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Tumour Infiltrating Lymphocytes (TILs) and immune composition in breast cancer patients from Kenya: Spatial distributions and associations with risk factors and tumour characteristics

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Abstract

Background

The immune landscape of breast cancer (BC) in patients from Sub Saharan Africa is understudied. Our aims were to describe the distribution of Tumour Infiltrating Lymphocytes (TILs) within the intratumoural stroma (sTILs) and the leading/invasive edge stroma (LE-TILs), and to evaluate TILs across BC subtypes with established risk factors and clinical characteristics in Kenyan women.

Methods

Visual quantification of sTILs and LE-TILs were performed on Haematoxylin and eosin -stained pathologically confirmed BC cases based on the International TIL working group guidelines. Tissue Microarrays were constructed and stained with immunohistochemistry (IHC) for CD3, CD4, CD8, CD68, CD20, and FOXP3.

Linear and logistic regression models were used to assess associations between risk factors and tumour features with IHC markers and total TILs, after adjusting for other covariates.

Results

A total of 226 invasive BC cases were included. Overall, LE-TIL (mean = 27.9, SD = 24.5) proportions were significantly higher than sTIL (mean = 13.5, SD = 15.8). Both sTILs and LE- TILs were predominantly composed of CD3, CD8, and CD68. We found higher TILs to be associated with high KI67/high grade and aggressive tumour subtypes, although these associations varied by TIL locations. Older age at menarche (≥ 15 vs. < 15 years) was associated with higher CD3 (OR: 2.06, 95%CI:1.26–3.37), but only for the intra-tumour stroma.

Conclusion

The TIL enrichment in more aggressive BCs is similar to previously published data in other populations. The distinct associations of sTIL/LE-TIL measures with most examined factors highlight the importance of spatial TIL evaluations in future studies.

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Data availability

The datasets used and/or analysed during the current study are available from the corresponding author upon request.

Abbreviations

BC:

Breast Cancer

BMI:

Body Mass Index

CTLs:

Cytotoxic T lymphocytes

ER:

Estrogen receptor

FFPE:

Formalin Fixed Paraffin Embedded

H & E:

Haematoxylin and Eosin

HER2:

Human Epidermal Growth Factor Receptor 2

IHC:

Immunohistochemistry

LE:

Leading edge stroma

LPBC:

Lymphocyte Predominant Breast Carcinoma

MDSC:

Myeloid-Derived Suppressor Cells

NACOSTI:

National Commission for Science Technology and Innovation

PCR:

Pathologic Complete Remission

PR:

Progesterone Receptor

TAM:

Tumour Associated Macrophages

TCGA:

The Cancer Genome Atlas

TIL:

Tumour Infiltrating Lymphocytes

TMA:

Tissue Microarrays

TN:

Triple Negative

TNBC:

Triple Negative Breast Cancer

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Acknowledgements

Tissue microarrays were constructed by the Human Tissue Acquisition & Pathology Core at Baylor College of Medicine. HTAP is funded by P30 Cancer Center Support Grant (NCI-CA125123). The authors would like to acknowledge Dr. Gretchen Gierach (Division of Cancer Epidemiology & Genetics, National Cancer Institute, USA) for her support. Angela Mutuku, Subash Govender, Johnstone Ngao, Raymond Kriel for providing logistical and technical support. JF/SS/FM acknowledge funding from UKRI grant reference MR/S015027/1. This research was supported by the Digital Computational Pathology Laboratory in the Department of Pathology and Cell Biology at Columbia University Irving Medical Center.

Funding

This research received no external funding. It was funded internally through the Deans Fund, Faculty of Health Sciences—East Africa Aga Khan University, Nairobi, Kenya. The research was partially supported by the intramural research program of the Division of Cancer Epidemiology & Genetics, National Cancer Institute, USA.

Author information

Author notes

  1. Xiaohong Rose Yang and Dhirendra Govender are Joint senior authors.

Authors and Affiliations

  1. Department of Pathology, Aga Khan University, East Africa, P.O Box30270- 00100, Nairobi, Kenya

    Shahin Sayed, Zahir Moloo, Mansoor Saleh, Asim Jamal Shaikh, Jasmit Shah & Veronica Ngundo

  2. Division of Anatomical Pathology, University of Cape Town, Cape Town, South Africa

    Shahin Sayed, Richard Naidoo & Dhirendra Govender

  3. Integrative Tumour Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA

    Hela Koka, Mustapha Abubakar & Xiaohong Rose Yang

  4. Department of Pathology and Cell Biology, Columbia University Medical Center, Columbia University, New York, NY, USA

    Kevin Gardner, Ambar Beatriz Caban-Ureña & Zhong Wang

  5. Department of Pathology/Division of Research, Peter MacCallum Cancer, Melbourne, VIC, 3000, Australia

    Roberto Salgado

  6. Department of Pathology & Immunology, Baylor College of Medicine, Houston, USA

    Daniel Rosen & Patricia Castro

  7. The Usher Institute and CRUK Edinburgh Cancer Centre, The University of Edinburgh, Edinburgh, Scotland

    Jonine Figueroa

  8. Department of Human Health Research Programme, Mount Kenya University, Thika, Kenya

    Francis Makokha

  9. Department of Biochemistry, University of Alberta, Edmonton, Canada

    Hien Khanh Ha

  10. Department of Pathology, University of Witwatersrand, Johannesburg, South Africa

    Pumza Magangane

  11. PathCare, Cape Town, South Africa

    Dhirendra Govender

  12. Department of Pathology, GZA-ZNA Hospitals, Wilrijk, Antwerp, Belgium

    Roberto Salgado

  13. Comprehensive Cancer Care and Research, Sultan Qaboos Comprehensive Cancer Care and Research Institute, Muscat, Oman

    Asim Jamal Shaikh

  14. Department of Pathology, ZAS Hospitals, Antwerp, Belgium

    Roberto Salgado

Authors
  1. Shahin Sayed
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  2. Hela Koka
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Contributions

Conceptualization, Shahin Sayed and Dhiren Govender; Data curation, Shahin Sayed, Hela Koka, Zahir Moloo, Ambar Caban, Patricia Castro, Jasmit Shah, Khanh Ha, Wang Zhong, Pumza Magangane and Veronica Ngundo; Formal analysis, Shahin Sayed, Hela Koka, Ambar Caban and Wang Zhong; Funding acquisition, Shahin Sayed; Investigation, Shahin Sayed and Patricia Castro; Methodology, Shahin Sayed, Mustapha Abubakar, Kevin Gardner, Daniel Rosen, Patricia Castro, Mansoor Saleh, Xiaohong Yang and Dhiren Govender; Project administration, Shahin Sayed and Veronica Ngundo; Resources, Mustapha Abubakar, Kevin Gardner, Daniel Rosen, Patricia Castro, Jonine Figueroa, Francis Makokha and Xiaohong Yang; Software, Wang Zhong; Supervision, Kevin Gardner, Richard Naidoo, Xiaohong Yang, and Dhiren Govender; Validation, Shahin Sayed, Mustapha Abubakar, Kevin Gardner, Zahir Moloo, Ambar Caban, Jasmit Shah, Xiaohong Yang and Dhiren Govender; Visualization, Shahin Sayed, Hela Koka, Mustapha Abubakar, Roberto Salgado, Mansoor Saleh, Asim Shaikh, Richard Naidoo and Xiaohong Yang; Writing – original draft, Shahin Sayed; Writing – review & editing, Hela Koka, Mustapha Abubakar, Kevin Gardner, Roberto Salgado, Zahir Moloo, Daniel Rosen, Mansoor Saleh, Asim Shaikh, Jonine Figueroa, Francis Makokha, Khanh Ha, Pumza Magangane, Richard Naidoo, Xiaohong Yang and Dhiren Govender.

Corresponding author

Correspondence to Shahin Sayed.

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Conflict of interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Ethical approval

The study was conducted in accordance with the Declaration of Helsinki and approved by the Research Ethics Committees of the Aga Khan University Hospital Nairobi (2016/REC-32 (v3) and the Faculty of Health Sciences Research Ethics Committee of the University of Cape Town (HREC 427/2016). The study was also permitted by the National Commission for Science Technology and Innovation, Kenya (Ref No: NACOSTI/P/19/72237/28785), License number: NACOSTI/P/19/993). The Reporting Recommendations for Tumour Marker Prognostic Studies (REMARK) criteria were observed. (McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM (2005) Reporting recommendations for tumour marker prognostic studies. J Clin Oncol 23(36):9067–9072).

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Patient consent was waived due to this being a retrospective study.

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Sayed, S., Koka, H., Abubakar, M. et al. Tumour Infiltrating Lymphocytes (TILs) and immune composition in breast cancer patients from Kenya: Spatial distributions and associations with risk factors and tumour characteristics. Breast Cancer Res Treat 199, 401–413 (2023). https://doi.org/10.1007/s10549-023-06921-3

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