Abstract
This article provides updates to readers based on the newly published Japanese Breast Cancer Society Clinical Practice Guidelines for Breast Cancer Screening and Diagnosis, 2022 Edition. These guidelines incorporate the latest evaluation of evidence from studies of diagnostic accuracy. For each clinical question, outcomes for benefits and harms were established, and qualitative or quantitative systematic reviews were conducted. Recommendations were determined through voting by a multidisciplinary group, and guidelines were documented to facilitate shared decision-making among patients and medical professionals. The guidelines address screening, surveillance, and pre- and postoperative diagnosis of breast cancer. In an environment that demands an integrated approach, decisions are needed on how to utilize modalities, such as mammography, ultrasound, MRI, and PET/CT. Additionally, it is vital to understand the appropriate use of new technologies, such as tomosynthesis, elastography, and contrast-enhanced ultrasound, and to consider how best to adapt these methods for individual patients.
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Introduction
The Japanese Breast Cancer Society (JBCS) Clinical Practice Guidelines for Breast Cancer Screening and Diagnosis, 2022 Edition provides consensus statements on current approaches to breast cancer screening and diagnosis. From the 2018 edition [1], the practice guidelines are intended to facilitate shared decision-making on all aspects of breast cancer screening and diagnosis. The guidelines were developed in accordance with the Minds Manual for Guideline Development 2020 ver. 3.0 [2]. Outcomes as specific indicators of benefits and harms were established and evaluated by quantitative or qualitative systematic review. QUADAS-2 (A Revised Tool for the Quality Assessment of Diagnostic Accuracy Studies 2) [3] was used to assess the quality of studies of diagnostic accuracy. Finally, recommendations were determined through discussion and voting at a recommendation decision meeting, including physicians, nurses, and breast cancer survivors. This article summarizes the practice guidelines, including eight clinical questions (CQs) and two background questions (BQs), supported by recommendations and evidence, along with the weight of consensus among the expert panelists and supporting references.
Practice guidelines for breast cancer screening
CQ1. Is handheld ultrasound recommended for population-based breast cancer screening?
Recommendation
We recommend use of handheld ultrasound as an adjunct to population-based breast cancer screening mammography. [Strength of Recommendation (SoR), 2; Strength of Evidence (SoE), moderate, consensus rate: 94% (45/48)].
We advise against using handheld ultrasound alone for population-based breast cancer screening. [Strength of Recommendation (SoR), 3; Strength of Evidence (SoE), moderate, consensus rate: 94% (40/46)].
Justification
The only randomized-controlled trial (RCT) of handheld ultrasound, J-START, found a significant increase in the number of Stage I breast cancers detected (control group, n = 48 cases; intervention group, n = 93) and a 50% reduction in intermediate-stage cancers (control group, n = 35; intervention group, n = 18) [4]. This suggests that combined use of ultrasound with mammography may indirectly contribute to a sense of reassurance among examinees. There is concern about an increase in false-positive results, but this can be managed at an acceptable level through appropriate quality control. Therefore, it is weakly recommended to conduct screening using both mammography and ultrasound, provided that proper quality control is ensured. On the other hand, the sensitivity of ultrasonography alone is not superior to that of mammography, and the mortality reduction proven with mammography has not been shown for ultrasound [5, 6]. Therefore, ultrasonography alone is not superior to mammography screening and it is weakly recommended to avoid screening using ultrasound alone.
Practice guidelines forbreast cancer surveillance
CQ2. Is contrast-enhanced breast MRI surveillance recommended for BRCA mutation carriers?
Recommendation
We recommend use of contrast-enhanced breast MRI surveillance for Japanese BRCA mutation carriers [SoR, 1; SoE, moderate, consensus rate: 80% (39/49)].
Justification
A qualitative systematic review was conducted for BRCA pathogenic variant carriers who did and did not undergo MRI-inclusive surveillance [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31]. The overall survival rate, sensitivity, and false-positive rate indicated favorable results with MRI-inclusive surveillance [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21]. Regarding the side effects of gadolinium contrast media, nephrogenic systemic fibrosis (NSF) can be managed through renal function evaluation. Long-term follow-up data showed no evidence of clinical symptoms associated with deposition of the contrast agent in the brain [31]. It is recommended that surveillance using contrast-enhanced breast MRI be performed at facilities with specialists with knowledge of this method and in collaboration with facilities that offer MRI-guided biopsy. For asymptomatic BRCA carriers, it is suggested to conduct surveillance at a center that provides genetic counseling and post-screening follow-up.
Practice guidelines for breast cancer diagnosis
CQ3. Is breast tomosynthesis as an adjunct to mammography recommended in a diagnostic setting?
Recommendation
We recommend breast tomosynthesis as an adjunct to mammography in a diagnostic setting [SoR, 2; SoE, weak, consensus rate: 88% (42/48)].
Justification
In a quantitative meta-analysis [32,33,34,35,36,37,38,39,40,41,42,43,44,45], we found pooled sensitivity of 86.9% and specificity of 88.4% for breast cancer diagnosis using tomosynthesis, with a false-positive rate from 0 to 67.6% [32,33,34,35,36,37,38,39,40,41]. Compared to mammography, tomosynthesis tended to have higher sensitivity and specificity for breast cancer diagnosis and a lower false-positive rate. With regard to radiation dose, the diagnostic reference level (DRL) for tomosynthesis is 1.5 mGy [46]. Dose reduction can be achieved using this value as a guide in image acquisition. Breast tomosynthesis prior to performance of diagnostic ultrasonography can provide more information and improve the diagnostic accuracy of ultrasonography, compared to prior 2D mammography.
CQ4. Is breast elastography as an adjunct to B-mode ultrasound recommended in a diagnostic setting?
Recommendation
We recommend breast elastography as an adjunct to B-mode ultrasound in a diagnostic setting. [SoR, 1–2; unable to reach an agreement; SoE, moderate, consensus rate: strongly recommended 33% (16/48), weakly recommended 56% (27/48), and weakly not recommended 10% (5/48)].
Justification
We performed a quantitative meta-analysis of 7 B-mode ultrasonography articles with 8 qualitative evaluations using strain elastography (SE), 4 semi-quantitative evaluations with SE, and 12 quantitative evaluations using shear-wave elastography (SWE). The results showed that addition of elastography to B-mode ultrasonography resulted in a marked improvement in specificity compared to B-mode ultrasonography alone, whether using SE (qualitative and semi-quantitative) or SWE (quantitative) [47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66]. Biopsy could be avoided in some lesions by adding elastography to B-mode ultrasonography. Because of the slight decrease in sensitivity, the decision to avoid biopsy in practice requires a comprehensive diagnosis that takes into account the elastography results based on differential diagnosis by B-mode ultrasonography.
The recommendation decision meeting did not reach a decision on the level of recommendation, because the opinions were divided between “strongly recommended” and “weakly recommended”.
CQ5. Is contrast-enhanced ultrasound recommended for distinguishing benign and malignant breast lesions?
Recommendation
We recommend use of contrast-enhanced ultrasound for distinguishing benign and malignant breast lesions [SoR, 2; SoE, moderate, consensus rate: 74% (35/47)].
Justification
We conducted a meta-analysis using ten papers [67,68,69,70,71,72,73,74,75,76] comparing conventional B-mode ultrasonography and contrast-enhanced ultrasonography in differentiating between benign and malignant breast lesions. The pooled sensitivity and specificity of B-mode ultrasonography as a control in the meta-analysis were 89.6% and 60.9%, respectively. Addition of contrast-enhanced ultrasonography to B-mode ultrasonography gave a pooled sensitivity and specificity of 95.1% and 80.9%, respectively, indicating improved diagnostic performance for breast masses. Thus, addition of contrast-enhanced ultrasonography to B-mode ultrasonography improves the diagnostic performance for breast lesions. However, this should be considered on a case-by-case basis, taking into account the additional information provided by contrast-enhanced ultrasonography and the possibility of substituting other examinations.
BQ1. Is an additional examination required for newly detected lesions on preoperative contrast-enhanced breast MRI?
Statement
For MRI-detected lesions that are suspected to be malignant on preoperative contrast-enhanced breast MRI, histological examination should be performed if there is an impact on the surgical procedure. However, the patient should be given multidisciplinary information by the medical provider, including additional examinations such as ultrasound, based on a reliable MRI diagnosis, and the indication for histological examination should reflect the values and wishes of the patient.
Justification
We conducted a qualitative systematic review [77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96] and found that false positives occurred in MRI-detected lesions in 44–64.6% of cases. In articles that examined MRI-detected lesions limited to the contralateral breast, false positives for these lesions were reported in 49–86.7% of cases. A 2010 RCT (Comparative Effectiveness of MRI in Breast Cancer (COMICE)) and other studies have found that preoperative MRI increases the number of total mastectomies [97]. Therefore, in principle, the decision on the surgical approach should not be based on preoperative MRI findings alone [98, 99]. Histological diagnosis is recommended for MRI-detected contralateral and ipsilateral lesions that are suspected to be malignant and may affect the surgical approach.
BQ2. Is whole-body examination with CT, PET, or PET-CT recommended for patients with stage I and II preoperative breast cancer?
Statement
Preoperative CT or PET-CT whole-body examination is of low significance in patients with stage I-II breast cancer without signs of distant metastasis. However, systemic examination by CT or PET-CT should be considered in patients who are eligible for preoperative chemotherapy, depending on breast cancer subtype, tumor grade, and patient background.
Justification
After a qualitative systematic review [100,101,102,103,104,105,106,107,108], we decided to define this statement as a BQ, because the previous studies did not provide sufficient evidence to make a decision, and it is unlikely that accumulation of future data will significantly change the outcome. A low prevalence of distant metastases was seen in stage I–II cancers. However, systemic examination should be considered based on the breast cancer subtype, tumor grade, and patient background, which may result in a higher frequency of metastases. In the diagnosis of distant metastasis, FDG-PET/CT has been reported to have high diagnostic performance with sensitivity of 96–100% and specificity of 91–100% [109]. The NCCN guidelines include FDG-PET/CT as an optional procedure for patients with cT2 or higher or cN + (Stage II or higher) when preoperative pharmacologic therapy is considered (since ver. 8.2021) [110]. In addition, some patients may wish to have the examination, and if the benefits and harms are fully explained to the patient and the physician determines that there is a need, it may be appropriate to perform the examination.
Data availability
Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.
Change history
11 December 2023
A Correction to this paper has been published: https://doi.org/10.1007/s12282-023-01533-7
References
Uematsu T, Nakashima K, Kikuchi M, Kubota K, Suzuki A, Nakano S, et al. The Japanese breast cancer society clinical practice guidelines for breast cancer screening and diagnosis 2018 edition. Breast Cancer. 2020;27:17–24.
Minds manual for guideline development 2020 ver.3.0. https://minds.jcqhc.or.jp/s/manual_2020_3_0. Accessed 23 Sep 2023
Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, QUADAS-2 Group, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155:529–36.
Ohuchi N, Suzuki A, Sobue T, Kawai M, Yamamoto S, Zheng YF, J-START investigator groups, et al. Sensitivity and specificity of mammography and adjunctive ultrasonography to screen for breast cancer in the Japan strategic anti-cancer randomized trial (J-START): a randomised controlled trial. Lancet. 2016;387:341–8.
Huang Y, Kang M, Li H, Li JY, Zhang JY, Liu LH, et al. Combined performance of physical examination, mammography, and ultrasonography for breast cancer screening among Chinese women: follow-up study. Curr Oncol. 2012;19:eS22-30.
Honjo S, Ando J, Tsukioka T, Morikubo H, Ichimura M, Sunagawa M, et al. Relative and combined performance of mammography and ultrasonography for breast cancer screening in the general population: a pilot study in Tochigi Prefecture. Japan Jpn J Clin Oncol. 2007;37:715–20.
Guindalini RSC, Zheng Y, Abe H, Whitaker K, Yoshimatsu TF, Walsh T, et al. Intensive surveillance with biannual dynamic contrast-enhanced magnetic resonance imaging downstages breast cancer in BRCA1 mutation carriers. Clin Cancer Res. 2019;25:1786–94.
Riedl CC, Luft N, Bernhart C, Weber M, Bernathova M, Tea MK, et al. Triple-modality screening trial for familial breast cancer underlines the importance of magnetic resonance imaging and questions the role of mammography and ultrasound regardless of patient mutation status, age, and breast density. J Clin Oncol. 2015;33:1128–35.
Warner E, Plewes DB, Hill KA, Causer PA, Zubovits JT, Jong RA, et al. Surveillance of BRCA1 and BRCA2 mutation carriers with magnetic resonance imaging, ultrasound, mammography, and clinical breast examination. JAMA. 2004;292:1317–25.
Bosse K, Graeser M, Goßmann A, Hackenbroch M, Schmutzler RK, Rhiem K. Supplemental screening ultrasound increases cancer detection yield in BRCA1 and BRCA2 mutation carriers. Arch Gynecol Obstet. 2014;289:663–70.
Kuhl CK, Schrading S, Leutner CC, Morakkabati-Spitz N, Wardelmann E, Fimmers R, et al. Mammography, breast ultrasound, and magnetic resonance imaging for surveillance of women at high familial risk for breast cancer. J Clin Oncol. 2005;23:8469–76.
Kriege M, Brekelmans CT, Obdeijn IM, Boetes C, Zonderland HM, Muller SH, et al. Factors affecting sensitivity and specificity of screening mammography and MRI in women with an inherited risk for breast cancer. Breast Cancer Res Treat. 2006;100:109–19.
Passaperuma K, Warner E, Causer PA, Hill KA, Messner S, Wong JW, et al. Long-term results of screening with magnetic resonance imaging in women with BRCA mutations. Br J Cancer. 2012;107:24–30.
Rijnsburger AJ, Obdeijn IM, Kaas R, Tilanus-Linthorst MM, Boetes C, Loo CE, et al. BRCA1-associated breast cancers present differently from BRCA2-associated and familial cases:long-term follow-up of the Dutch MRISC Screening Study. J Clin Oncol. 2010;28:5265–73.
Bick U, Engel C, Krug B, Heindel W, Fallenberg EM, Rhiem K, German Consortium for Hereditary Breast and Ovarian Cancer (GC-HBOC), et al. High-risk breast cancer surveillance with MRI:10-year experience from the German consortium for hereditary breast and ovarian cancer. Breast Cancer Res Treat. 2019;175:217–28.
Cortesi L, Canossi B, Battista R, Pecchi A, Drago A, Dal Molin C, et al. Breast ultrasonography(BU)in the screening protocol for women at hereditary-familial risk of breast cancer: has the time come to rethink the role of BU according to different risk categories? Int J Cancer. 2019;144:1001–9.
Hagen AI, Kvistad KA, Maehle L, Holmen MM, Aase H, Styr B, et al. Sensitivity of MRI versus conventional screening in the diagnosis of BRCA-associated breast cancer in a national prospective series. Breast. 2007;16:367–74.
Evans DG, Kesavan N, Lim Y, Gadde S, Hurley E, Massat NJ, MARIBS Group, Howell A, Duffy SW, et al. MRI breast screening in high-risk women: cancer detection and survival analysis. Breast Cancer Res Treat. 2014;145:663–72.
Chéreau E, Uzan C, Balleyguier C, Chevalier J, de Paillerets BB, Caron O, et al. Characteristics, treatment, and outcome of breast cancers diagnosed in BRCA1 and BRCA2 gene mutation carriers in intensive screening programs including magnetic resonance imaging. Clin Breast Cancer. 2010;10:113–8.
Evans DG, Harkness EF, Howell A, Wilson M, Hurley E, Holmen MM, et al. Intensive breast screening in BRCA2 mutation carriers is associated with reduced breast cancer specific and all-cause mortality. Hered Cancer Clin Pract. 2016;14:8.
Giannakeas V, Lewinski J, Gronwald J, Moller P, Armel S, Lynch HT, et al. Mammography screening and the risk of breast cancer in BRCA1 and BRCA2 mutation carriers: a prospective study. Breast Cancer Res Treat. 2014;147:113–8.
Narod SA, Lubinski J, Ghadirian P, Lynch HT, Moller P, Foulkes WD, Hereditary Breast Cancer Clinical Study Group, et al. Screening mammography and risk of breast cancer in BRCA1 and BRCA2 mutation carriers: a case-control study. Lancet Oncol. 2006;7:402–6.
Pijpe A, Andrieu N, Easton DF, Kesminiene A, Cardis E, Noguès C, GENEPSO; EMBRACE; HEBON, et al. Exposure to diagnostic radiation and risk of breast cancer among carriers of BRCA1/2 mutations:retrospective cohort study (GENE-RAD-RISK). BMJ. 2012;345:e5660.
Phi XA, Greuter MJW, Obdeijn IM, Oosterwijk JC, Feenstra TL, Houssami N, et al. Should women with a BRCA1/2 mutation aged 60 and older be offered intensified breast cancer screening? A Cost-Eff Anal Breast. 2019;45:82–8.
Petelin L, Trainer AH, Mitchell G, Liew D, James PA. Cost-effectiveness and comparative effectiveness of cancer risk management strategies in BRCA1/2 mutation carriers: a systematic review. Genet Med. 2018;20:1145–56.
Spiegel TN, Esplen MJ, Hill KA, Wong J, Causer PA, Warner E. Psychological impact of recall on women with BRCA mutations undergoing MRI surveillance. Breast. 2011;20:424–30.
Rijnsburger AJ, Essink-Bot ML, van Dooren S, Borsboom GJ, Seynaeve C, Bartels CC, et al. Impact of screening for breast cancer in high-risk women on health-related quality of life. Br J Cancer. 2004;91:69–76.
Essink-Bot ML, Rijnsburger AJ, van Dooren S, de Koning HJ, Seynaeve C. Women’s acceptance of MRI in breast cancer surveillance because of a familial or genetic predisposition. Breast. 2006;15:673–6.
O’Neill SM, Rubinstein WS, Sener SF, Weissman SM, Newlin AC, West DK, et al. Psychological impact of recall in high-risk breast MRI screening. Breast Cancer Res Treat. 2009;115:365–71.
Chiarelli AM, Blackmore KM, Muradali D, Done SJ, Majpruz V, Weerasinghe A, et al. Performance measures of magnetic resonance imaging plus mammography in the high risk ontario breast screening program. J Natl Cancer Inst. 2020;112:136–44.
Sardanelli F, Cozzi A, Trimboli RM, Schiaffino S. Gadolinium retention and breast MRI screening:more harm than good? AJR Am J Roentgenol. 2020;214:324–7.
Gilbert FJ, Tucker L, Gillan MG, Willsher P, Cooke J, Duncan KA, et al. The TOMMY trial: a comparison of TOMosynthesis with digital MammographY in the UK NHS breast screening programme: a multicentre retrospective reading study comparing the diagnostic performance of digital breast tomosynthesis and digital mammography with digital mammography alone. Health Technol Assess. 2015;19(i–xxv):1–136.
Waldherr C, Cerny P, Altermatt HJ, Berclaz G, Ciriolo M, Buser K, et al. Value of one-view breast tomosynthesis versus two-view mammography in diagnostic workup of women with clinical signs and symptoms and in women recalled from screening. AJR Am J Roentgenol. 2013;200:226–31.
Tagliafico A, Mariscotti G, Durando M, Stevanin C, Tagliafico G, Martino L, et al. Characterisation of microcalcification clusters on 2D digital mammography(FFDM)and digital breast tomosynthesis (DBT):does DBT underestimate microcalcification clusters? Results of a multicentre study. Eur Radiol. 2015;25:9–14.
Mall S, Noakes J, Kossoff M, Lee W, McKessar M, Goy A, et al. Can digital breast tomosynthesis perform better than standard digital mammography work-up in breast cancer assessment clinic? Eur Radiol. 2018;28:5182–94.
You C, Zhang Y, Gu Y, Xiao Q, Liu G, Shen X, et al. Comparison of the diagnostic performance of synthesized two-dimensional mammography and full-field digital mammography alone or in combination with digital breast tomosynthesis. Breast Cancer. 2020;27:47–53.
Bahl M, Mercaldo S, Vijapura CA, McCarthy AM, Lehman CD. Comparison of performance metrics with digital 2D versus tomosynthesis mammography in the diagnostic setting. Eur Radiol. 2019;29:477–84.
Krammer J, Stepniewski K, Kaiser CG, Brade J, Riffel P, Schoenberg SO, et al. Value of additional digital breast tomosynthesis for preoperative staging of breast cancer in dense breasts. Anticancer Res. 2017;37:5255–61.
Chan HP, Helvie MA, Hadjiiski L, Jeffries DO, Klein KA, Neal CH, et al. Characterization of breast masses in digital breast tomosynthesis and digital mammograms: an observer performance study. Acad Radiol. 2017;24:1372–9.
Bian T, Lin Q, Cui C, Li L, Qi C, Fei J, et al. Digital breast tomosynthesis:a new diagnostic method for mass-like lesions in dense breasts. Breast J. 2016;22:535–40.
Bansal GJ, Young P. Digital breast tomosynthesis within a symptomatic “one-stop breast clinic” for characterization of subtle findings. Br J Radiol. 2015;88:20140855.
Clauser P, Nagl G, Helbich TH, Pinker-Domenig K, Weber M, Kapetas P, et al. Diagnostic performance of digital breast tomosynthesis with a wide scan angle compared to full-field digital mammography for the detection and characterization of microcalcifications. Eur J Radiol. 2016;85:2161–8.
Paulis LE, Lobbes MB, Lalji UC, Gelissen N, Bouwman RW, Wildberger JE, et al. Radiation exposure of digital breast tomosynthesis using an antiscatter grid compared with full-field digital mammography. Invest Radiol. 2015;50:679–85.
Choi Y, Woo OH, Shin HS, Cho KR, Seo BK, Choi GY. Quantitative analysis of radiation dosage and image quality between digital breast tomosynthesis (DBT) with two-dimensional synthetic mammography and full-field digital mammography (FFDM). Clin Imaging. 2019;55:12–7.
Kang HJ, Chang JM, Lee J, Song SE, Shin SU, Kim WH, et al. Replacing single-view mediolateral oblique(MLO)digital mammography(DM)with synthesized mammography(SM)with digital breast tomosynthesis(DBT)images: comparison of the diagnostic performance and radiation dose with two-view DM with or without MLO-DBT. Eur J Radiol. 2016;85:2042–8.
Japan Network for Research and Information on Medical Exposure; J-RIME: Japanese Diagnostic Reference Levels (DRLs) 2020. http://www.radher.jp/J-RIME/report/JapanDRL2020_jp.pdf. Accessed 23 Sep 2023
Ng WL, Rahmat K, Fadzli F, Rozalli FI, Mohd-Shah MN, Chandran PA, et al. Shearwave elastography increases diagnostic accuracy in characterization of breast lesions. Medicine (Baltimore). 2016;95: e3146.
Watanabe T, Yamaguchi T, Okuno T, Konno S, Takaki R, Sato M, et al. Utility of B-mode, color doppler and elastography in the diagnosis of breast cancer: results of the CD-CONFIRM multicenter study of 1351 breast solid masses. Ultrasound Med Biol. 2021;47:3111–21.
Han J, Li F, Peng C, Huang Y, Lin Q, Liu Y, et al. Reducing unnecessary biopsy of breast lesions:preliminary results with combination of strain and shear-wave elastography. Ultrasound Med Biol. 2019;45:2317–27.
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 trial. Eur J Cancer. 2022;161:1–9.
Berg WA, Cosgrove DO, Doré CJ, Schäfer FK, Svensson WE, Hooley RJ, BE1 Investigators, et al. Shear-wave elastography improves the specificity of breast US: the BE1 multinational study of 939 masses. Radiology. 2012;262:435–49.
Chang JM, Won JK, Lee KB, Park IA, Yi A, Moon WK. Comparison of shear-wave and strain ultrasound elastography in the differentiation of benign and malignant breast lesions. AJR Am J Roentgenol. 2013;201:W347–56.
Bai M, Zhang HP, Xing JF, Shi QS, Gu JY, Li F, et al. Acoustic radiation force impulse technology in the differential diagnosis of solid breast masses with different sizes: which features are most efficient? Biomed Res Int. 2015;2015: 410560.
Huang Y, Li F, Han J, Peng C, Li Q, Cao L, et al. Shear wave elastography of breast lesions:quantitative analysis of elastic heterogeneity improves diagnostic performance. Ultrasound Med Biol. 2019;45:1909–17.
Wang ZL, Li JL, Li M, Huang Y, Wan WB, Tang J. Study of quantitative elastography with supersonic shear imaging in the diagnosis of breast tumours. Radiol Med. 2013;118:583–90.
Redling K, Schwab F, Siebert M, Schötzau A, Zanetti-Dällenbach R. Elastography complements ultrasound as principle modality in breast lesion assessment. Gynecol Obstet Invest. 2017;82:119–24.
Moon JH, Koh SH, Park SY, Hwang JY, Woo JY. Comparison of the SRmax, SRave, and color map of strain-elastography in differentiating malignant from benign breast lesions. Acta Radiol. 2019;60:28–34.
Yi A, Cho N, Chang JM, Koo HR, La Yun B, Moon WK. Sonoelastography for 1,786 non-palpable breast masses: diagnostic value in the decision to biopsy. Eur Radiol. 2012;22:1033–40.
Zhou J, Zhan W, Dong Y, Yang Z, Zhou C. Stiffness of the surrounding tissue of breast lesions evaluated by ultrasound elastography. Eur Radiol. 2014;24:1659–67.
Zheng X, Huang Y, Wang Y, Liu Y, Li F, Han J, et al. Combination of different types of elastography in downgrading ultrasound breast imaging-reporting and data system category 4a breast lesions. Breast Cancer Res Treat. 2019;174:423–32.
Yoon JH, Song MK, Kim EK. Semi-quantitative strain ratio in the differential diagnosis of breast masses: measurements using one region-of-interest. Ultrasound Med Biol. 2016;42(8):1800–6.
Li XL, Ren WW, Fu HJ, He YP, Wang Q, Sun LP, et al. Shear wave speed imaging of breast lesions: speed within the lesion, fat-to-lesion speed ratio, or gland-to-lesion speed ratio? Clin Hemorheol Microcirc. 2017;67:81–90.
Wang Q, Li XL, He YP, Alizad A, Chen S, Zhao CK, et al. Three-dimensional shear wave elastography for differentiation of breast lesions: an initial study with quantitative analysis using three orthogonal planes. Clin Hemorheol Microcirc. 2019;71:311–24.
Li DD, Xu HX, Guo LH, Bo XW, Li XL, Wu R, et al. Combination of two-dimensional shear wave elastography with ultrasound breast imaging reporting and data system in the diagnosis of breast lesions:a new method to increase the diagnostic performance. Eur Radiol. 2016;26:3290–300.
Stachs A, Hartmann S, Stubert J, Dieterich M, Martin A, Kundt G, et al. Differentiating between malignant and benign breast masses:factors limiting sonoelastographic strain ratio. Ultraschall Med. 2013;34:131–6.
Xiao Y, Yu Y, Niu L, Qian M, Deng Z, Qiu W, et al. Quantitative evaluation of peripheral tissue elasticity for ultrasound-detected breast lesions. Clin Radiol. 2016;71:896–904.
Cheng M, Tong W, Luo J, Li M, Liang J, Pan F, et al. Value of contrast-enhanced ultrasound in the diagnosis of breast US-BI-RADS 3 and 4 lesions with calcifications. Clin Radiol. 2020;75:934–41.
Pan J, Tong W, Luo J, Liang J, Pan F, Zheng Y, et al. Does contrast-enhanced ultrasound (CEUS) play a better role in diagnosis of breast lesions with calcification? A comparison with MRI. Br J Radiol. 2020;93:20200195.
Shao SH, Li CX, Yao MH, Li G, Li X, Wu R. Incorporation of contrast-enhanced ultrasound in the differential diagnosis for breast lesions with inconsistent results on mammography and conventional ultrasound. Clin Hemorheol Microcirc. 2020;74:463–73.
Miyamoto Y, Ito T, Takada E, Omoto K, Hirai T, Moriyasu F. Efficacy of sonazoid (perflubutane) for contrast-enhanced ultrasound in the differentiation of focal breast lesions:phase 3 multicenter clinical trial. AJR Am J Roentgenol. 2014;202:W400–7.
Du J, Wang L, Wan CF, Hua J, Fang H, Chen J, et al. Differentiating benign from malignant solid breast lesions: combined utility of conventional ultrasound and contrast-enhanced ultrasound in comparison with magnetic resonance imaging. Eur J Radiol. 2012;81:3890–9.
Zhao H, Xu R, Ouyang Q, Chen L, Dong B, Huihua Y. Contrast-enhanced ultrasound is helpful in the differentiation of malignant and benign breast lesions. Eur J Radiol. 2010;73:288–93.
Liu H, Jiang YX, Liu JB, Zhu QL, Sun Q. Evaluation of breast lesions with contrast-enhanced ultrasound using the microvascular imaging technique: initial observations. Breast. 2008;17:532–9.
Ricci P, Cantisani V, Ballesio L, Pagliara E, Sallusti E, Drudi FM, et al. Benign and malignant breast lesions:efficacy of real time contrast-enhanced ultrasound vs. magnetic resonance imaging. Ultraschall Med. 2007;28:57–62.
Zhang XL, Guan J, Li MZ, Liu MJ, Guo Y, Zheng YL, et al. Adjunctive targeted contrast-enhanced ultrasonography for the work-up of breast imaging reporting and data system category 3 and 4 lesions. J Med Imaging Radiat Oncol. 2016;60:485–91.
Xiao X, Dong L, Jiang Q, Guan X, Wu H, Luo B. Incorporating contrast-enhanced ultrasound into the BI-RADS scoring system improves accuracy in breast tumor diagnosis: a preliminary study in China. Ultrasound Med Biol. 2016;42:2630–8.
Lee SE, Lee JH, Han K, Kim EK, Kim MJ, Moon HJ, et al. BI-RADS category 3, 4, and 5 lesions identified at preoperative breast MRI in patients with breast cancer: implications for management. Eur Radiol. 2020;30:2773–81.
Lim HI, Choi JH, Yang JH, Han BK, Lee JE, Lee SK, et al. Does pre-operative breast magnetic resonance imaging in addition to mammography and breast ultrasonography change the operative management of breast carcinoma? Breast Cancer Res Treat. 2010;119:163–7.
Behrendt CE, Tumyan L, Gonser L, Shaw SL, Vora L, Paz IB, et al. Evaluation of expert criteria for preoperative magnetic resonance imaging of newly diagnosed breast cancer. Breast. 2014;23:341–5.
Cheung JY, Moon JH. Follow-up design of unexpected enhancing lesions on preoperative MRI of breast cancer patients. Diagn Interv Radiol. 2015;21:16–21.
Gutierrez RL, DeMartini WB, Silbergeld JJ, Eby PR, Peacock S, Javid SH, et al. High cancer yield and positive predictive value:outcomes at a center routinely using preoperative breast MRI for staging. AJR Am J Roentgenol. 2011;196:W93–9.
Paudel N, Bethke KP, Wang LC, Strauss JB, Hayes JP, Donnelly ED. Impact of breast MRI in women eligible for breast conservation surgery and intra-operative radiation therapy. Surg Oncol. 2018;27:95–9.
Fan XC, Nemoto T, Blatto K, Mangiafesto E, Sundberg J, Chen A, et al. Impact of presurgical breast magnetic resonance imaging (MRI) on surgical planning- a retrospective analysis from a private radiology group. Breast J. 2013;19:134–41.
Gurdal SO, Ozcinar B, Kayahan M, Igci A, Tunaci M, Ozmen V, et al. Incremental value of magnetic resonance imaging for breast surgery planning. Surg Today. 2013;43:55–61.
Lamb LR, Oseni TO, Lehman CD, Bahl M. Pre-operative MRI in patients with ductal carcinoma in situ: is MRI useful for identifying additional disease? Eur J Radiol. 2020;129: 109130.
Saha S, Freyvogel M, Johnston G, Lawrence L, Conlin C, Hicks R, et al. The prognostic value of additional malignant lesions detected by magnetic resonance imaging versus mammography. Am J Surg. 2015;209:398–402.
Calvo-Plaza I, Ugidos L, Miró C, Quevedo P, Parras M, Márquez C, et al. Retrospective study assessing the role of MRI in the diagnostic procedures for early breast carcinoma: a correlation of new foci in the MRI with tumor pathological features. Clin Transl Oncol. 2013;15:205–10.
Lee SH, Kim SM, Jang M, Yun BL, Kang E, Kim SW, et al. Role of second-look ultrasound examinations for MR-detected lesions in patients with breast cancer. Ultraschall Med. 2015;36:140–8.
He H, Plaxco JS, Wei W, Huo L, Candelaria RP, Kuerer HM, et al. Incremental cancer detection using breast ultrasonography versus breast magnetic resonance imaging in the evaluation of newly diagnosed breast cancer patients. Br J Radiol. 2016;89:20160401.
Hill MV, Beeman JL, Jhala K, Holubar SD, Rosenkranz KM, Barth RJ Jr. Relationship of breast MRI to recurrence rates in patients undergoing breast-conservation treatment. Breast Cancer Res Treat. 2017;163:615–22.
Kim TH, Kang DK, Jung YS, Kim KS, Yim H. Contralateral enhancing lesions on magnetic resonance imaging in patients with breast cancer: role of second-look sonography and imaging findings of synchronous contralateral cancer. J Ultrasound Med. 2012;31:903–13.
DeMartini WB, Hanna L, Gatsonis C, Mahoney MC, Lehman CD. Evaluation of tissue sampling methods used for MRI-detected contralateral breast lesions in the American college of radiology imaging network 6667 trial. AJR Am J Roentgenol. 2012;199:W386–91.
Bernard JR Jr, Vallow LA, DePeri ER, McNeil RB, Feigel DG, Amar S, et al. In newly diagnosed breast cancer, screening MRI of the contralateral breast detects mammographically occult cancer, even in elderly women:the mayo clinic in Florida experience. Breast J. 2010;16:118–26.
Mahoney MC, Gatsonis C, Hanna L, DeMartini WB, Lehman C. Positive predictive value of BI-RADS MR imaging. Radiology. 2012;264:51–8.
Susnik B, Schneider L, Swenson KK, Krueger J, Braatz C, Lillemoe T, et al. Predictive value of breast magnetic resonance imaging in detecting mammographically occult contralateral breast cancer: Can we target women more likely to have contralateral breast cancer? J Surg Oncol. 2018;118:221–7.
Kim JY, Cho N, Koo HR, Yi A, Kim WH, Lee SH, et al. Unilateral breast cancer:screening of contralateral breast by using preoperative MR imaging reduces incidence of metachronous cancer. Radiology. 2013;267:57–66.
Turnbull L, Brown S, Harvey I, Olivier C, Drew P, Napp V, et al. Comparative effectiveness of MRI in breast cancer (COMICE) trial: a randomised controlled trial. Lancet. 2010;375:563–71.
Spick C, Baltzer PA. Diagnostic utility of second-look US for breast lesions identified at MR imaging: systematic review and meta-analysis. Radiology. 2014;273:401–9.
Uematsu T, Takahashi K, Nishimura S, Watanabe J, Yamasaki S, Sugino T, et al. Real-time virtual sonography examination and biopsy for suspicious breast lesions identified on MRI alone. Eur Radiol. 2016;26:1064–72.
Gunalp B, Ince S, Karacalioglu AO, Ayan A, Emer O, Alagoz E. Clinical impact of(18)F-FDG PET/CT on initial staging and therapy planning for breast cancer. Exp Ther Med. 2012;4:693–8.
Riedl CC, Slobod E, Jochelson M, Morrow M, Goldman DA, Gonen M, et al. Retrospective analysis of 18F-FDG PET/CT for staging asymptomatic breast cancer patients younger than 40 years. J Nucl Med. 2014;55:1578–83.
Nursal GN, Nursal TZ, Aytac HO, Hasbay B, Torun N, Reyhan M, et al. Is PET/CT necessary in the management of early breast cancer? Clin Nucl Med. 2016;41:362–5.
Ulaner GA, Castillo R, Goldman DA, Wills J, Riedl CC, Pinker-Domenig K, et al. (18)F-FDG-PET/CT for systemic staging of newly diagnosed triple-negative breast cancer. Eur J Nucl Med Mol Imaging. 2016;43:1937–44.
Lebon V, Alberini JL, Pierga JY, Diéras V, Jehanno N, Wartski M. Rate of distant metastases on 18F-FDG PET/CT at Initial staging of breast cancer: comparison of women younger and older than 40 years. J Nucl Med. 2017;58:252–7.
Alongi P, Evangelista L, Caobelli F, Spallino M, Gianolli L, Midiri M, et al. Diagnostic and prognostic value of 18F-FDG PET/CT in recurrent germinal tumor carcinoma. Eur J Nucl Med Mol Imaging. 2018;45:85–94.
Singh S, Raghavan B, Geethapriya S, Sathyasree VV, Govindaraj J, Padmanabhan G, et al. PET-CT upstaging of unilateral operable breast cancer and its correlation with molecular subtypes. Indian J Radiol Imaging. 2020;30:319–26.
Gangadaran SGD. Rational use of imaging to stage breast cancer: evidences for a selective approach. Indian J Med Paediatr Oncol. 2017;38:427–9.
Han S, Choi JY. Impact of 18F-FDG PET, PET/CT, and PET/MRI on staging and management as an initial staging modality in breast cancer: a systematic review and meta-analysis. Clin Nucl Med. 2021;46:271–82.
Brennan ME, Houssami N. Evaluation of the evidence on staging imaging for detection of asymptomatic distant metastases in newly diagnosed breast cancer. Breast. 2012;21:112–23.
National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology. Breast Cancer. Version 8.2021. https://www.nccn.org/. Accessed 23 Sep 2023
Acknowledgements
The JBCS Clinical Practice Guidelines Breast Cancer Screening and Diagnosis Subcommittee would like to thank all Clinical Practice Guidelines Committee members, experts who worked with the committee, the expert panel including representative breast cancer survivors who provided rating statements, and the Evaluation Committee. The authors would also like to extend our heartfelt gratitude to Takayoshi Uematsu, Yoshihito Goto, Akihiro Sakurai, and Takeo Nakayama for their invaluable guidance and support as external committee members. Furthermore, the authors express our profound gratitude for the significant contributions made by Mami Iima, Shotaro Inoue, Rie Ohta, Shorato Kanao, Takeshi Kamiya, Reina Sakaguchi, Sayaka Sakurai, Nozomi Satani, Akiko Satoh, Akie Tanaka, Kaori Tane, Junko Tsuchida, Masae Torii, Roka Namoto Matsubayashi, Miki Hasegawa, Maya Honda, Akiko Mizuto, Mio Mori, and Sachiko Yuen, as members of the Systematic Review Committee.
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Kubota, K., Nakashima, K., Nakashima, K. et al. The Japanese breast cancer society clinical practice guidelines for breast cancer screening and diagnosis, 2022 edition. Breast Cancer 31, 157–164 (2024). https://doi.org/10.1007/s12282-023-01521-x
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DOI: https://doi.org/10.1007/s12282-023-01521-x