The site of the Media Sphera Publishers contains materials intended solely for healthcare professionals.
By closing this message, you confirm that you are a certified medical professional or a student of a medical educational institution.

Zamyatina S.V.

Altai State Medical University

Elchaninova S.A.

Altai State Medical University

Raevskikh V.M.

Altai State Medical University

Dudareva Yu.A.

Altai State Medical University

Rachenkova T.V.

Altai State Medical University

Cytokines in normal pregnancy and miscarriage

Authors:

Zamyatina S.V., Elchaninova S.A., Raevskikh V.M., Dudareva Yu.A., Rachenkova T.V.

More about the authors

Journal: Russian Journal of Human Reproduction. 2024;30(1): 72‑81

Read: 1589 times


To cite this article:

Zamyatina SV, Elchaninova SA, Raevskikh VM, Dudareva YuA, Rachenkova TV. Cytokines in normal pregnancy and miscarriage. Russian Journal of Human Reproduction. 2024;30(1):72‑81. (In Russ.)
https://doi.org/10.17116/repro20243001172

Recommended articles:
Immu­nological aspe­cts of reccurent pregnancy loss. Russian Journal of Human Reproduction. 2024;(5):64-71
The role of immuno-inflammatory factors in the deve­lopment of nega­tive symptoms in schi­zophrenia. S.S. Korsakov Journal of Neurology and Psychiatry. 2024;(11):42-48
Inflammatory aging. Part 1. The principal biochemical mechanisms. Russian Journal of Preventive Medi­cine. 2024;(12):145-150
Early pregnancy loss: the influence of endo­genous risk factors. Russian Bulletin of Obstetrician-Gynecologist. 2024;(6):50-58
Sexual function of women during pregnancy. Russian Bulletin of Obstetrician-Gynecologist. 2024;(6):112-117

References:

  1. PrabhuDas M, Bonney E, Caron K, Dey S, Erlebacher A, Fazleabas A, Fisher S, Golos T, Matzuk M, McCune JM, Mor G, Schulz L, Soares M, Spencer T, Strominger J, Way SS, Yoshinaga K.. Immune mechanisms at the maternal-fetal interface: perspectives and challenges. Nature Immunology. 2015;16(4):328-334.  https://doi.org/10.1038/ni.3131
  2. Wei Y, Ding J, Li J, Cai S, Liu S, Hong L, Yin T, Zhang Y, Diao L. Metabolic Reprogramming of Immune Cells at the Maternal-Fetal Interface and the Development of Techniques for Immunometabolism. Frontiers in Immunology. 2021;12:717014. https://doi.org/10.3389/fimmu.2021.717014
  3. Aghaeepour N, Ganio EA, Mcilwain D, Tsai AS, Tingle M, Van Gassen S, Gaudilliere DK, Baca Q, McNeil L, Okada R, Ghaemi MS, Furman D, Wong RJ, Winn VD, Druzin ML, El-Sayed YY, Quaintance C, Gibbs R, Darmstadt GL, Shaw GM, Stevenson DK, Tibshirani R, Nolan GP, Lewis DB, Angst MS, Gaudilliere B. An immune clock of human pregnancy. Science Immunology. 2017;2(15): eaan2946. https://doi.org/10.1126/sciimmunol.aan2946
  4. Abu-Raya B., Michalski C., Sadarangani M., Lavoie PM. Maternal Immunological Adaptation during Normal Pregnancy. Frontiers in Immunology. 2020;11:575197. https://doi.org/10.3389/fimmu.2020.575197
  5. Dobrokhotova YuEG, Ankovskaya LV, Bachareva IV, Svitich OA, Malashenko SV, Magomedova AM. Role of immune mechanisms in the pathogenesis of miscarriage. Akusherstvo i ginekologiya. 2016; 7:5-10. (In Russ.). https://doi.org/10.18565/aig.2016.7.5-10
  6. Savel’eva GM, Suhih GT, Serov VN, Radzinskij VE. Akusherstvo: nacional’noe rukovodstvo. M.: GEOTAR-Media; 2021. (In Russ.).
  7. Yockey LJ, Iwasaki A. Interferons and Proinflammatory Cytokines in Pregnancy and Fetal Development. Immunity. 2018;49(3):397-412.  https://doi.org/10.1016/j.immuni.2018.07.017
  8. Ashford KB, Chavan N, Ebersole JL, Wiggins AT, Sharma S, McCubbin A, Barnett J, O’Brien J. Patterns of Systemic and Cervicovaginal Fluid Inflammatory Cytokines throughout Pregnancy. American Journal of Perinatology. 2018;35(5):455-462.  https://doi.org/10.1055/s-0037-1608677
  9. Buxton MA, Meraz-Cruz N, Sánchez BN, Foxman B, Gronlund CJ, Beltran-Montoya J, Castillo-Castrejon M, O’Neill MS, Vadillo-Ortega F. Repeated Measures of Cervicovaginal Cytokines during Healthy Pregnancy: Understanding «Normal» Inflammation to Inform Future Screening. American Journal of Perinatology. 2020; 37(6):613-620.  https://doi.org/10.1055/s-0039-1685491
  10. Petrov YuA, Arnd IG, Bachtina AS. Immunological aspects of pregnancy loss. Glavnyj vrach Yuga Rossii. 2021;1(76):38-41. (In Russ.).
  11. Fu B, Li X, Sun R, Tong X, Ling B, Tian Z, Wei H. Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface. Proceedings of the National Academy of Sciences of the USA 2013;110(3):E231-E240. https://doi.org/10.1073/pnas.1206322110
  12. Pitman H, Innes BA, Robson SC, Bulmer JN, Lash GE. Altered expression of interleukin-6, interleukin-8 and their receptors in decidua of women with sporadic miscarriage. Human Reproduction. 2013;28(8):2075-2086. https://doi.org/10.1093/humrep/det233
  13. Lash GE, Ernerudh J. Decidual cytokines and pregnancy complications: focus on spontaneous miscarriage. Journal of Reproductive Immunology. 2015;108:83-89.  https://doi.org/10.1016/j.jri.2015.02.003
  14. Park S, You YA, Yun H, Choi SJ, Hwang HS, Choi SK, Lee SM, Kim YJ. Cervicovaginal fluid cytokines as predictive markers of preterm birth in symptomatic women. Obstetrics and Gynecology Science. 2020;63(4):455-463.  https://doi.org/10.5468/ogs.19131
  15. Rozner AE, Durning M, Kropp J, Wiepz GJ, Golos TG. Macrophages modulate the growth and differentiation of rhesus monkey embryonic trophoblasts. American Journal of Reproductive Immunology. 2016;76(5):364-375.  https://doi.org/10.1111/aji.12564
  16. En’kova EV, Gribanova VA, Voronina EV, et al. The analysis of the cytocinestatus at the complications of pregnancy. Sistemnyj analiz i upravlenie v biomedicinskih sistemah. 2011;10(4):930-932. (In Russ.).
  17. Levkovich MA, Nefedova DD, Tsaturyan LD, Berdichevskaya EM. Summary immunological aspects miscarriage. Sovremennye problemy nauki i obrazovaniya. 2016;3:186. 
  18. Lebedeva EI, Yavorskaya SD, Momot AP Fadeeva NI, Kuznetsova TA. Improvement of perinatal outcomes in patients with recurrent miscarriages by correction of fibrinolytic reactions. Byulleten’ medicinskoj nauki. 2021;3(23):4-10. (In Russ.). https://doi.org/10.31684/25418475_2021_3_4
  19. Nachalov YuV, M Sokolova T, Usova AV. Content of pro- and antiinflammatory cytokines in women with unpregnancy after conservative therapy. Vestnik novyh medicinskih tekhnologij. 2008;15(2): 50-52. (In Russ.).
  20. Murzabekova GS, Tleuberdieva FN, Dzoz LS. Change of levels of TNF-α and IL-6 in groups with loss pregnancy, infected by genital herpes. Vestnik Novosibirskogo gosudarstvennogo universiteta. Seriya: Biologiya, klinicheskaya medicina. 2007;5(3):57-59. (In Russ.).
  21. Robinson DP, Klein SL. Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Hormones and Behavior. 2012;62(3):263-271.  https://doi.org/10.1016/j.yhbeh.2012.02.023
  22. Kumar P, Magon N. Hormones in pregnancy. Nigerian Medical Journal. 2012;53(4):179-183.  https://doi.org/10.4103/0300-1652.107549
  23. De Oliveira LG, Lash GE, Murray-Dunning C, Bulmer JN, Innes BA, Searle RF, Sass N, Robson SC. Role of interleukin 8 in uterine natural killer cell regulation of extravillous trophoblast cell invasion. Placenta. 2010;31(7):595-601.  https://doi.org/10.1016/j.placenta.2010.04.012
  24. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Müller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochemical Journal 2003;374(1):1-20.  https://doi.org/10.1042/BJ20030407
  25. Lin MT, Lin BR, Chang CC, Chu CY, Su HJ, Chen ST, Jeng YM, Kuo ML. IL-6 induces AGS gastric cancer cell invasion via activation of the c-Src/RhoA/ROCK signaling pathway. International Journal of Cancer. 2007;120(12):2600-2608. https://doi.org/10.1002/ijc.22599
  26. Hadley EE, Richardson LS, Torloni MR, Menon R. Gestational tissue inflammatory biomarkers at term labor: A systematic review of literature. American Journal of Reproductive Immunology. 2018; 79(2):10.1111/aji.12776. https://doi.org/10.1111/aji.12776
  27. Menon R, Bonney EA, Condon J, Mesiano S, Taylor RN. Novel concepts on pregnancy clocks and alarms: redundancy and synergy in human parturition. Human Reproduction Update. 2016;22(5):535-560.  https://doi.org/10.1093/humupd/dmw022
  28. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. Journal of Reproductive Immunology. 2008;79(1):50-57.  https://doi.org/10.1016/j.jri.2008.04.002
  29. Rinaldi SF, Makieva S, Saunders PT, Rossi AG, Norman JE. Immune cell and transcriptomic analysis of the human decidua in term and preterm parturition. Molecular Human Reproduction. 2017; 23(10):708-724.  https://doi.org/10.1093/molehr/gax038
  30. Oger S, Méhats C, Dallot E, Ferré F, Leroy MJ. Interleukin-1beta induces phosphodiesterase 4B2 expression in human myometrial cells through a prostaglandin E2- and cyclic adenosine 3’,5’-monophosphate-dependent pathway. The Journal of Clinical Endocrinology and Metabolism. 2002;87(12):5524-5531. https://doi.org/10.1210/jc.2002-020575
  31. Tribe RM, Moriarty P, Dalrymple A, Hassoni AA, Poston L. Interleukin-1beta induces calcium transients and enhances basal and store operated calcium entry in human myometrial smooth muscle. Biology of Reproduction. 2003;68(5):1842-1849. https://doi.org/10.1095/biolreprod.102.011403
  32. Manning R, James CP, Smith MC, Innes BA, Stamp E, Peebles D, Bajaj-Elliott M, Klein N, Bulmer JN, Robson SC, Lash GE. Predictive value of cervical cytokine, antimicrobial and microflora levels for pre-term birth in high-risk women. Scientific Reports. 2019; 9(1):11246. https://doi.org/10.1038/s41598-019-47756-7
  33. DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, Sun CL, Goltsman DS, Wong RJ, Shaw G, Stevenson DK, Holmes SP, Relman DA. Temporal and spatial variation of the human microbiota during pregnancy. Proceedings of the National Academy of Sciences of the USA. 2015;112(35):11060-11065. https://doi.org/10.1073/pnas.1502875112
  34. Kindinger LM, MacIntyre DA, Lee YS, Marchesi JR, Smith A, McDonald JA, Terzidou V, Cook JR, Lees C, Israfil-Bayli F, Faiza Y, Toozs-Hobson P, Slack M, Cacciatore S, Holmes E, Nicholson JK, Teoh TG, Bennett PR. Relationship between vaginal microbial dysbiosis, inflammation, and pregnancy outcomes in cervical cerclage. Science Translational Medicine. 2016;8(350):350ra102. https://doi.org/10.1126/scitranslmed.aag1026
  35. Kolesnyk NN. Local and system changes in cytokine balance by cervical insufficiency in different gestational ages. Zdorov’e zhenshchiny. 2015;10(106):108. (In Russ.).
  36. Amabebe E, Chapman DR, Stern VL, Stafford G, Anumba DOC. Mid-gestational changes in cervicovaginal fluid cytokine levels in asymptomatic pregnant women are predictive markers of inflammation-associated spontaneous preterm birth. Journal of Reproductive Immunology. 2018;126:1-10.  https://doi.org/10.1016/j.jri.2018.01.001
  37. Zenclussen AC, Hämmerling GJ. Cellular Regulation of the Uterine Microenvironment That Enables Embryo Implantation. Frontiers in Immunology. 2015;6:321.  https://doi.org/10.3389/fimmu.2015.00321
  38. Sadowsky DW, Adams KM, Gravett MG, Witkin SS, Novy MJ. Preterm labor is induced by intraamniotic infusions of interleukin-1beta and tumor necrosis factor-alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. American Journal of Obstetrics and Gynecology. 2006;195(6):1578-1589. https://doi.org/10.1016/j.ajog.2006.06.072
  39. Agrawal V, Hirsch E. Intrauterine infection and preterm labor. Seminars in Fetal and Neonatal Medicine. 2012;17(1):12-19.  https://doi.org/10.1016/j.siny.2011.09.001
  40. Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Bieda J, Chaemsaithong P, Miranda J, Chaiworapongsa T, Ravel J. The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal delivery at term. Microbiome. 2014;2:18.  https://doi.org/10.1186/2049-2618-2-18
  41. Taylor BD, Holzman CB, Fichorova RN, Tian Y, Jones NM, Fu W, Senagore PK. Inflammation biomarkers in vaginal fluid and preterm delivery. Human Reproduction. 2013;28(4):942-952.  https://doi.org/10.1093/humrep/det019
  42. Gargano JW, Holzman C, Senagore P, Thorsen P, Skogstrand K, Hougaard DM, Rahbar MH, Chung H. Mid-pregnancy circulating cytokine levels, histologic chorioamnionitis and spontaneous preterm birth. Journal of Reproductive Immunology. 2008;79(1):100-110.  https://doi.org/10.1016/j.jri.2008.08.006
  43. Puchner K, Iavazzo C, Gourgiotis D, Boutsikou M, Baka S, Hassiakos D, Kouskouni E, Economou E, Malamitsi-Puchner A, Creatsas G. Mid-trimester amniotic fluid interleukins (IL-1β, IL-10 and IL-18) as possible predictors of preterm delivery. In Vivo. 2011; 25(1):141-148. 
  44. Savchenko TN, Tochieva MKh, Agaeva MI, Dergacheva I, Shmarina GV, Kofiadi IA. The cytokine status in women with non-carrying of pregnancy and concomitant candidiasis infection. Lechenie i profilaktika. 2015;2(14):24-27. (In Russ.).
  45. Kemp MW, Saito M, Newnham JP, Nitsos I, Okamura K, Kallapur SG. Preterm birth, infection, and inflammation advances from the study of animal models. Reproductive Sciences. 2010;17(7):619-628.  https://doi.org/10.1177/1933719110373148
  46. Grigsby PL, Novy MJ, Adams Waldorf KM, Sadowsky DW, Gravett MG. Choriodecidual inflammation: a harbinger of the preterm labor syndrome. Reproductive Sciences. 2010;17(1):85-94.  https://doi.org/10.1177/1933719109348025
  47. Tereshkina IV, Klemente Apumaita HM, Grechkanev GO. Habitual noncarrying of autoimmune genesis — the effectiveness of ozonotherapy. Medicinskij al’manah. 2009;4(9):74-77. (In Russ.).
  48. Novikova SV, Dal’nikovskaya LA, Budykina TS, Biryukova NV, Klimova IV. Diagnostic and prognostic value of the study of biochemical markers of the threat of abortion in women with a short cervix. Rossijskij vestnik akushera-ginekologa. 2020;20(4):18-26. (In Russ.). https://doi.org/
  49. Deng W, Yuan J, Cha J, Sun X, Bartos A, Yagita H, Hirota Y, Dey SK. Endothelial Cells in the Decidual Bed Are Potential Therapeutic Targets for Preterm Birth Prevention. Cell Reports. 2019; 27(6): 1755-1768.e4.  https://doi.org/10.1016/j.celrep.2019.04.049
  50. Schatz F, Guzeloglu-Kayisli O, Arlier S, Kayisli UA, Lockwood CJ. The role of decidual cells in uterine hemostasis, menstruation, inflammation, adverse pregnancy outcomes and abnormal uterine bleeding. Human Reproduction Update. 2016;22(4):497-515.  https://doi.org/10.1093/humupd/dmw004
  51. Altmäe S, Segura MT, Esteban FJ, Bartel S, Brandi P, Irmler M, Beckers J, Demmelmair H, López-Sabater C, Koletzko B, Krauss-Etschmann S, Campoy C. Maternal Pre-Pregnancy Obesity Is Associated with Altered Placental Transcriptome. PLoS One. 2017; 12(1):e0169223. https://doi.org/10.1371/journal.pone.0169223
  52. Dosch NC, Guslits EF, Weber MB, Murray SE, Ha B, Coe CL, Auger AP, Kling PJ. Maternal Obesity Affects Inflammatory and Iron Indices in Umbilical Cord Blood. The Journal of Pediatrics. 2016;172:20-28.  https://doi.org/10.1016/j.jpeds.2016.02.023
  53. Wang Y, Shi D, Chen L. Lipid profile and cytokines in hypertension of pregnancy: A comparison of preeclampsia therapies. The Journal of Clinical Hypertension (Greenwich). 2018;20(2):394-399.  https://doi.org/10.1111/jch.13161
  54. Aggarwal R, Jain AK, Mittal P, Kohli M, Jawanjal P, Rath G. Association of pro- and anti-inflammatory cytokines in preeclampsia. Journal of Clinical Laboratory Analysis. 2019;33(4):e22834. https://doi.org/10.1002/jcla.22834
  55. Romero R, Gotsch F, Pineles B, Kusanovic JP. Inflammation in pregnancy: its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutrition Reviews. 2007;65(12 Pt 2):S194-S202. https://doi.org/10.1111/j.1753-4887.2007.tb00362.x
  56. Vrachnis N, Karavolos S, Iliodromiti Z, Sifakis S, Siristatidis C, Mastorakos G, Creatsas G. Review: Impact of mediators present in amniotic fluid on preterm labour. In Vivo. 2012;26(5):799-812. 
  57. Nenadić DB, Pavlović MD. Cervical fluid cytokines in pregnant women: Relation to vaginal wet mount findings and polymorphonuclear leukocyte counts. European Journal of Obstetrics and Gynecology and Reproductive Biology. 2008;140(2):165-170.  https://doi.org/10.1016/j.ejogrb.2008.02.020
  58. Zhang J, Dunk CE, Lye SJ. Sphingosine signalling regulates decidual NK cell angiogenic phenotype and trophoblast migration. Human Reproduction. 2013;28(11):3026-3037. https://doi.org/10.1093/humrep/det339
  59. Amabebe E, Reynolds S, He X, Wood R, Stern V, Anumba DOC. Infection/inflammation-associated preterm delivery within 14 days of presentation with symptoms of preterm labour: A multivariate predictive model. PLoS One. 2019;14(9):e0222455. https://doi.org/10.1371/journal.pone.0222455
  60. Kalinka J, Sobala W, Wasiela M, Brzezińska-Błaszczyk E. Decreased proinflammatory cytokines in cervicovaginal fluid, as measured in midgestation, are associated with preterm delivery. American Journal of Reproductive Immunology. 2005;54(2):70-76.  https://doi.org/10.1111/j.1600-0897.2005.00289.x
  61. Witkin SS, Mendes-Soares H, Linhares IM, Jayaram A, Ledger WJ, Forney LJ. Influence of vaginal bacteria and D- and L-lactic acid isomers on vaginal extracellular matrix metalloproteinase inducer: implications for protection against upper genital tract infections. mBio. 2013;4(4):e00460-13.  https://doi.org/10.1128/mBio.00460-13
  62. Pomini F, Caruso A, Challis JR. Interleukin-10 modifies the effects of interleukin-1beta and tumor necrosis factor-alpha on the activity and expression of prostaglandin H synthase-2 and the NAD+-dependent 15-hydroxyprostaglandin dehydrogenase in cultured term human villous trophoblast and chorion trophoblast cells. The Journal of Clinical Endocrinology and Metabolism. 1999;84(12):4645-4651. https://doi.org/10.1210/jcem.84.12.6188
  63. Diago Almela VJ, Martinez-Varea A, Perales-Puchalt A, Alonso-Diaz R, Perales A. Good prognosis of cerclage in cases of cervical insufficiency when intra-amniotic inflammation/infection is ruled out. Journal of Maternal-Fetal and Neonatal Medicine. 2015;28(13): 1563-1568. https://doi.org/10.3109/14767058.2014.960836
  64. Romero R, Avila C, Santhanam U, Sehgal PB. Amniotic fluid interleukin 6 in preterm labor. Association with infection. Journal of Clinical Investigation. 1990;85(5):1392-1400. https://doi.org/10.1172/JCI114583
  65. Holst RM, Mattsby-Baltzer I, Wennerholm UB, Hagberg H, Jacobsson B. Interleukin-6 and interleukin-8 in cervical fluid in a population of Swedish women in preterm labor: relationship to microbial invasion of the amniotic fluid, intra-amniotic inflammation, and preterm delivery. Acta Obstetricia et Gynecologica Scandinavica. 2005;84(6):551-557.  https://doi.org/10.1111/j.0001-6349.2005.00708.x
  66. Donders GG, Vereecken A, Bosmans E, Dekeersmaecker A, Salembier G, Spitz B. Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. BJOG: An International Journal of Obstetrics and Gynaecology. 2002;109(1):34-43.  https://doi.org/10.1111/j.1471-0528.2002.00432.x
  67. Vogel I, Thorsen P, Curry A, Sandager P, Uldbjerg N. Biomarkers for the prediction of preterm delivery. Acta Obstetricia et Gynecologica Scandinavica. 2005;84(6):516-525.  https://doi.org/10.1111/j.0001-6349.2005.00771.x
  68. Jacobsson B, Mattsby-Baltzer I, Andersch B, Bokström H, Holst RM, Nikolaitchouk N, Wennerholm UB, Hagberg H. Microbial invasion and cytokine response in amniotic fluid in a Swedish population of women with preterm prelabor rupture of membranes. Acta Obstetricia et Gynecologica Scandinavica. 2003;82(5):423-431.  https://doi.org/10.1034/j.1600-0412.2003.00157.x
  69. Rizzo G, Capponi A, Vlachopoulou A, Angelini E, Grassi C, Romanini C. Ultrasonographic assessment of the uterine cervix and interleukin-8 concentrations in cervical secretions predict intrauterine infection in patients with preterm labor and intact membranes. Ultrasound in Obstetrics and Gynecology 1998;12(2):86-92.  https://doi.org/10.1046/j.1469-0705.1998.12020086.x
  70. Rizzo G, Capponi A, Rinaldo D, Tedeschi D, Arduini D, Romanini C. Interleukin-6 concentrations in cervical secretions identify microbial invasion of the amniotic cavity in patients with preterm labor and intact membranes. American Journal of Obstetrics and Gynecology. 1996;175(4 Pt 1):812-817.  https://doi.org/10.1016/s0002-9378(96)80004-4
  71. Tsiartas P, Holst RM, Wennerholm UB, Hagberg H, Hougaard DM, Skogstrand K, Pearce BD, Thorsen P, Kacerovsky M, Jacobsson B. Prediction of spontaneous preterm delivery in women with threatened preterm labour: a prospective cohort study of multiple proteins in maternal serum. BJOG. 2012;119(7):866-873.  https://doi.org/10.1111/j.1471-0528.2012.03328.x
  • Braems G, Denys H, De Wever O, Cocquyt V, Van den Broecke R. Use of tamoxifen before and during pregnancy. The Oncologist. 2011;16(11):1547-51.  https://doi.org/10.1634/theoncologist.2011-0121
  • Egashira K, Hiasa K, Yokota N, Kawamura T, Matsushita T, Okugawa K, Yahata H, Sonoda K, Kato K. Infertility after abdominal trachelectomy. Acta Obstetricia et Gynecologica Scandinavica. 2018; 97(11):1358-1364. https://doi.org/10.1111/aogs.13429
  • Schimberni M, Morgia F, Colabianchi J, Giallonardo A, Piscitelli C, Giannini P, Montigiani M, Sbracia M. Natural-cycle in vitro fertilization in poor responder patients: a survey of 500 consecutive cycles. Fertility and Sterility. 2009;92(4):1297-1301. https://doi.org/10.1016/j.fertnstert.2008.07.1765
  • De Marco MP, Montanari G, Ruscito I, Giallonardo A, Ubaldi FM, Rienzi L, Costanzi F, Caserta D, Schimberni M, Schimberni M. Natural Cycle Results in Lower Implantation Failure than Ovarian Stimulation in Advanced-Age Poor Responders Undergoing IVF: Fertility Outcomes from 585 Patients. Reproductive Sciences. 2021; 28(7):1967-1973. https://doi.org/10.1007/s43032-020-00455-5
  • Chan JL, Johnson LN, Efymow BL, Sammel MD, Gracia CR. Outcomes of ovarian stimulation after treatment with chemotherapy. Journal of Assisted Reproduction and Genetics. 2015;32(10):1537-1545. https://doi.org/10.1007/s10815-015-0575-2
  • Checa Vizcaíno MA, Corchado AR, Cuadri ME, Comadran MG, Brassesco M, Carreras R. The effects of letrozole on ovarian stimulation for fertility preservation in cancer-affected women. Reproductive Biomedicine Online. 2012;24(6):606-610.  https://doi.org/10.1016/j.rbmo.2012.02.020
  • Oktay K, Türkçüoğlu I, Rodriguez-Wallberg KA. GnRH agonist trigger for women with breast cancer undergoing fertility preservation by aromatase inhibitor/FSH stimulation. Reproductive Biomedicine Online. 2010;20(6):783-788.  https://doi.org/10.1016/j.rbmo.2010.03.004
  • Azim AA, Costantini-Ferrando M, Oktay K. Safety of fertility preservation by ovarian stimulation with letrozole and gonadotropins in patients with breast cancer: a prospective controlled study. Journal of Clinical Oncology. 2008;26(16):2630-2635. https://doi.org/10.1200/JCO.2007.14.8700
  • Turan V, Bedoschi G, Moy F, Oktay K. Safety and feasibility of performing two consecutive ovarian stimulation cycles with the use of letrozole-gonadotropin protocol for fertility preservation in breast cancer patients. Fertility and Sterility. 2013;100(6):1681-5.e1.  https://doi.org/10.1016/j.fertnstert.2013.08.030
  • Rosenberg E, Fredriksson A, Einbeigi Z, Bergh C, Strandell A. No increased risk of relapse of breast cancer for women who give birth after assisted conception. Human Reproduction Open. 2019;(4): hoz039. https://doi.org/10.1093/hropen/hoz039
  • Sonigo C, Sermondade N, Calvo J, Benard J, Sifer C, Grynberg M. Impact of letrozole supplementation during ovarian stimulation for fertility preservation in breast cancer patients. European Journal of Obstetrics and Gynecology and Reproductive Biology. 2019;4:100049. https://doi.org/10.1016/j.eurox.2019.100049
  • Bonardi B, Massarotti C, Bruzzone M, Goldrat O, Mangili G, Anserini P, Spinaci S, Arecco L, Del Mastro L, Ceppi M, Demeestere I, Lambertini M. Efficacy and Safety of Controlled Ovarian Stimulation With or Without Letrozole Co-administration for Fertility Preservation: A Systematic Review and Meta-Analysis. Frontiers in Oncology. 2020;10:574669. https://doi.org/10.3389/fonc.2020.574669
  • Chian RC, Buckett WM, Tulandi T, Tan SL. Prospective randomized study of human chorionic gonadotrophin priming before immature oocyte retrieval from unstimulated women with polycystic ovarian syndrome. Human Reproduction. 2000;15(1):165-170.  https://doi.org/10.1093/humrep/15.1.165
  • Holzer H, Scharf E, Chian RC, Demirtas E, Buckett W, Tan SL. In vitro maturation of oocytes collected from unstimulated ovaries for oocyte donation. Fertility and Sterility. 2007;88(1):62-67.  https://doi.org/10.1016/j.fertnstert.2006.11.087
  • Kedem A, Yerushalmi GM, Brengauz M, Raanani H, Orvieto R, Hourvitz A, Meirow D. Outcome of immature oocytes collection of 119 cancer patients during ovarian tissue harvesting for fertility preservation. Journal of Assisted Reproduction and Genetics. 2018;35(5): 851-856.  https://doi.org/10.1007/s10815-018-1153-1
  • Park CW, Lee SH, Yang KM, Lee IH, Lim KT, Lee KH, Kim TJ. Cryopreservation of in vitro matured oocytes after ex vivo oocyte retrieval from gynecologic cancer patients undergoing radical surgery. Clinical and Experimental Reproductive Medicine. 2016;43(2):119-125.  https://doi.org/10.5653/cerm.2016.43.2.119
  • Kawamura K, Cheng Y, Kawamura N, Takae S, Okada A, Kawagoe Y, Mulders S, Terada Y, Hsueh AJ. Pre-ovulatory LH/hCG surge decreases C-type natriuretic peptide secretion by ovarian granulosa cells to promote meiotic resumption of pre-ovulatory oocytes. Human Reproduction. 2011;26(11):3094-3101. https://doi.org/10.1093/humrep/der282
  • Mohsenzadeh M, Khalili MA, Tabibnejad N, Yari N, Agha-Rahimi A, Karimi-Zarchi M. Embryo Cryopreservation Following In-Vitro Maturation for Fertility Preservation in a Woman with Mullerian Adenosarcoma: A Case Report. Journal of Human Reproductive Sciences. 2017;10(2):138-141.  https://doi.org/10.4103/jhrs.JHRS_93_16
  • Kirillova A, Bunyaeva E, Van Ranst H, Khabas G, Farmakovskaya M, Kamaletdinov N, Nazarenko T, Abubakirov A, Sukhikh G, Smitz JEJ. Improved maturation competence of ovarian tissue oocytes using a biphasic in vitro maturation system for patients with gynecological malignancy: a study on sibling oocytes. Journal of Assisted Reproduction and Genetics. 2021;38(6):1331-1340. https://doi.org/10.1007/s10815-021-02118-z
  • Sanchez F, Le AH, Ho VNA, Romero S, Van Ranst H, De Vos M, Gilchrist RB, Ho TM, Vuong LN, Smitz J. Biphasic in vitro maturation (CAPA-IVM) specifically improves the developmental capacity of oocytes from small antral follicles. Journal of Assisted Reproduction and Genetics. 2019;36(10):2135-2144. https://doi.org/10.1007/s10815-019-01551-5
  • De Roo C, Tilleman K. In Vitro Maturation of Oocytes Retrieved from Ovarian Tissue: Outcomes from Current Approaches and Future Perspectives. Journal of Clinical Medicine. 2021;10(20):4680. https://doi.org/10.3390/jcm10204680
  • Dinikina YuV, Belogurova MB, Govorov IE, Gamzatova ZKh, Pervunina TM, Komlichenko EV. Cryopreservation of ovarian tissue in girls with oncological diseases: a multidisciplinary approach. Rossijskij zhurnal detskoj gematologii i onkologii. 2019;6(3):59-67.  https://doi.org/10.21682/2311-1267-2019-6-3-59-67
  • Abakushina EV, Otoi T, Kaprin AD. Recovery options of reproductive function of cancer patients due to transplantation of cryopreserved ovarian tissue. Geny i kletki. 2015;10(1):18-27. (In Russ.).
  • Gougeon A, Chainy GB. Morphometric studies of small follicles in ovaries of women at different ages. Journal of Reproduction and Fertility. 1987;81(2):433-442.  https://doi.org/10.1530/jrf.0.0810433
  • Dolmans MM, von Wolff M, Poirot C, Diaz-Garcia C, Cacciottola L, Boissel N, Liebenthron J, Pellicer A, Donnez J, Andersen CY. Transplantation of cryopreserved ovarian tissue in a series of 285 women: a review of five leading European centers. Fertility and Sterility. 2021;115(5):1102-1115. https://doi.org/10.1016/j.fertnstert.2021.03.008
  • Donnez J, Dolmans MM. Ovarian cortex transplantation: 60 reported live births brings the success and worldwide expansion of the technique towards routine clinical practice. Journal of Assisted Reproduction and Genetics. 2015;32(8):1167-1170. https://doi.org/10.1007/s10815-015-0544-9
  • Roness H, Meirow D. Fertility preservation: Follicle reserve loss in ovarian tissue transplantation. Reproduction. 2019;158(5):F35-F44.  https://doi.org/10.1530/REP-19-0097
  • Nisolle M, Casanas-Roux F, Qu J, Motta P, Donnez J. Histologic and ultrastructural evaluation of fresh and frozen-thawed human ovarian xenografts in nude mice. Fertility and Sterility. 2000;74(1): 122-129.  https://doi.org/10.1016/s0015-0282(00)00548-3
  • Tanaka A, Nakamura H, Tabata Y, Fujimori Y, Kumasawa K, Kimura T. Effect of sustained release of basic fibroblast growth factor using biodegradable gelatin hydrogels on frozen-thawed human ovarian tissue in a xenograft model. The Journal of Obstetrics and Gynaecology Research. 2018;44(10):1947-1955. https://doi.org/10.1111/jog.13726
  • Wallace WH, Kelsey TW. Human ovarian reserve from conception to the menopause. PLoS One. 2010;5(1):e8772. https://doi.org/10.1371/journal.pone.0008772
  • Dolmans MM, Marinescu C, Saussoy P, Van Langendonckt A, Amorim C, Donnez J. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood. 2010;116(16):2908-2914. https://doi.org/10.1182/blood-2010-01-265751
  • Diaz-Garcia C, Domingo J, Garcia-Velasco JA, Herraiz S, Mirabet V, Iniesta I, Cobo A, Remohí J, Pellicer A. Oocyte vitrification versus ovarian cortex transplantation in fertility preservation for adult women undergoing gonadotoxic treatments: a prospective cohort study. Fertility and Sterility. 2018;109(3):478-485.e2.  https://doi.org/10.1016/j.fertnstert.2017.11.018
  • Arvold ND, Taghian AG, Niemierko A, Abi Raad RF, Sreedhara M, Nguyen PL, Bellon JR, Wong JS, Smith BL, Harris JR. Age, breast cancer subtype approximation, and local recurrence after breast-conserving therapy. Journal of Clinical Oncology. 2011;29(29): 3885-3891. https://doi.org/10.1200/JCO.2011.36.1105
  • Gellert SE, Pors SE, Kristensen SG, Bay-Bjørn AM, Ernst E, Yding Andersen C. Transplantation of frozen-thawed ovarian tissue: an update on worldwide activity published in peer-reviewed papers and on the Danish cohort. Journal of Assisted Reproduction and Genetics. 2018;35(4):561-570.  https://doi.org/10.1007/s10815-018-1144-2
  • Salim N, Tumanova K, Stolbovoy A, Zvereva D, Popodko A Nosov V. Adaptive VMAT Radiotherapy to Avoid Brachytherapy in Cervical Cancer Treatment. International Journal of Radiation Oncology and Biology and Physics. 2022;114(supp 3):e262.
  • Bystrova O, Lapina E, Kalugina A, Lisyanskaya A, Tapilskaya N, Manikhas G. Heterotopic transplantation of cryopreserved ovarian tissue in cancer patients: a case series. Gynecological Endocrinology. 2019;35(12):1043-1049. https://doi.org/10.1080/09513590.2019.1648413
  • Donnez J. Chemotherapy and decline of the ovarian reserve: How can we explain it and how to prevent it? Fertility and Sterility. 2020; 114(4):722-724.  https://doi.org/10.1016/j.fertnstert.2020.08.010
  • ESHRE Guideline Group on Female Fertility Preservation; Anderson RA, Amant F, Braat D, D’Angelo A, Chuva de Sousa Lopes SM, Demeestere I, Dwek S, Frith L, Lambertini M, Maslin C, Moura-Ramos M, Nogueira D, Rodriguez-Wallberg K, Vermeulen N. ESHRE guideline: female fertility preservation. Human Reproduction Open. 2020;2020(4):hoaa052. https://doi.org/10.1093/hropen/hoaa052
  • Kindinger LM, Kyrgiou M, MacIntyre DA, Cacciatore S, Yulia A, Cook J, Terzidou V, Teoh TG, Bennett PR. Preterm Birth Prevention Post-Conization: A Model of Cervical Length Screening with Targeted Cerclage. PLoS One. 2016;11(11):e0163793. https://doi.org/10.1371/journal.pone.0163793
  • Kyrgiou M, Athanasiou A, Paraskevaidi M, Mitra A, Kalliala I, Martin-Hirsch P, Arbyn M, Bennett P, Paraskevaidis E. Adverse obstetric outcomes after local treatment for cervical preinvasive and early invasive disease according to cone depth: systematic review and meta-analysis. BMJ. 2016;354:i3633. https://doi.org/10.1136/bmj.i3633
  • Li X, Li J, Wu X. Incidence, risk factors and treatment of cervical stenosis after radical trachelectomy: A systematic review. European Journal of Cancer. 2015;51(13):1751-1759. https://doi.org/10.1016/j.ejca.2015.05.012
  • Kasuga Y, Ikenoue S, Tanaka M, Ochiai D. Management of pregnancy after radical trachelectomy. Gynecological Oncology. 2021; 162(1):220-225.  https://doi.org/10.1016/j.ygyno.2021.04.023
  • Šimják P, Cibula D, Pařízek A, Sláma J. Management of pregnancy after fertility-sparing surgery for cervical cancer. Acta Obstetricia et Gynecologica Scandinavia. 2020;99(7):830-838.  https://doi.org/10.1111/aogs.13917
  • Sato Y, Hidaka N, Sakai A, Kido S, Fujita Y, Okugawa K, Yahata H, Kato K. Evaluation of the efficacy of vaginal progesterone in preventing preterm birth after abdominal trachelectomy. European Journal of Obstetrics Gynecology and Reproducive Biology. 2021;259: 119-124.  https://doi.org/10.1016/j.ejogrb.2021.02.009
  • Signorello LB, Cohen SS, Bosetti C, Stovall M, Kasper CE, Weathers RE, Whitton JA, Green DM, Donaldson SS, Mertens AC, Robison LL, Boice JD Jr. Female survivors of childhood cancer: preterm birth and low birth weight among their children. Journal of National Cancer Institute. 2006;98(20):1453-1461. https://doi.org/10.1093/jnci/djj394
  • Schumer ST, Cannistra SA. Granulosa cell tumor of the ovary. Journal of Clinical Oncology. 2003;21(6):1180-1189. https://doi.org/10.1200/JCO.2003.10.019
  • Spanos CP, Mamopoulos A, Tsapas A, Syrakos T, Kiskinis D. Female fertility and colorectal cancer. International Journal of Colorectal Diseases. 2008;23(8):735-743.  https://doi.org/10.1007/s00384-008-0483-3
  • Lopategui DM, Yechieli R, Ramasamy R. Oncofertility in sarcoma patients. Translational Andrology and Urology. 2017;6(5):951-958.  https://doi.org/10.21037/tau.2017.07.03
  • Practice Committees of the American Society for Reproductive Medicine and the Society for Assisted Reproductive Technology. Mature oocyte cryopreservation: a guideline. Fertility and Sterility. 2013;99(1):37-43.  https://doi.org/10.1016/j.fertnstert.2012.09.028
  • Akhmedova ZB, Umarova SG, Ashurova MJ. Fertility and Hodgkin’s lymphoma. Vestnik Avicennyt. 2013;(2):167-172. (In Russ.).
  • Hodgson DC, Pintilie M, Gitterman L, Dewitt B, Buckley CA, Ahmed S, Smith K, Schwartz A, Tsang RW, Crump M, Wells W, Sun A, Gospodarowicz MK. Fertility among female hodgkin lymphoma survivors attempting pregnancy following ABVD chemotherapy. Hematological Oncology. 2007;25(1):11-15.  https://doi.org/10.1002/hon.802
  • Watson M, Wheatley K, Harrison GA, Zittoun R, Gray RG, Goldstone AH, Burnett AK. Severe adverse impact on sexual functioning and fertility of bone marrow transplantation, either allogeneic or autologous, compared with consolidation chemotherapy alone: analysis of the MRC AML 10 trial. Cancer. 1999;86(7):1231-1239. https://doi.org/10.1002/(sici)1097-0142(19991001)86:7<1231::aid-cncr18>3.0.co;2-y
  • Email Confirmation

    An email was sent to test@gmail.com with a confirmation link. Follow the link from the letter to complete the registration on the site.

    Email Confirmation

    We use cооkies to improve the performance of the site. By staying on our site, you agree to the terms of use of cооkies. To view our Privacy and Cookie Policy, please. click here.