ORIGINAL ARTICLE
Magnetic Resonance Imaging and Pathologic Findings of 26 Cases With Uterine Adenomatoid Tumors Qiuhua Meng, MD, PhD,* Qingsi Zeng, BS,* Xiaomei Wu, MD, PhD,* Qi Wan, MD,* Yongxia Lei, MD,* Ting Song, MD, PhD,† Xia Gu, MD, PhD,‡ Guobing Hong, MD, PhD,§ Wenhao Zhang, BS,* and Xinchun Li, MD, PhD* Objective: To analyze the magnetic resonance imaging (MRI) features and pathologic findings of uterine adenomatoid tumors (ATs) for improved diagnostic accuracy and facilitating differential diagnosis of the tumors. Methods: We investigated retrospectively 26 patients with uterine ATs confirmed by pathology. Before operation, all patients accepted multiple MRI scans, including T1-weighted image (T1WI), T2-weighted image (T2WI), T2WI/spectrally adiabatic inversion recovery, and T1-weighted enhanced imaging. Two radiologists reviewed all the MRI sequences on PACS workstations for all patients to evaluate the location, shape, size, margin, intensity, and enhancement of ATs. Results: All uterine ATs exhibited either single round solid (n = 24) or predominantly cystic (n = 2) masses with either well-defined (n = 23) or ill-defined margin (n = 3). The diameter range of the tumors was 1.0 to 7.0 cm (mean, 3.8 cm). Solid masses were isointensive on T1WI and hypointensive on T2WI with moderate enhancement. The degree of enhancement in solid tumors was either lower than (18/24 [75%]) or equal to (6/24 [25%]) that of the myometrium. Predominantly cystic masses presented as cystic lesions with a little irregular solid nodule inside. The cystic parts were hypointensive on T1WI and hyperintensive on T2WI without enhancement, whereas the solid nodules were isointensive on both T1WI and T2WI with moderate enhancement. A large part of the uterine ATs (69.2% [18/26]) coexisted with other uterine diseases. On pathology, uterine ATs were characterized as gland-like structures with irregular expansion of tubular cavities, which might be correlated with low enhancement of tumors. The tumors were lined with flat or cuboidal mesothelial cells and residue of smooth muscle component, which might contribute to their hypointensive appearance on T2WI. Conclusions: Small solid uterine masses with homogeneous hypointensity on T2WI and lower enhancement or cystic lesions with inner irregular solid nodule may indicate the diagnosis of uterine ATs, and final diagnosis can be determined with pathology. Key Words: adenomatoid tumor, uterus, magnetic resonance imaging, pathology (J Comput Assist Tomogr 2015;39: 499–505)
A
denomatoid tumor (AT) was firstly named by Golden and Ash,1 in 1945, which is an extremely rare benign mesothelial tumor arising in the genital systems of both males and females, such as epididymis, uterus, fallopian tubes, and ovaries. In females, the most common sites are in the fallopian tubes and the uterus.1,2 It occasionally occurs outside the genital systems, From the *Department of Radiology, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, PR China; †Department of Radiology, The Third Affiliated Hospital of Guangzhou Medical University, Guangzhou, PR China; ‡Department of Radiology, The Fifth Affiliated Hospital of Sun Yat-sen University, Zhuhai, PR China; and §Department of Pathology. The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, PR China. Received for publication November 8, 2014; accepted March 4, 2015. Reprints: Xinchun Li, MD, PhD, Department of Radiology, The First Affiliated Hospital of Guangzhou Medical University, 151 Yanjiangxi Rd, Guangzhou, PR China, 510120 (e‐mail: [email protected]). The authors declare no conflict of interest. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
including adrenal gland, pancreas, peritoneal, omentum, and mesentery.3 Uterine ATs are benign mesothelial tumors composed of gland-like structures arising in uterine serosa and myometrium. Although diagnosis of uterine ATs increased in recent years due to advanced technology (radio scanning, electron microscope, immunohistochemistry),4 most of them were misdiagnosed as leiomyoma because uterine ATs shared the same imaging features of leiomyoma.5 Although AT and leiomyoma are both benign tumor, a few large leiomyomas have increased risk of malignancy, whereas recurrence or metastasis has never been reported in ATs.5 Moreover, leiomyoma is sensitive for hormone therapy, whereas AT has unclear responses to hormone therapy.5 In case AT is misdiagnosed as leiomyoma, unnecessary hormone therapy may be administrated. The identification of ATs also helps in postoperative counseling because ATs do not recur but fibroids may do.6 Therefore, it is important to differentiate ATs from other benign diseases. To our best knowledge, up to now, there are only a few reports describing briefly magnetic resonance imaging (MRI) appearance of ATs. Mitsumori et al5 reported 2 cases of solid ATs with well-defined margin. Kim et al7 reported one case presented as a cystic mass. Harada et al2 reported a cystic ATwhich appeared as a high-intensity area on T2-weighted image (T2WI) with the margin and septum of the tumor enhanced slightly. The comprehensive MRI features of uterine ATs have not been investigated in detail yet. The purpose of the present study is to analyze the MRI features and pathologic findings of uterine ATs for improved diagnostic accuracy and facilitating differential diagnosis of the tumors.
MATERIALS AND METHODS Patients This retrospective study was approved by the institutional review board with a waiver of the written informed consent. We searched for patients with uterine ATs in the pathologic database in our hospital between January 2005 and June 2013. All ATs were confirmed by pathology. The inclusion criteria were as follows: (1) patients underwent surgical resection, (2) pelvis MRI images were available, (3) and clearly position-marked lesions in gross pathology when there were multiple lesions. The exclusion criteria were as follows: (a) no quality MRI images were available (n = 1), (b) lesions were not clearly position-marked in gross pathology (n = 1), and (c) position-marked lesions in gross pathology could not be corresponded to the position of lesions on MRI images (n = 3). Among inclusive cases, most uterine ATs (23/26 [88.5%]) were misdiagnosed as leiomyoma by MRI and ultrasound. The average patient age was 41 years (range, 24–58 years). The clinical symptoms were various: a mass on lower abdomen (n = 4), vaginal irregular bleeding (n = 14), belly ache (n = 5), and no apparent symptoms (n = 3). Eighteen cases had other diseases, including uterine fibroids, adenomyosis, endometrial cancer, uterine cervix cancer, appendix abscess, and cyst. All
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patients underwent surgical resection including hysterectomy and laparoscopic tumor excision. The time interval between the MRI scan and surgery was 7 days or less. The tumors did not recur after operation for 1-year imaging follow-up, which was performed by a single gynecologic radiologist.
MRI Scans Magnetic resonance imaging was performed in all cases with a 1.5-T unit (Nova Dual; Philips, Amsterdam, the Netherlands) and a body phased-array coil. T1-weighted image (T1WI; repetition time [TR]/echo time [TE], 300–500/10–20 milliseconds), T2WI (TR/TE, 3200–3500/80–100 milliseconds), and T2WI/the spectrally adiabatic inversion recovery (SPAIR) sequence (T2WI/ SPAIR; TR/TE: 3200–3500/80–100 milliseconds) were performed with the matrix of 512 512, field of view of 350 to 450 mm, number of signals averaged of 2 to 4, and slice thickness/gap of 5–6/1.0 mm. Gadodiamide injection (GE Healthcare, Ireland) was injected in all patients at a dose of 0.1 mmol/kg when performing contrast-enhanced MR scanning including axial, sagittal, and coronal fat-suppressed T1-weighted sequences. Two gynecologic radiologists both with more than 15-years experience reviewed in consensus the MRI characteristics of ATs on PACS workstations, without knowing histopathologic results. The MRI characteristics included location, shape, size, margin, intensity, and enhancement. An AT was in submucosa when 80% portion of the AT was located in the submucosa or in subserosa when 80% portion of the AT was located in the subserosa. The signal intensity was evaluated on T1WI, T2WI, and postcontrast images. For size, the term diameter of a tumor indicated “the maximum diameter” on T2WI. If the margin could be clearly identified on T2WI or on contrast-enhanced images, it was called “well defined.” On the contrary, if the margin could not be clearly identified, it was called “ill defined.” The pseudocapsule was referred to a circular ring around the tumor with low or high intensity on T2WI and enhanced T1WI. For the degree of enhancement of ATs, we used myometrium enhancement as a reference. If the enhancement of lesion was lower or higher than the myometrium enhancement, it was called “lower or higher enhancement.” If the enhancement of lesion was equal to enhancement of
myometrium, it was called “iso-enhancement.” The lesions were categorized into 3 types: solid, solid-cystic, and predominantly cystic. Predominantly cystic or solid-cystic ATs in this study were referred to the tumors mainly composed of cystic lesions (cystic portion ≥ 80% or 50% ≤ cystic portion < 80%, respectively, showed as hyperintense in T2WI and no enhancement after gadolinium administration), with or without solid nodule inside the lesion.
Pathology Examination All tumors were removed by surgery (the marking of the lesions was done according to the position of the tumor by the surgeon before pathology judge), fixed in 10% neutral formalin, embedded in paraffin, sliced, and hematoxylin and eosin (HE) stained. Among them, 6 cases were also stained by specific stain such as Alician blue and periodic acid–Schiff. Immunohistochemical (IHC) staining was used in 13 cases to differentiate ATs from other diseases. Immunohistochemical antigens included claritin (CR), mesothelial cell (MC), cluster of differentiation 34 (CD34), cytokeratin (CK), vimentin (VIM), muscle-specific actin (SMA), and Wilms tumor 1 (WT-1). All specimens were reviewed together by 2 pathologists. The diagnosis of uterine ATs was made when there was evidence showing that tumor had gland-like structure or irregular expansion of the tubular cavities, lined with flat or cuboidal neoplastic cells. In case diagnosis of AT could not be reached in consensus, IHC staining was ordered. Adenomatoid tumor was positive to CR, MC, or CK but negative to CD34, which indicated a mesothelial origin.
RESULTS Location, Size, and Shape All tumor exhibited as either a single round solid mass (n = 24; Figs. 1–4) or a predominantly cystic round mass (n = 2; Figs. 5 and 6). The locations included uterine horn (3 cases), lateral wall of the uterine body (2 cases), the anterior wall (12 cases), the posterior wall (6 cases), the submucosa (1 case), and the subserosa (2 cases; Fig. 4). The diameter of the tumor was 1.0 to 7.0 cm (mean, 3.8 cm): 5 cases, at least 5 cm; 7 cases, 3 to 5 cm; and 14 cases, less than 3 cm.
FIGURE 1. A–F, A 40-year-old woman with uterine AT (long arrow; B): the tumor appears homogeneously isointensive on axial T1WI (A) and heterogeneously hypointensive on T2WI with iso and high-intensity signals inside (B, D). C and E, The tumor exhibited obvious enhancement equal to the myometrium, and the margin was well defined with a pseudocapsule (short arrow) on contrast-enhanced axial/sagittal T1WI image. F, On microscopy, tumor was composed of canalicular spaces (diamond arrow) lined with flattened cells and admixed with smooth muscle and fibrous tissue (HE stain, original magnification 100). Figure 1 can be viewed online in color at www.jcat.org.
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FIGURE 2. A–I, A 26-year-old women with uterine AT (long arrow; D) in the posterior wall of the uterus (forked tail arrow; D):the tumor appears homogeneously hypointensive on axial T1WI (A) and nearly homogeneously hypointensive (long arrow) on T2WI (B, D), which exhibited heterogeneously moderate enhancement (long arrow; C), and the enhancement degree was lower than that of the myometrium on contrast-enhanced axial/sagittal T1WI image (C, E). F, On microscopy, the tumor was composed of canalicular spaces lined with flattened cells and admixed with smooth muscle (diamond arrow) and fibrous tissue (HE stain, original magnification 100). G–I, Immunohistochemical staining demonstrated positive to CR, MC, and WT-1 (original magnification 100; long arrow). Figure 2 can be viewed online in color at www.jcat.org.
MRI Findings Solid tumors were isointensive on T1WI, hypointensive on T2WI (Fig. 3), and moderately enhanced (with heterogeneous
patterns in 6 cases [Fig. 3] and homogeneous patterns in 18 cases [Fig. 4]). Degree of enhancement was either lower than (n = 18; Fig. 4) or equal to that of the myometrium (n = 6; Fig. 1). The ATs had either well-defined (21/24 [87.5%]) or ill-defined
FIGURE 3. A–F, A 44-year-old women with uterine AT (long arrow; B, E) in the right lateral wall and uterine adenomyoma (black short arrow; B, E) in the left lateral wall of the uterus (forked tail arrow; B): the tumor appeared homogeneously isointensive on axial T1WI image (A) and nearly homogeneously hypointensive on T2WI image (B, D). D and E, The tumor exhibited heterogeneous obvious enhancement; the enhancement degree was the same as the myometrium on contrast-enhanced axial/coronal T1WI image. F, On microscopy, the tumor was composed of gland-like structure lined with flattened cells and admixed with smooth muscle and fibrous tissue (HE stain, original magnification 100). Figure 3 can be viewed online in color at www.jcat.org. © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 4. A–H, A 38-year-old women with uterine AT (long arrow; B) at the left subserosa and uterine fibroids (short arrow; B) with septum (diamond arrow; B) in the posterior wall of the uterus (forked tail arrow): the tumor appears homogeneously hypointensive, relative to the myometrium on axial T1WI image (A), and nearly homogeneously hypointensive on T2WI (B, C). D, The tumor exhibited homogeneously moderate enhancement on contrast-enhanced coronal T1WI image (long arrow). E, On microscopy, the tumor was composed of gland-like structure lined with flattened cells and admixed with smooth muscle and fibrous tissue (HE stain, original magnification 100). F–H, Immunohistochemical staining was positive to CR, MC, and VIM (original magnification 200; long arrow). Figure 4 can be viewed online in color at www.jcat.org.
margins (3/24 [12.5%]). The margins appeared most clear on T2WIs and enhanced T1WIs. Among all the solid tumors, 6 cases had patchy signals of lower intensity on T1WI and slightly higher intensity on T2WI, and 2 cases had signals of circular low intensity
on T2WI and enhancement around the tumor, which resembled signs of pseudocapsule (Fig. 1; Table 1). The predominantly cystic masses presented as well-defined cystic lesions with an irregular solid nodule inside. The cystic
FIGURE 5. A–F, A 58-year-old women with uterine AT (long arrow; D) at the anterior wall of the uterus (forked tail arrow; D) and endometrial cancer inside the cavity of the uterus (short arrow, D); the tumor presented as a cystic lesion (long arrow; B) with an irregular solid nodule inside (black short arrow; B), of which cystic parts showed low intensity on T1WI (A) and obviously high intensity on T2WI (B) without enhancement, and solid parts demonstrated nearly the same intensity as myometrium on T1WI, T2WI, and enhanced T1WI (long arrow; E). F, On microscopy, the tumor was composed of canalicular spaces, lined with flat or cuboidal MCs and smooth muscle (HE stain, original magnification 100). Figure 5 can be viewed online in color at www.jcat.org.
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FIGURE 6. A–F, A 36-year-old women with uterine AT (long arrow, A) at the right subserosa of the uterus: The tumor presented as a cystic lesion (long arrow, B) with an irregular solid nodule inside (black short arrow, B), of which cystic parts showed low intensity on T1WI (A), and solid parts demonstrated nearly the same intensity as the myometrium on T1WI and obviously high intensity on T2WI without enhancement, T2WI, and enhanced T1WI (long arrow; D). E, On microscopy, the tumor was composed of angiomatous-like cavities, lined with flat or cuboidal MCs and smooth muscle (HE stain, original magnification 100). F, Mucus appeared as blue in the cavity (Alician blue, original magnification 100; long arrow). Figure 6 can be viewed online in color at www.jcat.org.
parts had low-intensity signals on T1WI and high-intensity signals on T2WI without enhancement, whereas the solid parts demonstrated nearly the same intensity as the myometrium on T1WI, T2WI, and contrast-enhanced T1WIs (Fig. 6).
Accompanying Lesions Eighteen cases of uterine ATs were associated with other uterine diseases including uterine leiomyoma (16 cases [61.54%]; Fig. 4), uterus adenomyosis (5 cases [19.23%]; Fig. 3), endometrial cancer (1 case [3.80%]; Fig. 5), uterine cervix cancer (2 cases [7.6%]), appendix abscess (1 case [3.80%]), and cyst (4 cases [15.38%]). Ascites or metastases were not found in all cases. The 16 concurrent uterine fibroids encountered along with ATs were round solid masses. The tumors were isointensive on T1WI, hypointensive on T2WI (heterogeneous with necrosis, septum, or sign of whirlpool in 13/16 [or 82%] cases [Fig. 4] and homogeneous in 3/16 [18%] cases), and with different degrees of enhancement (heterogeneous in 13/16 [82%] cases [Fig. 4] and homogeneous in 3/16 [18%] cases). Degree of enhancement was higher than (11/16 [69%] cases) or equal to (2/16 [13%] cases)
TABLE 1. MRI Features of ATs
Imaging Feature Cystic Solid Homogeneous hypointensity on T2WI/SPAIR Patchy higher intensity on T2WI/SPAIR Lower enhancement Homogeneous enhancement Well-defined margin Signs of pseudocapsule
No. Positive Cases
No. Total Cases
%
2 24 18
26 26 24
7.7 92.3 75
6
24
25
18 18 21 2
24 24 24 24
75 75 87.5 8.3
that of the myometrium. The tumors all had well-defined margin, and 8 (50% [8/16]) cases showed signs of pseudocapsule. The 5 concurrent uterine adenomyosis encountered along with ATs were all diffusive and they appeared hypointensive with mixed multiple punctate hyperintensive signals on T2WIs and isointensive on T1WIs with an ill-defined margin (Fig. 3).
Pathologic Findings The ATs were located intramurally (n = 23), subserosally (n = 2), or submucosally (n = 1). No capsule was found on gross specimens of the tumors. The tumor color on the cutting surface was gray-white or gray-yellow, and degenerative areas, cavity, or mucus was found on a few tumors (8 cases [30.7%]). Under microscopy, tumor morphology was variable and appeared as adenoid, angiomatous, lacuna, or cystic structures in the hyperplasia of smooth muscle tissue, lined with flat or cuboidal MCs. Mucus could be detected in 2 cases (Fig. 6). According to histologic types of ATs studied by Quigley and Hart,3 the adenoid type and angiomatoid type were most frequent. Combinations of 2 or more patterns occurred in all tumors, but usually 1 major type prevailed in each case. Immunohistochemical analysis revealed that ATs stained positive to CR (13/13 [100%]), MC (12/13 [92.3%]), CK (10/13 [76.9%]), VIM (8/13 [61.5%]), SMA (6/13 [46.2%]), and WT-1 (5/13 [38.5%]) and negative to CD34 (13/13 [100%]; Figs. 2 and 4).
DISCUSSION Uterine AT is an uncommon benign tumor which can be found in 1.2% of all women.8 The actual incidence is probably higher because of misdiagnosis and missed diagnosis.9 The tissue origin of uterine ATs has been debated for many years. The hypotheses include middle kidney, mesothelium, müllerian epithelium, and vascular derived. Some scholars ever considered ATs as a reaction to inflammation but not a real tumor.10,11 Pathologists struggled investigating this tumor. It was found recently that AT cells expressed CK, VIM, and calretinin, indicating its originating from mesothelium.10,12,13 Adenomatoid tumors were
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officially classified as mesothelial tumors by World Health Organization in the 2003 revision.14 Uterine ATs often occur in women in reproductive ages. Patient's age at the initial diagnosis ranges from 26 to 55 years (with mean age of 41 years) in the literature.15,16 In our study, the average age was 41 years (range, 24–58 years), consistent with previous studies. Clinical manifestations of uterine ATs are nonspecific and variable, including vaginal bleeding, menorrhagia, and abdominal masses.17 Most of uterine ATs are located in the uterus wall, the subserosa near the uterine horn.4,7 The tumors often present as a solitary solid mass with the diameter ranging from 2 to 10 cm (usually small, mean diameter of 2.1 cm).10 In gross examination, ATs are soft and moist; some cases have mucus degeneration. The tumors can show invasive growing patterns due to the lack of capsules.6,18 Pseudocapsules were observed occasionally in a few reports.7 Under microscopy, the tumor is characterized by having gland-like structures and irregular expansion of the tubular cavities, lined with flat or cuboidal MCs and with stromal fibrous and residue of smooth muscle components.19,20 Common histologic types of ATs include adenoid type, angiomatous type, solid type, and cystic type.3,7,10,21 Another classification method was proposed by Tiltman22: plexiform, tubular, canalicular, and mixed types. However, up to now, there were no unified classification standards. The adenoid type in the first classification method corresponds to the tubular type in the second classification method, the angiomatoid type corresponds to the canalicular type, and the solid type corresponds to the plexiform type. Quigley and Hart3 found that there were 2 types or more than 2 kinds of organizations, with one of them being predominant. In our study, we also found that combinations of 2 or more patterns occurred in all tumors, and usually one prevailed in each case. Adenoid and angiomatous types were the most common patterns in our study. It was reported that uterine ATs were positive to VIM and CK, whereas negative to CD34, periodic acid–Schiff, and EMAF8.4,21 In 13 cases with IHC stain in our study, ATs were positive to antigens of mesothelial or epithelial-derived origin, that is, CR (100%), MC (92.3%), CK (76.9%), VIM (61.5%), SMA (46.2%), and WT-1 (38.5%), consistent with previous reports.4,22 The treatment for uterine ATs was usually surgical resection, including hysterectomy and laparoscopic tumor excision. The prognosis was good and recurrence or metastasis had never been reported in the literature. In this study, no tumors recurred in the 1-year follow-up after the operation. Magnetic resonance imaging plays an important role in pelvis disease. The MRI appearance of uterine ATs was firstly described by Mitsumori et al5 (2 solid mass). It was found that uterine ATs appeared a single solid, small, well, or ill-circumscribed mass locating in the myometrium or serosa with low signal intensity in T1WIs and low or high signal intensity in T2WIs. These masses might show mild to moderate enhancement after gadolinium administration.3,7,16 The rare appearance of ATs included cystic type, diffuse type, and infarction type.21–23 In our series, there were 2 types: solid pattern (24/26 [92.3%]) and predominantly cystic pattern (2/26 [7.7%]). The results also indicated that solid pattern was the most common appearance of uterine ATs. Solid ATs were often hypointensive on T2WI. It might be related to tumor containing much smooth muscle. Solid ATs presented moderate enhancement and degree of enhancement was usually lower than that of the myometrium (18/24 [75%]), probably due to the reduction of interstitial vessel resulting from the lacunar-like arrangement of ATs tumor cells. In predominantly cystic ATs, the cystic parts were not enhanced, whereas the irregular solid nodule was moderately enhanced. The 2 predominantly cystic cases corresponded to the angiomatous type under microscopy. The findings described earlier are consistent with previous reports.2,7 Although they lack capsules, due to its expansion, most margins
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of the tumors (21/24 [87.5%]) in our cases appeared well defined in the T2WI and contrast-enhanced T1WI. Among them, 2 cases appeared circular hypointensive in the T2WI and enhanced T1WI around the tumor, resembling signs of pseudocapsule, consistent with the report of Mitsumori etal.5 Our results indicated that a well-defined margin was the common characteristic of most uterine ATs. Uterine ATs usually coexisted with other diseases such as uterine fibroids and adenomyosis. Adenomatoid tumors and leiomyomas were reported to coexist in 60% cases, possibly due to ATs stimulating smooth muscle hyperplasia.10 In this study, there were also 16 cases (16/26 [61.54%]) of uterine ATs accompanying with uterine fibroids, which could be easily misdiagnosed as multiple uterine leiomyomas. Uterine ATs should be differentiated from following diseases. First, uterine fibroids appear hypointensive or isointensive in the T2WI and resemble ATs due to containing a large number of smooth muscle cells. It is difficult to differentiate them based solely on MRI appearance, especially when the tumor is small. However, there are a few clues to distinguish them according to the literature5,10 and our study: (1) the diameter of ATs is often less than 5 cm, whereas that of uterine fibroids is often larger than 5 cm; (2) ATs are likely homogeneous with little necrosis in the T2WIs, whereas uterine fibroids are heterogeneous in the T2WIs with necrosis, septum, and sign of whirlpool due to degeneration; (3) degree of enhancement in ATs is likely lower than that of uterine fibroids; and (4) sign of pseudocapsule in ATs is much lower than that in uterine fibroids. Second, uterine adenomyoma appears hypointensive with mixed multiple punctate hyperintensity in the T2WI and or isointensive or hyperintensive (ectopic endometrial island bleeding) in the T1WI with a well- or illcircumscribed margin and accompanied by uterus junctional zone thickening, which can be used to easily differentiate uterine adenomyoma from most ATs. Finally, uterine sarcoma is usually a larger mass showing signals hypointensive in the T1WI and slightly hyperintensive in the T2WI with obvious necrosis and cystic change, which may help to differentiate uterine sarcoma from uterine ATs. In summary, the imaging features of uterine ATs include a small solid mass with well- or ill-defined margin, homogeneously hypointensive in the T2WI, and lower enhancement, or cystic lesion with irregular solid nodule. One should pay attention to the possibility of ATs in the differential diagnosis of uterine masses. Confirmation diagnosis of ATs should be based on pathologic and IHC analyses. ACKNOWLEDGMENT We thank Mrs Gu Yinyin for pathologic diagnosis for this article. REFERENCES 1. Golden A, Ash JE. Adenomatoid tumors of the genital tract. Am J Pathol. 1945;21:63–79. 2. Harada N, Nobuhara I, Haruta N. Giant cystic adenomatoid tumour of the uterus. J Obstet Gynaecol. 2012;32:407–408. 3. Quigley JC, Hart WR. Adenomatoid tumors of the uterus. Am J Clin Pathol. 1981;76:627–635. 4. Irikoma M, Takahashi K, Kurioka H, et al. Uterine adenomatoid tumors confirmed by immunohistochemical staining. Arch Gynecol Obstet. 2001;265:151–154. 5. Mitsumori A, Morimoto M, Matsubara S, et al. MR appearance of adenomatoid tumor of the uterus. J Comput Assist Tomogr. 2000;24:610–613.
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6. Kalidindi M, Odejinmi F. Laparoscopic excision of uterine adenomatoid tumour: two cases and literature review. Arch Gynecol Obstet. 2010;281:311–315. 7. Kim JY, Jung K, Sung N K, et al. Cystic adenomatoid tumor of the uterus. AJR Am J Roentgenol. 2002;179:1068–1070. 8. Christensen C. Adenomatoid tumours of the uterus. Eur J Gynecol Oncol. 1990;11:85–89. 9. Nakayama H, Teramoto H, Teramoto M. True incidence of uterine adenomatoid tumors. Biomed Rep. 2013;1:352–354. 10. Nogales FF, Isaac MA, Hardisson D, et al. Adenomatoid tumors of the uterus: an analysis of 60 cases. Int J Gynecol Pathol. 2002;21:34–40. 11. Ross MJ, Welch WR, Scufiy RE. Multilocular peritoneal inclusion cysts (so-called cystic mesotheliomas). Cancer. 1989;64:1336–1346. 12. Christensen C, Bichel P. Adenomatoid tumor of uterus case report. Br J Obstet Gynaecol. 1988;95:524–526. 13. Sangoi AR, McKenney JK, Schwartz EJ, et al. Adenomatoid tumors of the female and male genital tracts: a clinicopathological and immunohistochemical study of 44 cases. Mod Pathol. 2009;22:1228. 14. Tavasso Ii FA, Devilee P. WHO Classification of Tumor, Pathology and Genetics of Tumor of the Breast and Female Genital Organs. Lyon: IARC press; 2003:243–244.
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15. Saran M, Sanghi A, Faruqi A. Adenomatoid tumor of the uterus presenting as cyst. J Obstet Gynaecol. 2007;27:637–638. 16. Huang CC, Chang DY, Chen CK, et al. Adenomatoid tumor of the female genital tract. Int J Gynecol Obstet. 1995;50:275–280. 17. Schwartz EJ, Longacre TA. Adenomatoid tumors of the female and male genital trInt. J Gynecol Pathol. 2004;23:123–128. 18. Sieunarine K, Cowie AS, Bartlett JD, et al. A novel approach in the management of a recurrent adenomatoid tumor of the uterus utilizing a Strassman technique. Int J Gynecol Cancer. 2005;15:671–675. 19. Hanada S, Okumura Y, Kaida K. Multicentric adenomatoid tumors involving uterus, ovary, and appendix. J Obstet Gynaecol Res. 2003;29:234–238. 20. De Rosa G, Boscaina A, Terracciano LM, et al. Giant adenomatoid tumors of the uterus. Int J Gynecol Pathol. 1992;11:156–160. 21. Palacios J, Manrique AS, Villaespesa AR, et al. Cystic adenomatoid tumor of the uterus. Int J Gynecol Pathol. 1991;10:296–301. 22. Tiltman AJ. Adenomatoid tumours of the uterus. Histopathology. 1980;4:437–443. 23. Terada T. An immunohistochemical study of adenomatoid tumors of the uterus and fallopian tube. Appl Immunohistochem Mol Morphol. 2012;20:173–176.
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Magnetic Resonance Imaging and Pathologic Findings of 26 Cases With Uterine Adenomatoid Tumors Qiuhua Meng, MD, PhD,* Qingsi Zeng, BS,* Xiaomei Wu, MD, PhD,* Qi Wan, MD,* Yongxia Lei, MD,* Ting Song, MD, PhD,† Xia Gu, MD, PhD,‡ Guobing Hong, MD, PhD,§ Wenhao Zhang, BS,* and Xinchun Li, MD, PhD* Objective: To analyze the magnetic resonance imaging (MRI) features and pathologic findings of uterine adenomatoid tumors (ATs) for improved diagnostic accuracy and facilitating differential diagnosis of the tumors. Methods: We investigated retrospectively 26 patients with uterine ATs confirmed by pathology. Before operation, all patients accepted multiple MRI scans, including T1-weighted image (T1WI), T2-weighted image (T2WI), T2WI/spectrally adiabatic inversion recovery, and T1-weighted enhanced imaging. Two radiologists reviewed all the MRI sequences on PACS workstations for all patients to evaluate the location, shape, size, margin, intensity, and enhancement of ATs. Results: All uterine ATs exhibited either single round solid (n = 24) or predominantly cystic (n = 2) masses with either well-defined (n = 23) or ill-defined margin (n = 3). The diameter range of the tumors was 1.0 to 7.0 cm (mean, 3.8 cm). Solid masses were isointensive on T1WI and hypointensive on T2WI with moderate enhancement. The degree of enhancement in solid tumors was either lower than (18/24 [75%]) or equal to (6/24 [25%]) that of the myometrium. Predominantly cystic masses presented as cystic lesions with a little irregular solid nodule inside. The cystic parts were hypointensive on T1WI and hyperintensive on T2WI without enhancement, whereas the solid nodules were isointensive on both T1WI and T2WI with moderate enhancement. A large part of the uterine ATs (69.2% [18/26]) coexisted with other uterine diseases. On pathology, uterine ATs were characterized as gland-like structures with irregular expansion of tubular cavities, which might be correlated with low enhancement of tumors. The tumors were lined with flat or cuboidal mesothelial cells and residue of smooth muscle component, which might contribute to their hypointensive appearance on T2WI. Conclusions: Small solid uterine masses with homogeneous hypointensity on T2WI and lower enhancement or cystic lesions with inner irregular solid nodule may indicate the diagnosis of uterine ATs, and final diagnosis can be determined with pathology. Key Words: adenomatoid tumor, uterus, magnetic resonance imaging, pathology (J Comput Assist Tomogr 2015;39: 499–505)
A
denomatoid tumor (AT) was firstly named by Golden and Ash,1 in 1945, which is an extremely rare benign mesothelial tumor arising in the genital systems of both males and females, such as epididymis, uterus, fallopian tubes, and ovaries. In females, the most common sites are in the fallopian tubes and the uterus.1,2 It occasionally occurs outside the genital systems, From the *Department of Radiology, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, PR China; †Department of Radiology, The Third Affiliated Hospital of Guangzhou Medical University, Guangzhou, PR China; ‡Department of Radiology, The Fifth Affiliated Hospital of Sun Yat-sen University, Zhuhai, PR China; and §Department of Pathology. The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, PR China. Received for publication November 8, 2014; accepted March 4, 2015. Reprints: Xinchun Li, MD, PhD, Department of Radiology, The First Affiliated Hospital of Guangzhou Medical University, 151 Yanjiangxi Rd, Guangzhou, PR China, 510120 (e‐mail: [email protected]). The authors declare no conflict of interest. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
including adrenal gland, pancreas, peritoneal, omentum, and mesentery.3 Uterine ATs are benign mesothelial tumors composed of gland-like structures arising in uterine serosa and myometrium. Although diagnosis of uterine ATs increased in recent years due to advanced technology (radio scanning, electron microscope, immunohistochemistry),4 most of them were misdiagnosed as leiomyoma because uterine ATs shared the same imaging features of leiomyoma.5 Although AT and leiomyoma are both benign tumor, a few large leiomyomas have increased risk of malignancy, whereas recurrence or metastasis has never been reported in ATs.5 Moreover, leiomyoma is sensitive for hormone therapy, whereas AT has unclear responses to hormone therapy.5 In case AT is misdiagnosed as leiomyoma, unnecessary hormone therapy may be administrated. The identification of ATs also helps in postoperative counseling because ATs do not recur but fibroids may do.6 Therefore, it is important to differentiate ATs from other benign diseases. To our best knowledge, up to now, there are only a few reports describing briefly magnetic resonance imaging (MRI) appearance of ATs. Mitsumori et al5 reported 2 cases of solid ATs with well-defined margin. Kim et al7 reported one case presented as a cystic mass. Harada et al2 reported a cystic ATwhich appeared as a high-intensity area on T2-weighted image (T2WI) with the margin and septum of the tumor enhanced slightly. The comprehensive MRI features of uterine ATs have not been investigated in detail yet. The purpose of the present study is to analyze the MRI features and pathologic findings of uterine ATs for improved diagnostic accuracy and facilitating differential diagnosis of the tumors.
MATERIALS AND METHODS Patients This retrospective study was approved by the institutional review board with a waiver of the written informed consent. We searched for patients with uterine ATs in the pathologic database in our hospital between January 2005 and June 2013. All ATs were confirmed by pathology. The inclusion criteria were as follows: (1) patients underwent surgical resection, (2) pelvis MRI images were available, (3) and clearly position-marked lesions in gross pathology when there were multiple lesions. The exclusion criteria were as follows: (a) no quality MRI images were available (n = 1), (b) lesions were not clearly position-marked in gross pathology (n = 1), and (c) position-marked lesions in gross pathology could not be corresponded to the position of lesions on MRI images (n = 3). Among inclusive cases, most uterine ATs (23/26 [88.5%]) were misdiagnosed as leiomyoma by MRI and ultrasound. The average patient age was 41 years (range, 24–58 years). The clinical symptoms were various: a mass on lower abdomen (n = 4), vaginal irregular bleeding (n = 14), belly ache (n = 5), and no apparent symptoms (n = 3). Eighteen cases had other diseases, including uterine fibroids, adenomyosis, endometrial cancer, uterine cervix cancer, appendix abscess, and cyst. All
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patients underwent surgical resection including hysterectomy and laparoscopic tumor excision. The time interval between the MRI scan and surgery was 7 days or less. The tumors did not recur after operation for 1-year imaging follow-up, which was performed by a single gynecologic radiologist.
MRI Scans Magnetic resonance imaging was performed in all cases with a 1.5-T unit (Nova Dual; Philips, Amsterdam, the Netherlands) and a body phased-array coil. T1-weighted image (T1WI; repetition time [TR]/echo time [TE], 300–500/10–20 milliseconds), T2WI (TR/TE, 3200–3500/80–100 milliseconds), and T2WI/the spectrally adiabatic inversion recovery (SPAIR) sequence (T2WI/ SPAIR; TR/TE: 3200–3500/80–100 milliseconds) were performed with the matrix of 512 512, field of view of 350 to 450 mm, number of signals averaged of 2 to 4, and slice thickness/gap of 5–6/1.0 mm. Gadodiamide injection (GE Healthcare, Ireland) was injected in all patients at a dose of 0.1 mmol/kg when performing contrast-enhanced MR scanning including axial, sagittal, and coronal fat-suppressed T1-weighted sequences. Two gynecologic radiologists both with more than 15-years experience reviewed in consensus the MRI characteristics of ATs on PACS workstations, without knowing histopathologic results. The MRI characteristics included location, shape, size, margin, intensity, and enhancement. An AT was in submucosa when 80% portion of the AT was located in the submucosa or in subserosa when 80% portion of the AT was located in the subserosa. The signal intensity was evaluated on T1WI, T2WI, and postcontrast images. For size, the term diameter of a tumor indicated “the maximum diameter” on T2WI. If the margin could be clearly identified on T2WI or on contrast-enhanced images, it was called “well defined.” On the contrary, if the margin could not be clearly identified, it was called “ill defined.” The pseudocapsule was referred to a circular ring around the tumor with low or high intensity on T2WI and enhanced T1WI. For the degree of enhancement of ATs, we used myometrium enhancement as a reference. If the enhancement of lesion was lower or higher than the myometrium enhancement, it was called “lower or higher enhancement.” If the enhancement of lesion was equal to enhancement of
myometrium, it was called “iso-enhancement.” The lesions were categorized into 3 types: solid, solid-cystic, and predominantly cystic. Predominantly cystic or solid-cystic ATs in this study were referred to the tumors mainly composed of cystic lesions (cystic portion ≥ 80% or 50% ≤ cystic portion < 80%, respectively, showed as hyperintense in T2WI and no enhancement after gadolinium administration), with or without solid nodule inside the lesion.
Pathology Examination All tumors were removed by surgery (the marking of the lesions was done according to the position of the tumor by the surgeon before pathology judge), fixed in 10% neutral formalin, embedded in paraffin, sliced, and hematoxylin and eosin (HE) stained. Among them, 6 cases were also stained by specific stain such as Alician blue and periodic acid–Schiff. Immunohistochemical (IHC) staining was used in 13 cases to differentiate ATs from other diseases. Immunohistochemical antigens included claritin (CR), mesothelial cell (MC), cluster of differentiation 34 (CD34), cytokeratin (CK), vimentin (VIM), muscle-specific actin (SMA), and Wilms tumor 1 (WT-1). All specimens were reviewed together by 2 pathologists. The diagnosis of uterine ATs was made when there was evidence showing that tumor had gland-like structure or irregular expansion of the tubular cavities, lined with flat or cuboidal neoplastic cells. In case diagnosis of AT could not be reached in consensus, IHC staining was ordered. Adenomatoid tumor was positive to CR, MC, or CK but negative to CD34, which indicated a mesothelial origin.
RESULTS Location, Size, and Shape All tumor exhibited as either a single round solid mass (n = 24; Figs. 1–4) or a predominantly cystic round mass (n = 2; Figs. 5 and 6). The locations included uterine horn (3 cases), lateral wall of the uterine body (2 cases), the anterior wall (12 cases), the posterior wall (6 cases), the submucosa (1 case), and the subserosa (2 cases; Fig. 4). The diameter of the tumor was 1.0 to 7.0 cm (mean, 3.8 cm): 5 cases, at least 5 cm; 7 cases, 3 to 5 cm; and 14 cases, less than 3 cm.
FIGURE 1. A–F, A 40-year-old woman with uterine AT (long arrow; B): the tumor appears homogeneously isointensive on axial T1WI (A) and heterogeneously hypointensive on T2WI with iso and high-intensity signals inside (B, D). C and E, The tumor exhibited obvious enhancement equal to the myometrium, and the margin was well defined with a pseudocapsule (short arrow) on contrast-enhanced axial/sagittal T1WI image. F, On microscopy, tumor was composed of canalicular spaces (diamond arrow) lined with flattened cells and admixed with smooth muscle and fibrous tissue (HE stain, original magnification 100). Figure 1 can be viewed online in color at www.jcat.org.
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FIGURE 2. A–I, A 26-year-old women with uterine AT (long arrow; D) in the posterior wall of the uterus (forked tail arrow; D):the tumor appears homogeneously hypointensive on axial T1WI (A) and nearly homogeneously hypointensive (long arrow) on T2WI (B, D), which exhibited heterogeneously moderate enhancement (long arrow; C), and the enhancement degree was lower than that of the myometrium on contrast-enhanced axial/sagittal T1WI image (C, E). F, On microscopy, the tumor was composed of canalicular spaces lined with flattened cells and admixed with smooth muscle (diamond arrow) and fibrous tissue (HE stain, original magnification 100). G–I, Immunohistochemical staining demonstrated positive to CR, MC, and WT-1 (original magnification 100; long arrow). Figure 2 can be viewed online in color at www.jcat.org.
MRI Findings Solid tumors were isointensive on T1WI, hypointensive on T2WI (Fig. 3), and moderately enhanced (with heterogeneous
patterns in 6 cases [Fig. 3] and homogeneous patterns in 18 cases [Fig. 4]). Degree of enhancement was either lower than (n = 18; Fig. 4) or equal to that of the myometrium (n = 6; Fig. 1). The ATs had either well-defined (21/24 [87.5%]) or ill-defined
FIGURE 3. A–F, A 44-year-old women with uterine AT (long arrow; B, E) in the right lateral wall and uterine adenomyoma (black short arrow; B, E) in the left lateral wall of the uterus (forked tail arrow; B): the tumor appeared homogeneously isointensive on axial T1WI image (A) and nearly homogeneously hypointensive on T2WI image (B, D). D and E, The tumor exhibited heterogeneous obvious enhancement; the enhancement degree was the same as the myometrium on contrast-enhanced axial/coronal T1WI image. F, On microscopy, the tumor was composed of gland-like structure lined with flattened cells and admixed with smooth muscle and fibrous tissue (HE stain, original magnification 100). Figure 3 can be viewed online in color at www.jcat.org. © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 4. A–H, A 38-year-old women with uterine AT (long arrow; B) at the left subserosa and uterine fibroids (short arrow; B) with septum (diamond arrow; B) in the posterior wall of the uterus (forked tail arrow): the tumor appears homogeneously hypointensive, relative to the myometrium on axial T1WI image (A), and nearly homogeneously hypointensive on T2WI (B, C). D, The tumor exhibited homogeneously moderate enhancement on contrast-enhanced coronal T1WI image (long arrow). E, On microscopy, the tumor was composed of gland-like structure lined with flattened cells and admixed with smooth muscle and fibrous tissue (HE stain, original magnification 100). F–H, Immunohistochemical staining was positive to CR, MC, and VIM (original magnification 200; long arrow). Figure 4 can be viewed online in color at www.jcat.org.
margins (3/24 [12.5%]). The margins appeared most clear on T2WIs and enhanced T1WIs. Among all the solid tumors, 6 cases had patchy signals of lower intensity on T1WI and slightly higher intensity on T2WI, and 2 cases had signals of circular low intensity
on T2WI and enhancement around the tumor, which resembled signs of pseudocapsule (Fig. 1; Table 1). The predominantly cystic masses presented as well-defined cystic lesions with an irregular solid nodule inside. The cystic
FIGURE 5. A–F, A 58-year-old women with uterine AT (long arrow; D) at the anterior wall of the uterus (forked tail arrow; D) and endometrial cancer inside the cavity of the uterus (short arrow, D); the tumor presented as a cystic lesion (long arrow; B) with an irregular solid nodule inside (black short arrow; B), of which cystic parts showed low intensity on T1WI (A) and obviously high intensity on T2WI (B) without enhancement, and solid parts demonstrated nearly the same intensity as myometrium on T1WI, T2WI, and enhanced T1WI (long arrow; E). F, On microscopy, the tumor was composed of canalicular spaces, lined with flat or cuboidal MCs and smooth muscle (HE stain, original magnification 100). Figure 5 can be viewed online in color at www.jcat.org.
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FIGURE 6. A–F, A 36-year-old women with uterine AT (long arrow, A) at the right subserosa of the uterus: The tumor presented as a cystic lesion (long arrow, B) with an irregular solid nodule inside (black short arrow, B), of which cystic parts showed low intensity on T1WI (A), and solid parts demonstrated nearly the same intensity as the myometrium on T1WI and obviously high intensity on T2WI without enhancement, T2WI, and enhanced T1WI (long arrow; D). E, On microscopy, the tumor was composed of angiomatous-like cavities, lined with flat or cuboidal MCs and smooth muscle (HE stain, original magnification 100). F, Mucus appeared as blue in the cavity (Alician blue, original magnification 100; long arrow). Figure 6 can be viewed online in color at www.jcat.org.
parts had low-intensity signals on T1WI and high-intensity signals on T2WI without enhancement, whereas the solid parts demonstrated nearly the same intensity as the myometrium on T1WI, T2WI, and contrast-enhanced T1WIs (Fig. 6).
Accompanying Lesions Eighteen cases of uterine ATs were associated with other uterine diseases including uterine leiomyoma (16 cases [61.54%]; Fig. 4), uterus adenomyosis (5 cases [19.23%]; Fig. 3), endometrial cancer (1 case [3.80%]; Fig. 5), uterine cervix cancer (2 cases [7.6%]), appendix abscess (1 case [3.80%]), and cyst (4 cases [15.38%]). Ascites or metastases were not found in all cases. The 16 concurrent uterine fibroids encountered along with ATs were round solid masses. The tumors were isointensive on T1WI, hypointensive on T2WI (heterogeneous with necrosis, septum, or sign of whirlpool in 13/16 [or 82%] cases [Fig. 4] and homogeneous in 3/16 [18%] cases), and with different degrees of enhancement (heterogeneous in 13/16 [82%] cases [Fig. 4] and homogeneous in 3/16 [18%] cases). Degree of enhancement was higher than (11/16 [69%] cases) or equal to (2/16 [13%] cases)
TABLE 1. MRI Features of ATs
Imaging Feature Cystic Solid Homogeneous hypointensity on T2WI/SPAIR Patchy higher intensity on T2WI/SPAIR Lower enhancement Homogeneous enhancement Well-defined margin Signs of pseudocapsule
No. Positive Cases
No. Total Cases
%
2 24 18
26 26 24
7.7 92.3 75
6
24
25
18 18 21 2
24 24 24 24
75 75 87.5 8.3
that of the myometrium. The tumors all had well-defined margin, and 8 (50% [8/16]) cases showed signs of pseudocapsule. The 5 concurrent uterine adenomyosis encountered along with ATs were all diffusive and they appeared hypointensive with mixed multiple punctate hyperintensive signals on T2WIs and isointensive on T1WIs with an ill-defined margin (Fig. 3).
Pathologic Findings The ATs were located intramurally (n = 23), subserosally (n = 2), or submucosally (n = 1). No capsule was found on gross specimens of the tumors. The tumor color on the cutting surface was gray-white or gray-yellow, and degenerative areas, cavity, or mucus was found on a few tumors (8 cases [30.7%]). Under microscopy, tumor morphology was variable and appeared as adenoid, angiomatous, lacuna, or cystic structures in the hyperplasia of smooth muscle tissue, lined with flat or cuboidal MCs. Mucus could be detected in 2 cases (Fig. 6). According to histologic types of ATs studied by Quigley and Hart,3 the adenoid type and angiomatoid type were most frequent. Combinations of 2 or more patterns occurred in all tumors, but usually 1 major type prevailed in each case. Immunohistochemical analysis revealed that ATs stained positive to CR (13/13 [100%]), MC (12/13 [92.3%]), CK (10/13 [76.9%]), VIM (8/13 [61.5%]), SMA (6/13 [46.2%]), and WT-1 (5/13 [38.5%]) and negative to CD34 (13/13 [100%]; Figs. 2 and 4).
DISCUSSION Uterine AT is an uncommon benign tumor which can be found in 1.2% of all women.8 The actual incidence is probably higher because of misdiagnosis and missed diagnosis.9 The tissue origin of uterine ATs has been debated for many years. The hypotheses include middle kidney, mesothelium, müllerian epithelium, and vascular derived. Some scholars ever considered ATs as a reaction to inflammation but not a real tumor.10,11 Pathologists struggled investigating this tumor. It was found recently that AT cells expressed CK, VIM, and calretinin, indicating its originating from mesothelium.10,12,13 Adenomatoid tumors were
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officially classified as mesothelial tumors by World Health Organization in the 2003 revision.14 Uterine ATs often occur in women in reproductive ages. Patient's age at the initial diagnosis ranges from 26 to 55 years (with mean age of 41 years) in the literature.15,16 In our study, the average age was 41 years (range, 24–58 years), consistent with previous studies. Clinical manifestations of uterine ATs are nonspecific and variable, including vaginal bleeding, menorrhagia, and abdominal masses.17 Most of uterine ATs are located in the uterus wall, the subserosa near the uterine horn.4,7 The tumors often present as a solitary solid mass with the diameter ranging from 2 to 10 cm (usually small, mean diameter of 2.1 cm).10 In gross examination, ATs are soft and moist; some cases have mucus degeneration. The tumors can show invasive growing patterns due to the lack of capsules.6,18 Pseudocapsules were observed occasionally in a few reports.7 Under microscopy, the tumor is characterized by having gland-like structures and irregular expansion of the tubular cavities, lined with flat or cuboidal MCs and with stromal fibrous and residue of smooth muscle components.19,20 Common histologic types of ATs include adenoid type, angiomatous type, solid type, and cystic type.3,7,10,21 Another classification method was proposed by Tiltman22: plexiform, tubular, canalicular, and mixed types. However, up to now, there were no unified classification standards. The adenoid type in the first classification method corresponds to the tubular type in the second classification method, the angiomatoid type corresponds to the canalicular type, and the solid type corresponds to the plexiform type. Quigley and Hart3 found that there were 2 types or more than 2 kinds of organizations, with one of them being predominant. In our study, we also found that combinations of 2 or more patterns occurred in all tumors, and usually one prevailed in each case. Adenoid and angiomatous types were the most common patterns in our study. It was reported that uterine ATs were positive to VIM and CK, whereas negative to CD34, periodic acid–Schiff, and EMAF8.4,21 In 13 cases with IHC stain in our study, ATs were positive to antigens of mesothelial or epithelial-derived origin, that is, CR (100%), MC (92.3%), CK (76.9%), VIM (61.5%), SMA (46.2%), and WT-1 (38.5%), consistent with previous reports.4,22 The treatment for uterine ATs was usually surgical resection, including hysterectomy and laparoscopic tumor excision. The prognosis was good and recurrence or metastasis had never been reported in the literature. In this study, no tumors recurred in the 1-year follow-up after the operation. Magnetic resonance imaging plays an important role in pelvis disease. The MRI appearance of uterine ATs was firstly described by Mitsumori et al5 (2 solid mass). It was found that uterine ATs appeared a single solid, small, well, or ill-circumscribed mass locating in the myometrium or serosa with low signal intensity in T1WIs and low or high signal intensity in T2WIs. These masses might show mild to moderate enhancement after gadolinium administration.3,7,16 The rare appearance of ATs included cystic type, diffuse type, and infarction type.21–23 In our series, there were 2 types: solid pattern (24/26 [92.3%]) and predominantly cystic pattern (2/26 [7.7%]). The results also indicated that solid pattern was the most common appearance of uterine ATs. Solid ATs were often hypointensive on T2WI. It might be related to tumor containing much smooth muscle. Solid ATs presented moderate enhancement and degree of enhancement was usually lower than that of the myometrium (18/24 [75%]), probably due to the reduction of interstitial vessel resulting from the lacunar-like arrangement of ATs tumor cells. In predominantly cystic ATs, the cystic parts were not enhanced, whereas the irregular solid nodule was moderately enhanced. The 2 predominantly cystic cases corresponded to the angiomatous type under microscopy. The findings described earlier are consistent with previous reports.2,7 Although they lack capsules, due to its expansion, most margins
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of the tumors (21/24 [87.5%]) in our cases appeared well defined in the T2WI and contrast-enhanced T1WI. Among them, 2 cases appeared circular hypointensive in the T2WI and enhanced T1WI around the tumor, resembling signs of pseudocapsule, consistent with the report of Mitsumori etal.5 Our results indicated that a well-defined margin was the common characteristic of most uterine ATs. Uterine ATs usually coexisted with other diseases such as uterine fibroids and adenomyosis. Adenomatoid tumors and leiomyomas were reported to coexist in 60% cases, possibly due to ATs stimulating smooth muscle hyperplasia.10 In this study, there were also 16 cases (16/26 [61.54%]) of uterine ATs accompanying with uterine fibroids, which could be easily misdiagnosed as multiple uterine leiomyomas. Uterine ATs should be differentiated from following diseases. First, uterine fibroids appear hypointensive or isointensive in the T2WI and resemble ATs due to containing a large number of smooth muscle cells. It is difficult to differentiate them based solely on MRI appearance, especially when the tumor is small. However, there are a few clues to distinguish them according to the literature5,10 and our study: (1) the diameter of ATs is often less than 5 cm, whereas that of uterine fibroids is often larger than 5 cm; (2) ATs are likely homogeneous with little necrosis in the T2WIs, whereas uterine fibroids are heterogeneous in the T2WIs with necrosis, septum, and sign of whirlpool due to degeneration; (3) degree of enhancement in ATs is likely lower than that of uterine fibroids; and (4) sign of pseudocapsule in ATs is much lower than that in uterine fibroids. Second, uterine adenomyoma appears hypointensive with mixed multiple punctate hyperintensity in the T2WI and or isointensive or hyperintensive (ectopic endometrial island bleeding) in the T1WI with a well- or illcircumscribed margin and accompanied by uterus junctional zone thickening, which can be used to easily differentiate uterine adenomyoma from most ATs. Finally, uterine sarcoma is usually a larger mass showing signals hypointensive in the T1WI and slightly hyperintensive in the T2WI with obvious necrosis and cystic change, which may help to differentiate uterine sarcoma from uterine ATs. In summary, the imaging features of uterine ATs include a small solid mass with well- or ill-defined margin, homogeneously hypointensive in the T2WI, and lower enhancement, or cystic lesion with irregular solid nodule. One should pay attention to the possibility of ATs in the differential diagnosis of uterine masses. Confirmation diagnosis of ATs should be based on pathologic and IHC analyses. ACKNOWLEDGMENT We thank Mrs Gu Yinyin for pathologic diagnosis for this article. REFERENCES 1. Golden A, Ash JE. Adenomatoid tumors of the genital tract. Am J Pathol. 1945;21:63–79. 2. Harada N, Nobuhara I, Haruta N. Giant cystic adenomatoid tumour of the uterus. J Obstet Gynaecol. 2012;32:407–408. 3. Quigley JC, Hart WR. Adenomatoid tumors of the uterus. Am J Clin Pathol. 1981;76:627–635. 4. Irikoma M, Takahashi K, Kurioka H, et al. Uterine adenomatoid tumors confirmed by immunohistochemical staining. Arch Gynecol Obstet. 2001;265:151–154. 5. Mitsumori A, Morimoto M, Matsubara S, et al. MR appearance of adenomatoid tumor of the uterus. J Comput Assist Tomogr. 2000;24:610–613.
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6. Kalidindi M, Odejinmi F. Laparoscopic excision of uterine adenomatoid tumour: two cases and literature review. Arch Gynecol Obstet. 2010;281:311–315. 7. Kim JY, Jung K, Sung N K, et al. Cystic adenomatoid tumor of the uterus. AJR Am J Roentgenol. 2002;179:1068–1070. 8. Christensen C. Adenomatoid tumours of the uterus. Eur J Gynecol Oncol. 1990;11:85–89. 9. Nakayama H, Teramoto H, Teramoto M. True incidence of uterine adenomatoid tumors. Biomed Rep. 2013;1:352–354. 10. Nogales FF, Isaac MA, Hardisson D, et al. Adenomatoid tumors of the uterus: an analysis of 60 cases. Int J Gynecol Pathol. 2002;21:34–40. 11. Ross MJ, Welch WR, Scufiy RE. Multilocular peritoneal inclusion cysts (so-called cystic mesotheliomas). Cancer. 1989;64:1336–1346. 12. Christensen C, Bichel P. Adenomatoid tumor of uterus case report. Br J Obstet Gynaecol. 1988;95:524–526. 13. Sangoi AR, McKenney JK, Schwartz EJ, et al. Adenomatoid tumors of the female and male genital tracts: a clinicopathological and immunohistochemical study of 44 cases. Mod Pathol. 2009;22:1228. 14. Tavasso Ii FA, Devilee P. WHO Classification of Tumor, Pathology and Genetics of Tumor of the Breast and Female Genital Organs. Lyon: IARC press; 2003:243–244.
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15. Saran M, Sanghi A, Faruqi A. Adenomatoid tumor of the uterus presenting as cyst. J Obstet Gynaecol. 2007;27:637–638. 16. Huang CC, Chang DY, Chen CK, et al. Adenomatoid tumor of the female genital tract. Int J Gynecol Obstet. 1995;50:275–280. 17. Schwartz EJ, Longacre TA. Adenomatoid tumors of the female and male genital trInt. J Gynecol Pathol. 2004;23:123–128. 18. Sieunarine K, Cowie AS, Bartlett JD, et al. A novel approach in the management of a recurrent adenomatoid tumor of the uterus utilizing a Strassman technique. Int J Gynecol Cancer. 2005;15:671–675. 19. Hanada S, Okumura Y, Kaida K. Multicentric adenomatoid tumors involving uterus, ovary, and appendix. J Obstet Gynaecol Res. 2003;29:234–238. 20. De Rosa G, Boscaina A, Terracciano LM, et al. Giant adenomatoid tumors of the uterus. Int J Gynecol Pathol. 1992;11:156–160. 21. Palacios J, Manrique AS, Villaespesa AR, et al. Cystic adenomatoid tumor of the uterus. Int J Gynecol Pathol. 1991;10:296–301. 22. Tiltman AJ. Adenomatoid tumours of the uterus. Histopathology. 1980;4:437–443. 23. Terada T. An immunohistochemical study of adenomatoid tumors of the uterus and fallopian tube. Appl Immunohistochem Mol Morphol. 2012;20:173–176.
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