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DOI:10.31557/APJCP.2019.20.8.

2247
Luminal B is the Most Common Intrinsic Molecular Subtypes of Breast Carcinoma

RESEARCH ARTICLE Editorial Process: Submission:04/27/2018 Acceptance:08/04/2019

Luminal B is the Most Common Intrinsic Molecular Subtypes of


Invasive Ductal Breast Carcinoma Patients in East Kalimantan,
Indonesia
Swandari Paramita1,2*, Eko Nugroho Raharjo3, Maria Niasari3, Fieska Azizah4,
Nur Ahlina Hanifah4
Abstract
Objective: Breast carcinoma has no longer been considered as a single and standalone disease. Its subtypes have
been known to vary in terms of risk factors, natural histories, and responses to therapies. In particular, intrinsic molecular
subtypes based on St. Gallen International Expert Consensus 2013 have classified breast carcinoma into luminal A,
luminal B, HER2+, and triple-negative, depending on the expression of ER, PgR, HER2, and Ki-67. Research on
intrinsic molecular subtypes of breast carcinoma in Indonesia, however, are rarely conducted, which then triggers
the intention to conduct this study. Methods: In this work, a retrospective study was conducted on 92 formalin-fixed
paraffin-embedded samples of invasive ductal breast carcinoma patients. These samples were from patients at Abdul
Wahab Sjahranie County General Hospital Samarinda, East Kalimantan, Indonesia, in 2016. Next, immunohistochemical
staining using anti-ER, PgR, HER2, and Ki-67 antibodies was applied to classify intrinsic molecular subtypes. Then, an
association between clinical and immunohistochemical factors with intrinsic molecular subtypes of breast carcinoma
were analyzed using Chi-square test. Results: Looking at results of the retrospective study, luminal B was discovered as
the most common intrinsic molecular subtypes of breast carcinoma (42.39%) in East Kalimantan, Indonesia. The next
ranks of breast carcinoma subtypes in the region included HER2+ (39.13%), triple-negative (10.87%), and luminal A
(7.61%). In fact, there was a significant association between age (p = 0.019) with intrinsic molecular subtypes of breast
carcinoma. Conclusion: The study found luminal B as the most common intrinsic molecular subtypes of Indonesian
breast carcinoma in the region under investigation. In the future, the higher positivity rate of luminal B in breast
carcinoma patients compared to prior studies would require further investigations.

Keywords: Luminal B- intrinsic molecular subtypes- breast carcinoma

Asian Pac J Cancer Prev, 20 (8), 2247-2252

Introduction In current advances, breast carcinoma has been


posited a heterogeneous disease. In other words, it has
Currently, breast carcinoma has been recognized as the no longer been considered as a single and standalone
world’s most commonly occuring cancer type. It has been one. Breast carcinoma subtypes can be determined by
estimated to cause deaths of over 500,000 women annually applying immunohistochemistry methods. These subtypes
all around the world. Besides, estimated 1.7 million cases have been known to vary in terms of risk factors, natural
of breast carcinoma are diagnosed every year (DeSantis et histories, and responses to therapies (Goldhirsch et al.,
al., 2014). In fact, almost a quarter of breast carcinoma are 2011). In 2013, St. Gallen International Expert Consensus
diagnosed in Asia-Pacific regions, in which Indonesia is in on the Primary Therapy of Early Breast Cancer has
third place. Among globally estimated 500,000 deaths of determined a classification of intrinsic molecular subtypes
females annually, about 22% deaths occur throughout the of breast carcinoma based of their clinicopathologic
Asia-Pacific region. Ranking third in the region, Indonesia surrogate definitions. The classification includes luminal
accounted for 17% of breast carcinoma deaths in second A, luminal B, HER2+, and triple-negative (Goldhirsch
place after China. Breast carcinoma has also estimated to et al., 2013).
account for 9% of cancer-related deaths among females In general, each subtypes group is characterized as
in the Asia-Pacific, ranking fourth behind lung, liver, and having different prognosis and response to therapy (Tao
stomach cancers (Youlden et al., 2014). et al., 2015). Luminal A particularly has a smaller tumor

1
Department of Community Medicine, 4Medical Doctor Program,Faculty of Medicine, 2Research Center of MCTrops, Mulawarman
University, 3Department of Pathological Anatomy, Abdul Wahab Sjahranie General County Hospital, Samarinda, East Kalimantan,
Indonesia. *For Correspondence: s.paramita@fk.unmul.ac.id
Asian Pacific Journal of Cancer Prevention, Vol 20 2247
Swandari Paramita et al

size, the best prognosis and the lowest recurrence rate than (Wolff et al., 2013). Then, tumors containing ≥ 14% of
other subtypes. Technically, it is characterized by higher nuclear Ki-67 expression was considered as having a high
levels of ER and lower levels of the proliferation-related Ki-67 rate (Cheang et al., 2009).
genes, including Ki-67. In practices, recommendations
for luminal A are mainly based on endocrine therapy Definition of intrinsic molecular subtypes
(Prat et al., 2013). Furthermore, Luminal B has an According to the 2013 St. Gallen Consensus, samples
aggressive phenotype and worse prognosis compared could be distinguished based on their ER, PgR, HER2,
to luminal A. It is characterized by higher levels of and Ki-67 expressions. Technically speaking, samples
growth factor receptor such as HER2, which activates were stated as luminal A (ER+, PgR+, HER2-, and Ki-67
signaling pathways (Yan et al., 2015). In details, HER2+ low), luminal B (ER+, PgR+, any HER2, and any Ki-67),
subtypes have a poor prognosis, and characterized by HER2+ (ER-, PgR-, and HER2 over-expressed) or triple
high proliferation rates. Therapy for luminal B subtype negative (ER-, PgR-, and HER2-) (Goldhirsch et al., 2013).
includes the uses of anti-HER2 such as Trastuzumab. In
terms of recommended therapies, luminal B delivers its Statistical analysis
best responses to neoadjuvant chemotherapy (Asif et al., In this study, a chi-square test was employed to examine
2016). Moreover, the triple-negative subtype has been the association of breast carcinoma intrinsic molecular
recognized to show the most aggressive behavior with subtypes with clinical and immunohistochemical factors.
the worst outcome. This subtype is not responding well The test applied values of p < 0.05 as considerably
to either endocrine or adjuvant chemotherapy. Requiring significant. All statistical analyses were performed in
a specific-targeted therapy, chemotherapy is hence stated PSPPIRE 1.0.1 software.
as the only choice of treatment. Then, these subtypes
have been actively studied by various researchers (Keam Results
et al., 2011).
In the literature, prior studies on intrinsic molecular Characteristics of patients
subtypes of breast carcinoma in Indonesia have been A total of 92 cases of breast carcinoma were included
focusing on ER, PgR, HER2, and Ki-67 markers. They in this study with the following clinical information. First,
are, however, largely produce different results (Prihantono the mean of patient’s age was 48.29 years old (ranged
et al., 2017a, 2017b; Rahmawati et al., 2018; Widodo et between 23-83 years old), while the mean of tumor
al., 2017, 2014). size was 5 cm (ranged between 1-17 cm). Besides, the
majority of patient’s histological grade was in the third
Materials and Methods group (68.48%). After the immunohistochemical staining
process, the ER, PgR, and HER2 positive expressions were
Patients
A retrospective study was performed at Abdul Wahab Table 1. Clinical and Immunohistochemical
Sjahranie County General Hospital, Samarinda, East Characteristics of Patients
Kalimantan, Indonesia, involving samples from patients Characteristics
between January-December 2016. An ethical clearance Age (years) Mean ± SD 48.29 ± 10.7
was obtained from the Ethical Review Committee of
Min – Max 23 – 83
the Faculty of Medicine, Mulawarman University,
Samarinda, Indonesia (49/KEPK-FK/VI/2017) before Tumor size (cm) Mean ± SD 5.00 ± 3.1
conducting the study. In addition to ER, PgR and HER2 Min – Max 1 – 17
status and Ki67 index, clinical information used in this Histological Grade 1 5 (5.43%)
included ages at diagnosis, tumor sizes, and histological 2 24 (29.09%)
grades. After data gathering, there were 92 cases
3 63 (68.48%)
during the period under investigation. These cases had
Molecular Subtypes Luminal A 7 (7.61%)
formalin-fixed paraffin-embedded blocks available for
immunohistochemical staining. Luminal B 39 (42.39%)
HER2+ 36 (39.13%)
Immunohistochemical Triple negative 10 (10.87%)
In this study, immunohistochemical staining method ER Negative 46 (50%)
was performed on formalin-fixed paraffin-embedded
Positive 46 (50%)
blocks. Technically, a section of blocks was stained with
primary antibodies for ER, PgR, HER2, and Ki-67 (all PgR Negative 47 (51.09%)
from Leica Biosystem, Newcastle, UK). An automated Positive 45 (48.91%)
immunohistochemical staining was conducted and assessed HER2 Negative 39 (42.39%)
in Leica BOND MAX (Leica Biosystem, Newcastle, UK). Positive 53 (57.61%)
Tumors with ≥ 1% positively nuclear-stained cells were
Ki-67 <14 % 15 (16.30%)
considered positive for both ER and PgR expression
(Hammond et al., 2010). Besides, HER2 positive was 14-30 % 18 (19.67%)
scored if the staining occured for > 10% of tumor cells >30 % 59 (64.13%)

2248 Asian Pacific Journal of Cancer Prevention, Vol 20


DOI:10.31557/APJCP.2019.20.8.2247
Luminal B is the Most Common Intrinsic Molecular Subtypes of Breast Carcinoma
Table 2. Association between Clinical and Immunohistochemical Factors with Intrinsic Molecular Subtypes
Characteristics All cases Luminal A Luminal B HER2+ Triple negative P value
n (%) n (%) n (%) n (%) n (%)
Age ≤ 35 ys 6 (6.5) 1 (14.3) 4 (10.3) 1 (2.8) 0 (0) 0.019†
> 35 ys 86 (93.5) 6 (85.7) 35 (89.7) 35 (97.2) 10 (100)
Size ≤ 2 cm 19 (20.7) 2 (28.6) 8 (20.5) 7 (19.4) 2 (20) 0.978
> 2 cm 73 (79.3) 5 (71.4) 31 (79.5) 29 (80.6) 8 (80)
Grade 1,2 29 (31.5) 3 (42.9) 13 (33.3) 7 (19.4) 6 (60) 0.091
3 63 (68.5) 4 (57.1) 26 (66.7) 29 (80.6) 4 (40)
ER Negative 46 (50) 0 (0) 0 (0) 36 (100) 10 (100) 0.000†
Positive 46 (50) 7 (100) 39 (100) 0 (0) 0 (0)
PgR Negative 48 (52.2) 0 (0) 3 (7.7) 36 (100) 9 (90) 0.000†
Positive 44 (47.8) 7 (100) 36 (92.3) 0 (0) 1 (10)
HER2 Negative 39 (42.4) 7 (100) 22 (56.4) 0 (0) 10 (100) 0.000†
Positve 53 (57.6) 0 (0) 17 (43.6) 36 (100) 0 (0)
Ki-67 Low 15 (16.3) 7 (100) 1 (2.6) 4 (11.1) 3 (30) 0.000†
High 77 (83.7) 0 (0) 38 (97.4) 32 (88.9) 7 (70)
†Chi-square, p value < 0.05

discovered to be 50%, 48.91%, and 57.61%, respectively. 5 cm (ranged between 1-17 cm). In fact, similar results
In particular, the majority of Ki-67 expressions were in the were discovered by other studies in Indonesia. It confirmed
high group (64.13%). Among observed samples, luminal B a behavior among breast carcinoma patients in Indonesia,
comprised the most common intrinsic molecular subtypes who, in most cases, reported their health condition when
in the population (42.39%), which was then followed their tumor had already become larger in size (Widodo
by HER2+ (39.13%), luminal A (10.87%), and triple- et al., 2017). On the other hand, the majority of patient’s
negative (7.61%). Table 1 presents the characteristics of histological grade in this research was in the high group
observed patients with breast carcinoma. (68.48%). Different results were revealed by other studies
in Indonesia, in which moderate differentiation was the
Association between clinical and immunohistochemical most common grade compared to high and low group.
factors with intrinsic molecular subtypes In practices, histological grading was the predictive and
Looking at the chi-square test, a significant result prognostic factor of breast carcinoma (Rahmawati et al.,
(p = 0.019) was revealed for the association of between 2018; Widodo et al., 2014).
age with intrinsic molecular subtypes of breast carcinoma. Furthermore, positive ER, PgR, and HER2 expression
In this study, luminal B was discovered as the most were discovered at 50%, 48.91%, and 76.09%, respectively.
commonly occuring subtypes in patients aged ≤ 35 It was parallel with the high frequency of positive HER2
years, while HER2+ was most common subtypes in older expressions (56.6%) found in prior study conducted in
patients. Table 2 exhibits the association between clinical Makassar, Indonesia (Prihantono et al., 2017b). Besides,
and immunohistochemical factors with intrinsic molecular the majority of Ki-67 expressions were in the high group
subtypes of breast carcinoma. (83.7%), which was similar to previous results of the study
in Makassar with Ki-67 positive index at about 54.2%
Discussion (Prihantono et al., 2017a).
Next, this study discovered luminal B to comprise the
This research had evaluated the distribution of most commonly occuring intrinsic molecular subtypes
intrinsic molecular subtypes of breast carcinoma and among observed population (42.39%). After luminal
studied their association and correlation with clinical B, the following ranks were HER2+ (39.13%), luminal
and immunohistochemical factors. In this study, samples A (6.52%), and triple-negative (4.36%). The result was
under investigation included 92 breast carcinoma patients. particularly similar to other studies that focused on cases
The mean age of these samples was 48.29 years old in Southeast Asia regions. Prior research in Vietnam, for
(ranged between 23-83 years old), which was in fact example, revealed a relatively high percentage of luminal B
similar to prior study in Makassar, Indonesia, with 46 subtype (56.5%) (Thang et al., 2015). In another research,
years old as the average age at diagnosis (Prihantono et the mean percentage of luminal B patients discovered in
al., 2017a). Besides, studies in Malaysia and Indonesia Myanmar was 46.2%, which was considerably higher than
indicated breast carcinoma to present at a younger age other subtypes (San et al., 2017). Results in Southeast Asia
for Indonesian women compared to Malaysian women. regions were also similar to studies conducted on breast
Ethnical and genetic differences might highlight these carcinoma cases in other Asia regions. Outside Asia, e.g.
results (Ng et al., 2011). in Morocco, luminal B was also discovered as the most
Furthermore, the mean of tumor size in this study was frequently occuring molecular subtype of breast cancer

Asian Pacific Journal of Cancer Prevention, Vol 20 2249


Swandari Paramita et al

(Fatemi et al., 2012). a number of pregnancies (Paramita et al., 2010).


In terms of clinical information, this study revealed a In general, the limitation of this study included
significant association between patients’ age with intrinsic additional focuses on other factors such as genetic
molecular subtypes of breast carcinoma. Apparently, background, while ethnical and risk factors were also
luminal B was the most common subtype in patients aged not evaluated. Further investigations of those factors
≤ 35 years, while HER2+ was the most common subtype would hence be necessary. Theoretically speaking,
in older patients. Results as such indicated younger extensive distributions of intrinsic molecular subtypes
patients to generally have the worst prognosis. Similar among worldwide population suggested the critical role
results were discovered by a previous study conducted of human races or ethnicities in distinguishing breast
in Turkey, in which older age was found to act as a risk carcinoma subtypes.
factor for HER2+ overexpressing subtype. Compared As the conclusion, this study discovered the frequency
to other subtypes, luminal B cases were more likely to of intrinsic molecular subtypes of breast carcinoma to
occur on patients with younger age at diagnosis (Turkoz vary among different human populations. In particular,
et al., 2013). the current work had confirmed luminal B as the most
However, of this study differed from previous reports commonly occuring intrinsic molecular subtypes of
in other provinces in Indonesia, which found luminal A as breast carcinoma in East Kalimantan, Indonesia. In
the most frequently occuring subtype (Rahmawati et al., terms of clinical information, age was found to be
2018; Widodo et al., 2017, 2014). Also, it was different associated with intrinsic molecular subtypes of breast
from prior research in Malaysia and Indonesia, which carcinoma. Therefore, the higher luminal B positivity
showed tumors suffered by Indonesian women to more rates in Indonesian patients would require a further
likely be HER2+ compared to Malaysian women (Ng et study. Findings of this study highlighted an urgent need
al., 2011). The higher HER2 positivity rate in Indonesia for a set of comprehensive breast carcinoma awareness
has been previously reported about 64.2% (Aryandono programs particularly in East Kalimantan, Indonesia. It
et al., 2006). should particularly be designed to encourage women to be
According to the 2013 St. Gallen Consensus, luminal aware of their breast carcinoma-related health conditions
B could be further distinguished by looking at ER, PgR, at earlier stages.
HER2, and Ki-67 expressions. The classification of
luminal B included luminal B-like HER2- (ER+, HER2-, Acknowledgments
and at least one of Ki-67 high or PgR-) and luminal B-like
HER2+ (ER+, any PgR, HER2 over-expressed, and any Acknowledgments to the Faculty of Medicine,
Ki-67) (Goldhirsch et al., 2013). Practically, estrogen and Mulawarman University, Samarinda, Indonesia, for
progesterone receptors (ER and PgR) and HER2 had been financing this research, as part of the implementation
stated as having critical influences on the management of of Research Grant of Mulawarman University year
breast cancer. Estrogen had particularly been posited as an of 2017. All procedures followed were following the
important mitogen exerting its activity by being bound to ethical standards from the Ethical Review Committee
its estrogen receptor (ER), which found in almost 80% of of the Faculty of Medicine, Mulawarman University,
breast cancer cases (Azizun-Nisa et al., 2008). Meanwhile, Samarinda, Indonesia. The authors declare that they have
PgR had been recognized as a surrogate marker of a no competing interests.
functional ER, which would be valuable in predicting
the behavior of breast carcinoma. It had been discovered Funding Statement
in almost 70% invasive breast carcinomas with a higher This research was funding by Research Grant of
positivity in postmenopausal women. The presence of Mulawarman University, Samarinda, Indonesia.
hormone receptors (ER and PgR) in the tumor tissues
were then stated as being well correlated with expected Statement conflict of Interest
responses to chemotherapy (Shaikh et al., 2016). The authors do not have any conflicts of interest to
Furthermore, HER2 had been recognized as a declare.
proto-oncogene located on chromosome 17q. Besides, it
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