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ORIGINAL ARTICLE
Year : 2022  |  Volume : 25  |  Issue : 1  |  Page : 97-104

Triple-negative Breast Cancer (TNBC) and Its Luminal Androgen Receptor (LAR) Subtype: A Clinicopathologic Review of Cases in a University Hospital in Northwestern Nigeria


Department of Pathology, Ahmadu Bello University Teaching Hospital, Zaria, Nigeria

Date of Submission14-Jul-2020
Date of Acceptance09-Sep-2021
Date of Web Publication19-Jan-2022

Correspondence Address:
Dr. A A Liman
Department of Pathology, Ahmadu Bello University Teaching Hospital, Zaria
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_437_20

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   Abstract 


Background: Breast cancer (BC) is a common malignancy; the most frequent in Nigeria. BC characteristically exhibits great biologic diversity. Amongst its variants, the triple-negative subtype is also characterized by heterogeneity (thus making it a study in diversity within diversity) and also by some unique clinicopathologic features including clinical aggressiveness, lack of response to current targeted therapies, and tendency to cluster amongst young premenopausal women especially in populations of women of African ancestry. Aims: The objective of this study was to conduct a retrospective clinicopathologic survey of all breast carcinomas to profile the triple-negative breast cancers (TNBCs) amongst them and illustrate their immunohistochemical pattern of luminal androgen receptors (LARs) expression. Patients and Methods: All the cases entered into the departmental records as breast carcinomas over the study period were extracted including patients' request cards, hematoxylin and eosin-stained slides, and paraffin-embedded tissue blocks of those diagnosed as triple-negative cancers. These were immunohistochemically stained using a monoclonal antibody for androgen receptor (AR). The whole data were analyzed and presented in tabular formats. Results: A total of 660 breast carcinomas of which 89 (13.48%) cases were identified as TNBCs with a mean age of occurrence of 42.89 ± 11.88 years. Most TNBCs (95.5%) were carcinoma no special type and 61.8% had low or intermediate histologic grading. LAR expression was noted in 11.24% of the TNBCs. Conclusion: Triple-negative cancer in this study shares some of the known characteristics but also portrays some divergence from the commonly described features.

Keywords: Breast cancer, subtypes, triple-negative


How to cite this article:
Liman A A, Kabir B, Abubakar M, Abdullahi S, Ahmed S A, Shehu S M. Triple-negative Breast Cancer (TNBC) and Its Luminal Androgen Receptor (LAR) Subtype: A Clinicopathologic Review of Cases in a University Hospital in Northwestern Nigeria. Niger J Clin Pract 2022;25:97-104

How to cite this URL:
Liman A A, Kabir B, Abubakar M, Abdullahi S, Ahmed S A, Shehu S M. Triple-negative Breast Cancer (TNBC) and Its Luminal Androgen Receptor (LAR) Subtype: A Clinicopathologic Review of Cases in a University Hospital in Northwestern Nigeria. Niger J Clin Pract [serial online] 2022 [cited 2022 Nov 30];25:97-104. Available from: https://www.njcponline.com/text.asp?2022/25/1/97/335982




   Introduction Top


Breast cancer (BC) is currently the most frequent malignant disease in Nigeria. It accounts for the highest number of new cancer cases; constituting 22.7% of all new cancer cases, in both sexes and all ages, in Nigeria, and 37% in the local women population even while occupying, according to the International Agency for Research on Cancer, the number one rank in cancer deaths (16.4%) and one of the highest cumulative risks (2.01) for dying from cancer in Nigeria.[1] BC; however, is not a single clinicopathologic entity; but a collection of several biologically different diseases; with respect to not only anatomical, morphological, immunohistochemical, and molecular features but also tumor grading, response to different treatment options, and prognostic profiles.

Notably, traditional classification schemes of BC (histology and slide-based techniques) are increasingly being replaced by molecular-based classification schemes. Perou and colleagues[2],[3] were the first to put forward a molecular classification of BC with the recognition of ER, PR, and HER-2/neu molecules as key players in breast carcinogenesis, defining the morphological and clinical behavior of the final tumor. Gene expression profiling has identified four distinct subtypes termed basal-like, HER-2 enriched, luminal A, and B cancers.

It is now accepted in modern practice that the established histopathologic classification has a limited clinical utility because of its insufficient prognostic and predictive power. However, significant progress has been made in the ability to type and subtype BCs with the discovery of these and other biomarkers toward which current therapeutic efforts are focused or being explored.[4],[5]

Although not synonymous, most triple-negative breast cancers (TNBCs) carry the “basal-like” molecular profile on gene expression assays but St Gallen 2013 (International Breast Cancer Conference) proposed that the triple-negative category might be used as a surrogate definition for basal-like category due to the high degree of overlap.[6]

Triple-negative disease, defined as tumors that are negative for ER, PR, and HER-2 represents a minority of BCs. However, because of the aggressive behavior, poor prognosis, and lack of targeted therapy in this category, TNBC, although being sensitive to chemotherapy, accounts for a disproportionate number of metastatic cancer cases and BC deaths. Compared with other BC subtypes, triple-negative tumors were often larger at the time of diagnosis, appear at a younger age, involved lymph nodes more frequently, and were often high-grade neoplasms and also had a higher proportion of distant – although not local – recurrence.[7] Other studies also suggest that patients with TNBC have a higher incidence of soft tissue and critical visceral organs, including lung, liver, and brain metastases.[8],[9],[10],[11] The increased frequency of triple-negative cancer, is said to, at least partly, explain the divergence in BC mortality between African-American women and white women.[12]

TNBC itself has now been recognized as a highly diverse group of cancers with six subtypes identified, displaying unique gene-expression profile ontologies including Basal-like (BL1 and BL2), immunomodulatory, mesenchymal, mesenchymal stem-like, and luminal androgen receptor (LAR) subtypes. The first established molecular classification for TNBC was suggested by Lehmann et al.,[13],[14] which they have recently revised to a more concise system consisting of only four subtypes are as follows: BL1, BL2, M, and LAR with implications in targeted chemotherapy (in both neoadjuvant and adju vant settings).

Although BC has long been perceived as a hormone-related tumor, accumulating evidence now suggests a role for androgen signaling in BC and androgen receptor (AR) is emerging as a practical marker and therapeutic target and prognostic indicator.[15],[16] AR acts both in a genomic and a nongenomic way, promoting in most cases, cellular proliferation and as a modulator of cancer progression.[15],[16],[17] The LAR subtype has apparently attracted more interest from researchers. There are; however, insufficient data in the current medical literature on TNBC in general and its subtypes including LAR in our environment.


   Patients and Methods Top


This study was carried out in the Pathology Department of a University Teaching Hospital in Northwestern Nigeria. Ethical clearance was obtained from the Health Research and Ethics Committee of the Teaching Hospital.

All cases of TNBC diagnosed during the 8-year period (January 2009 to December 2016) under study were included. The patients' request forms (for demographic and clinicopathologic details), pertinent hematoxylin and eosin (H and E) slides, immunohistochemistry slides for ER, PR, and HER2/neu, as well as the relevant paraffin-embedded tissue blocks (PETBs), were all retrieved from departmental archives. Where required, for the purpose of examining histologic/morphologic features, fresh H and E sections were made from the PETBs.

Indirect immunohistochemical staining for AR was done on each TNBC case to determine the AR expression by the tumor cells. Sections were made at 2–3 microns from the PETB and placed on charged slides (Bio Optica). The sections were then deparaffinized in xylene, rehydrated in decreasing concentrations of alcohol, and then sequentially incubated with hydrogen peroxide block (HRP), protein block, anti-AR antibody, complement, HRP conjugate, and diaminobenzidine (DAB), chromogen/substrate mixture (Dako) with the DAB Detection Kit (Dako) for about 10 minutes each and rinsed each time in a buffer. The slides were counterstained with hematoxylin, then dehydrated and coverslips applied. All steps were performed at room temperature. Both negative and positive controls were run alongside the tests. The slides were viewed under the light microscope and brown granular nuclear staining was interpreted as positive AR, whereas bluish staining of the nuclei was interpreted as negative. Simultaneously, all the cases of TNBC were reexamined/reviewed and immunohistochemical scoring for ER, PR, and HER2/neu was done according to the American Society of Clinical Oncology/College of American Pathologists Criteria.

The LAR biomarker expression was detected and semi-quantitatively quantified as the percentage of immune-positive tumor cells on the total of tumor cells. Two independent observers evaluated all the samples and discordance of >10% of positive cells were resolved by consensus after a joint review using a multiheaded microscope. As clear guidelines for AR expression have not been available until now, we have not used a cutoff value (AR was done and considered positive if ≥10% of tumor cells showed nuclear staining). The collected data were subjected to descriptive statistical analysis using Excel 2016 (16.0) and expressed in tabular formats.


   Results Top


During the study period, a total of 660 invasive breast carcinomas were diagnosed in the institution [Table 1] and [Table 2]. All the patients in this study cohort were Nigerians of African descent. All but three cases were female thus making the F: M ratio = 219:1. The ages of 22 patients were not found in the records – registered only as adults; the average age of 638 patients [Table 1] given was 45.98 years with a SD of 12.07 years. For the 636 female patients whose ages were specified the mean age was 45.90 (SD = 12.03) with an age range between 17 and 93 years, whereas the average age of the male patients was 60 years.
Table 1: Frequency distribution by age of breast cancers in ABUTH, Zaria

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Table 2: Frequency distribution of breast cancer by histologic subtype in ABUTH, Zaria

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Invasive carcinoma NST constituted the most common histologic subtype with 629 cases (95.3%) followed in descending order by special subtypes (4.7%); lobular carcinoma (11 cases), metaplastic carcinoma (6 cases), both medullary and mucinous types (4 cases each), mixed types (3 cases; mixed NST with 2 lobular and 1 mucinous carcinomas), papillary variant (2 cases), and signet ring cell type (1 case) [Table 2].

About 53.8% of the 638 tumors (grades were not available for 20 cases) were grade 2 using the semiquantitative Modified Bloom and Richardson System [Table 3]. Of the remainder, 212 cases (33.2%) and 85 cases (25.1%), respectively, were grades 3 and 1.
Table 3: Frequency distribution of breast cancers by histologic grade in ABUTH, Zaria

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There were 89 cases of TNBCs from the 660 BCs diagnosed here comprising 13.48% of all breast carcinomas. All the 89 patients with TNBC were female; none of the 3 male cases showed a triple-negative pattern. The mean age of occurrence of TNBC was 42.89 ± 11.88 years (age range: 21–72 years) [Table 4]. The annual distribution pattern of TNBC over the study period disclosed a range of 4–15 cases per annum with an annual average rate of 8.1 cases [Table 5].
Table 4: Frequency distribution table for TNBC by age in ABUTH, Zaria

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Table 5: Frequency distribution table expressing the annual distribution pattern of TNBC in ABUTH, Zaria

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Of the 89 TNBCs, a large majority (95.5%) was invasive carcinoma NST with one case each represented by medullary, mucinous, signet ring cell, and papillary subtypes (4.5%) [Table 6]. Most (49 cases or 55.1%) of the 89 patients had grade 2 tumors, whereas 34 (38.2%) had grade 3 malignancies with a minority (6.7%) having had a grade 1 cancer. Both the medullary and mucinous special subtypes had a grade 3 tumor, whereas the signet ring cell and papillary cases were diagnosed as grade 1 tumors [Table 6].
Table 6: Frequency distribution of TNBC by histologic grade; also outlining the AR status

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Mitotic counts evaluated for all the TNBCs using the numerical scoring system of 1–3 in fixed field areas of 10 HPF (high power field) as recorded at diagnosis showed 34 cases exhibited a score of 3, whereas 49 cases with a score of 2 and 6 with a score of 1 [Table 7].
Table 7: Frequency distribution of TNBC in ABUTH, Zaria by grade and mitotic index

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Only 10 of the 89 cases (11.2%) of the TNBCs expressed the LAR antigen [Table 4], [Table 6], and [Table 8]. Of these eight were invasive carcinoma NST [Figure 1],[Figure 2],[Figure 3],[Figure 4] with one each of the mucinous and papillary special subtypes of invasive breast carcinoma. The age range for the LAR subtype patients was 25–75 years with a mean age of 48.60 years (SD = 12.09) [Table 9]. Of the 10 LAR cases, only 3 were grade 3 malignancies with the remaining 70% noted as grades 2 and 1; 5 and 2 cases, respectively. In addition, only two of those exhibited a mitotic count with a numerical score of 3; the rest having a corresponding mitotic count of 2 (6 cases) and 1 (2 cases).
Figure 1: Photomicrograph showing an invasive tumor composed of pleomorphic vesicular nuclei with prominent nucleoli and moderate cytoplasm within a fibrocollagenous stroma (H and E x400 magnification)

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Figure 2: Photomicrograph of invasive carcinoma NST showing positive nuclear reaction to antiandrogen antibodies (immunohistochemical stain x400)

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Figure 3: Photomicrograph showing an invasive tumor disposed in nests, the tumor cells are negative to antiestrogen antibodies (immunohistochemical stain x400 magnification)

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Figure 4: Photomicrograph showing an invasive tumor disposed in nests, the tumor cells are negative to Her 2 antibodies (immunohistochemical stain x400 magnification)

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Table 8: Frequency distribution of LAR expression of TNBC in ABUTH, Zaria by histologic subtypes

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Table 9: Frequency distribution of LAR subtype of TNBC by age in ABUTH, Zaria

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   Discussion Top


The results of this study reveal that triple-negative disease constitutes 13.48% of all breast carcinomas in this setting. This compares favorably with rates described amongst whites in America and elsewhere (12–24% incidence rates).[4],[18],[19],[20],[21] There; however, is seen a sharp contrast with figures in published works from various regions of Nigeria where Mandong et al.[22] in Jos, North-Central Nigeria; Ukah and colleagues[23] from the South-East; Usman et al.[24] from Kano, North-West; and Adisa and co-workers[25] in Aba, South-Eastern region (46%); demonstrated 41.3%, 46.3%, 46.6%, and 46.0% occurrences, respectively, in the various locales. Other figures previously reported from Nigeria that are outside the range of what we found in our present study include; the works of Adeniji AA et al.[26] and Makanjola et al.,[27] both in Lagos, South-Western region (47.4% and (87%, respectively); the report by Minoza and colleagues[28] from Maiduguri, North-Eastern Nigeria (52.6%); and that of Dodiyi-Manuel and Athanasius[29] in Port-Harcourt, South-Southern region of Nigeria. In addition, in two separate works from Ilorin, North-Central Nigeria,[30],[31] Adeniji and co-workers reported two different variants of triple-negative cancer; basal-like (ER-ve, PR-ve, HER2-ve, CK5/6+ve, and/or EGFR+) and unclassified (negative for all five markers) as, respectively, constituting 25% and 24% of all breast carcinomas. It would be noted although, that the present study was conducted on a much larger population of BC cases than these above-mentioned works.

The TNBC frequency ratio established here also diverges from the incidences of TNBC established in Black women in the Carolina Breast Cancer Study (27% of BC burden) as well as in studies from Mali (46%) and Ghana (as high as 82%), in West Africa and from surveys in Southern India and Malaysia.[12],[32],[33],[34],[35] It might be safe to postulate that the incidences of TNBC and indeed its LAR variant in our BC patients may even be lower than illustrated here because the laboratory does not have control over some of the pre-analytic variables and these invariably may affect detection rates of ER, PR, and HER-2.

Several of the epidemiologic and clinicopathologic studies reviewed here have demonstrated that TNBCs tend to cluster in the younger premenopausal patient population. The average age for diagnosis of TNBC in this review has been shown to be 42.89 ± 11.88 years. This is slightly lower than the mean age in the general BC population in this environment (45.98 ± 12.03 years) [Table 1] which is a much younger age distribution pattern than amongst Caucasians (60–69 years peak age range).[19],[36] The LAR subtype of the TNBC in this survey by contrast showed a mean age higher than that of the TNBC and higher too than of the larger BC population of 660 (48.60 years; SD = 12.09) [Table 9]. It is not surprising that all the cases of TNBC, and the LAR tumors, were females, given the very low frequency of male BC in this study population; 3 out of 660 (<0.5%).

Most TNBCs are said to be ductal in origin; invasive carcinoma NST; however, several other aggressive phenotypes appear to be overrepresented including metaplastic, atypical, or typical medullary, and adenoid-cystic.[37],[38] Invasive carcinoma NST makes up about the same proportion of the TNBCs (95.5%) as in the general BC pool (95.3%) which correspond positively with the findings in the earlier works in West Africa notwithstanding the assertion by the World Health Organization attributing the lack of application of strict criteria for inclusion in the special types and also the fact that tumors with a combination of the NST and special-type patterns are not universally recognized as a separate mixed category as responsible for the very high frequency of NST in published series.[22],[25],[32],[36]

Although from the very beginning, TNBCs have been acknowledged and documented as commonly a high-grade disease, the findings here show a pattern with 61.8% of the TNBCs exhibiting histologic grades 2 and 1 morphologies against the backdrop of the general BC population with about 67% with histologic grades 1 and 2 tumors; thus, not markedly divergent from the local BCs.[5],[7],[12] Considering the level of mitoses as an important grading index, the fact that only 32.2% of the TNBCs in this series showed a high degree of mitotic activity possibly will reinforce the point made here.

It was observed in this study that even in the special-types category; recognized in many studies as aggressive phenotypes, and said to be overrepresented in the triple-negative group; only half of them (medullary and mucinous subtypes) were grade 3 tumors, with the other half (papillary and signet ring cell types) identified as histologic grade 1 neoplasm.[5],[37],[38],[39]

AR detection is still not routinely performed in BCs even with AR emerging as a new marker and a potential new therapeutic target; but TNBCs generally are acknowledged to have a low-frequency expression of AR expression compared with other BC subtypes, with as few as 12% of them expressing AR.[15],[16],[40],[41],[42] The frequency ratio of 11.2% of the LAR tumor variant in this study is not far off from that evaluation. It is of note that only 30% of this tumor-subtype were high-grade variety thus depicting a lower pathologic grading than the TNBC or the general BC population in this study.


   Conclusion Top


This study has not only confirmed some of the known characteristics of TNBC, but also highlighted some peculiarities of TNBC and its LAR subtype in our environment, in terms of comparative incidences amongst black populations and histologic characteristics; by revealing a lower rate of occurrence and a lesser histologic grading in a black population. A much larger multicenter study to explore the epidemiologic and wider clinicopathologic features of TNBC in the indigenous people here may help to further elucidate their patterns.

Ethical approval

Ethical clearance was obtained from the Health Research and Ethics Committee of ABUTH.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]



 

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