Screening
For reference: Categorization in the Japanese mammography guidelines and those of the Breast Imaging Reporting and Data System
The Breast Imaging Reporting and Data System (BI-RADS) developed by the American College of Radiology (ACR) as a standardized quality assessment tool for drawing up imaging findings and reports is universally recognized. In Japan, the “Guidelines for Mammography” complied on the basis of the 2nd edition of BI-RADS were published in 1999. According to those guidelines, mammogram findings are finally assessed for malignancy using 5 grading categories, i.e., category 1 or 2 requiring no additional detailed examination and categories 3–5 warranting further detailed examinations.
The 4th edition of BI-RADS [1], on the other hand, is designed to provide a general flow of the breast cancer screening process as follows: lesions presenting screening mammographic findings based on which malignancy cannot be negated are classified into category 0 and subjected to detailed examination performed later, i.e., additional mammography and ultrasonography at the initial screening site; if no malignant findings are noted in the detailed examination, the lesion is classified into category 1 or 2; if findings are probably benign (malignancy level: ≤2 %) requiring a follow-up at 6 months later, the lesion is classified into category 3; or if a higher malignancy level is suspected, the lesion is classified into category 4 or 5, warranting histopathological examination.
It is often the case in Japan at present that screening and the subsequent medical workup are conducted at different facilities, so that radiologists and other physicians at the latter sites may experience some difficulty in referring to screening mammograms. Eventually, it is considered necessary for precise control of accurate screening in Japan to classify lesions presenting findings that correspond to BI-RADS category 0 into categories 3–5. It is thus of urgent necessity for us to seek efficient interlacing of the current Japanese classification scheme with the international standard BI-RADS classification system.
CQ1. Is breast cancer screening by clinical breast examination alone recommendable?
Recommendation
Screening for breast cancer by clinical breast examination alone is not recommended (Grade D).
Japan is the only country in which breast cancer screening solely based on clinical breast examination has been extensively performed. The odds ratio of a group of subjects receiving a screening within 1 year from the day on which the subject was diagnosed as having breast cancer is 0.93 (95 % CI 0.48–1.79) and there was no mortality rate-reducing effect according to a case–control study in Japan [2].
The outcome of breast cancer is relatively favorable even in a patient who has begun treatment after subjectively noticing a palpable mass, and screening by clinical breast examination alone is thus considered to be of some definite significance including an enlightening effect, though its sensitivity is low, in a stage of social maturation which has not progressed as far as it could; however, it will not surpass imaging-based screening in terms of assessment effectiveness.
CQ2. Is screening mammography recommended for subjects aged 50 years or older?
Recommendation
Mammographic screening for breast cancer in women aged 50 years or older is strongly recommended (Grade A).
Mammographic screening in women 50 years of age or older is widely conducted in Europe and the United States, and, in Japan, the Ministry of Health, Labour and Welfare issued a circular notice to the effect that mammographic screening would be a standard method of breast cancer screening in subjects from the age of 50 or older, effective from 2000 on. In recent years, however, over-diagnosis has been and is subject to lively controversy as a disadvantage of screening by mammography [3]. The definition thereof consists not in false positive on screening but in discovery and treatment of breast cancer that has no impact on the vital prognosis even without administering treatment. Physicians should be cognizant of the presence of over-diagnosis in conducting breast cancer screening and provide relevant information to subjects undergoing the screening.
CQ3 Is screening mammography recommended to subjects in their forties?
Recommendation
Mammographic screening for breast cancer in women in their forties is recommended (Grade B).
In the U.S. Preventive Services Task Force (USPSTF) 2009 recommendation statement, screening mammography in individuals of ages between 39 and 49 years is placed as a Grade C recommendation [4]. Screening mammography is considered to have relatively high usefulness in such a subpopulation because the breast cancer incidence rate peaks in individuals in the latter half of their forties in Japan. Nationwide surveys are yet to be made, but it is infeasible under the present circumstances to directly apply in Japan those interpretations based on Europe/US data as they are; therefore, it is considered appropriate to continue the use of current recommendations for the time being.
CQ4. Is breast cancer screening mammography with concomitant ultrasonography recommended?
Recommendation
There are not sufficient grounds for recommending breast cancer screening by ultrasonography as yet (Grade C1).
Mammography is an effective method of breast cancer screening with a proven mortality rate-reducing effect, but it cannot be negated that the effectiveness of mammography is relatively low in cases of dense breasts and in young women. At present, however, ultrasonography lacks rational grounds for its effectiveness and is not recommended as a tool for population-based (organized) screening [5–7]. Its application as an ancillary optional screening tool for mammographic screening of dense breast cases and young women is expected. In such instances, nevertheless, subjects to be examined should be given an explanation about disadvantages such as the potential need for an expensive complete medical workup.
CQ5. Is digital mammography equally as recommendable as screen film mammography in screening for breast cancer?
Recommendation
In the screening for breast cancer, digital mammography is equally as strongly recommendable as screen film mammography (Grade A).
Currently, the use of the digital mammography is increasing rapidly. The Digital Mammographic Imaging Screening Trial (DMIST) was designed to measure clinically important differences in diagnostic accuracy between digital and film mammography [8]. A total of 49,528 asymptomatic women presenting for screening mammography in the United States and Canada underwent both digital and film mammography. In the entire population, the diagnostic accuracy of digital and film mammography was similar (difference between methods in the area under the ROC curve, 0.03; 95 % confidence interval, −0.02 to 0.08; P = 0.18). However, the accuracy of digital mammography was significantly higher than that of film mammography among women under the age of 50 years (difference in the area under the curve, 0.15; 95 % confidence interval, 0.05–0.25; P = 0.002), women with heterogeneously dense or extremely dense breasts on mammography (difference, 0.11; 95 % confidence interval, 0.04–0.18; P = 0.003), and premenopausal or perimenopausal women (difference, 0.15; 95 % confidence interval, 0.05–0.24; P = 0.002).
CQ7. Is FDG-PET recommended for breast cancer screening?
Recommendation
FDG-PET is not recommendable for breast cancer screening (Grade D).
There has been no evidence shown to enable a definitive judgment as to whether screening with FDG-PET has any breast cancer mortality rate-reducing effect or not. Furthermore, the breast cancer detection rate by screening with FDG-PET is lower than that by the current breast cancer screening with mammography combined with clinical breast examination [10]. Further, a FDG-PET is extremely expensive, and this procedure has the disadvantage of entailing systemic exposure. Therefore, FDG-PET is not useful as a screening method for breast cancer.
Diagnosis
CQ1. Is diagnostic mammography recommended in young women?
Recommendation
Diagnostic mammography performed with meticulous care may be considered, although there are as yet no sufficient scientific grounds for application of diagnostic mammography in young women (Grade C1).
Application of this procedure in the clinical practice setting should be judged taking into consideration the lower breast cancer incidence rate for women under 30 or 35 years of age as compared to women in their forties or fifties, and also with an understanding of the merits and drawbacks of this diagnostic modakity [11, 12].
CQ2. Is ultrasonography recommended as a tool for differential assessment of benign/malignant mass lesion of the breast?
Recommendation
The performance of ultrasonography is recommended for diagnostic differentiation between benign and malignant mass lesions of the breast (Grade B).
The BI-RADS for Ultrasound [13] provides information to enable standardization of terms of imaging findings and homogeneous diagnosis, and it has been reported that the true positive ratio is 71.3 %, the positive predictive value 67.8 %, and negative predictive value 92.3 % in the diagnostic differentiation between benign and malignant solid masses of the breast [14, 15]. However, although the diagnostic validity is high for masses greater than a certain size, there are noticeable differences in interobserver findings as to small lesions where the accuracy of diagnosis is in no way high [16, 17]. Further improvement of accuracy through the further technical development of instrument/apparatus with microlesions in view and introduction of new applications is expected.
CQ3. Is ultrasonography recommended as a means for breast cancer detection in the clinical practice setting?
Recommendation
Ultrasonography is recommended for patients in whom mammography and palpation have failed to detect abnormalities (Grade B)
Relatively not much importance has been attached to ultrasonographic diagnosis in Europe and the United States, both of which have a long history of mammography; however, ultrasonography is gradually being seen in a new light in recent years with the improvement of ultrasonographic diagnostic apparatus and diagnostic techniques.
It has been reported that a large-scale multicenter prospective study using ultrasonography and mammography for breast cancer screening (Study ACRIN6666) demonstrated that discoveries of breast cancer increased by 1.1–7.2 persons per 1,000 and the false positive rate also increased as a result of concomitant application of ultrasonography [18]. In Japan as well, concomitant application of ultrasonography in breast cancer screening is currently being investigated and a large-scale clinical study [19] is in progress. The study is probably the largest randomized clinical study in the world, with more than 75,000 subjects enrolled besides introduction of the accuracy control of ultrasonography. Results of the study will strongly influence the future trend of breast ultrasonography.
CQ4. Is the application of ultrasonography to the clinical assessment of mass diameter in breast cancer recommended?
Recommendation
Ultrasonography is more recommended than palpation, mammography, and MRI in assessing the clinical mass diameter of breast cancer (Grade B).
Precise measurement of breast mass diameter is important for preoperative diagnostic staging of the disease, decision on a surgical resection procedure, and selection of an appropriate postoperative adjunctive therapy. Ultrasonography is considered to be more useful in determining the mass diameter as compared to palpation and mammography. In a study conducted including MRI, the coefficient of correlation with pathological mass diameter was 0.98 for MRI, 0.45 for ultrasonography, and 0.46 for mammography [20]. However, ultrasonography is procedurally simple without entailing radiation exposure; thus is considered a routinely used tool appropriate for preoperative evaluation.
As regards tumors infiltrating adjacent tissues, nevertheless, problems such as whether the measurement should encompass marginal echogenic haloes around a mass or not, and how to measure the diameter of a mass that has deformed in consequence of treatment, are yet to be solved, so that the criteria for accuracy control of the measurement method need to be standardized.
CQ5. Is flow imaging in ultrasonography recommendable for diagnostic differentiation between benign and malignant mass lesions?
Recommendation
Flow imaging in ultrasonography performed with meticulous care may be considered although there is no sufficient scientific ground as yet for diagnostic differentiation between benign and malignant mass lesions (Grade C1).
Flow imaging (general term for tumor vascularity, Doppler, contrast enhanced ultrasonography, etc.) is installed as a standard device in virtually all breast ultrasonography systems but there are no established diagnostic criteria. Further, examination by flow imaging involves measurement errors due to performance and setting of the system parameters or variations in the operator’s technical skill that cannot be disregarded. Such errors are magnified particularly when studying microlesions. Necessary requirements remain, such as improvement of precision of the apparatus, standardization of the settings, and accuracy control of the examination technique [21].
CQ7. Are CT and MRI recommended in determining diagnosis and treatment policies for intra-breast lesions?
Recommendation
-
1.
MRI is recommended in determining diagnosis and treatment policies for intra-breast lesions (Grade B).
-
2.
CT is not recommended in determining diagnosis and treatment policies for intra-breast lesions (Grade D).
It is rather uncommon that MRI is performed in determining diagnosis and treatment policies for intra-breast lesions in the clinical practice setting where the indication for biopsy is determined according to categorization of respective examination procedures in the case of a lesion identified by mammography or ultrasonography and the lesion is subjected to imaging-guided biopsy. However, MRI obviously has higher diagnostic performance than mammography and ultrasonography and is considered useful in such cases where it is difficult to decide definitively on the indication for biopsy due to inconsistencies among clinical findings and mammographic and ultrasonographic findings or where it is difficult to perform imaging-guided biopsy by mammography or ultrasonography. In the EUSOBI guideline as well, evaluation of lesions of which diagnosis by mammography or ultrasonography is inconclusive constitutes an indication for MRI [30].
Meanwhile, there is no published study demonstrating superiority in diagnostic performance of CT to mammography and ultrasonography. The grounds, on which the verification of the usefulness of CT in determining the diagnosis and treatment policies for intra-breast lesions can be based, are, therefore, insufficient. Furthermore, CT has a major drawback in that any attempt to conduct a dynamic study for kinetic analysis of lesions will eventually lead to increased exposure to X-rays so that performance of CT for determining diagnosis and treatment policies for intra-breast lesions cannot be recommended.
CQ8. Are CT and MRI recommended for diagnosing the extent of breast cancer?
Recommendation
-
1.
MRI is recommended for diagnosing the extent of breast cancer (Grade B).
-
2.
CT may be more effective than conventional clinical findings, mammography, and ultrasonography in diagnosing the extent of breast cancer prior to breast-conserving surgery in patients in whom MRI cannot be performed (Grade C1).
It has been documented in many papers that the diagnostic validity of MRI breast cancer extent assessment is higher as compared to mammography and ultrasonography. In recent years, however, a report has appeared demonstrating no significant difference in the percentage of cases requiring reoperation (19 vs. 19 %) between a group of MRI-examined patients (n = 816) and a non-MRI-examined patient group (n = 807) [31]. It has been pointed out, nevertheless, that the percentage of cases requiring reoperation substantially varies among medical institutions [32] and that information gained by MRI scanning with the patient in the prone position may not be correctly reflected in breast-conserving surgery. Subsequently, an additional report has been published indicating the usefulness of preoperative MRI in a study that employed the percentage of cases requiring reoperation as an endpoint [33] as well as a report not indicating the usefulness of preoperative MRI [34], so further accumulation of pertinent data is anticipated.
There is no certain evidence at present to indicate that breast MRI scanning should be performed as a routine preoperative examination in cases of breast-conserving surgery. The usefulness of preoperative MRI as evaluated using the percentage of cases requiring reoperation as an endpoint is currently subject to worldwide controversy. However, it is unquestionably clear that MRI is superior to any other imaging examinations in respect of accuracy of diagnosis of the extent of breast cancer.
It is a noticeable characteristic feature of medical practice in Japan that contrast-enhanced CT has been frequently adopted in the evaluation of the extent of breast cancer [35]. However, it has been reported that CT and MRI are virtually comparable in terms of diagnostic specificity but the former is significantly lower in sensitivity and in accurate diagnosis rate [36, 37]. Contrast-enhanced CT may have potential usefulness in preoperatively diagnosing the extent of breast cancer in patients in whom MRI cannot be performed due to claustrophobia, implanted metal devices, or adverse reactions to contrast medium.
CQ9. Is MRI recommended for detecting multifocal breast cancer undetectable by mammography and ultrasonography?
Recommendation
MRI is recommended for detecting multifocal breast cancer which is undetectable by mammography and ultrasonography (Grade B).
The usefulness of MRI in detecting multifocal breast cancer that cannot be detected by mammography and ultrasonography has been recognized from early on in Europe and the United States. Therefore, stress has been placed on the need for MRI-guided biopsy from the first half of the 1990s, and the procedure is stated as an essential technique in the European and U.S. guidelines [30, 38]. A unicenter study with MRI-guided biopsy in Japan showed that the frequency with which breast cancer was detected was 33 % (34/102) [39]. Currently, measures to cope with lesions detectable only by MRI should be examined since MRI-guided biopsy is not included in the category of techniques acceptable for national health insurance reimbursement in this country.
CQ10. Are bone scintigraphy, liver ultrasonography, and FDG-PET recommended as preoperative examinations?
Recommendation
-
1.
Liver ultrasonography, bone scintigraphy, and FDG-PET are not recommended as preoperative examinations (staging) in patients with stage I or II initial primary breast cancer presenting with no symptoms or findings indicative of distant metastasis (Grade C2).
-
2.
Liver ultrasonography, bone scintigraphy, and FDG-PET performed with meticulous care as preoperative examinations (staging) may be considered in patients with stage I or II initial primary breast cancer presenting with symptoms and findings indicative of distant metastasis and in patients with stage III initial primary breast cancer, although there are no sufficient corroborative scientific grounds (Grade C1).
The usefulness of bone scintigraphy, liver ultrasonography, and FDG-PET as preoperative examinations (staging) of stage I to II initial primary breast cancer with low incidence of distant metastasis is insignificant. However, bone scintigraphy, liver ultrasonography, and FDG-PET (including PET/CT) may be considered in such patients who present with metastasis-related clinical manifestations such as localized bone pain or abdominal symptoms or who show blood biochemical test abnormalities such as elevation of alkaline phosphatase and hepatic dysfunction as well as in patients with stage III or more advanced breast cancer with a high risk of distant metastasis [40–42].
CQ11. Is imaging diagnosis recommended for evaluation of axillary lymph nodes?
Recommendation
-
1.
Ultrasonography performed with meticulous care may be considered although there are no sufficient scientific grounds for evaluation of the axillary lymph node (Grade C1).
-
2.
Application of CT or PET solely for the purpose of evaluating axillary lymph nodes is basically not recommended because scientific grounds for their application seem to be insufficient (Grade C2).
Sporadic reports have described the superior diagnostic sensitivity of axillary lymph node evaluation by means of ultrasonography, CT, or FDG-PET, and the accurate diagnosis rate with these modalities is higher as compared to palpation. All these procedures have relatively high image-diagnostic specificity and, therefore, are considered amply applicable in the clinical setting [43, 44]. Nevertheless, omitting sentinel node biopsies solely on account of negative findings in diagnostic imaging should be avoided, as well as the selection of axillary regional lymphadenectomy just because of positive findings in diagnostic imaging. There are no ample grounds for recommending the application of CT or FDG-PET, besides ultrasonography, for the sole purpose of axillary lymph node evaluation [45, 46].
CQ12. Is imaging diagnosis more useful than a clinical breast examination in interpreting therapeutic responses to neoadjuvant chemotherapy?
Recommendation
Evaluation by imaging diagnosis is more recommended than clinical breast examination in interpreting therapeutic responses to neoadjuvant chemotherapy. However, no conclusions have been reached yet as to the selection of the proper modality or modalities, and the proper evaluation protocol (Grade B).
Recognition of imaging diagnosis is emerging as a tool for early prediction of clinical responses to neoadjuvant chemotherapy and has obviously greater usefulness than a clinical breast examination [47]. However, the accuracy control of image-diagnosis instruments in evaluating neoadjuvant chemotherapy is still not sufficient. Studies are currently in progress regarding not merely dimensional but also morphologic changes in tumors, changes in image pattern, changes on diffusion-weighted imaging, and the like, so that no conclusions have been reached yet as to selection of the proper modality (or modalities) and appropriate evaluation protocol. Study of the results of further investigations will clarify the usefulness and techniques of imaging modalities, timing of image evaluation, and so on.
CQ13. Is FDG-PET recommended at least for detecting postoperative recurrence and metastasis of breast cancer in patients suspected to have some signs of recurrence?
Recommendation
FDG-PET is recommended for detecting postoperative local recurrence and metastasis in breast cancer patients with positive clinical test findings (Grade B).
FDG-PET is not recommended as a post-breast surgery routine examination. However, FDG-PET is commonly performed as a tool for identifying metastasis and determining treatment policies in patients suspected to have recurrence from physical findings, other imaging examinations, or tumor markers and in those with a proven local recurrence: FDG-PET is considered useful in such patient groups [48–50].
CQ14. Is biopsy recommended in cases of distant recurrence?
Recommendation
-
1.
Biopsy is recommended in the case of a lesion likely to be a distant recurrence lesion which cannot be concluded to be of breast cancer origin (Grade A).
-
2.
Biopsy performed with meticulous care may be considered, though lacking in sufficient scientific grounds as yet, in the case of a lesion likely to be a distant recurrence lesion which can be concluded to be of breast cancer origin where ER, PgR, and HER2 of the primary lesion are unknown or where relevant laboratory test data are not really reliable (Grade B).
Whilst biopsy should be considered in the case of a lesion which cannot be definitively identified as being a distant recurrence of a breast cancer lesion, treatment may be brought forward without conducting a biopsy if the lesion is conclusively a distant recurrence lesion and if immunohistochemical data concerning the primary lesion are reliable. However, biopsy of the distant recurrence lesion may have to be considered whenever feasible if ER, PgR, and HER2 data at the initial surgery are unknown or not considered reliable [51–54].
In conducting a biopsy, the benefits and disadvantages should be fully taken into account and patient pain and complications must be minimized. A biopsy should be performed only when the patient has been given an adequate explanation of his/her disease condition and in cooperation with other related departments. Since facilities available for the safe conduct of biopsies of distant recurrence lesions are limited, such a facility should be entrusted with carrying out the biopsy without hesitation if the current facility lacks any of the capability or capacity for carrying out biopsies.
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This article is an English digested edition of the Nyugan Shinryo guideline 2013 nen ban, published by Kanehara & Co., LTD.
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Tozaki, M., Isomoto, I., Kojima, Y. et al. The Japanese Breast Cancer Society Clinical Practice Guideline for screening and imaging diagnosis of breast cancer. Breast Cancer 22, 28–36 (2015). https://doi.org/10.1007/s12282-014-0557-8
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DOI: https://doi.org/10.1007/s12282-014-0557-8