Pathogenesis and malignant transformation of adenomyosis (Review)
- Authors:
- Natsuki Koike
- Taihei Tsunemi
- Chiharu Uekuri
- Juria Akasaka
- Fuminori Ito
- Aiko Shigemitsu
- Hiroshi Kobayashi
-
Affiliations: Department of Obstetrics and Gynecology, Nara Medical University, Kashihara, Nara 634-8522, Japan - Published online on: December 13, 2012 https://doi.org/10.3892/or.2012.2184
- Pages: 861-867
This article is mentioned in:
Abstract
Ferenczy A: Pathophysiology of adenomyosis. Hum Reprod Update. 4:312–322. 1998. View Article : Google Scholar | |
Templeman C, Marshall SF, Ursin G, Horn-Ross PL, Clarke CA, Allen M, Deapen D, Ziogas A, Reynolds P, Cress R, Anton-Culver H, West D, Ross RK and Bernstein L: Adenomyosis and endometriosis in the California Teachers Study. Fertil Steril. 90:415–424. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lalović N, Cvijanović R, Vladicić ND, Marić R, Jokanović D and Skipina DB: Adenomyomatosis of the gallbladder - case report. Med Pregl. 64:323–326. 2011. | |
Kayahara M, Ohta T, Kitagawa H, Miwa K, Urabe T and Murata T: Adenomyomatosis of the papilla of Vater: a case illustrating diagnostic difficulties. Dig Surg. 18:139–142. 2001. View Article : Google Scholar : PubMed/NCBI | |
Matsumoto T and Shimada K: A case of gallbladder cancer arising from the Rokitansky-Aschoff sinus. Jpn J Clin Oncol. 39:7762009. View Article : Google Scholar : PubMed/NCBI | |
Krutsay M: Adenomyosis of the common bile duct. Magy Onkol. 54:179–180. 2010.(In Hungarian). | |
Benagiano G, Brosens I and Carrara S: Adenomyosis: new knowledge is generating new treatment strategies. Womens Health. 5:297–311. 2009.PubMed/NCBI | |
Parrott E, Butterworth M, Green A, White IN and Greaves P: Adenomyosis - a result of disordered stromal differentiation. Am J Pathol. 159:623–630. 2001. View Article : Google Scholar : PubMed/NCBI | |
Mori T, Ohta Y and Nagasawa H: Ultrastructural changes in uterine myometrium of mice with experimentally-induced adenomyosis. Experientia. 40:1385–1387. 1984. View Article : Google Scholar : PubMed/NCBI | |
Hever A, Roth RB, Hevezi PA, Lee J, Willhite D, White EC, Marin EM, Herrera R, Acosta HM, Acosta AJ and Zlotnik A: Molecular characterization of human adenomyosis. Mol Hum Reprod. 12:737–748. 2006. View Article : Google Scholar | |
Barcena de Arellano ML, Gericke J, Reichelt U, Okuducu AF, Ebert AD, Chiantera V, Schneider A and Mechsner S: Immunohistochemical characterization of endometriosis-associated smooth muscle cells in human peritoneal endometriotic lesions. Hum Reprod. 26:2721–2730. 2011. | |
Mechsner S, Grum B, Gericke C, Loddenkemper C, Dudenhausen JW and Ebert AD: Possible roles of oxytocin receptor and vasopressin-1α receptor in the pathomechanism of dysperistalsis and dysmenorrhea in patients with adenomyosis uteri. Fertil Steril. 94:2541–2546. 2010. | |
Mehasseb MK, Bell SC, Brown L, Pringle JH and Habiba M: Phenotypic characterisation of the inner and outer myometrium in normal and adenomyotic uteri. Gynecol Obstet Invest. 71:217–224. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mehasseb MK, Panchal R, Taylor AH, Brown L, Bell SC and Habiba M: Estrogen and progesterone receptor isoform distribution through the menstrual cycle in uteri with and without adenomyosis. Fertil Steril. 95:2228–2235. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jaffer S, Shynlova O and Lye S: Mammalian target of rapamycin is activated in association with myometrial proliferation during pregnancy. Endocrinology. 150:4672–4680. 2009. View Article : Google Scholar : PubMed/NCBI | |
Shynlova O, Kwong R and Lye SJ: Mechanical stretch regulates hypertrophic phenotype of the myometrium during pregnancy. Reproduction. 139:247–253. 2010. View Article : Google Scholar : PubMed/NCBI | |
Treloar SA, Bell TA, Nagle CM, Purdie DM and Green AC: Early menstrual characteristics associated with subsequent diagnosis of endometriosis. Am J Obstet Gynecol. 202:534.e1–6. 2010.PubMed/NCBI | |
Mechsner S, Bartley J, Infanger M, Loddenkemper C, Herbel J and Ebert AD: Clinical management and immunohistochemical analysis of umbilical endometriosis. Arch Gynecol Obstet. 280:235–242. 2009. View Article : Google Scholar : PubMed/NCBI | |
van Kaam KJ, Schouten JP, Nap AW, Dunselman G and Groothuis PG: Fibromuscular differentiation in deeply infiltrating endometriosis is a reaction of resident fibroblasts to the presence of ectopic endometrium. Hum Reprod. 23:2692–2700. 2008.PubMed/NCBI | |
Leyendecker G, Wildt L and Mall G: The pathophysiology of endometriosis and adenomyosis: tissue injury and repair. Arch Gynecol Obstet. 280:529–538. 2009. View Article : Google Scholar : PubMed/NCBI | |
Walter I, Handler J, Reifinger M and Aurich C: Association of endometriosis in horses with differentiation of periglandular myofibroblasts and changes of extracellular matrix proteins. Reproduction. 121:581–586. 2001. View Article : Google Scholar : PubMed/NCBI | |
Chen YJ, Li HY, Huang CH, Twu NF, Yen MS, Wang PH, Chou TY, Liu YN, Chao KC and Yang MH: Oestrogen-induced epithelial-mesenchymal transition of endometrial epithelial cells contributes to the development of adenomyosis. J Pathol. 222:261–270. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhou S, Yi T, Liu R, Bian C, Qi X, He X, Wang K, Li J, Zhao X, Huang C and Wei Y: Proteomics identification of annexin A2 as a key mediator in the metastasis and proangiogenesis of endometrial cells in human adenomyosis. Mol Cell Proteomics. 11:M112.0179882012. View Article : Google Scholar : PubMed/NCBI | |
Greaves P and White IN: Experimental adenomyosis. Best Pract Res Clin Obstet Gynaecol. 20:503–510. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kang S, Li SZ, Wang N, Zhou RM, Wang T, Wang DJ, Li XF, Bui J and Li Y: Association between genetic polymorphisms in fibroblast growth factor (FGF)1 and FGF2 and risk of endometriosis and adenomyosis in Chinese women. Hum Reprod. 25:1806–1811. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hinoki A, Kimura K, Higuchi S, Eguchi K, Takaguri A, Ishimaru K, Frank GD, Gerthoffer WT, Sommerville LJ, Autieri MV and Eguchi S: p21-activated kinase 1 participates in vascular remodeling in vitro and in vivo. Hypertension. 55:161–165. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kim SR, Kim SH, Lee HW, Chae HD, Kim CH and Kang BM: Increased expression of p21-activated kinase in adenomyosis. Fertil Steril. 94:1125–1128. 2010. View Article : Google Scholar : PubMed/NCBI | |
Meenakshi M and McCluggage WG: Vascular involvement in adenomyosis: report of a large series of a common phenomenon with observations on the pathogenesis of adenomyosis. Int J Gynecol Pathol. 29:117–121. 2010. View Article : Google Scholar : PubMed/NCBI | |
Sieiński W: Tumor-like intravascular proliferations of the stroma in adenomyosis. Patol Pol. 44:1–4. 1993.PubMed/NCBI | |
Mori A, Zhai YL, Toki T, Nikaido T and Fujii S: Distribution and heterogeneity of mast cells in the human uterus. Hum Reprod. 12:368–372. 1997. View Article : Google Scholar : PubMed/NCBI | |
Menzies FM, Shepherd MC, Nibbs RJ and Nelson SM: The role of mast cells and their mediators in reproduction, pregnancy and labour. Hum Reprod Update. 17:383–396. 2011. View Article : Google Scholar : PubMed/NCBI | |
Anaf V, Chapron C, El Nakadi I, De Moor V, Simonart T and Noël JC: Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis. Fertil Steril. 86:1336–1343. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kusakabe KT, Abe H, Kondo T, Kato K, Okada T and Otsuki Y: DNA microarray analysis in a mouse model for endometriosis and validation of candidate factors with human adenomyosis. J Reprod Immunol. 85:149–160. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wang F, Wen Z, Li H, Yang Z, Zhao X and Yao X: Human leukocyte antigen-G is expressed by the eutopic and ectopic endometrium of adenomyosis. Fertil Steril. 90:1599–1604. 2008. View Article : Google Scholar : PubMed/NCBI | |
Choi KC, Leung PC and Jeung EB: Biology and physiology of Calbindin-D9k in female reproductive tissues: involvement of steroids and endocrine disruptors. Reprod Biol Endocrinol. 3:662005. View Article : Google Scholar : PubMed/NCBI | |
Wang F, Li H, Yang Z, Du X, Cui M and Wen Z: Expression of interleukin-10 in patients with adenomyosis. Fertil Steril. 91:1681–1685. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kang S, Zhao X, Xing H, Wang N, Zhou R, Chen S, Li W, Zhao J, Duan Y, Sun D and Li Y: Polymorphisms in the matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-2 and the risk of human adenomyosis. Environ Mol Mutagen. 49:226–231. 2008. View Article : Google Scholar : PubMed/NCBI | |
Chen YJ, Li HY, Chang YL, Yuan CC, Tai LK, Lu KH, Chang CM and Chiou SH: Suppression of migratory/invasive ability and induction of apoptosis in adenomyosis-derived mesenchymal stem cells by cyclooxygenase-2 inhibitors. Fertil Steril. 94:1972–1979. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kang R, Zeh HJ, Lotze MT and Tang D: The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18:571–580. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ren Y, Mu L, Ding X and Zheng W: Decreased expression of Beclin 1 in eutopic endometrium of women with adenomyosis. Arch Gynecol Obstet. 282:401–406. 2010. View Article : Google Scholar : PubMed/NCBI | |
Liu X, Nie J and Guo SW: Elevated immunoreactivity against class I histone deacetylases in adenomyosis. Gynecol Obstet Invest. 74:50–55. 2012. View Article : Google Scholar : PubMed/NCBI | |
Suire RA, Goodman DG, Valerio MG, Fredrickson TN, Strandberg JD, Levitt MH, Lingeman CH, Harshbarger JC and Dawe CJ: Female reproductive system. Pathology of Laboratory Animals. 2. Benirschke K, Garner FM and Jones TC: Springer-Verlag; New York, NY: pp. 1051–1262. 1978 | |
Oehler MK, Greschik H, Fischer DC, Tong X, Schuele R and Kieback DG: Functional characterization of somatic point mutations of the human estrogen receptor alpha (hERalpha) in adenomyosis uteri. Mol Hum Reprod. 10:853–860. 2004. View Article : Google Scholar : PubMed/NCBI | |
Mehasseb MK, Bell SC and Habiba MA: The effects of tamoxifen and estradiol on myometrial differentiation and organization during early uterine development in the CD1 mouse. Reproduction. 138:341–350. 2009. View Article : Google Scholar : PubMed/NCBI | |
Green AR, Styles JA, Parrott EL, Gray D, Edwards RE, Smith AG, Gant TW, Greaves P, Al-Azzawi F and White IN: Neonatal tamoxifen treatment of mice leads to adenomyosis but not uterine cancer. Exp Toxicol Pathol. 56:255–263. 2005. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Zhang SF, Zou SE, Xia X and Bao L: Accumulation of nerve growth factor and its receptors in the uterus and dorsal root ganglia in a mouse model of adenomyosis. Reprod Biol Endocrinol. 9:302011. View Article : Google Scholar : PubMed/NCBI | |
Sampson JA: Endometrial carcinoma of the ovary arising in endometrial tissue of that organ. Arch Surg. 10:1–72. 1925. View Article : Google Scholar | |
Motohara K, Tashiro H, Ohtake H, Saito F, Ohba T and Katabuchi H: Endometrioid adenocarcinoma arising in adenomyosis: elucidation by periodic magnetic resonance imaging evaluations. Int J Clin Oncol. 13:266–270. 2008. View Article : Google Scholar | |
Kumar D and Anderson W: Malignancy in endometriosis interna. J Obstet Gynaecol Br Emp. 65:435–437. 1958. View Article : Google Scholar : PubMed/NCBI | |
Colman HI and Rosenthal AH: Carcinoma developing in areas of adenomyosis. Obset Gynecol. 14:342–348. 1959.PubMed/NCBI | |
Ismiil ND, Rasty G, Ghorab Z, Nofech-Mozes S, Bernardini M, Thomas G, Ackerman I, Covens A and Khalifa MA: Adenomyosis is associated with myometrial invasion by FIGO 1 endometrial adenocarcinoma. Int J Gynecol Pathol. 26:278–283. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kucera E, Hejda V, Dankovcik R, Valha P, Dudas M and Feyereisl J: Malignant changes in adenomyosis in patients with endometrioid adenocarcinoma. Eur J Gynaecol Oncol. 32:182–184. 2011.PubMed/NCBI | |
Hernandez E and Woodruff JD: Endometrial adenocarcinoma arising in adenomyosis. Am J Obstet Gynecol. 138:827–832. 1980.PubMed/NCBI | |
Kazandi M, Zeybek B, Terek MC, Zekioglu O, Ozdemir N and Oztekin K: Grade 2 endometrioid adenocarcinoma arising from adenomyosis of the uterus: report of a case. Eur J Gynaecol Oncol. 31:719–721. 2010.PubMed/NCBI | |
Rolly F: Über einen Fall von Adenomyoma Uteri, Übergang in Karzinom und Metastasenbildung. Virchows Arch. 150:5551897.(In German). | |
Abushahin N, Zhang T, Chiang S, Zhang X, Hatch K and Zheng W: Serous endometrial intraepithelial carcinoma arising in adenomyosis: a report of 5 cases. Int J Gynecol Pathol. 30:271–281. 2011. View Article : Google Scholar : PubMed/NCBI | |
Puppa G, Shozu M, Perin T, Nomura K, Gloghini A, Campagnutta E and Canzonieri V: Small primary adenocarcinoma in adenomyosis with nodal metastasis: a case report. BMC Cancer. 7:1032007. View Article : Google Scholar : PubMed/NCBI | |
Takeuchi K, Yamanaka Y, Hamana S, Ohara N and Maruo T: Invasive adenocarcinoma arising from uterine adenomyosis involving the rectosigmoid colon. Int J Gynecol Cancer. 14:1004–1006. 2004. View Article : Google Scholar : PubMed/NCBI | |
Izadi-Mood N, Samadi N, Sarmadi S and Eftekhar Z: Papillary serous carcinoma arising from adenomyosis presenting as intramural leiomyoma. Arch Iran Med. 10:2582–2560. 2007.PubMed/NCBI | |
Hirabayashi K, Yasuda M, Kajiwara H, Nakamura N, Sato S, Nishijima Y, Mikami M and Osamura RY: Clear cell adenocarcinoma arising from adenomyosis. Int J Gynecol Pathol. 28:262–266. 2009. View Article : Google Scholar : PubMed/NCBI | |
Jha P, Ansari C, Coakley FV, Wang ZJ, Yeh BM, Rabban J and Poder L: Case report: imaging of Mullerian adenosarcoma arising in adenomyosis. Clin Radiol. 64:645–648. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ohta Y, Hamatani S, Suzuki T, Ikeda K, Kiyokawa K, Shiokawa A, Kushima M and Ota H: Clear cell adenocarcinoma arising from a giant cystic adenomyosis: a case report with immunohistochemical analysis of laminin-5 gamma2 chain and p53 overexpression. Pathol Res Pract. 204:677–682. 2008. View Article : Google Scholar : PubMed/NCBI | |
Couto D, Mota F, Silva T and de Oliveira C: Adenocarcinoma arising in adenomyosis: report of an unusual case. Acta Obstet Gynecol Scand. 83:406–408. 2004. View Article : Google Scholar : PubMed/NCBI | |
Woodruff JD, Erozan YS and Genadry R: Adenocarcinoma arising in adenomyosis detected by atypical cytology. Obstet Gynecol. 67:145–148. 1986.PubMed/NCBI | |
Koshiyama M, Suzuki A, Ozawa M, Fujita K, Sakakibara A, Kawamura M, Takahashi S, Fujii H, Hirano T, Okagaki A, Nagano T and Ban C: Adenocarcinomas arising from uterine adenomyosis: a report of four cases. Int J Gynecol Pathol. 21:2392–2345. 2002. View Article : Google Scholar | |
Kuwashima Y, Uehara T, Kishi K, Tajima H, Shiromizu K, Matsuzawa M and Takayama S: Intramural adenocarcinoma of the uterus, arisen from adenomyosis uteri, showing unique histologic appearances. Report of two cases. Eur J Gynaecol Oncol. 15:418–423. 1994. | |
Rubod C, Narducci F, Delattre C, Decocq J, Verbert A and Delahousse G: Endometrioid adenocarcinoma arising from adenomyosis. A case report and literature review. J Gynecol Obstet Biol Reprod. 33:140–144. 2004.PubMed/NCBI | |
Takai N, Akizuki S, Nasu K, Etoh Y and Miyakawa I: Endometrioid adenocarcinoma arising from adenomyosis. Gynecol Obstet Invest. 48:141–144. 1999. View Article : Google Scholar | |
Heo SH, Lee KH, Kim JW and Jeong YY: Unusual manifestation of endometrioid adenocarcinoma arising from subserosal cystic adenomyosis of the uterus: emphasis on MRI and positron emission tomography CT findings. Br J Radiol. 84:e210–212. 2011. | |
Boes AS, Tousseyn T, Vandenput I, Timmerman D, Vergote I, Moerman P and Amant F: Pitfall in the diagnosis of endometrial cancer: case report of an endometrioid adenocarcinoma arising from uterine adenomyosis. Eur J Gynaecol Oncol. 32:431–434. 2011.PubMed/NCBI | |
Goumenou AG, Arvanitis DA, Matalliotakis IM, Koumantakis EE and Spandidos DA: Loss of heterozygosity in adenomyosis on hMSH2, hMLH1, p16Ink4 and GALT loci. Int J Mol Med. 6:667–671. 2000.PubMed/NCBI | |
Jones RK, Searle RF and Bulmer JN: Apoptosis and bcl-2 expression in normal human endometrium, endometriosis and adenomyosis. Hum Reprod. 13:3496–3502. 1998. View Article : Google Scholar : PubMed/NCBI | |
Nie Jichan, Liu Xishi and Guo SW: Promoter hypermethylation of progesterone receptor isoform B (PR-B) in adenomyosis and its rectification by a histone deacetylase inhibitor and a demethylation agent. Reprod Sci. 17:995–1005. 2010. View Article : Google Scholar : PubMed/NCBI |