Comparison of contrast-enhanced mammography and breast magnetic resonance in the evaluation of response to neoadjuvant chemotherapy

doi:10.21203/rs.3.rs-4073077/v1

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Comparison of contrast-enhanced mammography and breast magnetic resonance in the evaluation of response to neoadjuvant chemotherapy

https://doi.org/10.21203/rs.3.rs-4073077/v1

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Objective: Contrast-enhanced mammography (CEM) is a relatively inexpensive and convenient new imaging method obtained by administering enhanced iodinated contrast agent using the dual-energy technique to evaluate tumor neovascularity. CEM provides similar morphological and physiological information to breast magnetic resonance (MRI), the gold standard for detecting breast cancer. We aimed to compare CEM techniques, which have increased in popularity in recent years, with MRI, which has been the gold standard imaging technique to date, using the histopathological evaluation of patients with breast cancer who were operated after receiving neoadjuvant chemotherapy (NAC).

Material and Method: CEM and breast MRI images of patients who were scheduled for surgery due to locally advanced breast cancer were taken before and after NAC. Responses to treatment and residual tumor sizes of patients operated after NAC were recorded.

Results: CEM estimated the residual tumor size to within 1 cm accuracy in 84.7% of the patients. MRI estimated the residual tumor size to within 1 cm accuracy in 76.4% of the patients. When we used histopathological evaluation as a reference, the Lin’s correlation concordance was higher for CEM than MRI. The sensitivity, NPV and PPV were higher compared to MRI. The superiority of MRI over CEM was its higher specificity rate.

Conclusion: Our findings showed that in patients receiving NAC, CEM was superior to MRI in identifying patients with pathological complete response and was at least as successful as MRI in patients with residual tumor.

CEM

MRI

NAC

Breast cancer

Neoadjuvant chemotherapy (NAC) is preferred to reduce micro metastatic disease, see response to chemotherapy, reduce tumor size, perform breast-conserving surgery, and avoid axillary dissection.[1]

Histopathological response after NAC determines the patient’s prognosis. Histopathological complete response is associated with longer disease-free survival and longer overall survival.[2] Histopathological complete response with NAC is seen at a rate of between 19% and 30% in breast cancer.[3] Imaging techniques are used before and after NAC to measure chemosensitivity and guide surgical planning. Post-NAC clinical examination, mammography, ultrasound, and breast MRI are used to predict pathological complete response. MRI is considered the gold standard imaging technique in terms of estimating both pathological response and residual tumor size.[4, 5] However, it is contraindicated in patients with metallic implants and pacemakers. Moreover, some patients develop anxiety due to claustrophobia or noise during MRI scans. It may not be preferred by patients due to its long scanning time.

Contrast-enhanced mammography (CEM) is a relatively inexpensive and convenient new imaging method obtained by administering enhanced iodinated contrast agent using the dual-energy technique to assess tumor neovascularity. It has higher diagnostic sensitivity compared to digital mammography and estimates lesion sizes more accurately.[6] CEM provides similar morphological and physiological information compared to MRI, which is the gold standard for detecting breast cancer.[7]

The aim of this study was to compare CEM techniques, which have increased in popularity in recent years, with MRI, which has been the gold standard imaging technique to date, using the histopathological evaluation of patients with breast cancer who were operated after receiving NAC.

The Study was approved by the Manisa Celal Bayar University’s Non-Invasive Clinical Research Ethics Committee (approval No: 227, date: 02/12/2021). It was designed as a prospective study and informed consent was obtained from all patients. We confirm that all methods were performed in accordance with relevant named guidelines and regulations.

Our study was conducted at Manisa Celal Bayar University Hafsa Sultan Hospital between December 2021 and June 2023. In the study 74 female patients were included. Patients who were older than 18 years of age, had histopathologically proven breast cancer, had an indication for NAC, and had no contraindications for CEM and MRI scan were included in the study. Patients with a history of allergy to iodine-based and gadolinium-based contrast agents, with renal failure, pregnant or suspected pregnancy, claustrophobia, weight not suitable for MRI, or with metallic implants were excluded from in the study.

As the NAC protocol, HER2-negative patients received 4 cycles of dose-dense AC (doxorubicin 60 mg/m2 plus cyclophosphamide 600 mg/m2 every two weeks) followed by paclitaxel 80 mg/m2 for 12 weeks. Patients who did not want to receive weekly treatment due to the COVID 19 pandemic were given 4 cycles of dose-dense AC followed by 4 cycles of dose-dense paclitaxel 175 mg/m2 (every 2 weeks). In triple negative patients, paclitaxel 80 mg/m2 plus carboplatin 2 AUC was given for 12 weeks following 4 cycles of intensive anthracycline. HER2-positive patients received 4 cycles of dose-dense anthracycline followed by 4 cycles of THP (docetaxel 75 mg/m2 plus trastuzumab 8 mg/kg as the initial loading dose then 6 mg/kg as the maintenance dose plus pertuzumab 840 mg as the loading dose then 420 mg as the maintenance dose) every 3 weeks. Additionally, depending on the clinician’s preference, HER2-positive patients received 6 cycles of TCHP (docetaxel 75 mg/m2 plus carboplatin 4–6 AUC plus trastuzumab 8 mg/kg as the initial loading dose then 6 mg/kg as the maintenance dose plus pertuzumab 840 mg as the loading dose then 420 mg as the maintenance dose) every 3 weeks.

CEM and MRI were applied to all patients before neoadjuvant chemotherapy and after the completion of treatment, with a maximum of 7 days in between, regardless of menstrual status.

All CEM images were obtained using the digital mammography device capable of dual energy acquisition (Pristina, GE, Reu De La Miniere, Buc, France) in our clinic. Before the scanning procedure, iodinated contrast agent (Opaxol 350 mg/ml, Kopaq 350 mg/ml) was injected intravenously, using an automatic injector system, at a dose of 1.5 ml/kg with the maximum dose being 100 ml. The scanning procedure was started 1.5 minutes after the injection of the contrast agent. The breast thought to have pathology was designated as the “target breast”, and the other breast was designated as the “non-target breast”. Low- and high-energy craniocaudal (CC) and then mediolateral-oblique 41 (MLO) images of both breasts (the target breast first) were taken. A value of 28–32 kVp was used in low-energy images, and a value of 45–49 kVp was used in high-energy images. Filtration material and kVp value were determined automatically by the device. The scanning time was approximately 5 minutes but could vary depending on patient compliance.

All breast MRI images were viewed in our clinic following the breast MRI protocol on a 1.5 Tesla MRI device (SignaHDx; General Electric, Milwaukee, WI, USA). Before the injection of the contrast agent, three preliminary and calibration images were taken. AxialFast Spin Echo T1A images; separate sagittal FSE fat-suppressed T2W images for each breast; diffusion-weighted images and sagittal, fat-suppressed, pre-contrast T1A 3D vibrant images were taken. Gadolinium-containing contrast agent (Gadobutrol – Gadonans, Gadoteric acid – Dotarem) was injected through the previously opened vascular access at a dose of 0.1 mmol/kg using an automatic injector. After the injection, five serial post-contrast sagittal fat suppressed, T1A 3D vibrant images were taken. Contrast-enhanced series were digitally subtracted from the first pre-contrast series to obtain subtractive images.

Radiological images were co-assessed by two radiologists with 32 years and 5 years of experience. Pre- and post-treatment CEM images were assessed together, pre- and post-treatment MRI images were assessed together, and a separate assessment was made with at least a 1-month interval in between. During the image assessment, the largest diameter of the contrast-enhancing lesion was measured in the recombined images for CEM and in the post-contrast T1-weighted images for MRI. In lesions with more than one focus, the largest focus was taken into account. Classification of response to treatment was made according to Response evaluation criteria in solid tumors (RECIST) 1.1 criteria.[8] Response was classified as follows: complete response (CR, disappearance of all lesions); partial response (PR, ≥ 30%-dimensional reduction), stable disease (SD, < 30% dimensional reduction /<20% dimensional increase) and progressive disease (PD, ≥ 20%-dimensional increase).

In the pathological evaluation, the tumor bed and the largest diameter of the residual tumor tissue were taken into account. Cases of residual ductal carcinoma in situ (DCIS) were classified as complete response.

STATISTICAL ANALYSIS

SPSS 15.0 for Windows and MedCalc 15.2 package were used for statistical analysis. The descriptive statistics were presented as mean, standard deviation, minimum, maximum and median for numeric variables, and as number and rate for categorical variables. The relationships between measurements were examined using Bland-Altman Plots, Lin’s concordance, Bivariate Pearson Correlation Analysis. The tumor sizes measured by CEM and MRI were examined along with the size measured in pathology (reference standard) - range from 1 cm to 1 cm. p < 0.05 was considered as the statistical alpha significance level.

74 patients were included in our study. Their median age was 48 years and 43.8% were post-menopausal. 93.2% had invasive ductal carcinoma subtype. The majority of patients were in clinical stage 2 before starting the treatment. Considering the molecular characteristics, 20.3% had triple negative, 6.8% had HER2-positive, estrogen-negative, 47.3% had luminal B, and 25.7% had luminal A disease. Most of them underwent radical mastectomy (Table1).

Table 1

Patient and tumor characteristics
Age Mean ± SD (Min-Max / Median)		48.5 ± 11.4 (29–75 / 48)
BRCA n (%)	0	14 (18.9)
	1	9 (12.2)
	2	51 (68.9)
Familial History n (%)	No	54 (73.0)
Familial History n (%)	Yes	20 (27.0)
Menopausal Status n (%)	Pre-Peri-menopausal	41 (56.2)
Menopausal Status n (%)	Post-menopausal	32 (43.8)
Molecular Characteristics n (%)	Luminal A	19 (25.7)
	Luminal B	35 (47.3)
	Her2 + Hormone Negative	5 (6.8)
	Triple Negative	15 (20.3)
Histological Subtype n (%)	Invasive Ductal	69 (93.2)
	Invasive Lobular	2 (2.7)
	Other	3 (4.1)
Location n (%)	Right Breast	37 (50.0)
	Left Breast	36 (48.6)
	Bilateral	1 (1.4)
Pre-Treatment Clinical Stage n (%)	Stage 1	5 (6,8)
	Stage 2	51 (68,9)
	Stage 3	18 (24.3)
TRU CUT Ki67 Mean ± SD (Min-Max)		35.4 ± 24.8 (2–95 / 30)
TRU CUT Ki67 Mean ± SD (Min-Max)		19.4 ± 25.4 (1–95 / 10)
Operation Type n (%)	Total Mastectomy	58 (78.4)
Operation Type n (%)	Lumpectomy	16 (21.6)
Neoadjuvant chemotherapy n (%)	4AC + 4P	22 (29.7)
	4AC + 12wP	20 (27.0)
	4AC + 12wPC	11 (14.9)
	4AC + 4P + H + P	19 (25.7)
	6TCHP	2 (2.7)
AC: dose dense doxorubicin cyclophosphamide P: paclitaxel wPC: weekly paclitaxel carboplatin PHP: paclitaxel trastuzumab pertuzumab TCHP: docetaxel carboplatin trastuzumab pertuzumab

Using histopathological assessment as a reference, CEM predicted pre- and post-NAC tumor size more accurately than MRI. As a result of the histopathological assessment, the mean tumor bed was 37.2 mm. The mean pre-NAC tumor size was 37.2 mm and 38.4 mm by CEM and MRI, respectively. The mean residual tumor size was 11.7 mm by histopathological assessment. The mean post-NAC tumor size was 10.7 mm and 13.3 mm by CEM and MRI, respectively (Table 2).

Table 2

Pre- and post-treatment mean tumor sizes (mm)
	Mean ± SD (Min-Max / Median)
Pre-CEM size	37.2 ± 22.3 (8-110 / 30)
Pre-MRI size	38.4 ± 21.7 (12–105 / 31.5)
Post-CEM size	10.7 ± 15.2 (0–70 / 4)
Post-MRI size	13.3 ± 16.4 (0–65 / 10)
Tumor bed size	37.2 ± 24.5 (6-105 / 30)
Residual tumor	11.4 ± 15.8 (0–94 / 5)
CEM: Contrast-enhanced mammography; MRI: Magnetic resonance imaging

The pre- and post-NAC correlation concordance was higher for CEM than MRI. The correlation concordance and Pearson correlation concordance between the pre-NAC CEM and the tumor bed having operative pathology was 0.73. The correlation concordance between the pre-NAC MRI and the tumor bed having operative pathology was 0.71. The correlation concordance and Pearson correlation concordance between the post-NAC CEM and the tumor bed having operational pathology was 0.77. The correlation concordance and Pearson correlation concordance between the post-NAC CEM and the residual tumor were 0.65 and 0.66, respectively (Table 3)

Table 3

Assess agreement between diagnostic imaging tools and pathology results.
	Concordance Correlation Coefficient (95% CI)	Pearson Correlation
Pre-CEM size vs. pre-MRI size	0.917 (0.869 to 0.948)	0.919
Pre-CEM size vs. tumor bed size	0.728 (0.591 to 0.824)	0.731
Pre-MRI size vs. tumor bed size	0.705 (0.554 to 0.811)	0.708
Post-CEM size vs. post-MRI size	0.848 (0.771 to 0.901)	0.862
Post-CEM size vs. residual tumor	0.769 (0.655 to 0.849)	0.770
Post-MRI size vs. residual tumor	0.653 (0.499 to 0.767)	0.658
CEM, contrast-enhanced mammography; MRI, magnetic resonance imaging

According to Bland-Altman plots, the difference between the post-NAC CEM and MRI tumor sizes was statistically significant and CEM showed the final tumor size better (Table 4).

Table 4

Bland–Altman plots visualize the differences between tumor size measured.
	Mean = 0 Arithmetic mean	95% CI	p (H₀: Mean = 0)
Pre-CEM size vs. pre-MRI size	-0.6	-2.8 to 1.6	0.608
Pre-CEM size vs. tumor bed size	-0.2	-4.4 to 4.1	0.943
Pre-MRI size vs. tumor bed size	1.0	-3.6 to 5.6	0.669
Post-CEM size vs. post-MRI size	-2.64	-4.6 to -0.7	0.0085
Post-CEM size vs. residual tumor	-0.7	-3.2 to 1.8	0.572
Post-MRI size vs. residual tumor	1.9	-1.3 to 5	0.235
CEM, contrast-enhanced mammography; MRI, magnetic resonance imaging

CEM estimated the residual tumor size to within 1 cm accuracy in 84.7% of the patients. It overestimated the residual tumor size in 6.9% of the patients. It underestimated the residual tumor size in 8.3% of the patients. MRI estimated the residual tumor size to within 1 cm accuracy in 76.4% of the patients. It overestimated the residual tumor size in 15.3% of the patients. It underestimated the residual tumor size in 8.3% of the patients (Table 5)

Table 5

Tumor size measured by CEM and by MRI is equivalent with tumor size measured in pathology (reference standard) within- 1 cm to 1 cm range.
	n (%)
CEM vs. pathology
CEM overestimate pathology (> 1 cm)	5 (6.9)
CEM underestimate pathology (< 1 cm)	6 (8.3)
CEM within 1 cm	61 (84.7)
MRI vs. pathology
MRI overestimate pathology (> 1 cm)	11 (15.3)
MRI underestimate pathology (< 1 cm)	6 (8.3)
MRI within 1 cm	55 (76.4)
CEM vs. MRI
CEM greater than MRI (> 1 cm)	-
CEM less than MRI (< 1 cm)	8 (10.8)
CEM within 1 cm vs. MRI	66 (89.2)
CEM, contrast-enhanced mammography; MRI, magnetic resonance imaging

Post-NAC histopathological complete response was seen in 23/74 patients. Histopathological complete response was accurately estimated in 21/23 and 16/23 patients by CEM and MRI, respectively. Sensitivity (91.3% vs 73.9%), specificity (70.6% vs 74.5%), negative predictive value (94.7% vs 86.4%), positive predictive value (58.3% vs 56.7%) (Table 6).

Table 6

Diagnostic performance
		Histopathology pCR	Histopathology non-pCR (pPR, pSD, pPD)
CEM	pCR	21	15	PPV 58.3% (CI 47.3–68.6%) PPV 94.7% (CI 82.6–98.6%)
CEM	Non-CR (PR, SD, PD)	2	36	PPV 58.3% (CI 47.3–68.6%) PPV 94.7% (CI 82.6–98.6%)
		Sensitivity 91.3% (CI 72-98.9%)	Specificity 70.6% (CI 56.2–82.5%)
MRI	pCR	17	13	PPV 56.7% (CI 43.5–68.9%) PPV 86.4% (CI 75.8–92.8%)
MRI	Non-CR (PR, SD, PD)	6	38	PPV 56.7% (CI 43.5–68.9%) PPV 86.4% (CI 75.8–92.8%)
		Sensitivity 73.9% (CI 51.6–89.8%)	Specificity 74.5% (CI 60.4–85.7%)
CEM: contrast-enhanced mammography MRI: magnetic resonance imaging PR: partial response SD: stable disease PD: progressive disease pCR: pathologic complete response pPR: pathologic partial response pSD: pathologic stable disease pPD: pathologic progressive disease PPV: positive predictive value NPV: negative predictive value.

In locally advanced breast cancer, imaging is requested for treatment planning before and after NAC. Even if a complete response is obtained with imaging techniques at the end of NAC, breast surgery is recommended according to our current knowledge. Today, MRI is recognized as the best imaging method for the clinical diagnosis, staging, follow-up, and monitoring of NAC response of breast cancer.[3, 5, 9] New imaging techniques are needed because MRI is contraindicated in case of metallic implants, has a long procedure time, and some patients experience claustrophobia and anxiety during the procedure. Recently, CEM a new imaging technique based on the combination of morphology and tumor neoangiogenesis, has been reported to perform at least as well as MRI.[10] CEM’s easier accessibility, lower price, and higher tolerability rates compared to MRI have made it a suitable alternative.[11] In addition, CEM has shown superiority over MRI by using both microcalcification (on the low-energy image) and contrast-enhancing structure (on the recombined image) in a single examination.[12, 13]

Most imaging methods overestimate or underestimate tumor size. Several variables such as pre-treatment tumor size, parenchymal distortion and asymmetry, calcification, edema, necrosis, histological subtype, and NAC selection affect tumor shrinkage.[7] The decrease in tumor cells after chemotherapy may not always be directly proportional to the reduction in tumor size. Because even if tumor cells are destroyed, fibrous stroma may still be present in the tumor bed. These issues make it difficult to predict the pathological response.[2] In our study, CEM accurately showed tumor size at a rate very close to the histopathological size. In almost 85% of the cases, the difference between CEM and the histopathological tumor size was within 1 cm. This rate is superior to MRI, which has been considered the gold standard imaging method so far (MRI 76.4%). In a study conducted in Brazil, which was similar to our study in terms of the design, the proportion of patients with a difference between CEM and histopathological tumor size within 1 cm was 70%.[14]

In our study, there was very strong concordance between the pathological residual tumor and CEM. The Lin’s correlation coefficient and Pearson correlation coefficient were higher for CEM than MRI (Lin’s correlation coefficients 0.77 vs 0.65, respectively). Studies conducted in the USA, Brazil and Italy have reported that the Lin’s correlation coefficients for CEM are similar, close to 0.8.[14–16] In our study, the correlation coefficient between CEM and MRI before NAC was 0.92, but it decreased to 0.85 after NAC. Similarly, in the study conducted by Lotti et al., the Lin’s correlation concordance between CEM and MRI was at the highest level before NAC but decreased after NAC.[16] The mean difference between the CEM and MRI tumor sizes before treatment was 0.6 cm, while being 2.6 cm after NAC. According to Bland-Altman plots, this difference is statistically significant. Bland-Altman plots show that CEM estimates tumor size more accurately, especially after NAC.

CEM was superior to MRI in estimating patients with histopathological complete response. In our study, the sensitivity, PPV and NPV were higher compared to MRI. The superiority of MRI over CEM was its higher specificity rate. The study conducted by Lotti et al. found that CEM had higher sensitivity, specificity, NPV, and PPV than MRI in identifying patients with pathological complete response.[16] The study conducted by Patel et al., CEM and MRI had almost similar sensitivity, specificity, PPV, and NPV in identifying patients with pathological complete response.[15] The study conducted by Barra et al. found that MRI had higher sensitivity and NPV, whereas CEM had higher specificity and PPV.[14] Elsaid et al. examined 21 patients who underwent NAC and found a sensitivity of 100% and specificity of 83% in identifying patients with pathological complete response by CEM.[17]

In our study, CEM identified patients with histopathological complete response with high success rate. However, there were a significant number of patients who had a complete response on CEM imaging but did not have a histopathological complete response (PPV: 58.3%). This is thought to be due to the fact that residual tumor cells, which are present as small foci in the tumor bed and receive the necessary molecules by diffusion rather than vascular perfusion, may have given false negative results in CEM.

It has been shown in previous studies and in our study that CEM can be used instead of or in conjunction with MRI. The image acquisition time for CEM is 7–10 minutes, while being longer than 30 minutes for MRI. In addition to being more comfortable for patients, it will also enable radiologists to use time more efficiently. However, it has some disadvantages compared to MRI. MRI has the advantage that the entire chest wall and axilla region can be imaged. MRI does not use Ionizing radiation and does not require compression. Although iodinated contrast agent is considered to be more hazardous than gadolinium contrast, the effects of gadolinium contrast agent accumulation on human health are controversial.[9] Although breast MRI is recommended as an imaging method in cases of dense breast, CEM has also performed well in this patient group.[7] Allergic reactions, extravasation and contrast nephropathy have rarely developed in patients given intravenous contrast agent for CEM. However, most side effects were mild and resolved spontaneously.

Our study has some limitations. No analysis was performed based on molecular characteristics (luminal, her2, basal like) to predict pathological complete response. We could not look at the effect of CEM for different histological subtypes because the study population included only 2 lobular cancer patients. MRI is considered the most accurate imaging tool in the diagnosis and staging of invasive lobular cancer. In a study conducted on a small number of patients with invasive lobular cancer, CEM showed similar performance to MRI.[18] Therefore, studies with a larger patient population are warranted regarding applicability in invasive lobular cancer patients and high-risk patients such as BRCA mutation.

This study showed that in patients receiving NAC, CEM was superior to MRI in predicting patients with pathological complete response and was at least as successful as MRI in patients with residual tumor. We find it more appropriate to use CEM instead of MRI, especially in patients who receive NAC. CEM is a reasonable option when MRI is unavailable or contraindicated. It even outperformed MRI with many of its features. We think that CEM will become more popular in the future.

ETHICAL APPROVAL The Health Sciences Ethics Committee approved this study of Manisa Celal Bayar University Faculty of Medicine with the decision dated 02/12/2021 and No. 227

PATIENT CONSENT: It is a prospective study and informed medical consent was obtained from all patients.

CONFLICT OF INTEREST: The authors declared no conflict of interest.

AUTHORS’ CONTRIBUTION: O.A, A.P.E., M.Ş, Ç.R.A, İ.Ş.Ö and F.E. collected the patient’s data, O.A. had done the statistical analysis and wrote the main manuscript text. All authors reviewed the manuscript.

DATA AVAILABILITY STATEMENT: The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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No competing interests reported.

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Comparison of contrast-enhanced mammography and breast magnetic resonance in the evaluation of response to neoadjuvant chemotherapy

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Abstract

INTRODUCTION

MATERIAL AND METHOD

STATISTICAL ANALYSIS

RESULTS

DISCUSSION

CONCLUSION

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References

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