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Published in: Reproductive Biology and Endocrinology 1/2016

Open Access 01-12-2016 | Research

Oestrogen-induced angiogenesis and implantation contribute to the development of parasitic myomas after laparoscopic morcellation

Authors: Ben-Shian Huang, Muh-Hwa Yang, Peng-Hui Wang, Hsin-Yang Li, Teh-Ying Chou, Yi-Jen Chen

Published in: Reproductive Biology and Endocrinology | Issue 1/2016

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Abstract

Background

Iatrogenic parasitic myomas (PMs), caused by intra-corporeal power morcellation during laparoscopy is gradually increasing. However, the pathogenesis and medical treatment of PMs remain largely unelucidated.

Methods

Laparoscopically-induced PM xenografted mouse model was conducted by xenografting human uterine myoma fragments into the abdominal cavity of SCID mice and hormonal manipulation was performed using this mouse model to demonstrate the role of oestrogen in the development of implanted PMs. Immunohistochemistry of oestrogen receptor α (ERα), progesterone receptor (PR), vimentin, vascular endothelial growth factor (VEGF), microvessel density (MVD) and Ki-67 index was performed and compared.

Results

In the patient with PMs, ERα, PR, angiogenesis and proliferative property expression were upregulated in PM lesions compared to uterine myomas. In the laparoscopically-induced PM mouse model, implanted myomas had more steroid receptor expressions, angiogenesis and proliferative property compared with pre-xenografted or non-implanted myoma. Depletion of oestrogen in the ovariectomized (OVX) mice decreased laparoscopically-induced PM implantations. In comparison, the implantations of PMs were increased with additional E2 supplement. Hormonal manipulation in the PM mouse model, including AI, GnRHa and SERM groups, were compared and AI significantly decreased the implantations, steroid receptor, angiogenesis, cell density, and proliferative index of PMs compared with control group. Furthermore, GnRHa significantly decreased VEGF and MVD expressions compared with control group.

Conclusions

These data highlight the crucial role of oestrogen in the development of laparoscopically-induced PMs and suggest that hormone manipulation may be a potential therapeutic agent.

Trial registration

This protocol was approved by the Human and Animal Institutional Review Board of Taipei Veterans General Hospital (VGHIRB No 2014-10-002C on Nov. 17th, 2014; IACUC 2014-119 on Aug. 22nd, 2014).
Appendix
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Literature
2.
go back to reference Chabbert-Buffet N, Esber N, Bouchard P. Fibroid growth and medical options for treatment. Fertil Steril. 2014;102:630–9.CrossRefPubMed Chabbert-Buffet N, Esber N, Bouchard P. Fibroid growth and medical options for treatment. Fertil Steril. 2014;102:630–9.CrossRefPubMed
3.
go back to reference Sami Walid M, Heaton RL. The role of laparoscopic myomectomy in the management of uterine fibroids. Curr Opin Obstet Gynecol. 2011;23:273–7.CrossRefPubMed Sami Walid M, Heaton RL. The role of laparoscopic myomectomy in the management of uterine fibroids. Curr Opin Obstet Gynecol. 2011;23:273–7.CrossRefPubMed
4.
go back to reference Steiner RA, Wight E, Tadir Y, Haller U. Electrical cutting device for laparoscopic removal of tissue from the abdominal cavity. Obstet Gynecol. 1993;81:471–4.PubMed Steiner RA, Wight E, Tadir Y, Haller U. Electrical cutting device for laparoscopic removal of tissue from the abdominal cavity. Obstet Gynecol. 1993;81:471–4.PubMed
5.
6.
go back to reference Park JY, Park SK, Kim DY, Kim JH, Kim YM, Kim YT, Nam JH. The impact of tumor morcellation during surgery on the prognosis of patients with apparently early uterine leiomyosarcoma. Gynecol Oncol. 2011;122:255–9.CrossRefPubMed Park JY, Park SK, Kim DY, Kim JH, Kim YM, Kim YT, Nam JH. The impact of tumor morcellation during surgery on the prognosis of patients with apparently early uterine leiomyosarcoma. Gynecol Oncol. 2011;122:255–9.CrossRefPubMed
7.
go back to reference Ostrzenski A. Uterine leiomyoma particle growing in an abdominal-wall incision after laparoscopic retrieval. Obstet Gynecol. 1997;89:853–4.CrossRefPubMed Ostrzenski A. Uterine leiomyoma particle growing in an abdominal-wall incision after laparoscopic retrieval. Obstet Gynecol. 1997;89:853–4.CrossRefPubMed
8.
go back to reference Cucinella G, Granese R, Calagna G, Somigliana E, Perino A. Parasitic myomas after laparoscopic surgery: an emerging complication in the use of morcellator? Description of four cases. Fertil Steril. 2011;96:e90–6.CrossRefPubMed Cucinella G, Granese R, Calagna G, Somigliana E, Perino A. Parasitic myomas after laparoscopic surgery: an emerging complication in the use of morcellator? Description of four cases. Fertil Steril. 2011;96:e90–6.CrossRefPubMed
9.
go back to reference Sinha R, Hegde A, Mahajan C, Dubey N, Sundaram M. Laparoscopic myomectomy: do size, number, and location of the myomas form limiting factors for laparoscopic myomectomy? J Minim Invasive Gynecol. 2008;15:292–300.CrossRefPubMed Sinha R, Hegde A, Mahajan C, Dubey N, Sundaram M. Laparoscopic myomectomy: do size, number, and location of the myomas form limiting factors for laparoscopic myomectomy? J Minim Invasive Gynecol. 2008;15:292–300.CrossRefPubMed
10.
go back to reference Yanazume S, Tsuji T, Yoshioka T, Yamasaki H, Yoshinaga M, Douchi T. Large parasitic myomas in abdominal subcutaneous adipose tissue along a previous myomectomy scar. J Obstet Gynaecol Res. 2012;38:875–9.CrossRefPubMed Yanazume S, Tsuji T, Yoshioka T, Yamasaki H, Yoshinaga M, Douchi T. Large parasitic myomas in abdominal subcutaneous adipose tissue along a previous myomectomy scar. J Obstet Gynaecol Res. 2012;38:875–9.CrossRefPubMed
11.
go back to reference Huang PS, Chang WC, Huang SC. Iatrogenic parasitic myoma: a case report and review of the literature. Taiwan J Obstet Gynecol. 2014;53:392–6.CrossRefPubMed Huang PS, Chang WC, Huang SC. Iatrogenic parasitic myoma: a case report and review of the literature. Taiwan J Obstet Gynecol. 2014;53:392–6.CrossRefPubMed
12.
go back to reference Park BJ, Kim YW, Maeng LS, Kim TE. Disseminated peritoneal leiomyomatosis after hysterectomy: a case report. J Reprod Med. 2011;56:456–60.PubMed Park BJ, Kim YW, Maeng LS, Kim TE. Disseminated peritoneal leiomyomatosis after hysterectomy: a case report. J Reprod Med. 2011;56:456–60.PubMed
13.
go back to reference Kumar S, Sharma JB, Verma D, Gupta P, Roy KK, Malhotra N. Disseminated peritoneal leiomyomatosis: an unusual complication of laparoscopic myomectomy. Arch Gynecol Obstet. 2008;278:93–5.CrossRefPubMed Kumar S, Sharma JB, Verma D, Gupta P, Roy KK, Malhotra N. Disseminated peritoneal leiomyomatosis: an unusual complication of laparoscopic myomectomy. Arch Gynecol Obstet. 2008;278:93–5.CrossRefPubMed
14.
go back to reference Sinha R, Sundaram M, Mahajan C, Sambhus A. Multiple leiomyomas after laparoscopic hysterectomy: report of two cases. J Minim Invasive Gynecol. 2007;14:123–7.CrossRefPubMed Sinha R, Sundaram M, Mahajan C, Sambhus A. Multiple leiomyomas after laparoscopic hysterectomy: report of two cases. J Minim Invasive Gynecol. 2007;14:123–7.CrossRefPubMed
15.
go back to reference Leren V, Langebrekke A, Qvigstad E. Parasitic leiomyomas after laparoscopic surgery with morcellation. Acta Obstet Gynecol Scand. 2012;91:1233–6.CrossRefPubMed Leren V, Langebrekke A, Qvigstad E. Parasitic leiomyomas after laparoscopic surgery with morcellation. Acta Obstet Gynecol Scand. 2012;91:1233–6.CrossRefPubMed
16.
go back to reference Donnez O, Squifflet J, Leconte I, Jadoul P, Donnez J. Posthysterectomy pelvic adenomyotic masses observed in 8 cases out of a series of 1405 laparoscopic subtotal hysterectomies. J Minim Invasive Gynecol. 2007;14:156–60.CrossRefPubMed Donnez O, Squifflet J, Leconte I, Jadoul P, Donnez J. Posthysterectomy pelvic adenomyotic masses observed in 8 cases out of a series of 1405 laparoscopic subtotal hysterectomies. J Minim Invasive Gynecol. 2007;14:156–60.CrossRefPubMed
17.
go back to reference Paul PG, Koshy AK. Multiple peritoneal parasitic myomas after laparoscopic myomectomy and morcellation. Fertil Steril. 2006;85:492–3.CrossRefPubMed Paul PG, Koshy AK. Multiple peritoneal parasitic myomas after laparoscopic myomectomy and morcellation. Fertil Steril. 2006;85:492–3.CrossRefPubMed
18.
go back to reference Van der Meulen JF, Pijnenborg J, Boomsma CM, Verberg M, Geomini P, Bongers MY. Parasitic myoma after laparoscopic morcellation: a systematic review of the literature. BJOG. 2016;123(1):69–75.CrossRefPubMed Van der Meulen JF, Pijnenborg J, Boomsma CM, Verberg M, Geomini P, Bongers MY. Parasitic myoma after laparoscopic morcellation: a systematic review of the literature. BJOG. 2016;123(1):69–75.CrossRefPubMed
19.
go back to reference Takeda A, Mori M, Sakai K, Mitsui T, Nakamura H. Parasitic peritoneal leiomyomatosis diagnosed 6 years after laparoscopic myomectomy with electric tissue morcellation: report of a case and review of the literature. J Minim Invasive Gynecol. 2007;14:770–5.CrossRefPubMed Takeda A, Mori M, Sakai K, Mitsui T, Nakamura H. Parasitic peritoneal leiomyomatosis diagnosed 6 years after laparoscopic myomectomy with electric tissue morcellation: report of a case and review of the literature. J Minim Invasive Gynecol. 2007;14:770–5.CrossRefPubMed
20.
go back to reference Epstein JH, Nejat EJ, Tsai T. Parasitic myomas after laparoscopic myomectomy: case report. Fertil Steril. 2009;91:932. e913-934.CrossRefPubMed Epstein JH, Nejat EJ, Tsai T. Parasitic myomas after laparoscopic myomectomy: case report. Fertil Steril. 2009;91:932. e913-934.CrossRefPubMed
22.
go back to reference Nezhat C, Kho K. Iatrogenic myomas: new class of myomas? J Minim Invasive Gynecol. 2010;17:544–50.CrossRefPubMed Nezhat C, Kho K. Iatrogenic myomas: new class of myomas? J Minim Invasive Gynecol. 2010;17:544–50.CrossRefPubMed
23.
go back to reference Larrain D, Rabischong B, Khoo CK, Botchorishvili R, Canis M, Mage G. “Iatrogenic” parasitic myomas: unusual late complication of laparoscopic morcellation procedures. J Minim Invasive Gynecol. 2010;17:719–24.CrossRefPubMed Larrain D, Rabischong B, Khoo CK, Botchorishvili R, Canis M, Mage G. “Iatrogenic” parasitic myomas: unusual late complication of laparoscopic morcellation procedures. J Minim Invasive Gynecol. 2010;17:719–24.CrossRefPubMed
24.
go back to reference Yang R, Xu T, Fu Y, Cui S, Yang S, Cui M. Leiomyomatosis peritonealis disseminata associated with endometriosis: A case report and review of the literature. Oncol Lett. 2015;9:717–20.PubMed Yang R, Xu T, Fu Y, Cui S, Yang S, Cui M. Leiomyomatosis peritonealis disseminata associated with endometriosis: A case report and review of the literature. Oncol Lett. 2015;9:717–20.PubMed
25.
go back to reference Holloran-Schwartz MB, Fierro M, Tritto A. Delayed presentation of a paracytic myoma fragment after laparoscopic supracervical hysterectomy requiring small bowel resection. A case report. J Reprod Med. 2015;60:75–7.PubMed Holloran-Schwartz MB, Fierro M, Tritto A. Delayed presentation of a paracytic myoma fragment after laparoscopic supracervical hysterectomy requiring small bowel resection. A case report. J Reprod Med. 2015;60:75–7.PubMed
27.
go back to reference Newbold RR, Moore AB, Dixon D. Characterization of uterine leiomyomas in CD-1 mice following developmental exposure to diethylstilbestrol (DES). Toxicol Pathol. 2002;30:611–6.CrossRefPubMed Newbold RR, Moore AB, Dixon D. Characterization of uterine leiomyomas in CD-1 mice following developmental exposure to diethylstilbestrol (DES). Toxicol Pathol. 2002;30:611–6.CrossRefPubMed
28.
go back to reference Kim JJ, Kurita T, Bulun SE. Progesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer. Endocr Rev. 2013;34:130–62.CrossRefPubMedPubMedCentral Kim JJ, Kurita T, Bulun SE. Progesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer. Endocr Rev. 2013;34:130–62.CrossRefPubMedPubMedCentral
29.
go back to reference Donnez J, Tatarchuk TF, Bouchard P, Puscasiu L, Zakharenko NF, Ivanova T, Ugocsai G, Mara M, Jilla MP, Bestel E, et al. Ulipristal acetate versus placebo for fibroid treatment before surgery. N Engl J Med. 2012;366:409–20.CrossRefPubMed Donnez J, Tatarchuk TF, Bouchard P, Puscasiu L, Zakharenko NF, Ivanova T, Ugocsai G, Mara M, Jilla MP, Bestel E, et al. Ulipristal acetate versus placebo for fibroid treatment before surgery. N Engl J Med. 2012;366:409–20.CrossRefPubMed
30.
go back to reference Talaulikar VS, Manyonda IT. Ulipristal acetate: a novel option for the medical management of symptomatic uterine fibroids. Adv Ther. 2012;29:655–63.CrossRefPubMed Talaulikar VS, Manyonda IT. Ulipristal acetate: a novel option for the medical management of symptomatic uterine fibroids. Adv Ther. 2012;29:655–63.CrossRefPubMed
31.
go back to reference Al-Talib A, Tulandi T. Pathophysiology and possible iatrogenic cause of leiomyomatosis peritonealis disseminata. Gynecol Obstet Invest. 2010;69:239–44.CrossRefPubMed Al-Talib A, Tulandi T. Pathophysiology and possible iatrogenic cause of leiomyomatosis peritonealis disseminata. Gynecol Obstet Invest. 2010;69:239–44.CrossRefPubMed
32.
go back to reference Chen YJ, Li HY, Huang CH, Twu NF, Yen MS, Wang PH, Chou TY, Liu YN, Chao KC, Yang MH. Oestrogen-induced epithelial-mesenchymal transition of endometrial epithelial cells contributes to the development of adenomyosis. J Pathol. 2010;222:261–70.CrossRefPubMed Chen YJ, Li HY, Huang CH, Twu NF, Yen MS, Wang PH, Chou TY, Liu YN, Chao KC, Yang MH. Oestrogen-induced epithelial-mesenchymal transition of endometrial epithelial cells contributes to the development of adenomyosis. J Pathol. 2010;222:261–70.CrossRefPubMed
33.
go back to reference Huang TS, Chen YJ, Chou TY, Chen CY, Li HY, Huang BS, Tsai HW, Lan HY, Chang CH, Twu NF, et al. Oestrogen-induced angiogenesis promotes adenomyosis by activating the Slug-VEGF axis in endometrial epithelial cells. J Cell Mol Med. 2014;18:1358–71.CrossRefPubMedPubMedCentral Huang TS, Chen YJ, Chou TY, Chen CY, Li HY, Huang BS, Tsai HW, Lan HY, Chang CH, Twu NF, et al. Oestrogen-induced angiogenesis promotes adenomyosis by activating the Slug-VEGF axis in endometrial epithelial cells. J Cell Mol Med. 2014;18:1358–71.CrossRefPubMedPubMedCentral
34.
go back to reference Carter JJ, Feingold DL, Kirman I, Oh A, Wildbrett P, Asi Z, Fowler R, Huang E, Whelan RL. Laparoscopic-assisted cecectomy is associated with decreased formation of postoperative pulmonary metastases compared with open cecectomy in a murine model. Surgery. 2003;134:432–6.CrossRefPubMed Carter JJ, Feingold DL, Kirman I, Oh A, Wildbrett P, Asi Z, Fowler R, Huang E, Whelan RL. Laparoscopic-assisted cecectomy is associated with decreased formation of postoperative pulmonary metastases compared with open cecectomy in a murine model. Surgery. 2003;134:432–6.CrossRefPubMed
35.
go back to reference Burns KA, Rodriguez KF, Hewitt SC, Janardhan KS, Young SL, Korach KS. Role of estrogen receptor signaling required for endometriosis-like lesion establishment in a mouse model. Endocrinology. 2012;153:3960–71.CrossRefPubMedPubMedCentral Burns KA, Rodriguez KF, Hewitt SC, Janardhan KS, Young SL, Korach KS. Role of estrogen receptor signaling required for endometriosis-like lesion establishment in a mouse model. Endocrinology. 2012;153:3960–71.CrossRefPubMedPubMedCentral
36.
go back to reference Sabnis G, Schayowitz A, Goloubeva O, Macedo L, Brodie A. Trastuzumab reverses letrozole resistance and amplifies the sensitivity of breast cancer cells to estrogen. Cancer Res. 2009;69:1416–28.CrossRefPubMedPubMedCentral Sabnis G, Schayowitz A, Goloubeva O, Macedo L, Brodie A. Trastuzumab reverses letrozole resistance and amplifies the sensitivity of breast cancer cells to estrogen. Cancer Res. 2009;69:1416–28.CrossRefPubMedPubMedCentral
37.
go back to reference Wilkosz S, Pullen N, de-Giorgio-Miller A, Ireland G, Herrick S. Cellular exchange in an endometriosis-adhesion model using GFP transgenic mice. Gynecol Obstet Invest. 2011;72:90–7.CrossRefPubMed Wilkosz S, Pullen N, de-Giorgio-Miller A, Ireland G, Herrick S. Cellular exchange in an endometriosis-adhesion model using GFP transgenic mice. Gynecol Obstet Invest. 2011;72:90–7.CrossRefPubMed
38.
go back to reference Everitt JI, Wolf DC, Howe SR, Goldsworthy TL, Walker C. Rodent model of reproductive tract leiomyomata. Clinical and pathological features. Am J Pathol. 1995;146:1556–67.PubMedPubMedCentral Everitt JI, Wolf DC, Howe SR, Goldsworthy TL, Walker C. Rodent model of reproductive tract leiomyomata. Clinical and pathological features. Am J Pathol. 1995;146:1556–67.PubMedPubMedCentral
39.
go back to reference Howe SR, Gottardis MM, Everitt JI, Goldsworthy TL, Wolf DC, Walker C. Rodent model of reproductive tract leiomyomata. Establishment and characterization of tumor-derived cell lines. Am J Pathol. 1995;146:1568–79.PubMedPubMedCentral Howe SR, Gottardis MM, Everitt JI, Goldsworthy TL, Wolf DC, Walker C. Rodent model of reproductive tract leiomyomata. Establishment and characterization of tumor-derived cell lines. Am J Pathol. 1995;146:1568–79.PubMedPubMedCentral
40.
go back to reference Walker CL, Hunter D, Everitt JI. Uterine leiomyoma in the Eker rat: a unique model for important diseases of women. Genes Chromosomes Cancer. 2003;38:349–56.CrossRefPubMed Walker CL, Hunter D, Everitt JI. Uterine leiomyoma in the Eker rat: a unique model for important diseases of women. Genes Chromosomes Cancer. 2003;38:349–56.CrossRefPubMed
41.
go back to reference Hassan MH, Eyzaguirre E, Arafa HM, Hamada FM, Salama SA, Al-Hendy A. Memy I: a novel murine model for uterine leiomyoma using adenovirus-enhanced human fibroid explants in severe combined immune deficiency mice. Am J Obstet Gynecol. 2008;199:156. e151-158.CrossRefPubMedPubMedCentral Hassan MH, Eyzaguirre E, Arafa HM, Hamada FM, Salama SA, Al-Hendy A. Memy I: a novel murine model for uterine leiomyoma using adenovirus-enhanced human fibroid explants in severe combined immune deficiency mice. Am J Obstet Gynecol. 2008;199:156. e151-158.CrossRefPubMedPubMedCentral
42.
go back to reference Cesen-Cummings K, Houston KD, Copland JA, Moorman VJ, Walker CL, Davis BJ. Uterine leiomyomas express myometrial contractile-associated proteins involved in pregnancy-related hormone signaling. J Soc Gynecol Investig. 2003;10:11–20.CrossRefPubMed Cesen-Cummings K, Houston KD, Copland JA, Moorman VJ, Walker CL, Davis BJ. Uterine leiomyomas express myometrial contractile-associated proteins involved in pregnancy-related hormone signaling. J Soc Gynecol Investig. 2003;10:11–20.CrossRefPubMed
43.
go back to reference Dixon D, He H, Haseman JK. Immunohistochemical localization of growth factors and their receptors in uterine leiomyomas and matched myometrium. Environ Health Perspect. 2000;108 Suppl 5:795–802.CrossRefPubMed Dixon D, He H, Haseman JK. Immunohistochemical localization of growth factors and their receptors in uterine leiomyomas and matched myometrium. Environ Health Perspect. 2000;108 Suppl 5:795–802.CrossRefPubMed
45.
go back to reference Drosch M, Bullerdiek J, Zollner TM, Prinz F, Koch M, Schmidt N. A novel mouse model that closely mimics human uterine leiomyomas. Fertil Steril. 2013;99:927–35. e926.CrossRefPubMed Drosch M, Bullerdiek J, Zollner TM, Prinz F, Koch M, Schmidt N. A novel mouse model that closely mimics human uterine leiomyomas. Fertil Steril. 2013;99:927–35. e926.CrossRefPubMed
46.
go back to reference Holdsworth-Carson SJ, Zaitseva M, Vollenhoven BJ, Rogers PA. Clonality of smooth muscle and fibroblast cell populations isolated from human fibroid and myometrial tissues. Mol Hum Reprod. 2014;20:250–9.CrossRefPubMed Holdsworth-Carson SJ, Zaitseva M, Vollenhoven BJ, Rogers PA. Clonality of smooth muscle and fibroblast cell populations isolated from human fibroid and myometrial tissues. Mol Hum Reprod. 2014;20:250–9.CrossRefPubMed
47.
go back to reference Awwad JT, Sayegh RA, Tao XJ, Hassan T, Awwad ST, Isaacson K. The SCID mouse: an experimental model for endometriosis. Hum Reprod. 1999;14:3107–11.CrossRefPubMed Awwad JT, Sayegh RA, Tao XJ, Hassan T, Awwad ST, Isaacson K. The SCID mouse: an experimental model for endometriosis. Hum Reprod. 1999;14:3107–11.CrossRefPubMed
49.
go back to reference Ono M, Qiang W, Serna VA, Yin P, Coon JS, Navarro A, Monsivais D, Kakinuma T, Dyson M, Druschitz S, et al. Role of stem cells in human uterine leiomyoma growth. PLoS One. 2012;7:e36935.CrossRefPubMedPubMedCentral Ono M, Qiang W, Serna VA, Yin P, Coon JS, Navarro A, Monsivais D, Kakinuma T, Dyson M, Druschitz S, et al. Role of stem cells in human uterine leiomyoma growth. PLoS One. 2012;7:e36935.CrossRefPubMedPubMedCentral
51.
go back to reference Marsh EE, Bulun SE. Steroid hormones and leiomyomas. Obstet Gynecol Clin North Am. 2006;33:59–67.CrossRefPubMed Marsh EE, Bulun SE. Steroid hormones and leiomyomas. Obstet Gynecol Clin North Am. 2006;33:59–67.CrossRefPubMed
52.
go back to reference Takeda A, Imoto S, Mori M, Yamada J, Nakamura H. Rapid growth of parasitic myoma in early pregnancy: previously undescribed manifestation of a rare disorder after laparoscopic-assisted myomectomy. Eur J Obstet Gynecol Reprod Biol. 2012;162:117–8.CrossRefPubMed Takeda A, Imoto S, Mori M, Yamada J, Nakamura H. Rapid growth of parasitic myoma in early pregnancy: previously undescribed manifestation of a rare disorder after laparoscopic-assisted myomectomy. Eur J Obstet Gynecol Reprod Biol. 2012;162:117–8.CrossRefPubMed
53.
go back to reference Banner AS, Carrington CB, Emory WB, Kittle F, Leonard G, Ringus J, Taylor P, Addington WW. Efficacy of oophorectomy in lymphangioleiomyomatosis and benign metastasizing leiomyoma. N Engl J Med. 1981;305:204–9.CrossRefPubMed Banner AS, Carrington CB, Emory WB, Kittle F, Leonard G, Ringus J, Taylor P, Addington WW. Efficacy of oophorectomy in lymphangioleiomyomatosis and benign metastasizing leiomyoma. N Engl J Med. 1981;305:204–9.CrossRefPubMed
54.
go back to reference Abu-Rustum NR, Curtin JP, Burt M, Jones WB. Regression of uterine low-grade smooth-muscle tumors metastatic to the lung after oophorectomy. Obstet Gynecol. 1997;89:850–2.CrossRefPubMed Abu-Rustum NR, Curtin JP, Burt M, Jones WB. Regression of uterine low-grade smooth-muscle tumors metastatic to the lung after oophorectomy. Obstet Gynecol. 1997;89:850–2.CrossRefPubMed
55.
go back to reference Rivera JA, Christopoulos S, Small D, Trifiro M. Hormonal manipulation of benign metastasizing leiomyomas: report of two cases and review of the literature. J Clin Endocrinol Metab. 2004;89:3183–8.CrossRefPubMed Rivera JA, Christopoulos S, Small D, Trifiro M. Hormonal manipulation of benign metastasizing leiomyomas: report of two cases and review of the literature. J Clin Endocrinol Metab. 2004;89:3183–8.CrossRefPubMed
56.
go back to reference Lewis EI, Chason RJ, DeCherney AH, Armstrong A, Elkas J, Venkatesan AM. Novel hormone treatment of benign metastasizing leiomyoma: an analysis of five cases and literature review. Fertil Steril. 2013;99:2017–24.CrossRefPubMedPubMedCentral Lewis EI, Chason RJ, DeCherney AH, Armstrong A, Elkas J, Venkatesan AM. Novel hormone treatment of benign metastasizing leiomyoma: an analysis of five cases and literature review. Fertil Steril. 2013;99:2017–24.CrossRefPubMedPubMedCentral
57.
go back to reference Shakir F, Hill N. A case of multiple morcelloma formation following laparoscopic sub-total hysterectomy. J Obstet Gynaecol. 2012;32:709.CrossRefPubMed Shakir F, Hill N. A case of multiple morcelloma formation following laparoscopic sub-total hysterectomy. J Obstet Gynaecol. 2012;32:709.CrossRefPubMed
58.
go back to reference Vargas MV, Cohen SL, Fuchs-Weizman N, Wang KC, Manoucheri E, Vitonis AF, Einarsson JI. Open power morcellation versus contained power morcellation within an insufflated isolation bag: comparison of perioperative outcomes. J Minim Invasive Gynecol. 2015;22:433–8.CrossRefPubMed Vargas MV, Cohen SL, Fuchs-Weizman N, Wang KC, Manoucheri E, Vitonis AF, Einarsson JI. Open power morcellation versus contained power morcellation within an insufflated isolation bag: comparison of perioperative outcomes. J Minim Invasive Gynecol. 2015;22:433–8.CrossRefPubMed
59.
go back to reference Cohen SL, Einarsson JI, Wang KC, Brown D, Boruta D, Scheib SA, Fader AN, Shibley T. Contained power morcellation within an insufflated isolation bag. Obstet Gynecol. 2014;124:491–7.CrossRefPubMed Cohen SL, Einarsson JI, Wang KC, Brown D, Boruta D, Scheib SA, Fader AN, Shibley T. Contained power morcellation within an insufflated isolation bag. Obstet Gynecol. 2014;124:491–7.CrossRefPubMed
60.
go back to reference Einarsson JI, Cohen SL, Fuchs N, Wang KC. In-Bag Morcellation. J Minim Invasive Gynecol. 2014;21:951–3.CrossRefPubMed Einarsson JI, Cohen SL, Fuchs N, Wang KC. In-Bag Morcellation. J Minim Invasive Gynecol. 2014;21:951–3.CrossRefPubMed
61.
go back to reference Srouji SS, Kaser DJ, Gargiulo AR. Techniques for contained morcellation in gynecologic surgery. Fertil Steril. 2015;103:e34.CrossRefPubMed Srouji SS, Kaser DJ, Gargiulo AR. Techniques for contained morcellation in gynecologic surgery. Fertil Steril. 2015;103:e34.CrossRefPubMed
62.
go back to reference Ghezzi F, Cromi A, Uccella S, Bogani G, Serati M, Bolis P. Transumbilical versus transvaginal retrieval of surgical specimens at laparoscopy: a randomized trial. Am J Obstet Gynecol. 2012;207:112. e111-116.CrossRefPubMed Ghezzi F, Cromi A, Uccella S, Bogani G, Serati M, Bolis P. Transumbilical versus transvaginal retrieval of surgical specimens at laparoscopy: a randomized trial. Am J Obstet Gynecol. 2012;207:112. e111-116.CrossRefPubMed
64.
go back to reference Jacobson GF, Shaber RE, Armstrong MA, Hung YY. Hysterectomy rates for benign indications. Obstet Gynecol. 2006;107:1278–83.CrossRefPubMed Jacobson GF, Shaber RE, Armstrong MA, Hung YY. Hysterectomy rates for benign indications. Obstet Gynecol. 2006;107:1278–83.CrossRefPubMed
65.
go back to reference Arai T, Yasuda Y, Takaya T, Shibayama M. Natural decrease of benign metastasizing leiomyoma. Chest. 2000;117:921–2.CrossRefPubMed Arai T, Yasuda Y, Takaya T, Shibayama M. Natural decrease of benign metastasizing leiomyoma. Chest. 2000;117:921–2.CrossRefPubMed
66.
go back to reference Wentling GK, Sevin BU, Geiger XJ, Bridges MD. Benign metastasizing leiomyoma responsive to megestrol: case report and review of the literature. Int J Gynecol Cancer. 2005;15:1213–7.CrossRefPubMed Wentling GK, Sevin BU, Geiger XJ, Bridges MD. Benign metastasizing leiomyoma responsive to megestrol: case report and review of the literature. Int J Gynecol Cancer. 2005;15:1213–7.CrossRefPubMed
67.
go back to reference Nasu K, Tsuno A, Takai N, Narahara H. A case of benign metastasizing leiomyoma treated by surgical castration followed by an aromatase inhibitor, anastrozole. Arch Gynecol Obstet. 2009;279:255–7.CrossRefPubMed Nasu K, Tsuno A, Takai N, Narahara H. A case of benign metastasizing leiomyoma treated by surgical castration followed by an aromatase inhibitor, anastrozole. Arch Gynecol Obstet. 2009;279:255–7.CrossRefPubMed
68.
go back to reference Egberts JH, Schafmayer C, Bauerschlag DO, Janig U, Tepel J. Benign abdominal and pulmonary metastasizing leiomyoma of the uterus. Arch Gynecol Obstet. 2006;274:319–22.CrossRefPubMed Egberts JH, Schafmayer C, Bauerschlag DO, Janig U, Tepel J. Benign abdominal and pulmonary metastasizing leiomyoma of the uterus. Arch Gynecol Obstet. 2006;274:319–22.CrossRefPubMed
69.
go back to reference Song H, Lu D, Navaratnam K, Shi G. Aromatase inhibitors for uterine fibroids. Cochrane Database Syst Rev. 2013;10:CD009505.PubMed Song H, Lu D, Navaratnam K, Shi G. Aromatase inhibitors for uterine fibroids. Cochrane Database Syst Rev. 2013;10:CD009505.PubMed
70.
go back to reference Sweet S, Legro RS, Coney P. A comparison of methods and results in recruiting white and black women into reproductive studies: the MMC-PSU cooperative center on reproduction experience. Contemp Clin Trials. 2008;29:478–81.CrossRefPubMed Sweet S, Legro RS, Coney P. A comparison of methods and results in recruiting white and black women into reproductive studies: the MMC-PSU cooperative center on reproduction experience. Contemp Clin Trials. 2008;29:478–81.CrossRefPubMed
71.
go back to reference Wang PH, Lee WL, Cheng MH, Yen MS, Chao KC, Chao HT. Use of a gonadotropin-releasing hormone agonist to manage perimenopausal women with symptomatic uterine myomas. Taiwan J Obstet Gynecol. 2009;48:133–7.CrossRefPubMed Wang PH, Lee WL, Cheng MH, Yen MS, Chao KC, Chao HT. Use of a gonadotropin-releasing hormone agonist to manage perimenopausal women with symptomatic uterine myomas. Taiwan J Obstet Gynecol. 2009;48:133–7.CrossRefPubMed
72.
go back to reference Parsanezhad ME, Azmoon M, Alborzi S, Rajaeefard A, Zarei A, Kazerooni T, Frank V, Schmidt EH. A randomized, controlled clinical trial comparing the effects of aromatase inhibitor (letrozole) and gonadotropin-releasing hormone agonist (triptorelin) on uterine leiomyoma volume and hormonal status. Fertil Steril. 2010;93:192–8.CrossRefPubMed Parsanezhad ME, Azmoon M, Alborzi S, Rajaeefard A, Zarei A, Kazerooni T, Frank V, Schmidt EH. A randomized, controlled clinical trial comparing the effects of aromatase inhibitor (letrozole) and gonadotropin-releasing hormone agonist (triptorelin) on uterine leiomyoma volume and hormonal status. Fertil Steril. 2010;93:192–8.CrossRefPubMed
73.
go back to reference Matta WH, Shaw RW, Hesp R, Evans R. Reversible trabecular bone density loss following induced hypo-oestrogenism with the GnRH analogue buserelin in premenopausal women. Clin Endocrinol (Oxf). 1988;29:45–51.CrossRef Matta WH, Shaw RW, Hesp R, Evans R. Reversible trabecular bone density loss following induced hypo-oestrogenism with the GnRH analogue buserelin in premenopausal women. Clin Endocrinol (Oxf). 1988;29:45–51.CrossRef
74.
go back to reference Jirecek S, Lee A, Pavo I, Crans G, Eppel W, Wenzl R. Raloxifene prevents the growth of uterine leiomyomas in premenopausal women. Fertil Steril. 2004;81:132–6.CrossRefPubMed Jirecek S, Lee A, Pavo I, Crans G, Eppel W, Wenzl R. Raloxifene prevents the growth of uterine leiomyomas in premenopausal women. Fertil Steril. 2004;81:132–6.CrossRefPubMed
75.
go back to reference Deng L, Wu T, Chen XY, Xie L, Yang J. Selective estrogen receptor modulators (SERMs) for uterine leiomyomas. Cochrane Database Syst Rev. 2012;10:CD005287.PubMed Deng L, Wu T, Chen XY, Xie L, Yang J. Selective estrogen receptor modulators (SERMs) for uterine leiomyomas. Cochrane Database Syst Rev. 2012;10:CD005287.PubMed
76.
go back to reference Mehine M, Makinen N, Heinonen HR, Aaltonen LA, Vahteristo P. Genomics of uterine leiomyomas: insights from high-throughput sequencing. Fertil Steril. 2014;102:621–9.CrossRefPubMed Mehine M, Makinen N, Heinonen HR, Aaltonen LA, Vahteristo P. Genomics of uterine leiomyomas: insights from high-throughput sequencing. Fertil Steril. 2014;102:621–9.CrossRefPubMed
Metadata
Title
Oestrogen-induced angiogenesis and implantation contribute to the development of parasitic myomas after laparoscopic morcellation
Authors
Ben-Shian Huang
Muh-Hwa Yang
Peng-Hui Wang
Hsin-Yang Li
Teh-Ying Chou
Yi-Jen Chen
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2016
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-016-0200-y

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