PDF herunterladen
Semin Reprod Med 2020; 38(02/03): 089-107
DOI: 10.1055/s-0040-1718920
Review Article

Epidemiology of Adenomyosis

Kristen Upson 
1   Department of Epidemiology and Biostatistics, College of Human Medicine, Michigan State University, East Lansing, Michigan
,
Stacey A. Missmer
1   Department of Epidemiology and Biostatistics, College of Human Medicine, Michigan State University, East Lansing, Michigan
2   Department of Obstetrics, Gynecology, and Reproductive Biology, College of Human Medicine, Michigan State University, Grand Rapids, Michigan
3   Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts
› Institutsangaben Funding This work was supported by the National Institute of Nursing Research (grant R00NR017191 to K.U.) and Eunice Kennedy Shriver National Institute of Child Health and Human Development (grant R01HD094842 to S.A.M.) of the National Institutes of Health. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
› Weitere Informationen
    Lizenzen und Reprints

Abstract

Adenomyosis, characterized by the presence of endometrial glands and stroma within the myometrium, can have a substantial impact on the quality of women's lives. Despite this, the epidemiologic research on this condition lags considerably behind that of other noncancerous reproductive health conditions. The lack of progress and knowledge is due in part to the challenges in designing valid epidemiologic studies, since the diagnosis of adenomyosis historically has been limited to the examination of uterine specimens from hysterectomy. This review describes the available data on the frequency of this condition and the epidemiologic investigation thus far into the risk factors for disease—highlighting the methodologic and inference challenges primarily around study sample selection. We conclude with providing recommendations for approaches to future epidemiologic study that capitalize on the advancements in imaging technology to detect adenomyosis and provide a fuller picture of the occurrence and risk factors for disease.

Keywords

adenomyosis - epidemiology - risk factors - prevalence - hysterectomy


Publikationsverlauf

Artikel online veröffentlicht:
26. Oktober 2020

© 2020. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Munro MG. Classification and reporting systems for adenomyosis. J Minim Invasive Gynecol 2020; 27 (02) 296-308
    CrossrefPubMedGoogle Scholar
  • 2 Emge LA. The elusive adenomyosis of the uterus. Its historical past and its present state of recognition. Am J Obstet Gynecol 1962; 83: 1541-1563
    CrossrefPubMedGoogle Scholar
  • 3 García-Solares J, Donnez J, Donnez O, Dolmans MM. Pathogenesis of uterine adenomyosis: invagination or metaplasia?. Fertil Steril 2018; 109 (03) 371-379
    CrossrefPubMedGoogle Scholar
  • 4 Vannuccini S, Tosti C, Carmona F. et al. Pathogenesis of adenomyosis: an update on molecular mechanisms. Reprod Biomed Online 2017; 35 (05) 592-601
    CrossrefPubMedGoogle Scholar
  • 5 Leyendecker G, Wildt L. A new concept of endometriosis and adenomyosis: tissue injury and repair (TIAR). Horm Mol Biol Clin Investig 2011; 5 (02) 125-142
    PubMedGoogle Scholar
  • 6 Leyendecker G, Wildt L, Mall G. The pathophysiology of endometriosis and adenomyosis: tissue injury and repair. Arch Gynecol Obstet 2009; 280 (04) 529-538
    CrossrefPubMedGoogle Scholar
  • 7 Nelsen LM, Lenderking WR, Pokrzywinski R. et al. Experience of symptoms and disease impact in patients with adenomyosis. Patient 2018; 11 (03) 319-328
    CrossrefPubMedGoogle Scholar
  • 8 Razavi M, Maleki-Hajiagha A, Sepidarkish M, Rouholamin S, Almasi-Hashiani A, Rezaeinejad M. Systematic review and meta-analysis of adverse pregnancy outcomes after uterine adenomyosis. Int J Gynaecol Obstet 2019; 145 (02) 149-157
    CrossrefPubMedGoogle Scholar
  • 9 Dueholm M. Uterine adenomyosis and infertility, review of reproductive outcome after in vitro fertilization and surgery. Acta Obstet Gynecol Scand 2017; 96 (06) 715-726
    CrossrefPubMedGoogle Scholar
  • 10 Vercellini P, Consonni D, Dridi D, Bracco B, Frattaruolo MP, Somigliana E. Uterine adenomyosis and in vitro fertilization outcome: a systematic review and meta-analysis. Hum Reprod 2014; 29 (05) 964-977
    CrossrefPubMedGoogle Scholar
  • 11 Younes G, Tulandi T. Effects of adenomyosis on in vitro fertilization treatment outcomes: a meta-analysis. Fertil Steril 2017; 108 (03) 483-490.e3
    CrossrefPubMedGoogle Scholar
  • 12 Taran FA, Weaver AL, Coddington CC, Stewart EA. Understanding adenomyosis: a case control study. Fertil Steril 2010; 94 (04) 1223-1228
    CrossrefPubMedGoogle Scholar
  • 13 Brinton LA, Gridley G, Persson I, Baron J, Bergqvist A. Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol 1997; 176 (03) 572-579
    CrossrefPubMedGoogle Scholar
  • 14 Kok VC, Tsai HJ, Su CF, Lee CK. The risks for ovarian, endometrial, breast, colorectal, and other cancers in women with newly diagnosed endometriosis or adenomyosis: a population-based study. Int J Gynecol Cancer 2015; 25 (06) 968-976
    CrossrefPubMedGoogle Scholar
  • 15 Yeh CC, Su FH, Tzeng CR, Muo CH, Wang WC. Women with adenomyosis are at higher risks of endometrial and thyroid cancers: a population-based historical cohort study. PLoS One 2018; 13 (03) e0194011
    CrossrefPubMedGoogle Scholar
  • 16 Koepsell TD, Weiss NS. Epidemiologic Methods: Studying the Occurrence of Illness. New York, NY: Oxford University Press; 2003
    Google Scholar
  • 17 Chapron C, Vannuccini S, Santulli P. et al. Diagnosing adenomyosis: an integrated clinical and imaging approach. Hum Reprod Update 2020; 26 (03) 392-411
    CrossrefPubMedGoogle Scholar
  • 18 Molitor JJ. Adenomyosis: a clinical and pathologic appraisal. Trans Pac Coast Obstet Gynecol Soc 1970; 38: 159-168
    PubMedGoogle Scholar
  • 19 Bird CC, McElin TW, Manalo-Estrella P. The elusive adenomyosis of the uterus--revisited. Am J Obstet Gynecol 1972; 112 (05) 583-593
    CrossrefPubMedGoogle Scholar
  • 20 Owolabi TO, Strickler RC. Adenomyosis: a neglected diagnosis. Obstet Gynecol 1977; 50 (04) 424-427
    PubMedGoogle Scholar
  • 21 Blum M. Adenomyosis: study in a Jewish female population. Int Surg 1981; 66 (04) 341-343
    PubMedGoogle Scholar
  • 22 Pendse V. Adenomyosis uteri. J Indian Med Assoc 1981; 76 (05) 75-77
    PubMedGoogle Scholar
  • 23 Rao BN, Persaud V. Adenomyosis uteri. Report on a 15-year study (1966-1980) at the University Hospital of the West Indies. West Indian Med J 1982; 31 (04) 205-212
    PubMedGoogle Scholar
  • 24 Fukamatsu Y, Tsukahara Y, Fukuta T. A clinicopathologic study on adenomyosis uteri. Nippon Sanka Fujinka Gakkai Zasshi 1984; 36 (03) 431-436
    PubMedGoogle Scholar
  • 25 Kilkku P, Erkkola R, Grönroos M. Non-specificity of symptoms related to adenomyosis. A prospective comparative survey. Acta Obstet Gynecol Scand 1984; 63 (03) 229-231
    CrossrefPubMedGoogle Scholar
  • 26 Harris WJ, Daniell JF, Baxter JW. Prior cesarean section. A risk factor for adenomyosis?. J Reprod Med 1985; 30 (03) 173-175
    PubMedGoogle Scholar
  • 27 Thompson JR, Davion RJ. Adenomyosis of the uterus: an enigma. J Natl Med Assoc 1986; 78 (04) 305-307
    PubMedGoogle Scholar
  • 28 Raju GC, Naraynsingh V, Woo J, Jankey N. Adenomyosis uteri: a study of 416 cases. Aust N Z J Obstet Gynaecol 1988; 28 (01) 72-73
    CrossrefPubMedGoogle Scholar
  • 29 Thomas Jr JS, Clark JF. Adenomyosis: a retrospective view. J Natl Med Assoc 1989; 81 (09) 969-972
    PubMedGoogle Scholar
  • 30 Shaikh H, Khan KS. Adenomyosis in Pakistani women: four year experience at the Aga Khan University Medical Centre, Karachi. J Clin Pathol 1990; 43 (10) 817-819
    CrossrefPubMedGoogle Scholar
  • 31 Chrysostomou M, Akalestos G, Kallistros S, Papadimitriou V, Nazar S, Chronis G. Incidence of adenomyosis uteri in a Greek population. Acta Obstet Gynecol Scand 1991; 70 (06) 441-444
    CrossrefPubMedGoogle Scholar
  • 32 Bocker J, Tadmor OP, Gal M, Diamant YZ. The prevalence of adenomyosis and endometriosis in an ultra-religious Jewish population. Asia Oceania J Obstet Gynaecol 1994; 20 (02) 125-129
    CrossrefPubMedGoogle Scholar
  • 33 Vercellini P, Parazzini F, Oldani S, Panazza S, Bramante T, Crosignani PG. Adenomyosis at hysterectomy: a study on frequency distribution and patient characteristics. Hum Reprod 1995; 10 (05) 1160-1162
    CrossrefPubMedGoogle Scholar
  • 34 Reinhold C, McCarthy S, Bret PM. et al. Diffuse adenomyosis: comparison of endovaginal US and MR imaging with histopathologic correlation. Radiology 1996; 199 (01) 151-158
    CrossrefPubMedGoogle Scholar
  • 35 Seidman JD, Kjerulff KH. Pathologic findings from the Maryland Women's Health Study: practice patterns in the diagnosis of adenomyosis. Int J Gynecol Pathol 1996; 15 (03) 217-221
    CrossrefPubMedGoogle Scholar
  • 36 Parazzini F, Vercellini P, Panazza S, Chatenoud L, Oldani S, Crosignani PG. Risk factors for adenomyosis. Hum Reprod 1997; 12 (06) 1275-1279
    CrossrefPubMedGoogle Scholar
  • 37 Vavilis D, Agorastos T, Tzafetas J. et al. Adenomyosis at hysterectomy: prevalence and relationship to operative findings and reproductive and menstrual factors. Clin Exp Obstet Gynecol 1997; 24 (01) 36-38
    PubMedGoogle Scholar
  • 38 Bergholt T, Eriksen L, Berendt N, Jacobsen M, Hertz JB. Prevalence and risk factors of adenomyosis at hysterectomy. Hum Reprod 2001; 16 (11) 2418-2421
    CrossrefPubMedGoogle Scholar
  • 39 Curtis KM, Hillis SD, Marchbanks PA, Peterson HB. Disruption of the endometrial-myometrial border during pregnancy as a risk factor for adenomyosis. Am J Obstet Gynecol 2002; 187 (03) 543-544
    CrossrefPubMedGoogle Scholar
  • 40 Panganamamula UR, Harmanli OH, Isik-Akbay EF, Grotegut CA, Dandolu V, Gaughan JP. Is prior uterine surgery a risk factor for adenomyosis?. Obstet Gynecol 2004; 104 (5, Pt 1): 1034-1038
    CrossrefPubMedGoogle Scholar
  • 41 Yeniel O, Cirpan T, Ulukus M. et al. Adenomyosis: prevalence, risk factors, symptoms and clinical findings. Clin Exp Obstet Gynecol 2007; 34 (03) 163-167
    PubMedGoogle Scholar
  • 42 Parazzini F, Mais V, Cipriani S, Busacca M, Venturini P. GISE. Determinants of adenomyosis in women who underwent hysterectomy for benign gynecological conditions: results from a prospective multicentric study in Italy. Eur J Obstet Gynecol Reprod Biol 2009; 143 (02) 103-106
    CrossrefPubMedGoogle Scholar
  • 43 Özkan ZS, Kumbak B, Cilgin H, Simsek M, Turk BA. Coexistence of adenomyosis in women operated for benign gynecological diseases. Gynecol Endocrinol 2012; 28 (03) 212-215
    CrossrefPubMedGoogle Scholar
  • 44 Saleh SS, Fram K. Histopathology diagnosis in women who underwent a hysterectomy for a benign condition. Arch Gynecol Obstet 2012; 285 (05) 1339-1343
    CrossrefPubMedGoogle Scholar
  • 45 Shrestha A, Shrestha R, Sedhai LB, Pandit U. Adenomyosis at hysterectomy: prevalence, patient characteristics, clinical profile and histopatholgical findings. Kathmandu Univ Med J (KUMJ) 2012; 10 (37) 53-56
    CrossrefPubMedGoogle Scholar
  • 46 Pervez SN, Javed K. Adenomyosis among samples from hysterectomy due to abnormal uterine bleeding. J Ayub Med Coll Abbottabad 2013; 25 (1-2): 68-70
    PubMedGoogle Scholar
  • 47 Li X, Liu X, Guo SW. Clinical profiles of 710 premenopausal women with adenomyosis who underwent hysterectomy. J Obstet Gynaecol Res 2014; 40 (02) 485-494
    CrossrefPubMedGoogle Scholar
  • 48 Whiteman MK, Hillis SD, Jamieson DJ. et al. Inpatient hysterectomy surveillance in the United States, 2000-2004. Am J Obstet Gynecol 2008; 198 (01) 34.e1-34.e7
    CrossrefPubMedGoogle Scholar
  • 49 Naftalin J, Hoo W, Pateman K, Mavrelos D, Holland T, Jurkovic D. How common is adenomyosis? A prospective study of prevalence using transvaginal ultrasound in a gynaecology clinic. Hum Reprod 2012; 27 (12) 3432-3439
    CrossrefPubMedGoogle Scholar
  • 50 Naftalin J, Hoo W, Nunes N, Holland T, Mavrelos D, Jurkovic D. Association between ultrasound features of adenomyosis and severity of menstrual pain. Ultrasound Obstet Gynecol 2016; 47 (06) 779-783
    CrossrefPubMedGoogle Scholar
  • 51 Pinzauti S, Lazzeri L, Tosti C. et al. Transvaginal sonographic features of diffuse adenomyosis in 18-30-year-old nulligravid women without endometriosis: association with symptoms. Ultrasound Obstet Gynecol 2015; 46 (06) 730-736
    CrossrefPubMedGoogle Scholar
  • 52 Tellum T, Nygaard S, Lieng M. Noninvasive diagnosis of adenomyosis: a structured review and meta-analysis of diagnostic accuracy in imaging. J Minim Invasive Gynecol 2020; 27 (02) 408-418.e3
    CrossrefPubMedGoogle Scholar
  • 53 Filip G, Balzano A, Cagnacci A. Histological evaluation of the prevalence of adenomyosis, myomas and of their concomitance. Minerva Ginecol 2019; 71 (03) 177-181
    CrossrefPubMedGoogle Scholar
  • 54 Nomelini RS, Ferreira FA, Borges RC, Adad SJ, Murta EF. Frequency of endometriosis and adenomyosis in patients with leiomyomas, gynecologic premalignant, and malignant neoplasias. Clin Exp Obstet Gynecol 2013; 40 (01) 40-44
    PubMedGoogle Scholar
  • 55 Mobarakeh MD, Maghsudi A, Rashidi I. Adenomyosis among samples from hysterectomy due to abnormal uterine bleeding in Ahwaz, southern Iran. Adv Biomed Res 2012; 1: 49
    CrossrefPubMedGoogle Scholar
  • 56 Sawke NG, Sawke GK, Jain H. Histopathology findings in patients presenting with menorrhagia: a study of 100 hysterectomy specimen. J Midlife Health 2015; 6 (04) 160-163
    CrossrefPubMedGoogle Scholar
  • 57 Sharma C, Sharma M, Raina R, Soni A, Chander B, Verma S. Gynecological diseases in rural India: a critical appraisal of indications and route of surgery along with histopathology correlation of 922 women undergoing major gynecological surgery. J Midlife Health 2014; 5 (02) 55-61
    CrossrefPubMedGoogle Scholar
  • 58 Abu Hashim H, Elaraby S, Fouda AA, Rakhawy ME. The prevalence of adenomyosis in an infertile population: a cross-sectional study. Reprod Biomed Online 2020; 40 (06) 842-850
    CrossrefPubMedGoogle Scholar
  • 59 Puente JM, Fabris A, Patel J. et al. Adenomyosis in infertile women: prevalence and the role of 3D ultrasound as a marker of severity of the disease. Reprod Biol Endocrinol 2016; 14 (01) 60
    CrossrefPubMedGoogle Scholar
  • 60 Matalliotaki C, Matalliotakis M, Ieromonachou P. et al. Co-existence of benign gynecological tumors with endometriosis in a group of 1,000 women. Oncol Lett 2018; 15 (02) 1529-1532
    PubMedGoogle Scholar
  • 61 Nikkanen V, Punnonen R. Clinical significance of adenomyosis. Ann Chir Gynaecol 1980; 69 (06) 278-280
    PubMedGoogle Scholar
  • 62 Di Donato N, Montanari G, Benfenati A. et al. Prevalence of adenomyosis in women undergoing surgery for endometriosis. Eur J Obstet Gynecol Reprod Biol 2014; 181: 289-293
    CrossrefPubMedGoogle Scholar
  • 63 Eisenberg VH, Arbib N, Schiff E, Goldenberg M, Seidman DS, Soriano D. Sonographic signs of adenomyosis are prevalent in women undergoing surgery for endometriosis and may suggest a higher risk of infertility. BioMed Res Int 2017; 2017: 8967803
    CrossrefPubMedGoogle Scholar
  • 64 Bazot M, Fiori O, Darai E. Adenomyosis in endometriosis--prevalence and impact on fertility. Evidence from magnetic resonance imaging. Hum Reprod 2006; 21 (04) 1101-1102 , author reply 1102–1103
    CrossrefPubMedGoogle Scholar
  • 65 Chapron C, Tosti C, Marcellin L. et al. Relationship between the magnetic resonance imaging appearance of adenomyosis and endometriosis phenotypes. Hum Reprod 2017; 32 (07) 1393-1401
    CrossrefPubMedGoogle Scholar
  • 66 Capezzuoli T, Vannuccini S, Fantappiè G. et al. Ultrasound findings in infertile women with endometriosis: evidence of concomitant uterine disorders. Gynecol Endocrinol 2020; 36 (09) 808-812
    CrossrefPubMedGoogle Scholar
  • 67 Kunz G, Beil D, Huppert P, Noe M, Kissler S, Leyendecker G. Adenomyosis in endometriosis--prevalence and impact on fertility. Evidence from magnetic resonance imaging. Hum Reprod 2005; 20 (08) 2309-2316
    CrossrefPubMedGoogle Scholar
  • 68 Dior UP, Nisbet D, Fung JN. et al. The association of sonographic evidence of adenomyosis with severe endometriosis and gene expression in eutopic endometrium. J Minim Invasive Gynecol 2019; 26 (05) 941-948
    CrossrefPubMedGoogle Scholar
  • 69 Kissler S, Zangos S, Kohl J. et al. Duration of dysmenorrhoea and extent of adenomyosis visualised by magnetic resonance imaging. Eur J Obstet Gynecol Reprod Biol 2008; 137 (02) 204-209
    CrossrefPubMedGoogle Scholar
  • 70 Larsen SB, Lundorf E, Forman A, Dueholm M. Adenomyosis and junctional zone changes in patients with endometriosis. Eur J Obstet Gynecol Reprod Biol 2011; 157 (02) 206-211
    CrossrefPubMedGoogle Scholar
  • 71 Lazzeri L, Di Giovanni A, Exacoustos C. et al. Preoperative and postoperative clinical and transvaginal ultrasound findings of adenomyosis in patients with deep infiltrating endometriosis. Reprod Sci 2014; 21 (08) 1027-1033
    CrossrefPubMedGoogle Scholar
  • 72 Donnez J, Dolmans MM, Fellah L. What if deep endometriotic nodules and uterine adenomyosis were actually two forms of the same disease?. Fertil Steril 2019; 111 (03) 454-456
    CrossrefPubMedGoogle Scholar
  • 73 Marcellin L, Santulli P, Bortolato S. et al. Anterior focal adenomyosis and bladder deep infiltrating endometriosis: Is there a link?. J Minim Invasive Gynecol 2018; 25 (05) 896-901
    CrossrefPubMedGoogle Scholar
  • 74 Morassutto C, Monasta L, Ricci G, Barbone F, Ronfani L. Incidence and estimated prevalence of endometriosis and adenomyosis in northeast Italy: a data linkage study. PLoS One 2016; 11 (04) e0154227
    CrossrefPubMedGoogle Scholar
  • 75 Yu O, Schulze-Rath R, Grafton J, Hansen K, Scholes D, Reed SD. Adenomyosis incidence, prevalence and treatment: United States population-based study 2006-2015. Am J Obstet Gynecol 2020; 223 (01) 94.e1-94.e10
    CrossrefPubMedGoogle Scholar
  • 76 Munro MG. Classification of menstrual bleeding disorders. Rev Endocr Metab Disord 2012; 13 (04) 225-234
    CrossrefPubMedGoogle Scholar
  • 77 Israel SL, Woutersz TB. Adenomyosis; a neglected diagnosis. Obstet Gynecol 1959; 14 (02) 168-173
    PubMedGoogle Scholar
  • 78 Benson RC, Sneeden VD. Adenomyosis: a reappraisal of symptomatology. Am J Obstet Gynecol 1958; 76 (05) 1044-1057 , discussion 1057–1061
    CrossrefPubMedGoogle Scholar
  • 79 Basak S, Saha A. Adenomyosis: still largely under-diagnosed. J Obstet Gynaecol 2009; 29 (06) 533-535
    CrossrefPubMedGoogle Scholar
  • 80 Bodur S, Dundar O, Pektas MK, Babayigit MA, Ozden O, Kucukodacı Z. The clinical significance of classical and new emerging determinants of adenomyosis. Int J Clin Exp Med 2015; 8 (05) 7958-7964
    PubMedGoogle Scholar
  • 81 Ajao MO, Oliveira Brito LG, Wang KC. et al. Persistence of symptoms after total vs supracervical hysterectomy in women with histopathological diagnosis of adenomyosis. J Minim Invasive Gynecol 2019; 26 (05) 891-896
    CrossrefPubMedGoogle Scholar
  • 82 Naftalin J, Hoo W, Pateman K, Mavrelos D, Foo X, Jurkovic D. Is adenomyosis associated with menorrhagia?. Hum Reprod 2014; 29 (03) 473-479
    CrossrefPubMedGoogle Scholar
  • 83 But I, Pakiž M, Rakić S. Overactive bladder symptoms and uterine adenomyosis--is there any connection?. Eur J Obstet Gynecol Reprod Biol 2011; 156 (01) 109-112
    CrossrefPubMedGoogle Scholar
  • 84 Ekin M, Cengiz H, Öztürk E, Kaya C, Yaşar L. Genitourinary symptoms in patients with adenomyosis. Int Urogynecol J Pelvic Floor Dysfunct 2013; 24 (03) 509-512
    CrossrefPubMedGoogle Scholar
  • 85 Aydin GA, Yavuz A. Adenomyosis and urinary system symptoms. Eur J Obstet Gynecol Reprod Biol 2018; 224: 74-76
    CrossrefPubMedGoogle Scholar
  • 86 Romanek K, Bartuzi A, Bogusiewicz M, Rechberger T. Risk factors for adenomyosis in patients with symptomatic uterine leiomyomas. Ginekol Pol 2010; 81 (09) 678-680
    PubMedGoogle Scholar
  • 87 Taran FA, Weaver AL, Coddington CC, Stewart EA. Characteristics indicating adenomyosis coexisting with leiomyomas: a case-control study. Hum Reprod 2010; 25 (05) 1177-1182
    CrossrefPubMedGoogle Scholar
  • 88 Shrestha A, Sedai LB. Understanding clinical features of adenomyosis: a case control study. Nepal Med Coll J 2012; 14 (03) 176-179
    PubMedGoogle Scholar
  • 89 Taran FA, Wallwiener M, Kabashi D. et al. Clinical characteristics indicating adenomyosis at the time of hysterectomy: a retrospective study in 291 patients. Arch Gynecol Obstet 2012; 285 (06) 1571-1576
    CrossrefPubMedGoogle Scholar
  • 90 Jean-Baptiste H, Tetrokalashvili M, Williams T, Fogel J, Hsu CD. Characteristics associated with postoperative diagnosis of adenomyosis or combined adenomyosis with fibroids. Int J Gynaecol Obstet 2013; 122 (02) 112-114
    CrossrefPubMedGoogle Scholar
  • 91 Boeer B, Wallwiener M, Rom J, Schoenfisch B, Brucker SY, Taran FA. Differences in the clinical phenotype of adenomyosis and leiomyomas: a retrospective, questionnaire-based study. Arch Gynecol Obstet 2014; 289 (06) 1235-1239
    CrossrefPubMedGoogle Scholar
  • 92 Brucker SY, Huebner M, Wallwiener M. et al. Clinical characteristics indicating adenomyosis coexisting with leiomyomas: a retrospective, questionnaire-based study. Fertil Steril 2014; 101 (01) 237-241.e1
    CrossrefPubMedGoogle Scholar
  • 93 Ates S, Ozcan P, Aydin S, Karaca N. Differences in clinical characteristics for the determination of adenomyosis coexisting with leiomyomas. J Obstet Gynaecol Res 2016; 42 (03) 307-312
    CrossrefPubMedGoogle Scholar
  • 94 Weiss G, Maseelall P, Schott LL, Brockwell SE, Schocken M, Johnston JM. Adenomyosis a variant, not a disease? Evidence from hysterectomized menopausal women in the Study of Women's Health Across the Nation (SWAN). Fertil Steril 2009; 91 (01) 201-206
    CrossrefPubMedGoogle Scholar
  • 95 Erekson EA, Weitzen S, Sung VW, Raker CA, Myers DL. Socioeconomic indicators and hysterectomy status in the United States, 2004. J Reprod Med 2009; 54 (09) 553-558
    PubMedGoogle Scholar
  • 96 Wilson LF, Mishra GD. Age at menarche, level of education, parity and the risk of hysterectomy: a systematic review and meta-analyses of population-based observational studies. PLoS One 2016; 11 (03) e0151398
    CrossrefPubMedGoogle Scholar
  • 97 Rothman KJ, Greenland S, Lash TL. Modern Epidemiology. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2008
    Google Scholar
  • 98 Wacholder S, McLaughlin JK, Silverman DT, Mandel JS. Selection of controls in case-control studies. I. Principles. Am J Epidemiol 1992; 135 (09) 1019-1028
    CrossrefPubMedGoogle Scholar
  • 99 Merrill RM. Hysterectomy surveillance in the United States, 1997 through 2005. Med Sci Monit 2008; 14 (01) CR24-CR31
    PubMedGoogle Scholar
  • 100 Trabert B, Weiss NS, Rudra CB, Scholes D, Holt VL. A case-control investigation of adenomyosis: impact of control group selection on risk factor strength. Womens Health Issues 2011; 21 (02) 160-164
    CrossrefPubMedGoogle Scholar
  • 101 Levgur M, Abadi MA, Tucker A. Adenomyosis: symptoms, histology, and pregnancy terminations. Obstet Gynecol 2000; 95 (05) 688-691
    CrossrefPubMedGoogle Scholar
  • 102 Templeman C, Marshall SF, Ursin G. et al. Adenomyosis and endometriosis in the California Teachers Study. Fertil Steril 2008; 90 (02) 415-424
    CrossrefPubMedGoogle Scholar
  • 103 Huang PC, Tsai EM, Li WF. et al. Association between phthalate exposure and glutathione S-transferase M1 polymorphism in adenomyosis, leiomyoma and endometriosis. Hum Reprod 2010; 25 (04) 986-994
    CrossrefPubMedGoogle Scholar
  • 104 Shrestha A. Risk factors for adenomyosis. J Nepal Health Res Counc 2012; 10 (22) 229-233
    PubMedGoogle Scholar
  • 105 Huang PC, Li WF, Liao PC, Sun CW, Tsai EM, Wang SL. Risk for estrogen-dependent diseases in relation to phthalate exposure and polymorphisms of CYP17A1 and estrogen receptor genes. Environ Sci Pollut Res Int 2014; 21 (24) 13964-13973
    CrossrefPubMedGoogle Scholar
  • 106 Kazemi E, Alavi A, Aalinezhad F, Jahanshahi K. Evaluation of the relationship between prior uterine surgery and the incidence of adenomyosis in the Shariati Hospital in Bandar-Abbas, Iran, from 2001 to 2011. Electron Physician 2014; 6 (03) 912-918
    PubMedGoogle Scholar
  • 107 Riggs JC, Lim EK, Liang D, Bullwinkel R. Cesarean section as a risk factor for the development of adenomyosis uteri. J Reprod Med 2014; 59 (1-2): 20-24
    PubMedGoogle Scholar
  • 108 Genc M, Genc B, Cengiz H. Adenomyosis and accompanying gynecological pathologies. Arch Gynecol Obstet 2015; 291 (04) 877-881
    CrossrefPubMedGoogle Scholar
  • 109 Güzel AI, Akselim B, Erkılınç S. et al. Risk factors for adenomyosis, leiomyoma and concurrent adenomyosis and leiomyoma. J Obstet Gynaecol Res 2015; 41 (06) 932-937
    CrossrefPubMedGoogle Scholar
  • 110 Gao M, Allebeck P, Mishra GD, Koupil I. Developmental origins of endometriosis: a Swedish cohort study. J Epidemiol Community Health 2019; 73 (04) 353-359
    CrossrefPubMedGoogle Scholar
  • 111 Aarestrup J, Jensen BW, Ulrich LG, Hartwell D, Trabert B, Baker JL. Birth weight, childhood body mass index and height and risks of endometriosis and adenomyosis. Ann Hum Biol 2020; 47 (02) 173-180
    CrossrefPubMedGoogle Scholar
  • 112 Bailey ZD, Krieger N, Agénor M, Graves J, Linos N, Bassett MT. Structural racism and health inequities in the USA: evidence and interventions. Lancet 2017; 389 (10077): 1453-1463
    CrossrefPubMedGoogle Scholar
  • 113 Hahn RA, Truman BI. Education improves public health and promotes health equity. Int J Health Serv 2015; 45 (04) 657-678
    CrossrefPubMedGoogle Scholar
  • 114 Udry JR. Age at menarche, at first intercourse, and at first pregnancy. J Biosoc Sci 1979; 11 (04) 433-441
    CrossrefPubMedGoogle Scholar
  • 115 Baird DD. Invited commentary: uterine leiomyomata-we know so little but could learn so much. Am J Epidemiol 2004; 159 (02) 124-126
    CrossrefPubMedGoogle Scholar
  • 116 Nnoaham KE, Webster P, Kumbang J, Kennedy SH, Zondervan KT. Is early age at menarche a risk factor for endometriosis? A systematic review and meta-analysis of case-control studies. Fertil Steril 2012; 98 (03) 702-712.e6
    CrossrefPubMedGoogle Scholar
  • 117 Dada OA, Laditan AA. Circulating hormonal levels during prolonged lactational amenorrhea. Clin Chim Acta 1982; 123 (03) 287-292
    CrossrefPubMedGoogle Scholar
  • 118 Karlsson C, Obrant KJ, Karlsson M. Pregnancy and lactation confer reversible bone loss in humans. Osteoporos Int 2001; 12 (10) 828-834
    CrossrefPubMedGoogle Scholar
  • 119 Sowers MR, Zheng H, McConnell D, Nan B, Harlow SD, Randolph Jr JF. Estradiol rates of change in relation to the final menstrual period in a population-based cohort of women. J Clin Endocrinol Metab 2008; 93 (10) 3847-3852
    CrossrefPubMedGoogle Scholar
  • 120 Pijnenborg R. The human decidua as a passage-way for trophoblast invasion: a review. Trophoblast Research. 1998; 11: 229-241
    PubMedGoogle Scholar
  • 121 Uduwela AS, Perera MA, Aiqing L, Fraser IS. Endometrial-myometrial interface: relationship to adenomyosis and changes in pregnancy. Obstet Gynecol Surv 2000; 55 (06) 390-400
    CrossrefPubMedGoogle Scholar
  • 122 Baird DD, Dunson DB. Why is parity protective for uterine fibroids?. Epidemiology 2003; 14 (02) 247-250
    CrossrefPubMedGoogle Scholar
  • 123 Opara EI, Zaidi J. The interpretation and clinical application of the word ‘parity’: a survey. BJOG 2007; 114 (10) 1295-1297
    CrossrefPubMedGoogle Scholar
  • 124 Struble J, Reid S, Bedaiwy MA. Adenomyosis: a clinical review of a challenging gynecologic condition. J Minim Invasive Gynecol 2016; 23 (02) 164-185
    CrossrefPubMedGoogle Scholar
  • 125 Taran FA, Stewart EA, Brucker S. Adenomyosis: epidemiology, risk factors, clinical phenotype and surgical and interventional alternatives to hysterectomy. Geburtshilfe Frauenheilkd 2013; 73 (09) 924-931
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 126 Nasu K, Takai N, Nishida M, Narahara H. Tumorigenic effects of tamoxifen on the female genital tract. Clin Med Pathol 2008; 1: 17-34
    CrossrefPubMedGoogle Scholar
  • 127 Ugwumadu AH, Bower D, Ho PK. Tamoxifen induced adenomyosis and adenomyomatous endometrial polyp. Br J Obstet Gynaecol 1993; 100 (04) 386-388
    CrossrefPubMedGoogle Scholar
  • 128 Cohen I, Beyth Y, Tepper R. et al. Adenomyosis in postmenopausal breast cancer patients treated with tamoxifen: a new entity?. Gynecol Oncol 1995; 58 (01) 86-91
    CrossrefPubMedGoogle Scholar
  • 129 Ascher SM, Johnson JC, Barnes WA, Bae CJ, Patt RH, Zeman RK. MR imaging appearance of the uterus in postmenopausal women receiving tamoxifen therapy for breast cancer: histopathologic correlation. Radiology 1996; 200 (01) 105-110
    CrossrefPubMedGoogle Scholar
  • 130 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 (03) 200-205
    CrossrefPubMedGoogle Scholar
  • 131 Bracht JR, Vieira-Potter VJ, De Souza Santos R, Öz OK, Palmer BF, Clegg DJ. The role of estrogens in the adipose tissue milieu. Ann N Y Acad Sci 2020; 1461 (01) 127-143
    CrossrefPubMedGoogle Scholar
  • 132 Progetto Menopausa Italia Study Group. Determinants of hysterectomy and oophorectomy in women attending menopause clinics in Italy. Maturitas 2000; 36 (01) 19-25
    CrossrefPubMedGoogle Scholar
  • 133 Terry KL, De Vivo I, Hankinson SE, Spiegelman D, Wise LA, Missmer SA. Anthropometric characteristics and risk of uterine leiomyoma. Epidemiology 2007; 18 (06) 758-763
    CrossrefPubMedGoogle Scholar
  • 134 Wise LA, Palmer JR, Spiegelman D. et al. Influence of body size and body fat distribution on risk of uterine leiomyomata in U.S. black women. Epidemiology 2005; 16 (03) 346-354
    CrossrefPubMedGoogle Scholar
  • 135 Whitcomb BW, Purdue-Smithe AC, Szegda KL. et al. Cigarette smoking and risk of early natural menopause. Am J Epidemiol 2018; 187 (04) 696-704
    CrossrefPubMedGoogle Scholar
  • 136 Barbieri RL, McShane PM, Ryan KJ. Constituents of cigarette smoke inhibit human granulosa cell aromatase. Fertil Steril 1986; 46 (02) 232-236
    CrossrefPubMedGoogle Scholar
  • 137 Michnovicz JJ, Hershcopf RJ, Naganuma H, Bradlow HL, Fishman J. Increased 2-hydroxylation of estradiol as a possible mechanism for the anti-estrogenic effect of cigarette smoking. N Engl J Med 1986; 315 (21) 1305-1309
    CrossrefPubMedGoogle Scholar
  • 138 Zoeller RT, Brown TR, Doan LL. et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology 2012; 153 (09) 4097-4110
    CrossrefPubMedGoogle Scholar
  • 139 Gore AC, Chappell VA, Fenton SE. et al. EDC-2: the Endocrine Society's second scientific statement on endocrine-disrupting chemicals. Endocr Rev 2015; 36 (06) E1-E150
    CrossrefPubMedGoogle Scholar
  • 140 Joshi N, Chan JL. Female genomics: infertility and overall health. Semin Reprod Med 2017; 35 (03) 217-224
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 141 Zondervan KT, Rahmioglu N, Morris AP. et al. Beyond endometriosis genome-wide association study: from genomics to phenomics to the patient. Semin Reprod Med 2016; 34 (04) 242-254
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 142 Gallagher CS, Mäkinen N, Harris HR. et al; 23andMe Research Team. Genome-wide association and epidemiological analyses reveal common genetic origins between uterine leiomyomata and endometriosis. Nat Commun 2019; 10 (01) 4857
    CrossrefPubMedGoogle Scholar
  • 143 Barban N, Jansen R, de Vlaming R. et al; BIOS Consortium, LifeLines Cohort Study. Genome-wide analysis identifies 12 loci influencing human reproductive behavior. Nat Genet 2016; 48 (12) 1462-1472
    CrossrefPubMedGoogle Scholar
  • 144 Lash TL, Fox MP, Fink AK. Applying Quantitative Bias Analysis to Epidemiologic Data. New York, NY: Springer Science + Business Media, LLC; 2009
    CrossrefGoogle Scholar
  • 145 Lash TL, Fox MP, MacLehose RF, Maldonado G, McCandless LC, Greenland S. Good practices for quantitative bias analysis. Int J Epidemiol 2014; 43 (06) 1969-1985
    CrossrefPubMedGoogle Scholar
  • 146 Centers for Disease Control and Prevention (CDC) National Center for Health Statistics. International Classification of Diseases, Ninth Revision (ICD-9). Available at: https://www.cdc.gov/nchs/icd/icd9.htm. Accessed July 2, 2020
    PubMedGoogle Scholar
  • 147 World Health Organization. International Classification of Diseases, 11th Revision for Mortality and Morbidity Statistics. 2018 . Available at: https://www.who.int/classifications/icd/en/. Accessed July 2, 2020
    PubMedGoogle Scholar
  • 148 Greenland S, Senn SJ, Rothman KJ. et al. Statistical tests, P values, confidence intervals, and power: a guide to misinterpretations. Eur J Epidemiol 2016; 31 (04) 337-350
    CrossrefPubMedGoogle Scholar
  • 149 Schmidt M, Rothman KJ. Mistaken inference caused by reliance on and misinterpretation of a significance test. Int J Cardiol 2014; 177 (03) 1089-1090
    CrossrefPubMedGoogle Scholar
  • 150 Greenland S, Pearl J, Robins JM. Causal diagrams for epidemiologic research. Epidemiology 1999; 10 (01) 37-48
    CrossrefPubMedGoogle Scholar
  • 151 Hernán MA, Hernández-Díaz S, Werler MM, Mitchell AA. Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Am J Epidemiol 2002; 155 (02) 176-184
    CrossrefPubMedGoogle Scholar
  • 152 White E, Armstrong BK, Saracci R. Principles of Exposure Measurement in Epidemiology: Collecting, Evaluating, and Improving Measures of Disease Risk Factors. 2nd ed. New York: Oxford University Press; 2008
    CrossrefGoogle Scholar
  • 153 Vandenbroucke JP, von Elm E, Altman DG. et al; STROBE Initiative. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Epidemiology 2007; 18 (06) 805-835
    CrossrefPubMedGoogle Scholar