Advertisement

Intracytoplasmic Morphologically Selected Sperm Injection

  • Pierre Vanderzwalmen
  • Romain Imbert
  • David Jareno Martinez
  • Astrid Stecher
  • Anne Vansteenbrugge
  • Sabine Vanderzwalmen
  • Barbara Wirleitner
  • Maximillian Murtinger
Chapter

Abstract

Intracytoplasmic morphologically selected sperm injection (IMSI) provides the opportunity to deselect morphologically abnormal spermatozoa presenting large vacuole-like structures (VLS), decreasing the risk of birth defects. According to the growing body of literature, VLS most likely reflect anomalies of sperm chromatin packaging rendering the DNA, at least in part, more vulnerable to reactive oxygen species (ROS). The importance of repackaging of the haploid genome before delivery in the oocyte is a crucial step. It is reported that VLS are related to alteration in the methylation pattern (hypermethylation) secondary to chromatin condensation failures. All these potential epigenetic pattern disturbances may represent the basis of numerous disorders in the offspring as well as for the future generation.

Debates and skepticism still exist about the efficiency of IMSI, mainly due to a low number of controlled randomized studies published yet. IMSI is indeed important: in women with advanced maternal age, possibly due to reduced correction and reparation capacity of spermatozoon defects in presence of aging oocyte, and in patients with failure of embryo development to the blastocyst stage in a previous in vitro fertilization (IVF) attempt.

Keywords

Spermatozoa Vacuoles Chromatin condensation Epigenetic Hypermethylation Oocyte aging 

References

  1. 1.
    Vawda A, Gunby J, Younglai E. Semen parameters as predictors of in-vitro fertilization: the importance of strict criteria morphology. Hum Reprod. 1996;11:1445–50.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Nikolettos N, Kiipker W, Demirel C, Schopper B, Blasig C, Sturm R, Felberbaum R, Bauer O, Diedrich K, Al-Hasani S. Fertilization potential of spermatozoa with abnormal morphology. Hum Reprod. 1999;14(Suppl. 1):47–70.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    De Vos A, Van De Velde H, Joris H, Verheyen G, Devroey P, Van Steirteghem A. Influence of individual sperm morphology on fertilization, embryo morphology, and pregnancy outcome of intracytoplasmic sperm injection. Fertil Steril. 2003;79:42–8.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Garolla A, Fortini D, Menegazzo M, De Toni L, Nicoletti V, Moretti A, Selice R, Engl B, Foresta C. High power magnification microscopy and functional status analysis of sperm in the evaluation and selection before ICSI. Reprod Biomed Online. 2008;17:610–6.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Bartoov B, Berkovitz A, Eltes F. Selection of spermatozoa with normal nuclei to improve the pregnancy rate with intracytoplasmic sperm injection. N Engl J Med. 2001;345:1067–8.CrossRefGoogle Scholar
  6. 6.
    Coppola G, Di Caprio G, Wilding M, Ferraro P, Esposito G, Di Matteo L, Dale R, Coppola G, Dale B. Digital holographic microscopy for the evaluation of human sperm structure. Zygote. 2013:1–9.Google Scholar
  7. 7.
    Boitrelle F, Ferfouri F, Petit JM, Segretain D, Tourain C, Bergere M, Bailly M, Vialard F, Albert M, Selva J. Large human sperm vacuoles observed in motile spermatozoa under high magnification: nuclear thumbprints linked to failure of chromatin condensation. Hum Reprod. 2011;26:1650–8.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Thomas Huser T, Orme C, Hollars CW, Corzett M, Balhorn R. Raman spectroscopy of DNA packaging in individual human sperm cells distinguishes normal from abnormal cells. J Biophotonics. 2009;2:322–32.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Saidi R, Rives N, Gruel E, Mazurier S, Mousset-Simeon N, Mace B. New classification of spermatocytogram at high magnification. Med Repro Gyn Endo. 2008;10:315–24.Google Scholar
  10. 10.
    Perdrix A, Saïdi R, Ménard JF, Gruel E, Milazzo JP, Macé B, Rives N. Relationship between conventional sperm parameters and motile sperm organelle morphology examination (MSOME). Int J Androl. 2012;35:491–8.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Franco J, Baruffi R, Mauri A, Petersen C, Oliveira J, Vagnini L. Significance of large nuclear vacuoles in human spermatozoa: implications for ICSI. Reprod Biomed Online. 2008;17:42–5.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Vanderzwalmen P, Bach M, Baramsai B, Neyer A, Schwerda D, Stecher A, Wirleitner B, Zintz M, Lejeune B, Vanderzwalmen S, Cassuto G, Zech M, Zech NH. Intracytoplasmic Morphologically selected sperm injection. In: Nagy ZP, et al., editors. Practical manual of in vitro fertilization: advanced methods and Novel devices. Springer-Verlag New York: Springer Science; 2012. p. 229–40.CrossRefGoogle Scholar
  13. 13.
    Cassuto NG, Bouret D, Plouchart JM, Jellad S, Vanderzwalmen P, Balet R, Larue L, Barak Y. A new real-time morphology classification for human spermatozoa: a link for fertilization and improved embryo quality. Fertil Steril. 2009;92:1616–25.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Auger J, Eustache F, Andersen A, Irvine D, Jørgensen N, Skakkebaek N, Suominen J, Toppari J, Vierula M, Jouannet P. Sperm morphological defects related to environment, lifestyle and medical history of 1001 male partners of pregnant women from four European cities. Hum Reprod. 2011;16:2710–7.CrossRefGoogle Scholar
  15. 15.
    Westbrook VA, Diekman AB, Klotz KL, Khole VV, von Kap-Herr C, Golden WL, Eddy RL, Shows TB, Stoler MH, Lee CY, Flickinger CJ, Herr JC. Spermatid-specific expression of the novel X-linked gene product SPAN-X localized to the nucleus of human spermatozoa. Biol Reprod. 2000;63:469–81.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Watanabe S, Tanaka A, Fujii S, Mizunuma H. No relationship between chromosome aberrations and vacuole-like structures on human sperm head. Hum Reprod. 2009;24:i96.CrossRefGoogle Scholar
  17. 17.
    Chemes HE, Alvarez SC. Tales of the tail and sperm head aches: changing concepts on the prognostic significance of sperm pathologies affecting the head, neck and tail. Asian J Androl. 2012;141:14–23.CrossRefGoogle Scholar
  18. 18.
    Auger J, Dadoune JP. Nuclear status of human sperm cells by transmission Electron microscopy and image cytometry: changes in nuclear shape and chromatin texture during Spermiogenesis and Epididymal transit. Biol Reprod. 1993;49:166–75.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Ward WS. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod. 2010;16:30–6.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Zheng H, Stratton C, Morozumi K, Jin J, Yanagimachi R, Yan W. Lack of Spem1 causes aberrant cytoplasm removal, sperm deformation, and male infertility. PNAS. 2007;104:6852–7.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Rousseaux S, Boussouar F, Gaucher J, Reynoird N, Montellier E, Curtet S, Vitte AL, Khochbin S. Molecular models for post-meiotic male genome reprogramming. Syst Biol Reprod Med. 2011;57:50–3.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Montellier E, Boussouar F, Rousseaux S, Zhang K, Buchou T, Fenaille F, Shiota H, Debernardi A, Héry P, Curtet S, Jamshidikia M, Barral S, Holota H, Bergon A, Lopez F, Guardiola P, Pernet K, Imbert J, Petosa C, Tan M, Zhao Y, Gérard M, Khochbin S. Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev. 2013;27:1680–92.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Miller D, Brinkworth M, Iles D. Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction. 2010;139:287–301.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Tavalaee M, Razavi S, Nasr-Esfahani MH. Influence of sperm chromatin anomalies on assisted reproductive technology outcome. Fertil Steril. 2009;91:1119–26.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Oliva R, Ballesca JL. Altered histone retention and epigenetic modifications in the sperm of infertile men. Asian J Androl. 2012;14:239–40.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Hammoud SS, Nix DA, Hammoud AO, Gibson M, Cairns BR, Carrell DT. Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Hum Reprod. 2011;26:2558–69.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Berkovitz A, Eltes F, Yaari S, Katz N, Barr I, Fishman A, Bartoov B. The morphological normalcy of the sperm nucleus and pregnancy rate of intracytoplasmic injection with morphologically selected sperm. Hum Reprod. 2005;20:185–90.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Hazout A, Dumont-Hassan M, Junca AM, Cohen Bacrie P, Tesarik J. High-magnification ICSI overcomes paternal effect resistant to conventional ICSI. Reprod Biomed Online. 2006;12:19–25.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Tanaka A, Nagayoshi M, Tanaka I, Kuzunoki H. Human sperm head vacuoles are physiological structures formed during the sperm development and maturation process. Fertil Stertil. 2012;98:315–20.CrossRefGoogle Scholar
  30. 30.
    Mundy AJ, Ryder TA, Edmonds DK. A quantitative study of sperm head ultrastructure in subfertile males with excess sperm precursors. Fertil Steril. 1994;61:751–4.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Sakkas D, Juan G, Alvarez JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 2010;93:1027–36.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Mahfouz R, Sharma R, Thiyagarajan A, Kale V, Gupta S, Sabanegh E, Agarwal A. Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species. Fertil Steril. 2010;94:2141–6.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Perdrix A, Travers A, Chelli MH, Escalier D, Do Rego JL, Milazzo JP, Mousset-Siméon N, Macé B, Rives N. Assessment of acrosome and nuclear abnormalities in human spermatozoa with large vacuoles. Hum Reprod. 2011;26:47–58.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Cassuto NG, Hazout A, Hammoud I, Balet R, Bouret D, Barak Y, Jellad S, Plouchart JM, Selva J, Yazbeck C. Correlation between DNA defect and sperm-head morphology. Reprod Biomed Online. 2012;24:211–8.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Franco JG Jr, Mauri AL, Petersen CG, Massaro FC, Silva LF, Felipe V, Cavagna M, Pontes A, Baruffi RL, Oliveira JB, Vagnini LD. Large nuclear vacuoles are indicative of abnormal chromatin packaging in human spermatozoa. Int J Androl. 2012;35:46–51.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Boitrelle F, Albert M, Petit J-M, Ferfouri F, Wainer R, Bergere M, Bailly M, Vialard F, Selva J. Small human sperm vacuoles observed under high magnification are pocket-like nuclear concavities linked to chromatin condensation failure. Reprod Biomed Online. 2013;27:201–11.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Wilding M, Coppola G, di Matteo L, Palagiano A, Fusco E, Dale B. Intracytoplasmic injection of morphologically selected spermatozoa (IMSI) improves outcome after assisted reproduction by deselecting physiologically poor quality spermatozoa. J Assist Reprod Genet. 2011;28:253–62.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Hammoud I, Boitrelle F, Ferfouri F, Vialard F, Bergere M, Wainer B, Bailly M, Albert M, Selva J. Selection of normal spermatozoa with a vacuole-free head (×6300) improves selection of spermatozoa with intact DNA in patients with high sperm DNA fragmentation rates. Andrologia. 2013;45:163–70.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Cayli S, Jakab A, Ovari L, Delpiano E, Celik-Ozenci C, Sakkas D, Ward D, Huszar G. Biochemical markers of sperm function: male fertility and sperm selection for ICSI. Reprod Biomed Online. 2003;7:462–8.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Perdrix A, Travers A, Clatot F, Sibert L, Mitchell V, Jumeau F, Macé B, Rives N. Modification of chromosomal architecture in human spermatozoa with large vacuoles. Andrology. 2013;1:57–66.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Virro MR, Larson-Cook KL, Evenson DP. Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertil Steril. 2004;81:1289–95.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Hammadeh M, Nkemayim D, Georg T, et al. Sperm morphology and chromatin condensation before and after semen processing. Arch Androl. 2000;44:221–6.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Gopalkrishnan K, Padwal V, Meherji PK, et al. Poor quality of sperm as it affects repeated early pregnancy loss. Arch Androl. 2000;45:111–7.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Aitken RJ, De Iuliis GN. Origins and consequences of DNA damage in male germ cells. Reprod Biomed Online. 2007;14:727–33.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Tesarik J. MSOME and sperm DNA integrity: Biological and clinical consideration. In: Agarwal, et al., editors. Non-invasive sperm selection for in vitro fertilization: Novel concepts and methods. New York: Springer Science + Business Media; 2015. p. 137–47.Google Scholar
  46. 46.
    Kumar M, Kumar K, Jain S, Hassan T, Dada R. Novel insights into the genetic and epigenetic paternal contribution to the human embryo. Clinics. 2013;68(1):5–14.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Shaoqin G, Zhenghui Z, Xueqian Z, Yuan H. Epigenetic modifications in human spermatozoon and its potential role in embryonic development. Yi Chuan. 2014;36:439–46.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Schagdarsurengin U, Paradowska A, Steger K. Analysing the sperm epigenome: roles in early embryogenesis and assisted reproduction. Nat Rev Urol. 2012;9:609–19.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Feinberg J, Bakulski K, Jaffe A, Tryggvadottir R, Brown S, Goldman L, Croen L, Hertz-Picciotto I, Newschaffer C, Fallin M, Feinberg A. Paternal sperm DNA methylation associated with early signs of autism risk in an autism-enriched cohort. Int J Epidemiol. 2015;44:1199–210.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Kobayashi H, Hiura H, John R, Sato A, Otsu E, Kobayashi N, Suzuki R, Suzuki F, Hayashi C, Utsunomiya T, Yaegashi N, Arima T. DNA methylation errors at imprinted loci after assisted conception originate in the parental sperm. Eur J Hum Genet. 2009;17:1582–91.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Montjean D, De La Grange P, Gentien D, Rapinat A, Belloc S, Cohen-Bacrie P, Menezo Y, Benkhalifa M. Sperm transcriptome profiling in oligozoospermia. J Assist Reprod Genet. 2012;29(1):3–10.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Marques CJ, Carvalho F, Sousa M, Barros A. Genomic imprinting in disruptive spermatogenesis. Lancet. 2004;363(9422):1700–2.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Houshdaran S, Cortessis VK, Siegmund K, Yang A, Laird PW, Sokol RZ. Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS ONE. 2007;2(12):e1289.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Barzideh J, Scott RJ, Aitken RJ. Analysis of the global methylation status of human spermatozoa and its association with the tendency of these cells to enter apoptosis. Andrologia. 2013;45:424–9.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Filipponi D, Feil R. Perturbation of genomic imprinting in oligozoospermia. Epigenetics. 2009;4(1):27–30.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Rajender S, Avery K, Agarwal A. Epigenetics, spermatogenesis and male infertility. Mutat Res. 2011;727(3):62–71.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Cassuto G, Montjean D, Siffroi JP, Bouret D, Marzouk F, Copin H, Benkhalifa M. Different levels of DNA methylation detected in human sperms after morphological selection using high magnification microscopy. Biomed Res Int. 2016;2016:1–7.  https://doi.org/10.1155/2016/6372171.CrossRefGoogle Scholar
  58. 58.
    Bartoov B, Berkovitz A, Eltes F, Kogosovsky A, Yagoda A, Lederman H, Artzi S, Gross M, Barak Y. Pregnancy rates are higher with intracytoplasmic morphologically selected sperm injection than with conventional intracytoplasmic injection. Fertil Steril. 2003;80:1413–9.CrossRefGoogle Scholar
  59. 59.
    Vanderzwalmen P, Hiemer A, Rubner P, Bach M, Neyer A, Stecher A, Uher P, Zintz M, Lejeune B, Vanderzwalmen S, Cassuto G, Zech NH. Blastocyst development after sperm selection at high magnification is associated with size and number of nuclear vacuoles. Reprod Biomed Online. 2008;17:617–27.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Cassuto NG, Bouret D, Plouchart JM, Jellad S, Vanderzwalmen P, Balet R, Larue L, Barak Y. A new real-time morphology classification for human spermatozoa: a link for fertilization and improved embryo quality. Fertil Steril. 2009;92:1616–25.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Knez K, Tomazevic T, Vrtacnik-Bokal E, Virant-Klun I. Developmental dynamics of IMSI-derived embryos: a time-lapse prospective study. Reprod Biomed Online. 2013;27(2):161–71.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Knez K, Zorn B, Tomazevic T, Vrtacnik-Bokal E, Virant-Klun I. The IMSI procedure improves poor embryo development in the same infertile couples with poor semen quality: a comparative prospective randomized study. Reprod Biol Endocrinol. 2011;9:123.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Neyer A, Zintz M, Stecher A, Bach M, Wirleitner B, Zech NH, Vanderzwalmen P. The impact of paternal factors on cleavage stage and blastocyst development analyzed by time-lapse imaging-a retrospective observational study. J Assist Reprod Genet. 2015;32:1607–14.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Simon L, Murphy K, Shamsi M, Liu L, Emery B, Aston K, Hotaling J, Carell D. Paternal influence of sperm DNA integrity on early embryonic development. Hum Reprod. 2014;29:2402–12.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Shoukir Y, Chardonnens D, Campana A, Sakkas D. Blastocyst development from supernumerary embryos after intracytoplasmic sperm injection: a paternal influence? Hum Reprod. 1998;13:1632–7.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Tesarik J, Greco E, Mendoza C. Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod. 2004;19:611–5.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Bartoov B, Berkovitz A, Eltes F, Kogosowski A, Menezo Y, Barak Y. Real-time fine morphology of motile human sperm cell is associated with IVF-ICSI outcome. J Androl. 2002;23:1–8.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Knez K, Zorn B, Tomazevic T, Vrtacnik–Bokal E, Virant-Klun I. The IMSI procedure improves poor embryo development in the same infertile couples with poor semen quality: A comparative prospective randomized study. Reprod Biol Endocrinol. 2011;9:123–30.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Larson KL, DeJonge CJ, Barnes AM, Jost LK, Evenson DP. Sperm chromatin structure assay parameters as predictors of failed pregnancy following assisted reproductive techniques. Hum Reprod. 2000;15:1717–22.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Nasr-Esfahani MH, Salehi M, Razavi S, Anjomshoa M, Rozbahani S, Moulavi F, Mardani M. Effect of sperm DNA damage and sperm protamine deficiency on fertilization and embryo development post-ICSI. Reprod Biomed Online. 2005;11:198–205.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Berkovitz A, Eltes F, Paul M. The chance of having a healthy normal child following intracytoplasmic morphologically-selected sperm injection (IMSI) treatment is higher compared to conventional IVF-ICSI treatment. Fertil Steril. 2007;88:S20.CrossRefGoogle Scholar
  72. 72.
    Cassuto NG, Hazout A, Bouret D, Balet R, Larue L, Benifla JL, Viot G. Low birth defects by deselecting abnormal spermatozoa before ICSI. Reprod Biomed Online. 2014;28:47–53.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Baccetti B, Burrini AG, Collodel G, Magnano AR, Piomboni P, Renieri T, Sensini C. Crater defect in human spermatozoa. Mol Reprod Develop. 1989;22:249–55.Google Scholar
  74. 74.
    Clermont Y. The cycle of the seminiferous epithelium in man. Am J Anat. 1963;112:35–51.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    De Vos A, Van de Velde H, Bocken G, Eylenbosch G, Franceus N, Meersdom G, Tistaert S, Vankelecom A, Tournaye H, Verheyen G. Does intracytoplasmic morphologically selected sperm injection improve embryo development? A randomized sibling-oocyte study. Hum Reprod. 2013;28:617–26.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Silva L, Oliveira J, Petersen C, Mauri A, Massaro F, Cavagna M, Baruffi RL, Franco JG Jr. The effects of male age on sperm analysis by motile sperm organelle morphology examination (MSOME). Reprod Biol Endocrinol. 2012;10:19.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    De Almeida Ferreira Braga DP, Setti AS, Figueira RC, Nichi M, Martinhago CD, Iaconelli A Jr, Borges E Jr. Sperm organelle morphologic abnormalities: contributing factors and effects on intracytoplasmic sperm injection cycles outcomes. Urology. 2011;78:786–91.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Kacem O, Sifer C, Barraud-Lange V, Ducot B, De Ziegler D, Poirot C, Wolf J. Sperm nuclear vacuoles, as assessed by motile sperm organellar morphological examination, are mostly of acrosomal origin. Reprod Biomed Online. 2010;20:132–7.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Montjean D, Belloc S, Benkhalifa M, Dalleac A, Ménézo Y. Sperm vacuoles are linked to capacitation and acrosomal status. Hum Reprod 2012; 27:2927–32.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Gatimel N, Léandri RD, Foliguet B, Bujan L, Parinaud J. Sperm cephalic vacuoles: new arguments for their non acrosomal origin in two cases of total globozoospermia. Andrology. 2013;1:52–6.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Neyer A, Vanderzwalmen P, Bach M, Stecher A, Spitzer D, Zech N. Sperm head vacuoles are not affected by in-vitro conditions, as analysed by a system of sperm-microcapture channels. Reprod Biomed Online. 2013;26:368–77.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Perdrix A, Rives N. Motile sperm organelle morphology examination (MSOME) and sperm head vacuoles: state of the art in. Hum Reprod Update. 2013;19:527–41.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Berkovitz A, Eltes F, Lederman H, Peer S, Ellenbogen A, Feldberg B, Bartoov B. How to improve IVF-ICSI outcome by sperm injection? Reprod Biomed Online. 2006;12:634–8.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Greco E, Scarselli F, Fabozzi G, Colasante A, Zavaglia D, Alviggi E, Litwicka K, Varricchio MT, Minasi M, Tesarik J. Sperm vacuoles negatively affect outcomes in intracytoplasmic morphologically selected sperm injection in terms of pregnancy, implantation, and live-birth rates. Fertil. Steril. 2013;100:379–85.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Antinori M, Licata E, Dani G, Cerusico F, Versaci C, D'Angelo D, Antinori S. Intracytoplasmic morphologically selected sperm injection: a prospective randomized trial. Reprod Biomed Online. 2008;16:835–41.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Nadalini M, Tarozzi N, Distratis V, Scaravelli G, Borini A. Impact of intracytoplasmic morphologically selected sperm injection on assisted reproduction outcome. Reprod Biomed Online. 2009;19:45–55.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Setti SA, Ferreira RC, Paes de Almeida Ferreira Braga D de Cassia Savio Figueira Rerreira Iaconelli A Jr., Borges E Jr. Intracytoplasmic sperm injection outcome versus intracytoplasmic morphologically selected sperm injection outcome: a meta-analysis. Reprod Biomed Online 2010;21:450–455.CrossRefGoogle Scholar
  88. 88.
    Delaroche L, Yazbeck C, Gout C, Kahn V, Oger P, Rougier N. Intracytoplasmic morphologically selected sperm injection (IMSI) after repeated IVF or ICSI failures: a prospective comparative study. Eur J Obstet Gynecol Reprod Biol. 2013;167:76–80.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Mauri A, Petersen C, Oliveira J, Massaro F, Baruffi R, Franco JG Jr. Comparison of day 2 embryo quality after conventional ICSI versus intracytoplasmic morphologically selected sperm injection (IMSI) using sibling oocytes. Eur J Obstet Gynecol Reprod Biol. 2010;150:42–6.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Leandri RD, Gachet A, Pfeffer J, Celebi C, Rives N, Carre-Pigeon F, Kulski O, Mitchell V, Parinaud J. Is intracytoplasmic morphologically selected sperm injection (IMSI) beneficial in the first ART cycle? A multicentric randomized controlled trial. Andrology. 2013;5:692–7.CrossRefGoogle Scholar
  91. 91.
    Dam AH, Feenstra I, Westphal JR, Ramos L, van Golde RJ, Kremer JA. Globozoospermia revisited. Hum Reprod Update. 2007;13:63–75.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Cox L, Larman MG, Saunders CM, Hashimoto K, Swann K, Lai FA. Sperm phospholipase Czeta from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction. 2002;124:611–23.PubMedCrossRefGoogle Scholar
  93. 93.
    Kashir J, Heindryckx B, Jones C, De Sutter P, Parrington J, Coward K. Oocyte activation, phospholipase C zeta and human infertility. Hum Reprod Update. 2010;16:690–703.PubMedCrossRefGoogle Scholar
  94. 94.
    Montag M, Köster M, van der Ven K, Bohlen U, van der Ven H. The benefit of artificial oocyte activation is dependent on the fertilization rate in a previous treatment cycle. Reprod Biomed Online. 2012;24(5):521–6.PubMedCrossRefGoogle Scholar
  95. 95.
    Stecher A, Bach M, Neyer A, Vanderzwalmen P, Zintz M, Zech NH. Case report: live birth following ICSI with non-vital frozen-thawed testicular sperm and oocyte activation with calcium ionophore. J Assist Reprod Genet. 2011;28:411–4.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Kashir J, Sermondade N, Sifer C, Lin Oo S, Jones C, Mounce G, Turner K, Child T, McVeigh E, Coward K. Motile sperm organelle morphology evaluation-selected globozoospermic human sperm with an acrosomal bud exhibits novel patterns and higher levels of phospholipase C zeta. Human Reprod. 2012;27(11):3150–60.CrossRefGoogle Scholar
  97. 97.
    Sermondade N, Hafhouf E, Dupont C, Bechoua S, Palacios C, Eustache F, Poncelet C, Benzacken B, Le´vy R, Sifer C. Successful childbirth after intracytoplasmic morphologically selected sperm injection without assisted oocyte activation in a patient with globozoospermia. Hum Reprod. 2011;26:2944–9.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Setti A, Figueira R, Braga D, Aoki T, Iaconelli A, Borges E. Intracytoplasmic morphologically selected sperm injection is beneficial in cases of advanced maternal age: a prospective randomized study. Eur J Obs Gynec Reprod Biol. 2013;171:286–90.CrossRefGoogle Scholar
  99. 99.
    Ménézo Y, Dale B, Cohen M. DNA damage and repair in human oocytes and embryos: a review. Zygote. 2010;18:357–65.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Brandriff B, Pedersen RA. Repair of the ultraviolet-irradiated male genome in fertilized mouse eggs. Science. 1981;211:1431–3.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Gunes S, Al-Sadaan M, Spermatogenesis AA. DNA damage and DNA repair mechanisms in male infertility. Reprod Biomed Online. 2015;31:309–19.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Kobayashi H, Sato A, Otsu E, et al. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet. 2007;16:2542–51.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Peer S, Eltes F, Berkovitz A, Yehuda R, Itsykson P, Bartoov B. Is fine morphology of the human sperm nuclei affected by in vitro incubation at 37 degrees C°? Fertil Steril. 2007;88:1589–94.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Vanderzwalmen P, Zech N, Lejeune B, Neyer A, Perrier d’´Hauterive S, Puissant F, Stecher A, Vanderzwalmen S, Wirleitner B, Gaspard O. Sperm vacuoles: Origin and implications. In: Agarwal A, et al., editors. Non-invasive sperm selection for in vitro fertilization: Novel concepts and methods. New York: Springer Science + Business media; 2015. p. 111–21.Google Scholar
  105. 105.
    Schwarz C, Köster M, van der Ven K, Montag M. Temperature-induced sperm nuclear vacuolization is dependent on sperm preparation. Andrologia. 2012;44(Suppl 1):126–9.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    Vanderzwalmen P, Bach M, Gaspard O, Lejeune B, Neyer A, Puissant F, Schuff M, Stecher A, Vanderzwalmen S, Wirleitner B, Zech NH. Morphological selection of gametes and embryos: Sperm. In: Montag M, editor. A practical guide to selecting gametes and embryos. United Kingdom: Cambridge University Press; 2014. p. 59–79.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Pierre Vanderzwalmen
    • 1
    • 2
  • Romain Imbert
    • 1
  • David Jareno Martinez
    • 1
  • Astrid Stecher
    • 2
  • Anne Vansteenbrugge
    • 1
  • Sabine Vanderzwalmen
    • 1
  • Barbara Wirleitner
    • 3
  • Maximillian Murtinger
    • 2
  1. 1.IVF Center CHIRECBraine l’Alleud-WaterlooBelgium
  2. 2.NextClinic IVF Centers. Prof. ZechBregenzAustria
  3. 3.IVF Centers Prof. Zech, IVF LaboratoryBregenzAustria

Personalised recommendations