Table Info

Table 3.

Treatment changes in LC due to the COVID-19 pandemic

NSCLC T1-T2 N0M0	Locally advanced NSCLC	Metastatic NSCLC	LS-SCLC	ES-SCLC
More use of 3D/IMRT RT or SBRT as an alternative to surgery	Less use of surgery	Shorter and more spaced chemotherapy and ICI regimens	More use of sequential CRT	Shorter and more spaced chemotherapy and ICI regimens
	More use of sequential CRT	Single-dose palliative RT	Hypofractionated RT	Single-dose palliative RT
	Hypofractionated RT	Less use of local treatments in oligometastatic patients	PCI vs. close follow-up	PCI vs. close follow-up
	Consolidative durvalumab Q4W	Less use of local treatments in oligometastatic patients	PCI vs. close follow-up	PCI vs. close follow-up

ES: extensive stage; IMRT: intensity-modulated RT

Declarations

Author contributions

AO, XMR, JLT, NLM, MLV, SP, and VVB: Conceptualization, Investigation, Writing—original draft, Writing—review & editing. PVN: Conceptualization, Investigation, Methodology, Writing—original draft, Writing—review & editing. AO, XMR, JLT, JZM, and FC: Validation, Writing—review & editing, Supervision. All authors read and approved the submitted version.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

Ethical approval is not required in narrative review, according to the institution and relevant policies.

Consent to participate

Not applicable.

Consent to publication

Not applicable.

Availability of data and materials

Not applicable.

Funding

Not applicable.

Copyright

References

Purohit D, Ahirwar AK, Sakarde A, Asia P, Gopal N. COVID-19 and lung pathologies. Horm Mol Biol Clin Investig. 2021;42:435–43. [DOI] [PubMed]

COVID-19 weekly epidemiological update [Internet]. [Cited 2023 Jan 14]. Available from: https://gacetamedica.com/wp-content/uploads/2022/10/20221005_Weekly_Epi_Update_112.pdf

Luo J, Rizvi H, Preeshagul IR, Egger JV, Hoyos D, Bandlamudi C, et al. COVID-19 in patients with lung cancer. Ann Oncol. 2020;31:1386–96. [DOI] [PubMed] [PMC]

Oldani S, Petrelli F, Dognini G, Borgonovo K, Parati MC, Ghilardi M, et al. COVID-19 and lung cancer survival: an updated systematic review and meta-analysis. Cancers (Basel). 2022;14:5706. [DOI] [PubMed] [PMC]

Rolfo C, Meshulami N, Russo A, Krammer F, García-Sastre A, Mack PC, et al. Lung cancer and severe acute respiratory syndrome coronavirus 2 infection: identifying important knowledge gaps for investigation. J Thorac Oncol. 2022;17:214–27. [DOI] [PubMed] [PMC]

Li Y, Niu L. Identification of the effects of COVID-19 on patients with pulmonary fibrosis and lung cancer: a bioinformatics analysis and literature review. Sci Rep. 2022;12:16040. [DOI] [PubMed] [PMC]

Bian DJH, Sabri S, Abdulkarim BS. Interactions between COVID-19 and lung cancer: lessons learned during the pandemic. Cancers (Basel). 2022;14:3598. [DOI] [PubMed] [PMC]

Ahmad S, Manzoor S, Siddiqui S, Mariappan N, Zafar I, Ahmad A, et al. Epigenetic underpinnings of inflammation: connecting the dots between pulmonary diseases, lung cancer and COVID-19. Semin Cancer Biol. 2022;83:384–98. [DOI] [PubMed] [PMC]

Gottschalk G, Knox K, Roy A. ACE2: at the crossroad of COVID-19 and lung cancer. Gene Rep. 2021;23:101077. [DOI] [PubMed] [PMC]

10.

Aramini B, Masciale V, Samarelli AV, Tonelli R, Cerri S, Clini E, et al. Biological effects of COVID-19 on lung cancer: can we drive our decisions. Front Oncol. 2022;12:1029830. [DOI] [PubMed] [PMC]

11.

Ji P, Zhu J, Zhong Z, Li H, Pang J, Li B, et al. Association of elevated inflammatory markers and severe COVID-19: a meta-analysis. Medicine (Baltimore). 2020;99:e23315. [DOI] [PubMed] [PMC]

12.

Zhu Z, Zheng Z, Liu J. Comparison of COVID-19 and lung cancer via reactive oxygen species signaling. Front Oncol. 2021;11:708263. [DOI] [PubMed] [PMC]

13.

Maheswari S, Pethannan R, Sabarimurugan S. Air pollution enhances susceptibility to novel coronavirus (COVID-19) infection – an impact study. Environ Anal Health Toxicol. 2020;35:e2020020-0. [DOI] [PubMed] [PMC]

14.

Reyes R, López-Castro R, Auclin E, García T, Chourio MJ, Rodriguez A, et al. MA03.08 impact of COVID-19 pandemic in the diagnosis and prognosis of lung cancer. J Thorac Oncol. 2021;16:S141. [DOI]

15.

Kasymjanova G, Anwar A, Cohen V, Sultanem K, Pepe C, Sakr L, et al. The impact of COVID-19 on the diagnosis and treatment of lung cancer at a Canadian academic center: a retrospective chart review. Curr Oncol. 2021;28:4247–55. [DOI] [PubMed] [PMC]

16.

Analyse des répercussions de la pandémie de la COVID-19 sur les soins et les services en cancérologie au Québec [Internet]. Gouvernement du Québec; c2021 [cited 2023 Jan 14]. Available from: https://publications.msss.gouv.qc.ca/msss/fichiers/2021/21-210-132W.pdf

17.

Jazieh AR, Akbulut H, Curigliano G, Rogado A, Alsharm AA, Razis ED, et al.; International Research Network on COVID-19 Impact on Cancer Care. Impact of the COVID-19 pandemic on cancer care: a global collaborative study. JCO Glob Oncol. 2020;6:1428–38. [DOI] [PubMed] [PMC]

18.

Park JY, Lee YJ, Kim T, Lee CY, Kim HI, Kim JH, et al. Collateral effects of the coronavirus disease 2019 pandemic on lung cancer diagnosis in Korea. BMC Cancer. 2020;20:1040. [DOI] [PubMed] [PMC]

19.

Maringe C, Spicer J, Morris M, Purushotham A, Nolte E, Sullivan R, et al. 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;21:1023–34. [DOI] [PubMed] [PMC]

20.

Cantini L, Mentrasti G, Russo GL, Signorelli D, Pasello G, Rijavec E, et al. Evaluation of COVID-19 impact on DELAYing diagnostic-therapeutic pathways of lung cancer patients in Italy (COVID-DELAY study): fewer cases and higher stages from a real-world scenario. ESMO Open. 2022;7:100406. Erratum in: ESMO Open. 2022;7:100471. [DOI] [PubMed] [PMC]

21.

Passaro A, Peters S, Mok TSK, Attili I, Mitsudomi T, de Marinis F. Testing for COVID-19 in lung cancer patients. Ann Oncol. 2020;31:832–4. [DOI] [PubMed] [PMC]

22.

Provencio M, Mazarico Gallego JM, Calles A, Antoñanzas M, Pangua C, Mielgo Rubio X, et al. Lung cancer patients with COVID-19 in Spain: GRAVID study. Lung Cancer. 2021;157:109–15. [DOI] [PubMed] [PMC]

23.

Wang L, Wang Y, Cheng X, Li X, Li J. Impact of coronavirus disease 2019 on lung cancer patients: a meta-analysis. Transl Oncol. 2023;28:101605. [DOI] [PubMed] [PMC]

24.

Calabrò L, Rossi G, Covre A, Morra A, Maio M. COVID and lung cancer. Curr Oncol Rep. 2021;23:134. [DOI] [PubMed] [PMC]

25.

Milette S, Fiset PO, Walsh LA, Spicer JD, Quail DF. The innate immune architecture of lung tumors and its implication in disease progression. J Pathol. 2019;247:589–605. [DOI] [PubMed]

26.

Passaro A, Bestvina C, Velez Velez M, Garassino MC, Garon E, Peters S. Severity of COVID-19 in patients with lung cancer: evidence and challenges. J Immunother Cancer. 2021;9:e002266. [DOI] [PubMed] [PMC]

27.

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. [DOI] [PubMed] [PMC]

28.

Dai M, Liu D, Liu M, Zhou F, Li G, Chen Z, et al. Patients with cancer appear more vulnerable to SARS-CoV-2: a multicenter study during the COVID-19 outbreak. Cancer Discov. 2020;10:783–91. [DOI] [PubMed] [PMC]

29.

Winkler T, Ben-David U. Elevated expression of ACE2 in tumor-adjacent normal tissues of cancer patients. Int J Cancer. 2020;147:3264–6. [DOI] [PubMed]

30.

Desai AD, Lavelle M, Boursiquot BC, Wan EY. Long-term complications of COVID-19. Am J Physiol Cell Physiol. 2022;322:C1–11. [DOI] [PubMed] [PMC]

31.

Bungaro M, Passiglia F, Scagliotti GV. COVID-19 and lung cancer: a comprehensive overview from outbreak to recovery. Biomedicines. 2022;10:776. [DOI] [PubMed] [PMC]

32.

Satterfield BA, Bhatt DL, Gersh BJ. Cardiac involvement in the long-term implications of COVID-19. Nat Rev Cardiol. 2022;19:332–41. [DOI] [PubMed] [PMC]

33.

Nalbandian A, Sehgal K, Gupta A, Madhavan MV, McGroder C, Stevens JS, et al. Post-acute COVID-19 syndrome. Nat Med. 2021;27:601–15. [DOI] [PubMed] [PMC]

34.

O’Mahoney LL, Routen A, Gillies C, Ekezie W, Welford A, Zhang A, et al. The prevalence and long-term health effects of long Covid among hospitalised and non-hospitalised populations: a systematic review and meta-analysis. EClinicalMedicine. 2023;55:101762. Erratum in: EClinicalMedicine. 2023;59:101959. [DOI] [PubMed] [PMC]

35.

Sha Z, Chang K, Mi J, Liang Z, Hu L, Long F, et al. The impact of the COVID-19 pandemic on lung cancer patients. Ann Palliat Med. 2020;9:3373–8. [DOI] [PubMed]

36.

Rugge M, Zorzi M, Guzzinati S. SARS-CoV-2 infection in the Italian Veneto region: adverse outcomes in patients with cancer. Nat Cancer. 2020;1:784–8. [DOI] [PubMed]

37.

Garassino MC, Whisenant JG, Huang LC, Trama A, Torri V, Agustoni F, et al.; TERAVOLT investigators. COVID-19 in patients with thoracic malignancies (TERAVOLT): first results of an international, registry-based, cohort study. Lancet Oncol. 2020;21:914–22. [DOI] [PubMed] [PMC]

38.

Peravali M, Joshi I, Ahn J, Kim C. A systematic review and meta-analysis of clinical characteristics and outcomes in patients with lung cancer with coronavirus disease 2019. JTO Clin Res Rep. 2021;2:100141. [DOI] [PubMed] [PMC]

39.

Prokop M, van Everdingen W, van Rees Vellinga T, Quarles van Ufford H, Stöger L, Beenen L, et al.; COVID-19 Standardized Reporting Working Group of the Dutch Radiological Society. CO-RADS: a categorical CT assessment scheme for patients suspected of having COVID-19—definition and evaluation. Radiology. 2020;296:E97–104. [DOI] [PubMed] [PMC]

40.

Liu G, Chen Y, Runa A, Liu J. Diagnostic performance of CO-RADS for COVID-19: a systematic review and meta-analysis. Eur Radiol. 2022;32:4414–26. [DOI] [PubMed] [PMC]

41.

Penha D, Pinto EG, Matos F, Hochhegger B, Monaghan C, Taborda-Barata L, et al. CO-RADS: coronavirus classification review. J Clin Imaging Sci. 2021;11:9. [DOI] [PubMed] [PMC]

42.

Mazzone PJ, Gould MK, Arenberg DA, Chen AC, Choi HK, Detterbeck FC, et al. Management of lung nodules and lung cancer screening during the COVID-19 pandemic: CHEST expert panel report. Chest. 2020;158:406–15. [DOI] [PubMed] [PMC]

43.

Randall RE, Griffin DE. Within host RNA virus persistence: mechanisms and consequences. Curr Opin Virol. 2017;23:35–42. [DOI] [PubMed] [PMC]

44.

Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395:1417–8. [DOI] [PubMed] [PMC]

45.

Moriguchi T, Harii N, Goto J, Harada D, Sugawara H, Takamino J, et al. A first case of meningitis/encephalitis associated with SARS-Coronavirus-2. Int J Infect Dis. 2020;94:55–8. [DOI] [PubMed] [PMC]

46.

Saini G, Aneja R. Cancer as a prospective sequela of long COVID-19. Bioessays. 2021;43:e2000331. [DOI] [PubMed] [PMC]

47.

Lin L, Luo S, Qin R, Yang M, Wang X, Yang Q, et al. Long-term infection of SARS-CoV-2 changed the body’s immune status. Clin Immunol. 2020;218:108524. [DOI] [PubMed] [PMC]

48.

Lan L, Xu D, Ye G, Xia C, Wang S, Li Y, et al. Positive RT-PCR test results in patients recovered from COVID-19. JAMA. 2020;323:1502–3. [DOI] [PubMed] [PMC]

49.

Baang JH, Smith C, Mirabelli C, Valesano AL, Manthei DM, Bachman MA, et al. Prolonged severe acute respiratory syndrome coronavirus 2 replication in an immunocompromised patient. J Infect Dis. 2021;223:23–7. [DOI] [PubMed] [PMC]

50.

Alpalhão M, Ferreira JA, Filipe P. Persistent SARS-CoV-2 infection and the risk for cancer. Med Hypotheses. 2020;143:109882. [DOI] [PubMed] [PMC]

51.

Tu SM. Stem cell theory of cancer: implications of a viral etiology in certain malignancies. Cancers (Basel). 2021;13:2738. [DOI] [PubMed] [PMC]

52.

Liapis I, Baritaki S. COVID-19 vs. cancer immunosurveillance: a game of thrones within an inflamed microenviroment. Cancers (Basel). 2022;14:4330. [DOI] [PubMed] [PMC]

53.

Habibzadeh P, Dastsooz H, Eshraghi M, Łos MJ, Klionsky DJ, Ghavami S. Autophagy: the potential link between SARS-CoV-2 and cancer. Cancers (Basel). 2021;13:5721. [DOI] [PubMed] [PMC]

54.

Jafarzadeh A, Gosain R, Mortazavi SMJ, Nemati M, Jafarzadeh S, Ghaderi A. SARS-CoV-2 infection: a possible risk factor for incidence and recurrence of cancers. Int J Hematol Oncol Stem Cell Res. 2022;16:117–27. [DOI] [PubMed] [PMC]

55.

Mesri EA, Feitelson MA, Munger K. Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe. 2014;15:266–82. [DOI] [PubMed] [PMC]

56.

Stingi A, Cirillo L. SARS-CoV-2 infection and cancer: evidence for and against a role of SARS-CoV-2 in cancer onset. Bioessays. 2021;43:e2000289. [DOI] [PubMed] [PMC]

57.

Slotman BJ, Cremades V, Kirby AM, Ricardi U. European radiation oncology after one year of COVID-19 pandemic. Clin Transl Radiat Oncol. 2021;28:141–3. [DOI] [PubMed] [PMC]

58.

Guckenberger M, Belka C, Bezjak A, Bradley J, Daly ME, DeRuysscher D, et al. Practice recommendations for lung cancer radiotherapy during the COVID-19 pandemic: an ESTRO-ASTRO consensus statement. Int J Radiat Oncol Biol Phys. 2020;107:631–40. [DOI] [PubMed] [PMC]

59.

Tan L, Wang Q, Zhang D, Ding J, Huang Q, Tang YQ, et al. Lymphopenia predicts disease severity of COVID-19: a descriptive and predictive study. Signal Transduct Target Ther. 2020;5:33. Erratum in: Signal Transduct Target Ther. 2020;5:61. [DOI] [PubMed] [PMC]

60.

Siavashpour Z, Goharpey N, Mobasheri M. Radiotherapy based management during Covid-19 pandemic – a systematic review of presented consensus and guidelines. Crit Rev Oncol Hematol. 2021;164:103402. [DOI] [PubMed] [PMC]

61.

Wang D, Bi N, Zhang T, Zhou Z, Xiao Z, Liang J, et al. Comparison of efficacy and safety between simultaneous integrated boost intensity-modulated radiotherapy and conventional intensity-modulated radiotherapy in locally advanced non-small-cell lung cancer: a retrospective study. Radiat Oncol. 2019;14:106. [DOI] [PubMed] [PMC]

62.

Fang P, Swanick CW, Pezzi TA, Liao Z, Welsh J, Lin SH, et al. Outcomes and toxicity following high-dose radiation therapy in 15 fractions for non-small cell lung cancer. Pract Radiat Oncol. 2017;7:433–41. [DOI] [PubMed]

63.

Couñago F, Navarro-Martin A, Luna J, Rodríguez de Dios N, Rodríguez A, Casas F, et al. GOECP/SEOR clinical recommendations for lung cancer radiotherapy during the COVID-19 pandemic. World J Clin Oncol. 2020;11:510–27. [DOI] [PubMed] [PMC]

64.

Turrisi AT 3rd, Kim K, Blum R, Sause WT, Livingston RB, Komaki R, et al. Twice-daily compared with once-daily thoracic radiotherapy in limited small-cell lung cancer treated concurrently with cisplatin and etoposide. N Engl J Med. 1999;340:265–71. [DOI] [PubMed]

65.

Faivre-Finn C, Snee M, Ashcroft L, Appel W, Barlesi F, Bhatnagar A, et al.; CONVERT Study Team. Concurrent once-daily versus twice-daily chemoradiotherapy in patients with limited-stage small-cell lung cancer (CONVERT): an open-label, phase 3, randomised, superiority trial. Lancet Oncol. 2017;18:1116–25. [DOI] [PubMed] [PMC]

66.

Wu AJ, Rimner A, Shepherd AF, Gelblum DY, Shaverdian N, Yorke E, et al. Thoracic radiation therapy during coronavirus disease 2019: provisional guidelines from a comprehensive cancer center within a pandemic epicenter. Adv Radiat Oncol. 2020;5:603–7. [DOI] [PubMed] [PMC]

67.

De Ruysscher D, Lueza B, Le Péchoux C, Johnson DH, O’Brien M, Murray N, et al.; RTT-SCLC Collaborative Group. Impact of thoracic radiotherapy timing in limited-stage small-cell lung cancer: usefulness of the individual patient data meta-analysis. Ann Oncol. 2016;27:1818–28. [DOI] [PubMed] [PMC]

68.

Sun JM, Ahn YC, Choi EK, Ahn MJ, Ahn JS, Lee SH, et al. Phase III trial of concurrent thoracic radiotherapy with either first- or third-cycle chemotherapy for limited-disease small-cell lung cancer. Ann Oncol. 2013;24:2088–92. Erratum in: Ann Oncol. 2014;25:1672. [DOI] [PubMed]

69.

Verma V, Simone CB 2nd, Allen PK, Gajjar SR, Shah C, Zhen W, et al. Multi-institutional experience of stereotactic ablative radiation therapy for stage I small cell lung cancer. Int J Radiat Oncol Biol Phys. 2017;97:362–71. [DOI] [PubMed]

70.

Takahashi T, Yamanaka T, Seto T, Harada H, Nokihara H, Saka H, et al. Prophylactic cranial irradiation versus observation in patients with extensive-disease small-cell lung cancer: a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 2017;18:663–71. [DOI] [PubMed]

71.

Chavez-MacGregor M, Lei X, Zhao H, Scheet P, Giordano SH. Evaluation of COVID-19 mortality and adverse outcomes in US patients with or without cancer. JAMA Oncol. 2022;8:69–78. [DOI] [PubMed] [PMC]

72.

Sharafeldin N, Bates B, Song Q, Madhira V, Yan Y, Dong S, et al. Outcomes of COVID-19 in patients with cancer: report from the national COVID cohort collaborative (N3C). J Clin Oncol. 2021;39:2232–46. [DOI] [PubMed] [PMC]

73.

Jee J, Foote MB, Lumish M, Stonestrom AJ, Wills B, Narendra V, et al. Chemotherapy and COVID-19 outcomes in patients with cancer. J Clin Oncol. 2020;38:3538–46. [DOI] [PubMed] [PMC]

74.

Liu H, Yang D, Chen X, Sun Z, Zou Y, Chen C, et al. The effect of anticancer treatment on cancer patients with COVID-19: a systematic review and meta-analysis. Cancer Med. 2021;10:1043–56. [DOI] [PubMed] [PMC]

75.

Joshi K, Muhith A, Obeid M, Milner-Watts C, Yousaf N, Popat S, et al. Safety monitoring of two and four-weekly adjuvant durvalumab for patients with stage III NSCLC: implications for the COVID-19 pandemic and beyond. Lung Cancer. 2021;156:147–50. [DOI] [PubMed] [PMC]

76.

Cantini L, Paoloni F, Pecci F, Spagnolo F, Genova C, Tanda ET, et al. Safety of extended interval dosing immune checkpoint inhibitors: a multicenter cohort study. J Natl Cancer Inst. 2023;115:796–804. [DOI] [PubMed] [PMC]

77.

Hijmering-Kappelle LBM, Hiltermann TJN, Bensch F. Safety and efficacy of extended interval dosing for immune checkpoint inhibitors in non-small cell lung cancer during the COVID-19 pandemic. Clin Lung Cancer. 2022;23:143–50. [DOI] [PubMed] [PMC]

78.

Sehgal K, Costa DB, Rangachari D. Extended-interval dosing strategy of immune checkpoint inhibitors in lung cancer: will it outlast the COVID-19 pandemic? Front Oncol. 2020;10:1193. [DOI] [PubMed] [PMC]

79.

Actualización en el posicionamiento y recomendaciones de SEOM en relación con la campaña de vacunación frente al COVID-19 en pacientes con cáncer [Internet]. [Cited 2023 Jan 14]. Available from: https://seom.org/images/Actualizacion_Posicionamiento_SEOM_Vacunas_COVID19.pdf

80.

Mei Q, Hu G, Yang Y, Liu B, Yin J, Li M, et al. Impact of COVID-19 vaccination on the use of PD-1 inhibitor in treating patients with cancer: a real-world study. J Immunother Cancer. 2022;10:e004157. [DOI] [PubMed] [PMC]

81.

Hirschbühl K, Schaller T, Märkl B, Claus R, Sipos E, Rentschler L, et al. High viral loads: what drives fatal cases of COVID-19 in vaccinees? – an autopsy study. Mod Pathol. 2022;35:1013–21. [DOI] [PubMed] [PMC]

82.

Addeo A, Shah PK, Bordry N, Hudson RD, Albracht B, Di Marco M, et al. Immunogenicity of SARS-CoV-2 messenger RNA vaccines in patients with cancer. Cancer Cell. 2021;39:1091–8.e2. [DOI] [PubMed] [PMC]

83.

Bowes CL, Naranbhai V, St Denis KJ, Lam EC, Bertaux B, Keane FK, et al. Heterogeneous immunogenicity of SARS-CoV-2 vaccines in cancer patients receiving radiotherapy. Radiother Oncol. 2022;166:88–91. [DOI] [PubMed] [PMC]

84.

Provencio M, Rodríguez-Abreu D, Ortega AL, Serrano G, Aguado C, Franco F, et al. Seroprevalence and immunological memory against SARS-CoV-2 in lung cancer patients: the SOLID study. Transl Lung Cancer Res. 2022;11:53–63. [DOI] [PubMed] [PMC]