Overview of the current state of uterine peristalsis (literature review)

• Eketerina D. Dubinskaya
• Svetlana N. Kolesnikova
• Elizaveta V. Alyoshkina
• Aleksandr S. Gasparov

Abstract

The following literature review provides up-to-date data on endometrial peristalsis, as well as its role in embryo implantation processes. The analysis of anatomical and physiological features, as well as hormonal and biologically active substances affecting the contraction of the myometrium is also presented.

It is shown that endometrial peristalsis (more precisely, myometrial peristalsis) is a crucial but still insufficiently studied factor that plays a significant role in the process of embryo implantation. A potential change in uterine peristalsis in the future may be a worthy predictor of endometrial receptivity. The development and implementation of medical and mathematical technology that allows accurate measurement of the parameters of endometrial waves (frequency, direction, intensity, etc.) will expand the prospects for personifying the possibility and potential effectiveness of embryo transfer in assisted reproductive technology programs and will also provide significant assistance in the diagnosis and treatment of unexplained fertility disorders.

Keywords:endometrial peristalsis; endometrial waves; infertility; embryo implantation; assisted reproductive technologies

REFERENCES

1. Centers for Disease Control and Prevention. Reproductive health. Infertility.

2. Clinical recommendations. Female infertility, 2021. (in Russian)

3. Fox C., Morin S., Jeong J.W., Scott R.T. Jr, Lessey B.A. Local and systemic factors and implantation: what is the evidence? Fertil Steril. 2016; 105 (4): 873–84. DOI: https://doi.org/10.1016/j.fertnstert.2016.02.018

4. Krutova V.A., Kovalenko Y.A. Modern concepts about uterine form of infertility // Sovremennye problemy nauki i obrazovaniya [Modern Problems of Science and Education]. 2018; (3). (in Russian)

5. Uryupina K.V., Kutsenko I.I., Kravtsova E.I., Kudlay J.V., Kravtsov I.I. Endometrial infertility in patients of late reproductive age (a review). Kubanskiy nauchniy meditsinskiy vestnik [Kuban Scientific Medical Bulletin]. 2020; 27 (6): 149–63. DOI: https://doi.org/10.25207/1608-6228-2020-27-6-149-163 (in Russian)

6. Pirtea P., de Ziegler D., Ayoubi J.M. Recurrent implantation failure – is it the egg or the chicken? Life (Basel). 2021; 12 (1): 39. DOI: https://doi.org/10.3390/life12010039 Epub 2021 Dec 27.

7. Silvestris E., de Pergola G., Rosania R., Loverro G. Obesity as disruptor of the female fertility. Reprod Biol Endocrinol. 2018; 16 (1): 22. DOI: https://doi.org/10.1186/s12958-018-0336-z

8. Lalani S., Nizami I., Hashmi A.A., Saifuddin A., Rehman R. Thyroid disfunction and infertility treatment. Acta Endocrinol (Buchar). 2017; 13 (3): 302–7. DOI: https://doi.org/10.4183/aeb.2017.302

9. Lessey B.A., Young S.L. What exactly is endometrial receptivity? Fertil Steril. 2019; 111 (4): 611–7. DOI: https://doi.org/10.1016/j.fertnstert.2019.02.009

10. Bellver J., Marín C., Lathi R.B., Murugappan G., Labarta E., Vidal C., et al. Obesity affects endometrial receptivity by displacing the window of implantation. Reprod Sci. 2021; 28 (11): 3171–80. DOI: https://doi.org/10.1007/s43032-021-00631-1

11. Kuijsters N.P.M., Methorst W.G., Kortenhorst M.S.Q., Rabotti C., Mischi M., Schoot B.C. Uterine peristalsis and fertility: current knowledge and future perspectives: a review and meta-analysis. Reprod Biomed Online. 2017; 35 (1): 50–71. DOI: https://doi.org/10.1016/j.rbmo.2017.03.019 Epub 2017 Apr 12.

12. Shaked S., Jaffa A.J., Grisaru D., Elad D. Uterine peristalsis-induced stresses within the uterine wall may sprout adenomyosis. Biomech Model Mechanobiol. 2015; 14 (3): 437–44. DOI: https://doi.org/10.1007/s10237-014-0614-4 Epub 2014 Sep 13. PMID: 25217062.

13. Yoshino O., Nishii O., Osuga Y., Asada H., Okuda S., Orisaka M., et al. Myomectomy decreases abnormal uterine peristalsis and increases pregnancy rate. J Minim Invasive Gynecol. 2012; 19 (1): 63–7. DOI: https://doi.org/10.1016/j.jmig.2011.09.010 Epub 2011 Nov 9. PMID: 22070929.

14. Mori K., Kitaya K., Ishikawa T., Hata Y. A pregnancy prediction system based on uterine peristalsis from ultrasonic images. Intell Autom Soft Comput. 2021; 29 (2): 335–52. DOI: https://doi.org/10.32604/iasc.2021.01010

15. Hunt S., Abdallah K.S., Ng E., et al. Impairment of uterine contractility is associated with unexplained infertility. Semin Reprod Med. 2020; 38 (1): 61–73. DOI: https://doi.org/10.1055/s-0040-1716409

16. Gasner A., Aatsha P.A. Physiology, uterus [Updated 2022 May 8]. In: StatPearls [Internet]. Treasure Island, FL: StatPearls Publishing, 2022 Jan. PMID: 3249150.

17. Kosmas I.P., Malvasi A., Vergara D., Mynbaev O.A., Sparic R., Tinelli A. Adrenergic and cholinergic uterine innervation and the impact on reproduction in aged women. Curr Pharm Des. 2020; 26 (3): 358–62. DOI: https://doi.org/10.2174/1381612826666200128092256

18. Noe M., Kunz G., Herbertz M., Mall G., Leyendecker G. The cyclic pattern of the immunocytochemical expression of oestrogen and progesterone receptors in human myometrial and endometrial layers: characterization of the endometrial-subendometrial unit. Hum Reprod. 1999; 14 (1): 190–7. DOI: https://doi.org/10.1093/humrep/14.1.190 PMID: 10374119.

19. Myers K.M., Elad D. Biomechanics of the human uterus. Wiley Interdiscip Rev Syst Biol Med. 2017; 9 (5): e1388. DOI: https://doi.org/10.1002/wsbm.1388

20. Tanos V., Lingwood L., Balami S. Junctional zone endometrium morphological characteristics and functionality: review of the literature. Gynecol Obstet Invest. 2020; 85 (2): 107–17. DOI: https://doi.org/10.1159/000505650

21. Huang M., Li X., Guo P., Yu Z., Xu Y., Wei Z. The abnormal expression of oxytocin receptors in the uterine junctional zone in women with endometriosis. Reprod Biol Endocrinol. 2017; 15 (1): 1. DOI: https://doi.org/10.1186/s12958-016-0220-7

22. Devedeux D., Marque C., Mansour S., Germain G., Duchêne J. Uterine electromyography: a critical review. Am J Obstet Gynecol. 1993; 169 (6): 1636–53. DOI: https://doi.org/10.1016/0002-9378(93)90456-s

23. Wray S., Jones K., Kupittayanant S., Li Y., Matthew A., Monir-Bishty E., et al. Calcium signaling and uterine contractility. J Soc Gynecol Investig. 2003; 10: 252–64. DOI: https://doi.org/10.1016/s1071-5576(03)00089-3

24. Myers K.M., Elad D. Biomechanics of the human uterus. Wiley Interdiscip Rev Syst Biol Med. 2017; 9 (5): e1388. DOI: https://doi.org/10.1002/wsbm.1388

25. Kuriyama H., Kitamura K., Itoh T., Inoue R. Physiological features of visceral smooth muscle cells, with special reference to receptors and ion channels. Physiol Rev. 1998; 78: 811920. DOI: https://doi.org/10.1152/physrev.1998.78.3.811

26. Garfield R.E., Blennerhassett M.G., Miller S.M. Control of myometrial contractility: role and regulation of gap junctions. Oxf Rev Reprod Biol. 1988; 10: 436–90.

27. Ijland M.M., Evers J.L., Dunselman G.A., van Katwijk C., Lo C.R., Hoogland H.J. Endometrial wavelike movements during the menstrual cycle. Fertil Steril. 1996; 65 (4): 746–9. DOI: https://doi.org/10.1016/s0015-0282(16)58207-7

28. Young R.C. The uterine pacemaker of labor. Best Pract Res Clin Obstet Gynaecol. 2018; 52: 68–87. DOI: https://doi.org/10.1016/j.bpobgyn.2018.04.002

29. Leyendecker G., Wildt L. A new concept of endometriosis and adenomyosis: tissue injury and repair (tiar). Horm Mol Biol Clin Investig. 2011; 5: 125–42. DOI: https://doi.org/10.1515/HMBCI.2011.002

30. Meirzon D., Jaffa A.J., Gordon Z., Elad D. A new method for analysis of non-pregnant uterine peristalsis using transvaginal ultrasound. Ultrasound Obstet Gynecol. 2011; 38: 217–24. DOI: https://doi.org/10.1002/uog.8950

31. Van Gestel I., IJland M., Hoogland H., Evers J. Endometrial wavelike activity in the non-pregnant uterus. Hum Reprod Update. 2003; 9 (2): 131–8. DOI: https://doi.org/10.1093/humupd/dmg011

32. Eytan O., Halevi I., Har-Toov J., Wolman I., Elad D., Jaffa A.J. Characteristics of uterine peristalsis in spontaneous and induced cycles. Fertil Steril. 2001; 76: 337–41. DOI: https://doi.org/10.1016/s0015-0282(01)01926-4

33. Kunz G., Leyendecker G. Uterine peristaltic activity during the menstrual cycle: characterization, regulation, function and dysfunction. Reprod Biomed Online. 2002; 4: 5–9. DOI: https://doi.org/10.1016/s1472-6483(12)60108-4

34. Bulletti C., de Ziegler D., Polli V., Diotallevi L., Ferro E.D., Flamigni C. Uterine contractility during the menstrual cycle. Hum Reprod. 2000; 15: 81–9. DOI: https://doi.org/10.1093/humrep/15.suppl_1.81

35. Aranda V., Cortez R., Fauci L. A model of Stokesian peristalsis and vesicle transport in a three-dimensional closed cavity. J Biomech. 2015; 48 (9): 1631–8. DOI: https://doi.org/10.1016/j.jbiomech.2015.02.029

36. Eytan O., Jaffa A.J., Elad D. Peristaltic flow in a tapered channel: application to embryo transport within the uterine cavity. Med Eng Phys. 2001; 23: 473–82. DOI: https://doi.org/10.1016/s1350-4533(01)00078-9

37. Singh N., Bahadur A., Mittal S., Malhotra N., Bhatt A. Predictive value of endometrial thickness, pattern and sub-endometrial blood flows on the day of hCG by 2D Doppler in in-vitro fertilization cycles: a prospective clinical study from a tertiary care unit. J Hum Reprod Sci. 2011; 4 (1): 29–33. DOI: https://doi.org/10.4103/0974-1208.82357

38. Mumusoglu S., Polat M., Ozbek I.Y., Bozdag G., Papanikolaou E.G., Esteves S.C., et al. Preparation of the endometrium for frozen embryo transfer: a systematic review. Front Endocrinol (Lausanne). 2021; 12: 688237. DOI: https://doi.org/10.3389/fendo.2021.688237

39. Hunt S., Abdallah K.S., Ng E., Rombauts L., Vollenhoven B., Mol B.W. Impairment of uterine contractility is associated with unexplained infertility. Semin Reprod Med. 2020; 38 (1): 61–73. DOI: https://doi.org/10.1055/s-0040-1716409

40. Meirzon D., Jaffa A.J., Gordon Z., Elad D. A new method for analysis of non-pregnant uterine peristalsis using transvaginal ultrasound. Ultrasound Obstet Gynecol. 2011; 38 (2): 217–24. DOI: https://doi.org/10.1002/uog.8950

41. Liu S., Zhang Q., Yin C., et al. An optimised repetition time (TR) for cine imaging of uterine peristalsis on 3 T MRI. Clin Radiol. 2018; 73 (7): 678.e7–12. DOI: https://doi.org/10.1016/j.crad.2018.03.012

42. Mori K., Tokunaga Y., Sakumoto T., et al. A uterine motion classification in MRI data for female infertility. Curr Med Imaging. 2020; 16 (5): 479–90. DOI: https://doi.org/10.2174/1573405614666180917123654

43. Kuijsters N.P.M., Methorst W.G., Kortenhorst M.S.Q., Rabotti C., Mischi M., Schoot B.C. Uterine peristalsis and fertility: current knowledge and future perspectives: a review and meta-analysis. Reprod Biomed Online. 2017; 35 (1): 50–71. DOI: https://doi.org/10.1016/j.rbmo.2017.03.019

44. Fornazari V.A.V., Salazar G.M.M., Vayego S.A., Nunes T.F., Goncalves B., Szejnfeld J., et al. Impact of uterine contractility on quality of life of women undergoing uterine fibroid embolization. CVIR Endovasc. 2019; 2 (1): 36. DOI: https://doi.org/10.1186/s42155-019-0080-2

45. Gestel I., IJland M.M., Hoogland H.J., Evers J.L. Endometrial wave-like activity in the non-pregnant uterus. Hum Reprod Update. 2003; 9: 131–8. DOI: https://doi.org/10.1093/humupd/dmg011

46. Zhu L., Li Y., Xu A. Influence of controlled ovarian hyperstimulation on uterine peristalsis in infertile women. Hum Reprod. 2012; 27 (9): 2684–9. DOI: https://doi.org/10.1093/humrep/des257

47. Moliner B., Llacer J., Sellers F., et al. 4D ultrasound as a method to assess uterine peristalsis. Fertil Steril. 2021; 116 (1): 272–4. DOI: https://doi.org/10.1016/j.fertnstert. 2021.02.01

48. Fanchin R., Ayoubi J.M., Olivennes F., et al. Hormonal influence on the uterine contractility during ovarian stimulation. Hum Reprod. 2000; 15 (suppl 1): 90–100.

49. Pierzyński P., Zbucka-Kretowska M. Uterine contractile activity at embryo transfer as a new pharmacotherapeutic target in assisted reproduction. Ginekol Pol. 2014; 85 (8): 609–13. DOI: https://doi.org/10.17772/gp/1780

50. Devyatova E.A., Tsaturova K.A., Vartanyan E.V. The role of evaluation of endometrial wavelike activity at prognosing of successful implantation. Problemy reproduktsii [Problems of Reproduction]. 2016; (4): 47–51. DOI: https://doi.org/10.17116/repro201622447-51 (in Russian)

51. Salekhov S.A., Korabel’nikova I.A., Gaydukov S.N., Mel’nikov I.A., Kudaybergenova L.T. pathogenetic features of low efficiency of intrauterine insemination. Mezhdunarodniy zhurnal meditsiny i psikhologii [International Journal of Medicine and Psychology]. 2020; 3 (2): 130–6. DOI: https://doi.org/10.34680/2076-8052.2020.4(120).46-49 (in Russian)

52. Ayoubi J.M., Epiney M., Brioschi P.A., et al. Comparison of changes in uterine contraction frequency after ovulation in the menstrual cycle and in in vitro fertilization cycles. Fertil Steril. 2003; 79 (5): 1101–5. DOI: https://doi.org/10.1016/s0015-0282(03)00179-1

53. Kuijsters N.P.M., Methorst W.G., Kortenhorst M.S.Q., et al. Uterine peristalsis and fertility: current knowledge and future perspectives: a review and meta-analysis. Reprod Biomed Online. 2017; 35 (1): 50–71. DOI: https://doi.org/10.1016/j.rbmo.2017.03.019

54. Zhu L., Che H.S., Xiao L., Li Y.P. Uterine peristalsis before embryo transfer affects the chance of clinical pregnancy in fresh and frozen-thawed embryo transfer cycles. Hum Reprod. 2014; 29 (6): 1238–43. DOI: https://doi.org/10.1093/humrep/deu058

55. Khairy M., Dhillon R.K., Chu J., Rajkhowa M., Coomarasamy A. The effect of peri-implantation administration of uterine relaxing agents in assisted reproduction treatment cycles: a systematic review and meta-analysis. Reprod Biomed Online. 2016; 32 (4): 362–76. DOI: https://doi.org/10.1016/j.rbmo.2016.01.004

56. Selvi İ., Erdem M., Demirdağ E., et al. Comparison of frozen-thawed embryo transfer protocols in patients with previous cycle cancellation due to uterine peristalsis: a pilot study. Turk J Med Sci. 2021; 51 (3): 1365–72. DOI: https://doi.org/10.3906/sag-2012-149

All articles in our journal are distributed under the Creative Commons Attribution 4.0 International License (CC BY 4.0 license)