ORIGINAL ARTICLE

Magnetic Resonance Imaging Findings in Atypical Polypoid Adenomyoma Go Nakai, PhD,* Remi Kitano, MD,* Kiyohito Yamamoto, MD,* Akira Higashiyama, MD,* Hiroshi Juri, PhD,* Takahiro Tsuboyama, PhD,* Kazuhiro Yamamoto, PhD,* Takashi Yamada, PhD,† Yoshinobu Hirose, PhD,† Masahide Ohmichi, PhD,‡ and Yoshifumi Narumi, PhD* Objectives: This article describes magnetic resonance imaging (MRI) findings in 3 cases of atypical polypoid adenomyoma (APAM). Methods: Clinical and MRI manifestations of 3 patients with APAM were evaluated. High b value diffusion-weighted and dynamic contrastenhanced images were performed. The size, shape, site of origin, and signal intensity (SI) of MRI findings were evaluated. Results: All patients (age range, 37–47 years; mean age, 40 years) had a chief complaint of atypical genital bleeding with no history of pregnancy. In 2 cases, cytology of the endometrium was positive, and pathological analysis of curettage specimens indicated endometrioid adenocarcinoma. The MRI revealed an endometrial polypoid mass arising from the upper corpus (50%) or lower uterine segment (50%). Except for 1 tumor that seemed to invade the myometrium of the uterine wall due to its irregular margin, all tumors were well circumscribed. On T2-weighted MRI scans, the SI of the tumor was homogenous and marginally hyperintense, and contained markedly hyperintense cystic foci. On T1-weighted images, all the tumors were isointense relative to the myometrium, and in 1 case, a number of cystic foci showed high SIs. In a dynamic contrast-enhanced study, solid portions other than the cystic foci showed contrast enhancement in the arterial phase and demonstrated a washout pattern or plateau pattern in the late phase. All tumors demonstrated high SIs on diffusionweighted images. Conclusions: Differentiating APAM from other malignant polypoid uterine endometrial tumors may still pose difficulties, especially when the tumor seems to invade the myometrium on MRI. Comprehensive clinical information about the patient including age, pathological assessment of the endometrium, and MRI findings should be essential to provide indication for a diagnosis of APAM. Key Words: atypical polypoid adenomyoma, uterine polypoid tumor, MRI, MRI findings, uterine polypoid lesion (J Comput Assist Tomogr 2015;39: 32–36)

A

typical polypoid adenomyoma (APAM) is a rare polypoid tumor of the uterus composed of atypical endometrial glands surrounded by smooth muscle. It often occurs in reproductive-age women with abnormal genital bleeding and can be a cause of female infertility. These tumors are often clinically confused with malignant tumors because their cytologic atypia causes tumor cytology results to be positive. Nonetheless, very few magnetic resonance imaging (MRI) findings of APAM have been reported. To the best of our knowledge, MRI findings including diffusion-weighted

From the Departments of *Radiology, †Pathology, ‡Obstetrics and Gynecology, Osaka Medical College, Takatsuki City, Osaka, Japan. Received for publication June 26, 2014; accepted September 8, 2014. Reprints: Go Nakai, MD, Department of Radiology, Osaka Medical College, 2–7 Daigaku-machi, Takatsuki City, Osaka 569–8686, Japan (e‐mail: [email protected]). The authors declare no conflict of interest. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License, where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially.

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(DW) and dynamic contrast-enhanced imaging have never been reported. Hence, the purpose of our study was to describe MRI findings in 3 patients with pathologically proven APAM.

MATERIALS AND METHODS Between 2012 and 2013, preoperative MRI examinations were performed in 3 patients with pathologically proven APAM. The requirement for institutional review board approval was waived. All patients had a chief complaint of atypical genital bleeding and had no history of pregnancy. In case 1, a 37-year-old overweight woman (body mass index, 33) underwent radical hysterectomy with bilateral salpingo-oophorectomy and pelvic lymphadenectomy. In case 2, a 47-year-old woman with no previous medical history underwent semiradical hysterectomy with bilateral salpingo-oophorectomy and pelvic lymphadenectomy. In case 3, a 37-year-old woman with a history of hysteroscopic resection showing APAM 2 years previously underwent transcervical resection. In both case 1 and case 2, cytology of the endometrium was positive, and pathological analysis of curettage specimens indicated endometrioid adenocarcinoma. A concomitant endometrial carcinoma inside the tumor was noted in case 1, and cervical intraepithelial neoplasia (CIN 3) was noted in case 2. The MRI scans of all patients were reviewed, and radiological findings were retrospectively correlated with histopathologic findings. The morphologic appearance of the lesion (ie, size, site of origin, shape, signal intensity [SI], presence of hemorrhage, and dynamic contrast enhancement pattern) was assessed. The site of origin of the tumor was divided into 2 regions: an upper uterine segment (fundus and corpus) and a lower uterine segment (up to the isthmus). The SI of the lesion on T2-weighted images (T2WIs) was not compared with the SI of the uterine myometrium, but rather to that of the abdominal rectus muscle, as the SI of the uterine myometrium can vary depending on the phase of the menstrual cycle. Magnetic resonance imaging was performed with a 3.0-T superconducting magnet (Signa HDxt 3.0 T; GE Healthcare, Milwaukee, Wis) for case 1 and a 1.5-T superconducting magnet (Achieva, Philips Healthcare, Best, the Netherlands) for the others using a phased array coil. T2-weighted images were acquired in 3 orthogonal planes (axial, sagittal, and coronal). The scanning parameters for T2WI at 1.5 T (at 3.0 T) were as follows: repetition time range/echo time range, 3682–5116/100 (3500–8571/87–104); slice thickness, 6 mm (5 mm); interslice gap, 1 mm; matrix, 231  336 to 276  400 mm (320  192); field-of-view, 25 cm (32 cm). The axial T1-weighted images (T1WIs) (500/9; 550/10) and fatsuppressed T1WIs (spectral attenuated inversion recovery, SPAIR; chemical shift selective) were acquired for all patients. Diffusionweighted images were acquired in the axial and/or sagittal plane using the single-shot echo-planar technique. The scanning parameters at b values of 0 and 1000 s/mm2 were as follows: 3482–3620/ 69–70 (8500/68); slice thickness, 5 to 6 mm (4 mm); interslice gap, 1 mm; matrix, 208; reconstruction, 384 (128  128); field-ofview, 36 cm; number of excitations, 12 (3). Diffusion-encoding

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Plateau Hyperenhancement High

Washout Hyperenhancement High

RESULTS

37 3 (Fig. 3)

HUS indicates higher uterine segment; LUS, lower uterine segment.

Pedunculated

47 2 (Fig. 2)

Atypical genital bleeding Atypical genital bleeding

51  26  34

LUS

Iso

HUS LUS HUS Sessile Pedunculated Sessile 40  19  15 27  34  48 87  49  50 Atypical genital bleeding 37 1 (Fig. 1)

MRI Findings in APAM

gradients were applied along the 3 orthogonal directions of motion-probing gradients. Unenhanced arterial-phase (30–60 s) and late-phase (150–180 s) gadoxetic acid–enhanced images were obtained using a fatsuppressed T1-weighted 3-dimensional sequence (enhanced T1 high-resolution isotropic volume examination, Philips Healthcare: 4.0/1.9; flip angle, 10 degrees; matrix, 208  186 mm and liver acquisition with volume acceleration, GE Healthcare: 4.4/2.0; flip angle, 15 degrees; matrix, 192  320 mm), using the SPAIR (spectral presaturation with inversion recovery) technique with a 5-mm section thickness and a field of 18.4 cm. A 0.01-mmol/kg body weight dose of contrast agent was administered intravenously using a power injector at a rate of 2.0 mL/s, followed by a 20-mL saline flush. A lesion was considered to show contrast enhancement when the SI was higher than that of the myometrium in the arterial phase. In the late phase, a washout pattern or plateau pattern was defined as when the SI of the lesion was lower than or equal to that of the myometrium, respectively.

Iso with high tiny foci Iso

Marginally high with high tiny foci Marginally high with high tiny foci

Washout Hyperenhancement High Marginally high with high tiny foci

Late Phase Arterial Phase SI on DW Imaging SI on T2WI Form Size, mm Symptom Age, y Case

TABLE 1. Summary of Cases and MRI Findings of APAM

Site of Origin

SI on T1WI

Dynamic Contrast Enhancement Pattern

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A summary of results is shown in Table 1. On MRI, the maximum diameter of lesions ranged from 40 to 87 mm (mean, 56.5 mm). Case 1 had 2 lesions, 1 of which was a sessile polypoid tumor arising from the upper uterine segment and the other a pedunculated tumor arising from the lower uterine segment (Fig. 1). Case 2 and 3 each had a single lesion, which was a sessile polypoid tumor arising from the upper uterine segment in case 2 and a pedunculated tumor arising from the lower uterine segment in case 3 (Figs. 2, 3). On T2WI, the SI of the tumor was homogeneously hyperintense relative to that of the abdominal rectus muscle, and there were markedly hyperintense cystic foci within the tumor in all cases (Figs. 1A–3A). The tumor arising from the upper uterine segment in case 1 seemed to invade the myometrium of the posterior uterine wall due to its irregular margin (Fig. 1A). On T1WI, the lesions were homogeneously isointense with the myometrium in 2 cases (cases 1 and 3) and isointense containing hyperintense tiny foci in 1 case (case 2) (Fig. 2B). All hyperintense areas on T1WI were not suppressed on SPAIR. All tumors demonstrated homogeneous high SIs on DW images (Figs. 1B, 3B). Apparent diffusion coefficient (ADC) maps showed restricted diffusion within all masses (Fig. 1C). On a dynamic contrast-enhanced study, solid portions other than the cystic foci showed contrast enhancement in the arterial phase (Figs. 1D, 2C, 3C) and demonstrated a washout pattern (case 1 and 2) (Fig. 1E) or plateau pattern (case 3) in the late phase. Histologic examination of the 3 cases revealed that the polypoid masses were composed of hyperplastic endometrial glands with varying degrees of hyperplasia and atypia admixed with a stromal component consisting of interlacing bundles of smooth muscle cells without nuclear atypia or mitosis (Fig. 1G). Markedly hyperintense areas on T2WI corresponded to relatively large-sized metaplastic endometrial glands within the tumor. A sessile tumor that seemed to invade the posterior wall on MRI scans of case 1 demonstrated partially ill-circumscribed borders with the myometrium histopathologically (Fig. 1H). The stalk of the pedunculated tumor in case 1 was histopathologically composed of mainly smooth muscle cells with abundant vessels and showed relative low SI with flow voids on T2WI and marked hyperintensity in the arterial phase on the fat-suppressed T1-weighted 3-dimensional sequence (Fig. 1D).

DISCUSSION Atypical polypoid adenomyoma of the uterus is an uncommon polypoid endometrial lesion that usually occurs in

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FIGURE 1. A 37-year-old overweight woman with atypical genital bleeding. A, Sagittal T2WI shows 2 masses protruding into the uterine cavity that are homogeneously hyperintense relative to the SI of the abdominal rectus muscle and contain markedly hyperintense cystic foci, one of which is a sessile polypoid tumor arising from the posterior wall of the uterine corpus (black arrows) and the other a pedunculated tumor arising from the anterior lower uterine segment (white arrows). The former seems to invade the myometrium of the posterior uterine wall due to its irregular margin. The stalk of the latter has low SI accompanied by flow voids (arrowhead). B, Sagittal DW images show masses as hyperintense. C, ADC map shows restricted diffusion within the masses. The ADC of the pedunculated tumor was 0.78  10−3 mm2/s. D and E, Fat-suppressed, dynamic gadolinium-enhanced coronal T1WI at the same level of the arrowhead on A shows contrast enhancement relative to the uterine posterior wall in the arterial phase (D) and washout in the late phase (E). The stalk is markedly hyperintense in the arterial phase (D, arrowhead). F, A gross view of the specimen shows 2 reddish masses in the uterine cavity. One mass consists of multiple sessile nodules adhered to the posterior wall of the uterine corpus (black arrows), and the other is a pedunculated tumor arising from the isthmus (white arrows). G, A photomicrograph shows hyperplastic endometrial glands with squamous metaplasia (arrow) admixed with a stromal component of interlacing bundles of smooth muscle cells. H, Photomicrograph corresponding to the posterior wall of the uterine corpus. A sessile tumor (T) that invades the myometrium minimally demonstrates partially ill-circumscribed borders with the myometrium (arrowheads). A tiny isolated lesion apart from the uterine cavity is seen in the myometrium (arrows). It also corresponded histologically to APAM.

premenopausal women (mean age, 40 years) who are on average younger than those with endometrial adenocarcinoma. This was newly described as a distinct disease entity by Mazur1 just 33 years ago. Of these patients, 32 (68%) of 47 patients were nulligravida,2,3 86 (70%) of 123 patients were nulliparous,2–7 and clinical histories of infertility are common (29.4%-35.3%).2,5 The pathology is characterized by biphasic proliferation of architecturally complex and cytologically atypical endometrial glands,

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typically with squamous metaplasia and a myofibromatous stromal component. The pathogenesis is considered to be nonneoplastic proliferation, possibly secondary to prolonged estrogenic stimulation of an endometrial stromal progenitor cell. Although whether there is any association between APAM and hormone therapy is unknown, APAM has been reported in patients receiving hormone therapy such as long-term tamoxifen therapy, estrogen supplementation therapy,3 luteal hormone therapy, or clomiphene therapy.2,5 © 2015 Wolters Kluwer Health, Inc. All rights reserved.

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J Comput Assist Tomogr • Volume 39, Number 1, January/February 2015

MRI Findings in APAM

FIGURE 2. A 47-year-old woman with atypical genital bleeding. A, Sagittal T2WI shows a mass protruding into uterine cavity as homogeneous and marginally hyperintense with markedly hyperintense cystic foci relative to the abdominal rectus muscle. B, Axial fat-suppressed T1WI (SPAIR) shows the mass as having homogeneous isointensity with hyperintense tiny foci (arrow). C, Axial fat-suppressed, dynamic gadolinium-enhanced T1WI shows contrast enhancement of the mass in the arterial phase. Diffusion-weighted imaging shows the mass as hyperintense (not shown). D, Gross view of specimen shows a sessile reddish yellow polypoid tumor arising from the anterior wall of the uterine corpus.

Thus estrogen-related factors have been considered to play an important role in the development of APAM.3,4 Although APAM does not invade the myometrium microscopically, parts of the border with the myometrium were ill-circumscribed

in case 1. Therefore, lesions sometimes seemed to invade the uterine myometrium minimally on MRI scans (Fig. 1A) as well as on the photomicrograph (Fig. 1H). Longacre et al5 reported the APAM of low malignant potential defined as the APAM with

FIGURE 3. A 37-year-old woman with a history of hysteroscopic resection showing APAM 2 years previously. A, Sagittal T2WI shows a polypoid mass arising from the isthmus and protruding into the cervical canal as marginally hyperintense with cystic foci that are markedly hyperintense relative to the abdominal rectus muscle. B, Sagittal DW imaging shows the mass as hyperintense. C, fat-suppressed, dynamic gadolinium-enhanced sagittal T1WI shows contrast enhancement of the mass in the arterial phase. © 2015 Wolters Kluwer Health, Inc. All rights reserved.

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markedly complex glands that are indistinguishable from welldifferentiated adenocarcinoma, which may be associated with superficial invasion into the myometrium. Our finding of the partially ill-circumscribed borders with the myometrium possibly corresponds to superficial invasion of the APAM of low malignant potential.5 The MRI findings in our study were mostly consistent with Yamashita et al.8 On T2WI, APAM was seen as a slightly hyperintense polypoid mass mixed with markedly hyperintense foci that corresponded to islands of metaplastic endometrial foci histopathologically. On T1WI, the tumors were isointense with the myometrium and occasionally had hyperintense cystic foci that were not suppressed on fat-suppressed T1WI (Fig. 2B). The contrastenhanced study showed irregular enhancement of the tumor. In our dynamic contrast-enhanced study, solid portions other than the cystic foci showed homogeneous early enhancement in the arterial phase and demonstrated a washout pattern or plateau pattern in the late phase. Solid parts of all tumors showed homogeneous hyperintensity on DW images, which were possibly related to its histology, namely, densely distributed atypical endometrioid glands with squamous metaplasia and smooth muscle cells, and the SI on T2WI may depend on the size and amount of glands within the tumor. Differential diagnostic considerations for a malignant uterine polypoid mass in the uterine cavity include endometrial stromal sarcoma, mixed müllerian malignant tumor, and endometrial carcinoma. However, endometrial stromal sarcoma typically shows intramyometrial wormlike nodular extension with irregular margin9 and rarely involves cystic tiny foci inside it. Although mixed müllerian malignant tumor shows extremely inhomogenous SI on T2WI and avid contrast-enhancement due to heterogeneous admixture of malignant epithelial and mesenchymal elements in different proportions.10 Concomitant foci of endometrial carcinoma have been reported in about 7% of patients with APAM.11 Although the association between APAM and endometrial cancer is unclear, being aware of this possibility is important. However, carcinoma foci within the tumor in case 1 could not be identified on MRI due to their tiny size. Therapy for APAM depends on multiple factors such as age at presentation and desire for childbearing among others. Because many patients are not only around 40 years but also nullipara, fertility-preserving treatment such as transcervical resection or dilatation and curettage have been performed as a conservative treatment. However, careful follow-up by hysteroscopic observation under direct vision is important because high recurrence rate has been reported in patients in whom complete resection cannot be attained.5,11,12 Thus simple hysterectomy should be preferred to obtain a complete removal of the lesion in perimenopausal or postmenopausal women especially when they are not improved by the conservative treatment. However, in clinical practice, cytology is often positive because of cytologic atypia5; moreover, differentiating APAM from endometrial carcinoma with myometrial invasion could be difficult even with a curettage specimen due to the limited collection

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of samples.3 Thus such cytologic results can lead to excessive treatment as seen in case 1 and 2 because a uterine polypoid mass protruding into the endocervical canal could be misinterpreted as cervical invasion of endometrial carcinoma. The finding of early enhancement in the dynamic contrast-enhanced study is an important clue in differentiating endometrial cancer from APAM. However, differentiating APAM from other malignant polypoid uterine endometrial tumors may still pose difficulties, especially when the tumor seems to invade the myometrium on MRI scans. Comprehensive clinical information about the patient including age, pathological assessment of the endometrium, and MRI findings should be essential to provide indication for a diagnosis of APAM. Inclusion of APAM in the differential diagnosis on MRI could prevent overtreatment and suggest another choice of treatment such as hysteroscopic resection for women who desire to preserve fertility.

REFERENCES 1. Mazur MT. Atypical polypoid adenomyomas of the endometrium. Am J Surg Pathol. 1981;5:473–482. 2. Matsumoto T, Hiura M, Baba T, et al. Clinical management of atypical polypoid adenomyoma of the uterus. A clinicopathological review of 29 cases. Gynecol Oncol. 2013;129:54–57. 3. Young RH, Treger T, Scully RE. Atypical polypoid adenomyoma of the uterus. A report of 27 cases. Am J Clin Pathol. 1986;86:139–145. 4. Clement PB, Young RH. Atypical polypoid adenomyoma of the uterus associated with Turner’s syndrome. A report of 3 cases, including a review of “estrogen-associated” endometrial neoplasms and neoplasms associated with Turner’s syndrome. Int J Gynecol Pathol. 1987;6:104–113. 5. Longacre TA, Chung MH, Rouse RV, Hendrickson MR. Atypical polypoid adenomyofibromas (atypical polypoid adenomyomas) of the uterus. A clinicopathologic study of 55 cases. Am J Surg Pathol. 1996;20:1–20. 6. Kim KR, Scully RE. Peritoneal keratin granulomas with carcinomas of endometrium and ovary and atypical polypoid adenomyoma of endometrium. A clinicopathological analysis of 22 cases. Am J Surg Pathol. 1990;14:925–932. 7. Delprado WJ, Stevens SM, Baird PJ. Atypical polypoid adenomyoma: a case report with ultrastructural examination. Pathology. 1985;17:522–525. 8. Yamashita Y, Torashima M, Hatanaka Y, et al. MR imaging of atypical polypoid adenomyoma. Comput Med Imaging Graph. 1995;19:351–355. 9. Koyama T, Togashi K, Konishi I, et al. MR imaging of endometrial stromal sarcoma: correlation with pathologic findings. AJR Am J Roentgenol. 1999;173:767–772. 10. Teo SY, Babagbemi KT, Peters HE, et al. Primary malignant mixed müllerian tumor of the uterus: findings on sonography, CT, and gadolinium-enhanced MRI. AJR Am J Roentgenol. 2008;191:278–283. 11. Heatley MK. Atypical polypoid adenomyoma: a systematic review of the English literature. Histopathology. 2006;48:609–610. 12. Di Spiezio Sardo A, Mazzon I, Gargano V, et al. Hysteroscopic treatment of atypical polypoid adenomyoma diagnosed incidentally in a young infertile woman. Fertil Steril. 2008;89:456.e9–456.e12.

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Magnetic resonance imaging findings in atypical polypoid adenomyoma.

This article describes magnetic resonance imaging (MRI) findings in 3 cases of atypical polypoid adenomyoma (APAM)...
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