Indian Journal of Surgical Oncology

https://doi.org/10.1007/s13193-025-02282-z

ORIGINAL ARTICLE

Landscape and Immuno‑Molecular Phenotyping of 301 Eastern

Indian Breast Carcinoma Cases– A Comparative Assessment of TNBC
Incidence
Amit Roy‑Chowdhury1,5,6 · Somya Saswati Swain2 · Ghanashyam Biswas3 · Dilip Kar4 ·
Sandip Kumar Mohanty2 · Birendranath Banerjee5,6

Received: 29 January 2025 / Revised: 19 March 2025 / Accepted: 21 March 2025

© The Author(s), under exclusive licence to Indian Association of Surgical Oncology 2025

Abstract

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In the 2022–2024 Globocan data, India alone contributed 15.5% (1.4 million) of the staggering 23.8% of breast carcinoma
(BC) cases globally and in the lot 0.85 million people succumbed to the disease. BC remains a complex and multifaceted
disease that poses a significant threat and is a public health concern. Region-specific molecular subtyping is required with

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the updating trends of the disease. The study was conducted retrospectively at the Central Reference Laboratory, inDNA
Life Sciences, Bhubaneswar, Odisha, from January 2021 to December 2023. A total of 301 BC patients were recruited in
the study from multiple institutions in a consecutive manner across West-Bengal and Odisha. Statistical analysis was per-

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formed using GraphPad Prism (version 8.3.0) software. The study included 294 (97.6%) women and 7 (2.3%) men. Invasive
ductal carcinoma (IDC) was the most common histopathologic type observed in 90.2% (n = 267) of patients. Majority of
them were diagnosed in the 4th to 6th decade of their life (n = 173; 58.45%) with a mean age of 50.8 years. ER + expression
was detected in 104 (35.1%) and PR + in 87 (29.4%) cases. HER-2/neu overexpression was observed in 89 (30.1%) cases. A

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striking 39.8% (n = 118) triple-negative or basal-like status was noted in the cohort. Immunohistochemistry-based classifica-
tion remains the gold-standard method for sub-typing of BC. The study highlights alarming numbers of TNBC cases and is

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the most prevalent sub-group in the 40–60 years age-group of eastern-Indian BC cases in comparison with region-specific
incidence. Additionally, concurrent use of HER2/neu FISH on equivocal cases revealed a HER2/neu positivity conversion
rate of 28%. Apart from studying the routine histo-molecular attributes, BRCA-based genetic screening needs to be brought

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into the mainstream testing for all clinically diagnosed BC cases.

* Birendranath Banerjee F o
Keywords Breast cancer · ER · PR · HER2/neu · FISH · Molecular typing · Immunohistochemistry · TNBC

Introduction
[email protected]; [email protected]
1
According to the recent 2022–2024 published data from
Molecular Stress and Stem Cell Biology Group, School
the Global Cancer Observatory, breast cancer (BC) is the
of Biotechnology, KIIT University, Bhubaneswar,
Odisha 751024, India most contributory malignancy in women globally with
2 23.8% of the reported over 9 million new cases [1]. India
Department of Histopathology, inDNA Life Sciences Private
Limited, Bhubaneswar, Odisha 751024, India alone contributed 15.5% of these cases with a stagger-
3 ing 26% of BC cases in the lot and 0.85 million people
Department of Oncology, Sparsh Hospitals, Bhubaneswar,
Odisha 751007, India succumbed to the disease. Also, according to predictions
4 from the International Agency for Research on Cancer
Department of Surgical Oncology, Utkal Hospital,
Bhubaneswar, Odisha 751021, India (IARC), the cancer burden is expected to rise from 01
5 million new cases in 2012 to over 1.7 million by 2035 [2].
inDNA Centre for Research and Innovation in Molecular
Diagnostics, inDNA Life Sciences Private Limited, As per the recent reports, India has emerged as the global
Bhubaneswar, Odisha 751024, India hub for cancer with lung and breast carcinoma taking the
6
JBS Haldane Centre of Molecular Medicine, Silicon top-spots. Also, as per the National Cancer Registry Pro-
University, Bhubaneswar, Odisha 751024, India gram, by the year 2003, BC had taken over as the leading

Vol.:(0123456789)
 Indian Journal of Surgical Oncology

cancer in India, surpassing carcinoma cervix. A signifi- Luminal BCs are a subtype of ER-positive tumors,
cant increasing trend was observed in Bhopal, Chennai accounting for approximately 60% of all BC cases in West-
and Delhi registries [3], while the current study focuses ern populations [9]. The enriched HER2 BC subtype con-
on the BC spectrum in the eastern region of the country. stitutes approximately 15% of cases and is identified by ele-
To note, the 5-year disease-free survival is < 60% in our vated expression of the HER2 receptor coupled with a lack
country which is remarkably low than the global scenario of estrogen and PR expression [10]. TNBC is a heterogene-
of > 95% [4], highlighting the need of special attention in ous group of breast tumors that lack expression of estrogen
the detection, understanding, management and treatment receptor (ER), progesterone receptor (PR) and HER2. This
strategies for the Indian BC patients. subtype accounts for approximately 15–20% of all BC cases
BC is characterized by its intricate clinical manifesta- and is more prevalent in younger women and individuals of
tions, molecular underpinnings and diverse treatment out- African American descent [11].
comes. Although there are well-defined treatment methods A recent study by Tittmann et al. revealed that HR + /
and protocols for different BC subtypes like hormone recep- HER2 − tumors are most prevalent in women over 60 years,
tor–positive (HR +) subtype, the triple-negative breast can- while women under 40 years have the lowest frequency of
cers (TNBC) do not have similar effective therapy options this subtype [12]. On the contrary, the proportion of TNBC
and, with the increasing incidence of BC in the country, subtype is found to be higher in younger BC patients than
the disease remains a significant public health concern [5].
In recent years, the field of BC research has witnessed a
remarkable shift, with the emergence of personalized risk-
based approaches that aim to optimize screening, preven-
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older [13]. The response to therapies and prognosis of BC
are influenced by the molecular subtype. Therefore, it is
essential to take into account both age and molecular sub-
type while screening and preventing BC. The present study
tion and treatment strategies [6]. Conventional histological
variables, such as the size of the tumor, the involvement of
lymph nodes, the kind and grade of the tumor, the invasion
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focuses on characterizing the BC molecular profile among

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301 Eastern Indian patients and draw comparison among
different geographical regions.
of lymphatic and blood vessels and the presence of immune
cell infiltration, are important indicators for predicting the
prognosis [7]. Ultimately, morphological analysis remains
the foundation of BC clinical decision-making. Molecular
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Material and Methods

subtyping is an essential and crucial technique for the man-

agement of BC. Histomorphology and immunohistochemis-
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A retrospective study was conducted at Central Reference
Laboratory, inDNA Life Sciences, Bhubaneswar, Odisha,

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try (IHC) is capable of distinguishing the five BC subtypes
by evaluating hormone receptors (HRs), human epidermal
growth factor receptor 2 (HER2) expression and prolifera-

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tion index biomarker [8]. The globally estimated incidence
from January 2021 to December 2023. A total of 301 BC
patients were recruited in the study from multiple institu-
tions in a consecutive manner across West-Bengal and Odi-
sha. Both surgically resected tissue specimens and available

Fig. 1  Global spectrum of

molecular subtypes of breast
carcinoma F o
rates for these subtypes are summarized in Fig. 1. formalin-fixed paraffin-embedded (FFPE) tissue specimens
Indian Journal of Surgical Oncology

were received for characterization and analysis. Clinical values were calculated as necessary. A p-value less than 0.05
records and a signed informed consent were collected from was deemed to be statistically significant.
each participating patient separately.

Histopathological Analysis Results

Laboratory standardized routine haematoxylin and eosin The study included a cohort of 301 patients diagnosed with
staining (H&E) methodology was opted as standard practice BC, consisting of 294 (97.6%) women and 7 (2.3%) men.
to visualize and characterize the prepared/collected FFPE Five cases (1.66%) were dropped from further characteriza-
tissue block samples. A nationally accredited histopatholo- tion and analysis due to pre-analytical error in tissue fixation
gist assisted with the analysis and staging of cancer samples and processing (Fig. 2). In the rest of the patient cohort of
following ASCO-CAP and AJCC staging 8th edition guide- 296 cases, majority of them were diagnosed in the 4th to
lines [14, 15]. Histopathological parameters were noted 6th decade of their life (n = 173; 58.45%) with a mean age
individually and an appropriate tissue block was selected of 50.8 years. Among females, 134 (45.3%) were postmeno-
for further examinations. pausal. The mean clinical tumor size for the available cases
(n = 152) was 3.56 cm, with 56.2% (n = 167) of the patients
Immunohistochemistry Analysis

The ER, PR, HER2/neu and Ki67 immunohistochemical

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belonging to the Nottingham clinical grade II, followed by
28.72% grade III (n = 85) and 14.86% grade I (n = 44). The
majority of the patients in study cohort were assessed with
MRM specimen (n = 133; 44.93%) with similar values for
staining results were evaluated using specific clones (EP1,
EP2, EP3 and MIB-1 respectively) (PathnSitu Biotechnolo-
gies, Pleasanton, CA, USA). The ALLRED scoring system

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Tru-cut biopsy (n = 127; 42.91%) while only 12.16% (n = 36)
were other biopsy types (lumpectomy, BCS and others).
IDC was the most common histopathologic type observed
was utilized to assess the expression of ER and PR. This sys-
tem takes into account both the proportion of positive cells
and the intensity of staining in those cells. The intensity is
graded on a scale of 0 (no staining) to 3 (strong staining)
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in 90.2% (n = 267) of patients, 1.4% (n = 4) invasive lobular
carcinoma, 1.0% (n = 3) ductal carcinoma in situ (DCIS),
2.0% (n = 6) metaplastic carcinoma and 5.4% (n = 16) cat-
egorized as Others (adenocarcinoma, squamous cell, micro-
[16]. A combined score of less than 2 is classified as negative,
while a score greater than 2 is considered positive. The Her2/
neu immunostaining results were interpreted based on the p
papillary, mixed and mucinous type) (Fig. 3).
Age-grouped correlation with distribution of histo-

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updated ASCO-CAP, 2018 guidelines. A score of 0/1 + was
classified as negative, a score of 2 + was considered intermedi-

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ate or equivocal and a score of 3 + was judged positive.
pathological case findings represents IDC to be the most
predominant carcinoma types across age-groups, while
incidence of IDC cases was similar in the age group < 40
and > 60 years, whereas no statistically significant varia-

HER2/neu FISH Analysis

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Fluorescence in situ hybridization (FISH) was performed
using XL ERBB2 (HER2/neu) amp Amplification Probe Kit,
tion in overall distribution was noted across age-groups
(p 0.326). The most prevalent pathological nodal stage in
the cohort was N0 (42.1%) followed by N1 (30.3%), N2
(18.6%) and N3 (9.0%) with a mean lymph node involve-
ment of 5.88 in N1, N2 and N3 subgroups. Lymphovas-
a dual probe assay (MetaSystems Probes GmbH, Germany). cular invasion (LVI) was seen in 47.4% of patients and
The MetaSystems ERBB2 Probe Kit has been designed to perineural invasion (PNI) in 18.9%. Only 3 cases (1.10%)
detect amplification of the HER-2/neu gene (17q12) using of bilateral breast carcinoma were noted, while almost
formalin-fixed, paraffin-embedded (FFPE) human tissue equal proportions of left (n = 136; 47.7%) and right later-
specimens. HER-2/neu scoring was done as per updated ality (n = 146; 51.2%) were observed in the patient cohort
ASCO/CAP guidelines, 2018 [17]. (Supplementary Table 1).

Statistical Analysis Immunohistochemical Profile

Clinicopathologic characteristics and age comparative cor- Positive ER expression was detected in 104 (35.1%) and PR
relation were calculated using non-parametric one-way positivity in 87 (29.4%) cases. Representative IHC expres-
ANOVA (analysis of variance) test for categorical variables. sion profile for the individual biomarkers on fixed cancer
The data was recorded and analyzed using GraphPad Prism tissue specimens is presented in Fig. 4.
(version 8.3.0) statistical software. Mean and percentage
 Indian Journal of Surgical Oncology

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Fig. 2  Segregation of recruited BC patients according to gender, histopathological type and Nottingham grade

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Fig. 3  Representative H & E–
stained images (40 ×) of histo-
pathological sub-types of breast
carcinoma cases from the cohort

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HER-2/neu overexpression was observed in 82 (27.7%) Proliferation index was evaluated with Ki67 (MiB1)
cases, while 25 (8.4%) cases were found with equivocal clone. A total of 109 (53.9%) cases presented with a
(2 +) expression. HER2/neu FISH confirmed 7 more cases Ki67 index of < 30% while 93 (46.1%) presented with
to be FISH positive and added to the final HER2-positive Ki67 > 30% in the patient cohort.
tally of 89 (30.1%) (Fig. 5).
Indian Journal of Surgical Oncology

Fig. 4  Representative IHC-

stained images (40 ×) of
biomarker expression in breast
carcinoma cases from the cohort

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Fig. 5  HER2/neu FISH confirmation of the HER2/neu IHC equivocal cases

Comparative Analysis of Biomarker Landscape 2021 International expert consensus. 28.4% (n = 84)
and TNBC Incidence of Breast Carcinoma Case’s cases belonged to Luminal-A, while 9.5% (n = 28) rep-
Across Indian Studies resented Luminal-B subtype, whereas 22.3% (n = 66)
cases were noted to be of HER2-enriched type. A strik-
Molecular Typing (St. Gallen, 2021 Consensus) ing 39.8% (n = 118) triple-negative or basal-like status
was noted in the current study cohort (Supplementary
Based on IHC profile, the cases were classified into four Table ​2 ).
distinct molecular sub-types as per St. Gallen/Vienna,
 Indian Journal of Surgical Oncology

Discussion As per the available literatures, the reported rate of BCS in

Indian studies has been approximately 20% [23]. Only 3.4% of
As per reports, India is the declared cancer capital of the current patient cohort had undergone BCS as a therapeutic
the world with staggering and rising figures of newly option. This can be attributed to factors such as limited patient
diagnosed cases every year and BC is playing a pivotal awareness and acceptance, socio-economic stress, inadequate
role in swelling up the numbers. The primary manage- infrastructure and lack of access to radiation facilities. These
ment of the disease has been surgery while adjuvant factors have also been emphasized in other Indian studies as
therapy has been tailored to the molecular phenotypes contributing to the low rate of BCS among Indian patients,
of the tumor [18]. This has led to a gradual decline in and this situation appears to persist [24].
mortality and improvement in OS. India is predominantly Molecular typing of cohort revealed the combined
being detected as the hub of young BC patients with a Luminal-A and Normal-like positivity to be 28.4% which
median age of < 50 years [8]. Similar to the numbers, is significantly lower than the globally projected numbers
the majority of the patients in this study presented in (Supplementary Fig. 6). Also, 9.5% of Luminal-B molecu-
the mid-age (40–60 years) group with more than 50% lar sub-type was noted which is again half of the expected
(n = 162) were premenopausal in the cohort. Similar to range. Other studies from India have also reported pre-
reported studies, IDC was the most prevalent type in the viously similar findings [25]. HER2/neu-enriched type
cohort (90.2%) across age-groups [19]. No significant
difference was noted in breast laterality involvement.
In the current study, 28.37% of patients presented with

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of BC cases were marginally higher (22.3%) in the cur-
rent cohort, while HER2/neu positivity rates of 20–50%
have been reported by various Indian researchers [26]. A
remarkably high basal-like/triple-negative type cases were

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locally advanced BC phenotype with involvement of the
axillary lymph nodes with a mean of 5.88 and majority noted (39.8%), which is nearly double the number seen
of them having N1 sub-type. Mean tumor size of 3.56 cm
was noted across the cohort with available clinico-histo-
pathological parameters with majority of patients belong-
ing to T1 and T2 subtype (n = 134). Based on the site of
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in other parts of the world and was comparable to other
Indian studies [27]. Indian population is also reported to
have early age of TNBC detection [28]. The mean age of
diagnosis of TNBC sub-type in the present cohort was
tumor, outer quadrant region of the mammary gland was
found to be the most involved (43.0%) followed by inner
quadrant (27.0%) and central region (21.2%). Paget’s
disease of breast is a rare histological type, representing
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50.2 years with median age of 50 years, signifying the
high prevalence of mid-age high-grade BC patients in the
cohort. Advanced molecular genetic studies targeting pri-
marily BRCA- and HRR-associated pathway genes are a

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only 1–3% of female breast cancers, while the current
study cohort presented 8.8% cases with the disease [20].
Nearly, 8.0% of the tumors were found to be multifocal
with mean tumor foci of 2.2. Age-dependent distribution
must to personalize targeted treatment and also to identify
the high-risk families carrying a clinically relevant patho-
genic/likely pathogenic gene variants for estimating and
strategizing the familial risk for other members. Several,

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of overall histological grade showed a weak significance
(p value 0.039) with dominance of high-grade tumors

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including 28.7% (n = 85) of grade III tumors. The cohort
also presented 3 patients with high-grade (III), bilateral
carcinoma of the breast. An elevated frequency of HER-2
targeted therapies like PARPi have been approved by the
US-FDA for the same but the correct, timely and seamless
identification of these gene mutation harbouring families
is the challenge in the eastern part of India. Apart from
routine histo-molecular subtyping, BRCA-based genetic
receptor overexpression, along with a high prevalence screening needs to be brought into the mainstream testing
of the triple-negative BC phenotype, is indicative of an for all clinically diagnosed BC cases.
unfavourable prognosis [21]. Likewise, those who are Although the current study was conducted using clas-
young to middle-aged when diagnosed, have not yet sical BC prognostic IHC and FISH biomarkers with ALL-
reached menopause, are at an advanced stage of the RED and ASCO-CAP (2018) guidelines, the interpreta-
disease, do not express hormone receptors and have an tion is still observer dependent for expression analysis and
overexpression of HER-2 are known to have a negative specifically does not highlight the HER-2 low positivity as
clinical prognosis. Furthermore, NCCN guideline recom- highlighted in the DESTINY-Breast04 trial. It can be sug-
mends recurrence prediction scoring for HR + , HER2/ gested that study from a larger cohort of patients will reit-
neu- BC subtypes which is routinely practiced in the clin- erate the occurrence and classification in a much explicit
ics with various available methods [22]. manner. The study findings are also limited to routine BC
biomarker analysis.
Indian Journal of Surgical Oncology

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of high-grade basal like/TNBC subtype in the eastern Indian therapy. Expert Rev Mol Diagn 18(3):227–243
BC patients as compared with the reported numbers from 8. Gogia A et al (2019) Clinicopathologic characteristics and treatment
outcomes of patients with up-front metastatic BC: single-center
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BC type in the cohort across age-groups. Also, incidentally, subtypes of BCs. Cancer Biol Ther 10(10):955–60
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Acknowledgements The authors would like to thank all the patients
who participated in this study. Also, we would like to acknowledge
inDNA Life Sciences for providing the advanced laboratory facili-
ties for conducting the experiments. The authors would also like to
acknowledge the technical support provided by Mr. Prasanjit Behera,
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staging system for bc, eighth edition: summary for clinicians. Eur J
Breast Health 17(3):234–238
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16. Ahmad Fauzi MF, Wan Ahmad WSHM, Jamaluddin MF, Lee JTH,
Khor SY, Looi LM, Abas FS, Aldahoul N (2022) Allred Scoring of
Funding The Work was supported by the intramural Research fund
ER-IHC Stained Whole-Slide Images for Hormone Receptor Status

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of Department of Research and Development, inDNA Life Sciences
in Breast Carcinoma. Diagnostics (Basel). 12(12):3093. https://​doi.​
Pvt. Ltd., which is a DSIR (Department of Scientific and Industrial
org/​10.​3390/​diagn​ostic​s1212​3093
Research) Government of India–accredited organization.

Data Availability All the relevant patient information and data will be
made available upon a reasonable written request to the correspond-
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17. Gordian-Arroyo AM, Zynger DL, Tozbikian GH (2019) Impact of
the 2018 ASCO/CAP HER2 guideline focused update. American
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Ethical Declarations The study was conducted abiding by the Helsinki

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and clinical relevance. Clin Med Insights Pathol. 21(8):23–31.
guidelines, 2013. Also, the study was reviewed and approved by inde- https://​doi.​org/​10.​4137/​CPath.​S31563.​PMID:​26740​749;​PMCID:​
pendent Institutional Review Board (IRB) of inDNA Life Sciences, PMC46​89326

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