Abstract
Objective:
This study aimed to assess the efficacy of MRI for differentiating between uterine submucosal polypoid adenomyomas (PAs) and endometrial polyps (EPs).
Methods:
MRI was used to examine 40 histopathologically confirmed benign polypoid endometrial tumors (8submucosal PAs and 32 EPs). Atypical PAs were excluded from this study. Quantitative measurements (maximum tumor diameter, maximum cyst diameter, number of cysts, and apparent diffusion coefficient values) and qualitative imaging findings (predominance of cystic or solid components as well as presence of cysts, hemorrhage, myometrial invasion, fluid–fluid level, and fibrous core) were correlated with the two pathologies.
Results:
The predominance of cystic components (37% vs 6%; p < 0.05) was more frequently observed in PAs than in EPs. The frequency of cysts (88% vs 25%; p < 0.01), hemorrhage (50% vs 9%; p < 0.05), and myometrial invasion (25% vs 0%; p < 0.05) were significantly higher in PAs than in EPs. No significant differences were observed in terms of the maximum tumor diameter, maximum cyst diameter, number of cysts, apparent diffusion coefficient values, and presence of fluid-fluid level and fibrous core between PAs and EPs.
Conclusion:
The differences of MR findings with emphasis on cystic components and hemorrhage may be useful for differentiating between PAs and EPs.
Advances in knowledge:
The predominance of cystic or solid components and the presence of cysts, hemorrhage, and myometrial invasion were useful MR findings for differentiating between PAs and EPs.
Introduction
Uterine adenomyoma is a benign mixed epithelial and mesenchymal tumor composed of a variable number of endometrial glands and endometrial-type stroma surrounded by smooth muscle.1 They usually manifest as submucosal polypoid masses or less commonly as myometrial or subserosal polypoid masses. Adenomyomas that manifest as polypoid masses protruding either into the endometrial cavity or outside the uterine surface are called polypoid adenomyomas (PAs). Submucosal PAs, which are also referred to as adenomyomatous polyps, typically develop in the lower segment of the uterine corpus but may occasionally develop in the upper corpus or fundus. Submucosal PAs usually occur in pre-menopausal females, and abnormal vaginal bleeding is the most commonly associated symptom.
An endometrial polyp (EP) is defined as a localized, disorganized proliferation of benign glandular and stromal elements that are usually elevated above the surface of the adjacent endometrium.2 EPs are relatively common, i.e. they are observed in up to 25% females worldwide. Although EPs can occur at any age, they are most frequently observed in perimenopausal females. Small EPs may be asymptomatic; however, they most commonly manifest as abnormal bleeding. Furthermore, females receiving hormone replacement therapy (HRT) or tamoxifen are at an increased risk of developing EPs.
Patients with EPs are reportedly at a 0–4.8% risk of developing endometrial cancer depending on the basis of which they are selected and the methods employed for their diagnosis.3 A linear relationship pertaining to the association of EPs with malignancies and increasing age has been observed; in addition, EPs have been reported to show a significantly higher association with malignancies in post-menopausal females.4 In contrast, although malignant transformation of adenomyosis has been well-recognized5 and atypical PAs have been found to have a propensity to malignant transformation,6 there is no evidence that adenomyomas represent pre-malignant lesions or that they are associated with an increased risk of developing a malignancy.7 Therefore, pre-operative differentiation between PAs and EPs is critical for the selection of the optimal therapeutic strategy. Several studies have focused on MR findings of PAs8–10 and EPs.11–13 However, no study has compared MR findings between PAs and EPs. Thus, in the present study, we aimed to assess the efficacy of MRI for differentiating between uterine submucosal PAs and EPs.
methods and Materials
Patients
The present study was approved by the human research committee of the institutional review board of Gifu University Hospital, and complied with the guidelines of the Health Insurance Portability and Accountability Act of 1996. The requirement for informed consent was waived due to the retrospective nature of this study. A search of our hospital’s electronic medical chart system for patients with histopathologically proven typical PAs and EPs between July 2004 and August 2017 yielded 20 submucosal PAs and 172 EPs. Atypical PAs were excluded from this study. Among them, we found 8 submucosal PAs and 45 EPs which underwent pre-operative MRI. Furthermore, 13 EPs were excluded from this study as the condition could not be identified in these patients on MRI because of their small tumor size.
In total, 8 submucosal PAs (8 patients; age range, 42–74 years; median age, 49 years; 4 pre-menopausal, 4 post-menopausal) and 32 EPs (32 patients; age range, 27–76 years; median age, 47 years; 19 pre-menopausal, 13 post-menopausal) were included in this study. In terms of localization, 6 (75%) PAs were located in the corpus and the remaining 2 (25%) in the cervix, whereas 26 (81%) EPs were located in the corpus and the remaining 6 (19%) in the cervix. No clinical symptoms were observed in 2 (25%) PAs and 17 (53%) EPs. Vaginal bleeding was observed in 6 (75%) PAs and 12 (38%) EPs. Hypermenorrhea was observed in 3 (38%) PAs and 3 (9%) EPs. Dysmenorrhea was observed in 0 (0%) PAs and 2 (6%) EPs. As other causes of vaginal bleeding, the use of estrogen was found in 1 of 6 (17%) PAs with vaginal bleeding, whereas that was not found in EPs. Meanwhile, the concomitance of adenomyosis was observed in 1 of 12 (8%) EPs with vaginal bleeding, whereas that was not observed in PAs. Seven (22%) patients with EPs used tamoxifen as hormonal therapy for breast cancer, whereas none (0%) of the patients with PAs used tamoxifen. Histological specimens were obtained via total hysterectomy in nine patients (two with PAs and seven with EPs) and via endometrial curettage in the remaining patients. Patient characteristics are summarized in Table 1.
Table 1. .
Patient characteristics
| Characteristics | Polypoid adenomyoma | Endometrial polyp |
| Number of patients | 8 | 32 |
| Age | ||
| Median | 49 | 47 |
| Range | 42–74 | 27–76 |
| Menopausal status | ||
| Pre-menopausal | 4 (50) | 19 (59) |
| Post-menopausal | 4 (50) | 13 (41) |
| Location | ||
| Corpus | 6 (75) | 26 (81) |
| Cervix | 2 (25) | 6 (19) |
| Clinical symptoms | ||
| Asymptomatic | 2.(25) | 17.(53) |
| Vaginal bleeding | 6.(75) | 12.(38) |
| Hypermenorrhea | 3.(38) | 3.(9) |
| Dysmenorrhea | 0.(0) | 2.(6) |
| Prior tamoxifen use | 0.(0) | 7.(22) |
| Reference standard | ||
| Hysterectomy | 2.(25) | 7.(22) |
| Curretage | 6.(75) | 25.(78) |
Data are numbers of patients, and numbers in parentheses are frequencies expressed as percentages.
MR imaging
MRI was performed using a 1.5 T MR imaging system (Intera Achieva 1.5 T Pulsar; Philips Medical Systems, Best, Netherlands) or a 3 T MR imaging system (Achieva Quasar Dual 3 T; Philips Medical Systems, Best, Netherlands). All MR images were obtained at a section thickness of 5 mm with 2 mm intersection gap and a 26 × 26–28 × 28 cm field of view. Axial, sagittal, and coronal T2 weighted fast spin-echo images [repetition time/echo time, (TR/TE), 3000–7402/90–100 ms] and axial T1 weighted spin echo images (TR/TE, 500–782/10–17 ms) were obtained for all 40 patients. Axial diffusion-weighted images (TR/TE, 4000–5000/69–72 ms) were obtained for 5 patients with PAs and 19 patients with EPs using a single-shot spin-echo echoplanar imaging sequence using a b-value of 0 and 1000 s mm–2. Axial and sagittal fat-suppressed gadolinium-enhanced T1 weighted spin echo images (TR/TE, 562–863/10–17 ms) were obtained after the intravenous injection of 0.1 mmol kg–1 of gadopentetate dimeglumine (Magnevist, Bayer HealthCare, Leverkusen, Germany) or Gadobutrol (Gadavist, Bayer HealthCare, Leverkusen, Germany) in 12 patients with EPs, but no patients with PAs underwent contrast-enhanced MRI.
Imaging assessment
Two radiologists with 19 and 5 years of post-training experience of gynecological imaging individually reviewed all the MR images, and any disagreements were resolved by consensus.
As a quantitative assessment, maximum tumor diameter was measured on T2 weighted images using axial, coronal, or sagittal planes. If cysts were observed within a tumor, maximum cyst diameter and number of cysts were measured. Apparent diffusion coefficient (ADC) values (×10−3 mm2s−1) were measured on ADC maps by placing regions of interest (ROIs) over the tumors. ROIs were placed to encompass lesions as much as possible while avoiding cystic components including hemorrhage by referring to the T1- and T2 weighted images.
As a qualitative assessment, the reviewers evaluated the predominance of cystic or solid components as well as presence of cysts, hemorrhage, fluid–fluid level, fibrous core, and myometrial invasion. Predominance of cystic or solid components was defined as the presence of cystic or solid components in more than half the area within the lesion. Marked hyperintense foci on T2 weighted images or unenhanced areas on contrast-enhanced T1 weighted images were regarded to show cysts. Hyperintense areas relative to the skeletal muscle on T1 weighted images were considered to show intratumoral hemorrhage. The presence of myometrial invasion and fluid–fluid level was assessed on T2 weighted images. Fibrous core was defined as the presence of a hypointense stripe at the site of attachment to the myometrium on T2 weighted images.
Statistical analysis
All statistical analyses were performed using SPSS v. 22.0 (SPSS, Inc, an IBM Company, Chicago, Illinois, IL). The Mann–Whitney U test was used to compare the quantitative results (maximum tumor diameter, maximum cyst diameter, number of cysts, and ADC values) between PAs and EPs. The χ2 test or Fisher exact test was performed to compare the qualitative results (predominance of cystic or solid components and presence of cysts, hemorrhage, myometrial invasion, fluid–fluid level, and fibrous core) between PAs and EPs. Null hypotheses of no difference were rejected if p-values were less than 0.05.
Results
The maximum tumor diameter was significantly larger in PAs than in EPs in cases where tamoxifen was not used (39.3 ± 17.3 mm vs 27.4 ± 19.1 mm; p < 0.05). In patients with EPs, the maximum tumor diameter was significantly larger in cases where tamoxifen was used than in those where it was not used (35.3 ± 9.7 mm vs 27.4 ± 19.1 mm; p < 0.05). However, no significant differences were observed in the maximum tumor diameter between PAs and EPs (39.3 ± 17.3 mm vs 29.2 ± 17.7 mm; p = 0.087) and between PAs and EPs in cases where tamoxifen was used (39.3 ± 17.3 mm vs 35.3 ± 9.7 mm; p = 0.908). When evaluating cysts, we observed no significant differences in the maximum cyst diameter (22.0 ± 20.0 mm vs 8.6 ± 6.2 mm; p = 0.063), number of cysts (8.7 ± 12.5 vs 4.3 ± 4.0; p = 0.679), and ADC values (1.35 ± 0.12 × 10−3 mm2 s−1 vs 1.34 ± 0.24 × 10−3 mm2 s−1; p = 0.696) between PAs and EPs. Quantitative measurements of PAs and EPs were summarized in Table 2.
Table 2. .
The imaging findings of polypoid adenomyoma and endometrial polyp
| Polypoid adenomyoma (n = 8) | Endometrial polyp (n = 32) | p-value | |
| Quantitative measurements | |||
| Maximum tumor diameter (mm) | 39.3 ± 17.3 | 29.2 ± 17.7 | 0.087 |
| Maximum cyst diameter (mm) | 22.0 ± 20.0 | 8.6 ± 6.2 | 0.063 |
| Number of cysts | 8.7 ± 12.5 | 4.3 ± 4.0 | 0.679 |
| ADC values (× 10–3 mm2 s–1) | 1.35 ± 0.12 | 1.34 ± 0.24 | 0.696 |
| Qualitative imaging findings | |||
| Predominant components | |||
| Cystic | 3 (37) | 2 (6) | 0.046a |
| Solid | 5 (63) | 30 (94) | |
| Cysts | 7 (88) | 8 (25) | 0.002a |
| Hemorrhage | 4 (50) | 3 (9) | 0.020a |
| Myometrial invasion | 2 (25) | 0 (0) | 0.036a |
| Fluid–fluid level | 1 (13) | 1 (3) | 0.364 |
| Fibrous core | 4 (50) | 25 (78) | 0.126 |
ADC, apparent diffusion coefficient.
Data are numbers ofpatients, and numbers in parentheses are frequencies expressed aspercentages.
aThe frequency of polypoid adenomyomas was significant higher thanthat of endometrial polyps (p < 0.05).
Table 2 also summarizes the qualitative imaging findings of PAs and EPs. The predominance of cystic components (37% vs 6%; p < 0.05) was more frequently observed in PAs than in EPs (Figures 1–3). A significantly higher frequency of cysts (88% vs 25%; p < 0.05), hemorrhage (50% vs 9%; p < 0.05), and myometrial invasion (25% vs 0%; p < 0.05) was observed in PAs than in EPs (Figures 1–3). However, no significant differences were observed in the presence of fluid-fluid level (13% vs 3%; p = 0.364) and fibrous core (50% vs 78%; p = 0.126) between PAs and EPs.
Figure 1.
A 43-year-old female with polypoid adenomyoma (a) Sagittal T2 weighted image (TR/TE, 3000/100 ms) shows a submucosal mass protruding into the endometrial cavity (arrow) with a large cystic component (arrow head). (b) Axial T2 weighted image (TR/TE, 4415/100 ms) shows a submucosal mass (arrow) with a large cystic component (arrow head). (c) Axial T1 weighted image (TR/TE, 607/10 ms) shows a hyperintense cystic component suggestive of hemorrhage (arrow head) within a submucosal mass (arrow). TE, echo time; TR, repetition time.
Figure 2.
A 45-year-old female with polypoid adenomyoma. (a) Sagittal T2 weighted image (TR/TE, 3276/90 ms) shows a submucosal mass protruding into the endocervical canal (arrow) with myometrial invasion (arrow head). (b) Axial T2 weighted image (TR/TE, 4415/100 ms) shows a submucosal mass (arrow) with multiple small cystic components (arrow heads). (c) Axial T1 weighted image (TR/TE, 556/12 ms) shows a slightly hyperintense cystic component suggestive of hemorrhage (arrow head) within a submucosal mass (arrow). TE, echo time; TR, repetition time.
Figure 3.
A 51-year-old female with endometrial polyp (a) Sagittal T2 weighted image (TR/TE, 7312/90 ms) shows a submucosal mass protruding into the endocervical canal (arrow) with a hypointense fibrous core (arrow head). (b) Axial T2 weighted image (TR/TE, 7402/90 ms) shows a submucosal mass (arrow) with a hypointense fibrous core (arrow head). (c) Axial T1 weighted image (TR/TE, 782/17 ms) shows a hypointense endometrial mass (arrow). TE, echo time; TR, repetition time.
Discussion
Histopathologically, adenomyomas comprise glands that may be cystically dilated, lined by endometrial-type epithelium, and surrounded by endometrial-type stroma; the latter is further surrounded by fascicles of smooth muscle, which is typically the predominant component.1,7,14 The cut surface of adenomyomas is yellow-tan or gray to white, with a firm rubbery consistency and a lobulated smooth surface. The surface displays a trabeculated appearance as a result of the presence of hypertrophied smooth muscle. It is important to histologically distinguish submucosal PAs from atypical PAs, EPs, adenofibromas, and adenosarcomas.
Adenomyomas often contain several small cystic spaces of varying sizes. Therefore, based on their macroscopic spectrum, adenomyomas can be classified into three groups: solid, solid and cystic, and cystic.7 Previous pathological investigations reported that the frequency of cysts in adenomyomas ranged from 19 to 72%.7,14 The difference in the frequency of cysts was affected by the different pathological definitions of cysts, ranging from simple glands lined by proliferative endometrial epithelium to more irregularly shaped glands and cysts. Cysts or stroma may contain areas of focal hemorrhage, filling cystic spaces with dark brown material.14
Takeuchi et al reported seven cases of uterine PAs, including five submucosal PAs, all of which contained cysts as well-demarcated round hyperintense areas on T2 weighted images and/or as well-demarcated round unenhanced areas on post-contrast T1 weighted images; in addition, four (57%) of the reported seven PAs contained hemorrhagic areas showing hyperintensity on T1 weighted images, reflecting functional endometrium and cystic dilatation of endometrial glands.8 Kitajima et al reported that five (63%) of eight submucosal PAs had cysts on T2- and T1 weighted images and two (25%) of eight submucosal PAs exhibited hemorrhage on T1 weighted images.9 Song et al reported that six (86%) of seven PAs, including three submucosal PAs, demonstrated the presence of cystic and hemorrhagic cavities on T2- and T1 weighted images.10 Among the eight submucosal PAs reported in our study, cysts were observed in 88% and hemorrhage in 50% of the cases. Thus, the observations of our study are similar to those of previous studies. Because our study revealed that cysts and hemorrhage were more frequently observed in PAs than in EPs, we believe that these represent the characteristic MR findings of PAs.
On the other hand, EPs are sessile or pedunculated projections of varying proportions of hypertrophied, hyperplastic, or neoplastic endometrial glands and stroma and arise from anywhere in the fundus or lower uterine segment. EPs typically have a smooth bosselated surface and appear fibrous at the cross-section, often with small cystic spaces reflecting dilation of glandular elements.2
Several radiological reports regarding cyst formation of EPs are available. Grasel et al reported that intratumoral cysts within EPs (hyperintensity on T2 weighted images) were observed in 38% of the cases analyzed by them.11 Park BK et al reported intratumoral cysts within hyperplastic EPs on T2 weighted and contrast-enhanced images in 20% of the observed cases.13 Hase et al reported that intratumoral cysts within EPs (discrete, smooth-walled cystic structures showing hyperintense areas within the lesion on T2 weighted images) were present in 55% and hemorrhage (hyperintense areas in the lesion on fat-suppressed T1 weighted images) in 35% of the observed cases.12 Among 32 EPs reported in our study, cysts were observed in 25% and hemorrhage in 9% of the cases; these findings were slightly different than those reported by Hase et al.12 An explanation for this is that the authors might have included PAs in the analysis of EPs because they did not state a pathological definition of EPs and smooth muscle tissues have been pathologically observed in some cases of EPs.12
In the present study, myometrial invasion was observed in 25% of PAs, whereas it was not observed in EPs. In general, there is a significant association between myometrial invasion and endometrial carcinoma. However, because endometrial carcinoma rarely shows intratumoral cysts, a diagnosis of PAs should be considered when endometrial tumors showing both myometrial invasion and intratumoral cysts are observed.
Grasel et al reported that a fibrous core (hypointensity on T2 weighted images) could be visualized in 64% of the evaluated EPs.11 Park et al reported that fibrous core within hyperplastic EPs was observed on T2 weighted and contrast-enhanced images in 40% of the evaluated cases.13 Hase et al described the presence of central fibrous core (hypointense strip in or at the center of the lesion on T2 weighted images) within 75% of observed EPs.12 Similar to previous studies, among the 32 EPs reported in the present study, fibrous core was observed in 78% of cases. Although fibrous core should be considered as a characteristic MR finding in case of EPs, no significant differences were observed in the frequency of fibrous core between PAs and EPs because half the PAs also showed fibrous core.
Tamoxifen, a selective estrogen receptor modulator, is one of the most commonly prescribed antineoplastic drugs worldwide.15 Schlesinger et al reported that among 79 post-menopausal females with EPs divided into three groups (28 receiving tamoxifen for breast cancer, 23 receiving HRT, and 28 untreated controls), the mean polyp size was greater in the tamoxifen group (29 mm) than in the HRT (11 mm) and UC (14 mm) groups.16 Similar to the above-mentioned study, we observed that the maximum diameter of EPs with the use of tamoxifen was significantly larger than that of EPs without the use of tamoxifen.
The most common presenting symptom of PAs is abnormal vaginal bleeding and vaginal bleeding has been reported to be observed in 58% of PAs.14 On the other hand, abnormal vaginal bleeding is also the most common presentation of EPs, the frequency of vaginal bleeding in EPs varies from 18 to 51%.17,18 Similar to these previous studies, vaginal bleeding was observed in 6 (75%) PAs and 12 (38%) EPs in the present study. The other causes of abnormal vaginal bleeding include malignancy, endocrine disorder, pregnancy, infection, and medication. In our study, although the use of estrogen was found in 1 of 6 (17%) PAs with vaginal bleeding and the concomitance of adenomyosis was observed in 1 of 12 (8%) EPs with vaginal bleeding, no other causes of vaginal bleeding were observed. Generally, abnormal uterine bleeding occurring in the perimenopausal or post-menopausal females should be considered the result of a malignancy until proved otherwise.19
This study had several limitations. First, the cohort size was relatively small because of the fact that the study was conducted at a single institution. Because PA is a rare uterine tumor, the number of PA cases was especially low. Second, because of the retrospective nature of this study, we did not obtain contrast-enhanced MR images for all patients. Therefore, the assessment of imaging findings of contrast-enhanced MR images was impossible and an accurate evaluation of cystic components within tumors on unenhanced MR images may not have been performed. It would have been more useful if all patients underwent contrast-enhanced MRI.
Conclusions
In this study, PAs sometimes show the predominance of cystic components, whereas EPs majority of the times show the predominance of solid components. Because the frequency of cysts, hemorrhage, and myometrial invasion were significantly higher in PAs than in EPs, these observations were considered to be characteristic MR findings suggestive of PAs.
Contributor Information
Masaya Kawaguchi, Email: kawamasaya0713@yahoo.co.jp.
Hiroki Kato, Email: hkato@gifu-u.ac.jp.
Natsuko Suzui, Email: nsuzui7@gifu-u.ac.jp.
Tatsuro Furui, Email: furui@gifu-u.ac.jp.
Ken-ichirou Morishige, Email: mken@gifu-u.ac.jp.
Satoshi Goshima, Email: goshima@gifu-u.ac.jp.
Masayuki Matsuo, Email: matsuo_m@gifu-u.ac.jp.
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