The Interplay of Lung Cancer, COVID-19, and Vaccines
Abstract
:1. Introduction
2. COVID-19 and Lung Cancer
Population | Number of Patients with Lung Cancer | Hospitalization among Patients with Lung Cancer | Mortality among Patients with Lung Cancer | Reference |
---|---|---|---|---|
Adult patients with solid or hematological malignancies | 1135 | - | CFR 32.4% | [31] |
Patients with lung cancer from a single center in New York City | 102 | 63 (62%) | 25 (25%) | [32] |
Patients with thoracic cancers from eight countries | 200 | 152 (76%) | 66 (33%) | [30] |
Patients from 14 hospitals in China | 22 | - | 4 (18%) | [9] |
Patients from the Veneto region (Italy) | 21 | 13 (62%) | 5 (24%) | [33] |
Adult patients with cancer enrolled in the UK Coronavirus Cancer Monitoring Project (UKCCMP) | 111 | - | 43 (39%) | [34] |
Patients included in the Dutch Oncology COVID-19 Consortium registry | 47 | - | 22 (47) | [35] |
3. COVID-19 and Anticancer Treatment with Immune Checkpoint Inhibitors
4. COVID-19 Vaccines in Patients with Cancer
5. Discussion and Open Questions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- King, J.; Criswell, A.; Mohon, R.; Fine, L. FP13.03 The Impact of the COVID-19 Pandemic on Lung Cancer Screening Programs in the United States. J. Thorac. Oncol. 2021, 16, S969. [Google Scholar] [CrossRef]
- Kaufman, H.W.; Chen, Z.; Niles, J.; Fesko, Y. Changes in the Number of US Patients With Newly Identified Cancer Before and During the Coronavirus Disease 2019 (COVID-19) Pandemic. JAMA Netw. Open 2020, 3, e2017267. [Google Scholar] [CrossRef] [PubMed]
- Maringe, C.; Spicer, J.; Morris, M.; Purushotham, A.; Nolte, E.; Sullivan, R.; Rachet, B.; Aggarwal, A. The Impact of the COVID-19 Pandemic on Cancer Deaths Due to Delays in Diagnosis in England, UK: A National, Population-Based, Modelling Study. Lancet Oncol. 2020, 21, 1023–1034. [Google Scholar] [CrossRef] [PubMed]
- Van Haren, R.M.; Delman, A.M.; Turner, K.M.; Waits, B.; Hemingway, M.; Shah, S.A.; Starnes, S.L. Impact of the COVID-19 Pandemic on Lung Cancer Screening Program and Subsequent Lung Cancer. J. Am. Coll. Surg. 2021, 232, 600–605. [Google Scholar] [CrossRef] [PubMed]
- Ministarstvo Zdravsta. Nacionalni Program Za Probir I Rano Otkrivanje Raka Pluća 2020–2024; Ministarstvo Zdravstva Zagreb: Zagreb, Croatia, 2020.
- Rolfo, C.; Meshulami, N.; Russo, A.; Krammer, F.; García-Sastre, A.; Mack, P.C.; Gomez, J.E.; Bhardwaj, N.; Benyounes, A.; Sirera, R.; et al. Lung Cancer and Severe Acute Respiratory Syndrome Coronavirus 2 Infection: Identifying Important Knowledge Gaps for Investigation. J. Thorac. Oncol. 2022, 17, 214–227. [Google Scholar] [CrossRef]
- Aboueshia, M.; Hussein, M.H.; Attia, A.S.; Swinford, A.; Miller, P.; Omar, M.; Toraih, E.A.; Saba, N.; Safah, H.; Duchesne, J.; et al. Cancer and COVID-19: Analysis of Patient Outcomes. Future Oncol. 2021, 17, 3499–3510. [Google Scholar] [CrossRef]
- Guan, W.; Liang, W.; Zhao, Y.; Liang, H.; Chen, Z.; Li, Y.; Liu, X.; Chen, R.; Tang, C.; Wang, T.; et al. Comorbidity and Its Impact on 1590 Patients with COVID-19 in China: A Nationwide Analysis. Eur. Respir. J. 2020, 55, 2000547. [Google Scholar] [CrossRef] [Green Version]
- Liang, W.; Guan, W.; Chen, R.; Wang, W.; Li, J.; Xu, K.; Li, C.; Ai, Q.; Lu, W.; Liang, H.; et al. Cancer Patients in SARS-CoV-2 Infection: A Nationwide Analysis in China. Lancet Oncol. 2020, 21, 335–337. [Google Scholar] [CrossRef]
- Yu, J.; Ouyang, W.; Chua, M.L.K.; Xie, C. SARS-CoV-2 Transmission in Patients With Cancer at a Tertiary Care Hospital in Wuhan, China. JAMA Oncol. 2020, 6, 1108. [Google Scholar] [CrossRef] [Green Version]
- Desai, A.; Sachdeva, S.; Parekh, T.; Desai, R. COVID-19 and Cancer: Lessons From a Pooled Meta-Analysis. JCO Glob. Oncol. 2020, 6, 557–559. [Google Scholar] [CrossRef]
- Yang, L.; Chai, P.; Yu, J.; Fan, X. Effects of Cancer on Patients with COVID-19: A Systematic Review and Meta-Analysis of 63,019 Participants. Cancer Biol. Med. 2021, 18, 298–307. [Google Scholar] [CrossRef] [PubMed]
- Blimark, C.; Holmberg, E.; Mellqvist, U.-H.; Landgren, O.; Bjorkholm, M.; Hultcrantz, M.; Kjellander, C.; Turesson, I.; Kristinsson, S.Y. Multiple Myeloma and Infections: A Population-Based Study on 9253 Multiple Myeloma Patients. Haematologica 2015, 100, 107–113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moujaess, E.; Kourie, H.R.; Ghosn, M. Cancer Patients and Research during COVID-19 Pandemic: A Systematic Review of Current Evidence. Crit. Rev. Oncol./Hematol. 2020, 150, 102972. [Google Scholar] [CrossRef]
- Qu, J.; Yang, R.; Song, L.; Kamel, I.R. Atypical Lung Feature on Chest CT in a Lung Adenocarcinoma Cancer Patient Infected with COVID-19. Ann. Oncol. 2020, 31, 825–826. [Google Scholar] [CrossRef] [PubMed]
- Zhu, W.J.; Wang, J.; He, X.H.; Qin, Y.; Yang, S.; Hu, X.S.; Wang, H.Y.; Huang, J.; Zhou, A.P.; Ma, F.; et al. The differential diagnosis of pulmonary infiltrates in cancer patients during the outbreak of the 2019 novel coronavirus disease. Zhonghua Zhong Liu Za Zhi 2020, 42, 305–311. [Google Scholar] [CrossRef] [PubMed]
- Jin, X.-H.; Zheng, K.I.; Pan, K.-H.; Xie, Y.-P.; Zheng, M.-H. COVID-19 in a Patient with Chronic Lymphocytic Leukaemia. Lancet Haematol. 2020, 7, e351–e352. [Google Scholar] [CrossRef]
- Das, S.; Johnson, D.B. Immune-Related Adverse Events and Anti-Tumor Efficacy of Immune Checkpoint Inhibitors. J. ImmunoTher. Cancer 2019, 7, 306. [Google Scholar] [CrossRef]
- Quach, H.; Dewan, A.; Davis, E.; Ancell, K.; Fan, R.; Ye, F.; Johnson, D. Association of Anti–Programmed Cell Death 1 Cutaneous Toxic Effects With Outcomes in Patients With Advanced Melanoma. JAMA Oncol. 2019, 5, 906–908. [Google Scholar] [CrossRef]
- Eggermont, A.M.M.; Kicinski, M.; Blank, C.U.; Mandala, M.; Long, G.V.; Atkinson, V.; Dalle, S.; Haydon, A.; Khattak, A.; Carlino, M.S.; et al. Association Between Immune-Related Adverse Events and Recurrence-Free Survival Among Patients With Stage III Melanoma Randomized to Receive Pembrolizumab or Placebo: A Secondary Analysis of a Randomized Clinical Trial. JAMA Oncol. 2020, 6, 519–527. [Google Scholar] [CrossRef] [Green Version]
- Gorospe, L.; Ayala-Carbonero, A.M.; Paredes-Rodríguez, P.; Muñoz-Molina, G.M.; Arrieta, P.; Mirambeaux-Villalona, R.M.; Vallejo-Ocaña, M.C.; Benito-Berlinches, A.; Lage-Alfranca, Y.; Gómez-Rueda, A. Challenges in Management of Patients With Lung Cancer in Times of COVID-19: An Imaging Perspective. Clin. Lung Cancer 2020, 21, 568–570. [Google Scholar] [CrossRef]
- Zhang, Y.-J.; Yang, W.-J.; Liu, D.; Cao, Y.-Q.; Zheng, Y.-Y.; Han, Y.-C.; Jin, R.-S.; Han, Y.; Wang, X.-Y.; Pan, A.-S.; et al. COVID-19 and Early-Stage Lung Cancer Both Featuring Ground-Glass Opacities: A Propensity Score-Matched Study. Transl. Lung Cancer Res. 2020, 9, 1516–1527. [Google Scholar] [CrossRef] [PubMed]
- Zhu, J.; Zhang, Y.; Gao, X.-H.; Xi, E.-P. Coronavirus Disease 2019 or Lung Cancer: A Differential Diagnostic Experience and Management Model From Wuhan. J. Thorac. Oncol. 2020, 15, e141–e142. [Google Scholar] [CrossRef] [PubMed]
- Rogiers, A.; Pires da Silva, I.; Tentori, C.; Tondini, C.A.; Grimes, J.M.; Trager, M.H.; Nahm, S.; Zubiri, L.; Manos, M.; Bowling, P.; et al. Clinical Impact of COVID-19 on Patients with Cancer Treated with Immune Checkpoint Inhibition. J. Immunother. Cancer 2021, 9, e001931. [Google Scholar] [CrossRef] [PubMed]
- Dobre, I.A.; Frank, A.J.; D’Silva, K.M.; Christiani, D.C.; Okin, D.; Sharma, A.; Montesi, S.B. Outcomes of Patients With Interstitial Lung Disease Receiving Programmed Cell Death 1 Inhibitors: A Retrospective Case Series. Clin. Lung Cancer 2021, 22, e738–e744. [Google Scholar] [CrossRef] [PubMed]
- Sullivan, R.J.; Johnson, D.B.; Rini, B.I.; Neilan, T.G.; Lovly, C.M.; Moslehi, J.J.; Reynolds, K.L. COVID-19 and Immune Checkpoint Inhibitors: Initial Considerations. J. Immunother. Cancer 2020, 8, e000933. [Google Scholar] [CrossRef] [PubMed]
- Johnson, D.B.; Taylor, K.B.; Cohen, J.V.; Ayoubi, N.; Haugh, A.M.; Wang, D.Y.; Schlick, B.D.; Voorhees, A.L.; Gage, K.L.; Fintelmann, F.J.; et al. Anti–PD-1–Induced Pneumonitis Is Associated with Persistent Imaging Abnormalities in Melanoma Patients. Cancer Immunol. Res. 2019, 7, 1755–1759. [Google Scholar] [CrossRef] [PubMed]
- Aschele, C.; Negru, M.E.; Pastorino, A.; Cavanna, L.; Zagonel, V.; Barone-Adesi, F.; Blasi, L. Incidence of SARS-CoV-2 Infection Among Patients Undergoing Active Antitumor Treatment in Italy. JAMA Oncol. 2021, 7, 304. [Google Scholar] [CrossRef]
- Wang, Q.; Berger, N.A.; Xu, R. Analyses of Risk, Racial Disparity, and Outcomes Among US Patients With Cancer and COVID-19 Infection. JAMA Oncol. 2021, 7, 220–227. [Google Scholar] [CrossRef]
- Garassino, M.C.; Whisenant, J.G.; Huang, L.-C.; Trama, A.; Torri, V.; Agustoni, F.; Baena, J.; Banna, G.; Berardi, R.; Bettini, A.C.; et al. COVID-19 in Patients with Thoracic Malignancies (TERAVOLT): First Results of an International, Registry-Based, Cohort Study. Lancet Oncol. 2020, 21, 914–922. [Google Scholar] [CrossRef]
- Tagliamento, M.; Agostinetto, E.; Bruzzone, M.; Ceppi, M.; Saini, K.S.; de Azambuja, E.; Punie, K.; Westphalen, C.B.; Morgan, G.; Pronzato, P.; et al. Mortality in Adult Patients with Solid or Hematological Malignancies and SARS-CoV-2 Infection with a Specific Focus on Lung and Breast Cancers: A Systematic Review and Meta-Analysis. Crit. Rev. Oncol. Hematol. 2021, 163, 103365. [Google Scholar] [CrossRef]
- Luo, J.; Rizvi, H.; Preeshagul, I.R.; Egger, J.V.; Hoyos, D.; Bandlamudi, C.; McCarthy, C.G.; Falcon, C.J.; Schoenfeld, A.J.; Arbour, K.C.; et al. COVID-19 in Patients with Lung Cancer. Ann. Oncol. 2020, 31, 1386–1396. [Google Scholar] [CrossRef] [PubMed]
- Rugge, M.; Zorzi, M.; Guzzinati, S. SARS-CoV-2 Infection in the Italian Veneto Region: Adverse Outcomes in Patients with Cancer. Nat. Cancer 2020, 1, 784–788. [Google Scholar] [CrossRef] [PubMed]
- Lee, L.Y.W.; Cazier, J.-B.; Starkey, T.; Briggs, S.E.W.; Arnold, R.; Bisht, V.; Booth, S.; Campton, N.A.; Cheng, V.W.T.; Collins, G.; et al. COVID-19 Prevalence and Mortality in Patients with Cancer and the Effect of Primary Tumour Subtype and Patient Demographics: A Prospective Cohort Study. Lancet Oncol. 2020, 21, 1309–1316. [Google Scholar] [CrossRef] [PubMed]
- de Joode, K.; Dumoulin, D.W.; Tol, J.; Westgeest, H.M.; Beerepoot, L.V.; van den Berkmortel, F.W.P.J.; Mutsaers, P.G.N.J.; van Diemen, N.G.J.; Visser, O.J.; Oomen-de Hoop, E.; et al. Dutch Oncology COVID-19 Consortium: Outcome of COVID-19 in Patients with Cancer in a Nationwide Cohort Study. Eur. J. Cancer 2020, 141, 171–184. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, R.; Costa de Oliveira, S. The Impact of Angiotensin-Converting Enzyme 2 (ACE2) Expression Levels in Patients with Comorbidities on COVID-19 Severity: A Comprehensive Review. Microorganisms 2021, 9, 1692. [Google Scholar] [CrossRef]
- Winkler, T.; Ben-David, U. Elevated Expression of ACE2 in Tumor-Adjacent Normal Tissues of Cancer Patients. Int. J. Cancer 2020, 147, 3264–3266. [Google Scholar] [CrossRef]
- Liu, A.; Zhang, X.; Li, R.; Zheng, M.; Yang, S.; Dai, L.; Wu, A.; Hu, C.; Huang, Y.; Xie, M.; et al. Overexpression of the SARS-CoV-2 Receptor ACE2 Is Induced by Cigarette Smoke in Bronchial and Alveolar Epithelia. J. Pathol. 2021, 253, 17–30. [Google Scholar] [CrossRef]
- Jia, W.; Wang, J.; Sun, B.; Zhou, J.; Shi, Y.; Zhou, Z. The Mechanisms and Animal Models of SARS-CoV-2 Infection. Front. Cell Dev. Biol. 2021, 9, 1129. [Google Scholar] [CrossRef]
- Howells, A.; Marelli, G.; Lemoine, N.R.; Wang, Y. Oncolytic Viruses—Interaction of Virus and Tumor Cells in the Battle to Eliminate Cancer. Front. Oncol. 2017, 7, 195. [Google Scholar] [CrossRef] [Green Version]
- Shang, C.; Liu, Z.; Zhu, Y.; Lu, J.; Ge, C.; Zhang, C.; Li, N.; Jin, N.; Li, Y.; Tian, M.; et al. SARS-CoV-2 Causes Mitochondrial Dysfunction and Mitophagy Impairment. Front. Microbiol. 2022, 12, 780768. [Google Scholar] [CrossRef]
- Taghizadeh-Hesary, F.; Akbari, H.; Bahadori, M.; Behnam, B. Targeted Anti-Mitochondrial Therapy: The Future of Oncology. Genes 2022, 13, 1728. [Google Scholar] [CrossRef] [PubMed]
- Topalian, S.L.; Hodi, F.S.; Brahmer, J.R.; Gettinger, S.N.; Smith, D.C.; McDermott, D.F.; Powderly, J.D.; Sosman, J.A.; Atkins, M.B.; Leming, P.D.; et al. Five-Year Survival and Correlates Among Patients With Advanced Melanoma, Renal Cell Carcinoma, or Non-Small Cell Lung Cancer Treated With Nivolumab. JAMA Oncol. 2019, 5, 1411–1420. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ribas, A.; Wolchok, J.D. Cancer Immunotherapy Using Checkpoint Blockade. Science 2018, 359, 1350–1355. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pardoll, D.M. The Blockade of Immune Checkpoints in Cancer Immunotherapy. Nat. Rev. Cancer 2012, 12, 252–264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bersanelli, M. Controversies about COVID-19 and Anticancer Treatment with Immune Checkpoint Inhibitors. Immunotherapy 2020, 12, 269–273. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grivas, P.; Khaki, A.R.; Wise-Draper, T.M.; French, B.; Hennessy, C.; Hsu, C.-Y.; Shyr, Y.; Li, X.; Choueiri, T.K.; Painter, C.A.; et al. Association of Clinical Factors and Recent Anticancer Therapy with COVID-19 Severity among Patients with Cancer: A Report from the COVID-19 and Cancer Consortium. Ann. Oncol. 2021, 32, 787–800. [Google Scholar] [CrossRef]
- Kuderer, N.M.; Choueiri, T.K.; Shah, D.P.; Shyr, Y.; Rubinstein, S.M.; Rivera, D.R.; Shete, S.; Hsu, C.-Y.; Desai, A.; de Lima Lopes, G.; et al. Clinical Impact of COVID-19 on Patients with Cancer (CCC19): A Cohort Study. Lancet 2020, 395, 1907–1918. [Google Scholar] [CrossRef]
- Chen, C.; Zhang, X.R.; Ju, Z.Y.; He, W.F. Advances in the research of mechanism and related immunotherapy on the cytokine storm induced by coronavirus disease 2019. Zhonghua Shao Shang Za Zhi 2020, 36, 471–475. [Google Scholar] [CrossRef]
- Xu, Z.; Shi, L.; Wang, Y.; Zhang, J.; Huang, L.; Zhang, C.; Liu, S.; Zhao, P.; Liu, H.; Zhu, L.; et al. Pathological Findings of COVID-19 Associated with Acute Respiratory Distress Syndrome. Lancet Respir. Med. 2020, 8, 420–422. [Google Scholar] [CrossRef]
- Barrière, J.; Re, D.; Peyrade, F.; Carles, M. Current Perspectives for SARS-CoV-2 Vaccination Efficacy Improvement in Patients with Active Treatment against Cancer. Eur. J. Cancer 2021, 154, 66–72. [Google Scholar] [CrossRef]
- Goshen-Lago, T.; Waldhorn, I.; Holland, R.; Szwarcwort-Cohen, M.; Reiner-Benaim, A.; Shachor-Meyouhas, Y.; Hussein, K.; Fahoum, L.; Baruch, M.; Peer, A.; et al. Serologic Status and Toxic Effects of the SARS-CoV-2 BNT162b2 Vaccine in Patients Undergoing Treatment for Cancer. JAMA Oncol. 2021, 7, 1507–1513. [Google Scholar] [CrossRef] [PubMed]
- Massarweh, A.; Eliakim-Raz, N.; Stemmer, A.; Levy-Barda, A.; Yust-Katz, S.; Zer, A.; Benouaich-Amiel, A.; Ben-Zvi, H.; Moskovits, N.; Brenner, B.; et al. Evaluation of Seropositivity Following BNT162b2 Messenger RNA Vaccination for SARS-CoV-2 in Patients Undergoing Treatment for Cancer. JAMA Oncol. 2021, 7, 1133–1140. [Google Scholar] [CrossRef]
- Thakkar, A.; Gonzalez-Lugo, J.D.; Goradia, N.; Gali, R.; Shapiro, L.C.; Pradhan, K.; Rahman, S.; Kim, S.Y.; Ko, B.; Sica, R.A.; et al. Seroconversion Rates Following COVID-19 Vaccination among Patients with Cancer. Cancer Cell 2021, 39, 1081–1090.e2. [Google Scholar] [CrossRef] [PubMed]
- Addeo, A.; Shah, P.K.; Bordry, N.; Hudson, R.D.; Albracht, B.; Di Marco, M.; Kaklamani, V.; Dietrich, P.-Y.; Taylor, B.S.; Simand, P.-F.; et al. Immunogenicity of SARS-CoV-2 Messenger RNA Vaccines in Patients with Cancer. Cancer Cell 2021, 39, 1091–1098.e2. [Google Scholar] [CrossRef] [PubMed]
- Monin, L.; Laing, A.G.; Muñoz-Ruiz, M.; McKenzie, D.R.; Del Barrio, I.D.M.; Alaguthurai, T.; Domingo-Vila, C.; Hayday, T.S.; Graham, C.; Seow, J.; et al. Safety and Immunogenicity of One versus Two Doses of the COVID-19 Vaccine BNT162b2 for Patients with Cancer: Interim Analysis of a Prospective Observational Study. Lancet Oncol. 2021, 22, 765–778. [Google Scholar] [CrossRef] [PubMed]
- Waissengrin, B.; Agbarya, A.; Safadi, E.; Padova, H.; Wolf, I. Short-Term Safety of the BNT162b2 MRNA COVID-19 Vaccine in Patients with Cancer Treated with Immune Checkpoint Inhibitors. Lancet Oncol. 2021, 22, 581–583. [Google Scholar] [CrossRef]
- Rossi, G.; Pezzuto, A.; Sini, C.; Tuzi, A.; Citarella, F.; McCusker, M.G.; Nigro, O.; Tanda, E.; Russo, A. Concomitant Medications during Immune Checkpoint Blockage in Cancer Patients: Novel Insights in This Emerging Clinical Scenario. Crit. Rev. Oncol. Hematol. 2019, 142, 26–34. [Google Scholar] [CrossRef]
- Fendler, A.; Shepherd, S.T.C.; Au, L.; Wilkinson, K.A.; Wu, M.; Byrne, F.; Cerrone, M.; Schmitt, A.M.; Joharatnam-Hogan, N.; Shum, B.; et al. Adaptive Immunity and Neutralizing Antibodies against SARS-CoV-2 Variants of Concern Following Vaccination in Patients with Cancer: The CAPTURE Study. Nat. Cancer 2021, 2, 1305–1320. [Google Scholar] [CrossRef]
- Oosting, S.F.; van der Veldt, A.A.M.; GeurtsvanKessel, C.H.; Fehrmann, R.S.N.; van Binnendijk, R.S.; Dingemans, A.-M.C.; Smit, E.F.; Hiltermann, T.J.N.; den Hartog, G.; Jalving, M.; et al. MRNA-1273 COVID-19 Vaccination in Patients Receiving Chemotherapy, Immunotherapy, or Chemoimmunotherapy for Solid Tumours: A Prospective, Multicentre, Non-Inferiority Trial. Lancet Oncol. 2021, 22, 1681–1691. [Google Scholar] [CrossRef]
- Shroff, R.T.; Chalasani, P.; Wei, R.; Pennington, D.; Quirk, G.; Schoenle, M.V.; Peyton, K.L.; Uhrlaub, J.L.; Ripperger, T.J.; Jergović, M.; et al. Immune Responses to COVID-19 MRNA Vaccines in Patients with Solid Tumors on Active, Immunosuppressive Cancer Therapy. medRxiv 2021. [Google Scholar] [CrossRef]
- Stampfer, S.D.; Goldwater, M.-S.; Jew, S.; Bujarski, S.; Regidor, B.; Daniely, D.; Chen, H.; Xu, N.; Li, M.; Green, T.; et al. Response to MRNA Vaccination for COVID-19 among Patients with Multiple Myeloma. Leukemia 2021, 35, 3534–3541. [Google Scholar] [CrossRef] [PubMed]
- Benjamini, O.; Rokach, L.; Itchaki, G.; Braester, A.; Shvidel, L.; Goldschmidt, N.; Shapira, S.; Dally, N.; Avigdor, A.; Rahav, G.; et al. Safety and Efficacy of the BNT162b MRNA COVID-19 Vaccine in Patients with Chronic Lymphocytic Leukemia. Haematologica 2022, 107, 625–634. [Google Scholar] [CrossRef] [PubMed]
- Yatim, N.; Boussier, J.; Tetu, P.; Smith, N.; Bruel, T.; Charbit, B.; Barnabei, L.; Corneau, A.; Da Meda, L.; Allayous, C.; et al. Immune Checkpoint Inhibitors Increase T Cell Immunity during SARS-CoV-2 Infection. Sci. Adv. 2021, 7, eabg4081. [Google Scholar] [CrossRef] [PubMed]
- Greenberger, L.M.; Saltzman, L.A.; Senefeld, J.W.; Johnson, P.W.; DeGennaro, L.J.; Nichols, G.L. Antibody Response to SARS-CoV-2 Vaccines in Patients with Hematologic Malignancies. Cancer Cell 2021, 39, 1031–1033. [Google Scholar] [CrossRef]
- Oosting, S.; Veldt, A.A.M.; Geurtsvankessel, C.; Fehrmann, R.S.N.; Binnendijk, R.S.; Dingemans, A.-M.C.; Smit, E.F.F.; Hiltermann, T.; Hartog, G.; Jalving, M.; et al. LBA8 Vaccination against SARS-CoV-2 in Patients Receiving Chemotherapy, Immunotherapy, or Chemo-Immunotherapy for Solid Tumors. Ann. Oncol. 2021, 32, S1337. [Google Scholar] [CrossRef]
- Ehmsen, S.; Asmussen, A.; Jeppesen, S.S.; Nilsson, A.C.; Østerlev, S.; Vestergaard, H.; Justesen, U.S.; Johansen, I.S.; Frederiksen, H.; Ditzel, H.J. Antibody and T Cell Immune Responses Following MRNA COVID-19 Vaccination in Patients with Cancer. Cancer Cell 2021, 39, 1034–1036. [Google Scholar] [CrossRef]
- Embi, P.J. Effectiveness of 2-Dose Vaccination with MRNA COVID-19 Vaccines Against COVID-19–Associated Hospitalizations Among Immunocompromised Adults—Nine States, January–September 2021. MMWR Morb. Mortal. Wkly. Rep. 2021, 70, 1553–1559. [Google Scholar] [CrossRef]
- Gounant, V.; Ferré, V.M.; Soussi, G.; Charpentier, C.; Flament, H.; Fidouh, N.; Collin, G.; Namour, C.; Assoun, S.; Bizot, A.; et al. Efficacy of Severe Acute Respiratory Syndrome Coronavirus-2 Vaccine in Patients With Thoracic Cancer: A Prospective Study Supporting a Third Dose in Patients With Minimal Serologic Response After Two Vaccine Doses. J. Thorac. Oncol. 2022, 17, 239–251. [Google Scholar] [CrossRef]
- Linardou, H.; Spanakis, N.; Koliou, G.-A.; Christopoulou, A.; Karageorgopoulou, S.; Alevra, N.; Vagionas, A.; Tsoukalas, N.; Sgourou, S.; Fountzilas, E.; et al. Responses to SARS-CoV-2 Vaccination in Patients with Cancer (ReCOVer Study): A Prospective Cohort Study of the Hellenic Cooperative Oncology Group. Cancers 2021, 13, 4621. [Google Scholar] [CrossRef]
- Shmueli, E.S.; Itay, A.; Margalit, O.; Berger, R.; Halperin, S.; Jurkowicz, M.; Levin, E.G.; Levy, I.; Olmer, L.; Regev-Yochay, G.; et al. Efficacy and Safety of BNT162b2 Vaccination in Patients with Solid Cancer Receiving Anticancer Therapy—A Single Centre Prospective Study. Eur. J. Cancer 2021, 157, 124–131. [Google Scholar] [CrossRef]
- Ligumsky, H.; Safadi, E.; Etan, T.; Vaknin, N.; Waller, M.; Croll, A.; Nikolaevski-Berlin, A.; Greenberg, I.; Halperin, T.; Wasserman, A.; et al. Immunogenicity and Safety of the BNT162b2 MRNA COVID-19 Vaccine Among Actively Treated Cancer Patients. JNCI J. Natl. Cancer Inst. 2022, 114, 203–209. [Google Scholar] [CrossRef]
- Barrière, J.; Chamorey, E.; Adjtoutah, Z.; Castelnau, O.; Mahamat, A.; Marco, S.; Petit, E.; Leysalle, A.; Raimondi, V.; Carles, M. Impaired Immunogenicity of BNT162b2 Anti-SARS-CoV-2 Vaccine in Patients Treated for Solid Tumors. Ann. Oncol. 2021, 32, 1053–1055. [Google Scholar] [CrossRef] [PubMed]
- Becerril-Gaitan, A.; Vaca-Cartagena, B.F.; Ferrigno, A.S.; Mesa-Chavez, F.; Barrientos-Gutiérrez, T.; Tagliamento, M.; Lambertini, M.; Villarreal-Garza, C. Immunogenicity and Risk of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection after Coronavirus Disease 2019 (COVID-19) Vaccination in Patients with Cancer: A Systematic Review and Meta-Analysis. Eur. J. Cancer 2022, 160, 243–260. [Google Scholar] [CrossRef] [PubMed]
- Mair, M.J.; Berger, J.M.; Berghoff, A.S.; Starzer, A.M.; Ortmayr, G.; Puhr, H.C.; Steindl, A.; Perkmann, T.; Haslacher, H.; Strassl, R.; et al. Humoral Immune Response in Hematooncological Patients and Health Care Workers Who Received SARS-CoV-2 Vaccinations. JAMA Oncol. 2022, 8, 106–113. [Google Scholar] [CrossRef] [PubMed]
- Peeters, M.; Verbruggen, L.; Teuwen, L.; Vanhoutte, G.; Vande Kerckhove, S.; Peeters, B.; Raats, S.; Van der Massen, I.; De Keersmaecker, S.; Debie, Y.; et al. Reduced Humoral Immune Response after BNT162b2 Coronavirus Disease 2019 Messenger RNA Vaccination in Cancer Patients under Antineoplastic Treatment. ESMO Open 2021, 6, 100274. [Google Scholar] [CrossRef] [PubMed]
- Rousseau, B.; Loulergue, P.; Mir, O.; Krivine, A.; Kotti, S.; Viel, E.; Simon, T.; de Gramont, A.; Goldwasser, F.; Launay, O.; et al. Immunogenicity and Safety of the Influenza A H1N1v 2009 Vaccine in Cancer Patients Treated with Cytotoxic Chemotherapy and/or Targeted Therapy: The VACANCE Study. Ann. Oncol. 2012, 23, 450–457. [Google Scholar] [CrossRef]
- Mazzone, P.J.; Gould, M.K.; Arenberg, D.A.; Chen, A.C.; Choi, H.K.; Detterbeck, F.C.; Farjah, F.; Fong, K.M.; Iaccarino, J.M.; Janes, S.M.; et al. Management of Lung Nodules and Lung Cancer Screening During the COVID-19 Pandemic: CHEST Expert Panel Report. Radiol. Imaging Cancer 2020, 2, e204013. [Google Scholar] [CrossRef] [Green Version]
- Wu, J.T.-Y.; La, J.; Branch-Elliman, W.; Huhmann, L.B.; Han, S.S.; Parmigiani, G.; Tuck, D.P.; Brophy, M.T.; Do, N.V.; Lin, A.Y.; et al. Association of COVID-19 Vaccination With SARS-CoV-2 Infection in Patients With Cancer: A US Nationwide Veterans Affairs Study. JAMA Oncol. 2022, 8, 281–286. [Google Scholar] [CrossRef]
- Hippisley-Cox, J.; Coupland, C.A.; Mehta, N.; Keogh, R.H.; Diaz-Ordaz, K.; Khunti, K.; Lyons, R.A.; Kee, F.; Sheikh, A.; Rahman, S.; et al. Risk Prediction of COVID-19 Related Death and Hospital Admission in Adults after COVID-19 Vaccination: National Prospective Cohort Study. BMJ 2021, 374, n2244. [Google Scholar] [CrossRef]
- Valanparambil, R.M.; Carlisle, J.; Linderman, S.L.; Akthar, A.; Millett, R.L.; Lai, L.; Chang, A.; McCook, A.A.; Switchenko, J.; Nasti, T.H.; et al. Antibody Response to SARS-CoV-2 MRNA Vaccine in Lung Cancer Patients: Reactivity to Vaccine Antigen and Variants of Concern. medRxiv 2022. [Google Scholar] [CrossRef]
- Fendler, A.; Shepherd, S.T.C.; Au, L.; Wu, M.; Harvey, R.; Schmitt, A.M.; Tippu, Z.; Shum, B.; Farag, S.; Rogiers, A.; et al. Omicron Neutralising Antibodies after Third COVID-19 Vaccine Dose in Patients with Cancer. Lancet 2022, 399, 905–907. [Google Scholar] [CrossRef]
- Shroff, R.T.; Chalasani, P.; Wei, R.; Pennington, D.; Quirk, G.; Schoenle, M.V.; Peyton, K.L.; Uhrlaub, J.L.; Ripperger, T.J.; Jergović, M.; et al. Immune Responses to Two and Three Doses of the BNT162b2 MRNA Vaccine in Adults with Solid Tumors. Nat. Med. 2021, 27, 2002–2011. [Google Scholar] [CrossRef]
- Naranbhai, V.; St. Denis, K.J.; Lam, E.C.; Ofoman, O.; Garcia-Beltran, W.F.; Mairena, C.B.; Bhan, A.K.; Gainor, J.F.; Balazs, A.B.; Iafrate, A.J.; et al. Neutralization Breadth of SARS-CoV-2 Viral Variants Following Primary Series and Booster SARS-CoV-2 Vaccines in Patients with Cancer. Cancer Cell 2022, 40, 103–108.e2. [Google Scholar] [CrossRef]
- Mairhofer, M.; Kausche, L.; Kaltenbrunner, S.; Ghanem, R.; Stegemann, M.; Klein, K.; Pammer, M.; Rauscher, I.; Salzer, H.J.F.; Doppler, S.; et al. Humoral and Cellular Immune Responses in SARS-CoV-2 MRNA-Vaccinated Patients with Cancer. Cancer Cell 2021, 39, 1171–1172. [Google Scholar] [CrossRef] [PubMed]
- McKenzie, D.R.; Muñoz-Ruiz, M.; Monin, L.; Alaguthurai, T.; Lechmere, T.; Abdul-Jawad, S.; Graham, C.; Pollock, E.; Graham, R.; Sychowska, K.; et al. Humoral and Cellular Immunity to Delayed Second Dose of SARS-CoV-2 BNT162b2 MRNA Vaccination in Patients with Cancer. Cancer Cell 2021, 39, 1445–1447. [Google Scholar] [CrossRef] [PubMed]
- Bange, E.M.; Han, N.A.; Wileyto, P.; Kim, J.Y.; Gouma, S.; Robinson, J.; Greenplate, A.R.; Hwee, M.A.; Porterfield, F.; Owoyemi, O.; et al. CD8+ T Cells Contribute to Survival in Patients with COVID-19 and Hematologic Cancer. Nat. Med. 2021, 27, 1280–1289. [Google Scholar] [CrossRef] [PubMed]
- Fendler, A.; Au, L.; Shepherd, S.T.C.; Byrne, F.; Cerrone, M.; Boos, L.A.; Rzeniewicz, K.; Gordon, W.; Shum, B.; Gerard, C.L.; et al. Functional Antibody and T Cell Immunity Following SARS-CoV-2 Infection, Including by Variants of Concern, in Patients with Cancer: The CAPTURE Study. Nat. Cancer 2021, 2, 1321–1337. [Google Scholar] [CrossRef] [PubMed]
- Soyfer, V.; Gutfeld, O.; Shamai, S.; Schlocker, A.; Merimsky, O. COVID-19 Vaccine-Induced Radiation Recall Phenomenon. Int. J. Radiat. Oncol. Biol. Phys. 2021, 110, 957–961. [Google Scholar] [CrossRef] [PubMed]
- Stewart, R.; McDowell, L. Radiation Recall Phenomenon Following COVID-19 Vaccination. Int. J. Radiat. Oncol. Biol. Phys. 2021, 111, 835–836. [Google Scholar] [CrossRef]
- Pavelić, K.; Kraljević Pavelić, S.; Brix, B.; Goswami, N. A Perspective on COVID-19 Management. J. Clin. Med. 2021, 10, 1586. [Google Scholar] [CrossRef]
- Chesney, J.; Puzanov, I.; Collichio, F.; Singh, P.; Milhem, M.M.; Glaspy, J.; Hamid, O.; Ross, M.; Friedlander, P.; Garbe, C.; et al. Randomized, Open-Label Phase II Study Evaluating the Efficacy and Safety of Talimogene Laherparepvec in Combination With Ipilimumab Versus Ipilimumab Alone in Patients With Advanced, Unresectable Melanoma. J. Clin. Oncol. 2018, 36, 1658–1667. [Google Scholar] [CrossRef]
- Trivanović, D.; Pavelić, K.; Peršurić, Ž. Fighting Cancer with Bacteria and Their Toxins. Int. J. Mol. Sci. 2021, 22, 12980. [Google Scholar] [CrossRef] [PubMed]
- Seneff, S.; Nigh, G.; Kyriakopoulos, A.M.; McCullough, P.A. Innate Immune Suppression by SARS-CoV-2 MRNA Vaccinations: The Role of G-Quadruplexes, Exosomes, and MicroRNAs. Food Chem. Toxicol. 2022, 164, 113008. [Google Scholar] [CrossRef]
- Poland, G.A.; Ovsyannikova, I.G.; Jacobson, R.M. Personalized Vaccines: The Emerging Field of Vaccinomics. Expert Opin. Biol. Ther. 2008, 8, 1659–1667. [Google Scholar] [CrossRef] [PubMed]
- Sahin, U.; Türeci, Ö. Personalized Vaccines for Cancer Immunotherapy. Science 2018, 359, 1355–1360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Röltgen, K.; Nielsen, S.C.A.; Silva, O.; Younes, S.F.; Zaslavsky, M.; Costales, C.; Yang, F.; Wirz, O.F.; Solis, D.; Hoh, R.A.; et al. Immune Imprinting, Breadth of Variant Recognition, and Germinal Center Response in Human SARS-CoV-2 Infection and Vaccination. Cell 2022, 185, 1025–1040.e14. [Google Scholar] [CrossRef]
Population | Publication Date | Cancer Type | Vaccine | Seroconversion Rate after 2nd Dose | Comment | Reference |
---|---|---|---|---|---|---|
Israel | May 2021 | Solid | Pfizer BNT162b2 | 90% | [53] | |
USA | May 2021 | Solid | Pfizer BNT162b2 | 80% | [61] | |
UK | June 2021 | Various | Pfizer BNT162b2 | 79% | [6] | |
Israel | July 2021 | Various | Pfizer BNT162b2 | 86% | [52] | |
USA | July 2021 | Hem (MM) | Pfizer BNT162b2 Moderna mRNA-1273 | 77% | [62] | |
Israel | July 2021 | Hem (CLL) | Pfizer BNT162b2 | 43% | [63] | |
USA | August 2021 | Various | Pfizer BNT162b2, Moderna mRNA-1273, Johnson & Johnson Ad26.COV2.S | 95% 94% 85% | Solid cancer 98%, ICIs 97%, Hem 85%, antiCD20+ 70%, stem cell transplants 73% | [54] |
France | August 2021 | Solid and hem | Pfizer BNT162b2 Moderna mRNA-1273 Janssen | 94% solid 85% hem | [64] | |
Switzerland | August 2021 | Various | Pfizer BNT162b2, Moderna mRNA-1273 | 93–95% | [55] | |
USA | August 2021 | Hem | Pfizer BNT162b2 Moderna mRNA-1273 | 75% | [65] | |
France | September 2021 | Solid | Pfizer BNT162b2 | 95% | [51] | |
Netherlands | September 2021 | Solid | Moderna mRNA-1273 | 97–100% | Chemotherapy 97.4% IO 99.3% Chemoth + IO 100% | [66] |
Denmark | September 2021 | Solid and hem | Pfizer BNT162b2 Moderna mRNA-1273 | 93% solid 66% hem | [67] | |
UK | September 2021 | Solid and hem | Pfizer BNT162b2 AstraZeneca | 85% solid 54% hem | [56] | |
USA | November 2021 | Solid and hem | Pfizer BNT162b2 Moderna mRNA-1273 | 72–84% solid 62–85% hem | [68] | |
France | February 2022 | Thoracic | Pfizer BNT162b2 | 94% | [69] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Trivanović, D.; Peršurić, Ž.; Agaj, A.; Jakopović, M.; Samaržija, M.; Bitar, L.; Pavelić, K. The Interplay of Lung Cancer, COVID-19, and Vaccines. Int. J. Mol. Sci. 2022, 23, 15067. https://doi.org/10.3390/ijms232315067
Trivanović D, Peršurić Ž, Agaj A, Jakopović M, Samaržija M, Bitar L, Pavelić K. The Interplay of Lung Cancer, COVID-19, and Vaccines. International Journal of Molecular Sciences. 2022; 23(23):15067. https://doi.org/10.3390/ijms232315067
Chicago/Turabian StyleTrivanović, Dragan, Željka Peršurić, Andrea Agaj, Marko Jakopović, Miroslav Samaržija, Lela Bitar, and Krešimir Pavelić. 2022. "The Interplay of Lung Cancer, COVID-19, and Vaccines" International Journal of Molecular Sciences 23, no. 23: 15067. https://doi.org/10.3390/ijms232315067