Adenomyosis: A Clinical Review of a Challenging Gynecologic Condition

Journal of Minimally Invasive Gynecology

Volumn 23, Issue 2, 2016, Pages 164-185

  Struble, Jennifer ^a   Reid, Shannon ^b   Bedaiwy, Mohamed A ^b  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adenomyosis; Imaging diagnostic criteria

Indexed keywords

AROMATASE INHIBITOR; BUSERELIN ACETATE; DANAZOL; GESTAGEN; GONADORELIN AGONIST; HORMONE; LEVONORGESTREL; NONSTEROID ANTIINFLAMMATORY AGENT; ORAL CONTRACEPTIVE AGENT; PLACEBO;

ADENOMYOSIS; CLINICAL FEATURE; DIFFERENTIAL DIAGNOSIS; DISEASE SEVERITY; DYSMENORRHEA; ELECTROCOAGULATION; ENDOMETRIOSIS; ENDOMETRIUM BIOPSY; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HYSTERECTOMY; HYSTEROSCOPY; INVAGINATION; LAPAROSCOPY; LEVONORGESTREL RELEASING INTRAUTERINE SYSTEM; LYMPH VESSEL; MENORRHAGIA; MUELLERIAN DUCT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; REVIEW; RISK FACTOR; UTERINE ARTERY EMBOLIZATION; BIOPSY; COMPLICATION; PATHOLOGY; SENSITIVITY AND SPECIFICITY; VAGINA;

ADENOMYOSIS; BIOPSY; DIAGNOSIS, DIFFERENTIAL; DYSMENORRHEA; FEMALE; HUMANS; HYSTERECTOMY; LAPAROSCOPY; MAGNETIC RESONANCE IMAGING; MENORRHAGIA; RISK FACTORS; SENSITIVITY AND SPECIFICITY; VAGINA;

EID: 84958181950     PISSN: 15534650     EISSN: 15534669     Source Type: Journal    
DOI: 10.1016/j.jmig.2015.09.018     Document Type: Review

References (106)

1. Garcia L., Isaacson K. Adenomyosis: review of the literature. J Minim Invasive Gynecol 2011, 18:428-437.
2. Benson R.C., Sneeden V.D. Adenomyosis: a reappraisal of symptomatology. Am J Obstet Gynecol 1958, 76:1044-1057. discussion 1057-1061.
3. Emge L.A. The elusive adenomyosis of the uterus. Its historical past and its present state of recognition. Am J Obstet Gynecol 1962, 83:1541-1563.
4. Levgur M., Abadi M.A., Tucker A. Adenomyosis: symptoms, histology, and pregnancy terminations. Obstet Gynecol 2000, 95:688-691.
5. Ryan G.L., Stolpen A., Van Voorhis B.J. An unusual cause of adolescent dysmenorrhea. Obstet Gynecol 2006, 108:1017-1022.
6. Farquhar C., Brosens I. Medical and surgical management of adenomyosis. Best Pract Res Clin Obstet Gynaecol 2006, 20:603-616.
7. Bergholt T., Eriksen L., Berendt N., Jacobsen M., Hertz J.B. Prevalence and risk factors of adenomyosis at hysterectomy. Hum Reprod 2001, 16:2418-2421.
8. Parazzini F., Vercellini P., Panazza S., Chatenoud L., Oldani S., Crosignani P.G. Risk factors for adenomyosis. Hum Reprod 1997, 12:1275-1279.
9. Vercellini P., Parazzini F., Oldani S., Panazza S., Bramante T., Crosignani P.G. Adenomyosis at hysterectomy: a study on frequency distribution and patient characteristics. Hum Reprod 1995, 10:1160-1162.
10. Slezak P., Tillinger K.G. The incidence and clinical importance of hysterographic evidence of cavities in the uterine wall. Radiology 1976, 118:581-586.
11. Takeda A., Sakai K., Mitsui T., Nakamura H. Laparoscopic management of juvenile cystic adenomyoma of the uterus: report of two cases and review of the literature. J Minim Invasive Gynecol 2007, 14:370-374.
12. Dogan E., Gode F., Saatli B., Secil M. Juvenile cystic adenomyosis mimicking uterine malformation: a case report. Arch Gynecol Obstet 2008, 278:593-595.
13. Kriplani A., Mahey R., Agarwal N., Bhatla N., Yadav R., Singh M.K. Laparoscopic management of juvenile cystic adenomyoma: four cases. J Minim Invasive Gynecol 2011, 18:343-348.
14. Taran F.A., Weaver A.L., Coddington C.C., Stewart E.A. Understanding adenomyosis: a case control study. Fertil Steril 2010, 94:1223-1228.
15. Templeman C., Marshall S.F., Ursin G., et al. Adenomyosis and endometriosis in the California Teachers Study. Fertil Steril 2008, 90:415-424.
16. Cohen I., Beyth Y., Tepper R., et al. Adenomyosis in postmenopausal breast cancer patients treated with tamoxifen: a new entity?. Gynecol Oncol 1995, 58:86-91.
17. Cohen I., Beyth Y., Shapira J., et al. High frequency of adenomyosis in postmenopausal breast cancer patients treated with tamoxifen. Gynecol Obstet Invest 1997, 44:200-205.
18. Zhou B., Yang L., Sun Q., et al. Cigarette smoking and the risk of endometrial cancer: a meta-analysis. Am J Med 2008, 121:501-508.e3.
19. Viswanathan A.N., Feskanich D., De Vivo I., et al. Smoking and the risk of endometrial cancer: results from the Nurses' Health Study. Int J Cancer 2005, 114:996-1001.
20. Green A.R., Styles J.A., Parrott E.L., et al. Neonatal tamoxifen treatment of mice leads to adenomyosis but not uterine cancer. Exp Toxicol Pathol 2005, 56:255-263.
21. Riggs J.C., Lim E.K., Liang D., Bullwinkel R. Cesarean section as a risk factor for the development of adenomyosis uteri. J Reprod Med 2014, 59:20-24.
22. Ferenczy A. Pathophysiology of adenomyosis. Hum Reprod Update 1998, 4:312-322.
23. Ostrzenski A. Extensive iatrogenic adenomyosis after laparoscopic myomectomy. Fertil Steril 1998, 69:143-145.
24. Ota H., Igarashi S., Hatazawa J., Tanaka T. Is adenomyosis an immune disease?. Hum Reprod Update 1998, 4:360-367.
25. Bergeron C., Amant F., Ferenczy A. Pathology and physiopathology of adenomyosis. Best Pract Res Clin Obstet Gynaecol 2006, 20:511-521.
26. Ficicioglu C., Tekin H.I., Arioglu P.F., Okar I. A murine model of adenomyosis: the effects of hyperprolactinemia induced by fluoxetine hydrochloride, a selective serotonin reuptake inhibitor, on adenomyosis induction in Wistar albino rats. Acta Eur Fertil 1995, 26:75-79.
27. Mori T., Singtripop T., Kawashima S. Animal model of uterine adenomyosis: is prolactin a potent inducer of adenomyosis in mice?. Am J Obstet Gynecol 1991, 165:232-234.
28. Danilovich N., Roy I., Sairam M.R. Emergence of uterine pathology during accelerated biological aging in FSH receptor-haploinsufficient mice. Endocrinology 2002, 143:3618-3627.
29. Campo S., Campo V., Benagiano G. Response: adenomyosis and infertility. Reprod Biomed Online 2012, 24:587.
30. Bedaiwy M.A., Dahoud W., Skomorovska-Prokvolit Y., Liu J.H., Falcone T., Mesiano S. Expression of progesterone receptor isoforms-and-in adenomyosis. Fertil Steril 2013, 100(Suppl 1):S387.
31. Enatsu A., Harada T., Yoshida S., Iwabe T., Terakawa N. Adenomyosis in a patient with the Rokitansky-Kuster-Hauser syndrome. Fertil Steril 2000, 73:862-863.
32. Campo S., Campo V., Benagiano G. Adenomyosis and infertility. Reprod Biomed Online 2012, 24:35-46.
33. Matsumoto Y., Iwasaka T., Yamasaki F., Sugimori H. Apoptosis and Ki-67 expression in adenomyotic lesions and in the corresponding eutopic endometrium. Obstet Gynecol 1999, 94:71-77.
34. Propst A.M., Quade B.J., Gargiulo A.R., Nowak R.A., Stewart E.A. Adenomyosis demonstrates increased expression of the basic fibroblast growth factor receptor/ligand system compared with autologous endometrium. Menopause 2001, 8:368-371.
35. Sasson I.E., Taylor H.S. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci 2008, 1127:106-115.
36. Du H., Taylor H.S. Stem cells and female reproduction. Reprod Sci 2009, 16:126-139.
37. Sahin A.A., Silva E.G., Landon G., Ordonez N.G., Gershenson D.M. Endometrial tissue in myometrial vessels not associated with menstruation. Int J Gynecol Pathol 1989, 8:139-146.
38. Huang F.J., Kung F.T., Chang S.Y., Hsu T.Y. Effects of short-course buserelin therapy on adenomyosis: a report of two cases. J Reprod Med Obstet Gynecol 1999, 44:741-744.
39. Shrestha A., Sedai L.B. Understanding clinical features of adenomyosis: a case control study. Nepal Med Coll J 2012, 14:176-179.
40. Ozdegirmenci O., Kayikcioglu F., Akgul M.A., et al. Comparison of levonorgestrel intrauterine system versus hysterectomy on efficacy and quality of life in patients with adenomyosis. Fertil Steril 2011, 95:497-502.
41. McElin T.W., Bird C.C. Adenomyosis of the uterus. Obstet Gynecol Annu 1974, 3:425-441.
42. Molinas C.R., Campo R. Office hysteroscopy and adenomyosis. Best Pract Res Clin Obstet Gynaecol 2006, 20:557-567.
43. Bragheto A.M., Caserta N., Bahamondes L., Petta C.A. Effectiveness of the levonorgestrel-releasing intrauterine system in the treatment of adenomyosis diagnosed and monitored by magnetic resonance imaging. Contraception 2007, 76:195-199.
44. Azziz R. Adenomyosis: current perspectives. Obstet Gynecol Clin North Am 1989, 16:221-235.
45. Koike H., Egawa H., Ohtsuka T., Yamaguchi M., Ikenoue T., Mori N. Correlation between dysmenorrheic severity and prostaglandin production in women with endometriosis. Prostaglandins Leukot Essent Fatty Acids 1992, 46:133-137.
46. McCausland A.M. Hysteroscopic myometrial biopsy: its use in diagnosing adenomyosis and its clinical application. Am J Obstet Gynecol 1992, 166:1619-1626. discussion 1626-1628.
47. Sammour A., Pirwany I., Usubutun A., Arseneau J., Tulandi T. Correlations between extent and spread of adenomyosis and clinical symptoms. Gynecol Obstet Invest 2002, 54:213-216.
48. Parker J.D., Leondires M., Sinaii N., Premkumar A., Nieman L.K., Stratton P. Persistence of dysmenorrhea and nonmenstrual pain after optimal endometriosis surgery may indicate adenomyosis. Fertil Steril 2006, 86:711-715.
49. Levgur M. Diagnosis of adenomyosis: a review. J Reprod Med 2007, 52:177-193.
50. Uduwela A.S., Perera M.A., Aiqing L., Fraser I.S. Endometrial-myometrial interface: relationship to adenomyosis and changes in pregnancy. Obstet Gynecol Surv 2000, 55:390-400.
51. Fernandez C., Ricci P., Fernandez E. Adenomyosis visualized during hysteroscopy. J Minim Invasive Gynecol 2007, 14:555-556.
52. Popp L.W., Schwiedessen J.P., Gaetje R. Myometrial biopsy in the diagnosis of adenomyosis uteri. Am J Obstet Gynecol 1993, 169:546-549.
53. Brosens J.J., Barker F.G. The role of myometrial needle biopsies in the diagnosis of adenomyosis. Fertil Steril 1995, 63:1347-1349.
54. Bazot M., Cortez A., Darai E., et al. Ultrasonography compared with magnetic resonance imaging for the diagnosis of adenomyosis: correlation with histopathology. Hum Reprod 2001, 16:2427-2433.
55. Sakhel K., Abuhamad A. Sonography of adenomyosis. J Ultrasound Med 2012, 31:805-808.
56. 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, 37:471-479.
57. Reinhold C, Tafazoli F, Mehio A, et al. Uterine adenomyosis: endovaginal US and MR imaging features with histopathologic correlation. Radiographics. 1999;19:Spec No:S147-S160.
58. Exacoustos C., Manganaro L., Zupi E. Imaging for the evaluation of endometriosis and adenomyosis. Best Pract Res Clin Obstet Gynaecol 2014, 28:655-681.
59. Reinhold C., McCarthy S., Bret P.M., et al. Diffuse adenomyosis: comparison of endovaginal US and MR imaging with histopathologic correlation. Radiology 1996, 199:151-158.
60. Gordts S., Brosens J.J., Fusi L., Benagiano G., Brosens I. Uterine adenomyosis: a need for uniform terminology and consensus classification. Reprod Biomed Online 2008, 17:244-248.
61. Reinhold C., Atri M., Mehio A., Zakarian R., Aldis A.E., Bret P.M. Diffuse uterine adenomyosis: morphologic criteria and diagnostic accuracy of endovaginal sonography. Radiology 1995, 197:609-614.
62. Brosens J.J., de Souza N.M., Barker F.G., Paraschos T., Winston R.M. Endovaginal ultrasonography in the diagnosis of adenomyosis uteri: identifying the predictive characteristics. Br J Obstet Gynaecol 1995, 102:471-474.
63. Togashi K., Ozasa H., Konishi I., et al. Enlarged uterus: differentiation between adenomyosis and leiomyoma with MR imaging. Radiology 1989, 171:531-534.
64. Dueholm M., Lundorf E., Hansen E.S., Sorensen J.S., Ledertoug S., Olesen F. Magnetic resonance imaging and transvaginal ultrasonography for the diagnosis of adenomyosis. Fertil Steril 2001, 76:588-594.
65. Ascher S.M., Arnold L.L., Patt R.H., et al. Adenomyosis: prospective comparison of MR imaging and transvaginal sonography. Radiology 1994, 190:803-806.
66. Champaneria R., Abedin P., Daniels J., Balogun M., Khan K.S. Ultrasound scan and magnetic resonance imaging for the diagnosis of adenomyosis: systematic review comparing test accuracy. Acta Obstet Gynecol Scand 2010, 89:1374-1384.
67. Streuli I., Dubuisson J., Santulli P., de Ziegler D., Batteux F., Chapron C. An update on the pharmacological management of adenomyosis. Expert Opin Pharmacother 2014, 15:2347-2360.
68. Marjoribanks J., Proctor M.L., Farquhar C. Nonsteroidal anti-inflammatory drugs for primary dysmenorrhoea. Cochrane Database Syst Rev 2003, 4:CD001751.
69. Fong Y.F., Singh K. Medical treatment of a grossly enlarged adenomyotic uterus with the levonorgestrel-releasing intrauterine system. Contraception 1999, 60:173-175.
70. Ishihara H., Kitawaki J., Kado N., Koshiba H., Fushiki S., Honjo H. Gonadotropin-releasing hormone agonist and danazol normalize aromatase cytochrome P450 expression in eutopic endometrium from women with endometriosis, adenomyosis, or leiomyomas. Fertil Steril 2003, 79(suppl 1):735-742.
71. Akira S., Iwasaki N., Ichikawa M., et al. Successful long-term management of adenomyosis associated with deep thrombosis by low-dose gonadotropin-releasing hormone agonist therapy. Clin Exp Obstet Gynecol 2009, 36:123-125.
72. Fedele L., Bianchi S., Raffaelli R., Portuese A., Dorta M. Treatment of adenomyosis-associated menorrhagia with a levonorgestrel-releasing intrauterine device. Fertil Steril 1997, 68:426-429.
73. Sheng J., Zhang W.Y., Zhang J.P., Lu D. The LNG-IUS study on adenomyosis: a 3-year follow-up study on the efficacy and side effects of the use of levonorgestrel intrauterine system for the treatment of dysmenorrhea associated with adenomyosis. Contraception 2009, 79:189-193.
74. Cho S., Nam A., Kim H., et al. Clinical effects of the levonorgestrel-releasing intrauterine device in patients with adenomyosis. Am J Obstet Gynecol 2008, 198:373.e1-373.e7.
75. Takebayashi T., Fujino Y., Umesaki N., Ogita S. Danazol suspension injected into the uterine cervix of patients with adenomyosis and myoma. Preliminary study. Gynecol Obstet Invest 1995, 39:207-211.
76. Igarashi M., Abe Y., Fukuda M., Ando A., Miyasaka M., Yoshida M. Novel conservative medical therapy for uterine adenomyosis with a danazol-loaded intrauterine device. Fertil Steril 2000, 74:412-413.
77. Shawki O.A. Danazol loaded intrauterine device (D-IUD): a novel conservative management for uterine adenomyosis. Middle East Fertil Soc J 2002, 7:214-220.
78. Grow D.R., Filer R.B. Treatment of adenomyosis with long-term GnRH analogues: a case report. Obstet Gynecol 1991, 78(Pt 2):538-539.
79. Noble L.S., Simpson E.R., Johns A., Bulun S.E. Aromatase expression in endometriosis. J Clin Endocrinol Metab 1996, 81:174-179.
80. Bulun S.E., Fang Z., Imir G., et al. Aromatase and endometriosis. Semin Reprod Med 2004, 22:45-50.
81. Nawathe A., Patwardhan S., Yates D., Harrison G.R., Khan K.S. Systematic review of the effects of aromatase inhibitors on pain associated with endometriosis. BJOG 2008, 115:818-822.
82. Wood C. Surgical and medical treatment of adenomyosis. Hum Reprod Update 1998, 4:323-336.
83. McCausland A.M., McCausland V.M. Depth of endometrial penetration in adenomyosis helps determine outcome of rollerball ablation. Am J Obstet Gynecol 1996, 174:1786-1793. 1793-1794.
84. El-Nashar S.A., Hopkins M.R., Creedon D.J., et al. Prediction of treatment outcomes after global endometrial ablation. Obstet Gynecol 2009, 113:97-106.
85. Pepas L., Deguara C., Davis C. Update on the surgical management of adenomyosis. Curr Opin Obstet Gynecol 2012, 24:259-264.
86. Gordts S., Campo R., Brosens I. Hysteroscopic diagnosis and excision of myometrial cystic adenomyosis. Gynecol Surg 2014, 11:273-278.
87. Jha R.C., Takahama J., Imaoka I., et al. Adenomyosis: MRI of the uterus treated with uterine artery embolization. AJR Am J Roentgenol 2003, 181:851-856.
88. Kim M.D., Kim S., Kim N.K., et al. Long-term results of uterine artery embolization for symptomatic adenomyosis. AJR Am J Roentgenol 2007, 188:176-181.
89. Popovic M., Puchner S., Berzaczy D., Lammer J., Bucek R.A. Uterine artery embolization for the treatment of adenomyosis: a review. J Vasc Interv Radiol 2011, 22:901-909. quiz 909.
90. Rabinovici J., Stewart E.A. New interventional techniques for adenomyosis. Best Pract Res Clin Obstet Gynaecol 2006, 20:617-636.
91. Taran F.A., Stewart E.A., Brucker S. Adenomyosis: epidemiology, risk factors, clinical phenotype and surgical and interventional alternatives to hysterectomy. Geburtshilfe Frauenheilkd 2013, 73:924-931.
92. Wang P.H., Liu W.M., Fuh J.L., Cheng M.H., Chao H.T. Comparison of surgery alone and combined surgical-medical treatment in the management of symptomatic uterine adenomyoma. Fertil Steril 2009, 92:876-885.
93. Fedele L., Bianchi S., Zanotti F., Marchini M., Candiani G.B. Fertility after conservative surgery for adenomyomas. Hum Reprod 1993, 8:1708-1710.
94. Wood C., Maher P., Hill D. Biopsy diagnosis and conservative surgical treatment of adenomyosis. J Am Assoc Gynecol Laparosc 1994, 1(Pt 1):313-316.
95. Phillips D.R., Nathanson H.G., Milim S.J., Haselkorn J.S. Laparoscopic bipolar coagulation for the conservative treatment of adenomyomata. J Am Assoc Gynecol Laparosc 1996, 4:19-24.
96. Nishida M., Takano K., Arai Y., Ozone H., Ichikawa R. Conservative surgical management for diffuse uterine adenomyosis. Fertil Steril 2010, 94:715-719.
97. Fujishita A., Masuzaki H., Khan K.N., Kitajima M., Ishimaru T. Modified reduction surgery for adenomyosis: a preliminary report of the transverse H incision technique. Gynecol Obstet Invest 2004, 57:132-138.
98. Rabinovici J., Inbar Y., Eylon S.C., Schiff E., Hananel A., Freundlich D. Pregnancy and live birth after focused ultrasound surgery for symptomatic focal adenomyosis: a case report. Hum Reprod 2006, 21:1255-1259.
99. Fukunishi H., Funaki K., Sawada K., Yamaguchi K., Maeda T., Kaji Y. Early results of magnetic resonance-guided focused ultrasound surgery of adenomyosis: analysis of 20 cases. J Minim Invasive Gynecol 2008, 15:571-579.
100. Zhou M., Chen J.Y., Tang L.D., Chen W.Z., Wang Z.B. Ultrasound-guided high-intensity focused ultrasound ablation for adenomyosis: the clinical experience of a single center. Fertil Steril 2011, 95:900-905.
101. Dicker R.C., Greenspan J.R., Strauss L.T., et al. Complications of abdominal and vaginal hysterectomy among women of reproductive age in the United States. The Collaborative Review of Sterilization. Am J Obstet Gynecol 1982, 144:841-848.
102. Furuhashi M., Miyabe Y., Katsumata Y., Oda H., Imai N. Comparison of complications of vaginal hysterectomy in patients with leiomyomas and in patients with adenomyosis. Arch Gynecol Obstet 1998, 262:69-73.
103. Meikle S.F., Nugent E.W., Orleans M. Complications and recovery from laparoscopy-assisted vaginal hysterectomy compared with abdominal and vaginal hysterectomy. Obstet Gynecol 1997, 89:304-311.
104. Candiani M., Izzo S., Bulfoni A., Riparini J., Ronzoni S., Marconi A. Laparoscopic vs vaginal hysterectomy for benign pathology. Am J Obstet Gynecol 2009, 200:368.e1-368.e7.
105. Ghezzi F., Uccella S., Cromi A., et al. Postoperative pain after laparoscopic and vaginal hysterectomy for benign gynecologic disease: a randomized trial. Am J Obstet Gynecol 2010, 203:118.e1-118.e8.
106. Stovall T.G., Ling F.W., Crawford D.A. Hysterectomy for chronic pelvic pain of presumed uterine etiology. Obstet Gynecol 1990, 75:676-679.