LEIOMYOMA AS AN INFERTILITY FACTOR: A SURGICAL REVIEW
Keywords:
leiomyoma, infertility, minimally invasive, hysteroscopy, laparoscopy
Abstract
Uterine fibroids are among the most common benign tumors in women of reproductive age. Their incidence is higher for African American women compared to Caucasian women. Women with fibroids may present with heterogeneous symptoms or may be diagnosed incidentally at routine checkups. Nowadays, a whole arsenal of diagnostic tools exists. Transvaginal ultrasound with color Doppler and 3D reconstruction, as well as hysteroscopy and nuclear magnetic resonance imaging (MRI), are the most useful. For the correct management of uterine fibroids, it is important to establish their location and type, according to existing classifications. Multiple studies have demonstrated their impact on fertility, especially in the case of submucosal, intracavitary ones. Most of the results in the literature on this issue come from assisted human reproduction clinics. This review aims to document the mechanisms by which uterine fibroids lead to low conception rates and clinical pregnancy rates and the available methods for their treatment to achieve pregnancy.
References
1. Wise LA, Laughlin-Tommaso SK. Epidemiology of uterine fibroids: from menarche to menopause. Clin Obstet Gynecol 2016;59(01): 2–24
2. Sparic R, Mirkovic L, Malvasi A, Tinelli A. Epidemiology of uterine myomas: a review. Int J Fertil Steril 2016;9(04):424–435
3. Marsh EE, Steinberg ML, Parker JB, Wu J, Chakravarti D, Bulun SE. Decreased expression of microRNA-29 family in leiomyoma contributes to increased major fibrillar collagen production. Fertil Steril 2016;106(03):766–772
4. Day Baird D, Dunson DB, Hill MC, Cousins D, Schectman JM. High cumulative inci- dence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol 2003;1:100–107
5. Marshall LM, Spiegelman D, Barbieri RL, Goldman MB, Manson JE, Colditz GA, Willett WC, Hunter DJ. Variation in the incidence of uterine leiomyoma among premenopausal women by age and race. Obstet Gynecol 1997;6:967–973.
6. Baird DD, Dunson DB, Hill MC, Cousins D, Schectman JM. High cumulative incidence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol 2003;188 (01):100–107
7. Kjerulff KH, Langenberg P, Seidman JD, Stolley PD, Guzinski GM. Uterine leiomyo- mas. Racial differences in severity, symptoms and age at diagnosis. J Reprod Med 1996;7:483–490.
8. Luoto R, Kaprio J, Rutanen EM, Taipale P, Perola M, Koskenvuo M. Heritability and risk factors of uterine fibroids–the Finnish Twin Cohort study. Maturitas 2000;37(01):15–26
9. Sato F, Mori M, Nishi M, Kudo R, Miyake H. Familial aggregation of uterine myomas in Japanese women. J Epidemiol 2002;12 (03):249–253
10. Fleischer R, Weston GC, Vollenhoven BJ, Rogers PA. Pathophy- siology of fibroid disease: angiogenesis and regulation of smooth muscle proliferation. Best Pract Res Clin Obstet Gynaecol 2008; 22(04):603–614
11. Dagur G, Suh Y, Warren K, Singh N, Fitzgerald J, Khan SA. Urological complications of uterine leiomyoma: a review of literature. Int Urol Nephrol 2016;48(06):941–948
12. Groszmann YS, Benacerraf BR. Complete evaluation of anatomy and morphology of the infertile patient in a single visit; the modern infertility pelvic ultrasound examination. Fertil Steril 2016;105(06):1381–1393
13. BullettiC,DEZieglerD,LeviSettiP,CicinelliE,PolliV,Stefanetti M. Myomas, pregnancy outcome, and in vitro fertilization. Ann NY Acad Sci 2004;1034:84–92
14. Zepiridis LI, Grimbizis GF, Tarlatzis BC. Infertility and uterine fibroids. Best Pract Res Clin Obstet Gynaecol 2016;34:66–73
15. Rackow BW, Arici A. Fibroids and in-vitro fertilization: which comes first? Curr Opin Obstet Gynecol 2005;17(03):225–231
16. Kim J. J., Sefton E. C. The role of progesterone signaling in the pathogenesis of uterine leiomyoma. Molecular and Cellular Endocrinology. 2012;358(2):223–231. doi: 10.1016/j.mce.2011.05.044.
17. Rein MS, Friedman AJ, Barbieri RL, Pavelka K, Fletcher JA, Morton CC. Cytogenic abnormalities in uterine leiomyomata. Obstet Gynecol 1991;77:923–6.
18. Islam MS, Protic O, Stortoni P, Grechi G, Lamanna P, Petraglia F, Castellucci M, Ciarmela P Fertil Steril. 2013 Jul; 100(1):178-93
19. Miska EA. How microRNAs control cell division, differentiation and death. Curr Opin Genet Dev 2005;15:563–8.
20. Marsh EE, Lin Z, Yin P, Milad M, Chakravarti D, Bulun SE. Differential ex- pression of microRNA species in human uterine leiomyoma versus normal myometrium. Fertil Steril 2008;89:1771–6.
21. Pan Q, Luo X, Chegini N. Differential expression of microRNAs in myome- trium and leiomyomas and regulation by ovarian steroids. J Cell Mol Med 2008;12:227–40.
22. Georgieva B, Milev I, Minkov I, Dimitrova I, Bradford AP, Baev V. Character- ization of the uterine leiomyoma microRNAome by deepsequencing. Ge- nomics 2012;93:275–81.
23. Ishikawa H, Reierstad S, Demura M, Rademaker AW, Kasai T, Inoue M, et al. High aromatase expression in uterine leiomyoma tissues of African- American women. J Clin Endocrinol Metab 2009;94:1752–6.
24. Ishikawa H, Ishi K, Serna VA, Kakazu R, Bulun SE, Kurita T. Progesterone is essential for maintenance and growth of uterine leiomyoma. Endocrinol- ogy 2010;151:2433–42.
25. Gao Z, Matsuo H, Nakago S, Kurachi O, Maruo T. p53 Tumor suppressor protein content in human uterine leiomyomas and its down-regulation by 17 beta-estradiol. J Clin Endocrinol Metab 2002;87:3915–20.
26. Andersen J, Grine E, Eng CL, Zhao K, Barbieri RL, Chumas JC, et al. Expres- sion of connexin-43 in human myometrium and leiomyoma. Am J Obstet Gynecol 1993;169:1266–76.
27. Lee EJ, Bajracharya P, Lee DM, Cho KH, Kim KJ, Bae YK, et al. Gene expres- sion profiles of uterine normal myometrium and leiomyoma andtheir es- trogen responsiveness in vitro. Korean J Pathol 2010;44:272–83.
28. Swartz CD, Afshari CA, Yu L, Hall KE, Dixon D. Estrogen-induced changes in IGF-I, Myb family and MAP kinase pathway genes in human uterine leio- myoma and normal uterine smooth muscle cell lines. Mol Hum Reprod 2005;11:441–50.
29. Kurachi O, Matsuo H, Samoto T, Maruo T. Tumor necrosis factor-a expres- sion in human uterine leiomyoma and its down-regulation by progester- one. J Clin Endocrinol Metab 2001;86:2275–80.
30. Yamada T, Nakago S, Kurachi O, Wang J, Takekida S, Matsuo H, et al. Pro- gesterone down-regulates insulin-like growth factor-I expression in cul- tured human uterine leiomyoma cells. Hum Reprod 2004;19:815–21.
31. Shimomura Y, Matsuo H, Samoto T, Maruo T. Up-regulation by progester- one of proliferating cell nuclear antigen and epidermal growth factor ex- pression in human uterine leiomyoma. J Clin Endocrinol Metab 1998;83: 2192–8.
32. Arici A, Sozen I. Transforming growth factor-beta3 is expressed at high levels in leiomyoma where it stimulates fibronectin expression and cell pro- liferation. Fertil Steril 2000;73:1006–11.
33. Matsuo H, Maruo T, Samoto T. Increased expression of Bcl-2 protein in hu- man uterine leiomyoma and its up-regulation by progesterone. J Clin Endo- crinol Metab 1997;82:293–9.
34. Tinelli A, Malvasi A, Rahimi S, Negro R, Cavallotti C, Vergara D, Vittori G, Mettler L. Myoma pseudocapsule: a distinct endocrino-anatomical entity in gynecological surgery. Gynecol Endocrinol. 2009 Oct;25(10):661-7. doi: 10.1080/09513590903015502. PMID: 19526398.
35. Arleo EK, Schwartz PE, Hui P, et al. Review of leiomyoma vari- ants. AJR. 2015;205:912–21.
36. McLucas B. Diagnosis, imaging and anatomical classification of uterine fibroids. Best Pract Res Clin Obstet Gynaecol. 2008;22:627–642
37. Munro MG, Crithcley HOD, Fraser IS, for the FIGO Working Group on Menstrual Disorders. The FIGO classification of causes of abnormal uterine bleeding. Int J Gynaecol Obstet. 2011; 113(1):1–2.
38. Kinkel K, Ascher SM, Reinhold C. Benign Disease of the Uterus. 2018 Mar 21. In: Hodler J, Kubik-Huch RA, von Schulthess GK, editors. Diseases of the Abdomen and Pelvis 2018-2021: Diagnostic Imaging - IDKD Book [Internet]. Cham (CH): Springer; 2018. Chapter 3. PMID: 31314373.
39. Parker WH. Etiology, symptomatology, and diagnosis of uterine myomas. Fertil Steril. 2007 Apr;87(4):725-36. doi: 10.1016/j.fertnstert.2007.01.093. PMID: 17430732.
40. Soares SR, Barbosa dos Reis MM, Camargos AF. Diagnostic accuracy of sonohysterography, transvaginal sonography, and hysterosalpingography in patients with uterine cavity diseases. Fertil Steril. 2000;73:406–411
41. Rashid SQ, Chou YH, Tiu CM, et al. Ultrasonography of uterine leiomyomas. J Med Ultrasound. 2016;24:3e12
42. Valentin L. Characterizing acute gynaecological pathology with ultrasound: an overview and case examples. Best Pract Res Clin Obstet Gynaecol. 2009 Oct; 23(5):577-93
43. Wallach EE, Vlahos NF. Uterine myomas: an overview of development, clinical features, and management. Obstet Gynecol. 2004 Aug; 104(2):393-406
44. Wilde S, Scott-Barrett S. Radiological appearances of uterine fibroids. Indian J Radiol Imaging. 2009;19(3):222-231. doi:10.4103/0971-3026.54887
45. Amant F, Coosemans A, Debiec-Rychter M, et al. Clinical management of uterine sarcomas. Lancet Oncol. 2009;10:1188.
46. Van den Bosch T, Van Schoubroeck D. Ultrasound diagnosis of endometriosis and adenomyosis: State of the art. Best Pract Res Clin Obstet Gynaecol. 2018 Aug;51:16-24. doi: 10.1016/j.bpobgyn.2018.01.013. Epub 2018 Feb 14. PMID: 29506961.
47. Sakhel K, Abuhamad A. Sonography of adenomyosis. J Ultrasound Med. 2012 May;31(5):805-8. doi: 10.7863/jum.2012.31.5.805. PMID: 22535729.
48. Exacoustos C, Brienza L, Di Giovanni A, et al. Adenomyosis: three-dimensional sonographic findings of the junctional zone and correlation with histology. Ultrasound Obstet Gynecol. 2011 Apr; 37(4):471-9
49. Testa AC, Di Legge A, Bonatti M, Manfredi R, Scambia G. Imaging techniques for evaluation of uterine myomas. Best Pract Res Clin Obstet Gynaecol. 2016 Jul;34:37-53. doi: 10.1016/j.bpobgyn.2015.11.014. Epub 2015 Nov 30. PMID: 26803557.
50. Exacoustos C, Romanini ME, Amadio A, et al. Can gray-scale and color Doppler sonography differentiate between uterine leiomyosarcoma and leiomyoma? J Clin Ultrasound. 2007 Oct; 35(8):449-57
51. Woźniak A, Woźniak S. Ultrasonography of uterine leiomyomas. Prz Menopauzalny. 2017;16(4):113-117. doi:10.5114/pm.2017.72754
52. Ludwin A, Ludwin I, Pityński K, et al. Transrectal ultrasound-guided hysteroscopic myomectomy of submucosal myomas with a varying degree of myometrial penetration. J Minim Invasive Gynecol. 2013 Sep-Oct; 20(5):672-85
53. Czuczwar P, Wozniak S, Szkodziak P, et al. Elastography improves the diagnostic accuracy of sonography in differentiating endometrial polyps and submucosal fibroids. J Ultrasound Med. 2016;35:2389–2395.
54. Cohen JR, Luxman D, Sagi J, et al. Ultrasonic "honeycomb" appearance of uterine submucous fibroids undergoing cystic degeneration. J Clin Ultrasound. 1995 Jun; 23(5):293- 6
55. Minsart AF, Ntoutoume Sima F, Vandenhoute K, Jani J, Van Pachterbeke C. Does three-dimensional power Doppler ultrasound predict histopathological findings of uterine fibroids? A preliminary study. Ultrasound Obstet Gynecol. 2012 Dec;40(6):714-20. doi: 10.1002/uog.11155. Epub 2012 Nov 16. PMID: 22581621.
56. Bonneau C, Thomassin-Naggara I, Dechoux S, et al. Value of ultrasonography and magnetic resonance imaging for the characterization of uterine mesenchymal tumors. Acta Obstet Gynecol Scand. 2014 Mar;93(3):261-8
57. Yang Q, Zhang LH, Su J, Liu J (2011) The utility of diffusion-weighted MR imaging in differentiation of uterine adenomyosis and leiomyoma. European journal of radiology. 2011: 79:e47-51.
58. Jondal DE, Wang J, Chen J, et al. Uterine fibroids: correlation between MRI appearance and stiffness via magnetic resonance elastography. Abdom Radiol (NY) 2017 doi: 10.1007/s00261-017-1314-1.
59. BullettiC,DEZieglerD,LeviSettiP,CicinelliE,PolliV,Stefanetti M. Myomas, pregnancy outcome, and in vitro fertilization. Ann NY Acad Sci 2004;1034:84–92
60. Zepiridis LI, Grimbizis GF, Tarlatzis BC. Infertility and uterine fibroids. Best Pract Res Clin Obstet Gynaecol 2016;34:66–73
61. Pritts EA, Parker WH, Olive DL. Fibroids and infertility: an updated systematic review of the evidence. Fertil Steril 2009; 91(04):1215–1223
62. Somigliana E, Vercellini P, Daguati R, Pasin R, De Giorgi O, Crosignani PG. Fibroids and female reproduction: a critical analysis of the evidence. Hum Reprod Update. 2007;13:465–476.
63. Buttram VC, Jr, Reiter RC. Uterine leiomyomata: etiology, symptomatology, and management. Fertil Steril. 1981;36:433–445.
64. Horne AW, Critchley HO. The effect of uterine fibroids on embryo implantation. Semin Reprod Med. 2007;25:483–489.
65. Practice Committee of American Society for Reproductive Medicine in collaboration with Society of Reproductive Surgeons. Myomas and reproductive function. Fertility and Sterility. 2008;90(5):S125–S130. doi: 10.1016/j.fertnstert.2008.09.012.
66. Donnez J., Jadoul P. What are the implications of myomas on fertility? A need for a debate? Human Reproduction. 2002;17(6):1424–1430. doi: 10.1093/humrep/17.6.1424.
67. Benecke C., Kruger T. F., Siebert T. I., Van der Merwe J. P., Steyn D. W. Effect of fibroids on fertility in patients undergoing assisted reproduction. A structured literature review. 2005;59:225–30.
68. Cook H, Ezzati M, Segars JH, McCarthy K. The impact of uterine leiomyomas on reproductive outcomes. Minerva Ginecol. 2010;62(3):225-236.
69. Deligdish L., Loewenthal M. Endometrial changes associated with myomata of the uterus. Journal of Clinical Pathology. 1970;23(8):676–680. doi: 10.1136/jcp.23.8.676.
70. Maguire M, Segars JH. Benign uterine disease: leiomyomata and benign polyps. In: Aplin JD, Fazleabas AT, Glasser SR, Giudice LC, editors. The Endometrium: Molecular, Cellular and Clinical Perspectives. 2nd Edition. Informa HealthCare; London, UK: 2008. pp. 797–812.
71. Sharma SP, Misra SD, Mittal VP. Endometrial changes--a criterion for the diagnosis of submucous uterine leiomyoma. Indian J Pathol Microbiol. 1979 Jan;22(1):33-6. PMID: 544482.
72. Rackow B. W., Taylor H. S. Submucosal uterine leiomyomas have a global effect on molecular determinants of endometrial receptivity. Fertility and Sterility. 2010;93(6):2027–2034. doi: 10.1016/j.fertnstert.2008.03.029.
73. Pritts E. A. Fibroids and infertility: a systematic review of the evidence. Obstetrical and Gynecological Survey. 2001;56(8):483–491. doi: 10.1097/00006254-200108000-00022.
74. Vlahos NF, Theodoridis TD, Partsinevelos GA. Myomas and Adenomyosis: Impact on Reproductive Outcome. Biomed Res Int. 2017;2017:5926470. doi:10.1155/2017/5926470
75. Sunkara S. K., Khairy M., El-Toukhy T., Khalaf Y., Coomarasamy A. The effect of intramural fibroids without uterine cavity involvement on the outcome of IVF treatment: a systematic review and meta-analysis. Human Reproduction. 2010;25(2):418–429. doi: 10.1093/humrep/dep396
76. Di Spiezio Sardo A., Mazzon I., Bramante S., et al. Hysteroscopic myomectomy: a comprehensive review of surgical techniques. Human Reproduction Update. 2008;14(2):101–119. doi: 10.1093/humupd/dmm041.
77. Loffer F. D. Hysteroscopic endometrial ablation with the ndiyag laser using a nontouch technique. Obstetrics and Gynecology. 1987;69(4):679–682.
78. Bulletti C, De Ziegler D, Setti PL, Cicinelli E, Polli V, Stefanetti M. Myomas, pregnancy outcome, and in vitro fertilization. Ann N Y Acad Sci. 2004;1034:84–92.
79. Casini ML, Rossi F, Agostini R, Unfer V. Effect of the position of fibroids on fertility. Gynecol Endocrinol. 2006;22:106–109.
80. Donnez J, Dolmans MM. Uterine fibroid management: from the present to the future. Hum Reprod Update. 2016;22(6):665-686. doi:10.1093/humupd/dmw023
81. Makris N, Vomvolaki E, Mantzaris G, Kalmantis K, Hatzipappas J, Antsaklis A. Role of a bipolar resectoscope in subfertile women with submucous myomas and menstrual disorders. J Obstet Gynaecol Res 2007;33(06):849–854
82. Shokeir TA. Hysteroscopic management in submucous fibroids to improve fertility. Arch Gynecol Obstet 2005;273(01):50–54
83. Giatras K, Berkeley AS, Noyes N, Licciardi F, Lolis D, Grifo JA. Fertility after hysteroscopic resection of submucous myomas. J Am Assoc Gynecol Laparosc 1999;6(02):155–158
84. Jefferys A, Akande V. Modern management of fibroids. Obstet Gynaecol Reprod Med 2016;26(05):127–132
85. Whynott RM, Vaught KCC, Segars JH. The Effect of Uterine Fibroids on Infertility: A Systematic Review. Semin Reprod Med. 2017 Nov;35(6):523-532. doi: 10.1055/s-0037-1607295. Epub 2017 Nov 3. PMID: 29100240.
86. Zupi E, Sbracia M, Marconi D, Munro MG. Myolysis of uterine fibroids: is there a role? Clin Obstet Gynecol 2006;49:821–33.
87. Seracchioli R, Rossi S, Govoni F, Rossi E, Venturoli S, Bulletti C, et al. Fertility and obstetric outcome after laparoscopic myomectomy of large myomata: a randomized comparison with abdominal myomectomy. Hum Reprod 2000;15:2663–8.
88. Vercellini P, Bocciolone L, Colombo A, Vendola N, Meschia M, Bolis G. Gonadotropin releasing hormone agonist treatment before hysterectomy for menorrhagia and uterine leiomyomas. Acta Obstet Gynecol Scand 1993;72:369–73.
89. Mazzon I. Palermo, Italy: COFESE: 1995. Nuova technical per la miometomia isteroscopia: enucleazione con ansa fredda.
90. Di Spiezio Sardo A., Calagna G., Scognamiglio M., O'Donovan P., Campo R., De Wilde R. L. Prevention of intrauterine post-surgical adhesions in hysteroscopy. A systematic review. European Journal of Obstetrics Gynecology and Reproductive Biology. 2016;203:182–192. doi: 10.1016/j.ejogrb.2016.05.050.
2. Sparic R, Mirkovic L, Malvasi A, Tinelli A. Epidemiology of uterine myomas: a review. Int J Fertil Steril 2016;9(04):424–435
3. Marsh EE, Steinberg ML, Parker JB, Wu J, Chakravarti D, Bulun SE. Decreased expression of microRNA-29 family in leiomyoma contributes to increased major fibrillar collagen production. Fertil Steril 2016;106(03):766–772
4. Day Baird D, Dunson DB, Hill MC, Cousins D, Schectman JM. High cumulative inci- dence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol 2003;1:100–107
5. Marshall LM, Spiegelman D, Barbieri RL, Goldman MB, Manson JE, Colditz GA, Willett WC, Hunter DJ. Variation in the incidence of uterine leiomyoma among premenopausal women by age and race. Obstet Gynecol 1997;6:967–973.
6. Baird DD, Dunson DB, Hill MC, Cousins D, Schectman JM. High cumulative incidence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol 2003;188 (01):100–107
7. Kjerulff KH, Langenberg P, Seidman JD, Stolley PD, Guzinski GM. Uterine leiomyo- mas. Racial differences in severity, symptoms and age at diagnosis. J Reprod Med 1996;7:483–490.
8. Luoto R, Kaprio J, Rutanen EM, Taipale P, Perola M, Koskenvuo M. Heritability and risk factors of uterine fibroids–the Finnish Twin Cohort study. Maturitas 2000;37(01):15–26
9. Sato F, Mori M, Nishi M, Kudo R, Miyake H. Familial aggregation of uterine myomas in Japanese women. J Epidemiol 2002;12 (03):249–253
10. Fleischer R, Weston GC, Vollenhoven BJ, Rogers PA. Pathophy- siology of fibroid disease: angiogenesis and regulation of smooth muscle proliferation. Best Pract Res Clin Obstet Gynaecol 2008; 22(04):603–614
11. Dagur G, Suh Y, Warren K, Singh N, Fitzgerald J, Khan SA. Urological complications of uterine leiomyoma: a review of literature. Int Urol Nephrol 2016;48(06):941–948
12. Groszmann YS, Benacerraf BR. Complete evaluation of anatomy and morphology of the infertile patient in a single visit; the modern infertility pelvic ultrasound examination. Fertil Steril 2016;105(06):1381–1393
13. BullettiC,DEZieglerD,LeviSettiP,CicinelliE,PolliV,Stefanetti M. Myomas, pregnancy outcome, and in vitro fertilization. Ann NY Acad Sci 2004;1034:84–92
14. Zepiridis LI, Grimbizis GF, Tarlatzis BC. Infertility and uterine fibroids. Best Pract Res Clin Obstet Gynaecol 2016;34:66–73
15. Rackow BW, Arici A. Fibroids and in-vitro fertilization: which comes first? Curr Opin Obstet Gynecol 2005;17(03):225–231
16. Kim J. J., Sefton E. C. The role of progesterone signaling in the pathogenesis of uterine leiomyoma. Molecular and Cellular Endocrinology. 2012;358(2):223–231. doi: 10.1016/j.mce.2011.05.044.
17. Rein MS, Friedman AJ, Barbieri RL, Pavelka K, Fletcher JA, Morton CC. Cytogenic abnormalities in uterine leiomyomata. Obstet Gynecol 1991;77:923–6.
18. Islam MS, Protic O, Stortoni P, Grechi G, Lamanna P, Petraglia F, Castellucci M, Ciarmela P Fertil Steril. 2013 Jul; 100(1):178-93
19. Miska EA. How microRNAs control cell division, differentiation and death. Curr Opin Genet Dev 2005;15:563–8.
20. Marsh EE, Lin Z, Yin P, Milad M, Chakravarti D, Bulun SE. Differential ex- pression of microRNA species in human uterine leiomyoma versus normal myometrium. Fertil Steril 2008;89:1771–6.
21. Pan Q, Luo X, Chegini N. Differential expression of microRNAs in myome- trium and leiomyomas and regulation by ovarian steroids. J Cell Mol Med 2008;12:227–40.
22. Georgieva B, Milev I, Minkov I, Dimitrova I, Bradford AP, Baev V. Character- ization of the uterine leiomyoma microRNAome by deepsequencing. Ge- nomics 2012;93:275–81.
23. Ishikawa H, Reierstad S, Demura M, Rademaker AW, Kasai T, Inoue M, et al. High aromatase expression in uterine leiomyoma tissues of African- American women. J Clin Endocrinol Metab 2009;94:1752–6.
24. Ishikawa H, Ishi K, Serna VA, Kakazu R, Bulun SE, Kurita T. Progesterone is essential for maintenance and growth of uterine leiomyoma. Endocrinol- ogy 2010;151:2433–42.
25. Gao Z, Matsuo H, Nakago S, Kurachi O, Maruo T. p53 Tumor suppressor protein content in human uterine leiomyomas and its down-regulation by 17 beta-estradiol. J Clin Endocrinol Metab 2002;87:3915–20.
26. Andersen J, Grine E, Eng CL, Zhao K, Barbieri RL, Chumas JC, et al. Expres- sion of connexin-43 in human myometrium and leiomyoma. Am J Obstet Gynecol 1993;169:1266–76.
27. Lee EJ, Bajracharya P, Lee DM, Cho KH, Kim KJ, Bae YK, et al. Gene expres- sion profiles of uterine normal myometrium and leiomyoma andtheir es- trogen responsiveness in vitro. Korean J Pathol 2010;44:272–83.
28. Swartz CD, Afshari CA, Yu L, Hall KE, Dixon D. Estrogen-induced changes in IGF-I, Myb family and MAP kinase pathway genes in human uterine leio- myoma and normal uterine smooth muscle cell lines. Mol Hum Reprod 2005;11:441–50.
29. Kurachi O, Matsuo H, Samoto T, Maruo T. Tumor necrosis factor-a expres- sion in human uterine leiomyoma and its down-regulation by progester- one. J Clin Endocrinol Metab 2001;86:2275–80.
30. Yamada T, Nakago S, Kurachi O, Wang J, Takekida S, Matsuo H, et al. Pro- gesterone down-regulates insulin-like growth factor-I expression in cul- tured human uterine leiomyoma cells. Hum Reprod 2004;19:815–21.
31. Shimomura Y, Matsuo H, Samoto T, Maruo T. Up-regulation by progester- one of proliferating cell nuclear antigen and epidermal growth factor ex- pression in human uterine leiomyoma. J Clin Endocrinol Metab 1998;83: 2192–8.
32. Arici A, Sozen I. Transforming growth factor-beta3 is expressed at high levels in leiomyoma where it stimulates fibronectin expression and cell pro- liferation. Fertil Steril 2000;73:1006–11.
33. Matsuo H, Maruo T, Samoto T. Increased expression of Bcl-2 protein in hu- man uterine leiomyoma and its up-regulation by progesterone. J Clin Endo- crinol Metab 1997;82:293–9.
34. Tinelli A, Malvasi A, Rahimi S, Negro R, Cavallotti C, Vergara D, Vittori G, Mettler L. Myoma pseudocapsule: a distinct endocrino-anatomical entity in gynecological surgery. Gynecol Endocrinol. 2009 Oct;25(10):661-7. doi: 10.1080/09513590903015502. PMID: 19526398.
35. Arleo EK, Schwartz PE, Hui P, et al. Review of leiomyoma vari- ants. AJR. 2015;205:912–21.
36. McLucas B. Diagnosis, imaging and anatomical classification of uterine fibroids. Best Pract Res Clin Obstet Gynaecol. 2008;22:627–642
37. Munro MG, Crithcley HOD, Fraser IS, for the FIGO Working Group on Menstrual Disorders. The FIGO classification of causes of abnormal uterine bleeding. Int J Gynaecol Obstet. 2011; 113(1):1–2.
38. Kinkel K, Ascher SM, Reinhold C. Benign Disease of the Uterus. 2018 Mar 21. In: Hodler J, Kubik-Huch RA, von Schulthess GK, editors. Diseases of the Abdomen and Pelvis 2018-2021: Diagnostic Imaging - IDKD Book [Internet]. Cham (CH): Springer; 2018. Chapter 3. PMID: 31314373.
39. Parker WH. Etiology, symptomatology, and diagnosis of uterine myomas. Fertil Steril. 2007 Apr;87(4):725-36. doi: 10.1016/j.fertnstert.2007.01.093. PMID: 17430732.
40. Soares SR, Barbosa dos Reis MM, Camargos AF. Diagnostic accuracy of sonohysterography, transvaginal sonography, and hysterosalpingography in patients with uterine cavity diseases. Fertil Steril. 2000;73:406–411
41. Rashid SQ, Chou YH, Tiu CM, et al. Ultrasonography of uterine leiomyomas. J Med Ultrasound. 2016;24:3e12
42. Valentin L. Characterizing acute gynaecological pathology with ultrasound: an overview and case examples. Best Pract Res Clin Obstet Gynaecol. 2009 Oct; 23(5):577-93
43. Wallach EE, Vlahos NF. Uterine myomas: an overview of development, clinical features, and management. Obstet Gynecol. 2004 Aug; 104(2):393-406
44. Wilde S, Scott-Barrett S. Radiological appearances of uterine fibroids. Indian J Radiol Imaging. 2009;19(3):222-231. doi:10.4103/0971-3026.54887
45. Amant F, Coosemans A, Debiec-Rychter M, et al. Clinical management of uterine sarcomas. Lancet Oncol. 2009;10:1188.
46. Van den Bosch T, Van Schoubroeck D. Ultrasound diagnosis of endometriosis and adenomyosis: State of the art. Best Pract Res Clin Obstet Gynaecol. 2018 Aug;51:16-24. doi: 10.1016/j.bpobgyn.2018.01.013. Epub 2018 Feb 14. PMID: 29506961.
47. Sakhel K, Abuhamad A. Sonography of adenomyosis. J Ultrasound Med. 2012 May;31(5):805-8. doi: 10.7863/jum.2012.31.5.805. PMID: 22535729.
48. Exacoustos C, Brienza L, Di Giovanni A, et al. Adenomyosis: three-dimensional sonographic findings of the junctional zone and correlation with histology. Ultrasound Obstet Gynecol. 2011 Apr; 37(4):471-9
49. Testa AC, Di Legge A, Bonatti M, Manfredi R, Scambia G. Imaging techniques for evaluation of uterine myomas. Best Pract Res Clin Obstet Gynaecol. 2016 Jul;34:37-53. doi: 10.1016/j.bpobgyn.2015.11.014. Epub 2015 Nov 30. PMID: 26803557.
50. Exacoustos C, Romanini ME, Amadio A, et al. Can gray-scale and color Doppler sonography differentiate between uterine leiomyosarcoma and leiomyoma? J Clin Ultrasound. 2007 Oct; 35(8):449-57
51. Woźniak A, Woźniak S. Ultrasonography of uterine leiomyomas. Prz Menopauzalny. 2017;16(4):113-117. doi:10.5114/pm.2017.72754
52. Ludwin A, Ludwin I, Pityński K, et al. Transrectal ultrasound-guided hysteroscopic myomectomy of submucosal myomas with a varying degree of myometrial penetration. J Minim Invasive Gynecol. 2013 Sep-Oct; 20(5):672-85
53. Czuczwar P, Wozniak S, Szkodziak P, et al. Elastography improves the diagnostic accuracy of sonography in differentiating endometrial polyps and submucosal fibroids. J Ultrasound Med. 2016;35:2389–2395.
54. Cohen JR, Luxman D, Sagi J, et al. Ultrasonic "honeycomb" appearance of uterine submucous fibroids undergoing cystic degeneration. J Clin Ultrasound. 1995 Jun; 23(5):293- 6
55. Minsart AF, Ntoutoume Sima F, Vandenhoute K, Jani J, Van Pachterbeke C. Does three-dimensional power Doppler ultrasound predict histopathological findings of uterine fibroids? A preliminary study. Ultrasound Obstet Gynecol. 2012 Dec;40(6):714-20. doi: 10.1002/uog.11155. Epub 2012 Nov 16. PMID: 22581621.
56. Bonneau C, Thomassin-Naggara I, Dechoux S, et al. Value of ultrasonography and magnetic resonance imaging for the characterization of uterine mesenchymal tumors. Acta Obstet Gynecol Scand. 2014 Mar;93(3):261-8
57. Yang Q, Zhang LH, Su J, Liu J (2011) The utility of diffusion-weighted MR imaging in differentiation of uterine adenomyosis and leiomyoma. European journal of radiology. 2011: 79:e47-51.
58. Jondal DE, Wang J, Chen J, et al. Uterine fibroids: correlation between MRI appearance and stiffness via magnetic resonance elastography. Abdom Radiol (NY) 2017 doi: 10.1007/s00261-017-1314-1.
59. BullettiC,DEZieglerD,LeviSettiP,CicinelliE,PolliV,Stefanetti M. Myomas, pregnancy outcome, and in vitro fertilization. Ann NY Acad Sci 2004;1034:84–92
60. Zepiridis LI, Grimbizis GF, Tarlatzis BC. Infertility and uterine fibroids. Best Pract Res Clin Obstet Gynaecol 2016;34:66–73
61. Pritts EA, Parker WH, Olive DL. Fibroids and infertility: an updated systematic review of the evidence. Fertil Steril 2009; 91(04):1215–1223
62. Somigliana E, Vercellini P, Daguati R, Pasin R, De Giorgi O, Crosignani PG. Fibroids and female reproduction: a critical analysis of the evidence. Hum Reprod Update. 2007;13:465–476.
63. Buttram VC, Jr, Reiter RC. Uterine leiomyomata: etiology, symptomatology, and management. Fertil Steril. 1981;36:433–445.
64. Horne AW, Critchley HO. The effect of uterine fibroids on embryo implantation. Semin Reprod Med. 2007;25:483–489.
65. Practice Committee of American Society for Reproductive Medicine in collaboration with Society of Reproductive Surgeons. Myomas and reproductive function. Fertility and Sterility. 2008;90(5):S125–S130. doi: 10.1016/j.fertnstert.2008.09.012.
66. Donnez J., Jadoul P. What are the implications of myomas on fertility? A need for a debate? Human Reproduction. 2002;17(6):1424–1430. doi: 10.1093/humrep/17.6.1424.
67. Benecke C., Kruger T. F., Siebert T. I., Van der Merwe J. P., Steyn D. W. Effect of fibroids on fertility in patients undergoing assisted reproduction. A structured literature review. 2005;59:225–30.
68. Cook H, Ezzati M, Segars JH, McCarthy K. The impact of uterine leiomyomas on reproductive outcomes. Minerva Ginecol. 2010;62(3):225-236.
69. Deligdish L., Loewenthal M. Endometrial changes associated with myomata of the uterus. Journal of Clinical Pathology. 1970;23(8):676–680. doi: 10.1136/jcp.23.8.676.
70. Maguire M, Segars JH. Benign uterine disease: leiomyomata and benign polyps. In: Aplin JD, Fazleabas AT, Glasser SR, Giudice LC, editors. The Endometrium: Molecular, Cellular and Clinical Perspectives. 2nd Edition. Informa HealthCare; London, UK: 2008. pp. 797–812.
71. Sharma SP, Misra SD, Mittal VP. Endometrial changes--a criterion for the diagnosis of submucous uterine leiomyoma. Indian J Pathol Microbiol. 1979 Jan;22(1):33-6. PMID: 544482.
72. Rackow B. W., Taylor H. S. Submucosal uterine leiomyomas have a global effect on molecular determinants of endometrial receptivity. Fertility and Sterility. 2010;93(6):2027–2034. doi: 10.1016/j.fertnstert.2008.03.029.
73. Pritts E. A. Fibroids and infertility: a systematic review of the evidence. Obstetrical and Gynecological Survey. 2001;56(8):483–491. doi: 10.1097/00006254-200108000-00022.
74. Vlahos NF, Theodoridis TD, Partsinevelos GA. Myomas and Adenomyosis: Impact on Reproductive Outcome. Biomed Res Int. 2017;2017:5926470. doi:10.1155/2017/5926470
75. Sunkara S. K., Khairy M., El-Toukhy T., Khalaf Y., Coomarasamy A. The effect of intramural fibroids without uterine cavity involvement on the outcome of IVF treatment: a systematic review and meta-analysis. Human Reproduction. 2010;25(2):418–429. doi: 10.1093/humrep/dep396
76. Di Spiezio Sardo A., Mazzon I., Bramante S., et al. Hysteroscopic myomectomy: a comprehensive review of surgical techniques. Human Reproduction Update. 2008;14(2):101–119. doi: 10.1093/humupd/dmm041.
77. Loffer F. D. Hysteroscopic endometrial ablation with the ndiyag laser using a nontouch technique. Obstetrics and Gynecology. 1987;69(4):679–682.
78. Bulletti C, De Ziegler D, Setti PL, Cicinelli E, Polli V, Stefanetti M. Myomas, pregnancy outcome, and in vitro fertilization. Ann N Y Acad Sci. 2004;1034:84–92.
79. Casini ML, Rossi F, Agostini R, Unfer V. Effect of the position of fibroids on fertility. Gynecol Endocrinol. 2006;22:106–109.
80. Donnez J, Dolmans MM. Uterine fibroid management: from the present to the future. Hum Reprod Update. 2016;22(6):665-686. doi:10.1093/humupd/dmw023
81. Makris N, Vomvolaki E, Mantzaris G, Kalmantis K, Hatzipappas J, Antsaklis A. Role of a bipolar resectoscope in subfertile women with submucous myomas and menstrual disorders. J Obstet Gynaecol Res 2007;33(06):849–854
82. Shokeir TA. Hysteroscopic management in submucous fibroids to improve fertility. Arch Gynecol Obstet 2005;273(01):50–54
83. Giatras K, Berkeley AS, Noyes N, Licciardi F, Lolis D, Grifo JA. Fertility after hysteroscopic resection of submucous myomas. J Am Assoc Gynecol Laparosc 1999;6(02):155–158
84. Jefferys A, Akande V. Modern management of fibroids. Obstet Gynaecol Reprod Med 2016;26(05):127–132
85. Whynott RM, Vaught KCC, Segars JH. The Effect of Uterine Fibroids on Infertility: A Systematic Review. Semin Reprod Med. 2017 Nov;35(6):523-532. doi: 10.1055/s-0037-1607295. Epub 2017 Nov 3. PMID: 29100240.
86. Zupi E, Sbracia M, Marconi D, Munro MG. Myolysis of uterine fibroids: is there a role? Clin Obstet Gynecol 2006;49:821–33.
87. Seracchioli R, Rossi S, Govoni F, Rossi E, Venturoli S, Bulletti C, et al. Fertility and obstetric outcome after laparoscopic myomectomy of large myomata: a randomized comparison with abdominal myomectomy. Hum Reprod 2000;15:2663–8.
88. Vercellini P, Bocciolone L, Colombo A, Vendola N, Meschia M, Bolis G. Gonadotropin releasing hormone agonist treatment before hysterectomy for menorrhagia and uterine leiomyomas. Acta Obstet Gynecol Scand 1993;72:369–73.
89. Mazzon I. Palermo, Italy: COFESE: 1995. Nuova technical per la miometomia isteroscopia: enucleazione con ansa fredda.
90. Di Spiezio Sardo A., Calagna G., Scognamiglio M., O'Donovan P., Campo R., De Wilde R. L. Prevention of intrauterine post-surgical adhesions in hysteroscopy. A systematic review. European Journal of Obstetrics Gynecology and Reproductive Biology. 2016;203:182–192. doi: 10.1016/j.ejogrb.2016.05.050.
Published
2021-12-12
How to Cite
[1]
F. Frîncu, “LEIOMYOMA AS AN INFERTILITY FACTOR: A SURGICAL REVIEW”, JSS, vol. 8, no. 4, Dec. 2021.
Section
Articles
