Performance of Elastography, Color Doppler and B Mode Ultrasound to Differentiate Fibroadenomas from Phyllodes Tumors

doi:10.37015/AUDT.2022.220003

Abstract

Abstract:

Objective: To evaluate and compare the diagnostic performance of B-mode ultrasound (B-mode US), strain elastography (SE), color Doppler ultrasound (color Doppler US) and the combination of these modalities in differentiation between fibroadenomas and phyllodes tumors.

Methods: This retrospective study included 220 breast lesions, between January 2016 and January 2018. B-mode US, strain elastography, and color Doppler US were realized to evaluate each lesion. The results of three modalities were compared between the B-mode US and the combination of B-mode US, elastography, and color Doppler US: sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and area under the receiver operating characteristic curve (AUC). The pathological findings were used as the reference standard.

Results: Among 220 breast masses, 189 of the lesions were fibroadenomas, 31 were phyllodes tumors. Addition of strain elastography and color Doppler US to B-mode US increased the specificity from 27.5% (95% confidence interval [CI]: 21.15%, 33.88%) to 95.24% (95% CI: 92.20%, 98.27%; P < 0.001); PPV from 16.46% (95% CI: 10.79%,22.14%) to 60.87% (95% CI: 40.92%, 80.82%; P < 0.001) and AUC from 0.584 (95% CI: 0.481, 0.687) to 0.886 (95% CI: 0.824, 0.948; P < 0.001).

Conclusion: The combination B-mode US, strain elastography and color Doppler US increase the diagnostic performance in distinguishing fibroadenomas from phyllodes tumors.

Key words: Breast; Elastography; Ultrasound; Color Doppler; Fibroadenoma; Phyllodes tumor

Lynda Aoudia, Amal Kouchkar, Salah Eddine Bendib. Performance of Elastography, Color Doppler and B Mode Ultrasound to Differentiate Fibroadenomas from Phyllodes Tumors. Advanced Ultrasound in Diagnosis and Therapy, 2022, 6(4): 195-203.

Figures/Tables 10

Table 1

Figure 1

Table 2

Table 3

Table 4

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

References 29

[1]	Jacobs TW, Chen YY, Guinee DG Jr, Holden JA, Cha I, Bauermeister DE, et al. Fibroepithelial lesions with cellular stroma on breast core needle biopsy: are there predictors of outcome on surgical excisio. Am J Clin Pathol 2005 ; 124: 342-354. doi: 10.1309/5N2C4N5XCB8XW8JL
[2]	Kuijper A, Buerger H, Simon R, Schaefer KL, Croonen A, Boecker W, et al. Analysis of the progression of fibroepithelial tumours of the breast by PCR-based clonality assa. J Pathol 2002; 197: 575-581. pmid: 12210075
[3]	Noguchi S, Yokouchi H, Aihara T, Motomura K, Inaji H, Imaoka S, et al. Progression of fibroadenoma to phyllodes tumor demonstrated by clonal analysi. Cancer 1995; 76: 1779-1785. pmid: 8625047
[4]	Lerwill MF. Biphasic lésions of breas. Semin Diagn Pathol 2004; 21: 48-56. doi: 10.1053/j.semdp.2003.10.003
[5]	Rowell MD, Perry RR, Hsiu JG, Barranco SC. Phyllodes tumor. Am J Surg 1993; 165: 376-379. pmid: 8383473
[6]	Chao TC, Lo YF, Chen SC, Chen MF. Sonographic features of phyllodes tumors of the breas. Ultrasound Obstet Gynecol 2002; 20: 64-71. doi: 10.1046/j.1469-0705.2002.00736.x
[7]	Park HL, Kwon SH, Chang SY, Huh JY, Kim JY, Shim JY, et al. Long-term follow-up result of benign phyllodes tumor of the breast diagnosed and excised by ultrasound-guided vacuum-assisted breast biops. J Breast Cancer 2012; 15: 224-229. doi: 10.4048/jbc.2012.15.2.224
[8]	Jacklin RK, Ridgway PF, Ziprin P, Healy V, Hadjiminas D, Darzi A. Optimising preoperative diagnosis in phyllodes tumour of the breast. J Clin Pathol. 2006; 59: 454- 459. pmid: 16461806
[9]	Ciatto S, Houssami N, Ambrogetti D, Bianchi S, Bonardi R, Brancato B, et al. Accuracy and underestimation of malignancy of breast core needle biopsy: the Florence experience of over 4000 consecutive biopsie. Breast Cancer Res Treat 2007; 101: 291-297. doi: 10.1007/s10549-006-9289-6
[10]	Lee AH, Hodi Z, Ellis IO, Elston CW. Histological features useful in the distinction of phyllodes tumour and fibroadenoma on needle core biopsy of the breas. Histopathology 2007; 51: 336-344. pmid: 17727475
[11]	D’Orsi, C.J., Sickles, E.A., Mendelson, E.B., Morris, E. A. ACR BI-RADS® ATLAS breast imaging reporting and data syste. American College of Radiology, Reston, VA, USA, 2013.
[12]	Itoh A, Ueno E, Tohno E, Kamma H, Takahashi H, Shiina T, et al. Breast disease: clinical application of US elastography for diagnosi. Radiology 2006; 239: 341-350.
[13]	Cho N, Jang M, Lyou CY, Park JS, Choi HY, Moon WK. Distinguishing benign from malignant masses at breast US: combined US elastography and color doppler US-influence on radiologist accurac. Radiology 2012; 262: 80-90.
[14]	Lee SH, Chang JM, Kim WH, Bae MS, Seo M, Koo HR, et al. Added value of shear-wave elastography for evaluation of breast masses detected with screening US imagin. Radiology 2014; 273: 61-69.
[15]	Choi JS, Han BK, Ko EY, Ko ES, Shin JH, Kim GR. Additional diagnostic value of shear- wave elastography and color Doppler US for evaluation of breast non-mass lesions detected at B-mode US. Eur Radiol 2016; 26: 3542-3549.
[16]	Singla V, Prakash A, Prabhakar N, Singh T, Bal A, Singh G, et al. Does shear wave elastography score over strain elastography in breast masses or vice vers. Curr Probl Diagn Radiol 2020; 49: 96-101. doi: S0363-0188(18)30272-X pmid: 30981528
[17]	Jia W, Luo T, Dong Y, Zhang X, Zhan W, Zhou J. Breast elasticity imaging techniques: comparison of strain elastography and shear-wave elastography in the same populatio. Ultrasound Med Biol 2021; 47: 104-113. doi: 10.1016/j.ultrasmedbio.2020.09.022
[18]	Golatta M, Pfob A, Büsch C, Bruckner T, Alwafai Z, Balleyguier C, et al. The potential of combined shear wave and strain elastography to reduce unnecessary biopsies in breast cancer diagnostics - An international, multicentre tria. Eur J Cancer 2022; 161:1-9. doi: 10.1016/j.ejca.2021.11.005
[19]	Yu Y, Ye X, Yang J, Chen L, Zhang M, He Y, et al. Application of a shear-wave elastography prediction model to distinguish between benign and malignant breast lesions and the adjustment of ultrasound breast imaging reporting and data system classifications. Clin Radiol 2022; 77: e147-e153.
[20]	Youden WJ. Index for rating diagnostic test. Cancer 1950; 3: 32-35. doi: 10.1002/1097-0142(1950)3:1<32::AID-CNCR2820030106>3.0.CO;2-3
[21]	Li LJ, Zeng H, Ou B, Luo BM, Xiao XY, Zhong WJ, et al. Ultrasonic elastography features of phyllodes tumors of the breast: a clinical researc. PLoS One 2014; 9: e85257.
[22]	Choi J, Koo JS. Comparative study of histological features between core needle biopsy and surgical excision in phyllodes tumo. Pathol Int 2012; 62: 120-126. doi: 10.1111/j.1440-1827.2011.02761.x
[23]	Kim GR, Choi JS, Han BK, Ko EY, Ko ES, Hahn SY. Combination of shear-wave elastography and color Doppler: Feasible method to avoid unnecessary breast excision of fibroepithelial lesions diagnosed by core needle biops. PLoS One 2017; 12: e0175380.
[24]	Chao TC, Lo YF, Chen SC, Chen MF. Phyllodes tumors of the breas. Eur Radiol 2003; 13: 88-93.
[25]	McNicholas MM, Mercer PM, Miller JC, McDermott EW, O'Higgins NJ, MacErlean DP. Color doppler sonography in the evaluation of palpable breast masse. AJR Am J Roentgenol 1993; 161: 765-71. doi: 10.2214/ajr.161.4.8372754
[26]	Gatta G, Iaselli F, Parlato V, Di Grezia G, Grassi R, Rotondo A. Differential diagnosis between fibroadenoma, giant fibroadenoma and phyllodes tumour: sonographic features and core needle biops. Radiol Med 2011; 116: 905-918. doi: 10.1007/s11547-011-0672-y pmid: 21509559
[27]	Wiratkapun C, Piyapan P, Lertsithichai P, Larbcharoensub N. Fibroadenoma versus phyllodes tumor: distinguishing factors in patients diagnosed with fibroepithelial lesions after a core needle biops. Diagn Interv Radiol 2014; 20: 27-33. doi: 10.5152/dir.2013.13133 pmid: 24356293
[28]	Jorge Blanco A, Vargas Serrano B, Rodríguez Romero R, Martínez Cendejas E. Phyllodes tumors of the breast. Eur Radiol 1999;9: 356-360.
[29]	Park HL, Kwon SH, Chang SY, Huh JY, Kim JY, Shim JY, et al. Long-term follow- up result of benign phyllodes tumor of the breast diagnosed and excised by ultrasound-guided vacuum-assisted breast biops. J Breast Cancer 2012; 15: 224-229. doi: 10.4048/jbc.2012.15.2.224

Characteristics	Fibroadenoma (n = 189)	Phyllodes tumor (n = 31)	P value
Lesion size (mm)			< 0.001
Mean ± SD	16.83 ± 8.03	30.61 ± 22.68
BI-RADS Lexicon
Shape			0.057
Oval	174 (92.1%)	25 (80.6%)
Round	8 (4.2%)	4 (12.9%)
Irregular	7 (3.7%)	2 (6.5%)
Orientation			≈ 1.000
Parallel	188 (99.5%)	31 (100%)
Not parallel	1 (0.5%)	0
Margin			0.034
Circumscribed	60 (31.7%)	4 (12.9%)
Micro lobulated	129 (68.3%)	27 (87.1%)
Boundary			< 0.001
Abrupt	189 (100%)	14 (45.2%)
Echogenic halo	0	7 (22.6%)
Echo pattern			0.471
Isoechoic	82 (43.4%)	14 (45.2%)
Hypoechoic	105 (55.5%)	16(51.6%)
Complex	2 (1.1%)	1 (3.2%)
Posterior features			0.466
No posterior features	177 (93.7%)	30 (96.8%)
Enhancement	2 (1.1%)	1 (3.2%)
Shadowing	7 (3.7%)	0
Combined	3 (1.5%)	0
Calcification			0.030
Absent	164 (86.8%)	31 (100%)
Present	25 (13.2%)	0
BI-RADS Category			0.18
3	52 (27.5%)	4 (12.9%)
4a	130 (68.8%)	24 (77.4%)
4b	1 (0.5%)	1 (3.2%)
4c	6 (3.2%)	2 (6.5%)

Characteristics	Fibroadenoma (n = 189)	Phyllodes tumor (n = 31)	P value
Color Doppler US			< 0.001
No vascularity	40 (21.2%)	1 (3.2%)
Vessels in rim	93 (49.2%)	9 (29.0%)
Vessels in rim and internal vascularity	56 (29.6%)	21 (67.7%)
Elasticity score			0.070
1	4 (2.1%)	0
2	140 (74.1%)	20 (64.5%)
3	44 (23.3%)	9 (29.0%)
4	1 (0.5%)	2 (6.5%)
Strain ratio			< 0.001
Mean ± SD	1.90 ± 1.07	3.23 ± 1.29

Characteristics	Mildly cellular stroma (n = 149)	Moderately cellular stroma (n = 40)	Markedly cellular stroma (n = 31)	P value
Elasticity score				0.061
1	2 (1.3%)	2 (5%)	0
2	115 (77.2%)	25 (62.5%)	20 (64.5%)
3	31 (20.8%)	13 (32.5%)	9 (29.0%)
4	1 (0.7%)	0	2 (6.5%)
Strain ratio				< 0.001
Mean ± SD	1.80 ± 1.08	2.28 ± 0.94	3.23 ± 1.29

Items	Sensibility	Specificity	PPV	PNV	Accuracy	AUC
B-mode US
BI-RADS Category ≥ 4a	87.1% (27/31)	27.5% (52/189)	16.5% (27/164)	92.3% (52/56)	35.9% (79/220)	0.584
Color Doppler US
High vascularity^**	67.7% (21/31)	70.4% (133/189)	27.3% (21/77)	93.0% (133/143)	70.0% (154/220)	0.713
P value	0.068	< 0.001^*	0.050	0.970	< 0.001^*	0.069
Strain elastography
Strain ratio ≥ 2.435^***	77.4 % (24/31)	82.5% (156/189)	42.1% (24/57)	95.7% (156/163)	81.8% (180/220)	0.865
P value	0.320	< 0.001^*	< 0.001^*	0.400	< 0.001^*	< 0.001^*
Combination of B-mode US and Color Doppler US
BI-RADS category ≥ 4a and high vascularity^**	58.1% (18/31)	76.7% (145/189)	29.0% (18/62)	91.8% (145/158)	74.1% (163/220)	0.733
P value	0.010^*	< 0.001^*	0.030	0.800	< 0.001^*	0.030
Combination of B-mode US and SE
BI-RADS category ≥ 4a and strain ratio ≥ 2.435^***	71.0% (22/31)	87.8% (166/189)	48.9% (22/45)	94.9% (166/175)	85.5% (188/220)	0.836
P value	0.120	<0.001^*	< 0.001^*	0.570	< 0.001^*	< 0.001^*
Combination of B-mode US, SE and color Doppler US
BI-RADS category ≥ 4a and strain ratio ≥ 2.435^* and high vascularity^	45.2% (14/31)	95.2% (180/189)	60.9% (14/23)	91.4% (180/197)	88.2% (194/220)	0.886
P value	<0.001^*	<0.001^*	<0.001^*	0.720	<0.001^*	< 0.001^*