{"paper_id":"96948c26-cb7e-466f-9c04-95c080da4920","body_text":"ORIGINAL ARTICLE\nPatients with adenomyosis are more likely\nto have deep endometriosis\nMidgley Gonzales & Leandro Accardo de Matos &\nManoel Orlando da Costa Gonçalves &\nRoberto Blasbalg & João Antônio Dias Junior &\nSérgio Podgaec & Edmund Chada Baracat &\nMaurício Simões Abrão\nReceived: 14 March 2012 / Accepted: 10 April 2012 / Published online: 3 May 2012\n# Springer-V erlag 2012\nAbstract This study seeks to analyze the association be-\ntween adenomyosis diagnosed by magnetic resonance im-\naging (MRI) and endometriosis. This is a prospective study\nof consecutive patients. One hundred fifty-two patients with\nhistologically confirmed endometriosis. Patients were sub-\nmitted to MRI, then divided into Group A (with adenomyo-\nsis) and Group B (without adenomyosis). Thickness of the\njunctional zone and the presence of intramyometrial cysts\nwere the principal criteria for diagnosis of adenomyosis.\nMRI data were correlated with clinical status, staging, sites\naffected, and histological classification of endometriosis.\nThe prevalence of adenomyosis in endometriosis patients\nwas 42.76 %. Patients with endometriosis and adenomyosis\nwere more likely than those without adenomyosis to report\nsevere or incapacitating dysmenorrhea (61.53 % in Group\nA; 44.83 % in Group B; p00.041) and deep dyspareunia\n(64.61 % in Group A; 41.38 % in Group B; p00.005), to\nhave stage IV endometriosis (50.77 % in Group A; 33.34 %\nin Group B; p00.03), to have endometriosis of the rectosig-\nmoid (49.23 % in Group A; 32.18 % in Group B; p00.033),\nand to have undifferentiated or mixed histological types of\nendometriosis (52.31 % in Group A; 34.48 % in Group B;\np00.028). A correlation was found between adenomyosis\nand deep endometriosis with poorer prognosis, particularly\nendometriosis of the rectosigmoid.\nKeywords Endometriosis . Adenomyosis . Magnetic\nresonance imaging\nIntroduction\nAdenomyosis is a gynecological disease characterized by\nthe presence of endometrial glands and stroma in the myo-\nmetrium, generally covered by smooth muscle hyperplasia\n[1–3]. Its prevalence is unclear, ranging from 15 % to 20 %\n[4–6] and reaching coefficients of up to 90 % when infertile\npatients are taken into consideration [ 7]. Classically, the\ndiagnosis of adenomyosis was based on histology [ 1, 2].\nMorphometric studies show that the myocytes of the sub-\nendometrial layer are characterized by a nuclear increase, a\nreduction in the extracellular matrix and in water volume\ncompared with cells located in the external layer of the\nmyometrium [ 8]. These cell differences observed in the\nsubendometrial myocytes and around foci of adenomyosis\npermit identification of the junctional zone and poorly de-\nfined low density areas of the myometrium on T2-weighted\nmagnetic resonance imaging (MRI) sequences [ 8].\nThe presence of endometrial components in the myome-\ntrium may be expressed by an increase in the thickness of\nthe junctional zone on MRI [ 9]. Most authors agree that a\njunctional zone thickness ≥12 mm is indicative of a uterus\nwith adenomyosis [ 5, 10, 11]. The presence of areas of low\nintensity and poorly defined borders surrounding points of\nM. Gonzales : J. A. Dias Junior : S. Podgaec : E. C. Baracat :\nM. S. Abrão ( *)\nDepartment of Obstetrics and Gynecology,\nUniversity of São Paulo Medical School,\nRua São Sebastião 550,\n04708-001 São Paulo, São Paulo, Brazil\ne-mail: msabrao@mac.com\nL. A. de Matos\n: M. O. da Costa Gonçalves\nDigimagem Diagnósticos,\nSão Paulo, Brazil\nR. Blasbalg\nDepartment of Radiology,\nUniversity of São Paulo Medical School,\nSão Paulo, Brazil\nGynecol Surg (2012) 9:259 –264\nDOI 10.1007/s10397-012-0746-4\n\nhigh signal intensity on T2-weighted sequences may repre-\nsent a second criterion for diagnosis [ 5, 11–15], constituting\nwhat are referred to as intramyometrial cysts [ 5].\nTransvaginal ultrasound is the natural first choice of\nimage modality when investigating pelvic pain and endo-\nmetriosis (including deep lesions) [ 16, 17]. MRI represents\nan accurate method for the detection of adenomyosis, sen-\nsitivity, and specificity varying from 86 % to 100 % [ 5, 14,\n18–22], making this a highly effective tool for the diagnosis\nof this disease [ 14].\nThere is a multitude of theories with respect to the asso-\nciation between adenomyosis and endometriosis; however,\nother investigators consider them to be two distinct entities\n[23, 24]. No studies have yet been performed to correlate the\ntwo diseases from a diagnostic point of view, taking into\nconsideration the relationship between the ectopic implan-\ntation of glands and endometrial stroma in the myometrium,\nand the sites of implantation and the severity of the foci of\nendometriosis. Therefore, the objective of the present study\nwas to evaluate the prevalence of adenomyosis in patients\nwith endometriosis and to verify the association of a diag-\nnosis of adenomyosis according to MRI and the following\nparameters of endometriosis: clinical status, staging [ 25],\nthe presence of undifferentiation according to histological\nclassification [ 26] and the sites affected by the disease\n(peritoneum, ovary, or deep endometriosis).\nMethods\nA total of 170 patients consecutively attending the Endo-\nmetriosis Clinic of the Teaching Hospital of the School of\nMedicine, University of São Paulo between February 2004\nand October 2008 with an indication for videolaparoscopy\nbased on clinical history, physical examination, pelvic\nechography, and MRI were evaluated according to the pro-\ntocol used in cases of patients with a clinical suspicion of\nendometriosis.\nIn accordance with MRI, the patients were divided into\ntwo groups: Group A in which MRI findings were indicative\nof adenomyosis and Group B in which there were no signs\nindicative of adenomyosis.\nFollowing surgery, 18 patients were excluded because\nthey did not present endometriosis at laparoscopy and/or\nhistological examination. According to the objectives of\nour study, to describe the MRI findings in patients with\nendometriosis, we decided to exclude these patients. The\nfollowing inclusion criteria were applied to patients in\nGroup A: age 20 –45 years, histologically confirmed endo-\nmetriosis, and MRI findings compatible with a diagnosis of\nadenomyosis. In addition, the patient should not have been\nin use of hormones in the 3 months preceding videolaparo-\nscopy (including GnRH analogs, progestogens, and\nhormonal contraceptives) and should have no contraindica-\ntions to undergoing MRI. For Group B, the same inclusion\ncriteria were applied as for Group A; however, MRI findings\nfor patients in this group had to indicate an absence of\nadenomyosis. The study was approved by the institution ’s\nInternal Review Board and all the patients read and signed\nan informed consent form.\nWith respect to the clinical status of endometriosis, the\npresence of acyclic pelvic pain, dysmenorrheal, and dyspareu-\nnia was recorded, as described by the patients with the use of a\nvisual analog scale. Cyclic bowel and urinary abnormalities\n(during menstruation) and infertility status were also recorded.\nIn these patients, endometriosis was classified during\nlaparoscopy as stages I to IV in accordance with the criteria\ndefined by the American Society for Reproductive Medicine\n(ASRM), 1996 revision [ 25].\nThe most important site affected by endometriosis was\ndefined in accordance with the severity of the disease in the\naffected organ. Three categories were established: peritoneal\nendometriosis, ovarian endometriosis, and deep endometri-\nosis (lesions with a depth>5 mm), which included retrocer-\nvical and bowel lesions as well as lesions of the ureter,\nbladder, and vagina.\nTissue was analyzed histologically in accordance with\nthe classification patterns proposed by Abrão et al. [ 26]:\nstromal,\nwell-differentiated glandular, undifferentiated glan-\ndular, or mixed differentiation glandular (presence of epi-\nthelia with well-differentiated and undifferentiated patterns\nat the same site). To facilitate analysis, differential was\ndefined as the presence or absence of endometriosis with\nan undifferentiated histological pattern, since this is the\nhistological type with the poorest prognosis [ 26].\nAll pelvic MRI exams were performed using a 1.5 Tesla\nGE Signa scanner (General Electric Medical Systems, Mil-\nwaukee, WI) or a 1.5 Tesla Philips scanner with an 8-\nchannel torso coil or cardiac coil for signal reception and\ntransmission. All the patients had fasted for 4 h prior to the\nexam and were placed in the dorsal decubitus position with\ntheir arms raised above their heads. V aginal gel was used\nwhen no contraindications were present. Gadolinium con-\ntrast medium (10 –20 ml) was manually injected intrave-\nnously at a speed of approximately 2.0 ml/s.\nMorphology of the junctional zone, a subendometrial\nregion of low signal intensity, was evaluated on T1- (axial\nplane) and T2-weighted sequences (axial, sagittal and coro-\nnal planes). T1-weighted sequences were used to detect\nhemorrhagic foci in the junctional zone and in the myome-\ntrium. The other morphological alterations were observed in\nthe T2-weighted sequences.\nTo determine a diagnosis of adenomyosis by pelvic MRI,\nthe following criteria were taken into consideration [ 5, 9]:\nfocal or diffuse thickening of the junctional zone ≥12 mm;\nthe presence of intramyometrial cysts, which consists of a\n260 Gynecol Surg (2012) 9:259 –264\n\nhigh signal area of the myometrium surrounded by an area\nof low intensity signal with poorly defined borders on T2-\nweighted sequences.\nCategorical variables were analyzed using the chi-square\ntest. Fisher ’s exact test was used whenever the distribution\nof the variable under analysis rendered the chi-square test\ninviable. The continuous quantitative variables were com-\npared using Student ’s t test. All statistical analyses were\nperformed using the SPSS sta tistical software program\n(SPSS Inc., USA), adopting a significance level of 5 %.\nResults\nA total of 152 women with endometriosis (diagnosed by\nhistopathology following videolaparoscopy) were analyzed,\n65 (42.8 %) of whom were found to have adenomyosis on\npelvic MRI (Group A), while 87 (56.2 %) did not (Group\nB). The clinical and epidemiological characteristics of the\nstudy participants are shown in Table 1.\nAn association was found between a diagnosis of adeno-\nmyosis (Group A) and a greater likelihood of dysmenorrhea\n(severe or incapacitating) and deep dyspareunia. No differ-\nences were found between the two groups with respect to\nany of the other symptoms and there were no differences in\nfindings detected at physical examination.\nWhen the staging of endometriosis obtained during video-\nlaparoscopy in the 152 patients was compared between the\ntwo study groups, a relationship was found between adeno-\nmyosis and advanced stages of endometriosis (Table 2). This\nassociation was present when patients with stages III and IV\nwere grouped together and became even more expressive\nwhen the presence of adenomyosis was investigated only in\npatients with stage IV endometriosis. Table 3 shows the dis-\ntribution of the patients with and without adenomyosis\naccording to the site most severely affected by pelvic\nendometriosis.\nIn the evaluation of the histological type of endometriosis\n(Table 4), the presence of undifferentiated or mixed histo-\nlogical patterns of endometriosis in the tissue studied was\nsignificantly more common in the patients with adenomyo-\nsis (Group A; p00.028).\nDiscussion\nGreat advances have been made in the field of diagnosis and\nin the surgical treatment of deep endometriosis. In addition,\nnew aspects are now beginning to be understood within the\nrealm of etiopathogeny. Little is known about adenomyosis.\nThere is an intuitive association with endometriosis. The\ntissues involved, the sites affected, the clinical status all\nconnect these two diseases; however, a more objective con-\nfirmation of this association is required. Evaluating the\ncharacteristics of the two study groups, no differences were\nfound between the two with respect to epidemiological\nparameters. There was a predominance of white patients,\nwhich is in agreement with data published by Arruda et al.\n[27]. The homogeneity found in the present study reinforces\nthe power of this present analysis, since the only difference\nbetween the two groups was the variable under investiga-\ntion: a diagnosis of adenomyosis on MRI.\nThe purpose of using imaging exams to diagnose adeno-\nmyosis is to study the disease in patients in whom hyster-\nectomy is not indicated. This became feasible and MRI is\nTable 1 Epidemiological and clinical characteristics of the patients in\nGroup A (with adenomyosis) compared to the patients in Group B\n(without adenomyosis)\nGroup A\n(N065)\nGroup B\n(N087)\np value\nSkin color\nY ellow 4 (6.15 %) 8 (9.19 %)\nWhite 47 (72.30 %) 58 (66.67 %)\nBlack 14 (21.55 %) 21 (24.14 %) 0.699\nPregnancies\n0 41 (63.10 %) 56 (64.37 %)\n1 20 (30.77 %) 26 (29.88 %)\n2 4 (6.15 %) 4 (4.60 %) 0.717\nMean age 33.43 32.82 0.474\nClinical data\nDysmenorrhea 40 (61.53 %) 39 (44.83 %) 0.041*\nAcyclic pelvic\npain\n22 (33.85 %) 19 (21.84 %) 0.099\nDyspareunia 42 (64.61 %) 36 (41.38 %) 0.005\nInfertility 31 (47.69 %) 41 (47.13 %) 0.945\nCyclic bowel\nsymptoms\n32 (49.23 %) 32 (36.78 %) 0.124\nCyclic urinary\nsymptoms\n3 (4.61 %) 7 (8.04 %) 0.517\n*p<0.05\nTable 2 Evaluation of the patients in Group A (with adenomyosis)\ncompared with the patients in Group B (without adenomyosis), accord-\ning to the stage of endometriosis (ASRM, 1996)\nStage Group A ( N065) Group B ( N087) p value\nI 9 (13.85 %) 26 (29.87 %) 0.020*\nII 14 (21.54 %) 19 (21.84 %) 0.965\nI/II 23 (35.38 %) 45 (51.72 %) 0.045*\nIII 9 (13.85 %) 13 (14.49 %) 0.849\nIV 33 (50.77 %) 29 (33.34 %) 0.030*\nIII/IV 42 (64.61 %) 42 (48.27 %) 0.045*\n*p<0.05\nGynecol Surg (2012) 9:259 –264 261\n\ncurrently considered to be a highly accurate tool for the\ndiagnosis of this pathology [ 7, 11, 12, 14, 28]. The radio-\nlogical criteria selected in the present study for the diagnosis\nof adenomyosis were those most generally accepted in the\nliterature: thickness of the junctional zone ≥12 mm and the\npresence of intramyometrial cysts, regions of hyperintense\nsignals surrounded by an area of low intensity signals and\npoorly defined borders on T2-weighted sequences [ 5, 14,\n19–21]. In the 152 patients with a diagnosis of endometri-\nosis in the present study, critical analysis of their MRI scans\nrevealed that 65 patients (42.8 %) had a diagnosis of adeno-\nmyosis. The coefficient depends to a great extent on the\ncharacteristics, principally the clinical characteristics of the\nstudy population [ 1, 29].\nThe prevalence of adenomyosis in patients with endome-\ntriosis has been evaluated in few studies. Bazot et al. [ 30]\nreported a prevalence of adenomyosis of 27 % in patients\nwith endometriosis. On the other hand, Kunz et al. [7 ]\nreported a prevalence of 79 %, which increased to 90 %\nwhen adenomyosis was diagnosed in patients with endome-\ntriosis and female infertility. Moreover, Larsen et al. [ 31]\nfound that in 34.6 % of patients with endometriosis had\nadenomyosis compared to 19.4 % in the control patients.\nIn a recent study published by Dai et al. [ 32], adenomyosis\nwas diagnosed in 15.8 % of patients presenting deep endo-\nmetriosis and it was significantly higher than in patients\nwithout deep endometriosis.\nParker et al. [ 28] evaluated chronic pelvic pain in women\nwith endometriosis and reported a prevalence of adenomyo-\nsis, as diagnosed by MRI, of 40 %. In the present study, the\npatients were symptomatic with respect to endometriosis,\nmeeting the criteria for an indication for videolaparoscopy.\nTherefore, the 42.8 % prevalence of adenomyosis in endo-\nmetriosis patients that was found in this study would appear\nto be compatible with the data in the literature considering\nthe characteristics of the study population. Furthermore,\nthere were statistically more cases of severe or incapacitat-\ning dysmenorrhea and deep dyspareunia in the group of\npatients with adenomyosis compared to the group with a\ndiagnosis of endometriosis alone. It is comprehensible that\ndysmenorrhea would be more severe in this group bearing in\nmind the factors triggered by the combination of these two\npathologies. Dyspareunia was more intense in patients of\nGroup A, probably as a result of the associated deep endo-\nmetriotic lesions, since the severity of symptoms is directly\nassociated with the depth of the lesions [ 33–35]. Therefore,\nas has been shown in cases of endometriosis in which there\nis a significant correlation between deep dyspareunia and\nretrocervical endometriotic lesions [ 36], the severity of the\nsymptoms in adenomyosis also correlates with the extension\nand depth of the myometrial invasion of the lesion [ 37, 38].\nWith respect to the endometriosis staging classification\nsystem proposed by the ASRM in 1985 and revised in 1996\n[25], adenomyosis was found to be associated with more\nadvanced stages of endometriosis, particularly stage IV of\nthe disease. These data are in agreement with a study pub-\nlished by Kunz et al. [ 7] in which these authors correlated\nmoderate and severe endometriosis with a junctional zone\nthickness of 12.4 mm (adenomyosis), with p00.02. The\nstage IV was also found among women with severe endo-\nmetriosis, 42.8 % had adenomyosis, with deeper wall inva-\nsion, compared to 29.4 % in the women with other stages of\nendometriosis [ 31].\nConsidering the site affected by endometriosis and its\nassociation with adenomyosis , a\n greater association was\nfound between adenomyosis and cases of deep retrocervical\nendometriosis (60 %; p00.01) and those in which endome-\ntriosis was affecting the rectosigmoid (49.2 %; p00.03).\nParker et al. [ 28] also suggested an association between\nadenomyosis and deep endometriosis; however, these\nauthors emphasized that due to the small sample size in\ntheir study, it was impossible to correlate the data with the\nstage of endometriosis.\nWith respect to the histological classification of the\ndisease [ 26], there was a significantly greater incidence of\nundifferentiated endometriosis, either in the pure or mixed\nform, in the group of patients with adenomyosis compared\nTable 3 Evaluation of the patients in Group A (with adenomyosis) in\nrelation to the patients in Group B (without adenomyosis), according to\nthe site of the endometriotic lesion\nSite Group A ( N065) Group B ( N087) p value\nPeritoneal 26 (40 %) 49 (56.32 %) 0.046*\nOvarian 42 (64.61 %) 45 (51.72 %) 0.112\nDeep\nRetrocervical 39 (60 %) 34 (39.08 %) 0.011*\nV agina 5 (7.69 %) 4 (4.60 %) 0.498\nBladder 6 (9.23 %) 8 (9.19 %) 0.994\nUreter 6 (9.23 %) 3 (3.45 %) 0.172\nRectosigmoid 32 (49.23 %) 28 (32.18 %) 0.033*\n*p<0.05\nTable 4 Evaluation of the patients in Group A (with adenomyosis) in\nrelation to the patients in Group B (without adenomyosis), according to\nthe presence of undifferentiated histological pattern in the endometri-\notic lesion\nHistology Group A\n(N065)\nGroup B\n(N087)\nWell-differentiated glandular or\nstromal disease\n31 (47.69 %) 57 (65.52 %)\nUndifferentiated glandular or mixed\ndisease\n34 (52.31 %) 30 (34.48 %)\np00.028\n262 Gynecol Surg (2012) 9:259 –264\n\nto the group of patients with endometriosis alone ( p00.028).\nThese data are compatible with the finding that patients with\nundifferentiated endometriosis have more severe forms of\nendometriosis [ 26, 39].\nThese findings confirm previous data correlating adeno-\nmyosis with deep endometriosis (principally bowel endo-\nmetriosis) and with advanced stages of the disease [ 25]. An\nassociation was therefore established between adenomyosis\nand cases of endometriosis with poor prognosis.\nDespite the lack of studies in which patients with endo-\nmetriosis were analyzed according to the present format,\nparticularly correlating endometriosis with adenomyosis, it\nis worth mentioning the publication of Landi et al. [ 11], who\nreported poorer prognosis in patients with concurrent adeno-\nmyosis and endometriosis. However, they did not establish\nany satisfactory association with staging or the site of foci of\nendometriosis. Peritoneal lesions present as epithelial glands\ncovered with endometrial-type stroma. This feature is absent\nin deep lesions that involve smooth muscle tissue [ 40, 41]\nsimilar to adenomyosis lesions. In the present study, an\nassociation was found between adenomyosis and deep en-\ndometriosis. It should be emphasized that it is the deep\nrather than the superficial endometriotic foci that resemble\nthose found in adenomyosis [ 42].\nWhen the three different forms of endometriosis, perito-\nneal, ovarian, and that affecting the rectovaginal septum\nwere defined, Nisolle and Donnez [ 43] attributed different\netiopathogenies to the peritoneal form of the disease\n(implants resulting from retrograde menstruation) and to the\ndeep lesions, said to correspond to an adenomyotic nodule\noriginating from Müllerian remnants by means of metaplasia\n[40, 41, 44]. These resemble an adenomyoma, an accumula-\ntion of smooth muscle tissue and endometrial glands with\nscarce stroma [40, 41, 44]. Well-grounded studies have shown\nthat the nodules of deep retrocervical, and bowel endometri-\nosis are not the result of deep infiltrative endometriosis but are\nsimilar to the nodules of adenomyosis that develop from\nMüllerian remnants by metaplasia [40, 41, 44].\nAs deep endometriosis, adenomyosis has also been\nexplained [ 4, 45] as a condition originating from Müllerian\nremnants by metaplasia. These authors presume that there\nare transitional quiescent Müllerian elements between the\nendometrium and the myometrium that would have the\ncapacity to develop by metaplasia.\nThe close association found in this study between adeno-\nmyosis and deep endometriosis, associated with advanced\nstages and pure or mixed undifferentiated histological pat-\nterns, permits some common theories to be expounded on\nthe genesis of endometriosis and that of adenomyosis.\nAccording to the present findings, adenomyosis may be inter-\npreted as a marker for deep endometriosis. 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