Revista de Senología y Patología Mamaria 36 (2023) 100438

www.elsevier.es/senologia

ORIGINAL ARTICLE

Correlation between late gadolinium enhancement

sequences in MRI and pathologic response after
neoadjuvant chemotherapy in breast cancer
Gines Hernandez Cortes a, , Vicente Martinez de Vega b , Silvia Fuertes Cabero c ,
⁎

Margarita Rubio Alonso d , Lucia Gonzalez Cortijo e , Raquel Murillo Garcia f ,

Ricardo Sainz de la Cuesta Abbad a
a
Department of Obstetrics and Gynecology, Hospital Universitario Quironsalud, Madrid, Spain
b
Department of Breast Image Diagnosis, Hospital Universitario Quironsalud, Madrid, Spain
c
Department of Nuclear Medicine, Hospital Universitario Quironsalud, Madrid, Spain
d
Deparment of Epidemiology, European University of Madrid, Madrid, Spain
e
Department of Medical Oncology, Hospital Universitario Quironsalud, Madrid, Spain
f
Department of Pathology, Hospital Universitario Quironsalud, Madrid, Spain

Received 26 April 2022; accepted 11 September 2022

Available online 18 January 2023

KEYWORDS Abstract
Neoadjuvant Objectives: To study the correlation between radiologic response observed by late enhance-
chemotherapy; ment sequences in MRI and pathologic response after neoadjuvant chemotherapy in patients
Magnetic resonance with breast cancer.
imaging; Material and methods: Retrospective observational study of 132 patients with 136 tumors (4
Breast cancer; with bilateral disease), treated consecutively with neoadjuvant chemotherapy at our institution
Pathologic response; between 2011 and 2017. In all cases, we performed 3 breast MRI's, using late enhancement
Contrast enhancement gadolinium sequences: the first prior to neoadjuvant chemotherapy, the second half way
through treatment, and the third at the completion of therapy. Following treatment, contrast
medium uptake in tumor bed was evaluated based on the Response Evaluation Criteria for Solid
Tumors (RECIST).
All patients underwent conservative or radical surgery. We compared the radiologic response
estimated by MRI, with the pathologic response observed in the surgical specimen, according to
Miller and Payne grading system. We calculated the sensitivity, specificity, and predictive values
of the test, and used the Spearman correlation coefficient to stablish correlations between the
parameters analyzed.
Results: Complete pathologic response (pCR) was observed in 58.1% (79/136). The percentage
of global radio-pathologic correlation was 88.97%. MRI showed a sensitivity of 78.9%, a
specificity of 79.7%, a positive-predictive value (PPV) of 73.8% and a negative-predictive value

Corresponding author.
⁎
E-mail address: gines.hernandez@quironsalud.es (G.H. Cortes).

https://doi.org/10.1016/j.senol.2022.100438
0214-1582/n 2022 SESPM. Published by Elsevier España, S.L.U. All rights reserved.
 G.H. Cortes, V.M. de Vega, S.F. Cabero, et al.

(NPV) of 84%. In patients with partial response, the Spearman correlation was positive (rho = 1,
P < .001). According to surrogate subtypes of breast cancer, we observed moderate correlation
for luminal tumors (rho = 0.63, P < .001) and poor correlation for non-luminal types (rho = 0,4,
P < .01).
Conclusions: Breast MRI, using late enhancement sequences, accurately predicts tumor
response to neoadjuvant chemotherapy, especially in cases of partial response to therapy and
in luminal surrogate tumoral subtypes.
n 2022 SESPM. Published by Elsevier España, S.L.U. All rights reserved.

PALABRAS CLAVE Correlación entre secuencias de realce tardío de gadolinio en RM y respuesta

Quimioterapia patológica tras quimioterapia neoadyuvante en cáncer de mama
neoadyuvante;
Resonancia magnética; Resumen
Cáncer de mama; Objetivos: Estudiar la correlación entre la respuesta radiológica observada mediante secuencias
respuesta patológica; de realce tardío en resonancia magnética y la respuesta patológica después de quimioterapia
realce de contraste neoadyuvante en pacientes con cáncer de mama.
Material y métodos: Estudio observacional retrospectivo de 132 pacientes con 136 tumores
(cuatro con enfermedad bilateral), tratados consecutivamente con quimioterapia neoadyuvante
en nuestra Institución entre 2011 y 2017. En todos los casos se realizaron tres resonancias
magnéticas de mama, utilizando secuencias de realce tardío de gadolinio: la primera antes de la
quimioterapia neoadyuvante, la segunda a mitad del tratamiento y la tercera al finalizar la
terapia. Después del tratamiento, la captación media de contraste en el lecho tumoral se evaluó
en función de los Criterios de Evaluación de la Respuesta para Tumores Sólidos (RECIST).
Todas las pacientes se sometieron a cirugía conservadora o radical. Comparamos la respuesta
radiológica estimada por resonancia magnética, con la respuesta patológica observada en la
pieza quirúrgica, valorada según clasificación de Miller y Payne. Se calcularon sensibilidad,
especificidad, valores predictivos y correlacion de Spearman para establecer correlaciones
entre los parametros analizados.
Resultados: Se observó respuesta patológica completa (pCR) en el 58,1% (79/136). El porcentaje
de correlación radiopatológica global fue del 88,97%. La RM mostró una sensibilidad del 78,9%,
una especificidad del 79,7%, un valor predictivo positivo (VPP) del 73,8% y un valor predictivo
negativo (VAN) del 84%. En pacientes con respuesta parcial, la correlación de Spearman fue
positiva (rho = 1, p < 0,001). De acuerdo con los tipos subrogados de cáncer de mama,
observamos una correlación moderada para los tumores luminales (rho = 0,63, p < 0,001) y una
correlación deficiente para los tipos no luminales (rho = 0,4, p < 0,01).
Conclusiones: La resonancia magnética de mama, utilizando secuencias de realce tardío,
predice con precisión la respuesta del tumor a la quimioterapia neoadyuvante, especialmente en
casos de respuesta parcial y especialmente en subtipos luminales.
n 2022 SESPM. Publicado por Elsevier España, S.L.U. Todos los derechos reservados.

Introduction chemotherapy,6 we decided to estimate the predictive

capacity of this technique. This was performed by comparing
Currently, neoadjuvant chemotherapy is considered a first-line the correlation between the radiologic response observed in
treatment for specific breast cancers. Among the possible the pre-surgical MRI, using late enhancement sequences,7
benefits of this strategy, we can highlight the following: the and the pathologic response observed in the surgical
under-staging of the initial tumor, the achievement of a more specimen. Theoretically, because of the antiangiogenic
conservative surgery, and the verification of tumor chemo- activity attributed to anthracycline and taxane-based
sensitivity in vivo.1,2 This approach has also been used to treat chemotherapy schemes,8 the contrast medium used in the
initially operable cancers, but with a high probability of early MRI takes longer time to reach the tumor bed. This
systemic spread. Moreover, evaluation of tumor response in the potentially results in a more reliable determination of its
surgical specimen, allows a more effective estimation of risk of presence or absence in the initial tumor site, thus facilitat-
recurrence, especially in tumors that reach a pathologic ing surgical planning after neoadjuvant chemotherapy. The
complete response (pCR).3–5 goal of this study was to investigate the correlation of the
Given that MRI is superior to both mammography and radiologic tumor response to neoadjuvant chemotherapy,
ultrasound for the evaluation of tumor size and disease using late enhancement sequences in MRI, with the patho-
extension, as well as to the response to neoadjuvant logical response observed in the surgical specimen.

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 Revista de Senología y Patología Mamaria 36 (2023) 100438

Material and methods Metastatic workup and chemotherapy regimens

Study population and selection of patients To determine cancer spread prior to chemotherapy, all
patients underwent computed tomography of the chest,
We designed a retrospective observational study, including abdomen, and pelvis; a bone scan; an axillary ultrasound and
breast cancer patients who had received neoadjuvant a diffusion-weighted MRI of the breast. Patients with
chemotherapy at our institution between 2011 and 2017. A suspicious lymph nodes on ultrasound had a fine needle
total of 132 patients with 136 tumors (4 with bilateral aspiration biopsy (FNAB) performed.
disease of different histology) were enrolled. Patients with The medical treatment scheme was adjusted according to
breast MRI performed in another center or with follow-up surrogate cancer subtype, including anthracyclines, tax-
shorter than 7 months, were excluded from the study. anes, carboplatin,13 and trastuzumab. Other chemotherapy
regimens were also used based in ongoing clinical trials.

Data inclusion
MRI diagnosis
An encrypted database was designed to collect clinical and
pathologic data. Patients were restaged using the 8th We performed 3 breast MRI's: the first prior to neoadjuvant
edition of the TNM classification of the American Joint chemotherapy, the second half way through treatment, and
Committee on Cancer (AJCC).9 the third at the completion of therapy.
The studies were performed in decubitus prone position,
using a 3.0 Tesla device (General Electric Medical Sys-
Diagnosis tems®), sequences enhanced in T1 and T2 in sagittal plane
followed by diffusion sequence in axial plane. These were
The diagnosis was made using image-guided core needle followed by the dynamic study with 3D T1-enhanced
biopsy (CNB) or vacuum aspiration biopsy (VAB). The gradient echo sequences (Fast Spoiled Gradient Echo:
histopathological report included data on histologic type FSPGR) with fat suppression in the bilateral sagittal plane.
and grade according to the Nottingham Prognostic Index.10 Images were obtained before and after intravenous injection
Hormonal receptor status was informed according to the of gadopentate dimeglumine, using an automatic injector
Allred Scoring System.11 Immunohistochemistry was used to (Magnevist®), delivering 0.1 mmol/l per kg weight, followed
determine both the Ki-67 proliferation index score and the by a 20 ml bolus of saline solution to flush the intravenous
degree of Her-2/neu expression. Equivocal Her-2 cases were cannula, at an injection rate of 3 ml/s. Slice thicknesses of
clarified using FISH (Fluorescence In Situ Hybridization). 2.5–3 mm were used, depending on breast size, with an in-
Tumors were reassigned to one of the currently accepted plane resolution of 0.8*0.6 mm. Temporal resolution of 60 s
surrogate subtypes of breast cancers, equivalent to the was achieved per 3D sequence. A total of seven 3D
molecular types described by Perou.12 Namely, Luminal A sequences were acquired, the first without contrast medium
(positive hormonal receptors, negative Her-2/negative neu and and the following 6 after administration of the medium. The
Ki-67 < 15%), Luminal B Her-2 negative (positive hormonal total duration for the dynamic study was 7 min (Fig. 1).
receptors, Her-2/neu negative and Ki-67 ≥ 15%), Luminal B Finally, after the dynamic study, late enhancement was
Her-2 positive (positive hormonal receptors and positive Her-2/ performed in the axial plane (3D VIBRANT) with fat
neu), Triple negative (negative hormonal receptors and suppression, achieving a resolution of 0.5*0.5 mm, acquiring
negative Her-2/neu), and pure overexpressed Her-2/neu a slice thickness of 2 mm for subsequent study. Examinations
(negative hormonal receptors and positive Her-2/neu). were interpreted by radiologists with more than 10 years of

Fig. 1 Dynamic study MRI. A: Pretreatment. B: Intermediate. C: End of treatment.

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experience in breast MRI. The response was analyzed using Breast and axillary surgery
late enhancement sequences, obtaining images at 2, 6 and
10 min. (Fig. 2). This protocol is used just when evaluating Both the conservative and the radical surgery were carried
patients treated with neoadjuvant chemotherapy. out by breast surgeons with over 10 years of experience.
Following neoadjuvant therapy, contrast medium uptake Following our clinical guidelines,16 all patients with clini-
in tumor bed was evaluated based on the Response cally negative axilla on starting neoadjuvant chemotherapy,
Evaluation Criteria for Solid Tumors (RECIST),14 categorizing underwent sentinel lymph node biopsy (SLNB) always after
the response as: treatment. In cases with initial axillary involvement, a
Complete Radiologic Response (CRR): no uptake. standard lymphadenectomy was performed.
Partial Response divided in:
Major Partial Response (MAJPR): minor focal uptakes of
approx. 4 mm.
Pathologic response
Minor Partial Response (MINPR): focal uptake greater
than 4 mm. Pathologic response to treatment was determined by Miller
No response (NR): no response or progression. and Payne's grading system.17 This classification includes the
following categories:
G1: minimal changes without significant reduction in
Localization technique invasive tumor cellularity.
G2: discrete decrease in invasive cellularity, less than
Patients with clinically negative lymph nodes prior to 30% of tumor mass.
neoadjuvant chemotherapy, had the residual tumor bed G3: significant decrease in invasive cellularity, between
marked and the sentinel lymph node identified, 24 h prior to 30% and 90% of the tumor mass.
surgery. MRI-guided Radioguided Occult Lesion Localization/ G4: marked decrease in invasive cellularity, greater than
Sentinel Node Occult Lesion Localization (ROLL/SNOLL) 90% of tumor mass.
techniques, previously described by our group,15 were used. G5: absence of invasive cellularity.

Fig. 2 Late enhancement study MRI.

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So, this classification considers pCR only when there was

Table 1 Clinical and pathological characteristics.
absence of infiltrating disease, allowing “in situ” disease.
Characteristics
Treatment and follow-up Age at diagnosis. Median (Interquartile 47 (42–56) years
range)
All patients treated with breast conservative surgery Family history of breast cancer
received post-operative radiotherapy. In addition, adjuvant Yes 46.3%
hormone therapy was prescribed to all hormone-dependent No 53.7%
tumors; as well trastuzumab for 1 year to Her-2/neu positive Tumoral size. Median 20.5 (14–28) mm
cancers. (Interquartile range)
Our follow-up protocol consisted in 3 months check-ups
during the first year, every 6-months for the following 4 Histological subtypes
years, and annually from then after, including annual breast Infiltrating ductal 131 (96.3%)
imaging studies. Infiltrating lobulillar 5 (3.7%)
The study was closed February 2020.
Surrogate subtypes
Luminal A 4 (2,9%)
Statistical analysis Her2 negative-luminal B 47 (34,6%)
Triple negative 34 (25%)
Patients' characteristics were determined by a descriptive Overexpressed Her2 17 (12.5%)
statistical study and they were classified according to the Her2 positive-luminal B 34 (25%)
surrogate subtype of the tumor. Frequencies were expressed
as absolute numbers and percentages for qualitative Stages
variables. Data corresponding to quantitative variables, Stage IIIA 4 (2.9%)
were summarized as means ± standard deviation, if they Stage IIIB 4 (2.9%)
followed a normal distribution; and median and interquartile Stage IIIC 5 (3.8%)
range, for variables with non-normal distributions. The Stage IV 3 (2.2%)
Kolmogorov–Smirnov test was applied to check for normal-
ity. Qualitative variables were compared using Pearson's χ2
cases showed a very important response to treatment. When
test. The variables analyzed correspond to the clinical and
analyzing the G5 response in relation to surrogate marker
pathological characteristics of the patients in the study, as
types, we found that tumors with overexpression of pure
well as the percentages of response obtained after neoad-
Her-2/neu disappeared in 94.1% of cases, triple negatives in
juvant chemotherapy of the different surrogate subtypes.
82.4%, Her-2 positive Luminal B in 55.9%, Her-2 negative
Percentage of global radio-pathologic concordance, were
Luminal B in 31.9%, and Luminal A in 25%. The differences in
calculated including all patients of the study, in addition to
the response rates obtained reached statistical significance
sensitivity, specificity, positive-predictive value (PPV), and
(P < .05).
negative-predictive value (NPV). Spearman's correlation
Concerning tumor bed assessment, CRR was observed in
coefficient was used to analyze the correlation between
75 tumors (55.1%), MAJPR in 51 (37.5%), MINPR in 9 (6.6%)
residual tumor size variable, found in the surgical specimen
and NR in 1 tumor (0.7%).
and the one observed by MRI. Given that the variables did
Considering pathologic response, we obtained the fol-
not follow a normal distribution, we used Spearman's rho,
lowing radiologic response results: sensitivity 78.9%, speci-
instead of Pearson's correlation coefficient.
ficity 79.7%, PPV 73.8%, and NPV 84%. The MRI
P-values lower than .05 were considered as statistically
underestimated the residual lesion in 9 cases (6.6%) and
significant.
overestimated in 6 (4.4%). We found a correct radio-
Statistical analysis was performed using the software
pathologic correlation in 88.97% of cases.
SPSS version 21 for Windows (IBM Corporation, Chicago, IL,
In the subgroup of patients with a partial response,
USA).
Spearman's correlation coefficient was used to calculate and
compare the residual tumor size observed in the pathology
Results specimen with that observed in the post-chemotherapy MRI.
Spearman's correlation was lineal and positive (rho = 1,
Table 1 summarizes the principal clinic-pathologic charac- P < .001) (Fig. 3). Analyzing it by surrogate subtypes, the
teristics of our patients. Most tumors corresponded to early coefficient reflected a moderate correlation for the luminal
stages (88.2%). Table 2 summarizes the chemotherapy cancers (rho = 0.63, P < .001); and a poor correlation for the
regimens used, the type of surgery performed and the pre- non-luminal types (rho = 0.4, P < .01).
surgical axillary status. Finally, the majority of patients had When analyzing the 15 discordant cases, different
tumors with luminal phenotypes (62.5%). The median follow- responses were observed in the pre-surgical MRI compared
up was 50 months (37–61). to the final pathology. Ten (46.7%) corresponded to luminal
We observed a G5, pathologic response after neoadjuvant tumors and the MRI overestimated the response in the
therapy (absence of invasive cellularity), in 58.1% of cases, majority of these cases (6). However, in 2 triple-negative
and a G4 response (marked decrease in invasive cellularity, tumors and in 3 pure Her-2 positive cancers, the MRI
greater than 90% of tumor mass), in 20.6%; hence 78.7% of underestimated the response.

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First, a clinical feature to highlight in our study is the high

Table 2 CT regimen, surgery, preCT axillary status.
pCR rate (58.1%) observed. This value is slightly higher
Chemotherapy regimen compared to other similar studies observed in the literature,
AC-T 55 (40.4%) ranging between 12% and 52%.19–21 This could partly be due
AC-T-Trastuzumab 45 (33.1%) to the way of evaluating response that differs among the
AC-T-Carboplatin 28 (20.6%) different studies. Not everyone uses Miller and Payne
T-Carboplatin 1 (0.7%) grading system that classifies a G5 response as an absence
Clinical trial scheme 7 (5.1%) of infiltrating component but allows the presence of in situ
carcinoma. In addition, we believe that the systematic use
Surgery type of targeted treatment in tumors overexpressing Her-2/neu,
Conservative 89 (65.4%) and the addition of carboplatin in cases of triple-negative
Radical 47 (34.6%) tumors, probably contributed to reach this high pCR rate.
Another factor that may have increased our percentage of
PreCT axillary status
pCR were our indications for neoadjuvant chemotherapy,
Positive 44 (32.35%)
based mainly on surrogate subtype and axillary status,
Negative 92 (67.65%)
resulting in more than 50% of our cases corresponding to
CT: chemotherapy. initial stages.
Overall, the values of sensitivity, specificity, PPV, and
NPV we obtained are within the ranges published in the
Only 3 patients had positive margins (2.2%) after
systematic review by Lobbes et al.6
conservative surgery and none required mastectomy. They
With a similar casuistic to our study, Weber et al.22 report
all underwent a re-operation to expand margins.
a PPV of 63.4% and a NPV of 84.1%, although these authors
consider a pCR as the absence of both an infiltrating
component and in situ carcinoma. This, once again,
Discussion introduces a differential factor between their study and
ours, given that the definition we used for pCR, according to
In this study, we investigated the predictive capacity of MRI the Miller and Payne grading system permits the presence of
using late gadolinium enhancement MRI sequences7 and in situ carcinoma.
pathologic response evaluation. An excellent correlation is Choi et al.23 use a software designed to estimate residual
observed between the residual tumor size after neoadju- tumor volume to distinguish between the pCR group and
vant chemotherapy measured in MRI and the size measured those with partial response, with sensitivity and specificity
in the surgical specimen, which allows a better estimate of values of 77.3 and 95%, respectively. This same group also
the real response obtained, and, therefore, a greater published a good radio-pathologic correlation using the
precision in the surgical design. So, our results suggest that Residual Cancer Burden Index (RCB).24 Comparatively, in
the use of late sequences in pre-surgical MRI is a useful our study, we obtain lower values of specificity and similar
tool to evaluate tumor response following neoadjuvant sensitivity, bearing in mind that pathologic responses were
chemotherapy. evaluated using different scales.
Previously, our group had performed a preliminary small Second, and from our perspective, the most important
size pilot study, analyzing late enhancement sequences for a finding in our study was the results obtained using Spearman
cohort of breast cancer patients treated with neoadjuvant rho analysis for cases with incomplete pCR. These presented
chemotherapy. In this series, we obtained a NPV of 100%.18 a lineal curve, reaching a statistically significant correlation
In the light of these promising results, in this study, we between residual tumor sizes in the pre-surgical MRI and in
included a larger number of patients and all surrogate breast the surgical specimen (Fig. 3). Therefore, in our experience
cancer subtypes. and in patients with partial pathologic response, late
enhancement sequences MRI accurately predicts the resid-
ual tumor size in breast cancer patients, following chemo-
therapy. This may be an important factor to avoid positive
margins in patients undergoing conservative surgery. In fact,
we only observed a 2.2% of affected margins in this series. As
we can see in Fig. 2 compared to Fig. 1 (both from the same
patient), the fact of obtaining late enhancement sequences
allows to avoid a false assessment of complete response by
image if only the dynamic study had been taken into
account, visualizing gadolinium enhancement in the images
obtained at 6 and 10 min.
When analyzing the RR in the different surrogate tumor
subtypes, we found that the luminal subtypes, had a
moderate but statistically significant correlation, which
was slightly higher than that reported by other authors.25
We should also take into account that these tumor subtypes
usually have a higher percentage of partial responses.
Fig. 3 Spearman's correlation in partial response subgroup. Therefore, MRI with late enhancement sequences, has a

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