ONCOLOGY LETTERS Dignostic vlue of ultrsound combined with mgnetic resonnce imging in different stges of brest cncer QIAOHONG PAN 1* nd JIANWU JI 2* Deprtments of 1 Ultrsound nd 2 MRI, Heping Hospitl Affilited to Chngzhi Medicl College, Chngzhi, Shnxi 046000, P.R. Chin Received August 2, 2018; Accepted September 28, 2018 DOI: 10.3892/ol.2018.9589 Abstrct. Dignostic vlue of ultrsound (US) nd mgnetic resonnce imging (MRI) in brest cncer were investigted. One hundred nd forty brest cncer ptients dignosed in Heping Hospitl Affilited to Chngzhi Medicl College from June 2016 to June 2018 were collected, used s brest cncer group, 80 ptients with benign brest tumor in the sme period were the benign group. Pthologicl results were used to compre the dignostic coincidence of US nd MRI in brest cncer ptients. The positive expression cse rtes of estrogen receptor nd progesterone receptor were significntly higher in brest cncer group thn those in benign group, but tht of humn epiderml growth fctor receptor 2 (Her-2) ws significntly lower in brest cncer group thn tht in benign group (ll P<0.05). The sensitivity (SEN) of MRI lone nd tht of US combined with MRI were higher thn tht of US lone (P<0.05). The specificity (SPE) of MRI lone ws lower thn tht of US lone nd US combined with MRI (P<0.05). The NPV of US combined with MRI ws significntly higher thn tht of US lone (P<0.05). The Youden index (YI) of US combined with MRI ws significntly higher thn tht of US lone nd MRI lone. In the dignosis of N2, tht of US combined with MRI ws significntly higher thn those of US lone nd MRI lone (P<0.05). In stges of M0 nd M1 mong three methods, those of MRI lone nd US combined with MRI were higher thn tht of US lone (P<0.05). US combined with MRI for the dignosis of brest cncer hs higher SEN nd SPE, with better ccurcy rte for the identifiction of ech stge. Reducing the incidence of missed dignosis nd misdignosis tht my be cused by single dignosis nd Correspondence to: Dr Jinwu Ji, Deprtment of MRI, Heping Hospitl Affilited to Chngzhi Medicl College, 110 Yn'n South Rod, Chngzhi, Shnxi 046000, P.R. Chin E-mil: w3r27f@163.com * Contributed eqully Key words: ultrsound, mgnetic resonnce imging, brest cncer, dignosis, TNM stging tretment, it is conducive to clinicl screening nd guiding clinicl symptomtic tretment. Introduction Brest cncer is gynecologicl mlignnt tumor cused by hormone secretion imblnce, nutritionl imblnce, virl stimultion, rdition fctors nd genetic bckground (1). As socil life rhythm ccelertes nd working methods chnge, the incidence of brest cncer hs incresed yer by yer, which hs lredy rnked first in the incidence of femle mlignnt tumors, seriously thretening women's physicl nd mentl helth. The clinicl mnifesttions of brest cncer re minly ornge-like chnges in the skin nd contour of the brest, with lumps in the brest, nipple dischrge nd swollen lymph nodes (2). Its erly cure rte is extremely high, so erly detection nd erly dignosis re very importnt for its prognosis. Moreover, different stges of brest cncer re treted differently. Therefore, the ccurte dignosis of different stges is lso very importnt for brest cncer tretment. With the development nd improvement of imging technologies such s ultrsound (US) nd mgnetic resonnce imging (MRI), imging methods hve plyed n incresingly importnt role in the dignosis of brest cncer (1,3). At present, TNM stging is the min stging method of brest cncer (4). Currently, physicl mens, physicl exmintion nd molybdenum plldium re minly used for stging cliniclly, with not enough sensitivity (5). Both US nd MRI re commonly used imging methods for the erly dignosis nd stging of brest cncer. There re studies on the clinicl vlue of MRI combined with US in the dignosis of brest cncer stging, but most studies re on T stging, with few studies on N nd M stging (6,7). Therefore, in this study, the dignostic vlue of US combined with MRI in the T, N nd M stging of brest cncer ws nlyzed, in order to provide more effective, sensitive nd ccurte detection progrm for the erly dignosis nd ccurte stging, improving the efficcy of ptients' subsequent tretment nd the prognoses. Ptients nd methods Reserch subjects. A totl of 140 brest cncer ptients dignosed in Heping Hospitl Affilited to Chngzhi Medicl College (Chngzhi, Chin) from June 2016 to June 2018 were
2 PAN nd JI: ULTRASOUND COMBINED WITH MRI IN BREAST CANCER collected, studied s the brest cncer group, 80 ptients with benign brest tumor treted in Heping Hospitl Affilited to Chngzhi Medicl College in the sme period were the benign group. Tumor size, brest cncer clssifiction nd other tumor lesions nd the dignosis of brest cncer re subject to pthologicl results. Inclusion criteri of the brest cncer group were: those confirmed s brest cncer by pthology; femles >18 yers old; those who signed the informed consent form. Exclusion criteri of the brest cncer group were: those with severe fungl bcteril virus infections; those with other severe bsic diseses such s hert, liver nd kidney; those with mentl illness nd mentl disorders; MRI nd US contrindictions; pregnnt or lctting women; those with incomplete clinicl dt; those unstisfied with US nd MRI exmintion imges cquired; those with incomplete pthologicl histologicl dt; those who hd received ny brest cncer-relted tretment within 3 months. Inclusion criteri of the benign group were: those with clinicl symptoms such s pinless lump, nipple dischrge nd nipple chnge; those dignosed s benign brest tumor by pthology nd clinicl plption; femles >18 yers old; those who signed the informed consent form. Exclusion criteri of the benign group were: those with severe fungl bcteril virus infections; those with other severe bsic diseses such s hert, liver nd kidney; those with mentl illness nd mentl disorders; MRI nd US contrindictions; pregnnt or lctting women; those with incomplete clinicl dt; those unstisfied with US nd MRI exmintion imges cquired; those with incomplete pthologicl histologicl dt. This study hs been pproved by the Ethics Committee of Heping Hospitl Affilited to Chngzhi Medicl College. Exmintion time. The brest lump tissue ws surgiclly resected for pthologicl exmintion, nd US nd MRI were performed t 1 week before opertion. US, MRI nd the combintion of the two were used to confirm the dignosis of brest cncer, nd then the TNM stging ws perform of the confirmed pthology. US exmintion. The Antres US dignostic pprtus (Beijing Orientl Mirun Medicl Devices Co., Ltd., Beijing, Chin) hs probe frequency of 8-15 MHz. The two-dimensionl US ws used to first investigte the shpe, size, mrgin, internl posterior echo nd internl clcifiction of the lesion for judging benign nd mlignnt ccording to the BI-RADS stndrd. The Color Doppler Flow Imging (CDFI) ws used to observe the blood flow distribution inside nd round the lesion, with blood flow resistnce index (RI) of mlignnt lesions of 0.70. Either the two-dimensionl US or CDFI detected the lesion s mlignnt nd tht ws dignosed s brest cncer. MRI exmintion. A 5T mgnetic resonnce scnner (Shenzhen Siemens Mgnetic Resonnce Co., Ltd., Shenzhen, Chin) nd bilterl brest surfce coil were used in MRI, with contrst gent s gdodimide injection (Shnghi Generl Electric Phrmceuticl Shnghi Co., Ltd., Shnghi, Chin; SFDA pprovl number: J20140164). MRI scn ws used to observe the shpe, mrgin nd internl structure of the tumor, nd brest cncer scn showed more lobulted or burr signs. The low signl of T1WI nd high signl of T2WI, with uneven Tble I. Criteri of T, N nd M stging. Stging T stging Tis in situ crcinom T1 T2 T3 T4 N stging N0 N1 N2 N3 M stging M0 M1 internl signl, were the enhnced performnce of the mesh or islnd MRI enhnced scnning for observing the tumor. The brest cncer lump showed ring-enhnced chnge. TNM stging. The brest lump tissue ws surgiclly resected for pthologicl exmintion, nd brest cncer ws stged ccording to the TNM stging (8). The T stging is minly bsed on tumor size, N stging on the swollen regionl lymph node nd metstsis, nd M stging on the distnt metstsis of the tumor. The criteri of T, N nd M stging re shown in Tble Ⅰ. Comprison indictors. Pthologicl results were used s the gold stndrd to compre the dignostic coincidence of US nd MRI in brest cncer ptients in different stges of T, N nd M. The sensitivity (SEN), specificity (SPE), negtive predictive vlue (NPV), positive predictive vlue (PPV) nd Youden index (YI) of ech group were compred. YI = SEN + SPE - 1. Sttisticl nlysis. SPSS19.0 softwre system (IBM, SPSS, Chicgo, IL, USA) ws used for dt nlysis. Mesurement dt were expressed s men ± SD nd tested by t-test. Count dt were expressed s % nd tested by Chi-squre test. The level of significnce is α=0.05. Results Tumor conditions No plpble lump in the brest Mximum dimeter of tumor: <2 cm Mximum dimeter of tumor: 2-5 cm Mximum dimeter of tumor: >5 cm Regrdless of tumor size, it hs lredy invded the chest wll or skin No plpble regionl lymph node Ipsilterl xillry lymph nodes swollen with ctivity Ipsilterl xillry lymph nodes swollen, fused to ech other nd even dhered to other tissues Ipsilterl internl mmmry lymph nodes with metstsis No distnt metstsis Distnt metstsis including lymph node metstsis on ipsilterl clvicle Generl clinicl dt of ptients. There ws no difference between brest cncer group nd benign group in generl clinicl dt such s ge, menopusl sttus, lesion size nd number nd tumor site (P>0.05), but significnt differences in the expression of estrogen receptor (ER), progesterone
ONCOLOGY LETTERS 3 Tble II. Generl clinicl dt of ptients. Brest cncer Benign group Clinicl dt group (n=140) (n=80) χ 2 vlue P-vlue Age 35.34±16.54 32.13±13.24 1.577 0.117 Menstrul sttus [n (%)] 2.020 0.155 Before menopuse 110 (78.57) 56 (70.00) After menopuse 30 (21.43) 24 (30.00) Lesion size (cm) 0.42-5.44 0.59-5.22 0.229 0.819 Lesion number [n (%)] 7.356 0.007 Single lesion 74 (52.86) 56 (70.00) Multiple lesions 66 (47.14) 24 (30.00) Tumor site 0.094 0.759 Left brest 74 (52.86) 44 (55.00) Right brest 66 (47.14) 36 (45.00) ER 36.780 <0.001 Negtive 49 (35.00) 62 (77.50) Positive 91(65.00) 18 (22.50) PR 6.890 0.009 Negtive 60 (42.86) 49 (61.25) Positive 80 (57.14) 31 (38.75) Her-2 55.210 <0.001 Negtive 92 (65.71) 11 (13.75) Positive 48 (34.29) 69 (86.25) Pthologicl clssifiction [n (%)] - - (WHO clssifiction criteri for brest cncer) Invsive ductl crcinom 32 (22.86) - Intrductl crcinom 20 (14.29) - Medullry crcinom 5 (3.57) - Ppillry crcinom 36 (25.71) - Simple crcinom 33 (23.57) - Apocrine crcinom 14 (10.00) - receptor (PR) nd humn epiderml growth fctor receptor 2 (Her-2). The positive expression cse rtes of ER nd PR were significntly higher in brest cncer group thn those in benign group, but tht of Her-2 ws significntly lower in brest cncer group thn tht in benign group (ll P<0.05) (Tble Ⅱ). Comprison of brest cncer dignosis between US nd MRI. Among 140 ptients dignosed s brest cncer by pthology, 107 ptients were dignosed by US, 125 ptients by MRI nd 129 ptients by US combined with MRI (+). Specific results re shown in Tble Ⅲ. The SEN of MRI lone ws not different from tht of US combined with MRI (P>0.05), but tht of MRI lone nd US combined with MRI ws higher thn tht of US lone (P<0.05). The SPE of US lone ws not different from tht of US combined with MRI (P>0.05), but tht of MRI lone ws lower thn tht of US lone nd US combined with MRI (P<0.05). The difference in the PPV mong the three methods ws not sttisticlly significnt (P>0.05). The NPV of US lone nd US combined with MRI ws not different from tht of MRI lone (P>0.05). The NPV of US combined with MRI ws significntly higher thn tht of US lone (P<0.05). Tble III. Results of US, MRI nd pthology for brest cncer dignosis. US/MRI Pthology Pthology detection results results (+) results (-) Totl US (+) 107 17 124 US (-) 33 63 96 Totl 140 80 220 MRI (+) 125 29 154 MRI (-) 15 51 66 Totl 140 80 220 US combined with MRI (+) 129 13 142 US combined with MRI (-) 11 67 78 Totl 140 80 220 The YI of US combined with MRI ws significntly higher thn tht of US lone nd MRI lone, nd tht of US lone ws
4 PAN nd JI: ULTRASOUND COMBINED WITH MRI IN BREAST CANCER Tble IV. Comprison of SEN, SPE, PPV nd NPV mong groups. Detection US MRI US combined indictors (%) (%) with MRI (%) χ 2 vlue P-vlue SEN 76.43 89.29 92.14 16.25 <0.001 SPE 78.75 63.75 83.75 b 9.349 <0.001 PPV 86.29 81.17 90.85 5.746 0.057 NPV 65.63 77.27 85.90 9.709 0.008 YI 55.18 53.04 75.89 - - P<0.05 compred with US. b P<0.05 compred with MRI. Figure 1. The SEN of MRI lone ws not different from tht of US combined with MRI (P>0.05), but tht of MRI lone nd US combined with MRI ws higher thn tht of US lone (P<0.05). The SPE of US lone ws not different from tht of US combined with MRI (P>0.05), but tht of MRI lone ws lower thn tht of US lone nd US combined with MRI (P<0.05). The difference in the PPV mong three methods ws not sttisticlly significnt (P>0.05). The NPV of US lone nd US combined with MRI ws not different from tht of MRI lone (P>0.05). The NPV of US combined with MRI ws significntly higher thn tht of US lone (P<0.05). The YI of US combined with MRI ws significntly higher thn tht of US lone nd MRI lone, nd tht of US lone ws not significntly different from tht of MRI lone. * P<0.05, with the sme dignostic efficcy indictor, compred with US; # P<0.05, with the sme dignostic efficcy indictor, compred with MRI. not significntly different from tht of MRI lone (Fig. 1 nd Tble Ⅳ). Comprison of T stging dignosis of brest cncer between US nd MRI. The evlution of T stging nd pthology of 140 ptients before opertion ws compred mong US, MRI nd US combined with MRI. The results showed tht the difference in the dignosis of T1 nd T3 mong three methods ws not sttisticlly significnt (P>0.05), with coincidence rtes of 100% in the evlution of T4. In the dignosis of T2, the coincidence rtes of MRI lone nd US combined with MRI were significntly higher thn tht of US lone (P<0.05), nd tht of MRI lone ws not significntly different thn tht of US combined with MRI (P>0.05) (Tble Ⅴ). Comprison of N stging dignosis of brest cncer between US nd MRI. The evlution of N stging nd pthology of 140 ptients before opertion ws compred mong US, MRI nd US combined with MRI. The results showed tht the difference in N1 nd N3 mong three methods ws not sttisticlly significnt (P>0.05). In the evlution of N0, the coincidence rtes of MRI lone nd US combined with MRI were higher thn tht of US lone (P<0.05), nd tht of MRI lone ws not different thn tht of US combined with MRI (P>0.05). In the dignosis of N2, tht of US combined with MRI ws significntly higher thn those of US lone nd MRI lone (P<0.05), nd tht of MRI lone ws not significntly different thn tht of US lone (P>0.05) (Tble Ⅵ). Comprison of M stging dignosis of brest cncer between US nd MRI. The evlution of M stging nd pthology of 140 ptients before opertion ws compred mong US, MRI nd US combined with MRI. The results showed tht in stges of M0 nd M1 mong the three methods, the coincidence rtes of MRI lone nd US combined with MRI were higher thn tht of US lone (P<0.05), nd tht of MRI lone ws not significntly different from tht of US combined with MRI (P>0.05) (Tble Ⅶ). Discussion In recent yers, s its incidence occurs t younger ge nd mortlity hs grdully incresed, brest cncer hs become the number one killer thretening femle helth (9,10). Clinicl fetures of erly brest cncer re typicl, with high misdignosis nd missed dignosis rtes, so most of brest cncer ptients re in the dvnced stge when dignosed. At present, there is no cler nd effective primry prevention method. Therefore, the erly detection nd ccurte preopertive stging nd tretment of brest cncer re crucil to improve the prognosis (11,12). Mny studies hve been reported on the vlue of US combined with MRI detection in brest cncer stging, but most of them only focus on T stging nd dignosis efficiency, few only on N nd M stging (13). Therefore, in this study, the dignostic vlue of US combined with MRI in the T, N nd M stging of brest cncer ws nlyzed, in order to provide more effective, sensitive nd ccurte detection progrm for the erly dignosis nd ccurte stging, improving the efficcy of ptients' subsequent tretment nd the prognoses. The positive expression cse rtes of ER nd PR were significntly higher in brest cncer group thn those in benign group, but tht of Her-2 ws significntly lower in brest cncer group thn tht in benign group. This is consistent with the findings of Li et l (14), in the study of ER, PR nd HER-2 expression in brest cncer nd their reltionship with tumor stging nd lymph node metstsis. ER, PR nd HER-2 re importnt indictors for judging the prognosis of the ptient. In the evlution of brest cncer T stging, US, MRI nd US combined with MRI hd coincidence rtes of 100% in the evlution of T4. The coincidence rtes of MRI lone nd US combined MRI in the dignosis of T2 were significntly higher thn tht of US lone, with no sttisticlly significnt difference in other stges. The ccurcy of MRI nd US for tumor lesion nd tumor size in newly dignosed non-high-risk brest cncer ptients ws compred by Segr et l (15). The
ONCOLOGY LETTERS 5 Tble V. Results of brest cncer T stging in US nd MRI. Pthologicl US consistent with MRI consistent with US combined with MRI consistent T stging pthology, n (%) pthology, n (%) with pthology, n (%) χ 2 vlue P-vlue T1 (n=13) 7 (53.85) 10 (76.92) 11 (84.62) 3.292 0.193 T2 (n=72) 50 (69.44) 62 (86.11) 64 (88.89),b 10.550 0.005 T3 (n=44) 39 (88.64) 42 (95.45) 43 (97.73) 4.827 0.090 T4 (n=11) 11 (100.00) 11 (100.00) 11 (100.00) - - Totl (n=140) 107 (76.43) 125 (89.29) 129 (92.14),b 16.250 <0.001 P<0.05 compred with US in the sme T stging. b P<0.05 compred with MRI in the sme T stging. Tble VI. Results of brest cncer N stging in US nd MRI. Pthologicl US consistent with MRI consistent with US combined with MRI consistent T stging pthology, n (%) pthology, n (%) with pthology, n (%) χ 2 vlue P-vlue N0 (n=75) 60 (80.00) 69 (92.00) 69 (92.00) 4.485 0.034 N1 (n=37) 30 (81.08) 32 (86.49) 34 (91.89) 1.850 0.397 N2 (n=20) 13 (65.00) 17 (85.00) 19 (95.00) 6.234 0.044 N3 (n=8) 4 (50.00) 7 (87.50) 7 (87.50) 4.200 0.135 Totl (n=140) 107 (76.43) 125 (89.29) 129 (92.14) 16.250 <0.001 P<0.05 compred with US in the sme N stging. Tble Ⅶ. Results of brest cncer M stging in US nd MRI. Pthologicl US consistent with MRI consistent with US combined with MRI consistent T stging pthology, n (%) pthology, n (%) with pthology, n (%) χ 2 vlue P-vlue M0 (n=124) 98 (79.03) 111 (89.52) 114 (91.94) 10.200 0.006 M1 (n=16) 9 (56.25) 14 (87.50) 15 (93.75) 7.832 0.020 Totl (n=140) 107 (76.43) 125 (89.29) 129 (92.14) 16.250 <0.001 P<0.05 compred with US in the sme M stging. results hve shown tht the difference in tumor size is not significnt between MRI nd pthologicl findings. Among molybdenum plldium, US nd MRI, brest cncer size is the most ccurte when mesured by MRI (15). In the evlution of brest cncer N stging, the coincidence rtes of MRI lone nd US combined with MRI were higher thn tht of US lone in the evlution of N0. In the dignosis of N2, tht of US combined with MRI ws significntly higher thn those of US lone nd MRI lone. In stge N2, the ipsilterl xillry lymph nodes of brest cncer ptients were swollen, fused to ech other nd even dhered to other tissues. Therefore, the key point in the exmintion is to judge the brest lymph node metstsis nd the orgn invsion round the brest. MRI soft tissue hs high resolution nd high field NMR. It cn be multi-sequence nd multi-ngle imging, more ccurte for observing brest lymph nodes nd brest circumference. Nevertheless, there re still some difficulties in identifying smller lymph nodes. After the use of developer, identifying the site nd shpe of the primry lesion, US cn lso evlute the obvious contrst effect between the strong echogenic surfce produced by ultrsound shdow gent nd the brest structure nd the tissue round the brest, so s to significntly improve the imge qulity nd better observe brest conditions. However, the xillry lymph in the stge of N2 fuse with ech other nd even dhere to other tissues, cusing certin degree of interference to coustic shdow, so US exmintion hs certin difficulties (16,17). In stges of M0 nd M1 mong the three methods, the coincidence rtes of MRI lone nd US combined with MRI were higher thn tht of US lone, nd tht of MRI lone ws not significntly different from tht of US combined with MRI. Clerly displying the locl irregulr thickening of the brest, MRI cn determine whether there is tumor invsion nd liver metstsis outside the brest, nd tumor recurrence. US for observing the hierrchicl structure of the brest cn determine the depth of lesion invsion nd lymph
6 PAN nd JI: ULTRASOUND COMBINED WITH MRI IN BREAST CANCER node metstsis round the brest, but it my be difficult to distinguish when ulcer or tumor lesions occur (18,19). In summry, US combined with MRI for the dignosis of brest cncer hs higher SEN nd SPE, with better ccurcy rte for the identifiction of ech stge. Reducing the incidence of missed dignosis nd misdignosis tht my be cused by single dignosis nd tretment, it is conducive to clinicl screening nd guiding clinicl symptomtic tretment nd worthy of clinicl promotion. Acknowledgements Not pplicble. Funding This study ws supported by the project of Chngzhi Medicl College Doctorl Scientific Reserch Strt-up Fund (no. BS15002). Avilbility of dt nd mterils The dtsets used nd/or nlyzed during the present study re vilble from the corresponding uthor on resonble request. Authors' contributions QP ws responsible for US exmintion. JJ nlyzed the dt of US nd MRI exmintion. Both uthors red nd pproved the finl mnuscript. Ethics pprovl nd consent to prticipte The study ws pproved by the Ethics Committee of Heping Hospitl Affilited to Chngzhi Medicl College (Chngzhi, Chin). Ptients who prticipted in this study, signed the informed consent nd hd complete clinicl dt. Ptient consent for publiction Not pplicble. Competing interests The uthors declre tht they hve no competing interests. References 1. Merckel LG, Knuttel FM, Deckers R, vn Dlen T, Schubert G, Peters NH, Weits T, vn Diest PJ, Mli WP, Vessen PH, et l: First clinicl experience with dedicted MRI-guided highintensity focused ultrsound system for brest cncer bltion. Eur Rdiol 26: 4037-4046, 2016. 2. Onitilo AA, Engel JM, Greenlee RT nd Mukesh BN: Brest cncer subtypes bsed on ER/PR nd Her2 expression: Comprison of clinicopthologic fetures nd survivl. Clin Med Res 7: 4-13, 2009. 3. 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