Breast cancer (BC) is the second important cause of cancer-related death a leading cause of death in female adults that mostly affects females [1]. In 2021, 280,000 cases of BC were diagnosed in the US, leading to over 43,000 deaths[2]. The BC prevalence in Iranian women is nearly 120 per 100000 people with an age-standardized rate of 33.21 per 100 000 people. The BC peak age is in the 4th and 5th decades [3].

The selection of systemic and local treatment for patients with BC depends on factors such as tissue type and tumor grade, primary tumor progress, lymph node status, presence of metastasis, and the status of tumor markers at the time of diagnosis [3,4]. The Multicentric and Multifocality of neoplastic lesions are decisive factors in choosing the type of treatment [5,6]. When there are 2 or more foci in one-quarter of the breast, it is called multi-focal type lesions, and when foci occur in different quadrants, it is called multi-focal type lesions [7,8]. The prevalence of multicentric and multifocal BC varies highly in the literature (6 - 60%) [9]. The main imaging modalities are magnetic resonance imaging (MRI), ultrasound (US), mammogram (MGM), and. Each modality has specific weaknesses and strengths in breast tumor evaluation [10,11]. Thus, multifocal (MF) and multicentric (MC) BC cases are increasing [12].

Among different attainable imaging techniques, mammography can detect neoplastic lesions in the breast as an inexpensive, reproducible, and available method [13]. Mammography (MG) sensitivity is associated with the breast structure. It reduces and ranges between 45% and about 60% in breasts, with a predominance of glandular tissue [14]. Particularly in women with dense breasts and young women, US is superior to MG, and differentiation between cysts and solid tumors is easier [15]. The specificity and sensitivity of US or MG are higher if US and MG are combined [16].

MRI, MG, extended with diffusion imaging (DWI/ADC) has a high level of septicity and sensitivity (over 85%) (18-20). In Akbari et al.’s study, the high sensitivity of MRI in identifying benign and malignant lesions is emphasized. Nonetheless, it has some limitations, such as false-positive results, leading to more aggressive treatment and management than necessary [17]. Opposite to MG, which underestimates the tumor size leading to incomplete resection, MRI is highly precise for the local extent of BC, carcinoma region, and tumor size. Also, some foci and carcinomas can be observed merely on breast MRI images [18].

Contrast-enhanced spectral mammography (CESM) as a novel recently developed technique was accepted by the FDA for clinical application in the US in 2011 [19]. It works based on imaging of tumor neoangiogenesis using a contrast compound (chelated iodine-associated X-ray contrast compound) [20]. The CESM sensitivity in diagnosing BC is over 90% [21]. As a result, in the present meta-analysis study, we had a comparison identifying imaging diagnosis methods such as ultrasound, MG, and MRI methods that were investigated for patients with multifocal and multicentric BC.

The current systematic review was done based on the Strengthening the Reporting of Observationally Studies in Epidemiology (STROBE) and Meta-Analyses of Observational Studies in Epidemiology (MOOSE) instructions for the review of analytical observational articles (cohort and case-control) [22,23].

A. Search strategy

All original studies were searched in Web of Science, Medline (PubMed), EMBASE, Scopus, and CINHAL from January 2017 to June 2022 with no language limitation. The keywords were BC, MRI, MG, US, and Multifocal. The included studies were observational studies on humans.

The initial search findings were reviewed, leading to the removal of some papers. Exclusion and inclusion criteria were set by two investigators separately (Figure 1).

B. Eligibility criteria

(1) The original article, (2) human population, (3) Studies that only examined multifocal lesions in BC patients, (4) Studies that investigated the sensitivity and specificity of the methods considered in this study in multifocal lesions. (5) The detection power in the tumor size was not considered, only in the efficiency studies, the sensitivity and specificity of the method were the criteria for selecting the articles. Studies that investigated lesions other than multifocal in BC patients and did not report the sensitivity and specificity of the methods in identifying multifocal lesions were excluded from the study.

C. Search Outcome

We detected 100 articles in databases. Duplicates (N = 20) were excluded. Based on the selection criteria, 80 abstracts were screened and 30 Records were excluded based on title/abstract. We detected 50 relevant published articles but after reading their full texts, 30 cases were excluded because of Reports excluded (n = 10), inconsistency with the objectives of the study (n = 7), not available full text (n = 3), and Review article (n = 4). Finally, 6 articles remained which include 1 cohort and 4 retrospective and 1 prospective (Figure 1).

The Quality Assessment Tool [24] assessed the quality of the quantitative studies. Using the STROBE list (Table 1), the quality of 30 articles was evaluated, and at least six appropriate articles were included. The examination of full-text articles was done before data extraction. The used list is the version developed based on an instrument designed by the Effective Public Health Practice Project [24].

The articles were evaluated independently by two researchers who evaluated the possible disagreement, and when no agreement was made, a third author (LS) assessed the study. Data extraction was done by two independent matched reviewers based on a uniform Excel sheet. A checklist was applied to extract data, like (1) publication year, (2) author, (3) country (4) type of study, (5) Number sample, (6) age (7), Assessment (N) (8) MG, (9) MRI, (10) CESM and (11) US. Data has been assembled in Table 2.

D. Statistical analysis

For each study, false positive (FP), true positive (TP), false negative (FN), and true negative (TN) values were calculated. The homogeneity of results was evaluated by the results of Cochran’s Q test and the inconsistency index (I2) and random-effects model was applied to determine the overall effect. Forest plots with descriptions of the results were applied to explain the estimates of the accuracy measures (sensitivities, specificities, negative and positive likelihood ratios (LRs) receiver operating characteristic curve (ROC), and diagnostic odds ratios (dOR), describing the relationship between sensitivity and specificity of the test) with 95% confidence intervals (CIs). An area under the curve (AUC) close to 1 indicates the good diagnostic performance of the method. Meta-Disc 1.4 was used for all statistical analyses.

Overall, 6 studies were analyzed and their characteristics are shown in Table 2. All patients in this study underwent imaging examination prior to operation to screen those suspected of having multifocal/multicentric BCs. The final diagnosis was made considering pathology, so all studies had a histopathologic examination and were cross-sectional, originating in China (N = 1), Italy (N = 2), Poland (N = 2), and Nederland (N = 1) .1 of these studies were cohort studies and 4 were retrospective studies and 1 was prospective. The age range from (pooled data) 496 samples was 57.3. Statically designed studies for comparing imaging methods with the histopathologic examination were as fellow: 4 studies MRI and CESM (29-32),4 studies MG and MRI (31-34),1 study MG, MRI, and CESM (29), and 1 study MRI, CESM, and US (30). And finally, Feng’s (29) US results had been excluded from analyses because None of the other studies had investigated this issue.

Measurements of the overall accuracy of MG and contrast-enhanced spectral mammography (CESM) compared with the histopathologic examination in the detection of multifocal and multicentric breast cancer (MMBC):

Using the results of 5 published articles for MG and CESM, the overall specificity and sensitivity were 89% (95% CI: 84-93) and 85% (95% CI: 81-88), respectively (Figure 1). The pooled positive and negative likelihood ratios (LRs) were respectively 5.47 (95% CI: 2.53-11.83) and 0.24 (95% CI: 0.12-0.48) (Figure 2). Pooled diagnostic odds ratios (dOR) were high, at 49.90 (95% CI: 17.76-94.21) (Figure 3). The AUC for MG and CESM was 0.94 (Figure 4).

Measurements of the overall accuracy of MRI compared with a histopathologic examination in the detection of multifocal and multicentric breast cancer (MMBC):

Using the results of 5 published articles for MRI, the overall specificity and sensitivity were 81% (95% CI: 73-87) and 85% (95% CI: 81-88), respectively (Figure 5). The pooled positive and negative likelihood ratios (LRs) were also 4.67 (95% CI: 1.81-12.09) and 0.07 (95% CI: 0.03-0.19), respectively (Figure 6). The pooled diagnostic odds ratios (dOR) were high and were 91.70 (95% CI: 37.59-223.69) (Figure 7). The AUC for MRI was 0.96 (Figure 8).

BC is a very common reason for death in adult females (35,36) with a prevalence of 1 out of 8 women and a risk of developing during the whole lifetime of 12.5% (37,38). As a result, considering the high prevalence of BC, examining diagnostic methods is of great importance. Following the development of pathology and imaging, there has been an increase in the detection rates of MC and MF BCs [25]. The main aim of this meta-analysis study was to compare diagnostic methods in identifying multifocal/multicentric lesions in BC patients.

Most recent studies have considered comparing the specificity and sensitivity of MRI and CESM for the detection of singular BC areas and omit additional neoplastic areas affecting the scope of surgical procedures [26], The occurrence of multicentric and multifocal BCs is between 9 and 75% [27], which differs because of using various imaging modalities or the histopathological sample collection method. Tot et al. [28] reported that 40% of BC showed simple (unifocal) subgross appearance, whereas 60% showed complex appearance with diffuse or multifocal components. Steinhof-Radwań ska et al. (2021) confirmed multi-centrality and multifocality of the lesions in 38 cases (38/71, which is 53.5% of all the tested cases) [29].

CESM offers a low-energy mammogram (LE-MG) and is a combined subtracted mammogram (RSM) following intravenously administration of iodinated contrast medium images in the examination session within a short duration [28]. CESM offers a morphologic assessment similar to routine digital MG and simultaneous tumor neovascularity evaluation as an indicator of malignancy. CESM exhibited an extremely high sensitivity to BC [30,31].

In our study, the overall specificity and sensitivity of mammography (CESM) were respectively 89% (95% CI: 84-93) and 85% (95% CI: 81-88) . In Taylor et al.’s study (2023), the sensitivity of the CEM method was reported to be up to 95% to identify breast lesions [32]. Tagliafico et al. [33] in their meta-analysis, declared a pooled sensitivity of 98% for CESM to detect BC, including over 900 lesions.

MRI method is widely used in BC patients because of its high specificity and sensitivity [34]. In such patients, in contrast to MG, MRI provides a doubled or even tripled sensitivity. MRI is helpful in patients who have lobular cancer and case with enhanced breast density. In such female patients, the MG efficacy is underestimated, and neoplastic lesions can be missed. Women who have high breast density can provide with systematic abbreviated MRI for screening [35].

In our study, the overall specificity and sensitivity of the MRI method were 81% (95% CI: 73-87) and 85% (95% CI: 81-88), respectively. In the study of Ahmed (2023), in the examination of breast lesions in patients, she introduced the MRI method as a suitable method for multifocal lesions [36]. In the study of Farghadani et al. (2021), the Specificity and accuracy of MRI were reported as 93.02 and 93.75%, respectively [37].

In the study of Feng [38] and Ferranti [39], the highest percentage was reported for the sensitivity of the MRI method. In the study of Akbari et al. (2019) with the aim of evaluating the diagnostic capabilities of different methods of BC, the sensitivity, accuracy, and specificity were 24.7%, 40.2%, specificity 82%, and the sensitivity, accuracy, and specificity of ultrasound were 26%, respectively. 41.44, a specificity of 58.2% was reported [40].

Generally, CESM can detect multifocal malignancies and its sensitivity has been widely reported as comparable to MRI breast with superior specificity [41,42]. Lee-Felker et al. declared an equal sensitivity for MRI and CESM (respectively 94% vs. 99%,) to detect index lesions as well as higher sensitivity for CESM than MRI (100% vs 91%, respectively) to detect secondary cancers [43].

Generally, CESM can detect multifocal malignancies, and its sensitivity has been reported comparable to MRI breast and with superior specificity [41,42], Lee-Felker et al. reported that CESM and MRI have similar sensitivity (94% vs 99%, respectively) in detecting index lesions and higher sensitivity of CESM (100% vs. 91%, respectively) in detecting secondary cancers [43].

Our study articles showed that in MG and CESM, the overall sensitivity and specificity were 85% and 89% (84-93), and on the other hand, in MRI, the overall sensitivity and specificity were 85% and 81%. But Radwanska’s study suggested that MRI and CESM provide better results in the diagnosis of MFMCC than MG, significantly affecting surgical decisions (31). Of course, the MRI method is the most sensitive tool for diagnosing BC in patients, but if a combination of new methods is used together, we will definitely achieve better results [44,45].

Precise breast imaging as well as visualization of additional cancer foci possibly decreases the postoperative breast radiotherapy quantity following conserving treatment in many patients. This procedure reduces the number of complications in patients, and consequently, treatment costs. Most of the studies compared the examined diagnostic methods on breast lesions in general, and few studies focused only on multifocal lesions, and the ultrasound method was mostly used to detect the mass by considering its size. Most studies of new methods such as CESM and its combination with MRI were investigated in the diagnosis of multifocal lesions.

We suggest that radiologists who wish to report on MG should be trained in this particular subject, and breast surgeons should be fully trained in breast ultrasound examination, and according to the results of this study, use the CEsM method and even combine it with MRi can be very effective in diagnosing multifocal lesions.

The authors declare no conflict of interests. All authors read and approved final version of the paper.

All authors contributed equally in this paper.

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