Original Article
Invasive cribriform carcinoma of the breast: mammographic, sonographic, MRI, and 18 F-FDG PET-CT features
Acta Radiologica 2015, Vol. 56(6) 644–651 ! The Foundation Acta Radiologica 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0284185114538425 acr.sagepub.com
Young Ju Lee1, Bo Bae Choi1 and Kwang Sun Suh2
Abstract Background: Invasive cribriform carcinoma (ICC) of the breast is a rare type of invasive carcinoma which shows a favorable prognosis and a lower frequency of axillary nodal metastases. Few imaging findings related to ICC have been reported. Purpose: To evaluate imaging findings with multiple imaging techniques in ICC of the breast. Material and Methods: Twenty-eight cases of histopathologically proven ICC of the breast were gathered for this study. We retrospectively reviewed the mammographic, sonographic, and magnetic resonance imaging (MRI) findings of ICC according to the American College of Radiology (ACR) breast imaging reporting and data system (BI-RADS) lexicon. 18 F-fluorodeoxyglucose positron emission tomography-computed tomography (18 F-FDG PET-CT) findings were also evaluated. Microscopic slides of surgical specimens were reviewed by a breast pathologist. Results: The mean age of the patients was 51 years. The most common mammographic findings were irregular shape (72.8%), spiculated margin (63.7%), and a high density (81.8%) mass. Microcalcifications were noted in 9/28 cases. The most common shape was pleomorphic (66.7%). The most common sonographic findings were irregular shape (77.8%), spiculated margin (29.6%), hypoechogenicity (81.5%), and no posterior acoustic features (85.2%). On MRI, most ICCs presented as irregular shaped mass (62.0%) and irregular (42.9%) margin. All four patients (16.0%) who presented with non-mass-like enhancement pattern showed a segmental distribution. The 18 F-FDG PET-CT showed a mean maximum standardized uptake value (SUVmax) of 5.90. Axillary nodal metastases were found in 17.9% (5/28) of the surgical specimens. Immunohistochemical studies showed a high positivity for estrogen and progesterone receptor (100% and 87.5%, respectively). Conclusion: The imaging features of invasive cribriform carcinoma are highly suggestive of malignancy and are not distinguishable from those of other breast cancers like infiltrating ductal carcinoma.
Keywords Breast, neoplasms – primary, mammography, ultrasound, magnetic resonance imaging (MRI), positron emission tomography (PET) Date received: 28 November 2013; accepted: 4 May 2014
Introduction Invasive cribriform carcinoma (ICC) is an unusual type of primary breast carcinoma that is composed of predominantly cribriform invasive components (1,2). In 1983, Page et al. initially described a separate histological type of breast carcinoma upon reviewing the histology and clinical data of 1003 invasive breast carcinomas (1). It was characterized as having a more favorable prognosis than ordinary breast carcinoma, and axillary node metastasis were uncommon (1,3,4).
1 Department of Radiology, Chungnam National University Hospital, Daejeon, Republic of Korea 2 Department of Pathology, Chungnam National University Hospital, Daejeon, Republic of Korea
Corresponding author: Bo Bae Choi, Department of Radiology, Chungnam National University Hospital, 282 Munhwa-ro, Jung-gu, Daejeon 301-721, Korea. Email: [email protected]
Lee et al. To the best of our knowledge, radiological reports on their imaging characteristics are limited because ICCs occur infrequently only. Previous studies consist of two case reports and two retrospective studies (5–8). The number of previously reported cases was low and the studies reported various findings on mammography, sonography, and magnetic resonance imaging (MRI). The purpose of this study was to investigate whole-breast imaging findings of ICC, including mammography, sonography, MRI, and 18 F-fluorodeoxyglucose positron emission tomography-computed tomography (18 F-FDG PET-CT).
Material and Methods Thirty-six patients with invasive cribriform carcinoma were identified in our computerized pathology database between July 2006 and February 2013. Five patients were excluded because the final pathologic diagnosis of the specimen was infiltrating ductal carcinoma (IDC), despite being confirmed as ICC on core-needle biopsy. Three more patients were excluded because radiologic images were not available. In total, 28 patients were included in this study. By mammography, craniocaudal and mediolateral oblique views were obtained using a Mammomat 3000 (Siemens Medical Solutions, Solna, Sweden) and Lorad M3 (Hologic Inc., Boston, MA, USA) mammography unit. Parenchymal patterns on mammograms were categorized as one of the following: almost entirely fatty; scattered fibroglandular tissue; heterogeneously dense; extremely dense. Each mammographic lesion was analyzed for mass characteristics (i.e. shape, margin, density), presence of architectural distortion, and the type of microcalcification according to the American College of Radiology (ACR) breast imaging reporting and data system (BI-RADS) lexicon. Ultrasound (US) was performed using a HDI 5000 (Advanced Technology Laboratories, Bothell, WA, USA) or IU22 (Philips Ultrasound, Bothell, WA, USA) US systems with a 5–12 MHz linear probe. We examined both breasts and the axillary lymph nodes. US imaging findings were reviewed for shape, orientation, margin, boundary, echogenicity, posterior acoustic features, and associated calcifications, and categorized according to the ACR BI-RADS final assessment. The largest diameter obtained from either the sagittal or transverse views was recorded as the maximum tumor diameter. On the basis of previous studies, we defined the presence of axillary lymph node metastasis on US when the lymph node had at least one of these findings: a mean longitudinal-transverse axis ratio of less than 1.5, presence of eccentric cortical thickening, or loss of a central fatty hilum (9).
645 MRI was performed using a 1.5-T scanner (Signa Excite, GE Healthcare, Milwaukee, WI, USA) equipped with a breast coil. Images were acquired in axial plane with the following sequences: axial, T2weighted, fat-suppressed, fast spin-echo imaging (TR/ TE, 5000/86; flip angle, 90 ; field of view [FOV], 300 mm; acquisition matrix, 256 256; number of excitations (NEX), 3; slice thickness, 4.5 mm); pre- and postcontrast, axial, T1-weighted (T1W) three-dimensional (3D) fast spoiled gradient-recalled echo sequence with parallel volume imaging (VIBRANT, GE Healthcare) (TR/TE, 6.5/3.1; flip angle, 10 ; FOV, 300 mm; acquisition matrix, 350 350; NEX, 1; slice thickness, 1.1 mm). Gadodiamide (Omniscan, GE Healthcare, Oslo, Norway) was administered as contrast agent with an intravenous bolus injection (0.2 mmol per kg of body weight) at 3 mL/s. Imaging was performed before the intravenous contrast agent bolus injection and four times after this injection for a period of 7.3 min. The image postprocessing, included the subtraction of unenhanced images from enhanced images, sagittal reformations, and 3D maximum-intensity projections by using the first contrast-enhanced series. The interpretation of the degree and patterns of enhancement was performed by visual assessment. Associated findings were recorded, such as nipple retraction, skin thickening, lymphadenopathy, hematoma, and invasion of the pectoralis muscle or chest wall. All mammograms, sonograms, and MR images were retrospectively reviewed in consensus by one radiologist with 6 years of experience in breast imaging and by one resident. 18 F-FDG PET-CT imaging was performed using a Discovery ST-16 system (GE Healthcare, Milwaukee, WI, USA). Normal fasting blood glucose levels (after fasting for at least 6 h) were determined to be 0.05). Accordingly, we found that the microcalcification in ICC should not to be related to DCIS components. An irregular shaped and irregular marginated mass was the most common MRI appearance in our study. So far, the MRI features of ICC have been described in one case only (7). Lim et al. reported that ICC displayed an oval shaped mass with homogenous early enhancement and delayed washout pattern based on the kinetic curve analysis (7). In the present study, the four remaining patients presented with a non-mass-like enhancement with segmental distribution (16.0%). Of those four patients, only three patients underwent surgery. In those patients, the mean extent of the primary lesion was 5.0 cm (range, 4.7–5.3 cm) at MRI. The histopathology report revealed that approximately 43.3% of the DCIS was associated with invasive cancer. The mean histologic size of the invasive carcinoma was 1.1 cm (range, 0.9–1.3 cm), which was smaller than the extent of the primary lesion at MRI. Previous studies explained that DCIS have a high relationship with non-mass-like enhancement (17–19). We postulate the different MRI presentation such as the non-masslike enhancement may be primarily due to DCIS components. We also investigated the 18 F-FDG PET-CT images of ICCs, which has not been reported yet. In our study, 87.0% (20/23) of lesions showed FDG uptake. Many published studies with preoperative 18 F-FDG PET-CT in patients with primary breast carcinoma have suggested that higher levels of FDG uptake are significantly correlated with a poor prognosis, similar tumor invasiveness (>2 cm), higher histological grade, negative hormonal receptor status, axillary lymph node metastasis, and histological type of primary breast carcinoma (IDC in comparison with invasive lobular carcinoma [ILC]) (20–26). Primary breast cancers with FDG high uptake (range, 4.1–7.4) are considered to have poor prognosis compared to those with low FDG uptake (range, 2.8–5.2) (27–30). The mean SUVmax value of the primary tumor was 5.90 (range, 1.2–14.3) in the present study. Compared with the aforementioned reports, our result of ICC showed relatively higher values, even though ICC has a favorable prognosis and a well-differentiated tumor. False negative results were found in 13% (3 of 23) of the patients. The false negative rate by PET-CT has been reported to be 23.7–46.5% in IDC and
650 60–65.2% in ILC (29,30). Low sensitivity was described for the detection of small lesions (10 mm) and lower histological grades on FDG PET in patients with primary breast carcinoma (30). The authors explained that a high rate of false negative result in ILC was affected by different microscopic growth pattern, such as lower tumor cell density and diffuse infiltration of the surrounding tissue (26,27,29). In our study, the tumor size was smaller than 1 cm and the histological grade was also well-differentiated in three patients with false negative findings. We postulate these factors could be a cause of false negative findings in the present study. The false negative rate of ICC in our study was relatively lower than that of IDC and ILC in previous reports (29,30). Because of the relatively small number of subjects, further research is necessary to evaluate the PET-CT findings of ICC and to compare them with IDC and ILC. Pure ICC is characterized by lower rates of axillary lymph node involvement, higher positive rates of ER and/or PR expression than in mixed ICC and IDC (1,3,4,31). Those characteristics are one of the important prognostic factors for breast cancer. In our cases, axillary nodal metastases were identified in only five tumors (17.9%) and the expression of ER (100%) and PR (87.5%) were high. These results concur with previous publications and could be considered to support the favorable prognosis of this carcinoma (1,3,31). As mentioned above, imaging findings of ICC are nonspecific. A histopathologic analysis through core needle biopsy or surgical resection is needed for a correct diagnosis. This study has several limitations. First, this was a retrospective study, so not all patients underwent all four imaging studies (mammography, sonography, MRI, and 18 F-FDG PET-CT). Second, the number of study patients was small because of the rarity of this tumor. Third, the study lacks a control group composed of patients who were diagnosed with IDC. A comparison of ICC with IDC should precede an analysis of the character of ICC. In conclusion, the imaging features of invasive cribriform carcinoma are highly suggestive of malignancy, usually presenting as an irregular and spiculated mass on mammography and sonography, an irregular enhancing mass on MRI and with a relatively higher SUVmax value on 18 F-FDG PET-CT. Conflict of interest None declared.
Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Acta Radiologica 56(6) References 1. Page DL, Dixon JM, Anderson TJ, et al. Invasive cribriform carcinoma of the breast. Histopathology 1983;7: 525–536. 2. Cribriform carcinoma. In: Rosen PP, ed. Rosen’s breast pathology, 2nd ed. Philadelphia: Lippincott Williams & Wilkins, 2001:551–553. 3. Venable JG, Schwartz AM, Silverberg SG. Infiltrating cribriform carcinoma of the breast: a distinctive clinicopathologic entity. Hum Pathol 1990;21:333–338. 4. Marzullo F, Zito F, Marzullo A, et al. Infiltrating cribriform carcinoma of the breast. A clinicopathologic and immunohistochemical study of 5 cases. Eur J Gynaecol Oncol 1996;17:228–231. 5. Stutz J, Evans A, Pinder S, et al. The radiological appearances of invasive cribriform carcinoma of the breast. Clin Radiol 1994;49:693–695. 6. Nishimura R, Ohsumi S, Teramoto N, et al. Invasive cribriform carcinoma with extensive microcalcifications in the male breast. Breast Cancer 2005;12:145–148. 7. Lim HS, Jeong SJ, Lee JS, et al. Sonographic findings of invasive cribriform carcinoma of the breast. J Ultrasound Med 2011;30:701–705. 8. Heo TW, Lim HS, Lee JS, et al. Invasive Cribriform Carcinoma of the Breast: A Case Report. J Korean Soc Radiol 2011;64:83–86. 9. Yang WT, Chang J, Metreweli C. Patients with breast cancer: differences in color Doppler flow and gray-scale US features of benign and malignant axillary lymph nodes. Radiology 2000;215:568–573. 10. Elston C, Ellis I. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991;19:403–410. 11. Cole-Beuglet C, Soriano R, Kurtz A, et al. Ultrasound analysis of 104 primary breast carcinomas classified according to histopathologic type. Radiology 1983;147: 191–196. 12. Thomas A, Thickman D, Rapp CL, et al. Solid breast nodules: use of sonography to distinguish between benign and malignant lesions. Radiology 1995;196:123–134. 13. Blaichman J, Marcus JC, Alsaadi T, et al. Sonographic appearance of invasive ductal carcinoma of the breast according to histologic grade. Am J Roentgenol 2012; 199:W402–W408. 14. Lamb PM, Perry NM, Vinnicombe SJ, et al. Correlation between ultrasound characteristics, mammographic findings and histological grade in patients with invasive ductal carcinoma of the breast. Clin Radiol 2000;55: 40–44. 15. Rotstein A, Neerhut P. Ultrasound characteristics of histologically proven grade 3 invasive ductal breast carcinoma. Australas Radiol 2005;49:476–479. 16. Schrading S, Kuhl CK. Mammographic, US, and MR imaging phenotypes of familial breast cancer. Radiology 2008;246:58–70. 17. Liberman L, Morris EA, Lee MJ, et al. Breast lesions detected on MR imaging: features and positive predictive value. Am J Roentgenol 2002;179:171–178.
Lee et al. 18. Tozaki M, Fukuda K. High-spatial-resolution MRI of non-masslike breast lesions: interpretation model based on BI-RADS MRI descriptors. Am J Roentgenol 2006; 18:330–337. 19. Orel S, Mendonca MH, Reynolds C, et al. MR imaging of ductal carcinoma in situ. Radiology 1997; 202:413–420. 20. Ueda S, Tsuda H, Asakawa H, et al. Clinicopathological and prognostic relevance of uptake level using 18F-fluorodeoxyglucose positron emission tomography/computed tomography fusion imaging (18F-FDG PET/CT) in primary breast cancer. Jpn J Clin Oncol 2008;38:250–258. 21. Kim BS, Sung SH. Usefulness of 18F-FDG uptake with clinicopathologic and immunohistochemical prognostic factors in breast cancer. Ann Nucl Med 2012;26:175–183. 22. Buck A, Schirrmeister H, Ku¨hn T, et al. FDG uptake in breast cancer: correlation with biological and clinical prognostic parameters. Eur J Nucl Med Mol Imaging 2002;29:1317–1323. 23. Song BI, Hong CM, Lee HJ, et al. Prognostic value of primary tumor uptake on F-18 FDG PET/CT in patients with invasive ductal breast cancer. Nucl Med Mol Imaging 2011;45:117–124. 24. Inoue T, Yutani K, Taguchi T, et al. Preoperative evaluation of prognosis in breast cancer patients by [(18)F]2-Deoxy-2-fluoro-D-glucose-positron emission tomography. J Cancer Res Clin Oncol 2004;130:273–278.
651 25. Seo HI, Bae YT, Han KT, et al. Clinicopathological characteristics in invasive ductal breast cancer with low FDG uptake in 18F-FDG PET/CT. J Breast Cancer 2010;13: 83–89. 26. Avril N, Menzel M, Dose J, et al. Glucose metabolism of breast cancer assessed by 18F-FDG PET; histologic and immunohistochemical tissue analysis. J Nucl Med 2001; 42:9–16. 27. Gil-Rendo A, Martinez-Regueria F, Zornoza G, et al. Association between [18F] fluorodeoxyglucose uptake and prognostic parameters in breast cancer. Br J Surg 2009;96:166–170. 28. Cermik TF, Mavi A, Basu S, et al. Impact of FDG PET on the preoperative staging of newly diagnosed breast cancer. Eur J Nucl Med Mol Imaging 2008;35:475–483. 29. Avril N, Rose C, Schelling M, et al. Breast imaging with positron emission tomography and fluorine-18 fluorodeoxyglucose: use and limitations. J Clin Oncol 2000;18: 3495–3502. 30. Kumar R, Chauhan A, Zhuang H, et al. Clinicopathologic factors associated with false negative FDG-PET in primary breast cancer. Breast Cancer Res Treat 2006;98:267–274. 31. Zhang W, Zhang T, Lin Z, et al. Invasive cribriform carcinoma in a Chinese population: comparison with lowgrade invasive ductal carcinoma-not otherwise specified. Int J Clin Exp Pathol 2013;6:445–457.
Copyright of Acta Radiologica is the property of Sage Publications, Ltd. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
Invasive cribriform carcinoma of the breast: mammographic, sonographic, MRI, and 18 F-FDG PET-CT features
Acta Radiologica 2015, Vol. 56(6) 644–651 ! The Foundation Acta Radiologica 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0284185114538425 acr.sagepub.com
Young Ju Lee1, Bo Bae Choi1 and Kwang Sun Suh2
Abstract Background: Invasive cribriform carcinoma (ICC) of the breast is a rare type of invasive carcinoma which shows a favorable prognosis and a lower frequency of axillary nodal metastases. Few imaging findings related to ICC have been reported. Purpose: To evaluate imaging findings with multiple imaging techniques in ICC of the breast. Material and Methods: Twenty-eight cases of histopathologically proven ICC of the breast were gathered for this study. We retrospectively reviewed the mammographic, sonographic, and magnetic resonance imaging (MRI) findings of ICC according to the American College of Radiology (ACR) breast imaging reporting and data system (BI-RADS) lexicon. 18 F-fluorodeoxyglucose positron emission tomography-computed tomography (18 F-FDG PET-CT) findings were also evaluated. Microscopic slides of surgical specimens were reviewed by a breast pathologist. Results: The mean age of the patients was 51 years. The most common mammographic findings were irregular shape (72.8%), spiculated margin (63.7%), and a high density (81.8%) mass. Microcalcifications were noted in 9/28 cases. The most common shape was pleomorphic (66.7%). The most common sonographic findings were irregular shape (77.8%), spiculated margin (29.6%), hypoechogenicity (81.5%), and no posterior acoustic features (85.2%). On MRI, most ICCs presented as irregular shaped mass (62.0%) and irregular (42.9%) margin. All four patients (16.0%) who presented with non-mass-like enhancement pattern showed a segmental distribution. The 18 F-FDG PET-CT showed a mean maximum standardized uptake value (SUVmax) of 5.90. Axillary nodal metastases were found in 17.9% (5/28) of the surgical specimens. Immunohistochemical studies showed a high positivity for estrogen and progesterone receptor (100% and 87.5%, respectively). Conclusion: The imaging features of invasive cribriform carcinoma are highly suggestive of malignancy and are not distinguishable from those of other breast cancers like infiltrating ductal carcinoma.
Keywords Breast, neoplasms – primary, mammography, ultrasound, magnetic resonance imaging (MRI), positron emission tomography (PET) Date received: 28 November 2013; accepted: 4 May 2014
Introduction Invasive cribriform carcinoma (ICC) is an unusual type of primary breast carcinoma that is composed of predominantly cribriform invasive components (1,2). In 1983, Page et al. initially described a separate histological type of breast carcinoma upon reviewing the histology and clinical data of 1003 invasive breast carcinomas (1). It was characterized as having a more favorable prognosis than ordinary breast carcinoma, and axillary node metastasis were uncommon (1,3,4).
1 Department of Radiology, Chungnam National University Hospital, Daejeon, Republic of Korea 2 Department of Pathology, Chungnam National University Hospital, Daejeon, Republic of Korea
Corresponding author: Bo Bae Choi, Department of Radiology, Chungnam National University Hospital, 282 Munhwa-ro, Jung-gu, Daejeon 301-721, Korea. Email: [email protected]
Lee et al. To the best of our knowledge, radiological reports on their imaging characteristics are limited because ICCs occur infrequently only. Previous studies consist of two case reports and two retrospective studies (5–8). The number of previously reported cases was low and the studies reported various findings on mammography, sonography, and magnetic resonance imaging (MRI). The purpose of this study was to investigate whole-breast imaging findings of ICC, including mammography, sonography, MRI, and 18 F-fluorodeoxyglucose positron emission tomography-computed tomography (18 F-FDG PET-CT).
Material and Methods Thirty-six patients with invasive cribriform carcinoma were identified in our computerized pathology database between July 2006 and February 2013. Five patients were excluded because the final pathologic diagnosis of the specimen was infiltrating ductal carcinoma (IDC), despite being confirmed as ICC on core-needle biopsy. Three more patients were excluded because radiologic images were not available. In total, 28 patients were included in this study. By mammography, craniocaudal and mediolateral oblique views were obtained using a Mammomat 3000 (Siemens Medical Solutions, Solna, Sweden) and Lorad M3 (Hologic Inc., Boston, MA, USA) mammography unit. Parenchymal patterns on mammograms were categorized as one of the following: almost entirely fatty; scattered fibroglandular tissue; heterogeneously dense; extremely dense. Each mammographic lesion was analyzed for mass characteristics (i.e. shape, margin, density), presence of architectural distortion, and the type of microcalcification according to the American College of Radiology (ACR) breast imaging reporting and data system (BI-RADS) lexicon. Ultrasound (US) was performed using a HDI 5000 (Advanced Technology Laboratories, Bothell, WA, USA) or IU22 (Philips Ultrasound, Bothell, WA, USA) US systems with a 5–12 MHz linear probe. We examined both breasts and the axillary lymph nodes. US imaging findings were reviewed for shape, orientation, margin, boundary, echogenicity, posterior acoustic features, and associated calcifications, and categorized according to the ACR BI-RADS final assessment. The largest diameter obtained from either the sagittal or transverse views was recorded as the maximum tumor diameter. On the basis of previous studies, we defined the presence of axillary lymph node metastasis on US when the lymph node had at least one of these findings: a mean longitudinal-transverse axis ratio of less than 1.5, presence of eccentric cortical thickening, or loss of a central fatty hilum (9).
645 MRI was performed using a 1.5-T scanner (Signa Excite, GE Healthcare, Milwaukee, WI, USA) equipped with a breast coil. Images were acquired in axial plane with the following sequences: axial, T2weighted, fat-suppressed, fast spin-echo imaging (TR/ TE, 5000/86; flip angle, 90 ; field of view [FOV], 300 mm; acquisition matrix, 256 256; number of excitations (NEX), 3; slice thickness, 4.5 mm); pre- and postcontrast, axial, T1-weighted (T1W) three-dimensional (3D) fast spoiled gradient-recalled echo sequence with parallel volume imaging (VIBRANT, GE Healthcare) (TR/TE, 6.5/3.1; flip angle, 10 ; FOV, 300 mm; acquisition matrix, 350 350; NEX, 1; slice thickness, 1.1 mm). Gadodiamide (Omniscan, GE Healthcare, Oslo, Norway) was administered as contrast agent with an intravenous bolus injection (0.2 mmol per kg of body weight) at 3 mL/s. Imaging was performed before the intravenous contrast agent bolus injection and four times after this injection for a period of 7.3 min. The image postprocessing, included the subtraction of unenhanced images from enhanced images, sagittal reformations, and 3D maximum-intensity projections by using the first contrast-enhanced series. The interpretation of the degree and patterns of enhancement was performed by visual assessment. Associated findings were recorded, such as nipple retraction, skin thickening, lymphadenopathy, hematoma, and invasion of the pectoralis muscle or chest wall. All mammograms, sonograms, and MR images were retrospectively reviewed in consensus by one radiologist with 6 years of experience in breast imaging and by one resident. 18 F-FDG PET-CT imaging was performed using a Discovery ST-16 system (GE Healthcare, Milwaukee, WI, USA). Normal fasting blood glucose levels (after fasting for at least 6 h) were determined to be 0.05). Accordingly, we found that the microcalcification in ICC should not to be related to DCIS components. An irregular shaped and irregular marginated mass was the most common MRI appearance in our study. So far, the MRI features of ICC have been described in one case only (7). Lim et al. reported that ICC displayed an oval shaped mass with homogenous early enhancement and delayed washout pattern based on the kinetic curve analysis (7). In the present study, the four remaining patients presented with a non-mass-like enhancement with segmental distribution (16.0%). Of those four patients, only three patients underwent surgery. In those patients, the mean extent of the primary lesion was 5.0 cm (range, 4.7–5.3 cm) at MRI. The histopathology report revealed that approximately 43.3% of the DCIS was associated with invasive cancer. The mean histologic size of the invasive carcinoma was 1.1 cm (range, 0.9–1.3 cm), which was smaller than the extent of the primary lesion at MRI. Previous studies explained that DCIS have a high relationship with non-mass-like enhancement (17–19). We postulate the different MRI presentation such as the non-masslike enhancement may be primarily due to DCIS components. We also investigated the 18 F-FDG PET-CT images of ICCs, which has not been reported yet. In our study, 87.0% (20/23) of lesions showed FDG uptake. Many published studies with preoperative 18 F-FDG PET-CT in patients with primary breast carcinoma have suggested that higher levels of FDG uptake are significantly correlated with a poor prognosis, similar tumor invasiveness (>2 cm), higher histological grade, negative hormonal receptor status, axillary lymph node metastasis, and histological type of primary breast carcinoma (IDC in comparison with invasive lobular carcinoma [ILC]) (20–26). Primary breast cancers with FDG high uptake (range, 4.1–7.4) are considered to have poor prognosis compared to those with low FDG uptake (range, 2.8–5.2) (27–30). The mean SUVmax value of the primary tumor was 5.90 (range, 1.2–14.3) in the present study. Compared with the aforementioned reports, our result of ICC showed relatively higher values, even though ICC has a favorable prognosis and a well-differentiated tumor. False negative results were found in 13% (3 of 23) of the patients. The false negative rate by PET-CT has been reported to be 23.7–46.5% in IDC and
650 60–65.2% in ILC (29,30). Low sensitivity was described for the detection of small lesions (10 mm) and lower histological grades on FDG PET in patients with primary breast carcinoma (30). The authors explained that a high rate of false negative result in ILC was affected by different microscopic growth pattern, such as lower tumor cell density and diffuse infiltration of the surrounding tissue (26,27,29). In our study, the tumor size was smaller than 1 cm and the histological grade was also well-differentiated in three patients with false negative findings. We postulate these factors could be a cause of false negative findings in the present study. The false negative rate of ICC in our study was relatively lower than that of IDC and ILC in previous reports (29,30). Because of the relatively small number of subjects, further research is necessary to evaluate the PET-CT findings of ICC and to compare them with IDC and ILC. Pure ICC is characterized by lower rates of axillary lymph node involvement, higher positive rates of ER and/or PR expression than in mixed ICC and IDC (1,3,4,31). Those characteristics are one of the important prognostic factors for breast cancer. In our cases, axillary nodal metastases were identified in only five tumors (17.9%) and the expression of ER (100%) and PR (87.5%) were high. These results concur with previous publications and could be considered to support the favorable prognosis of this carcinoma (1,3,31). As mentioned above, imaging findings of ICC are nonspecific. A histopathologic analysis through core needle biopsy or surgical resection is needed for a correct diagnosis. This study has several limitations. First, this was a retrospective study, so not all patients underwent all four imaging studies (mammography, sonography, MRI, and 18 F-FDG PET-CT). Second, the number of study patients was small because of the rarity of this tumor. Third, the study lacks a control group composed of patients who were diagnosed with IDC. A comparison of ICC with IDC should precede an analysis of the character of ICC. In conclusion, the imaging features of invasive cribriform carcinoma are highly suggestive of malignancy, usually presenting as an irregular and spiculated mass on mammography and sonography, an irregular enhancing mass on MRI and with a relatively higher SUVmax value on 18 F-FDG PET-CT. Conflict of interest None declared.
Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Acta Radiologica 56(6) References 1. Page DL, Dixon JM, Anderson TJ, et al. Invasive cribriform carcinoma of the breast. Histopathology 1983;7: 525–536. 2. Cribriform carcinoma. In: Rosen PP, ed. Rosen’s breast pathology, 2nd ed. Philadelphia: Lippincott Williams & Wilkins, 2001:551–553. 3. Venable JG, Schwartz AM, Silverberg SG. Infiltrating cribriform carcinoma of the breast: a distinctive clinicopathologic entity. Hum Pathol 1990;21:333–338. 4. Marzullo F, Zito F, Marzullo A, et al. Infiltrating cribriform carcinoma of the breast. A clinicopathologic and immunohistochemical study of 5 cases. Eur J Gynaecol Oncol 1996;17:228–231. 5. Stutz J, Evans A, Pinder S, et al. The radiological appearances of invasive cribriform carcinoma of the breast. Clin Radiol 1994;49:693–695. 6. Nishimura R, Ohsumi S, Teramoto N, et al. Invasive cribriform carcinoma with extensive microcalcifications in the male breast. Breast Cancer 2005;12:145–148. 7. Lim HS, Jeong SJ, Lee JS, et al. Sonographic findings of invasive cribriform carcinoma of the breast. J Ultrasound Med 2011;30:701–705. 8. Heo TW, Lim HS, Lee JS, et al. Invasive Cribriform Carcinoma of the Breast: A Case Report. J Korean Soc Radiol 2011;64:83–86. 9. Yang WT, Chang J, Metreweli C. Patients with breast cancer: differences in color Doppler flow and gray-scale US features of benign and malignant axillary lymph nodes. Radiology 2000;215:568–573. 10. Elston C, Ellis I. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991;19:403–410. 11. Cole-Beuglet C, Soriano R, Kurtz A, et al. Ultrasound analysis of 104 primary breast carcinomas classified according to histopathologic type. Radiology 1983;147: 191–196. 12. Thomas A, Thickman D, Rapp CL, et al. Solid breast nodules: use of sonography to distinguish between benign and malignant lesions. Radiology 1995;196:123–134. 13. Blaichman J, Marcus JC, Alsaadi T, et al. Sonographic appearance of invasive ductal carcinoma of the breast according to histologic grade. Am J Roentgenol 2012; 199:W402–W408. 14. Lamb PM, Perry NM, Vinnicombe SJ, et al. Correlation between ultrasound characteristics, mammographic findings and histological grade in patients with invasive ductal carcinoma of the breast. Clin Radiol 2000;55: 40–44. 15. Rotstein A, Neerhut P. Ultrasound characteristics of histologically proven grade 3 invasive ductal breast carcinoma. Australas Radiol 2005;49:476–479. 16. Schrading S, Kuhl CK. Mammographic, US, and MR imaging phenotypes of familial breast cancer. Radiology 2008;246:58–70. 17. Liberman L, Morris EA, Lee MJ, et al. Breast lesions detected on MR imaging: features and positive predictive value. Am J Roentgenol 2002;179:171–178.
Lee et al. 18. Tozaki M, Fukuda K. High-spatial-resolution MRI of non-masslike breast lesions: interpretation model based on BI-RADS MRI descriptors. Am J Roentgenol 2006; 18:330–337. 19. Orel S, Mendonca MH, Reynolds C, et al. MR imaging of ductal carcinoma in situ. Radiology 1997; 202:413–420. 20. Ueda S, Tsuda H, Asakawa H, et al. Clinicopathological and prognostic relevance of uptake level using 18F-fluorodeoxyglucose positron emission tomography/computed tomography fusion imaging (18F-FDG PET/CT) in primary breast cancer. Jpn J Clin Oncol 2008;38:250–258. 21. Kim BS, Sung SH. Usefulness of 18F-FDG uptake with clinicopathologic and immunohistochemical prognostic factors in breast cancer. Ann Nucl Med 2012;26:175–183. 22. Buck A, Schirrmeister H, Ku¨hn T, et al. FDG uptake in breast cancer: correlation with biological and clinical prognostic parameters. Eur J Nucl Med Mol Imaging 2002;29:1317–1323. 23. Song BI, Hong CM, Lee HJ, et al. Prognostic value of primary tumor uptake on F-18 FDG PET/CT in patients with invasive ductal breast cancer. Nucl Med Mol Imaging 2011;45:117–124. 24. Inoue T, Yutani K, Taguchi T, et al. Preoperative evaluation of prognosis in breast cancer patients by [(18)F]2-Deoxy-2-fluoro-D-glucose-positron emission tomography. J Cancer Res Clin Oncol 2004;130:273–278.
651 25. Seo HI, Bae YT, Han KT, et al. Clinicopathological characteristics in invasive ductal breast cancer with low FDG uptake in 18F-FDG PET/CT. J Breast Cancer 2010;13: 83–89. 26. Avril N, Menzel M, Dose J, et al. Glucose metabolism of breast cancer assessed by 18F-FDG PET; histologic and immunohistochemical tissue analysis. J Nucl Med 2001; 42:9–16. 27. Gil-Rendo A, Martinez-Regueria F, Zornoza G, et al. Association between [18F] fluorodeoxyglucose uptake and prognostic parameters in breast cancer. Br J Surg 2009;96:166–170. 28. Cermik TF, Mavi A, Basu S, et al. Impact of FDG PET on the preoperative staging of newly diagnosed breast cancer. Eur J Nucl Med Mol Imaging 2008;35:475–483. 29. Avril N, Rose C, Schelling M, et al. Breast imaging with positron emission tomography and fluorine-18 fluorodeoxyglucose: use and limitations. J Clin Oncol 2000;18: 3495–3502. 30. Kumar R, Chauhan A, Zhuang H, et al. Clinicopathologic factors associated with false negative FDG-PET in primary breast cancer. Breast Cancer Res Treat 2006;98:267–274. 31. Zhang W, Zhang T, Lin Z, et al. Invasive cribriform carcinoma in a Chinese population: comparison with lowgrade invasive ductal carcinoma-not otherwise specified. Int J Clin Exp Pathol 2013;6:445–457.
Copyright of Acta Radiologica is the property of Sage Publications, Ltd. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
