DOI: https://doi.org/10.21203/rs.3.rs-15930/v1
Background: Bibliometric analysis of mainly cited articles is used to provide information on trends in a specific research field and objective indicators of the scientific impact of the publication. With bibliometric and network analysis, we map the scientific landscape of chimeric antigen receptors T-cells (CAR-T) research.
Methods: Extract 100 most cited articles published over the last decade (from January 1, 2009 to Dec 31, 2018; 10 years) from the Web of Science Core Collection with bibliographic details; year of publication, country of author, funding agencies, research organization, author information, and keywords.
Results: Of the 100 papers identified, most (92%) were written in the US. US government agencies and non-profit organizations provided the most funding, and the papers funded by the NIH had the most citations, followed by those funded by the Alliance for Cancer Gene Therapy (US). 33 papers out of the top 100 most cited papers were published from the University of Pennsylvania. As for authors, Carl H. June participated in 30 papers, followed by Bruce L. Levine who participated in 11 papers. As for journals, Blood (n=20), published the most papers, followed by Science Translational Medicine (n=10). The most frequently used keyword was “adoptive immunotherapy” (n=37), followed by “lymphocytes” (n=27), and “antitumor-activity” (n=25).
Conclusion: We performed the quantitative bibliometric analysis of funding bodies, countries, organizations, journals, authors, and keywords for the CAR-T research trends and landscape. Moving forward, Analysis of highly influential CAR-T articles provides insight into areas for future development.
This preprint is available for download as a PDF.
Table 1. Status of CAR-T approved by FDA or in Phase III clinical trials (as of July 1, 2019)
|
Kymriah®
|
Yescarta® (Axicabtagene
|
Lisocaptagene
(Liso-cel,
|
BB2121 |
Company |
Novartis |
Gilead (Kite) |
Celgene |
Celgene/Bluebird |
Format Co-stimaulation |
CARa-T;
|
CAR-T;
|
CAR-T;
|
CAR-T;
|
Phase III Name |
B-ALLb: ELINA/ DLBCLc: JULIET |
TOWER |
TRANSFORM |
RRMM |
Status |
Approved by USFDA |
Approved by USFDA |
Phase III (NCT03575351) |
Phase III
|
Cost (US) |
$475,000 for B-ALL;
|
$373,000 |
NAh |
NA |
Indication |
B-ALL, R/R DLBCL |
R/R DLBCL; PMBCLg |
R/R DLBCL; CLLi |
MMj |
Sourced T-Cell |
Patient PBMCse;
|
Patient PBMCs;
|
Patient CD4 and CD8 T
|
Patient PBMCs;
|
Vector |
Lentivirus |
Retrovirus |
Lentivirus |
Lentivirus |
Patient group (=No.) |
B-ALL=63, R/R DLBCL=93 |
101 |
73* |
33* |
ORR |
B-ALL=ND, DLBCL=52% |
83% |
80%* |
85%* |
CR |
B-ALL=83%, DLBCL=40% |
58% |
59%* |
45%* |
PR |
B-ALL=20%, DLBCL=12% |
25% |
21%* |
39% |
Median response
(months) |
B-ALL=NR, DLBCL=11.7m |
11.1m |
10.2m* |
11.8m* |
aCAR: chimeric antigen receptor, bB-ALL: B-cell acute lymphoblastic leukemia, cDLBCL: diffuse large B-cell lymphoma’dR/R: relapsed or refractory, ePBMC: peripheral blood mononuclear cells
fCD: cluster of differentiation, gPMBCL: primary mediastinal large B-cell lymphoma, hNA; not applicable, iCLL: chronic lymphocytic leukemia, jMM: multiple myeloma
*Data from the Phase I trial result
Table 2. Status of countries / funding organizations that top 100 cited publications related to CAR-T
Rank |
Country |
Number of Publications |
Funding Organizations |
Number of Publications |
ACPIa |
Sum of Times Cited |
1 |
USA |
92 |
NIH (USA) |
29 |
222.83 |
6462 |
2 |
Germany |
11 |
LLS (USA) |
8 |
264.38 |
2115 |
3 |
England |
5 |
NCI (USA) |
8 |
295.50 |
2364 |
4 |
Italy |
5 |
LRF (USA) |
7 |
145.00 |
1015 |
5 |
Canada |
4 |
NIH+NCI (USA) |
7 |
187.14 |
1310 |
6 |
China |
4 |
NCI+NIH+HHS (USA) |
6 |
118.00 |
708 |
7 |
Australia |
3 |
ACGT (USA) |
5 |
550.40 |
2752 |
8 |
Netherlands |
3 |
DOD (USA) |
5 |
170.40 |
852 |
9 |
France |
2 |
Novartis (SUI*) |
5 |
138.20 |
691 |
10 |
Israel |
2 |
Burroughs Wellcome Fund (USA) |
4 |
123.25 |
493 |
aACPI: Average Citations per Item field (average number of times a record has been cited) [10]
bNCI: National Cancer Institute; cLLS: Leukemia & Lymphoma Society; dNIH: National Institutes of Health;
eLRF: Lymphoma Research Foundation; fHHS: Health and Human Services; gACGT: Alliance for Cancer Gene Therapy; hDOD = Department of Defense; *Based on the location of the headquarters
Table 3. Status of journal titles that top 100 cited publications related to CAR-T
Rank |
Journal Titles (Country) |
Number of Publications |
APCIa |
Sum of Times Cited |
IFb |
1 |
Blood (USA) |
20 |
185.75 |
3715 |
16.56 |
2 |
Cancer Research (USA) |
10 |
132.00 |
1320 |
8.38 |
3 |
Science Translational Medicine (USA) |
10 |
376.80 |
3768 |
17.16 |
4 |
Clinical Cancer Research (USA) |
7 |
159.89 |
1119 |
8.91 |
5 |
Cancer Immunology Research (USA) |
6 |
168.83 |
1013 |
8.62 |
6 |
Journal of Clinical Investigation (USA) |
6 |
247.33 |
1484 |
12.28 |
7 |
Nature Reviews Clinical Oncology (USA) |
5 |
186.80 |
934 |
34.11 |
8 |
New England Journal of Medicine (USA) |
5 |
275.60 |
1378 |
70.67 |
9 |
Journal of Clinical Oncology (USA) |
4 |
300.25 |
1201 |
28.25 |
10 |
Nature Medicine (USA) |
4 |
168.75 |
675 |
30.64 |
aACPI: Average Citations per Item field (average number of times a record has been cited) [10]
bImpact factor is based on Journal Citation Reports in June 2019.
Table 4. The 100 most cited articles from the Journal of CAR-T
Title |
Journal |
Published year |
Total citation (n) |
T Cells with Chimeric Antigen Receptors Have Potent Antitumor Effects and Can Establish Memory in Patients with Advanced Leukemia |
SCIENCE TRANSLATIONAL MEDICINE |
2011 |
1,052 |
T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial |
LANCET |
2015 |
954 |
Efficacy and Toxicity Management of 19-28z CAR T Cell Therapy in B Cell Acute Lymphoblastic Leukemia |
SCIENCE TRANSLATIONAL MEDICINE |
2014 |
935 |
Chemotherapy-Refractory Diffuse Large B-Cell Lymphoma and Indolent B-Cell Malignancies Can Be Effectively Treated With Autologous T Cells Expressing an Anti-CD19 Chimeric Antigen Receptor |
JOURNAL OF CLINICAL ONCOLOGY |
2015 |
644 |
CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients |
JOURNAL OF CLINICAL INVESTIGATION |
2011 |
522 |
Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia |
SCIENCE TRANSLATIONAL MEDICINE |
2015 |
484 |
Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma |
BLOOD |
2011 |
465 |
CD19 CAR-T cells of defined CD4(+): CD8(+) composition in adult B cell ALL patients |
JOURNAL OF CLINICAL INVESTIGATION |
2016 |
424 |
Axicabtagene Ciloleucel CAR T-Cell Therapy in Refractory Large B-Cell Lymphoma |
NEW ENGLAND JOURNAL OF MEDICINE |
2017 |
380 |
Tisagenlecleucel in Children and Young Adults with B-Cell Lymphoblastic Leukemia |
NEW ENGLAND JOURNAL OF MEDICINE |
2018 |
347 |
Antibody-modified T cells: CARs take the front seat for hematologic malignancies |
BLOOD |
2014 |
331 |
Mesothelin-Specific Chimeric Antigen Receptor mRNA-Engineered T Cells Induce Antitumor Activity in Solid Malignancies |
CANCER IMMUNOLOGY RESEARCH |
2014 |
322 |
4-1BB costimulation ameliorates T cell exhaustion induced by tonic signaling of chimeric antigen receptors |
NATURE MEDICINE |
2015 |
308 |
Regression of Glioblastoma after Chimeric Antigen Receptor T-Cell Therapy |
NEW ENGLAND JOURNAL OF MEDICINE |
2016 |
283 |
Anti-PD-1 Antibody Therapy Potently Enhances the Eradication of Established Tumors By Gene-Modified T Cells |
CLINICAL CANCER RESEARCH |
2013 |
280 |
Human Epidermal Growth Factor Receptor 2 (HER2) -Specific Chimeric Antigen Receptor-Modified T Cells for the Immunotherapy of HER2-Positive Sarcoma |
JOURNAL OF CLINICAL ONCOLOGY |
2015 |
279 |
Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation |
BLOOD |
2013 |
269 |
Treatment of Metastatic Renal Cell Carcinoma With CAIX CAR-engineered T cells: Clinical Evaluation and Management of On-target Toxicity |
MOLECULAR THERAPY |
2013 |
263 |
Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning |
BLOOD |
2012 |
260 |
The future of cancer treatment: immunomodulation, CARs and combination immunotherapy |
NATURE REVIEWS CLINICAL ONCOLOGY |
2016 |
258 |
Targeting a CAR to the TRAC locus with CRISPR/Cas9 enhances tumour rejection |
NATURE |
2017 |
249 |
Immunotherapy of non-Hodgkin's lymphoma with a defined ratio of CD8(+) and CD4(+) CD19-specific chimeric antigen receptor-modified T cells |
SCIENCE TRANSLATIONAL MEDICINE |
2016 |
249 |
Decade-Long Safety and Function of Retroviral-Modified Chimeric Antigen Receptor T Cells |
SCIENCE TRANSLATIONAL MEDICINE |
2012 |
249 |
CD19-targeted chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia |
BLOOD |
2015 |
239 |
Long-Term Follow-up of CD19 CAR Therapy in Acute Lymphoblastic Leukemia |
NEW ENGLAND JOURNAL OF MEDICINE |
2018 |
225 |
Toxicities of chimeric antigen receptor T cells: recognition and management |
BLOOD |
2016 |
222 |
Multiple Injections of Electroporated Autologous T Cells Expressing a Chimeric Antigen Receptor Mediate Regression of Human Disseminated Tumor |
CANCER RESEARCH |
2010 |
219 |
Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors |
NATURE REVIEWS CLINICAL ONCOLOGY |
2013 |
215 |
The Principles of Engineering Immune Cells to Treat Cancer |
CELL |
2017 |
209 |
Molecular remission of infant B-ALL after infusion of universal TALEN gene-edited CAR T cells |
SCIENCE TRANSLATIONAL MEDICINE |
2017 |
206 |
T Cells Expressing Chimeric Antigen Receptors Can Cause Anaphylaxis in Humans |
CANCER IMMUNOLOGY RESEARCH |
2013 |
206 |
Chimeric antigen receptor T-cell therapy - assessment and management of toxicities |
NATURE REVIEWS CLINICAL ONCOLOGY |
2018 |
187 |
Identification of Predictive Biomarkers for Cytokine Release Syndrome after Chimeric Antigen Receptor T-cell Therapy for Acute Lymphoblastic Leukemia |
CANCER DISCOVERY |
2016 |
185 |
Toxicity and management in CAR T-cell therapy |
MOLECULAR THERAPY-ONCOLYTICS |
2016 |
182 |
Receptor Affinity and Extracellular Domain Modifications Affect Tumor Recognition by ROR1-Specific Chimeric Antigen Receptor T Cells |
CLINICAL CANCER RESEARCH |
2013 |
182 |
Design and development of therapies using chimeric antigen receptor-expressing T cells |
IMMUNOLOGICAL REVIEWS |
2014 |
181 |
Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor |
BLOOD |
2010 |
181 |
T cells expressing an anti-B-cell maturation antigen chimeric antigen receptor cause remissions of multiple myeloma |
BLOOD |
2016 |
178 |
Human CAR T cells with cell-intrinsic PD-1 checkpoint blockade resist tumor-mediated inhibition |
JOURNAL OF CLINICAL INVESTIGATION |
2016 |
178 |
Distinct Signaling of Coreceptors Regulates Specific Metabolism Pathways and Impacts Memory Development in CAR T Cells |
IMMUNITY |
2016 |
176 |
Expression of a Functional CCR2 Receptor Enhances Tumor Localization and Tumor Eradication by Retargeted Human T cells Expressing a Mesothelin-Specific Chimeric Antibody Receptor |
CLINICAL CANCER RESEARCH |
2011 |
174 |
Chimeric antigen receptor-modified T cells derived from defined CD8(+) and CD4(+) subsets confer superior antitumor reactivity in vivo |
LEUKEMIA |
2016 |
172 |
A foundation for universal T-cell based immunotherapy: T cells engineered to express a CD19-specific chimeric-antigen-receptor and eliminate expression of endogenous TCR |
BLOOD |
2012 |
172 |
Allogeneic T Cells That Express an Anti-CD19 Chimeric Antigen Receptor Induce Remissions of B-Cell Malignancies That Progress After Allogeneic Hematopoietic Stem-Cell Transplantation Without Causing Graft-Versus-Host Disease |
JOURNAL OF CLINICAL ONCOLOGY |
2016 |
171 |
CAR T cell immunotherapy for human cancer |
SCIENCE |
2018 |
164 |
Immune responses to transgene and retroviral vector in patients treated with ex vivo-engineered T cells |
BLOOD |
2011 |
163 |
A single dose of peripherally infused EGFRvIII-directed CAR T cells mediates antigen loss and induces adaptive resistance in patients with recurrent glioblastoma |
SCIENCE TRANSLATIONAL MEDICINE |
2017 |
162 |
Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies |
IMMUNOLOGICAL REVIEWS |
2015 |
162 |
Persistence and Efficacy of Second Generation CAR T Cell Against the LeY Antigen in Acute Myeloid Leukemia |
MOLECULAR THERAPY |
2013 |
159 |
Structural Design of Engineered Costimulation Determines Tumor Rejection Kinetics and Persistence of CAR T Cells |
CANCER CELL |
2015 |
158 |
Rational development and characterization of humanized anti-EGFR variant III chimeric antigen receptor T cells for glioblastoma |
SCIENCE TRANSLATIONAL MEDICINE |
2015 |
155 |
Regional delivery of mesothelin-targeted CAR T cell therapy generates potent and long-lasting CD4-dependent tumor immunity |
SCIENCE TRANSLATIONAL MEDICINE |
2014 |
153 |
T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and antitumor effects against human acute myeloid leukemia |
BLOOD |
2013 |
153 |
Closely related T-memory stem cells correlate with in vivo expansion of CAR.CD19-T cells and are preserved by IL-7 and IL-15 |
BLOOD |
2014 |
151 |
Driving CAR T-cells forward |
NATURE REVIEWS CLINICAL ONCOLOGY |
2016 |
149 |
In Vivo Persistence, Tumor Localization, and Antitumor Activity of CAR-Engineered T Cells Is Enhanced by Costimulatory Signaling through CD137 (4-1BB) |
CANCER RESEARCH |
2011 |
145 |
Recognition of Glioma Stem Cells by Genetically Modified T Cells Targeting EGFRvIII and Development of Adoptive Cell Therapy for Glioma |
HUMAN GENE THERAPY |
2012 |
143 |
IL-12 Release by Engineered T Cells Expressing Chimeric Antigen Receptors Can Effectively Muster an Antigen-Independent Macrophage Response on Tumor Cells That Have Shut Down Tumor Antigen Expression |
CANCER RESEARCH |
2011 |
143 |
Phase 1 Results of ZUMA-1: A Multicenter Study of KTE-C19 Anti-CD19 CAR T Cell Therapy in Refractory Aggressive Lymphoma |
MOLECULAR THERAPY |
2017 |
142 |
Acquisition of a CD19-negative myeloid phenotype allows immune escape of MLL-rearranged B-ALL from CD19 CAR-T-cell therapy |
BLOOD |
2016 |
141 |
Heparanase promotes tumor infiltration and antitumor activity of CAR-redirected T lymphocytes |
NATURE MEDICINE |
2015 |
141 |
Multifactorial T-cell Hypofunction That Is Reversible Can Limit the Efficacy of Chimeric Antigen Receptor-Transduced Human T cells in Solid Tumors |
CLINICAL CANCER RESEARCH |
2014 |
141 |
Multiplex Genome Editing to Generate Universal CAR T Cells Resistant to PD1 Inhibition |
CLINICAL CANCER RESEARCH |
2017 |
139 |
CD22-targeted CAR T cells induce remission in B-ALL that is naive or resistant to CD19-targeted CAR immunotherapy |
NATURE MEDICINE |
2018 |
138 |
The Nonsignaling Extracellular Spacer Domain of Chimeric Antigen Receptors Is Decisive for In Vivo Antitumor Activity |
CANCER IMMUNOLOGY RESEARCH |
2015 |
137 |
Multiplex Genome-Edited T-cell Manufacturing Platform for Off-the-Shelf Adoptive T-cell Immunotherapies |
CANCER RESEARCH |
2015 |
134 |
CD27 costimulation augments the survival and antitumor activity of redirected human T cells in vivo |
BLOOD |
2012 |
134 |
Endothelial Activation and Blood-Brain Barrier Disruption in Neurotoxicity after Adoptive Immunotherapy with CD19 CAR-T Cells |
CANCER DISCOVERY |
2017 |
127 |
Engineered CAR T Cells Targeting the Cancer-Associated Tn-Glycoform of the Membrane Mucin MUC1 Control Adenocarcinoma |
IMMUNITY |
2016 |
127 |
Intent-to-treat leukemia remission by CD19 CAR T cells of defined formulation and dose in children and young adults |
BLOOD |
2017 |
124 |
Phase I trials using Sleeping Beauty to generate CD19-specific CAR T cells |
JOURNAL OF CLINICAL INVESTIGATION |
2016 |
123 |
T Cells Expressing CD19/CD20 Bispecific Chimeric Antigen Receptors Prevent Antigen Escape by Malignant B Cells |
CANCER IMMUNOLOGY RESEARCH |
2016 |
117 |
Affinity-Tuned ErbB2 or EGFR Chimeric Antigen Receptor T Cells Exhibit an Increased Therapeutic Index against Tumors in Mice |
CANCER RESEARCH |
2015 |
115 |
Novel immunotherapies in lymphoid malignancies |
NATURE REVIEWS CLINICAL ONCOLOGY |
2016 |
114 |
Chimeric Antigen Receptor T Cells with Dissociated Signaling Domains Exhibit Focused Antitumor Activity with Reduced Potential for Toxicity In Vivo |
CANCER IMMUNOLOGY RESEARCH |
2013 |
112 |
Tandem CAR T cells targeting HER2 and IL13R alpha 2 mitigate tumor antigen escape |
JOURNAL OF CLINICAL INVESTIGATION |
2016 |
111 |
Cancer immunotherapy: harnessing the immune system to battle cancer |
JOURNAL OF CLINICAL INVESTIGATION |
2015 |
111 |
Targeting Fibroblast Activation Protein in Tumor Stroma with Chimeric Antigen Receptor T Cells Can Inhibit Tumor Growth and Augment Host Immunity without Severe Toxicity |
CANCER IMMUNOLOGY RESEARCH |
2014 |
111 |
CD19-targeted CAR T-cell therapeutics for hematologic malignancies: interpreting clinical outcomes to date |
BLOOD |
2016 |
108 |
A Chimeric Switch-Receptor Targeting PD1 Augments the Efficacy of Second-Generation CAR T Cells in Advanced Solid Tumors |
CANCER RESEARCH |
2016 |
106 |
Ibrutinib enhances chimeric antigen receptor T-cell engraftment and efficacy in leukemia |
BLOOD |
2016 |
106 |
Tuning Sensitivity of CAR to EGFR Density Limits Recognition of Normal Tissue While Maintaining Potent Antitumor Activity |
CANCER RESEARCH |
2015 |
105 |
ICOS-based chimeric antigen receptors program bipolar T(H)17/T(H)1 cells |
BLOOD |
2014 |
105 |
Mesothelin-Targeted CARs: Driving T Cells to Solid Tumors |
CANCER DISCOVERY |
2016 |
104 |
CAR-T cells and solid tumors: tuning T cells to challenge an inveterate foe |
TRENDS IN MOLECULAR MEDICINE |
2012 |
104 |
Phase I Hepatic Immunotherapy for Metastases Study of Intra-Arterial Chimeric Antigen Receptor-Modified T-cell Therapy for CEA(+) Liver Metastases |
CLINICAL CANCER RESEARCH |
2015 |
103 |
Chimeric Antigen Receptor Therapy |
NEW ENGLAND JOURNAL OF MEDICINE |
2018 |
102 |
Tumor-Promoting Desmoplasia Is Disrupted by Depleting FAP-Expressing Stromal Cells |
CANCER RESEARCH |
2015 |
102 |
Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template |
SCIENCE TRANSLATIONAL MEDICINE |
2015 |
101 |
Making Better Chimeric Antigen Receptors for Adoptive T-cell Therapy |
CLINICAL CANCER RESEARCH |
2016 |
97 |
Treatment of Advanced Leukemia in Mice with mRNA Engineered T Cells |
HUMAN GENE THERAPY |
2011 |
97 |
Kinetics and biomarkers of severe cytokine release syndrome after CD19 chimeric antigen receptor-modified T-cell therapy |
BLOOD |
2017 |
96 |
Durable Molecular Remissions in Chronic Lymphocytic Leukemia Treated With CD19-Specific Chimeric Antigen Receptor-Modified T Cells After Failure of Ibrutinib |
JOURNAL OF CLINICAL ONCOLOGY |
2017 |
95 |
Switch-mediated activation and retargeting of CAR-T cells for B-cell malignancies |
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA |
2016 |
94 |
Engineering CAR-T cells: Design concepts |
TRENDS IN IMMUNOLOGY |
2015 |
91 |
Global Manufacturing of CAR T Cell Therapy |
MOLECULAR THERAPY-METHODS & CLINICAL DEVELOPMENT |
2017 |
90 |
Reprogramming CD19-Specific T Cells with IL-21 Signaling Can Improve Adoptive Immunotherapy of B-Lineage Malignancies |
CANCER RESEARCH |
2011 |
88 |
Tumor indoleamine 2,3-dioxygenase (IDO) inhibits CD19-CAR T cells and is downregulated by lymphodepleting drugs |
BLOOD |
2015 |
87 |
Armed Oncolytic Virus Enhances Immune Functions of Chimeric Antigen Receptor-Modified T Cells in Solid Tumors |
CANCER RESEARCH |
2014 |
87 |
Chimeric Antigen Receptors Modified T-Cells for Cancer Therapy |
JNCI-JOURNAL OF THE NATIONAL CANCER INSTITUTE |
2016 |
86 |
The authorial organizations and affiliations of the top 10 were summarized in Table 5. We found that the most cited publications were authored in the University of Pennsylvania (n=33), followed by the University of Texas (n=15). However, the difference in citation frequency was more than double. These are then proceeded by the Memorial Sloan Kettering Cancer Center (n=14), University of Washington (n=13), and Fred Hutchinson Cancer Center (n=12; Table 5). The University of Pennsylvania is the top-cited publication, along with the most cited author (C. H. June; n=30). Subsequently, B. L. Levine (University of Pennsylvania) and S. R. Riddell (Fred Hutchinson Cancer Research Center) published 11 articles each, from the top 100 most cited papers. Also notable was that the organizations and authors of the top 10 most cited papers were all from the US.
Table 5. Status of institutions / authors (affiliations) organizations that top 100 cited publications related to CAR-T from 2009 to 2019
Rank |
Institutions |
Number of Publications |
Authors (Affiliation) |
Number of Publications |
ACPIa |
Sum of Times Cited |
1 |
University of Pennsylvania (UPENN) |
33 |
Carl H. June (UPENN) |
30 |
208.13 |
6244 |
2 |
University of Texas MD (UT MD) Anderson Cancer Center |
15 |
Bruce L. Levine (UPENN) |
11 |
314.00 |
3454 |
3 |
Memorial Sloan Kettering Cancer Center (MSKCC) |
14 |
Stanley R. Riddell
|
11 |
168.91 |
1858 |
4 |
University of Washington (UW) |
13 |
Gianpietro Dotti (UT MD) |
10 |
221.50 |
2215 |
5 |
Fred Hutchinson Cancer Center (FHCC) |
12 |
Michel Sadelain (MSKCC) |
9 |
265.22 |
2387 |
6 |
National Institutes of Health (NIH) |
11 |
John Scholler (UPENN) |
9 |
154.33 |
1389 |
7 |
National Cancer Institute (NCI) |
11 |
Michael C V Jensen (SCRI) |
8 |
196.63 |
1573 |
8 |
Seattle Children’s |
11 |
Steven M. Albelda (UPENN) |
7 |
182.71 |
1279 |
9 |
Baylor College of Medicine (BCM) |
10 |
Renier J. Brentjens (MSKCC) |
7 |
186.71 |
1159 |
10 |
Children’s Hospital of Philadelphia (CHOP) |
8 |
Stephan A. Grupp (CHOP) |
7 |
394.29 |
2760 |
aACPI: Average Citations per Item field (average number of times a record has been cited) [10]
Please verify. Table 3 is cited after Table 4. Consider reordering.
Table 6. Frequency of keyword that top 100 cited publications related to CAR-T from 2009 to Jun 2019
Keyword |
Frequency |
Keyword |
Frequency |
Adoptive immunotherapy |
37 |
Acute lymphoblastic-leukemia |
11 |
Lymphocytes |
27 |
Lymphoma |
10 |
Antitumor activity |
25 |
Sustained remissions |
10 |
Persistence |
19 |
Activation |
9 |
Cancer |
18 |
CD28 costimulation |
9 |
Expression |
17 |
Gene-therapy |
9 |
Therapy |
17 |
Phase-i |
9 |
In vivo |
13 |
Transplantation |
9 |
Leukemia |
13 |
Adverse event |
8 |
B-cell |
12 |
Chronic lymphocytic-leukemia |
7 |