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Published in: European Radiology 5/2018

Open Access 01-05-2018 | Breast

Breast lesions classified as probably benign (BI-RADS 3) on magnetic resonance imaging: a systematic review and meta-analysis

Authors: Claudio Spick, Hubert Bickel, Stephan H. Polanec, Pascal A. Baltzer

Published in: European Radiology | Issue 5/2018

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Abstract

Purpose

To investigate prevalence, malignancy rates, imaging features, and follow-up intervals for probably benign (BI-RADS 3) lesions on breast magnetic resonance imaging (MRI).

Methods

A systematic database-review of articles published through 22/06/2016 was performed. Eligible studies reported BI-RADS 3 lesions on breast MRI. Two independent reviewers performed a literature review and data extraction. Data collection included study characteristics, number/type of BI-RADS 3 lesions, final diagnosis (histopathology and/or follow-up). Sources of bias (QUADAS-2) were assessed. Meta-analysis included data-pooling, heterogeneity testing, and meta-regression.

Results

Fifteen studies were included. Prevalence was reported in 11 studies (range: 1.2-24.3%). Malignancy rates ranged between 0.5-10.1% (pooled 61/2814, 1.6%, 95%-CI:0.9-2.3% (random-effects-model), I2=53%, P=0.007). In a subgroup of 11 studies (2183 lesions), highest malignancy rates were observed in non-mass lesions (pooled 25/714, 2.3%, 95%-CI:0.8-3.9%, I2=52%, P=0.021) followed by mass lesions (pooled 15/771, 1.5%, 95%-CI:0.7-2.4%, I2=0%, P=0.929), and foci (pooled 10/698, 1%, 95%-CI:0.3-1.7%, I2=0%, P=0.800). There was non-significant negative association between prevalence and malignancy rates (P=0.077). Malignant lesions were diagnosed at all follow-up time points.

Conclusion

While prevalence of MRI BI-RADS 3 lesions was strongly heterogeneous, pooled malignancy rates met BI-RADS benchmarks (<2%). Malignancy rates varied, exceeding 2% in non-mass lesions. Twenty-four-month surveillance is required to detect all malignant lesions.

Key points

• Probably benign (BI-RADS 3) lesions showed a pooled malignancy-rate of 1.6% (95%-CI:0.9-2.3%).
• Malignancy rates differ and are highest in non-mass lesions (2.3%, 95%-CI:0.8-3.9%).
• The prevalence of BI-RADS 3 lesions on breast MRI ranged from 1.2-24.3%.
• Malignant lesions were diagnosed at follow-up time points up to 24 months.
Literature
1.
go back to reference American College of Radiology Breast Imaging Reporting and Data System (BI-RADS). 5th ed. Reston, VA: American College of Radiology; 2013. American College of Radiology Breast Imaging Reporting and Data System (BI-RADS). 5th ed. Reston, VA: American College of Radiology; 2013.
2.
go back to reference Comstock C, Sung JS (2013) BI-RADS 3 for magnetic resonance imaging. Magn Reson Imaging Clin N Am 21:561–570CrossRefPubMed Comstock C, Sung JS (2013) BI-RADS 3 for magnetic resonance imaging. Magn Reson Imaging Clin N Am 21:561–570CrossRefPubMed
3.
go back to reference Lee KA (2014) Breast Imaging Reporting and Data System category 3 for magnetic resonance imaging. Top Magn Reson Imaging TMRI 23:337–344CrossRefPubMed Lee KA (2014) Breast Imaging Reporting and Data System category 3 for magnetic resonance imaging. Top Magn Reson Imaging TMRI 23:337–344CrossRefPubMed
4.
go back to reference Moher D, Liberati A, Tetzlaff J et al (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097CrossRefPubMedPubMedCentral Moher D, Liberati A, Tetzlaff J et al (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097CrossRefPubMedPubMedCentral
5.
go back to reference Jalali S, Wohlin C (2012) Systematic literature studies: database searches vs. backward snowballing. ACM Press, p 29 Jalali S, Wohlin C (2012) Systematic literature studies: database searches vs. backward snowballing. ACM Press, p 29
6.
go back to reference Whiting PF, Rutjes AWS, Westwood ME et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536CrossRefPubMed Whiting PF, Rutjes AWS, Westwood ME et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536CrossRefPubMed
8.
go back to reference Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558CrossRefPubMed Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558CrossRefPubMed
9.
go back to reference Duval S, Tweedie R (2000) Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463CrossRefPubMed Duval S, Tweedie R (2000) Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463CrossRefPubMed
10.
go back to reference Kuhl CK, Schmutzler RK, Leutner CC et al (2000) Breast MR imaging screening in 192 women proved or suspected to be carriers of a breast cancer susceptibility gene: preliminary results. Radiology 215:267–279CrossRefPubMed Kuhl CK, Schmutzler RK, Leutner CC et al (2000) Breast MR imaging screening in 192 women proved or suspected to be carriers of a breast cancer susceptibility gene: preliminary results. Radiology 215:267–279CrossRefPubMed
11.
go back to reference Liberman L, Morris EA, Benton CL et al (2003) Probably benign lesions at breast magnetic resonance imaging: preliminary experience in high-risk women. Cancer 98:377–388CrossRefPubMed Liberman L, Morris EA, Benton CL et al (2003) Probably benign lesions at breast magnetic resonance imaging: preliminary experience in high-risk women. Cancer 98:377–388CrossRefPubMed
12.
go back to reference Kriege M, Brekelmans CTM, Boetes C et al (2004) Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. N Engl J Med 351:427–437CrossRefPubMed Kriege M, Brekelmans CTM, Boetes C et al (2004) Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. N Engl J Med 351:427–437CrossRefPubMed
13.
go back to reference Sadowski EA, Kelcz F (2005) Frequency of malignancy in lesions classified as probably benign after dynamic contrast-enhanced breast MRI examination. J Magn Reson Imaging JMRI 21:556–564CrossRefPubMed Sadowski EA, Kelcz F (2005) Frequency of malignancy in lesions classified as probably benign after dynamic contrast-enhanced breast MRI examination. J Magn Reson Imaging JMRI 21:556–564CrossRefPubMed
14.
go back to reference Eby PR, DeMartini WB, Gutierrez RL et al (2009) Characteristics of probably benign breast MRI lesions. AJR Am J Roentgenol 193:861–867CrossRefPubMed Eby PR, DeMartini WB, Gutierrez RL et al (2009) Characteristics of probably benign breast MRI lesions. AJR Am J Roentgenol 193:861–867CrossRefPubMed
15.
go back to reference Weinstein SP, Hanna LG, Gatsonis C et al (2010) Frequency of malignancy seen in probably benign lesions at contrast-enhanced breast MR imaging: findings from ACRIN 6667. Radiology 255:731–737CrossRefPubMedPubMedCentral Weinstein SP, Hanna LG, Gatsonis C et al (2010) Frequency of malignancy seen in probably benign lesions at contrast-enhanced breast MR imaging: findings from ACRIN 6667. Radiology 255:731–737CrossRefPubMedPubMedCentral
16.
go back to reference Hauth E, Umutlu L, Kümmel S et al (2010) Follow-up of probably benign lesions (BI-RADS 3 category) in breast MR imaging. Breast J 16:297–304CrossRefPubMed Hauth E, Umutlu L, Kümmel S et al (2010) Follow-up of probably benign lesions (BI-RADS 3 category) in breast MR imaging. Breast J 16:297–304CrossRefPubMed
17.
go back to reference Marshall AL, Domchek SM, Weinstein SP (2012) Follow-up frequency and compliance in women with probably benign findings on breast magnetic resonance imaging. Acad Radiol 19:406–411CrossRefPubMed Marshall AL, Domchek SM, Weinstein SP (2012) Follow-up frequency and compliance in women with probably benign findings on breast magnetic resonance imaging. Acad Radiol 19:406–411CrossRefPubMed
18.
go back to reference Lourenco AP, Chung MTM, Mainiero MB (2014) Probably benign breast MRI lesions: frequency, lesion type, and rate of malignancy. J Magn Reson Imaging JMRI 39:789–794CrossRefPubMed Lourenco AP, Chung MTM, Mainiero MB (2014) Probably benign breast MRI lesions: frequency, lesion type, and rate of malignancy. J Magn Reson Imaging JMRI 39:789–794CrossRefPubMed
19.
go back to reference Bahrs SD, Baur A, Hattermann V et al (1987) (2014) BI-RADS® 3 lesions at contrast-enhanced breast MRI: is an initial short-interval follow-up necessary? Acta Radiol Stockh Swed 55:260–265 Bahrs SD, Baur A, Hattermann V et al (1987) (2014) BI-RADS® 3 lesions at contrast-enhanced breast MRI: is an initial short-interval follow-up necessary? Acta Radiol Stockh Swed 55:260–265
20.
go back to reference Spick C, Szolar DHM, Baltzer PA et al (2014) Rate of malignancy in MRI-detected probably benign (BI-RADS 3) lesions. AJR Am J Roentgenol 202:684–689CrossRefPubMed Spick C, Szolar DHM, Baltzer PA et al (2014) Rate of malignancy in MRI-detected probably benign (BI-RADS 3) lesions. AJR Am J Roentgenol 202:684–689CrossRefPubMed
21.
go back to reference Grimm LJ, Anderson AL, Baker JA et al (2015) Frequency of malignancy and imaging characteristics of probably benign lesions seen at breast MRI. AJR Am J Roentgenol 205:442–447CrossRefPubMed Grimm LJ, Anderson AL, Baker JA et al (2015) Frequency of malignancy and imaging characteristics of probably benign lesions seen at breast MRI. AJR Am J Roentgenol 205:442–447CrossRefPubMed
22.
go back to reference Chikarmane SA, Birdwell RL, Poole PS et al (2016) Characteristics, malignancy rate, and follow-up of BI-RADS category 3 lesions identified at breast MR imaging: implications for MR image interpretation and management. Radiology 280:707–715CrossRefPubMed Chikarmane SA, Birdwell RL, Poole PS et al (2016) Characteristics, malignancy rate, and follow-up of BI-RADS category 3 lesions identified at breast MR imaging: implications for MR image interpretation and management. Radiology 280:707–715CrossRefPubMed
23.
go back to reference Boisserie-Lacroix M, Ziadé C, Hurtevent-Labrot G et al (2016) Is a one-year follow-up an efficient method for better management of MRI BI-RADS(®) 3 lesions? Breast Edinb Scotl 27:1–7CrossRef Boisserie-Lacroix M, Ziadé C, Hurtevent-Labrot G et al (2016) Is a one-year follow-up an efficient method for better management of MRI BI-RADS(®) 3 lesions? Breast Edinb Scotl 27:1–7CrossRef
24.
go back to reference Guillaume R, Taieb S, Ceugnart L et al (2016) BIRADS 3 MRI lesions: Was the initial score appropriate and what is the value of the blooming sign as an additional parameter to better characterize these lesions? Eur J Radiol 85:337–345CrossRefPubMed Guillaume R, Taieb S, Ceugnart L et al (2016) BIRADS 3 MRI lesions: Was the initial score appropriate and what is the value of the blooming sign as an additional parameter to better characterize these lesions? Eur J Radiol 85:337–345CrossRefPubMed
26.
go back to reference Schnall MD, Blume J, Bluemke DA et al (2006) Diagnostic architectural and dynamic features at breast MR imaging: multicenter study. Radiology 238:42–53CrossRefPubMed Schnall MD, Blume J, Bluemke DA et al (2006) Diagnostic architectural and dynamic features at breast MR imaging: multicenter study. Radiology 238:42–53CrossRefPubMed
27.
go back to reference Baltzer PAT, Benndorf M, Dietzel M et al (2010) False-positive findings at contrast-enhanced breast MRI: a BI-RADS descriptor study. AJR Am J Roentgenol 194:1658–1663CrossRefPubMed Baltzer PAT, Benndorf M, Dietzel M et al (2010) False-positive findings at contrast-enhanced breast MRI: a BI-RADS descriptor study. AJR Am J Roentgenol 194:1658–1663CrossRefPubMed
28.
go back to reference Woitek R, Spick C, Schernthaner M, et al (2017) A simple classification system (the Tree flowchart) for breast MRI can reduce the number of unnecessary biopsies in MRI-only lesions. Eur Radiol Woitek R, Spick C, Schernthaner M, et al (2017) A simple classification system (the Tree flowchart) for breast MRI can reduce the number of unnecessary biopsies in MRI-only lesions. Eur Radiol
29.
go back to reference Marino MA, Clauser P, Woitek R et al (2016) A simple scoring system for breast MRI interpretation: does it compensate for reader experience? Eur Radiol 26:2529–2537CrossRefPubMed Marino MA, Clauser P, Woitek R et al (2016) A simple scoring system for breast MRI interpretation: does it compensate for reader experience? Eur Radiol 26:2529–2537CrossRefPubMed
30.
go back to reference Baum F, Fischer U, Vosshenrich R, Grabbe E (2002) Classification of hypervascularized lesions in CE MR imaging of the breast. Eur Radiol 12:1087–1092CrossRefPubMed Baum F, Fischer U, Vosshenrich R, Grabbe E (2002) Classification of hypervascularized lesions in CE MR imaging of the breast. Eur Radiol 12:1087–1092CrossRefPubMed
31.
go back to reference Partridge SC, Nissan N, Rahbar H et al (2017) Diffusion-weighted breast MRI: Clinical applications and emerging techniques. J Magn Reson Imaging JMRI 45:337–355CrossRefPubMed Partridge SC, Nissan N, Rahbar H et al (2017) Diffusion-weighted breast MRI: Clinical applications and emerging techniques. J Magn Reson Imaging JMRI 45:337–355CrossRefPubMed
32.
go back to reference Pinker K, Bickel H, Helbich TH et al (2013) Combined contrast-enhanced magnetic resonance and diffusion-weighted imaging reading adapted to the “Breast Imaging Reporting and Data System” for multiparametric 3-T imaging of breast lesions. Eur Radiol 23:1791–1802CrossRefPubMed Pinker K, Bickel H, Helbich TH et al (2013) Combined contrast-enhanced magnetic resonance and diffusion-weighted imaging reading adapted to the “Breast Imaging Reporting and Data System” for multiparametric 3-T imaging of breast lesions. Eur Radiol 23:1791–1802CrossRefPubMed
33.
go back to reference Baltzer A, Dietzel M, Kaiser CG, Baltzer PA (2016) Combined reading of contrast enhanced and diffusion weighted magnetic resonance imaging by using a simple sum score. Eur Radiol 26:884–891CrossRefPubMed Baltzer A, Dietzel M, Kaiser CG, Baltzer PA (2016) Combined reading of contrast enhanced and diffusion weighted magnetic resonance imaging by using a simple sum score. Eur Radiol 26:884–891CrossRefPubMed
34.
go back to reference Spick C, Pinker-Domenig K, Rudas M et al (2014) MRI-only lesions: application of diffusion-weighted imaging obviates unnecessary MR-guided breast biopsies. Eur Radiol 24:1204–1210CrossRefPubMed Spick C, Pinker-Domenig K, Rudas M et al (2014) MRI-only lesions: application of diffusion-weighted imaging obviates unnecessary MR-guided breast biopsies. Eur Radiol 24:1204–1210CrossRefPubMed
35.
go back to reference Woodhams R, Matsunaga K, Iwabuchi K et al (2005) Diffusion-weighted imaging of malignant breast tumors: the usefulness of apparent diffusion coefficient (ADC) value and ADC map for the detection of malignant breast tumors and evaluation of cancer extension. J Comput Assist Tomogr 29:644–649CrossRefPubMed Woodhams R, Matsunaga K, Iwabuchi K et al (2005) Diffusion-weighted imaging of malignant breast tumors: the usefulness of apparent diffusion coefficient (ADC) value and ADC map for the detection of malignant breast tumors and evaluation of cancer extension. J Comput Assist Tomogr 29:644–649CrossRefPubMed
Metadata
Title
Breast lesions classified as probably benign (BI-RADS 3) on magnetic resonance imaging: a systematic review and meta-analysis
Authors
Claudio Spick
Hubert Bickel
Stephan H. Polanec
Pascal A. Baltzer
Publication date
01-05-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 5/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-5127-y

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