Adenomyosis represents abnormal proliferation of stroma and endometrial glands within the myometrium, and, is associated with myometrial hypertrophy and hyperplasia1. With a growing trend of women delaying conception, the incidence of adenomyosis in subfertile and infertile women, as well as those seeking in vitro fertilization (IVF)/intracytoplasmic sperm injection (ICSI) is on the rise. A direct causal relationship between adenomyosis and subfertility or infertility has been proposed in literature; however, no accurate representative data is available due to the lack of randomized surgical trials. In a meta-analysis, Vercellini and colleagues reported that women with adenomyosis had a 28% reduction in the likelihood of clinical pregnancy at IVF/ICSI when compared with women without adenomyosis. The impact of adenomyosis on IVF/ICSI is primarily 2-fold, and is related to the reduced probability of conception as well as the potential increased risk of miscarriage. In such a scenario, screening for adenomyosis in subfertile or infertile patients potentially earmarked for IVF/ICSI procedures would be advisable2–4. With rapid advances in the field of imaging technology, transabdominal and transvaginal ultrasonography (USG) as well as magnetic resonance imaging (MRI) are routinely used as noninvasive screening tests in clinical practice to diagnose adenomyosis. Transabdominal and transvaginal USG are the first-line imaging investigations, however, as these are highly operator dependent, with significant intraobserver and interobserver variability in the findings, high resolution pelvic MRI is considered the current reference standard for noninvasive imaging of pelvic structures due to its multiplanar capabilities, excellent soft tissue resolution, repeatability, and reproducibility. In addition to detecting adenomyosis, MRI frequently helps determine its associations such as pelvic endometriosis and its complications such as frozen pelvis, or differentiate it from mimics such as leiomyomas, endometrial polyps or myometrial contraction. In this study, our principal objective was to assess the impact of high-resolution MRI to detect the subtle nuances of uterine adenomyosis and its associations, and, identify its key mimics prevailing in a subset of subfertile or infertile women, and create a structured reporting template which will contain standardized lexicon as well as comprehensive and accurate information.
Materials and methods
This is a retrospective HIPPA compliant study. Inclusion criteria consisted of (a) clinically diagnosed cases of primary infertility; (b) suspicion of adenomyosis on transabdominal and transvaginal USG; (c) nonvisualization/obscuration of the junctional zone; (d) multiparametric MRI performed at 3 T. Exclusion criteria included (a) other causes of primary infertility including Mullerian ductal anomalies, ovulation factors, and, hormonal factors such as hypothalamic-pituitary axis abnormalities; (b) secondary infertility. We searched our database and identified a cohort of 114 patients who underwent unenhanced multiparametric MRI of the pelvis on a 3 T system between July 2011 and March 2017 at our institution to rule out adenomyosis as a cause of primary infertility.
Patients were scanned on a 3 T MRI system (Magnetom Skyra, Siemens Healthcare) using a phased-array body coil. The scan protocol included the following sequences: T2-weighted (T2W) turbo spin-echo (TSE) in the sagittal [repetition time (TR)/echo time (TE)=4100/84 s; slice thickness=3 mm, interslice gap=0.3 mm; number of excitations (NEX)=2; field of view (FOV)=200×200; matrix=307×384; parallel imaging factor=2], coronal (TR/TE=3700/86 s; slice thickness=3 mm, interslice gap=0.3 mm; NEX=2; FOV=200×200; matrix=307×384; parallel imaging factor=2), and axial (TR/TE=4100/94 s; slice thickness=3 mm, interslice gap=0.6 mm; NEX=3; FOV=200×200; matrix=307×384; parallel imaging factor=2) planes; T1-weighted (T1W) TSE in the axial plane (TR/TE=550/10 s; slice thickness=3 mm, interslice gap=0.6 mm; NEX=2; FOV=200×200; matrix=224×320; parallel imaging factor=2); axial single-shot echo-planar diffusion-weighted (TR/TE=5600/61; slice thickness=5 mm; interslice gap=0.5 mm; FOV=380×380 mm; matrix=113×192; parallel imaging factor=2; NEX=2; b-values=0, 50, 700, and 1400 s/mm2) and an inline reconstruction of the ADC map; T1W fat suppressed TSE in the axial plane (TR/TE=550/10 s; slice thickness=3 mm, interslice gap=0.6 mm; NEX=2; FOV=200×200; matrix=224×320; parallel imaging factor=2); 3-dimensional T1W fat suppressed gradient echo sagittal plane (TR/TE=3.97/1.93 s; slice thickness=2 mm, interslice gap=0.4 mm; NEX=2; FOV=350×260; matrix=169×320; parallel imaging factor=2).
All examinations were transferred and interpreted on an advanced Syngo Via VB10 workstation (Siemens Healthcare), and the images were reviewed independently by a specialist in pelvic imaging.
Of a cohort of 114 patients, 38 patients were diagnosed with adenomyosis, with focal adenomyosis in 20 patients, and diffuse adenomyosis in 18 patients. Isolated adenomyosis was seen in 10 patients. A total of 28 patients had adenomyosis in combination with other pathologies (8 patients had fibroids, 3 patients had pelvic endometriosis, 7 patients had pelvic endometriosis and ovarian endometrioma, 1 patient had ovarian endometrioma, 1 patient had hematosalpinx, and 5 patients had fibroids, pelvic endometriosis, and ovarian endometrioma). Of the remaining 76 patients, 45 patients had fibroids, 12 patients had isolated junctional zone thickening without dilated endometrial glands or an indistinct interface with the outer myometrium, 1 patient had myometrial contraction which mimicked focal adenomyosis, and 18 patients had no uterine or pelvic abnormalities.
Adenomyosis was a terminology first described in modern literature in 1972, and, referred to the abnormal presence of ectopic endometrial glands and stroma deep within the myometrium, associated with secondary hypertrophy and hyperplasia of the uterine smooth muscle which results in a mildly enlarged globular and dysmorphic uterine corpus that is rarely twice the normal size5–7. The most widespread and accepted hypothesis is the abnormal invagination of the basal layer of the endometrium into the myometrium. Alternative hypotheses include abnormal migration of the basal layer of the endometrium along the intramyometrial lymphatic channels or the presence of ectopic intramyomterial endometrial tissue which initiates a de novo metaplastic process in the uterine wall8,9. The intramural endometrial glands generally have the same histologic appearance as the basal layer of the endometrium, are responsive to endogenous estrogen stimulation, and, show proliferative or occasionally cystic patterns, with cellular atypia being an uncommon feature. However, unlike in endometriosis, adenomyosis does not show marked hemorrhagic changes or inflammatory response. Some studies have shown that the myometrium could play a role in the development of adenomyosis as well, which may be secondary to local factors, as noted by the presence of smooth muscle metaplasia, and fibroblast to myofibroblast transdifferentiation9,10. There is a lack of accurate data on the prevalence of adenomyosis in the general gynecologic population, as the majority of published literature comes from histologic analysis of surgical specimens which is most often not available in patients with subfertility or infertility. Vercellini et al11 reported wide variations in the incidence of adenomyosis between racial and ethnic groups and different geographic regions but could not reliably assess whether these were due to patient-related factors or differential diagnostic criteria; however, no randomized controlled study has been performed to assess for any demographic variation in the prevalence and incidence of the disease. Review of published literature shows that the reported prevalence of adenomyosis varies widely between 8% and 62%, and, this is attributable to the usage of different diagnostic criteria. The incidence of adenomyosis begins in mid-30s and peaks in fifth decade1,12. Harada et al13 stated that ∼80% of women diagnosed with adenomyosis are between 40 and 50 years old, whereas only 20% of adenomyosis involves women below the age of 40 years.
Pathology is the current gold standard for the diagnosis of adenomyosis, which can be definitively diagnosed only through histologic sections of the myometrium obtained on hysterectomy specimens. The diagnosis is rarely established on routine curettage as the lesions are usually deep seated and pose a significant challenge to obtain representative tissue sample. Hysterosalpingographic (HSG) findings of adenomyosis are not always diagnostic as similar findings can occur in vascular or lymphatic invasion. USG has the advantages of lower cost and easier availability as compared to MRI, and, hence it has become the first-line noninvasive imaging modality of choice in the evaluation of pelvic disorders such as adenomyosis. Many studies have compared the impact of MRI versus USG in the noninvasive diagnosis of adenomyosis; while some show equivalent results between the 2 modalities, the majority agrees that pelvic MRI is the superior imaging technique. MRI is presently used as a problem solving tool, particularly in cases with equivocal findings on USG or where presence of associated pathologies like fibroids limit detailed and accurate USG assessment. MRI gives an added value after transvaginal ultrasonography diagnosis of adenomyosis in 88% of patients by providing a diagnostic alternative in 33% of cases, otherwise questioning the diagnosis in an additional 11%, and by providing supplementary diagnostic information in another 44%. Overall MRI is considered the reference imaging standard for noninvasive diagnosis of adenomyosis14–18.
First described by Hricak et al19, the junctional zone (Fig. 1) represents the interface between the endometrial lining and the outer myometrium, and, shows considerable variations in thickness throughout the menstrual cycle. The junctional zone may appear physiologically thickened in the initial proliferative phase of the menstrual cycle. During the initial proliferative phase of the cycle, junctional zone thickness between 8 and 12 mm is considered nonspecific, and it is recommended that repeat imaging studies should be performed during the secretory phase of the menstrual cycle to accurately re-assess the junctional zone20. In general to avoid any misinterpretation, MR should be avoided during the initial proliferative phase of the menstrual cycle. If there is a strong clinical suspicion of adenomyosis in the presence of a junctional zone which measures 8–12 mm, one should look for the following key features: (a) difference between the maximum and the minimum thickness of the junctional zone of >5 mm; (b) indistinctness of the borders of the junctional zone with the myometrium; (c) internal heterogeneity in the signal intensity of the junctional zone. Anecdotally, on high-resolution MRI, we may detect focal junctional zone thickening >12 mm, without indistinctness of its margins and the absence of dilated endometrial glands; these findings are of equivocal significance, and, we advocate follow-up imaging at 6–12 months interval as these could represent precursors of definitive adenomyosis. In our study 12 patients were detected with isolated junctional zone thickening without dilated endometrial glands or an indistinct interface with the outer myometrium (Fig. 2). In 2008, Gordt et al’s21 proposed a classification for adenomyosis, which has yet not been validated by further randomised studies, and, includes the following criteria: simple junctional zone hyperplasia (thickness >8 mm but <12 mm on T2W images in women aged 35 y or younger); partial or diffuse adenomyosis (thickness >12 mm; high signal intensity myometrial foci; involvement of the outer myometrium <1/3, <2/3, and >2/3), adenomyoma (myometrial mass with indistinct margins with primarily low signal intensity on all MRI sequences). Though, Novellas et al20 has reported that the junctional zone may not be visible in 20% of premenopausal women, a consensus exists that adenomyosis may be strongly considered with a junctional zone thickness of >12 mm.
Adenomyosis presents as 2 distinctive subtypes including either diffuse thickening of junctional zone (Fig. 3) or as a focal form or adenomyoma (Fig. 4) which presents as a focal ovoid mass often situated in the myometrium with blurring of the junctional zone—myometrial interface. In our study 20 patients were detected with focal adenomyosis and 18 patients had diffuse adenomyosis. The classic MRI findings of adenomyosis (Table 1) include the following: (a) bulky uterus which is usually asymmetrically enlarged with the fundal region and posterior wall being more commonly affected; (b) focal or diffuse thickening of the junctional zone which measures 12 mm or more; (c) low T2 signal intensity areas with indistinct margins representing the infiltrated and thickened myometrium; (d) presence of punctate (round to spherical shape) or tubular T2 high-intensity foci within these areas of abnormal intramyometrial tissue which represent dilated ectopic endometrial glands with few of these glands demonstrating intrasubstance T1 hyperintense foci representing hemorrhage20,22–24.
Adenomyosis is related to both infertility and parity. Numerous studies have reported the relationship between parity and adenomyosis, with the incidence of adenomyosis being higher in multiparous women as compared with nulliparous individuals12,25–30. Review of literature shows that few mechanisms have been proposed linking parity with the development of adenomyosis, and include the following: (a) the invasive nature of the gestational trophoblastic tissue into the myometrium may allow adenomyotic foci (endometrial glands) to gain access to the myometrium; (b) the hormonal environment of the pregnancy may favor formation of ectopic endometrial glands within the uterine myometrium; (c) the iatrogenic development of adenomyosis secondary to implantation of endometrial tissue within the myometrium due to cesarean sections25,31. Other risk factors that have been known to increase the potential risk for the development of adenomyosis include endometrial hyperplasia, spontaneous and recurrent abortions, endometriosis, smoking, and iatrogenic causes such as curettage32. The high estrogen dependency nature of adenomyosis was reported by Bergeron et al8, who reported a high incidence of adenomyosis in 60% of postmenopausal women on long-term Tamoxifen therapy. Adenomyosis is reported to be clinically asymptomatic in one-third of all cases. The most frequent clinical manifestations include menorrhagia, dysmenorrhea, metrorrhagia, and dyspareunia. Munro et al33 reported that menorrhagia and dysmenorrhea may be directly related to the depth of penetration and the density of endometrial glands within the myometrial tissue.
Both adenomyosis and endometriosis are estrogen dependent conditions, which may co-exist in the same individual. In our series, 17 patients had adenomyosis in combination with some form of pelvic endometriosis (3 patients had pelvic endometriosis, 7 patients had pelvic endometriosis and ovarian endometrioma, 1 patient had ovarian endometrioma, 1 patient had hematosalpinx, and 5 patients had a combination of fibroids, pelvic endometriosis, and ovarian endometrioma). Endometriosis is defined as the presence of functioning endometrial tissue in an ectopic location. Different theories have been put forward to explain the pathogenesis of endometriosis; however, no single theory can account for the variable locations of endometriosis34,35. The estimated prevalence of endometriosis in patients with infertility varies between 25% and 50%, whereas about 30%–50% women suffering from endometriosis have infertility. Three distinctive forms of pelvic endometriosis have been described36,37, which include the following: superficial peritoneal, ovarian, and deep pelvic endometriosis. Deep pelvic endometriosis is further subcategorized into different types depending on its location37–40 including: (a) anterior compartment; (b) middle compartment; (c) posterior compartment. The gold standard for diagnosis of endometriosis is a combination of laparoscopy followed by histopathologic confirmation of ectopic endometrial glandular/stromal tissue. In 2012, the Practice Committee of the American Society for Reproductive Medicine no longer recommended performing laparoscopy on asymptomatic women with infertility to check for endometriosis. Hudelist et al41 in their study have shown that usual median period for diagnosis of endometriosis is about 10.4 (SD=7.9) years from the first clinical symptomatic presentation. Because of significant overlap of clinical symptoms the patients are often mislabeled. Considering recent advances in USG and MRI, this time lag for the delayed diagnosis is unacceptable especially in symptomatic individuals as it delays definitive treatment. If clinically sufficient information is obtained on transvaginal USG further evaluation by MRI is usually not done. But if the USG findings are indeterminate or there is strong clinical suspicion of retroperitoneal involvement or adhesions, then MRI is the modality of choice. Bazot et al42 reported a sensitivity of 90.3%, specificity of 91%, positive predictive value of 92.1%, negative predictive value of 89%, and an accuracy of 90.8% of 1.5 T MRI in the evaluation of deep pelvic endometriosis. With advent of higher field strengths leading to improved signal-to-noise ratio, there is overall improved diagnostic accuracy for endometriosis. Hottat et al43 reported a sensitivity, specificity, positive and negative predictive values, and accuracy for the diagnosis of deep endometriosis at 3 T MRI of 96.3%, 100%, 100%, 93.3%, and 97.6%, respectively, depending on the location of deep endometriosis. Endometriotic deposits have variable signal characteristics depending upon extent of hemorrhage and fibrosis38. Nonfibrotic deposits can follow signal intensity paralleling the normal endometrium appearing hyperintense on T2W image and hypointense on T1W image sequences. Repeated cyclical hemorrhage and fibrotic changes leads to predominantly hypointense signal both on the T1W and T2W sequences. Occasionally, these lesions may show hyperintense signal intensity on both the T1 and T2W images. Nonfibrotic implants can enhance following the contrast administration; however, this does not add any additional value in the diagnosis due to lack of both sensitivity and specificity of this finding. When affected by endometriosis, the uterosacral ligaments can appear thickened and may produce uterine retraction to the more affected side. The torus uterinus is an area where endometriotic implants are frequently located, and often induces uterine retroflexion along with posterosuperior retraction of the posterior fornix (Fig. 5). Often, a hydrosalpinx/hematosalpinx may be seen in patients with endometriosis, and appear as thick walled tubular or convoluted adnexal structures containing fluid, mucinous or hemorrhagic material39,44. An endometrioma (Fig. 6) is a localized form of endometriosis usually affecting the ovary, with a reported prevalence varying between 17% and 44% in patients with endometriosis. Endometriomas appear as cysts with T1 high signal contents which reveal T2 shading, with or without internal septations or mural based nodules representing retracted blood clots44. Cyst rupture can lead to dense adhesions that makes surgical removal a strenuous task45. The existing literature supports an adverse effect of both superficial endometriosis and ovarian endometriomas on ovulation rates, markers of ovarian reserve, and response to ovarian stimulation46. The imaging differentials of endometriomas include functional hemorrhagic cysts which typically resolve over follow-up imaging in 6–8 weeks in contrast to the endometriomas which show no significant interval regression. Presence of the T2 shading sign is a more classic feature of an endometrioma rather than a hemorrhagic cyst47,48.
In our series, 8 patients had adenomyosis in combination with fibroids. Differentiation between adenomyoma and leiomyoma is essential as the surgical approach varies between both these entities. Leiomyoma (Fig. 7) can be enucleated in contrast to an adenomyoma which requires hysterectomy as a definitive surgical management. Leiomyomas have the following characteristics on high-resolution MRI: (a) well circumscribed masses; (b) round to oval in shape; (c) normal appearing junctional zone; (d) demonstrate prominent peripheral and internal vasculature; (e) Usually appear dark on both T1W/T2W images, except when they demonstrate varying patterns of degeneration; (f) depending on their (submucosal or intramural) location exert mass effect on the endometrial cavity or on the adjacent pelvic structures (intramural or subserosal).
Uterine contractions49 can simulate myometrial masses, with low signal on T2W, mimicking a leiomyoma or focal adenomyoma. The transient nature of myometrial contraction (Fig. 8) is the most helpful criteria to differentiate from the remaining entities, which can be confirmed by cine MRI or obtaining sequential MRI at different time point intervals.
The main strengths of our study include the homogenous subset of infertile/subfertile patients who were all evaluated with MRI scans on a 3 T system based on an index of suspicion for adenomyosis raised on either transabdominal and transvaginal USG. All MRI scans were performed using standardized protocols and the same operator reviewed and reported the images using a standardized reporting template, thus obviating interobserver variation. The main limitation included the absence of histologic confirmation of adenomyosis; however, it is accepted that noninvasive imaging tools such as USG and MRI have reached a very high level of accuracy and concordance with histologic findings, hence obviating the need for histopathological confirmation. This was a retrospective study on a small subset of infertile patients who presented to the IVF clinical unit with a suspicion of adenomyosis on USG. MRI was not performed in every patient who presented to the infertility clinic and was limited only to a subset of patients in whom a pelvic pathology was suspected, and, hence may have led to overestimation of the prevalence of adenomyosis in the overall infertile patient population. In conclusion, our retrospective study, demonstrates the ability of high-resolution MRI at 3 T to detect the subtle nuances of adenomyosis, and, its relationship with pelvic endometriosis.
Source of funding
Conflicts of interest disclosure
The authors declare that they have no financial conflict of interest with regard to the content of this report.
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