Superficial Peritoneal Endometriosis: Clinical Characteristics of 203 Confirmed Cases and 1292 Endometriosis-Free Controls

The aim of this study was to characterize a large sample of women with superficial peritoneal endometriosis (SUP) and no other types of endometriosis in order to test the association of SUP with gynecologic symptoms. We included 203 cases of histologically proven SUP and 1292 endometriosis-free controls diagnosed between January 2004 and July 2017. The participants were non-pregnant patients aged 18 to 42 years submitted to a laparoscopy or laparotomy for a benign gynecologic condition. We excluded all cases of ovarian endometrioma, deep infiltrating endometriosis, and women who had previously undergone an endometriosis surgery. All patients underwent face-to-face interviews, thorough preoperative physical examination, and transvaginal ultrasound. Pain severity was assessed preoperatively through an 11-point numerical rating scale. The association of SUP with gynecologic symptoms was adjusted for potential confounders using multivariable logistic regression. The presence of SUP was associated with lower body weight (59.8 vs. 63.5 kg) and body mass index (21.8 vs. 23.3 kg/m2), and a higher frequency of smoking habit (41.6% vs. 32.8%) and of positive familial history of endometriosis (7.0% vs. 2.3%). Moreover, SUP was associated with an increased risk of primary infertility (adjusted prevalence ratio [PR] 1.83, 95% confidence interval [CI] 1.46–2.24), moderate to intense dysmenorrhea (PR 1.43, 95% CI 1.31–1.52), and moderate to intense deep dyspareunia (PR 1.50, 95% CI 1.25–1.75). In conclusion, in this large surgical series, isolated SUP was independently associated to primary infertility and moderate to severe painful symptoms. Similar content being viewed by others

Chapron C, Tosti C, Marcellin L, et al. Relationship between the magnetic resonance imaging appearance of adenomyosis and endometriosis phenotypes. Hum Reprod. 2017;32:1393–401. Vercellini P, Giudice LC, Evers JL, Abrao MS. Reducing low-value care in endometriosis between limited evidence and unresolved issues: a proposal. Hum Reprod. 2015;30:1996–2004. Akande VA, Hunt LP, Cahill DJ, Jenkins JM. Differences in time to natural conception between women with unexplained infertility and infertile women with minor endometriosis. Hum Reprod. 2004;19:96–103. Schliep KC, Mumford SL, Peterson CM, Chen Z, Johnstone EB, Sharp HT, et al. Pain typology and incident endometriosis. Hum Reprod. 2015;30:2427–38. Chapron C, Fauconnier A, Dubuisson JB, Barakat H, Vieira M, Breart G. Deep infiltrating endometriosis: relation between severity of dysmenorrhoea and extent of disease. Hum Reprod. 2003;18:760–6. Griffiths AN, Koutsouridou RN, Penketh RJ. Rectovaginal endometriosis -- a frequently missed diagnosis. J Obstet Gynaecol. 2007;27:605–7. Santulli P, Lamau MC, Marcellin L, Gayet V, Marzouk P, Borghese B, et al. Endometriosis-related infertility: ovarian endometrioma per se is not associated with presentation for infertility. Hum Reprod. 2016;31:1765–75. Chapron C, Santulli P, de Ziegler D, Noel JC, Anaf V, Streuli I, et al. Ovarian endometrioma: severe pelvic pain is associated with deeply infiltrating endometriosis. Hum Reprod. 2012;27:702–11. Allaire C, Williams C, Bodmer-Roy S, et al. Chronic pelvic pain in an interdisciplinary setting: 1-year prospective cohort. Am J Obstet Gynecol. 2018;218:114.e1–e12. Abrao MS, Goncalves MO, Dias JA Jr, Podgaec S, Chamie LP, Blasbalg R. Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis. Hum Reprod. 2007;22:3092–7. Piketty M, Chopin N, Dousset B, Millischer-Bellaische AE, Roseau G, Leconte M, et al. Preoperative work-up for patients with deeply infiltrating endometriosis: transvaginal ultrasonography must definitely be the first-line imaging examination. Hum Reprod. 2009;24:602–7. Johnson NP, Hummelshoj L, Adamson GD, Keckstein J, Taylor HS, Abrao MS, et al. World Endometriosis Society consensus on the classification of endometriosis. Hum Reprod. 2017;32:315–24. Schmidt CO, Kohlmann T. When to use the odds ratio or the relative risk? Int J Public Health. 2008;53:165–7. Machin D, Campbell M, Fayers P, Pinol A. Sample size tables for clinical studies. 2nd Edition ed.: Blackwell Science, 1997. Tanbo T, Fedorcsak P. Endometriosis-associated infertility: aspects of pathophysiological mechanisms and treatment options. Acta Obstet Gynecol Scand. 2017;96:659–67. Bernardi M, Lazzeri L, Perelli F, Reis FM, Petraglia F. Dysmenorrhea and related disorders. F1000Res. 2017; 6: 1645. Chiantera V, Abesadze E, Mechsner S. How to understand the complexity of endometriosis-related pain. Journal of Endometriosis and Pelvic Pain Disorders. 2017;9:30–8. Morotti M, Vincent K, Becker CM. Mechanisms of pain in endometriosis. Eur J Obstet Gynecol Reprod Biol. 2017;209:8–13. Tsigkou A, Reis FM, Ciarmela P, Lee MH, Jiang B, Tosti C, et al. Expression levels of myostatin and matrix metalloproteinase 14 mRNAs in uterine leiomyoma are correlated with dysmenorrhea. Reprod Sci. 2015;22:1597–602. Barcena de Arellano ML, Mechsner S. The peritoneum--an important factor for pathogenesis and pain generation in endometriosis. J Mol Med (Berl). 2014;92:595–602. Holdsworth-Carson SJ, Dior UP, Colgrave EM, et al. The association of body mass index with endometriosis and disease severity in women with pain. Journal of Endometriosis and Pelvic Pain Disorders. 2018;2284026518773939. Shah DK, Correia KF, Vitonis AF, Missmer SA. Body size and endometriosis: results from 20 years of follow-up within the Nurses’ Health Study II prospective cohort. Hum Reprod. 2013;28:1783–92. Hoshiai H, Ishikawa M, Sawatari Y, Noda K, Fukaya T. Laparoscopic evaluation of the onset and progression of endometriosis. Am J Obstet Gynecol. 1993;169:714–9. Thomas EJ, Cooke ID. Impact of gestrinone on the course of asymptomatic endometriosis. Br Med J (Clin Res Ed). 1987;294:272–4. Moen MH, Stokstad T. A long-term follow-up study of women with asymptomatic endometriosis diagnosed incidentally at sterilization. Fertil Steril. 2002;78:773–6. Berube S, Marcoux S, Langevin M, Maheux R. Fecundity of infertile women with minimal or mild endometriosis and women with unexplained infertility. The Canadian Collaborative Group on Endometriosis. Fertil Steril. 1998;69:1034–41. Jacobson TZ, Duffy JM, Barlow D, Farquhar C, Koninckx PR, Olive D. Laparoscopic surgery for subfertility associated with endometriosis. Cochrane Database Syst Rev. 2010:CD001398. Jacobson TZ, Duffy JM, Barlow D, Koninckx PR, Garry R. Laparoscopic surgery for pelvic pain associated with endometriosis. Cochrane Database Syst Rev. 2009:CD001300. Funding FMR was a recipient of a scholarship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil, # 201876/2017-5). Author information Authors and Affiliations Corresponding author Ethics declarations We used a prospectively managed database previously approved by the Institutional Review Board and all participants provided informed consent to have their data anonymously used in future research. Conflict of Interest The authors declare that they have no conflict of interest. Electronic Supplementary Material ESM1 (download DOCX ) (DOCX 15 kb) Rights and permissions About this article Cite this article Reis, F.M., Santulli, P., Marcellin, L. et al. Superficial Peritoneal Endometriosis: Clinical Characteristics of 203 Confirmed Cases and 1292 Endometriosis-Free Controls. Reprod. Sci. 27, 309–315 (2020). https://doi.org/10.1007/s43032-019-00028-1 Received: Accepted: Published: Version of record: Issue date: DOI: https://doi.org/10.1007/s43032-019-00028-1