Spatial analyses of immune cell infiltration in cancer: current methods and future directions: A report of the International Immuno‐Oncology Biomarker Working Group on Breast Cancer-Reference-Cited by-同舟云学术

Spatial analyses of immune cell infiltration in cancer: current methods and future directions: A report of the International Immuno‐Oncology Biomarker Working Group on Breast Cancer

Published:2023-08 Issue:5 Volume:260 Page:514-532
ISSN:0022-3417
Container-title:The Journal of Pathology
language:en
Short-container-title:The Journal of Pathology

Author:

Page David B¹^ORCID,Broeckx Glenn²³,Jahangir Chowdhury Arif⁴^ORCID,Verbandt Sara⁵,Gupta Rajarsi R⁶^ORCID,Thagaard Jeppe⁷⁸,Khiroya Reena⁹,Kos Zuzana¹⁰,Abduljabbar Khalid¹¹,Acosta Haab Gabriela¹²,Acs Balazs¹³¹⁴,Akturk Guray¹⁵,Almeida Jonas S¹⁶,Alvarado‐Cabrero Isabel¹⁷,Azmoudeh‐Ardalan Farid¹⁸,Badve Sunil¹⁹,Baharun Nurkhairul Bariyah²⁰,Bellolio Enrique R²¹,Bheemaraju Vydehi²²,Blenman Kim RM²³²⁴,Botinelly Mendonça Fujimoto Luciana²⁵,Bouchmaa Najat²⁶,Burgues Octavio²⁷,Cheang Maggie Chon U²⁸,Ciompi Francesco²⁹,Cooper Lee AD³⁰,Coosemans An³¹,Corredor Germán³²,Dantas Portela Flavio Luis³³^ORCID,Deman Frederik²,Demaria Sandra³⁴³⁵,Dudgeon Sarah N³⁶,Elghazawy Mahmoud³⁷³⁸^ORCID,Ely Scott³⁹,Fernandez‐Martín Claudio⁴⁰,Fineberg Susan⁴¹,Fox Stephen B⁴²,Gallagher William M⁴,Giltnane Jennifer M⁴³,Gnjatic Sacha⁴⁴,Gonzalez‐Ericsson Paula I⁴⁵^ORCID,Grigoriadis Anita⁴⁶⁴⁷^ORCID,Halama Niels⁴⁸,Hanna Matthew G⁴⁹,Harbhajanka Aparna⁵⁰,Hardas Alexandros⁵¹^ORCID,Hart Steven N⁵²^ORCID,Hartman Johan¹⁴⁵³^ORCID,Hewitt Stephen⁵⁴,Hida Akira I⁵⁵,Horlings Hugo M⁵⁶,Husain Zaheed⁵⁷,Hytopoulos Evangelos⁵⁸,Irshad Sheeba⁵⁹,Janssen Emiel AM⁶⁰⁶¹,Kahila Mohamed⁶²,Kataoka Tatsuki R⁶³^ORCID,Kawaguchi Kosuke⁶⁴,Kharidehal Durga²²,Khramtsov Andrey I⁶⁵,Kiraz Umay⁶⁰⁶¹,Kirtani Pawan⁶⁶,Kodach Liudmila L⁶⁷,Korski Konstanty⁶⁸,Kovács Anikó⁶⁹⁷⁰,Laenkholm Anne‐Vibeke⁷¹⁷²,Lang‐Schwarz Corinna⁷³,Larsimont Denis⁷⁴,Lennerz Jochen K⁷⁵,Lerousseau Marvin⁷⁶⁷⁷⁷⁸,Li Xiaoxian⁷⁹,Ly Amy⁸⁰,Madabhushi Anant⁸¹,Maley Sai K⁸²,Manur Narasimhamurthy Vidya⁸³,Marks Douglas K⁸⁴,McDonald Elizabeth S⁸⁵,Mehrotra Ravi⁸⁶⁸⁷,Michiels Stefan⁸⁸,Minhas Fayyaz ul Amir Afsar⁸⁹,Mittal Shachi⁹⁰,Moore David A⁹¹,Mushtaq Shamim⁹²,Nighat Hussain⁹³,Papathomas Thomas⁹⁴⁹⁵,Penault‐Llorca Frederique⁹⁶,Perera Rashindrie D⁹⁷⁹⁸,Pinard Christopher J⁹⁹¹⁰⁰¹⁰¹¹⁰²,Pinto‐Cardenas Juan Carlos¹⁰³,Pruneri Giancarlo¹⁰⁴¹⁰⁵,Pusztai Lajos¹⁰⁶¹⁰⁷,Rahman Arman⁴,Rajpoot Nasir Mahmood¹⁰⁸,Rapoport Bernardo Leon¹⁰⁹¹¹⁰,Rau Tilman T¹¹¹^ORCID,Reis‐Filho Jorge S¹¹²^ORCID,Ribeiro Joana M¹¹³,Rimm David⁶²¹¹⁴^ORCID,Vincent‐Salomon Anne¹¹⁵,Salto‐Tellez Manuel¹¹⁶¹¹⁷,Saltz Joel¹¹⁸,Sayed Shahin¹¹⁹,Siziopikou Kalliopi P¹²⁰,Sotiriou Christos¹²¹¹²²,Stenzinger Albrecht¹²³,Sughayer Maher A¹²⁴,Sur Daniel¹²⁵,Symmans Fraser¹²⁶,Tanaka Sunao¹²⁷,Taxter Timothy¹²⁸,Tejpar Sabine⁵,Teuwen Jonas¹²⁹,Thompson E Aubrey¹³⁰,Tramm Trine¹³¹,Tran William T¹³²,van der Laak Jeroen¹³³,van Diest Paul J¹³⁴¹³⁵,Verghese Gregory E⁴⁶⁴⁷^ORCID,Viale Giuseppe¹³⁶,Vieth Michael¹³⁷,Wahab Noorul¹³⁸^ORCID,Walter Thomas⁷⁶⁷⁷⁷⁸,Waumans Yannick¹³⁹,Wen Hannah Y⁴⁹,Yang Wentao¹⁴⁰,Yuan Yinyin¹⁴¹,Adams Sylvia⁸⁴¹⁴²,Bartlett John Mark Seaverns¹⁴³,Loibl Sibylle¹⁴⁴,Denkert Carsten¹⁴⁵,Savas Peter⁹⁸¹⁴⁶,Loi Sherene⁹⁸¹⁴⁷,Salgado Roberto²⁹⁸,Specht Stovgaard Elisabeth¹⁴⁸¹⁴⁹

Affiliation:

1. Earle A Chiles Research Institute Providence Cancer Institute Portland OR USA

2. Department of Pathology GZA‐ZNA Hospitals Antwerp Belgium

3. Centre for Oncological Research (CORE), MIPPRO, Faculty of Medicine Antwerp University Antwerp Belgium

4. UCD School of Biomolecular and Biomedical Science University College Dublin Dublin Ireland

5. Digestive Oncology, Department of Oncology KU Leuven Leuven Belgium

6. Department of Biomedical Informatics Stony Brook University Stony Brook NY USA

7. Technical University of Denmark Kongens Lyngby Denmark

8. Visiopharm A/S Hørsholm Denmark

9. Department of Cellular Pathology University College Hospital London UK

10. Department of Pathology and Laboratory Medicine, BC Cancer Vancouver Centre University of British Columbia Vancouver BC Canada

11. Centre for Evolution and Cancer The Institute of Cancer Research London UK

12. Hospital Maria Curie Buenos Aires Argentina

13. Department of Oncology and Pathology Karolinska Institutet Stockholm Sweden

14. Clinical Pathology and Cancer Diagnostics Karolinska University Hospital Stockholm Sweden

15. Translational Molecular Biomarkers Merck & Co Inc Kenilworth NJ USA

16. National Cancer Institute Division of Cancer Epidemiology and Genetics (DCEG) Rockville MD USA

17. Oncology Hospital Star Medica Centro Mexico

18. Tehran University of Medical Sciences Tehran Iran

19. Pathology and Laboratory Medicine Emory University School of Medicine, Emory University Winship Cancer Institute Atlanta GA USA

20. The National University of Malaysia Kuala Lumpur Malaysia

21. Departamento de Anatomía Patológica, Facultad de Medicina Universidad de La Frontera Temuco Chile

22. Department of Pathology Narayana Medical College Nellore India

23. Internal Medicine Section of Medical Oncology and Yale Cancer Center Yale School of Medicine New Haven CT USA

24. Computer Science Yale School of Engineering and Applied Science New Haven CT USA

25. Amazonas Federal University Manaus Brazil

26. Institute of Biological Sciences, Faculty of Medical Sciences Mohammed VI Polytechnic University (UM6P) Ben‐Guerir Morocco

27. Pathology Department Hospital Cliníco Universitario de Valencia/Incliva Valencia Spain

28. Head of Integrative Genomics Analysis in Clinical Trials, ICR‐CTSU, Division of Clinical Studies Institute of Cancer Research London UK

29. Radboud University Medical Center Department of Pathology Nijmegen The Netherlands

30. Department of Pathology Northwestern Feinberg School of Medicine Chicago IL USA

31. Department of Oncology, Laboratory of Tumor Immunology and Immunotherapy KU Leuven Leuven Belgium

32. Biomedical Engineering Department Emory University Atlanta GA USA

33. Hospital Universitário Getúlio Vargas Manaus Brazil

34. Department of Radiation Oncology Weill Cornell Medical College New York NY USA

35. Department of Pathology Weill Cornell Medicine New York NY USA

36. Conputational Biology and Bioinformatics Yale University New Haven CT USA

37. University of Surrey Guildford UK

38. Ain Shams University Cairo Egypt

39. Translational Pathology Translational Sciences and Diagnostics/Translational Medicine/R&D, Bristol Myers Squibb Princeton NJ USA

40. Instituto Universitario de Investigación en Tecnología Centrada en el Ser Humano, HUMAN‐tech Universitat Politècnica de València Valencia Spain

41. Montefiore Medical Center and the Albert Einstein College of Medicine New York NY USA

42. Department of Pathology, Peter MacCallum Cancer Centre and Sir Peter MacCallum Department of Oncology University of Melbourne Melbourne VIC Australia

43. Genentech South San Francisco CA USA

44. Department of Oncological Sciences, Medicine Hem/Onc, and Pathology, Tisch Cancer Institute – Precision Immunology Institute Icahn School of Medicine at Mount Sinai New York NY USA

45. Department of Medicine Vanderbilt University Medical Center Nashville TN USA

46. Cancer Bioinformatics, School of Cancer & Pharmaceutical Sciences, Faculty of Life Sciences and Medicine King's College London London UK

47. Breast Cancer Now Research Unit, School of Cancer and Pharmaceutical Sciences, Faculty of Life Sciences and Medicine King's College London London UK

48. Translational Immunotherapy German Cancer Research Center Heidelberg Germany

49. Memorial Sloan Kettering Cancer Center New York NY USA

50. Case Western University Cleveland OH USA

51. Pathobiology & Population Sciences The Royal Veterinary College London UK

52. Laboratory Medicine and Pathology Mayo Clinic Rochester MN USA

53. Department of Oncology‐Pathology Karolinska Institutet Stockholm Sweden

54. Department of Pathology, Center for Cancer Research, National Cancer Institute National Institutes of Health Bethesda MD USA

55. Department of Pathology Matsuyama Shimin Hospital Matsuyama Japan

56. Division of Pathology Netherlands Cancer Institute (NKI) Amsterdam The Netherlands

57. Praava Health Dhaka Bangladesh

58. iRhythm Technologies Inc. San Francisco CA USA

59. King's College London & Guy's & St Thomas’ NHS Trust London UK

60. Department of Pathology Stavanger University Hospital Stavanger Norway

61. Department of Chemistry, Bioscience and Environmental Technology University of Stavanger Stavanger Norway

62. Department of Pathology Yale University School of Medicine New Haven CT USA

63. Department of Pathology Iwate Medical University Iwate Japan

64. Department of Breast Surgery Kyoto University Graduate School of Medicine Kyoto Japan

65. Pathology and Laboratory Medicine Ann & Robert H. Lurie Children's Hospital of Chicago Chicago IL USA

66. Department of Histopathology Aakash Healthcare Super Speciality Hospital New Delhi India

67. Department of Pathology Netherlands Cancer Institute – Antoni van Leeuwenhoek Hospital Amsterdam The Netherlands

68. Data, Analytics and Imaging, Product Development F.Hoffmann‐La Roche AG Basel Switzerland

69. Department of Clinical Pathology Sahlgrenska University Hospital Gothenburg Sweden

70. Institute of Biomedicine, Sahlgrenska Academy University of Gothenburg Gothenburg Sweden

71. Surgical Pathology Zealand University Hospital Roskilde Denmark

72. Surgical Pathology University of Copenhagen Copenhagen Denmark

73. Institute of Pathology, Klinikum Bayreuth GmbH Friedrich‐Alexander‐University Erlangen‐Nuremberg Bayreuth Germany

74. Institut Jules Bordet Université Libre de Bruxelles Brussels Belgium

75. Center for Integrated Diagnostics Massachusetts General Hospital/Harvard Medical School Boston MA USA

76. Centre for Computational Biology (CBIO) Mines Paris, PSL University Paris France

77. Institut Curie PSL University Paris France

78. INSERM, U900 Paris France

79. Pathology and Laboratory Medicine Emory University Atlanta GA USA

80. Department of Pathology Massachusetts General Hospital Boston MA USA

81. Biomedical Engineering, Radiology and Imaging Sciences, Biomedical Informatics, Pathology Georgia Institute of Technology and Emory University Atlanta GA USA

82. NRG Oncology/NSABP Foundation Pittsburgh PA USA

83. Manipal Hospitals Bangalore India

84. Perlmutter Cancer Center NYU Langone Health New York NY USA

85. Breast Cancer Translational Research Group University of Pennsylvania Philadelphia PA USA

86. Indian Cancer Genome Atlas Pune India

87. Centre for Health, Innovation and Policy Foundation Noida India

88. Office of Biostatistics and Epidemiology, Gustave Roussy, Oncostat U1018, Inserm University Paris‐Saclay, Ligue Contre le Cancer labeled Team Villejuif France

89. Tissue Image Analytics Centre, Warwick Cancer Research Centre, PathLAKE Consortium, Department of Computer Science University of Warwick Coventry UK

90. Department of Chemical Engineering, Department of Laboratory Medicine and Pathology University of Washington Seattle WA USA

91. CRUK Lung Cancer Centre of Excellence, UCLH London UK

92. Department of Biochemistry Ziauddin University Karachi Pakistan

93. Pathology and Laboratory Medicine All India Institute of Medical Sciences Raipur India

94. Institute of Metabolism and Systems Research University of Birmingham Birmingham UK

95. Department of Clinical Pathology Drammen Sykehus, Vestre Viken HF Drammen Norway

96. Centre Jean Perrin, INSERM U1240 Imagerie Moléculaire et Stratégies Théranostiques Université Clermont Auvergne Clermont‐Ferrand France

97. School of Electrical, Mechanical and Infrastructure Engineering University of Melbourne Melbourne VIC Australia

98. Division of Cancer Research Peter MacCallum Cancer Centre Melbourne VIC Australia

99. Radiogenomics Laboratory Sunnybrook Health Sciences Centre Toronto ON Canada

100. Department of Clinical Studies, Ontario Veterinary College University of Guelph Guelph ON Canada

101. Department of Oncology Lakeshore Animal Health Partners Mississauga ON Canada

102. Centre for Advancing Responsible and Ethical Artificial Intelligence (CARE‐AI) University of Guelph Guelph ON Canada

103. Diagnostico de Salud Animal SA Ciudad de México Mexico

104. Department of Pathology and Laboratory Medicine Fondazione IRCCS Istituto Nazionale dei Tumori Milan Italy

105. Faculty of Medicine and Surgery University of Milan Milan Italy

106. Yale Cancer Center New Haven CT USA

107. Department of Medical Oncology Yale School of Medicine New Haven CT USA

108. University of Warwick Warwick UK

109. The Medical Oncology Centre of Rosebank Johannesburg South Africa

110. Department of Immunology, Faculty of Health Sciences University of Pretoria Pretoria South Africa

111. Institute of Pathology University Hospital Düsseldorf and Heinrich‐Heine‐University Düsseldorf Düsseldorf Germany

112. Pathology and Laboratory Medicine Memorial Sloan Kettering Cancer Center New York NY USA

113. Département de Médecine Oncologique Institute Gustave Roussy Villejuif France

114. Department of Medicine Yale University School of Medicine New Haven CT USA

115. Department of Diagnostic and Theranostic Medicine Institut Curie, University Paris‐Sciences et Lettres Paris France

116. Integrated Pathology Unit Institute of Cancer Research London UK

117. Precision Medicine Centre Queen's University Belfast Belfast UK

118. Department of Biomedical Informatics Stony Brook Medicine New York NY USA

119. Department of Pathology Aga Khan University Nairobi Kenya

120. Department of Pathology, Section of Breast Pathology Northwestern University Feinberg School of Medicine Chicago IL USA

121. Breast Cancer Translational Research Laboratory J.‐C. Heuson, Institut Jules Bordet Hôpital Universitaire de Bruxelles (HUB), Université Libre de Bruxelles (ULB) Brussels Belgium

122. Medical Oncology Department, Institut Jules Bordet, Hôpital Universitaire de Bruxelles (HUB) Université Libre de Bruxelles Brussels Belgium

123. Institute of Pathology University Hospital Heidelberg, Centers for Personalized Medicine (ZPM) Heidelberg Germany

124. King Hussein Cancer Center Amman Jordan

125. Department of Medical Oncology University of Medicine and Pharmacy “Iuliu Hatieganu” Cluj‐Napoca Romania

126. University of Texas MD Anderson Cancer Center Houston TX USA

127. Kyoto University Kyoto Japan

128. Tempus Labs Chicago IL USA

129. AI for Oncology Lab Netherlands Cancer Institute Amsterdam The Netherlands

130. Mayo Clinic Jacksonville FL USA

131. Pathology, and Institute of Clinical Medicine Aarhus University Hospital Aarhus Denmark

132. Department of Radiation Oncology University of Toronto and Sunnybrook Health Sciences Centre Toronto ON Canada

133. Department of Pathology Radboud University Medical Center Nijmegen The Netherlands

134. Department of Pathology University Medical Center Utrecht Utrecht The Netherlands

135. Johns Hopkins Oncology Center Baltimore MD USA

136. Department of Pathology European Institute of Oncology & University of Milan Milan Italy

137. Institute of Pathology Klinikum Bayreuth GmbH, Friedrich‐Alexander‐University Erlangen‐Nuremberg Bayreuth Germany

138. Tissue Image Analytics Centre, Department of Computer Science University of Warwick Coventry UK

139. CellCarta NV Antwerp Belgium

140. Fudan Medical University Shanghai Cancer Center Shanghai PR China

141. Translational Molecular Pathology, Division of Pathology and Laboratory Medicine The University of Texas MD Anderson Cancer Center Houston TX USA

142. Department of Medicine NYU Grossman School of Medicine Manhattan NY USA

143. University of Edinburgh Edinburgh UK

144. Department of Medicine and Research German Breast Group Neu‐Isenburg Germany

145. Institut für Pathologie Philipps‐Universität Marburg und Universitätsklinikum Marburg Marburg Germany

146. Sir Peter MacCallum Department of Medical Oncology University of Melbourne Melbourne VIC Australia

147. Sir Peter MacCallum Department of Oncology University of Melbourne Melbourne VIC Australia

148. Department of Pathology Herlev and Gentofte Hospital Herlev Denmark

149. Faculty of Health and Medical Sciences Copenhagen University Copenhagen Denmark

Abstract

AbstractModern histologic imaging platforms coupled with machine learning methods have provided new opportunities to map the spatial distribution of immune cells in the tumor microenvironment. However, there exists no standardized method for describing or analyzing spatial immune cell data, and most reported spatial analyses are rudimentary. In this review, we provide an overview of two approaches for reporting and analyzing spatial data (raster versus vector‐based). We then provide a compendium of spatial immune cell metrics that have been reported in the literature, summarizing prognostic associations in the context of a variety of cancers. We conclude by discussing two well‐described clinical biomarkers, the breast cancer stromal tumor infiltrating lymphocytes score and the colon cancer Immunoscore, and describe investigative opportunities to improve clinical utility of these spatial biomarkers. © 2023 The Pathological Society of Great Britain and Ireland.

Funder

Svenska Sällskapet för Medicinsk Forskning

DOD Peer Reviewed Cancer Research Program

U.S. Department of Defense

National Institutes of Health

National Health and Medical Research Council

Higher Education Authority

Irish Cancer Society

Breast Cancer Now

Cancer Research UK

Japan Society for the Promotion of Science

National Cancer Institute