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10.1136/bmjopen-2022-069788
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Original Research
Radiology and Imaging
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Meta-analysis and systematic review of the diagnostic value of contrast-enhanced spectral mammography for the detection of breast cancer
Liu Jiulin 121321842637@qq.com

Xiao Ran 3787637577@qq.com

Yin Huijia 1289353978@qq.com

Hu Ying 1422093889@qq.com

Zhen Siyu 11778634194@qq.com

Zhou Shihao 12zsh940626556@163.com

http://orcid.org/0000-0001-8516-1396
Han Dongming 1625492590@qq.com

1 Department of Magnetic Resonance Imaging (MRI), The First Affiliated Hospital of Xinxiang Medical University, Weihui, Henan, China
2 Department of Radiology, Luoyang Orthopedic-Traumatological Hospital of Henan Province (Henan Provincial Orthopedic Hospital), Zhengzhou, Henan, China
3 Department of Respiratory Medicine, The First Affiliated Hospital of Xinxiang Medical University, Weihui, Henan, China
Dr; 625492590@qq.com
None declared.

Supplemental material: Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

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https://creativecommons.org/licenses/by-nc/4.0/ This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

Abstract

Objective

The objective is to evaluate the diagnostic effectiveness of contrast-enhanced spectral mammography (CESM) in the diagnosis of breast cancer.

Design

Data sources

PubMed, Embase and Cochrane libraries up to 18 June 2022.

Eligibility criteria for selecting studies

We included trials studies, compared the results of different researchers on CESM in the diagnosis of breast cancer, and calculated the diagnostic value of CESM for breast cancer.

Data extraction and synthesis

Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2) evaluated the methodological quality of all the included studies. The study followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses specification. In addition to sensitivity and specificity, other important parameters were explored in an analysis of CESM accuracy for breast cancer diagnosis. For overall accuracy estimation, summary receiver operating characteristic curves were calculated. STATA V.14.0 was used for all analyses.

Results

This meta-analysis included a total of 12 studies. According to the summary estimates for CESM in the diagnosis of breast cancer, the pooled sensitivity and specificity were 0.97 (95% CI 0.92 to 0.98) and 0.76 (95% CI 0.64 to 0.85), respectively. Positive likelihood ratio was 4.03 (95% CI 2.65 to 6.11), negative likelihood ratio was 0.05 (95% CI 0.02 to 0.09) and the diagnostic odds ratio was 89.49 (95% CI 45.78 to 174.92). Moreover, there was a 0.95 area under the curve.

Conclusions

The CESM has high sensitivity and good specificity when it comes to evaluating breast cancer, particularly in women with dense breasts. Thus, provide more information for clinical diagnosis and treatment.

breast imaging
breast tumours
diagnostic radiology
Henan Medical Science and Technology Research Program LHGJ20210498
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pmcSTRENGTHS AND LIMITATIONS OF THIS STUDY

This systematic review was a comprehensive search of experimental and observational studies on contrast-enhanced spectral mammography (CESM) in the diagnosis of breast cancer.

We included only prospective studies. Prospective studies were of higher quality with less bias, and our study screening criteria were developed prior to the meta-analysis.

The study was conducted by two people and was strictly based on inclusion criteria.

The data in this study were summarised using sound statistical methods.

A recent literature was added, and a literature from the same institution included only the most recent or the largest sample size.

We summarised the sensitivity and specificity of CESM in the diagnosis of breast cancer.

Introduction

Globally, female breast cancer has overtaken lung cancer as the leading cause of cancer death, making it the fifth most common cause of death.1 From the mid-20th century, the incidence of breast cancer in women has been increasing slowly by about 0.5% per year.2 At present, the diagnostic methods of breast cancer include MRI, full field digital mammography (FFDM) and ultrasound (US). MRI is the most sensitive examination in the diagnosis of breast cancer at present.3 However, it has some disadvantages such as no claustrophobic and high price. In addition, although FFDM is an effective diagnostic method for breast cancer, it also has the hazard of recall and needs further testing.4 Ultrasonography has good diagnostic efficacy for breast cancer, especially in women with dense breasts; however, it has a relatively low positive predictive value.5 Contrast-enhanced spectral mammography (CESM), which visualises breast neovascularisation in a manner similar to MRI, is an emerging technology that uses iodine contrast agent.6 CESM has the advantages of patient friendliness and low cost. Previous studies have shown that CESM has obvious advantages in displaying lesions compared with US. The advantage of CESM is that it can show changes in anatomy and local blood perfusion, which may be caused by tumour angiogenesis.7 Moreover, CESM is useful in detecting the suspicious findings in routine breast imaging7 and the sensitivity and specificity of CESM are different in different studies.

It has been reported that several meta-analyses have been conducted regarding the diagnostic performance of CESM for breast cancer; however, their pooled results were different and had several limitations.811 On the one hand, the sensitivity and specificity differed across the above-mentioned meta-analyses.8 10 11 On the other hand, the numbers of included studies were limited. In addition, partial meta-analyses included none-English studies and overlapped studies, which might affect their pooled results. In the past few years, several studies evaluating the diagnostic value of CESM in breast cancer have been published. Therefore, we conducted this meta-analysis using available evidence to comprehensively determine whether CESM is effective in detecting breast cancer in women.

Material and methods

As recommended by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA), we conducted our study followed the PRISMA specification,12 which met the requirements of diagnostic systematic review.

Search strategy

To evaluate the accuracy of CESM in diagnosing breast cancer, we retrieved the following databases: PubMed, Embase and Cochrane library. Two reviewers, JL and RX, independently searched the above databases up to the date of 18 June 2022. Our searching terms included ‘contrast-enhanced spectral mammography’, ‘Dual-Energy Contrast-Enhanced Spectral Mammography’, ‘CESM’, ‘contrast-enhanced digital mammography’, ‘CEDM’, ‘Breast Neoplasms’, ‘Breast Neoplasm’, ‘Breast Tumor’, ‘Breast Tumors’, ‘Breast Cancer’, ‘Malignant Neoplasm of Breast’, ‘Breast Malignant Neoplasm’, ‘Breast Carcinomas’, ‘Breast Carcinoma’, ‘breast mass’, ‘breast lesion’, ‘breast lesions’, ‘breast diseases’. In addition, the references of all the included studies were also reviewed.

Inclusion and exclusion criteria

Following is the list of inclusion criteria: (1) studies diagnosing breast cancer, (2) studies provided data on the sensitivity and specificity, (3) studies involving ≥10 patients or case, (4) English language and(5) prospective studies. Following is the list of exclusion criteria: (1) overlapped research, (2) commentaries, letters, editorials or abstracts or (3) studies referencing artificial intelligence and radiomics.

Study screening

The titles and abstracts of the literature in the electronic databases were initially screened by two authors, following the above criteria for inclusion and exclusion. Each of the two researchers screened two times to avoid omission. If there is any disagreement, the third author was consulted to decide. Eligibly downloaded full texts and further screened. First, if the authors and institutions of the study are the same, we will include the most recently published studies with the largest sample size. If the research institutions are the same, but the authors are different, we will send an email to the corresponding authors to ask. If we do not receive a reply, we will include the most recently published studies having the largest sample size.

Data abstraction

Two reviewers extracted data. If necessary, the difference shall be solved by the third reviewer. Each study was analysed for the following information: first author name, publication year, country, the numbers of patients and lesions, median age, the results of true positive (TP), false positive (FP), false negative (FN) and true negative (TN).

Quality assessment

The quality of the methodology included in the publication was assessed by the Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2).13 QUADAS-2 were mainly focused on the following four domains: patient selection, index test, reference standard and flow and timing, with minimal overlapping, which present the main quality of the diagnostic study. Each domain is assessed according to risk of bias, with the three domains assessed according to applicability. The risk of bias was considered low if the study met the above criteria and high otherwise. Disagreements between the two reviewers on quality assessment were resolved by consensus.

Statistical analysis

STATA V.14.0 was used for all analyses. I2 measure was used to quantify the heterogeneity between studies. If there is no statistical heterogeneity, the fixed effect model is used to consolidate the data. On the contrary, the random effect model is used to summarise the data. The sensitivity was shown in the form TP/(TP+FN), where TP represents the number of true-positive results and FN represent the number of FN results. The specificity was shown in the form TN/(TN+FP), where TN represent the number of TN results and FP represent the number of FN results.14 We also computed other significant measures on the evaluation of diagnostic experiments such as positive likelihood ratio (PLR) and negative likelihood ratio (NLR) and diagnostic OR (DOR). The summary receiver operating characteristic curve ROC (SROC) curve and the area under the curve (AUC) of the SROC curve were also computed.

Results

Study characteristics

After a systematic search, we included 12 studies.1526 The complete selection process is in detail in PRISMA flowchart (figure 1). From 544 screened studies, 85 studies were subjected to full text reading. The characteristics of all the 12 included studies are shown in table 1. These 12 studies are all prospective studies published between 2014 and 2022. Most patients had US, mammography and related examinations before CESM examination. The dense breast we collected account for approximately two-thirds. In addition, the methodological quality assessment of all included studies was shown in online supplemental table 1.

Table 1 Study characteristics of each included study

Author	Year	Patients	Lesions	BC	DCIS	Median age (range)	Projection used	Inclusion criteria	Contrast media	Country	
Ferranti et al25	2022	118	142	88	NR	48.5	CC+MLO	Suspicious findings on FFDM and US	Visipaque320	Italy	
Sudhir et al24	2021	130	166	87	14	45	CC+MLO	Dense breasts detected on 2D MG	Omnipaque350	India	
Mohamed et al23	2021	25	56	14	NR	41 (21–66)	CC+MLO	With dense breasts	Ultravist300 or Omnipaque300	Egypt	
Lu et al21	2020	115	131	64	2	47.4 (15–75)	CC+MLO	With dense breasts	Iohexol	China	
Yasin and Ghany20	2019	50	28	28	NR	52 (33–83)	CC+MLO	Breast lesion on BIRADS 4 on MG and US	Visipaque	Egypt	
Petrillo et al22	2020	100	134	81	16	NR	CC+MLO	BIRADS 3, 4 or 5 on MG and/or US	Visipaque320	Italy	
Xing et al19	2019	235	263	177	6	51 (25–82)	NR	Suspicious findings on US or clinical	Iohexol	China	
Mori et al18	2017	72	143	58	18	48 (22–77)	CC+MLO	BIRADS 3–5 by MG or US	Omnipaque300	Japan	
Helal et al26	2017	30	35	21	NR	46.8	CC+MLO	BIRADS 3, 4 on imaging	Omnipaque300	Egypt	
Wang et al17	2016	68	77	48	5	52.9 (31–82)	CC+MLO	suspicious findings on MG and/or US	Omnipaque	China	
Mokhtar and Mahmoud16	2014	60	60	44	0	20–70	CC+MLO	with dense breasts	Omnepac	Egypt	
Luczyńska et al15	2014	174	191	114	19	55.7	CC+MLO	suspicious findings on MG	Ultravist370	Poland	
BC, breast cancer; BI-RADSBreast Imaging Reporting and Data SystemCC, craniocaudal; DCIS, ductal carcinoma in situ; FFDMfull field digital mammographyMG, mammography; MLO, mediolateral oblique; NR, not reportedUS, ultrasound

Figure 1 The figure shows the workflow for study screening and selection. CESM, contrast-enhanced spectral mammography.

Diagnostic accuracy of CESM

The sensitivity and specificity values were shown in Forest plots (figure 2). A very high pooled test sensitivity of 0.97 (95% CI 0.92 to 0.98) was estimated. The pooled specificity was 0.76 (95% CI 0.64 to 0.85). The PLR was 4.03 (95% CI 2.65 to 6.11), NLR was 0.05 (95% CI 0.02 to 0.09) (figure 3) and DOR was 89.49 (95% CI 45.78 to 174.92) (online supplemental figure 1). I2 values of sensitivity, specificity, PLR, NLR and DOR were 76.60%, 87.95%, 86.25%, 65.73% and 99.78%, respectively.

Figure 2 Forest plot of estimates of sensitivity and specificity for contrast-enhanced spectral mammography in the diagnosis of breast cancer.

Figure 3 Forest plot of estimates of positive likelihood ratio and negative likelihood ratio for contrast-enhanced spectral mammography in the diagnosis of breast cancer.

As shown in figure 4, the SROC curve shows an AUC of 0.95 (0.93 to 0.97). CI is an interval estimation based on the average point estimation. The prediction interval is the interval estimation based on the individual value point estimation.

Figure 4 The plot shows the summary bivariate ROC curve for CESM diagnostic accuracy. AUC, area under the curve; CESM, contrast-enhanced spectral mammography; ROC, receiver operating characteristic curve; SENS, sensitivity; SPEC, specificity; SROC, summary receiver operating characteristic curve.

A confidence contour and a prediction contour were shown in the figure.

Fagan plots were drawn to understand the prior probability (current incidence) and the posterior probability (incidence estimated from this diagnostic experiment). In our sample, the pretest probability of malignancy was 50%, with a positive finding at CESM a post-test probability of 80% while a negative finding a post-test probability of 4% (online supplemental figure 2).

Regression analysis

We analysed some covariates (number of lesions, number of patients, being dense breast or not, year of publication) possible influence on the diagnostic accuracy of CESM. The regression analysis showed that the sensitivity of the studies that only included dense breast was different from that of other studies, but both were high (online supplemental figure 3). In addition, a limited number of studies were included, which reduced the reliability of the regression analysis.

Publication bias

A funnel plot drawn with Stata V.14.0 software was used to analyse the publication bias of the included studies (online supplemental figure 4). The included studies were evenly distributed on both sides of the regression line, showing that the included literatures had no obvious publication bias (p=0.78).

Discussion

CESM is emerging as a valuable tool for the diagnosis and staging of breast cancer. CESM combines the contrast enhancement effect caused by tumour neovascularisation with the information of anatomical changes. The lesions were highlighted by reciprocal subtraction of the images, which further increased the sensitivity of CESM for the diagnosis of breast cancer. It improves the accuracy in diagnosing breast cancer, providing more accurate tumour size and identification of multifocal disease, especially in patients with the dense type of breast.27

Results showed that the pooled sensitivity (0.97, 95% CI 0.92 to 0.98) was higher and the pooled specificity (0.76, 95% CI 0.64 to 0.85) was slightly lower than a previous meta-analysis9 which indicated a pooled sensitivity of 0.89 (95% CI 0.88 to 0.91) and a pooled specificity of 0.84 (95% CI 0.82 to 0.85). The reason for the high sensitivity may be that our study went through more rigorous study screening, included the latest literature, and CESM has been increasingly used in clinical practice in recent years. Another point is that all the studies we included are prospective studies, which are less susceptible to bias than retrospective studies. Another previous meta-analysis8 has obtained that CESM has high sensitivity for the diagnosis of breast cancer, but it has low specificity. This may be due to the following reasons: three studies included by the meta-analysis were similar and written by the same first author; the meta-analysis only included eight studies and the pooled specificity were obtained by six literatures. All the reasons may result in some bias. However, during our screening, there are five studies from the same authors152831 and with similar results, we only included one in which the study type was prospective and with large sample size and longest time span.

In addition, compared with other studies, this study included the latest studies in recent years, and conducted a more rigorous article screening, with each of the two researchers screening two times.

The DOR is a common statistic in epidemiology that expresses the strength of the association between exposure and disease.32 The diagnostic DOR for a test is the ratio of the odds of being positive in the disease to the odds of being positive in the non-disease. In our meta-analysis, the DOR was 89.49 (95% CI45.78 to 174.92), which was high. It indicated that if CESM showed a positive result, the probability of a true breast cancer being correctly diagnosed was 89.49 to 1. DOR offers considerable advantages in a meta-analysis of diagnostic studies by combining results from different studies into a more precise pooled estimate. The I2 statistic, also known as the inconsistency index, is a measure of heterogeneity or variability across studies in a meta-analysis. It quantifies the proportion of total variation in effect estimates that is due to heterogeneity rather than chance. Differences in study populations: the studies included in the meta-analysis may have varied in terms of patient characteristics, such as age, mammary gland type, disease severity or comorbidities. These differences can contribute to heterogeneity in the estimated DOR. Clinical and contextual factors: heterogeneity in DOR can also arise from differences in the clinical context, such as variations in disease prevalence, healthcare settings or geographic locations.

The SROC curve method takes into account the possible heterogeneity of thresholds.33 The SROC indicates the relationship between the TP rate and FP rate at different diagnostic thresholds.34 In general, the AUC of a diagnostic method between 0.5 and 0.7 means low accuracy, 0.7 and 0.9 means good accuracy, above 0.9 high accuracy. The SROC curve shows an AUC of 0.95, indicating high accuracy.

The study of Hobbs et al35 reminds of that patients’ preferences for CESM will provide further evidence supporting the adoption of CESM as an alternative to ce-MRI in selected clinical indications, if diagnostic non-inferiority of CESM is confirmed. Ferranti et al25 suggested that CESM may provide compensation for MRI through a slight FN tendency. Furthermore, Clauser et al36 thought the specificity of CESM is higher than that of MRI. CEM determines breast cancer based on tumour angiogenesis assessment.24 Growth factors secreted by cancer cells promote the formation of new blood vessels during division and proliferate to tumour cells. It is because of the increased vascular endothelial cell gap and permeability that the contrast in the tumour area is enhanced. CESM may combine the high sensitivity of MRI with the low cost and availability of FFDM.37

However, there are some limitations in the study. First, primary source participants were all patients with lesions diagnosed by breast US or mammography. This may induce a selection bias. Second, the majority of the main participants were with dense breast. This point, while highlighting the superiority of CESM over dense breast examination, may still be subject to some bias. Third, due to the excessive number of retrieved literatures, we only included prospective studies and studies writing in English. In this way, some reliable studies and results may be missed.

Conclusion

The CESM has high sensitivity and good specificity when it comes to evaluating breast cancer, particularly in women with dense breasts. Thus, provide more information for clinical diagnosis and treatment.

supplementary material

10.1136/bmjopen-2022-069788 online supplemental file 1

10.1136/bmjopen-2022-069788 online supplemental file 2

10.1136/bmjopen-2022-069788 online supplemental file 3

10.1136/bmjopen-2022-069788 online supplemental file 4

10.1136/bmjopen-2022-069788 online supplemental file 6

Data availability statement

Data sharing not applicable as no datasets generated and/or analysed for this study.

Review Process File
3 9 2024

Funding: This work has received funding by the Henan Medical Science and Technology Research Program (LHGJ20210498,LHGJ20230528).

Prepublication history and additional supplemental material for this paper are available online. To view these files, please visit the journal online (https://doi.org/10.1136/bmjopen-2022-069788).

Patient consent for publication: Not applicable.

Ethics approval: Not applicable.

Provenance and peer review: Not commissioned; externally peer reviewed.

Patient and public involvement: Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.
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References

1 Sung H Ferlay J Siegel RL et al Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries CA Cancer J Clin 2021 71 209 49 10.3322/caac.21660 33538338
2 Siegel RL Miller KD Fuchs HE et al Cancer statistics, 2022 CA Cancer J Clin 2022 72 7 33 10.3322/caac.21708 35020204
3 Mann RM Cho N Moy L Breast MRI: State of the art Radiology 2019 292 520 36 10.1148/radiol.2019182947 31361209
4 Houssami N Should tomosynthesis replace mammography for breast cancer screening? Lancet Oncol 2022 23 554 5 10.1016/S1470-2045(22)00215-7 35427472
5 Loibl S Poortmans P Morrow M et al Breast cancer Lancet 2021 397 1750 69 10.1016/S0140-6736(20)32381-3 33812473
6 Patel BK Lobbes MBI Lewin J Contrast enhanced spectral mammography: a review Semin Ultrasound CT MR 2018 39 70 9 10.1053/j.sult.2017.08.005
7 Jochelson MS Lobbes MBI Contrast-enhanced mammography: state of the art Radiology 2021 299 36 48 10.1148/radiol.2021201948 33650905
8 Tagliafico AS Bignotti B Rossi F et al Diagnostic performance of contrast-enhanced spectral mammography: systematic review and meta-analysis Breast 2016 28 13 9 10.1016/j.breast.2016.04.008 27161411
9 Zhu X Huang J-M Zhang K et al Diagnostic value of contrast-enhanced spectral mammography for screening breast cancer: systematic review and meta-analysis Clin Breast Cancer 2018 18 e985 95 10.1016/j.clbc.2018.06.003 29983379
10 Suter MB Pesapane F Agazzi GM et al Diagnostic accuracy of contrast-enhanced spectral mammography for breast lesions: a systematic review and meta-analysis Breast 2020 53 8 17 10.1016/j.breast.2020.06.005 32540554
11 Xiang W Rao H Zhou L A meta-analysis of contrast-enhanced spectral mammography versus MRI in the diagnosis of breast cancer Thorac Cancer 2020 11 1423 32 10.1111/1759-7714.13400 32233072
12 McInnes MDF Moher D Thombs BD et al Preferred reporting items for a systematic review and meta-analysis of diagnostic test accuracy studies: the PRISMA-DTA statement JAMA 2018 319 388 96 10.1001/jama.2017.19163 29362800
13 Whiting PF Rutjes AWS Westwood ME et al QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies Ann Intern Med 2011 155 529 36 10.7326/0003-4819-155-8-201110180-00009
14 Psoter KJ Roudsari BS Dighe MK et al Biostatistics primer for the radiologist AJR Am J Roentgenol 2014 202 W365 75 10.2214/AJR.13.11657 24660735
15 Luczyńska E Heinze-Paluchowska S Dyczek S et al Contrast-enhanced spectral mammography: comparison with conventional mammography and histopathology in 152 women Korean J Radiol 2014 15 689 96 10.3348/kjr.2014.15.6.689 25469079
16 Mokhtar O Mahmoud S Can contrast enhanced mammography solve the problem of dense breast lesions? Egypt J Radiol Nucl Med 2014 45 1043 52 10.1016/j.ejrnm.2014.04.007
17 Wang Q Li K Wang L et al Preclinical study of diagnostic performances of contrast-enhanced spectral mammography versus MRI for breast diseases in China Springerplus 2016 5 763 10.1186/s40064-016-2385-0
18 Mori M Akashi-Tanaka S Suzuki S et al Diagnostic accuracy of contrast-enhanced spectral mammography in comparison to conventional full-field digital mammography in a population of women with dense breasts Breast Cancer 2017 24 104 10 10.1007/s12282-016-0681-8 26942415
19 Xing D Lv Y Sun B et al Diagnostic value of contrast-enhanced spectral mammography in comparison to magnetic resonance imaging in breast lesions J Comput Assist Tomogr 2019 43 245 51 10.1097/RCT.0000000000000832 30531546
20 Yasin R El Ghany EA BIRADS 4 breast lesions: comparison of contrast-enhanced spectral mammography and contrast-enhanced MRI Egypt J Radiol Nucl Med 2019 50 10.1186/s43055-019-0043-6
21 Lu Z Hao C Pan Y et al Contrast-enhanced spectral mammography versus ultrasonography: diagnostic performance in symptomatic patients with dense breasts Korean J Radiol 2020 21 442 9 10.3348/kjr.2019.0393 32193892
22 Petrillo A Fusco R Vallone P et al Digital breast tomosynthesis and contrast-enhanced dual-energy digital mammography alone and in combination compared to 2D digital synthetized mammography and MR imaging in breast cancer detection and classification Breast J 2020 26 860 72 10.1111/tbj.13739 31886607
23 Mohamed SAS Moftah SG Chalabi NAEM et al Added value of contrast-enhanced spectral mammography in symptomatic patients with dense breasts Egypt J Radiol Nucl Med 2021 52 10.1186/s43055-020-00372-2
24 Sudhir R Sannapareddy K Potlapalli A et al Diagnostic accuracy of contrast-enhanced digital mammography in breast cancer detection in comparison to tomosynthesis, synthetic 2D mammography and tomosynthesis combined with ultrasound in women with dense breast Br J Radiol 2021 94 20201046 10.1259/bjr.20201046 33242249
25 Ferranti FR Vasselli F Barba M et al Diagnostic accuracy of Contrast-Enhanced, Spectral Mammography (CESM) and 3T magnetic resonance compared to full-field digital mammography plus ultrasound in breast lesions: results of a (Pilot) open-label, single-centre prospective study Cancers (Basel) 2022 14 1351 10.3390/cancers14051351 35267659
26 Helal M Abu Samra MF Ibraheem MA et al Accuracy of CESM versus conventional mammography and ultrasound in evaluation of BI-RADS 3 and 4 breast lesions with pathological correlation Egypt J Radiol Nucl Med 2017 48 741 50 10.1016/j.ejrnm.2017.03.004
27 James JJ Tennant SL Contrast-enhanced spectral mammography (CESM) Clin Radiol 2018 73 715 23 10.1016/j.crad.2018.05.005 29937340
28 Luczyńska E Heinze S Adamczyk A et al Comparison of the mammography, contrast-enhanced spectral mammography and ultrasonography in a group of 116 patients Anticancer Res 2016 36 4359 66 27466557
29 Łuczyńska E Heinze-Paluchowska S Hendrick E et al Comparison between breast MRI and contrast-enhanced spectral mammography Med Sci Monit 2015 21 1358 67 10.12659/MSM.893018 25963880
30 Luczynska E Niemiec J Ambicka A et al Correlation between blood and lymphatic vessel density and results of contrast-enhanced spectral mammography Pol J Pathol 2015 66 310 22 10.5114/pjp.2015.54965 26619110
31 Łuczyńska E Niemiec J Hendrick E et al Degree of Enhancement on Contrast Enhanced Spectral Mammography (CESM) and Lesion Type on Mammography (MG): comparison based on histological results Med Sci Monit 2016 22 3886 93 10.12659/msm.900371 27768681
32 Glas AS Lijmer JG Prins MH et al The diagnostic odds ratio: a single indicator of test performance J Clin Epidemiol 2003 56 1129 35 10.1016/s0895-4356(03)00177-x 14615004
33 Takwoingi Y Guo B Riley RD et al Performance of methods for meta-analysis of diagnostic test accuracy with few studies or sparse data Stat Methods Med Res 2017 26 1896 911 10.1177/0962280215592269 26116616
34 Dimou N Bagos P Meta-analysis methods of diagnostic test accuracy studies Methods Mol Biol 2022 2345 173 85 10.1007/978-1-0716-1566-9_11 34550591
35 Hobbs MM Taylor DB Buzynski S et al Contrast-enhanced spectral mammography (CESM) and contrast enhanced MRI (CEMRI): patient preferences and tolerance J Med Imaging Radiat Oncol 2015 59 300 5 10.1111/1754-9485.12296 25900704
36 Clauser P Baltzer PAT Kapetas P et al Low-dose, contrast-enhanced mammography compared to contrast-enhanced breast MRI: a feasibility study J Magn Reson Imaging 2020 52 589 95 10.1002/jmri.27079 32061002
37 Bicchierai G Tonelli P Piacenti A et al Evaluation of contrast-enhanced digital mammography (CEDM) in the preoperative staging of breast cancer: large-scale single-center experience Breast J 2020 26 1276 83 10.1111/tbj.13766 31999029
