原发性乳腺淋巴瘤

Mammographic and sonographic findings of primary breast lymphomaChae Yeon Lyou,Sang Kyu Yang 4,Du Hwan Choe,Byung Hee Lee,Kie Hwan KimDepartment of Radiology,Korea Cancer Center Hospital,Seoul,KoreaReceived 5December 2006;accepted 15February 2007AbstractThe objective of this study was to describe the mammographic and sonographic appearances of primary lymphoma of the breast.We retrospectively reviewed the mammographic and ultrasonographic images of 12patients with primary lymphoma of the breast.Descriptions of imaging findings were made according to the Breast Imaging Reporting and Data System lexicon by two radiologists.Mammography was performed on 11patients.Most of the lesions were shown to be oval-shaped (72.7%)and high-density (90.9%)masses on mammography.Ultrasound examination was performed on 8patients.The lymphomas were commonly single (75%),circumscribed (50%)or microlobulated (37.5%),and oval (50%)masses on sonography.The echo pattern of the mass was hypoechoic in 7patients (87.5%)but hyperechoic in 1patient (12.5%).No mass had spiculated margins or calcifications.Ipsilateral axillary lymph node involvement was noted in 1patient.In conclusion,most primary lymphomas of the breast present as oval-shaped and high-density masses on mammography and as single and hypoechoic masses with circumscribed or microlobulated margins on sonography.D 2007Elsevier Inc.All rights reserved.Keywords:Breast;Lymphoma;Ultrasound;Mammography1.IntroductionThe breast is an uncommon site of development for malignant lymphomas despite the relative frequency of primary extranodal non-Hodgkin lymphomas.Breast lym-phomas can be either primary or secondary.Secondary breast lymphomas more commonly occur in association with extramammary non-Hodgkin lymphomas.Primary breast lymphomas are less common,accounting for only 0.05%–0.53%of all breast malignancies [1].There are few articles about the imaging findings of primary breast lymphoma in the radiology literature [2–7].Data on the sonographic appearance of primary breast lymphomas are even more limited than those on its mammographic appearance.We reviewed 12cases of primary lymphoma of the breast to determine the mammo-graphic and sonographic characteristics of this rare diseasewith the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS)lexicon [8].2.Materials and methodsA retrospective review of medical records at our institution that date between January 1993and October 2006revealed 12patients with primary breast lymphoma.All cases were diagnosed based on pathological demonstration after surgical biopsy or ultrasound (US)-guided core needle biopsy and satisfied the specific diagnostic criteria described by Wise-man and Liao [9]for primary lymphoma of the breast,including histological evidence of a close association between the mammary tissue and the lymphomatous infiltrate as well as absence of disseminated lymphoma or preceding extramammary lymphoma at the time of diagnosis.Presence of homolateral axillary node involvement is acceptable provided that both lesions developed simultaneously.The patients’ages at the time of the diagnosis as well as their physical findings and clinical status were abstracted from the medical records.We reviewed the pathological0899-7071/07/$–see front matter D 2007Elsevier Inc.All rights reserved.doi:10.1016/j.clinimag.2007.02.0284Corresponding author.Department of Radiology,Korea Cancer Center Hospital,215-4Gongneung-Dong,Nowon-Gu,Seoul 139-706,Korea.Tel.:+8229701576;fax:+8229702433.E-mail address:twoscan@ (S.K.Yang).Clinical Imaging 31(2007)234–238reports of all lesions and then determined the histological subtypes of lymphoma according to the classification by the World Health Organization.Mammograms were available for11patients.Mammog-raphy was performed using dedicated film-screen equipment (Senographe600T,GE Health Care)and single-emulsion film.Images were obtained in two standard planes(medio-lateral oblique and craniocaudal).US of the breast was also performed before biopsy in eight images were obtained using HDI5000 (Advanced Technology Laboratories,Bothell,WA,USA) and SSD-5500(Aloka,Tokyo,Japan)with a5-to12-MHz linear array.Mammograms and US images were reviewed by two radiologists,and the imaging appearances were determined by consensus.Descriptions of imaging findings were made according to the BI-RADS lexicon.Mammograms were reviewed to determine the presence of focal masses,the shape,margin,and density of the masses,calcifications,and axillary images were assessed for the presence of masses,the number and size of the masses,shape,margins,echo pattern,orientation,posterior acoustic features,and presence of calcifications.3.ResultsAll12patients were women;at the time of their diagnosis,their ages ranged from23to62years(mean age=46years).Breast symptoms in all patients were present as palpable lumps.Pain was present in only1patient. Clinical evidence of skin retraction and nipple discharge were absent in all patients.The right breast was involved in 5patients(41.7%),whereas the left was involved in 7(58.3%).All patients were diagnosed as having non-Hodgkin lymphoma,with the most common subtype being diffuse large B-cell lymphoma(83.4%,n=10/12)(Fig.1C and1D). One patient had a small lymphocytic B-cell lymphoma (8.3%,n=1/12),and another had a Burkitt-like high-grade B-cell lymphoma(8.3%,n=1/12).On mammography,all breast lesions presented as masses (100%,n=11/11).Eight of the masses were oval(72.7%, n=8/11),two were round(18.2%,n=2/11),and one was irregular(9.1%,n=1/11)(Table1).All except one were high-density masses(90.9%,n=10/11),and one was isodense to the adjacent glandular tissue(9.1%,n=1/11). Four masses had indistinct margins(36.3%,n=4/11),three had circumscribed margins(27.3%,n=3/11),and another three had obscured margins(27.3%,n=3/11).No mass had calcifications(Figs.1A,2A,and3A).Ipsilateral axillary lymphadenopathy was noted in one patient.On US,most patients presented with a single mass(75%, n=6/8),but two patients had multiple masses.The diameter of masses ranged from0.7to 5.9cm(mean diame-ter=2.3F1.7cm).The long axis of all masses paralleled the skin line(wider-than-tall or horizontal orientation).The shape of masses appeared as oval(50%,n=4/8),irregular (37.5%,n=3/8),or round(12.5%,n=1/8).Circumscribed and microlobulated margins were common—in50%(n=4/ 8)and37.5%(n=3/8)of the masses,respectively(Table2). The echo pattern of the mass was hypoechoic in seven patients(87.5%)(Fig.1B and Fig.2B)but hyperechoic in one patient(12.5%)(Fig.3B).Posterior enhancement was observed in six patients(75%),no posterior acoustic feature was observed in two(25%),and posterior acoustic shadowing was not observed in any patient.No mass had spiculated margins or calcifications.4.DiscussionPrimary lymphomas of the breast are rare,accounting for only1.7%–2.2%of extranodal lymphomas and for only 0.4%–0.7%of all non-Hodgkin lymphomas[10].To our knowledge,there are only few articles about breast lymphomas,except for case reports,in the radiology literature.We tried to describe the characteristics of the mammographic and sonographic features of primary breast lymphomas with the BI-RADS lexicon.A primary breast lymphoma may be very well defined and may be mistaken for a benign process,most notably in patients younger than35years[2],in whom cysts and fibroadenomas are more common.The key in the evaluation of these cases remains to be adequate tissue biopsy for histopathological evaluation and immunophe-notyping[11].The original diagnostic criteria for primary breast lymphoma were suggested by Wiseman and Liao [9]in1972.In our series,diffuse large B-cell lymphoma was the most frequent histological subtype.This result is consistent with the findings of another study[10]. Table1Mamographic findings of primary breast lymphomas(n=11) Mammographic finding Sample distribution[n(%)] ShapeRound2(18.2)Oval8(72.7)Lobular0(0)Irregular1(9.1)MarginCircumscribed3(27.3) Microlobulated1(9.1)Obscured3(27.3)Indistinct4(36.3)Spiculated0(0)DensityHigh10(90.9)Equal1(9.1)Low0(0)Fat containing0(0)CalcificationsPresent0(0)Absent11(100)C.Y.Lyou et al./Clinical Imaging31(2007)234–238235Lieberman et al.[7]reported that the imaging pattern of mammary non-Hodgkin lymphoma was unrelated to its histopathological subtype.Symptoms of mammary lymphomas may mimic those of carcinoma and cause difficulties in differential diagnosis.Breast lymphomas usually present as solitary painless lumps in younger patients as compared with breast carcinomas [12].This most likely reflects the relatively rapid growth of these lesions,as compared with breast carcinomas,especially in younger patients.The literature reveals that breast lymphomas can occasionally present as a diffuse rapid breast enlargement in the younger age group or as breast skin thickening caused by lymphatic blockage by lymphomas,resulting in retrograde edema [3].In our series,the age range of the patients at diagnosis was 23–62years (mean age=46years).All patients had a palpable lump.Pain was present in one patient.The right breast was involved in five patients (41.7%),whereas the left was involved in seven (58.3%).An unexplained right-sided predominance,in contrast to left-sided predominance documented in breast carcinomas,was classically described in primary lymphomas of the breast [1,8,13,14],but this was not noted in our series.Several studies had been performed to confirm the mammographic appearance of breast lymphomas.Lieber-man et al.[7]reviewed among 29women 32cases of non-Hodgkin lymphoma,of which 21(66%)were classified as primary breast non-Hodgkin lymphomas;mammograms revealed solitary and uncalcified masses in 69%of the cases,multiple masses in 9%,and diffuse increased opacity with skin thickening in 9%.Four cases (13%)had normal findings.Paulus [3]presented 31patientswithFig.1.Images for a 47-year-old woman with diffuse large B-cell lymphoma.(A)Craniocaudal mammogram of the right breast showing a high-density and oval mass (white arrows)with partially obscured margins (black arrows).(B)US image showing a 3-cm-diameter,hypoechoic,and oval mass (white arrows)with microlobulated margins (black arrows)and posterior acoustic enhancement.(C)Low-power view of surgical biopsy specimen showing that lymphocytic infiltrates replaced the normal architecture of the underlying breast parenchyma (hematoxylin–eosin,original magnification Â40).(D)High-power view showing that the mass is composed of medium-sized to large lymphoid cells with oval-to-round vesicular nuclei with fine chromatin.The cytoplasm is scanty and amphophilic to basophilic (hematoxylin–eosin,original magnification Â200).C.Y.Lyou et al./Clinical Imaging 31(2007)234–238236mammographic changes of proven reticuloendothelial system disease in which the masses in breast lymphomas were of homogeneous density and did not contain tumor calcifications and noted that there was no stromal distortion of the surrounding breast parenchyma as is recognized and often found in breast carcinomas.A less common mammographic finding of lymphomas is diffuse increased parenchyma density with or that without skin thickening.This pattern of involvement is predominantly observed in patients with a high-grade lymphoma [5].Axillary lymphadenopathy may be associated with primary lymphoma of the breast,but this is not a prominent feature of most reported cases [2,15–18].Mammographically,a solitary mass was the most common radiological pattern in our study.Most masses had an oval shape and were of high density.Margins were variable.Calcifications present in up to half of thecarcinomas were not seen in our series of lymphomas,in agreement with previous series [2,4,5,7].Desmoplastic or fibrotic reaction with architectural distortion often seen surrounding breast carcinomas was not demonstrated in the masses.Diffuse increased parenchymal density was not observed in any patient.Not much has been written about US findings of breast lymphomas [4–7].A hypoechoic,homogeneous,or hetero-geneous well-defined mass is the most common US finding among patients with malignant lymphoma of the breast [6,7].However,a wide spectrum of appearances,ranging from well defined to poorly defined,focal to diffuse [4–7],and hypoechoic to hyperechoic [4],has been described in previously reported series.Primary breast lymphoma can be present as an elongated cystic structure or an ellipsoid,well-defined,and complex lesion on US [11,17].There is one case of primary breast lymphoma that mimicked acute mastitis in a young woman [18].In our study,most masses showed an oval shape with circumscribed or microlobulated margins and a hypoechoic echo pattern,and one case showed a hyperechoic echo pattern on US.All masses had a horizontal orientation to the skin line.Most of themassesFig. 2.Images for a 56-year-old woman with diffuse large B-cell lymphoma.(A)Mediolateral oblique mammogram of the left breast showing a high-density and oval mass (white arrows)with partially indistinct margins (black arrows).(B)US image showing a large and hypoechoic mass (arrows)with irregularmargins.Fig. 3.Images for a 50-year-old woman with diffuse large B-cell lymphoma.(A)Craniocaudal mammogram of the right breast showing a high-density and round mass (arrows)in the outer part of the breast.(B)US image showing a circumscribed hyperechoic mass (arrows).C.Y.Lyou et al./Clinical Imaging 31(2007)234–238237showed posterior acoustic enhancement.No mass had spiculated or angulated margins.The greatest limitations of our study are caused by the small sample size,which is a direct reflection of the rarity of this lesion.Characterization of a larger number of primary breast lymphoma cases would be necessary to draw conclusions of any meaningful significance.Although the small study population with this rare disease clearly limits the value of the data obtained,certain tendencies were observed.In conclusion,most primary breast lymphomas present as oval-shaped and high-density masses on mammography and as single and hypoechoic masses with circumscribed or microlobulated margins on US.References[1]Brustein S,Filippa DA,Kimmel M,Lieberman PH,Rosen PP.Malignant lymphoma of the breast:a study of 53patients.Ann Surg 1987;205:144–50.[2]Meyer JE,Kopans DB,Long JC.Mammographic appearance ofmalignant lymphoma of the breast.Radiology 1980;135:623–6.[3]Paulus DD.Lymphoma of the breast.Radiol Clin North Am1982;20:561–8.[4]Jackson FI,Lalani ZH.Breast lymphoma:radiologic imaging andclinical appearance.Can Assoc Radiol J 1991;42:48–54.[5]Sabate JM,Gomez A,Torrubia S,Camins A,Rosen N,De Las HerasV ,Villalba-Nuno V .Lymphoma of the breast:clinical and radiologic features with pathologic correlation in 28patients.Breast J 2002;8:294–304.[6]Pope TL,Brenbridge AN,Sloop FB,Morris JR,Carpenter J.Primaryhistiocytic lymphoma of the breast:mammographic,sonographic and pathologic correlation.J Clin Ultrasound 1985;13:667–70.[7]Lieberman L,Giess CS,Dershaw DD,Louie DC,Deutch BM.Non-Hodgkin lymphoma of the breast:imaging characteristics and cor-relation with histopathologic findings.Radiology 1994;192:157–60.[8]American College of Radiology.Breast Imaging Reporting and DataSystem:BI-RADS atlas.4th ed.Reston (Va)7American College of Radiology;2003.[9]Wiseman C,Liao KT.Primary lymphoma of the breast.Cancer1972;29:1705–12.[10]Topalovski M,Crisan D,Mattson JC.Lymphoma of the breast Aclinicopathological study of primary and secondary cases.Arch Pathol Lab Med 1999;123:1208–18.[11]Mason HS,Johari V ,March DE,Crisi GM.Primary breast lymphoma:radiologic and pathologic findings.Breast J 2005;11:495–6.[12]Giardini R,Piccolo C,Rilke F.Primary non-Hodgkin’s lymphomas ofthe female breast.Cancer 1992;69:725–35.[13]Mambo NC,Burke JS,Butler JJ.Primary malignant lymphomas ofthe breast.Cancer 1977;39:2033–40.[14]Schouten JT,Weese JL,Carbone PP.Lymphoma of the breast.AnnSurg 1981;194:749–53.[15]Assaly T,Palayew MJ,Lisbona A,Alpert L.General case of the day.Radiographics 1992;12:602–5.[16]Watson AP,Fraser SE.Primary lymphoma of the breast.AustralasRadiol 2000;44:234–6.[17]Gal-Gombos EC,Esserman LE,Poniecka AW,Poppiti RJ.Is apseudocystic serpentine mass a sonographic indicator of breast lymphoma?Radiologic–histologic correlation of an unusual finding.AJR Am J Roentgenol 2001;176:734–6.[18]Grubstein A,Givon-Madhala O,Morgenstern S,Cohen M.Extranodalprimary B-cell non-Hodgkin lymphoma of the breast mimicking acute mastitis.J Clin Ultrasound 2005;33:140–2.Table 2Ultrasonographic findings of primary breast lymphomas (n =8)Ultrasonographic finding Sample distribution [n (%)]Shape Oval 4(50)Round 1(12.5)Irregular 3(37.5)Orientation Parallel 8(100)Not parallel 0(0)MarginCircumscribed 4(50)Indistinct 1(12.5)Angular0(0)Microlobulated 3(37.5)Spiculated 0(0)Echo pattern Anechoic 0(0)Hyperechoic 1(12.5)Complex 0(0)Hypoechoic 7(87.5)Isoechoic0(0)Posterior acoustic feature No posterior acoustic feature 2(25)Enhancement 6(75)Shadowing 0(0)Combined 0(0)Calcifications Present 0(0)Absent8(100)C.Y.Lyou et al./Clinical Imaging 31(2007)234–238238。