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Pathological response and tumor stroma immunogenic features predict long-term survival in non-small cell lung cancer after neoadjuvant chemotherapy

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Abstract

Purpose

Major pathological response (MPR) has become a surrogate endpoint for overall survival (OS) in non-small cell lung cancer (NSCLC) after neoadjuvant therapy, however, the prognostic histologic features and optimal N descriptor after neoadjuvant therapy are poorly defined.

Methods

We retrospectively analyzed data from 368 NSCLC patients who underwent surgery after neoadjuvant chemotherapy (NAC) from January 2010 to December 2020. The percentage of residual viable tumors in the primary tumor, lymph nodes (LN), and inflammation components within the tumor stroma were comprehensively reviewed. The primary endpoint was OS.

Results

Of the 368 enrolled patients, 12.0% (44/368) achieved MPR in the primary tumor, which was associated with significantly better OS (HR, 0.36 0.17–0.77, p = 0.008) and DFS (HR = 0.59, 0.36–0.92, p = 0.038). In patients who did not have an MPR, we identified an immune-activated phenotype in primary tumors, characterized by intense tumor-infiltrating lymphocyte or multinucleated giant cell infiltration, that was associated with similar OS and DFS as patients who had MPR. Neoadjuvant pathologic grade (NPG), consisting of MPR and immune-activated phenotype, identified 30.7% (113/368) patients that derived significant OS (HR 0.28, 0.17–0.46, p < 0.001) and DFS (HR 0.44, 0.31–0.61, p < 0.001) benefit from NAC. Moreover, the combination of NPG and the number of positive LN stations (nS) in the multivariate analysis had a higher C-index (0.711 vs. 0.663, p < 0.001) than the ypTNM Stage when examining OS.

Conclusion

NPG integrated with nS can provide a simple, practical, and robust approach that may allow for better stratification of patients when evaluating neoadjuvant chemotherapy in clinical practice.

Graphical Abstract

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Data availability

Anonymized detailed clinico-pathological data and the R-Script used for data analysis are available upon request to the authors.

Abbreviations

MPR:

Major pathological response

NAC:

Neoadjuvant chemotherapy

IASLC:

The International Association for the Study of Lung Cancer

RVT:

Residual viable tumor

RVT-T:

Residual viable tumor in primary tumors

RVT-N:

Residual viable tumor in affected lymph nodes

TILs:

Tumor-infiltrating lymphocytes

MNGCs:

Multinucleated giant cells

NPG:

Neoadjuvant pathologic grade

OS:

Overall survival

DFS:

Disease-free survival

N+ numbers:

The number of metastatic LN

nS:

The number of involved nodal stations

LN harvested:

The total number of LN dissected

NS:

The number of LN harvested stations

N+ ratio:

The ratio of metastatic LN (N+ numbers/LN harvested)

New N stage:

The new N descriptor proposed by the IASLC staging

References

  1. P. Expert Consensus, B. Kidane, M. Bott, J. Spicer, L. Backhus, J. Chaft, N. Chudgar, Y. Colson, T.A. D’Amico, E. David, J. Lee, S. Najmeh, B. Sepesi, C. Shu, J. Yang, S. Swanson, B. Stiles, J. Thorac. Cardiovasc. Surg. 166, 637–654 (2023). https://doi.org/10.1016/j.jtcvs.2023.04.039

    Article  Google Scholar 

  2. P.M. Forde, J. Spicer, S. Lu, M. Provencio, T. Mitsudomi, M.M. Awad, E. Felip, S.R. Broderick, J.R. Brahmer, S.J. Swanson, K. Kerr, C. Wang, T.E. Ciuleanu, G.B. Saylors, F. Tanaka, H. Ito, K.N. Chen, M. Liberman, E.E. Vokes, J.M. Taube, C. Dorange, J. Cai, J. Fiore, A. Jarkowski, D. Balli, M. Sausen, D. Pandya, C.Y. Calvet, N. Girard, I. CheckMate, N. Engl. J. Med. 386, 1973–1985 (2022). https://doi.org/10.1056/NEJMoa2202170

    Article  Google Scholar 

  3. H. Wakelee, M. Liberman, T. Kato, M. Tsuboi, S.H. Lee, S. Gao, K.N. Chen, C. Dooms, M. Majem, E. Eigendorff, G.L. Martinengo, O. Bylicki, D. Rodriguez-Abreu, J.E. Chaft, S. Novello, J. Yang, S.M. Keller, A. Samkari, J.D. Spicer, K.-. Investigators, N. Engl. J. Med. 389, 491–503 (2023). https://doi.org/10.1056/NEJMoa2302983

    Article  Google Scholar 

  4. W.D. Travis, S. Dacic, I. Wistuba, L. Sholl, P. Adusumilli, L. Bubendorf, P. Bunn, T. Cascone, J. Chaft, G. Chen, T.Y. Chou, W. Cooper, J.J. Erasmus, C.G. Ferreira, J.M. Goo, J. Heymach, F.R. Hirsch, H. Horinouchi, K. Kerr, M. Kris, D. Jain, Y.T. Kim, F. Lopez-Rios, S. Lu, T. Mitsudomi, A. Moreira, N. Motoi, A.G. Nicholson, R. Oliveira, M. Papotti, U. Pastorino, L. Paz-Ares, G. Pelosi, C. Poleri, M. Provencio, A.C. Roden, G. Scagliotti, S.G. Swisher, E. Thunnissen, M.S. Tsao, J. Vansteenkiste, W. Weder, Y. Yatabe, J. Thorac. Oncol. 15, 709–740 (2020). https://doi.org/10.1016/j.jtho.2020.01.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. M.D. Hellmann, J.E. Chaft, W.N. William Jr., V. Rusch, K.M. Pisters, N. Kalhor, A. Pataer, W.D. Travis, S.G. Swisher, M.G. Kris, M.D.A.L.C.C.G. University of Texas, Lancet Oncol. 15, e42–50 (2014). https://doi.org/10.1016/S1470-2045(13)70334-6

    Article  CAS  Google Scholar 

  6. T.R. Cottrell, E.D. Thompson, P.M. Forde, J.E. Stein, A.S. Duffield, V. Anagnostou, N. Rekhtman, R.A. Anders, J.D. Cuda, P.B. Illei, E. Gabrielson, F.B. Askin, N. Niknafs, K.N. Smith, M.J. Velez, J.L. Sauter, J.M. Isbell, D.R. Jones, R.J. Battafarano, S.C. Yang, L. Danilova, J.D. Wolchok, S.L. Topalian, V.E. Velculescu, D.M. Pardoll, J.R. Brahmer, M.D. Hellmann, J.E. Chaft, A. Cimino-Mathews, J.M. Taube, Ann. Oncol. 29, 1853–1860 (2018). https://doi.org/10.1093/annonc/mdy218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. J.E. Stein, E.J. Lipson, T.R. Cottrell, P.M. Forde, R.A. Anders, A. Cimino-Mathews, E.D. Thompson, M.E. Allaf, M. Yarchoan, J. Feliciano, H. Wang, E.M. Jaffee, D.M. Pardoll, S.L. Topalian, J.M. Taube, Clin. Cancer. Res. 26, 545–551 (2020). https://doi.org/10.1158/1078-0432.CCR-19-2379

    Article  CAS  PubMed  Google Scholar 

  8. V. Pelekanou, D.E. Carvajal-Hausdorf, M. Altan, B. Wasserman, C. Carvajal-Hausdorf, H. Wimberly, J. Brown, D. Lannin, L. Pusztai, D.L. Rimm, Breast Cancer Res. 19(91) (2017). https://doi.org/10.1186/s13058-017-0884-8

  9. M.V. Dieci, C. Criscitiello, A. Goubar, G. Viale, P. Conte, V. Guarneri, G. Ficarra, M.C. Mathieu, S. Delaloge, G. Curigliano, F. Andre, Ann. Oncol. 25, 611–618 (2014). https://doi.org/10.1093/annonc/mdt556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. C. Denkert, G. von Minckwitz, S. Darb-Esfahani, B. Lederer, B.I. Heppner, K.E. Weber, J. Budczies, J. Huober, F. Klauschen, J. Furlanetto, W.D. Schmitt, J.U. Blohmer, T. Karn, B.M. Pfitzner, S. Kümmel, K. Engels, A. Schneeweiss, A. Hartmann, A. Noske, P.A. Fasching, C. Jackisch, M. van Mackelenbergh, P. Sinn, C. Schem, C. Hanusch, M. Untch, S. Loibl, Lancet Oncol. 19, 40–50 (2018). https://doi.org/10.1016/s1470-2045(17)30904-x

    Article  PubMed  Google Scholar 

  11. Y. Qu, K. Emoto, T. Eguchi, R.G. Aly, H. Zheng, J.E. Chaft, K.S. Tan, D.R. Jones, M.G. Kris, P.S. Adusumilli, W.D. Travis, J. Thorac. Oncol. 14, 482–493 (2019). https://doi.org/10.1016/j.jtho.2018.11.017

    Article  PubMed  Google Scholar 

  12. R.U. Osarogiagbon, P. Van Schil, D.J. Giroux, E. Lim, P.M. Putora, Y. Lievens, G. Cardillo, H.K. Kim, G. Rocco, A. Bille, H. Prosch, F.S. Vasquez, K.K. Nishimura, F. Detterbeck, R. Rami-Porta, V.W. Rusch, H. Asamura, J. Huang, N.D.S. Members of the, J. Thorac. Oncol. 18, 410–418 (2023). https://doi.org/10.1016/j.jtho.2022.12.009

    Article  Google Scholar 

  13. X. Liu, W. Sun, J. Wu, Y. Feng, L. Mao, M. Chen, X. Yang, H. Wang, K. Chi, Y. Yang, D. Lin, Mod. Pathol. 34, 1990–1998 (2021). https://doi.org/10.1038/s41379-021-00871-1

    Article  CAS  PubMed  Google Scholar 

  14. A. Pataer, A. Weissferdt, A.A. Vaporciyan, A.M. Correa, B. Sepesi, I.I. Wistuba, J.V. Heymach, T. Cascone, S.G. Swisher, J. Thorac. Oncol. 16, 1289–1297 (2021). https://doi.org/10.1016/j.jtho.2021.03.029

    Article  PubMed  Google Scholar 

  15. W.D. Travis, E. Brambilla, A.G. Nicholson, Y. Yatabe, J.H.M. Austin, M.B. Beasley, L.R. Chirieac, S. Dacic, E. Duhig, D.B. Flieder, K. Geisinger, F.R. Hirsch, Y. Ishikawa, K.M. Kerr, M. Noguchi, G. Pelosi, C.A. Powell, M.S. Tsao, I. Wistuba, W.H.O. Panel, J. Thorac. Oncol. 10, 1243–1260 (2015). https://doi.org/10.1097/JTO.0000000000000630

    Article  Google Scholar 

  16. S. Hendry, R. Salgado, T. Gevaert, P.A. Russell, T. John, B. Thapa, M. Christie, K. van de Vijver, M.V. Estrada, P.I. Gonzalez-Ericsson, M. Sanders, B. Solomon, C. Solinas, G. Van den Eynden, Y. Allory, M. Preusser, J. Hainfellner, G. Pruneri, A. Vingiani, S. Demaria, F. Symmans, P. Nuciforo, L. Comerma, E.A. Thompson, S. Lakhani, S.R. Kim, S. Schnitt, C. Colpaert, C. Sotiriou, S.J. Scherer, M. Ignatiadis, S. Badve, R.H. Pierce, G. Viale, N. Sirtaine, F. Penault-Llorca, T. Sugie, S. Fineberg, S. Paik, A. Srinivasan, A. Richardson, Y. Wang, E. Chmielik, J. Brock, D.B. Johnson, J. Balko, S. Wienert, V. Bossuyt, S. Michiels, N. Ternes, N. Burchardi, S.J. Luen, P. Savas, F. Klauschen, P.H. Watson, B.H. Nelson, C. Criscitiello, S. O’Toole, D. Larsimont, R. de Wind, G. Curigliano, F. Andre, M. Lacroix-Triki, M. van de Vijver, F. Rojo, G. Floris, S. Bedri, J. Sparano, D. Rimm, T. Nielsen, Z. Kos, S. Hewitt, B. Singh, G. Farshid, S. Loibl, K.H. Allison, N. Tung, S. Adams, K. Willard-Gallo, H.M. Horlings, L. Gandhi, A. Moreira, F. Hirsch, M.V. Dieci, M. Urbanowicz, I. Brcic, K. Korski, F. Gaire, H. Koeppen, A. Lo, J. Giltnane, M.C. Rebelatto, K.E. Steele, J. Zha, K. Emancipator, J.W. Juco, C. Denkert, J. Reis-Filho, S. Loi, S.B. Fox, Adv. Anat. Pathol. 24, 235–251 (2017). https://doi.org/10.1097/PAP.0000000000000162

    Article  PubMed  PubMed Central  Google Scholar 

  17. J.L. Moore, M. Green, A. Santaolalla, H. Deere, R.P.T. Evans, M. Elshafie, A. Lavery, D.T. McManus, A. McGuigan, R. Douglas, J. Horne, R. Walker, H. Mir, M. Terlizzo, S.K. Kamarajah, M. Van Hemelrijck, N. Maisey, A. Sita-Lumsden, S. Ngan, M. Kelly, C.R. Baker, S. Kumar, J. Lagergren, W.H. Allum, J.A. Gossage, E.A. Griffiths, H.I. Grabsch, R.C. Turkington, T.J. Underwood, E.C. Smyth, R.C. Fitzgerald, D. Cunningham, A.R. Davies, J. Clin. Oncol. (2023). https://doi.org/10.1200/JCO.23.00139

    Article  PubMed  PubMed Central  Google Scholar 

  18. T. Hagi, T. Makino, M. Yamasaki, K. Yamashita, K. Tanaka, T. Saito, T. Takahashi, Y. Kurokawa, M. Motoori, Y. Kimura, K. Nakajima, E. Morii, H. Eguchi, Y. Doki, Ann. Surg. 275, 1121–1129 (2022). https://doi.org/10.1097/sla.0000000000004238

    Article  PubMed  Google Scholar 

  19. V.W. Rusch, H. Asamura, H. Watanabe, D.J. Giroux, R. Rami-Porta, P. Goldstraw, J. Thorac. Oncol. 4, 568–577 (2009). https://doi.org/10.1097/JTO.0b013e3181a0d82e

    Article  PubMed  Google Scholar 

  20. B.J. Park, T.H. Kim, S. Shin, H.K. Kim, Y.S. Choi, J. Kim, J.I. Zo, Y.M. Shim, J.H. Cho, J. Thorac. Oncol. 14, 1962–1969 (2019). https://doi.org/10.1016/j.jtho.2019.07.034

    Article  PubMed  Google Scholar 

  21. J.M. Bland, D.G. Altman, Stat. Methods Med. Res. 8, 135–160 (1999). https://doi.org/10.1177/096228029900800204

    Article  CAS  PubMed  Google Scholar 

  22. Y. Benjamini, Y. Hochberg, J. R. Stat. Soc. Series B Stat. Methodol. 57, 289–300 (1995). https://doi.org/10.1111/j.2517-6161.1995.tb02031.x

    Article  Google Scholar 

  23. B. Lausen, W. Sauerbrei, M. Schumacher, Contr. Stat. 17, 483–496 (1994). https://doi.org/10.1007/978-3-642-57991-2_28

  24. F.E. Harrell Jr, K.L. Lee, D.B. Mark, Stat. Med. 15, 361–387 (1996). https://doi.org/10.1002/(sici)1097-0258(19960229)15:4<361::Aid-sim168>3.0.Co;2-4

    Article  PubMed  Google Scholar 

  25. H. Akaike, Biogeochemistry 1998, 199–213 (1998). https://doi.org/10.1007/978-1-4612-1694-0_15

  26. S.J. Luen, R. Salgado, M.V. Dieci, A. Vingiani, G. Curigliano, R.E. Gould, C. Castaneda, T. D’Alfonso, J. Sanchez, E. Cheng, E. Andreopoulou, M. Castillo, S. Adams, S. Demaria, W.F. Symmans, S. Michiels, S. Loi, Ann. Oncol. 30, 236–242 (2019). https://doi.org/10.1093/annonc/mdy547

    Article  CAS  PubMed  Google Scholar 

  27. A. Pataer, A. Weissferdt, A.M. Correa, A.A. Vaporciyan, B. Sepesi, J.V. Heymach, S. Berezowska, T. Cascone, S.G. Swisher, JTO Clin. Res. Rep. 3, 100420 (2022). https://doi.org/10.1016/j.jtocrr.2022.100420

    Article  PubMed  PubMed Central  Google Scholar 

  28. P. Zens, C. Bello, A. Scherz, J. Koenigsdorf, A. Pollinger, R.A. Schmid, A. Ochsenbein, C. Neppl, R. Langer, S. Berezowska, Mod. Pathol. 34, 1333–1344 (2021). https://doi.org/10.1038/s41379-021-00777-y

    Article  PubMed  PubMed Central  Google Scholar 

  29. A. Saqi, K.O. Leslie, A.L. Moreira, S. Lantuejoul, C.A. Shu, N.A. Rizvi, J.R. Sonett, K. Tajima, S.W. Sun, B.J. Gitlitz, T.V. Colby, JTO Clin. Res. Rep. 3, 100310 (2022). https://doi.org/10.1016/j.jtocrr.2022.100310

    Article  PubMed  PubMed Central  Google Scholar 

  30. K. Junker, K. Langner, F. Klinke, U. Bosse, M. Thomas, Chest 120, 1584–1591 (2001). https://doi.org/10.1378/chest.120.5.1584

    Article  CAS  PubMed  Google Scholar 

  31. A. Pataer, N. Kalhor, A.M. Correa, M.G. Raso, J.J. Erasmus, E.S. Kim, C. Behrens, J.J. Lee, J.A. Roth, D.J. Stewart, A.A. Vaporciyan, I.I. Wistuba, S.G. Swisher, M.D.A.L.C.C.R.G. University of Texas, J. Thorac. Oncol. 7, 825–832 (2012). https://doi.org/10.1097/JTO.0b013e318247504a

    Article  Google Scholar 

  32. K. Junker, M. Thomas, K. Schulmann, F. Klinke, U. Bosse, K.M. Muller, J. Cancer Res. Clin. Oncol. 123, 469–477 (1997). https://doi.org/10.1007/BF01192200

    Article  CAS  PubMed  Google Scholar 

  33. M. Larroquette, J.P. Guegan, B. Besse, S. Cousin, M. Brunet, S. Le Moulec, F. Le Loarer, C. Rey, J.C. Soria, F. Barlesi, A. Bessede, J.Y. Scoazec, I. Soubeyran, A. Italiano, J. Immunother. Cancer 10 (2022). https://doi.org/10.1136/jitc-2021-003890

  34. E.R. Parra, J. Zhang, M. Jiang, A. Tamegnon, R.K. Pandurengan, C. Behrens, L. Solis, C. Haymaker, J.V. Heymach, C. Moran, J.J. Lee, D. Gibbons, I.I. Wistuba, Nat. Commun. 14, 2364 (2023). https://doi.org/10.1038/s41467-023-37905-y

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  35. L. Seymour, G. Le Teuff, E. Brambilla, F.A. Shepherd, J.C. Soria, R. Kratzke, S. Graziano, J.Y. Douillard, R. Rosell, A. Reiman, B. Lacas, B. Lueza, S. Aviel-Ronen, A. McLeer, T. Le Chevalier, R. Pirker, M. Filipits, A. Dunant, J.P. Pignon, M.S. Tsao, L.A.-B.S. Committee, Clin. Lung Cancer 20, 66–73 e66 (2019). https://doi.org/10.1016/j.cllc.2018.10.001

    Article  CAS  Google Scholar 

  36. E. Brambilla, G. Le Teuff, S. Marguet, S. Lantuejoul, A. Dunant, S. Graziano, R. Pirker, J.Y. Douillard, T. Le Chevalier, M. Filipits, R. Rosell, R. Kratzke, H. Popper, J.C. Soria, F.A. Shepherd, L. Seymour, M.S. Tsao, J. Clin. Oncol. 34, 1223–1230 (2016). https://doi.org/10.1200/JCO.2015.63.0970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. P. Zens, C. Bello, A. Scherz, M. von Gunten, A. Ochsenbein, R.A. Schmid, S. Berezowska, Mod. Pathol. 35, 1848–1859 (2022). https://doi.org/10.1038/s41379-022-01139-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. R. Ding, P. Prasanna, G. Corredor, C. Barrera, P. Zens, C. Lu, P. Velu, P. Leo, N. Beig, H. Li, P. Toro, S. Berezowska, V. Baxi, D. Balli, M. Belete, D.L. Rimm, V. Velcheti, K. Schalper, A. Madabhushi, NPJ Precis. Oncol. 6(33) (2022). https://doi.org/10.1038/s41698-022-00277-5

  39. X. Zheng, A. Weigert, S. Reu, S. Guenther, S. Mansouri, B. Bassaly, S. Gattenlohner, F. Grimminger, S. Pullamsetti, W. Seeger, H. Winter, R. Savai, Cancer Res. 80, 4414–4425 (2020). https://doi.org/10.1158/0008-5472.CAN-20-0069

    Article  CAS  PubMed  Google Scholar 

  40. J. Huang, R.U. Osarogiagbon, D.J. Giroux, K.K. Nishimura, A. Bille, G. Cardillo, F. Detterbeck, K. Kernstine, H.K. Kim, Y. Lievens, E. Lim, E. Marom, H. Prosch, P.M. Putora, R. Rami-Porta, D. Rice, G. Rocco, V.W. Rusch, I. Opitz, F.S. Vasquez, P. Van Schil, C.-F. Jeffrey Yang, H. Asamura, J. Thorac. Oncol. (2023). https://doi.org/10.1016/j.jtho.2023.10.012

    Article  PubMed  Google Scholar 

  41. L. Xu, H. Su, Y. She, C. Dai, M. Zhao, J. Gao, H. Xie, Y. Ren, D. Xie, C. Chen, Chest 159, 2458–2469 (2021). https://doi.org/10.1016/j.chest.2020.12.012

    Article  PubMed  Google Scholar 

  42. S. Dacic, W. Travis, M. Redman, A. Saqi, W.A. Cooper, A. Borczuk, J.-H. Chung, C. Glass, J.M. Lopez, A.C. Roden, L. Sholl, A. Weissferdt, J. Posadas, A. Walker, H. Zhu, M.T. Wijeratne, C. Connolly, M. Wynes, N. Bota-Rabassedas, B. Sanchez-Espiridion, J.J. Lee, S. Berezowska, T.-Y. Chou, K. Kerr, A. Nicholson, C. Poleri, K.A. Schalper, M.-S. Tsao, D.P. Carbone, N. Ready, T. Cascone, J. Heymach, B. Sepesi, C. Shu, N. Rizvi, J. Sonett, N. Altorki, M. Provencio, P.A. Bunn, M.G. Kris, C.P. Belani, K. Kelly, I. Wistuba, J. Thorac. Oncol. 18, 1290–1302 (2023). https://doi.org/10.1016/j.jtho.2023.07.017

    Article  CAS  PubMed  Google Scholar 

  43. A. Weissferdt, A. Pataer, S.G. Swisher, J.V. Heymach, D.L. Gibbons, T. Cascone, B. Sepesi, Lung Cancer 154, 76–83 (2021). https://doi.org/10.1016/j.lungcan.2021.02.014

    Article  CAS  PubMed  Google Scholar 

  44. E. Provenzano, V. Bossuyt, G. Viale, D. Cameron, S. Badve, C. Denkert, G. MacGrogan, F. Penault-Llorca, J. Boughey, G. Curigliano, J.M. Dixon, L. Esserman, G. Fastner, T. Kuehn, F. Peintinger, G. von Minckwitz, J. White, W. Yang, W.F. Symmans, Mod. Pathol. 28, 1185–1201 (2015). https://doi.org/10.1038/modpathol.2015.74

    Article  PubMed  Google Scholar 

  45. G.M. Blumenthal, P.A. Bunn Jr, J.E. Chaft, C.E. McCoach, E.A. Perez, G.V. Scagliotti, D.P. Carbone, H. Aerts, D.L. Aisner, J. Bergh, D.A. Berry, A. Jarkowski, N. Botwood, D.A.E. Cross, M. Diehn, N.L. Drezner, R.C. Doebele, C.M. Blakely, W.E.E. Eberhardt, E. Felip, L. Gianni, S.P. Keller, P.J. Leavey, S. Malik, F. Pignatti, T.M. Prowell, M.W. Redman, N.A. Rizvi, R. Rosell, V. Rusch, D. de Ruysscher, L.H. Schwartz, R. Sridhara, R.A. Stahel, S. Swisher, J.M. Taube, W.D. Travis, P. Keegan, J.R. Wiens, I.I. Wistuba, M.W. Wynes, F.R. Hirsch, M.G. Kris, J. Thorac. Oncol. 13, 1818–1831 (2018). https://doi.org/10.1016/j.jtho.2018.09.017

    Article  CAS  PubMed  Google Scholar 

  46. PATHOLOGIC RESPONSE PROJECT. [Available from: https://www.iaslc.org/pathologic-response-project]

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Acknowledgements

The authors would like to thank Dr. Hu Xiao for her support revising our manuscript.

Funding

This work was supported by the National Natural Sciences Foundation (82103238), Beijing Hope Run Special Fund of Cancer Foundation of China (No. LC2022B19) and National Anti-Tumor Drug Surveillance System of National Cancer Center (DSS-YSF-2023022).

Author information

Authors and Affiliations

  1. Department of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, China

    Shuaibo Wang, Renda Li, Zhenlin Yang, Li Fu, Hang Yi, Zhuoheng Lv, Huandong Huo, Donghui Jin & Yousheng Mao

  2. Department of Pathology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, China

    Xujie Sun, Jiyan Dong, Li Liu, Na Cheng & Lin Yang

  3. Surgery Centre of Diabetes Mellitus, Beijing Shijitan Hospital, Capital Medical University, Beijing, 100036, China

    Hao Zhao

  4. Department of Anesthesiology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, China

    Yalong Wang

Authors
  1. Shuaibo Wang
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  2. Xujie Sun
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  3. Jiyan Dong
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  4. Li Liu
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  5. Hao Zhao
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  6. Renda Li
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  7. Zhenlin Yang
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  8. Na Cheng
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  9. Yalong Wang
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  10. Li Fu
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  11. Hang Yi
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  12. Zhuoheng Lv
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  13. Huandong Huo
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  14. Donghui Jin
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  15. Yousheng Mao
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  16. Lin Yang
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Contributions

Conceptualization, Data curation, Formal analyses, Methodology, Visualization, Writing—original draft: S.W.; Data Curation, Writing—Review: X.S., J.D., L.L.; Data Curation, Writing—Review & Editing, Funding acquisition: R.L.; Writing—Review: Z.Y.; Resources, Writing—Review: N.C.; Resources, Writing—Review: L.F.; Resources, Writing—Review: H.Y.; Resources, Writing—Review: Z.L., D.J., H.H.; Writing—Review: Y.W.; Resources, Writing—Review & Editing: L.Y.; Conceptualization, Data curation, Formal analyses, Methodology, Project administration, Resources, Supervision, Writing—original draft, Writing—Review & Editing: L.Y. & Y.M.

Corresponding authors

Correspondence to Yousheng Mao or Lin Yang.

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The study was performed in accordance with the Declaration of Helsinki.

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Wang, S., Sun, X., Dong, J. et al. Pathological response and tumor stroma immunogenic features predict long-term survival in non-small cell lung cancer after neoadjuvant chemotherapy. Cell Oncol. (2024). https://doi.org/10.1007/s13402-023-00914-6

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