braham S., BibiM., Saad A., Mougou-Zerelli S.: Sperm fluorescent in situ hybridisationstudy of interchromosomal effect in six Tunisian carriers of reciprocaland Robertsonian translocations. Andrologia, 2018; 50: e12949
  Google Scholar
• 29. Han J.Y., Choo K.H., Shaffer L.G.: Molecular cytogenetic characterizationof 17 rob(13q14q) Robertsonian translocations by FISH, narrowingthe region containing the breakpoints. Am. J. Hum. Genet., 1994;55: 960–967
  Google Scholar
• 30. Hassold T., Hunt P.: To err (meiotically) is human: The genesis ofhuman aneuploidy. Nat. Rev. Genet., 2001; 2: 280–291
  Google Scholar
• 31. Hatakeyama C., Gao H., Harmer K., Ma S.: Meiotic segregation patternsand ICSI pregnancy outcome of a rare (13;21) Robertsonian translocationcarrier: A case report. Hum. Reprod., 2006; 21: 976–979
  Google Scholar
• 32. Honda H., Miharu N., Samura O., He H., Ohama K.: Meiotic segregationanalysis of a 14;21 Robertsonian translocation carrier by fluorescencein situ hybridization. Hum. Genet., 2000; 106: 188–193
  Google Scholar
• 33. Hook E.B.: Exclusion of chromosomal mosaicism: Tables of 90%,95%, and 99% confidence limits and comments on use. Am. J. Hum.Genet., 1977; 29: 94–97
  Google Scholar
• 34. Ioannou D., Fortun J., Tempest H.G.: Meiotic nondisjunction andsperm aneuploidy in humans. Reproduction, 2019; 157: R15–R31
  Google Scholar
• 35. Ioannou D., Tempest H.G.: Meiotic nondisjunction: Insights intothe origin and significance of aneuploidy in human spermatozoa. Adv.Exp. Med. Biol., 2015; 868: 1–21
  Google Scholar
• 36. Jarmuz-Szymczak M., Janiszewska J., Szyfter K., Shaffer L.G.: Narrowingthe localization of the region breakpoint in most frequent Robertsoniantranslocations. Chromosome. Res., 2014; 22: 517–532
  Google Scholar
• 37. Kékesi A., Erdei E., Török M., Drávucz S., Tóth A.: Segregation ofchromosomes in spermatozoa of four Hungarian translocation carriers.Fertil. Steril., 2007; 88: 212.e5–11
  Google Scholar
• 38. Kim S.R., Shaffer L.G.: Roberstonian translocations: Mechanisms offormation, aneuploidy, and uniparental disomy and diagnostic considerations.Genet. Test., 2002; 6: 163–168
  Google Scholar
• 39. Kirkpatrick G., Ferguson K.A., Gao H., Tang S., Chow V., Yuen B.H., MaS.: A comparison of sperm aneuploidy rates between infertile men withnormal and abnormal karyotypes. Hum. Reprod., 2008; 23: 1679–1683
  Google Scholar
• 40. Kirkpatrick G., Ren H., Liehr T., Chow V., Ma S.: Meiotic and spermaneuploidy studies in three carriers of Robertsonian translocationsand small supernumerary marker chromosomes. Fertil. Steril., 2015;103: 1162–1169
  Google Scholar
• 41. Lamotte A., Martinez G., Devillard F., Hograindleur J.P., Satre V.,Coutton C., Harbuz R., Amblard F., Lespinasse J., Benchaib M., BessonnatJ., Brouillet S., Hennebicq S.: Is sperm FISH analysis still useful forRobertsonian translocations? Meiotic analysis for 23 patients and reviewof the literature. Basic. Clin. Androl., 2018; 28: 5
  Google Scholar
• 42. Luciani J.M., Guichaoua M.R., Mattei A., Morazzani M.R.: Pachyteneanalysis of a man with a 13q;14q translocation and infertility. Behaviorof the trivalent and nonrandom association with the sex vesicle. Cytogenet.Cell Genet., 1984; 38: 14–22
  Google Scholar
• 43. Machev N., Gosset P., Warter S., Treger M., Schillinger M., VivilleS.: Fluorescence in situ hybridization sperm analysis of six translocationcarriers provides evidence of an interchromosomal effect. Fertil.Steril., 2005; 84: 365–373
  Google Scholar
• 44. Mahjoub M., Mehdi M., Brahem S., Elghezal H., Ibala S., Saad A.:Chromosomal segregation in spermatozoa of five Robertsonian translocationcarriers t(13;14). J. Assist. Reprod. Genet., 2011; 28: 607–613
  Google Scholar
• 45. Martin R.H.: Cytogenetic analysis of sperm from a male heterozygousfor a 13;14 Robertsonian translocation. Hum. Genet., 1988; 80:357–361
  Google Scholar
• 46. Martin R.H., Ko E., Hildebrand K.: Analysis of sperm chromosomecomplements from a man heterozygous for a robertsonian translocation45,XY,t(15q;22q). Am. J. Med. Genet., 1992; 43: 855–857
  Google Scholar
• 47. Mau-Holzmann U.A.: Somatic chromosomal abnormalities in infertilemen and women. Cytogenet. Genome. Res., 2005; 111: 317–336
  Google Scholar
• 48. Mayeur A., Ahdad N., Hesters L., Brisset S., Romana S., Tosca L.,Tachdjian G., Frydman N.: Chromosomal translocations and semenquality: A study on 144 male translocation carriers. Reprod. Biomed.Online, 2019; 38: 46–55
  Google Scholar
• 49. McGowan-Jordan J., Simons A., Schmid M.: ISCN 2016: An InternationalSystem for Human Cytogenomic Nomenclature (2016). Karger,Basel 2016
  Google Scholar
• 50. Mennicke K., Diercks P., Schlieker H., Bals-Pratsch M., al Hasani S.,Diedrich K., Schwinger E.: Molecular cytogenetic diagnostics in sperm.Int. J. Androl., 1997; 20: 11–19
  Google Scholar
• 51. Moradkhani K., Puechberty J., Bhatt S., Lespinasse J., Vago P., LefortG., Sarda P., Hamamah S., Pellestor F.: Rare Robertsonian translocationsand meiotic behaviour: Sperm FISH analysis of t(13;15) and t(14;15)translocations: a case report. Hum. Reprod., 2006; 21: 3193–3198
  Google Scholar
• 52. Moradkhani K., Puechberty J., Bhatt S., Vago P., Janny L., Lefort G.,Hamamah S., Sarda P., Pellestor F.: Meiotic segregation of rare Robertsoniantranslocations: Sperm analysis of three t(14q;22q) cases. Hum.Reprod., 2006; 21: 1166–1171
  Google Scholar
• 53. Morel F., Roux C., Bresson J.L.: FISH analysis of the chromosomalstatus of spermatozoa from three men with 45,XY,der(13;14)(q10;q10)karyotype. Mol. Hum. Reprod., 2001; 7: 483–488
  Google Scholar
• 54. Nielsen J., Wohlert M.: Chromosome abnormalities found among34,910 newborn children: Results from a 13-year incidence study inArhus, Denmark. Hum. Genet., 1991; 87: 81–83
  Google Scholar
• 55. Nishikawa N., Sato T., Suzumori N., Sonta S., Suzumori K.: Meioticsegregation analysis in male translocation carriers by using fluorescentin situ hybridization. Int. J. Androl., 2008; 31: 60–66
  Google Scholar
• 56. Ogawa S., Araki S., Araki Y., Ohno M., Sato I.: Chromosome analysisof human spermatozoa from an oligoasthenozoospermic carrier for a13;14 Robertsonian translocation by their injection into mouse oocytes.Hum. Reprod., 2000; 15: 1136–1139
  Google Scholar
• 57. Ogur G., Van Assche E., Vegetti W., Verheyen G., Tournaye H., BonduelleM., Van Steirteghem A., Liebaers I.: Chromosomal segregationin spermatozoa of 14 Robertsonian translocation carriers. Mol. Hum.Reprod., 2006; 12: 209–215
  Google Scholar
• 58. Olszewska M., Fraczek M., Huleyuk N., Czernikiewicz A., Wiland E.,Boksa M., Zastavna D., Panasiuk B., Midro A.T., Kurpisz M.: Chromatinstructure analysis of spermatozoa from reciprocal chromosome translocation(RCT) carriers with known meiotic segregation patterns. Reprod.Biol., 2013; 13: 209–220
  Google Scholar
• 59. Olszewska M., Huleyuk N., Fraczek M., Zastavna D., Wiland E., KurpiszM.: Sperm FISH and chromatin integrity in spermatozoa from at(6;10;11) carrier. Reproduction, 2014; 147: 659–670
  Google Scholar
• 60. Page S.L., Shaffer L.G.: Nonhomologous Robertsonian translocationsform predominantly during female meiosis. Nat. Genet., 1997;15: 231–232
  Google Scholar
• 61. Page S.L., Shin J.C., Han J.Y., Choo K.H., Shaffer L.G.: Breakpoint diversityillustrates distinct mechanisms for Robertsonian translocationformation. Hum. Mol. Genet., 1996; 5: 1279–1288
  Google Scholar
• 62. Pellestor F.: Analysis of meiotic segregation in a man heterozygousfor a 13;15 Robertsonian translocation and a review of the literature.Hum. Genet., 1990; 85: 49–54
  Google Scholar
• 63. Pellestor F., Imbert I., Andréo B., Lefort G.: Study of the occurrenceof interchromosomal effect in spermatozoa of chromosomal rearrangementcarriers by fluorescence in-situ hybridization and primed in-situlabelling techniques. Hum. Reprod., 2001; 16: 1155–1164
  Google Scholar
• 64. Pellestor F., Sele B., Jalbert H.: Chromosome analysis of spermatozoafrom a male heterozygous for a 13;14 Robertsonian translocation.Hum. Genet., 1987; 76: 116–120
  Google Scholar
• 65. Perrin A., Morel F., Douet-Guilbert N., Le Bris M.J., Amice J., AmiceV., De Braekeleer M.: A study of meiotic segregation of chromosomesin spermatozoa of translocation carriers using fluorescent in situ hybridisation.Andrologia, 2010; 42: 27–34
  Google Scholar
• 66. Perrin A., Nguyen M.H., Bujan L., Vialard F., Amice V., GuéganicN., Douet-Guilbert N., De Braekeleer M., Morel F.: DNA fragmentationis higher in spermatozoa with chromosomally unbalanced content inmen with a structural chromosomal rearrangement. Andrology, 2013;1: 632–638
  Google Scholar
• 67. Pylyp L.Y., Zukin V.D., Bilko N.M.: Chromosomal segregation insperm of Robertsonian translocation carriers. J. Assist. Reprod. Genet.,2013; 30: 1141–1145
  Google Scholar
• 68. Rives N., Ravel C., Duchesne V., Siffroi J.P., Mousset-Siméon N., MacéB.: Molecular cytogenetics analysis with whole chromosome paintprobes of sperm nuclei from a (13;15) Robertsonian translocation carrier.J. Hum. Genet., 2005; 50: 360–364
  Google Scholar
• 69. Rogenhofer N., Dürl S., Ochsenkühn R., Neusser M., Aichinger E.,Thaler C.J., Müller S.: Case report: Elevated sperm aneuploidy levels inan infertile Robertsonian translocation t(21;21) carrier with possibleinterchromosomal effect. J. Assist. Reprod. Genet., 2012; 29: 343–346
  Google Scholar
• 70. Rouen A., Balet R., Dorna M., Hyon C., Pollet-Villard X., Chantot-Bastaraud S., Joyé N., Portnoï M.F., Cassuto N.G., Siffroi J.P.: Discontinuousgradient centrifugation (DGC) decreases the proportion of chromosomallyunbalanced spermatozoa in chromosomal rearrangementcarriers. Hum. Reprod., 2013; 28: 2003–2009
  Google Scholar
• 71. Rouen A., Carlier L., Heide S., Egloff M., Marzin P., Ader F., SchwartzM., Rogers E., Joyé N., Balet R., Lédée N., Prat-Ellenberg L., Cassuto N.G.,Siffroi J.P.: Potential selection of genetically balanced spermatozoa basedon the hypo-osmotic swelling test in chromosomal rearrangement carriers.Reprod. Biomed. Online, 2017; 35: 372–378
  Google Scholar
• 72. Rousseaux S., Chevret E., Monteil M., Cozzi J., Pelletier R., DelafontaineD., Sèle B.: Sperm nuclei analysis of a Robertsonian t(14q21q) carrier,by FISH, using three plasmids and two YAC probes. Hum. Genet.,1995; 96: 655–660
  Google Scholar
• 73. Roux C., Tripogney C., Morel F., Joanne C., Fellmann F., ClavequinM.C., Bresson J.L.: Segregation of chromosomes in sperm of Robertsoniantranslocation carriers. Cytogenet. Genome. Res., 2005; 111: 291–296
  Google Scholar
• 74. Sarrate Z., Vidal F., Blanco J.: Role of sperm fluorescent in situ hybridizationstudies in infertile patients: Indications, study approach,and clinical relevance. Fertil. Steril., 2010; 93: 1892–1902
  Google Scholar
• 75. Scriven P.N., Flinter F.A, Braude P.R., Ogilvie C.M.: Robertsoniantranslocations – reproductive risks and indications for preimplantationgenetic diagnosis. Hum. Reprod., 2001; 16: 2267–2273
  Google Scholar
• 76. Seabright M.: A rapid banding technique for human chromosomes.Lancet, 1971; 2: 971–972
  Google Scholar
• 77. Shi Q., Martin R.H.: Aneuploidy in human spermatozoa: FISH analysisin men with constitutional chromosomal abnormalities, and in infertilemen. Reproduction, 2001; 121: 655–666
  Google Scholar
• 78. Sobotka V., Vozdova M., Heracek J., Rubes J.: A rare Robertsoniantranslocation rob(14;22) carrier with azoospermia,meiotic defects, andtesticular sperm aneuploidy. Syst. Biol. Reprod. Med., 2015; 61: 245–250
  Google Scholar
• 79. Song J., Li X., Sun L., Xu S., Liu N., Yao Y., Liu Z., Wang W., Rong H.,Wang B.: A family with Robertsonian translocation: A potential mechanismof speciation in humans. Mol. Cytogenet., 2016; 9: 48
  Google Scholar
• 80. Syme R.M., Martin R.H.: Meiotic segregation of a 21;22 Robertsoniantranslocation. Hum. Reprod., 1992; 7: 825–829
  Google Scholar
• 81. Tempest H.G., Ko E., Rademaker A., Chan P., Robaire B., Martin R.H.:Intra-individual and inter-individual variations in sperm aneuploidyfrequencies in normal men. Fertil. Steril., 2009; 91: 185–192
  Google Scholar
• 82. Therman E., Susman B., Denniston C.: The nonrandom participationof human acrocentric chromosomes in Robertsonian translocations.Ann. Hum. Genet., 1989; 53: 49–65
  Google Scholar
• 83. Vegetti W., Van Assche E., Frias A., Verheyen G., Bianchi M.M., BonduelleM., Liebaers I., Van Steirteghem A.: Correlation between semenparameters and sperm aneuploidy rates investigated by fluorescencein-situ hybridization in infertile men. Hum. Reprod., 2000; 15: 351–365
  Google Scholar
• 84. Veld P.A., Weber R.F., Los F.J., den Hollander N., Dhont M., PietersM.H., Van Hemel J.O.: Two cases of Robertsonian translocations in oligozoospermicmales and their consequences for pregnancies inducedby intracytoplasmic sperm injection. Hum. Reprod., 1997; 12: 1642–1644
  Google Scholar
• 85. Vozdova M., Oracova E., Kasikova K., Prinosilova P., Rybar R., HorinovaV., Gaillyova R., Rubes J.: Balanced chromosomal translocations inmen: Relationships among semen parameters, chromatin integrity,sperm meiotic segregation and aneuploidy. J. Assist. Reprod. Genet.,2013; 30: 391–405
  Google Scholar
• 86. Wang B., Nie B., Tang D., Li R., Liu X., Song J., Wang W., Liu Z.:Analysis of meiotic segregation patterns and interchromosomal effects in sperm from 13 Robertsonian translocations. Balkan J. Med.Genet., 2017; 20: 43–50
  Google Scholar
• 87. Wiland E., Olszewska M., Huleyuk N., Chernykh V.B., KurpiszM.: The effect of Robertsonian translocation on the intranuclearpositioning of NORs (nucleolar organizing regions) in human spermcells. Sci. Rep., 2019; 9: 2213
  Google Scholar
• 88. World Health Organization: WHO laboratory manual for the examinationand processing of human semen, 5th ed. World Health Organization,2010
  Google Scholar
• 89. Xu S., Tang D., Fang K., Xia Y., Song J., Wang W., Cheng M., WangB.: Analysis of meiotic segregation patterns and interchromosomal effectsin sperm from a Robertsonian translocation family. BiomedicalRes., 2014; 25: 233–239
  Google Scholar
• 90. Zhao W.W., Wu M., Chen F., Jiang S., Su H., Linag J., Deng C., Hu C.,Yu S.: Robertsonian translocations: An overview of 872 Robertsoniantranslocations identified in a diagnostic laboratory in China. PLoS One,2015; 10: 0122647
  Google Scholar

Full text