Effect of tyrosine kinase inhibitors on male fertility in patients with chronic phase chronic myeloid leukemia

References

• Wang C, Swerdloff RS. Limitations of semen analysis as a test of male fertility and anticipated needs from newer tests. Fertil Steril. 2014;102(6):1502–1507. doi:10.1016/j.fertnstert.2014.10.021
   PubMed Web of Science ®Google Scholar
• Lorenzi, E., Simonelli, M., Persico, P., Dipasquale, A., & Santoro, A. (2021). Risks of molecular targeted therapies to fertility and safety during pregnancy: a review of current knowledge and future needs. Expert Opinion on Drug Safety, 20(5), 503–521. https://doi.org/10.1080/14740338.2021.1893299
   Google Scholar
• Smith G, Apperley J, Milojkovic D, et al. A British society for haematology guideline on the diagnosis and management of chronic myeloid leukaemia. Br J Haematol. 2020;191(2):171–193. doi:10.1111/bjh.16971
   PubMed Web of Science ®Google Scholar
• NCCN. NCCN clinical practice guidelines in oncology (NCCN guidelines®) chronic myeloid leukemia. https://www.nccn.org/professionals/physician_gls/pdf/cml.pdf. Updated 2023. Accessed 4/16, 2023.
   Google Scholar
• Hochhaus A, Baccarani M, Silver RT, et al. European LeukemiaNet 2020 recommendations for treating chronic myeloid leukemia. Leukemia. 2020;34(4):966–984. doi:10.1038/s41375-020-0776-2
   PubMed Web of Science ®Google Scholar
• World Health Organization. WHO laboratory manual for the examination and processing of human semen (FIFTH EDITION). https://www.who.int/docs/default-source/reproductive-health/srhr-documents/infertility/examination-and-processing-of-human-semen-5ed-eng.pdf?sfvrsn=5227886e_2. Updated 2010. Accessed 4/25, 2021.
   Google Scholar
• Nurmio M, Toppari J, Zaman F, et al. Inhibition of tyrosine kinases PDGFR and C-kit by imatinib mesylate interferes with postnatal testicular development in the rat. Int J Androl. 2007;30(4):366–376; discussion 376. doi:10.1111/j.1365-2605.2007.00755.x
   PubMedGoogle Scholar
• Ramstein JJ, Tsai KK, Smith JF. Tyrosine kinase inhibitors and male reproductive health. Clin Pharmacol Ther. 2017;102(5):754–756. doi:10.1002/cpt.813
   PubMed Web of Science ®Google Scholar
• Imatinib SmPC. https://www.medicines.org.uk/emc/product/7779/smpc. Updated 2019. Accessed 14 December, 2019.
   Google Scholar
• FDA. Bosutinib package insert. https://www.accessdata.fda.gov/drugsatfda_docs/label/2017/20334s007s008lbl.pdf. Updated 20/12/2023.
   Google Scholar
• FDA. Dasatinib package insert. Updated 20 October 2023
   Google Scholar
• FDA. Ponatinib package insert. https://www.accessdata.fda.gov/drugsatfda_docs/label/2012/203469lbl.pdf. Updated 20/12/2023.
   Google Scholar
• Nilotinib SmPC. https://www.medicines.org.uk/emc/product/5852/smpc. Updated 2019. Accessed 14 December 2019, 2019.
   Google Scholar
• Schultheis B, Nijmeijer BA, Yin H, et al. Imatinib mesylate at therapeutic doses has no impact on folliculogenesis or spermatogenesis in a leukaemic mouse model. Leuk Res. 2012;36(3):271–274. doi:10.1016/j.leukres.2011.09.025
   PubMed Web of Science ®Google Scholar
• Heim C, Minniear K, Dann CT. Imatinib has deleterious effects on differentiating spermatogonia while sparing spermatogonial stem cell self renewal. Reprod Toxicol. 2011;31(4):454–463. doi:10.1016/j.reprotox.2010.12.056
   PubMed Web of Science ®Google Scholar
• Hashemnia SMR, Atari-Hajipirloo S, Roshan-Milani S, et al. Imatinib alters cell viability but not growth factors levels in TM4 sertoli cells. Int J Reprod Biomed. 2016;14(9):577–582.
   PubMedGoogle Scholar
• Ahmadi N, Samaee S, Yokel RA, et al. Imatinib mesylate effects on zebrafish reproductive success: gonadal development, gamete quality, fertility, embryo-larvae viability and development, and related genes. Toxicol Appl Pharmacol. 2019;379:114645. doi:10.1016/j.taap.2019.114645
   PubMed Web of Science ®Google Scholar
• Cengiz Seval G, Özkavukçu S, Seval M, et al. Gonadotoxic effects of nilotinib in chronic myeloid leukemia treatment dose in a mouse model. Turk J Haematol. 2017;34(2):137–142. doi:10.4274/tjh.2016.0092
   PubMed Web of Science ®Google Scholar
• Seval G, Ozkavukcu S, Seval M, et al. The effect of nilotinib in chronic myeloid leukemia treatment dose on spermatogenesis and folliculogenesis in a healthy mouse model. Blood. 2014;124(21):1799–1799. doi:10.1182/blood.V124.21.1799.1799
   PubMed Web of Science ®Google Scholar
• Ozkavukcu S, Kuscu N, Adiguzel D, et al. Deleterious reproductive effects of nilotinib in mouse model. Reproduction. 2021;161(3):295–306. doi:10.1530/REP-20-0548
   PubMed Web of Science ®Google Scholar
• Khaleel KJ, Al-Hindawi M, Alwan LH, et al. Effects of tyrosine kinase inhibitors (nilotinib) on male mice infertility. EJMCM. 2020;7(3):3608–3614.
   Google Scholar
• Palani R, Milojkovic D, Apperley JF. Managing pregnancy in chronic myeloid leukaemia. Ann Hematol. 2015;94 Suppl 2(S2):S167–S176. doi:10.1007/s00277-015-2317-z
   PubMedGoogle Scholar
• Abruzzese E, Trawinska MM, de Fabritiis P, et al. Management of pregnant chronic myeloid leukemia patients. Expert Rev Hematol. 2016;9(8):781–791. doi:10.1080/17474086.2016.1205479
   PubMed Web of Science ®Google Scholar
• Rambhatla A, Strug MR, De Paredes JG, et al. Fertility considerations in targeted biologic therapy with tyrosine kinase inhibitors: a review. J Assist Reprod Genet. 2021;38(8):1897–1908. doi:10.1007/s10815-021-02181-6
   PubMed Web of Science ®Google Scholar
• Carlier P, Markarian M, Bernard N, et al. Pregnancy outcome among partners of male patients receiving imatinib, dasatinib or nilotinib in chronic myeloid leukemia: reports collected by the French network pharmacovigilance centers. Arch Gynecol Obstet. 2017;295(4):1059–1271. doi:10.1007/s00404-016-4262-z
   PubMed Web of Science ®Google Scholar
• Szakács Z, Hegyi PJ, Farkas N, et al. Pregnancy outcomes of women whom spouse fathered children after tyrosine kinase inhibitor therapy for chronic myeloid leukemia: a systematic review. PLoS One. 2020;15(12):e0243045. doi:10.1371/journal.pone.0243045
   PubMed Web of Science ®Google Scholar
• Shash E, Bassi S, Cocorocchio E, et al. Fatherhood during imatinib. Acta Oncol. 2011;50(5):734–735. doi:10.3109/0284186X.2011.577562
   PubMed Web of Science ®Google Scholar
• Ramasamy K, Hayden J, Lim Z, et al. Successful pregnancies involving men with chronic myeloid leukaemia on imatinib therapy. Br J Haematol. 2007;137(4):374–375. doi:10.1111/j.1365-2141.2007.06542.x
   PubMed Web of Science ®Google Scholar
• Breccia M, Cannella L, Montefusco E, et al. Male patients with chronic myeloid leukemia treated with imatinib involved in healthy pregnancies: report of five cases. Leuk Res. 2008;32(3):519–520. doi:10.1016/j.leukres.2007.07.022
   PubMed Web of Science ®Google Scholar
• Ault P, Kantarjian H, O'Brien S, et al. Pregnancy among patients with chronic myeloid leukemia treated with imatinib. J Clin Oncol. 2006;24(7):1204–1208. doi:10.1200/JCO.2005.04.6557
   PubMed Web of Science ®Google Scholar
• Cortes JE, Gambacorti-Passerini C, Deininger M, et al. Pregnancy outcomes in patients treated with bosutinib. Int J Hematol Oncol. 2020;9(2):IJH26. doi:10.2217/ijh-2020-0004
   PubMedGoogle Scholar
• Chang X, Zhou L, Chen X, et al. Impact of imatinib on the fertility of male patients with chronic myelogenous leukaemia in the chronic phase. Target Oncol. 2017;12(6):827–832. doi:10.1007/s11523-017-0521-6
   PubMed Web of Science ®Google Scholar
• Seshadri T, Seymour JF, McArthur GA. Oligospermia in a patient receiving imatinib therapy for the hypereosinophilic syndrome. N Engl J Med. 2004;351(20):2134–2135. doi:10.1056/NEJM200411113512024
   PubMed Web of Science ®Google Scholar
• Mariani S, Basciani S, Fabbri A, et al. Severe oligozoospermia in a young man with chronic myeloid leukemia on long-term treatment with imatinib started ­before puberty. Fertil Steril. 2011;95(3):1120.e15-1120–e17. doi:10.1016/j.fertnstert.2010.08.060
   Web of Science ®Google Scholar
• Ma Y, At S, Vd S. Effects of tyrosine kinase inhibitors on spermatogenesis and pituitary gonadal axis in males with chronic myeloid leukemia. J Cancer Res Ther. 2014;2(8):116–121. doi:10.14312/2052-4994.2014-18
   Google Scholar
• Nicolini F, Alcazer V, Huguet F, et al. CML patients show sperm alterations at diagnosis that are not improved with imatinib treatment. Leuk Res. 2016;48:80–83. doi:10.1016/j.leukres.2016.07.008
   PubMed Web of Science ®Google Scholar