The gut microbiome, immune check point inhibition and immune-related adverse events in non-small cell lung cancer

1.

Suau, A., Bonnet, R., Sutren, M., Godon, J. J., Gibson, G. R., Collins, M. D., & Doré, J. (1999). Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied and Environment Microbiology, 65(11), 4799–4807. https://doi.org/10.1128/aem.65.11.4799-4807.1999CrossRef

2.

Mazmanian, S. K., Liu, C. H., Tzianabos, A. O., & Kasper, D. L. (2005). An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell, 122(1), 107–118. https://doi.org/10.1016/j.cell.2005.05.007CrossRefPubMed

3.

Nakatsuji, T., Chen, T. H., Narala, S., Chun, K. A., Two, A. M., Yun, T., Shafiq, F., Kotol, P. F., Bouslimani, A., Melnik, A. V., Latif, H., Kim, J. N., Lockhart, A., Artis, K., David, G., Taylor, P., Streib, J., Dorrestein, P. C., Grier, A., Gill, S. R., et al. (2017). Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci Transl Med, 9(378). https://doi.org/10.1126/scitranslmed.aah4680

4.

Hooper, L. V., Littman, D. R., & Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science, 336(6086), 1268–1273. https://doi.org/10.1126/science.1223490CrossRefPubMedPubMedCentral

5.

Lee, Y. K., & Mazmanian, S. K. (2010). Has the microbiota played a critical role in the evolution of the adaptive immune system? Science, 330(6012), 1768–1773. https://doi.org/10.1126/science.1195568CrossRefPubMedPubMedCentral

6.

Chen, D. S., & Mellman, I. (2017). Elements of cancer immunity and the cancer-immune set point. Nature, 541(7637), 321–330. https://doi.org/10.1038/nature21349CrossRefPubMed

7.

Collado, M. C., Derrien, M., Isolauri, E., de Vos, W. M., & Salminen, S. (2007). Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Applied and Environment Microbiology, 73(23), 7767–7770. https://doi.org/10.1128/aem.01477-07CrossRef

8.

Fluckiger, A., Daillère, R., Sassi, M., Sixt, B. S., Liu, P., Loos, F., Richard, C., Rabu, C., Alou, M. T., Goubet, A.-G., Lemaitre, F., Ferrere, G., Derosa, L., Duong, C. P. M., Messaoudene, M., Gagné, A., Joubert, P., Sordi, L. D., Debarbieux, L., Simon, S., et al. (2020). Cross-reactivity between tumor MHC class I– restricted antigens and an enterococcal bacteriophage. Science, 369(6506), 936–942. https://doi.org/10.1126/science.aax0701CrossRefPubMed

9.

Nishida, A., Inoue, R., Inatomi, O., Bamba, S., Naito, Y., & Andoh, A. (2018). Gut microbiota in the pathogenesis of inflammatory bowel disease. Clinical Journal of Gastroenterology, 11(1), 1–10. https://doi.org/10.1007/s12328-017-0813-5CrossRefPubMed

10.

Blaser, M. J. (2016). Antibiotic use and its consequences for the normal microbiome. Science, 352(6285), 544–545. https://doi.org/10.1126/science.aad9358CrossRefPubMedPubMedCentral

11.

Holota, Y., Dovbynchuk, T., Kaji, I., Vareniuk, I., Dzyubenko, N., Chervinska, T., Zakordonets, L., Stetska, V., Ostapchenko, L., Serhiychuk, T., & Tolstanova, G. (2019). The long-term consequences of antibiotic therapy: Role of colonic short-chain fatty acids (SCFA) system and intestinal barrier integrity. PLoS ONE, 14(8), e0220642–e0220642. https://doi.org/10.1371/journal.pone.0220642CrossRefPubMedPubMedCentral

12.

Palleja, A., Mikkelsen, K. H., Forslund, S. K., Kashani, A., Allin, K. H., Nielsen, T., Hansen, T. H., Liang, S., Feng, Q., Zhang, C., Pyl, P. T., Coelho, L. P., Yang, H., Wang, J., Typas, A., Nielsen, M. F., Nielsen, H. B., Bork, P., Wang, J., Vilsbøll, T., et al. (2018). Recovery of gut microbiota of healthy adults following antibiotic exposure. Nature Microbiology, 3(11), 1255–1265. https://doi.org/10.1038/s41564-018-0257-9CrossRefPubMed

13.

Maier, L., Pruteanu, M., Kuhn, M., Zeller, G., Telzerow, A., Anderson, E. E., Brochado, A. R., Fernandez, K. C., Dose, H., Mori, H., Patil, K. R., Bork, P., & Typas, A. (2018). Extensive impact of non-antibiotic drugs on human gut bacteria. Nature, 555(7698), 623–628. https://doi.org/10.1038/nature25979CrossRefPubMedPubMedCentral

14.

Jackson, M. A., Goodrich, J. K., Maxan, M. E., Freedberg, D. E., Abrams, J. A., Poole, A. C., Sutter, J. L., Welter, D., Ley, R. E., Bell, J. T., Spector, T. D., & Steves, C. J. (2016). Proton pump inhibitors alter the composition of the gut microbiota. Gut, 65(5), 749–756. https://doi.org/10.1136/gutjnl-2015-310861CrossRefPubMed

15.

Pierrard, J., & Seront, E. (2019). Impact of the gut microbiome on immune checkpoint inhibitor efficacy-a systematic review. Current Oncology, 26(6), 395–403. https://doi.org/10.3747/co.26.5177CrossRefPubMedPubMedCentral

16.

Li, J., Jia, H., Cai, X., Zhong, H., Feng, Q., Sunagawa, S., Arumugam, M., Kultima, J. R., Prifti, E., Nielsen, T., Juncker, A. S., Manichanh, C., Chen, B., Zhang, W., Levenez, F., Wang, J., Xu, X., Xiao, L., Liang, S., Zhang, D., et al. (2014). An integrated catalog of reference genes in the human gut microbiome. Nature Biotechnology, 32(8), 834–841. https://doi.org/10.1038/nbt.2942CrossRefPubMed

17.

Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J., & Knight, R. (2011). UniFrac: An effective distance metric for microbial community comparison. ISME Journal, 5(2), 169–172. https://doi.org/10.1038/ismej.2010.133CrossRefPubMed

18.

Manchester, M., & Anand, A. (2017). Chapter Two - Metabolomics: Strategies to define the role of metabolism in virus infection and pathogenesis. In M. Kielian, T. C. Mettenleiter, & M. J. Roossinck (Eds.), Advances in virus research (Vol. 98, pp. 57–81). Academic Press. https://doi.org/10.1016/bs.aivir.2017.02.001

19.

McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., Andersen, G. L., Knight, R., & Hugenholtz, P. (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME Journal, 6(3), 610–618. https://doi.org/10.1038/ismej.2011.139CrossRefPubMed

20.

Davis, C., Kota, K., Baldhandapani, V., Gong, W., Abubucker, S., Becker, E., Martin, J., Wylie, K. M., Khetani, R., Hudson, M. E., Weinstock, G. M., & Mitreva, M. (2015). mBLAST: Keeping up with the sequencing explosion for (meta)genome analysis. J Data Mining Genomics Proteomics, 4(3). https://doi.org/10.4172/2153-0602.1000135

21.

Johnson, J. S., Spakowicz, D. J., Hong, B.-Y., Petersen, L. M., Demkowicz, P., Chen, L., Leopold, S. R., Hanson, B. M., Agresta, H. O., Gerstein, M., Sodergren, E., & Weinstock, G. M. (2019). Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nature Communications, 10(1), 5029. https://doi.org/10.1038/s41467-019-13036-1CrossRefPubMedPubMedCentral

22.

Grim, C. J., Daquigan, N., Lusk Pfefer, T. S., Ottesen, A. R., White, J. R., & Jarvis, K. G. (2017). High-resolution microbiome profiling for detection and tracking of Salmonella enterica. Frontiers in Microbiology, 8, 1587. https://doi.org/10.3389/fmicb.2017.01587CrossRefPubMedPubMedCentral

23.

Brumfield, K. D., Huq, A., Colwell, R. R., Olds, J. L., & Leddy, M. B. (2020). Microbial resolution of whole genome shotgun and 16S amplicon metagenomic sequencing using publicly available NEON data. PLoS ONE, 15(2), e0228899. https://doi.org/10.1371/journal.pone.0228899CrossRefPubMedPubMedCentral

24.

Durazzi, F., Sala, C., Castellani, G., Manfreda, G., Remondini, D., & De Cesare, A. (2021). Comparison between 16S rRNA and shotgun sequencing data for the taxonomic characterization of the gut microbiota. Science and Reports, 11(1), 3030. https://doi.org/10.1038/s41598-021-82726-yCrossRef

25.

Kuczynski, J., Lauber, C. L., Walters, W. A., Parfrey, L. W., Clemente, J. C., Gevers, D., & Knight, R. (2011). Experimental and analytical tools for studying the human microbiome. Nature Reviews Genetics, 13(1), 47–58. https://doi.org/10.1038/nrg3129CrossRefPubMedPubMedCentral

26.

Keegan, K. P., Glass, E. M., & Meyer, F. (2016). MG-RAST, a metagenomics service for analysis of microbial community structure and function. Methods in Molecular Biology, 1399, 207–233. https://doi.org/10.1007/978-1-4939-3369-3_13CrossRefPubMed

27.

Beghini, F., McIver, L. J., Blanco-Miguez, A., Dubois, L., Asnicar, F., Maharjan, S., Mailyan, A., Manghi, P., Scholz, M., Thomas, A. M., Valles-Colomer, M., Weingart, G., Zhang, Y., Zolfo, M., Huttenhower, C., Franzosa, E. A., & Segata, N. (2021). Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3. Elife, 10. https://doi.org/10.7554/eLife.65088

28.

Viaud, S., Saccheri, F., Mignot, G., Yamazaki, T., Daillère, R., Hannani, D., Enot, D. P., Pfirschke, C., Engblom, C., Pittet, M. J., Schlitzer, A., Ginhoux, F., Apetoh, L., Chachaty, E., Woerther, P. L., Eberl, G., Bérard, M., Ecobichon, C., Clermont, D., Bizet, C., et al. (2013). The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science, 342(6161), 971–976. https://doi.org/10.1126/science.1240537CrossRefPubMedPubMedCentral

29.

Daillère, R., Vétizou, M., Waldschmitt, N., Yamazaki, T., Isnard, C., Poirier-Colame, V., Duong, C. P. M., Flament, C., Lepage, P., Roberti, M. P., Routy, B., Jacquelot, N., Apetoh, L., Becharef, S., Rusakiewicz, S., Langella, P., Sokol, H., Kroemer, G., Enot, D., Roux, A., et al. (2016). Enterococcus hirae and Barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects. Immunity, 45(4), 931–943. https://doi.org/10.1016/j.immuni.2016.09.009CrossRefPubMed

30.

Oh, B., Boyle, F., Pavlakis, N., Clarke, S., Guminski, A., Eade, T., Lamoury, G., Carroll, S., Morgia, M., Kneebone, A., Hruby, G., Stevens, M., Liu, W., Corless, B., Molloy, M., Libermann, T., Rosenthal, D., & Back, M. (2021). Emerging evidence of the gut microbiome in chemotherapy: A clinical review [Mini Review]. Front Oncol, 11. https://doi.org/10.3389/fonc.2021.706331

31.

Zhao, Z., Fei, K., Bai, H., Wang, Z., Duan, J., & Wang, J. (2021). Metagenome association study of the gut microbiome revealed biomarkers linked to chemotherapy outcomes in locally advanced and advanced lung cancer. Thorac Cancer, 12(1), 66–78. https://doi.org/10.1111/1759-7714.13711CrossRefPubMed

32.

McQuade, J. L., Daniel, C. R., Helmink, B. A., & Wargo, J. A. (2019). Modulating the microbiome to improve therapeutic response in cancer. The Lancet Oncology, 20(2), e77–e91. https://doi.org/10.1016/S1470-2045(18)30952-5CrossRefPubMed

33.

Dunn, G. P., Old, L. J., & Schreiber, R. D. (2004). The three Es of cancer immunoediting. Annual Review of Immunology, 22, 329–360. https://doi.org/10.1146/annurev.immunol.22.012703.104803CrossRefPubMed

34.

Naidoo, J., Page, D. B., & Wolchok, J. D. (2014). Immune checkpoint blockade. Hematology/oncology Clinics of North America, 28(3), 585–600. https://doi.org/10.1016/j.hoc.2014.02.002CrossRefPubMed

35.

Reck, M., Rodriguez-Abreu, D., Robinson, A. G., Hui, R., Csoszi, T., Fulop, A., Gottfried, M., Peled, N., Tafreshi, A., Cuffe, S., O’Brien, M., Rao, S., Hotta, K., Leiby, M. A., Lubiniecki, G. M., Shentu, Y., Rangwala, R., Brahmer, J. R., & Investigators, K.-. (2016). Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med, 375(19), 1823-1833. https://doi.org/10.1056/NEJMoa1606774

36.

Mok, T. S. K., Wu, Y.-L., Kudaba, I., Kowalski, D. M., Cho, B. C., Turna, H. Z., Castro, G., Jr., Srimuninnimit, V., Laktionov, K. K., Bondarenko, I., Kubota, K., Lubiniecki, G. M., Zhang, J., Kush, D., Lopes, G., Adamchuk, G., Ahn, M.-J., Alexandru, A., Altundag, O., Alyasova, A., et al. (2019). Pembrolizumab versus chemotherapy for previously untreated, PD-L1-expressing, locally advanced or metastatic non-small-cell lung cancer (KEYNOTE-042): A randomised, open-label, controlled, phase 3 trial. The Lancet, 393(10183), 1819–1830. https://doi.org/10.1016/S0140-6736(18)32409-7CrossRef

37.

Gandhi, L., Rodriguez-Abreu, D., Gadgeel, S., Esteban, E., Felip, E., De Angelis, F., Domine, M., Clingan, P., Hochmair, M. J., Powell, S. F., Cheng, S. Y., Bischoff, H. G., Peled, N., Grossi, F., Jennens, R. R., Reck, M., Hui, R., Garon, E. B., Boyer, M., Rubio-Viqueira, B., et al. (2018). Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. New England Journal of Medicine, 378(22), 2078–2092. https://doi.org/10.1056/NEJMoa1801005CrossRefPubMed

38.

Paz-Ares, L., Luft, A., Vicente, D., Tafreshi, A., Gumus, M., Mazieres, J., Hermes, B., Cay Senler, F., Csoszi, T., Fulop, A., Rodriguez-Cid, J., Wilson, J., Sugawara, S., Kato, T., Lee, K. H., Cheng, Y., Novello, S., Halmos, B., Li, X., Lubiniecki, G. M., et al. (2018). Pembrolizumab plus chemotherapy for squamous non-small-cell lung cancer. New England Journal of Medicine, 379(21), 2040–2051. https://doi.org/10.1056/NEJMoa1810865CrossRefPubMed

39.

Hellmann, M. D., Paz-Ares, L., Bernabe Caro, R., Zurawski, B., Kim, S. W., Carcereny Costa, E., Park, K., Alexandru, A., Lupinacci, L., de la Mora Jimenez, E., Sakai, H., Albert, I., Vergnenegre, A., Peters, S., Syrigos, K., Barlesi, F., Reck, M., Borghaei, H., Brahmer, J. R., O’Byrne, K. J., et al. (2019). Nivolumab plus ipilimumab in advanced non-small-cell lung cancer. New England Journal of Medicine, 381(21), 2020–2031. https://doi.org/10.1056/NEJMoa1910231CrossRefPubMed

40.

Paz-Ares, L., Ciuleanu, T. E., Cobo, M., Schenker, M., Zurawski, B., Menezes, J., Richardet, E., Bennouna, J., Felip, E., Juan-Vidal, O., Alexandru, A., Sakai, H., Lingua, A., Salman, P., Souquet, P. J., De Marchi, P., Martin, C., Pérol, M., Scherpereel, A., Lu, S., et al. (2021). First-line nivolumab plus ipilimumab combined with two cycles of chemotherapy in patients with non-small-cell lung cancer (CheckMate 9LA): An international, randomised, open-label, phase 3 trial. The Lancet Oncology, 22(2), 198–211. https://doi.org/10.1016/s1470-2045(20)30641-0CrossRefPubMed

41.

Socinski, M. A., Jotte, R. M., Cappuzzo, F., Orlandi, F., Stroyakovskiy, D., Nogami, N., Rodriguez-Abreu, D., Moro-Sibilot, D., Thomas, C. A., Barlesi, F., Finley, G., Kelsch, C., Lee, A., Coleman, S., Deng, Y., Shen, Y., Kowanetz, M., Lopez-Chavez, A., Sandler, A., Reck, M., et al. (2018). Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC. New England Journal of Medicine, 378(24), 2288–2301. https://doi.org/10.1056/NEJMoa1716948CrossRefPubMed

42.

Antonia, S. J., Villegas, A., Daniel, D., Vicente, D., Murakami, S., Hui, R., Yokoi, T., Chiappori, A., Lee, K. H., de Wit, M., Cho, B. C., Bourhaba, M., Quantin, X., Tokito, T., Mekhail, T., Planchard, D., Kim, Y. C., Karapetis, C. S., Hiret, S., Ostoros, G., et al. (2017). Durvalumab after chemoradiotherapy in stage III non-small-cell lung cancer. New England Journal of Medicine, 377(20), 1919–1929. https://doi.org/10.1056/NEJMoa1709937CrossRefPubMed

43.

Schoenfeld, A. J., Antonia, S. J., Awad, M. M., Felip, E., Gainor, J., Gettinger, S. N., Hodi, F. S., Johnson, M. L., Leighl, N. B., Lovly, C. M., Mok, T., Perol, M., Reck, M., Solomon, B., Soria, J. C., Tan, D. S. W., Peters, S., & Hellmann, M. D. (2021). Clinical definition of acquired resistance to immunotherapy in patients with metastatic non-small-cell lung cancer. Annals of Oncology, 32(12), 1597–1607. https://doi.org/10.1016/j.annonc.2021.08.2151CrossRefPubMed

44.

Borghaei, H., Paz-Ares, L., Horn, L., Spigel, D. R., Steins, M., Ready, N. E., Chow, L. Q., Vokes, E. E., Felip, E., Holgado, E., Barlesi, F., Kohlhäufl, M., Arrieta, O., Burgio, M. A., Fayette, J., Lena, H., Poddubskaya, E., Gerber, D. E., Gettinger, S. N., Rudin, C. M., et al. (2015). Nivolumab versus docetaxel in advanced nonsquamous non–small-cell lung cancer. New England Journal of Medicine, 373(17), 1627–1639. https://doi.org/10.1056/NEJMoa1507643CrossRefPubMed

45.

Brahmer, J., Reckamp, K. L., Baas, P., Crinò, L., Eberhardt, W. E. E., Poddubskaya, E., Antonia, S., Pluzanski, A., Vokes, E. E., Holgado, E., Waterhouse, D., Ready, N., Gainor, J., Arén Frontera, O., Havel, L., Steins, M., Garassino, M. C., Aerts, J. G., Domine, M., Paz-Ares, L., et al. (2015). Nivolumab versus docetaxel in advanced squamous-cell non–small-cell lung cancer. New England Journal of Medicine, 373(2), 123–135. https://doi.org/10.1056/NEJMoa1504627CrossRefPubMed

46.

Rittmeyer, A., Barlesi, F., Waterkamp, D., Park, K., Ciardiello, F., von Pawel, J., Gadgeel, S. M., Hida, T., Kowalski, D. M., Dols, M. C., Cortinovis, D. L., Leach, J., Polikoff, J., Barrios, C., Kabbinavar, F., Frontera, O. A., De Marinis, F., Turna, H., Lee, J. S., Ballinger, M., et al. (2017). Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): A phase 3, open-label, multicentre randomised controlled trial. Lancet, 389(10066), 255–265. https://doi.org/10.1016/s0140-6736(16)32517-xCrossRefPubMed

47.

Herbst, R. S., Baas, P., Kim, D. W., Felip, E., Pérez-Gracia, J. L., Han, J. Y., Molina, J., Kim, J. H., Arvis, C. D., Ahn, M. J., Majem, M., Fidler, M. J., de Castro, G., & Jr., Garrido, M., Lubiniecki, G. M., Shentu, Y., Im, E., Dolled-Filhart, M., & Garon, E. B. (2016). Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): A randomised controlled trial. Lancet, 387(10027), 1540–1550. https://doi.org/10.1016/s0140-6736(15)01281-7CrossRefPubMed

48.

Herbst, R. S., Giaccone, G., de Marinis, F., Reinmuth, N., Vergnenegre, A., Barrios, C. H., Morise, M., Felip, E., Andric, Z., Geater, S., Ozguroglu, M., Zou, W., Sandler, A., Enquist, I., Komatsubara, K., Deng, Y., Kuriki, H., Wen, X., McCleland, M., Mocci, S., et al. (2020). Atezolizumab for first-line treatment of PD-L1-selected patients with NSCLC. New England Journal of Medicine, 383(14), 1328–1339. https://doi.org/10.1056/NEJMoa1917346CrossRefPubMed

49.

Carbone, D. P., Reck, M., Paz-Ares, L., Creelan, B., Horn, L., Steins, M., Felip, E., van den Heuvel, M. M., Ciuleanu, T.-E., Badin, F., Ready, N., Hiltermann, T. J. N., Nair, S., Juergens, R., Peters, S., Minenza, E., Wrangle, J. M., Rodriguez-Abreu, D., Borghaei, H., Blumenschein, G. R., et al. (2017). First-line nivolumab in stage IV or recurrent non–small-cell lung cancer. New England Journal of Medicine, 376(25), 2415–2426. https://doi.org/10.1056/NEJMoa1613493CrossRefPubMed

50.

Socinski, M. A., Jotte, R. M., Cappuzzo, F., Orlandi, F., Stroyakovskiy, D., Nogami, N., Rodríguez-Abreu, D., Moro-Sibilot, D., Thomas, C. A., Barlesi, F., Finley, G., Kelsch, C., Lee, A., Coleman, S., Deng, Y., Shen, Y., Kowanetz, M., Lopez-Chavez, A., Sandler, A., & Reck, M. (2018). Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC. New England Journal of Medicine, 378(24), 2288–2301. https://doi.org/10.1056/NEJMoa1716948CrossRefPubMed

51.

Reck, M., Rodríguez-Abreu, D., Robinson, A. G., Hui, R., Csőszi, T., Fülöp, A., Gottfried, M., Peled, N., Tafreshi, A., Cuffe, S., O’Brien, M., Rao, S., Hotta, K., Leal, T. A., Riess, J. W., Jensen, E., Zhao, B., Pietanza, M. C., & Brahmer, J. R. (2021). Five-year outcomes with pembrolizumab versus chemotherapy for metastatic non-small-cell lung cancer with PD-L1 tumor proportion score ≥ 50. Journal of Clinical Oncology, 39(21), 2339–2349. https://doi.org/10.1200/jco.21.00174CrossRefPubMedPubMedCentral

52.

Borghaei, H., Gettinger, S., Vokes, E. E., Chow, L. Q. M., Burgio, M. A., de Castro Carpeno, J., Pluzanski, A., Arrieta, O., Frontera, O. A., Chiari, R., Butts, C., Wójcik-Tomaszewska, J., Coudert, B., Garassino, M. C., Ready, N., Felip, E., García, M. A., Waterhouse, D., Domine, M., Barlesi, F., et al. (2021). Five-year outcomes from the randomized, phase III trials CheckMate 017 and 057: Nivolumab versus docetaxel in previously treated non-small-cell lung cancer. Journal of Clinical Oncology, 39(7), 723–733. https://doi.org/10.1200/jco.20.01605CrossRefPubMedPubMedCentral

53.

Gettinger, S., Horn, L., Jackman, D., Spigel, D., Antonia, S., Hellmann, M., Powderly, J., Heist, R., Sequist, L. V., Smith, D. C., Leming, P., Geese, W. J., Yoon, D., Li, A., & Brahmer, J. (2018). Five-year follow-up of nivolumab in previously treated advanced non-small-cell lung cancer: Results from the CA209-003 study. Journal of Clinical Oncology, 36(17), 1675–1684. https://doi.org/10.1200/jco.2017.77.0412CrossRefPubMed

54.

Anagnostou, V., Niknafs, N., Marrone, K., Bruhm, D. C., White, J. R., Naidoo, J., Hummelink, K., Monkhorst, K., Lalezari, F., Lanis, M., Rosner, S., Reuss, J. E., Smith, K. N., Adleff, V., Rodgers, K., Belcaid, Z., Rhymee, L., Levy, B., Feliciano, J., Hann, C. L., et al. (2020). Multimodal genomic features predict outcome of immune checkpoint blockade in non-small-cell lung cancer. Nat Cancer, 1(1), 99–111. https://doi.org/10.1038/s43018-019-0008-8CrossRefPubMedPubMedCentral

55.

Rizvi, H., Sanchez-Vega, F., La, K., Chatila, W., Jonsson, P., Halpenny, D., Plodkowski, A., Long, N., Sauter, J. L., Rekhtman, N., Hollmann, T., Schalper, K. A., Gainor, J. F., Shen, R., Ni, A., Arbour, K. C., Merghoub, T., Wolchok, J., Snyder, A., Chaft, J. E., et al. (2018). Molecular determinants of response to anti-programmed cell death (PD)-1 and anti-programmed death-ligand 1 (PD-L1) blockade in patients with non-small-cell lung cancer profiled with targeted next-generation sequencing. Journal of Clinical Oncology, 36(7), 633–641. https://doi.org/10.1200/jco.2017.75.3384CrossRefPubMedPubMedCentral

56.

Uruga, H., & Mino-Kenudson, M. (2021). Predictive biomarkers for response to immune checkpoint inhibitors in lung cancer: PD-L1 and beyond. Virchows Archiv, 478(1), 31–44. https://doi.org/10.1007/s00428-021-03030-8CrossRefPubMed

57.

Postow, M. A., Sidlow, R., & Hellmann, M. D. (2018). Immune-related adverse events associated with immune checkpoint blockade. New England Journal of Medicine, 378(2), 158–168. https://doi.org/10.1056/NEJMra1703481CrossRefPubMed

58.

Naidoo, J., Page, D. B., Li, B. T., Connell, L. C., Schindler, K., Lacouture, M. E., Postow, M. A., & Wolchok, J. D. (2015). Toxicities of the anti-PD-1 and anti-PD-L1 immune checkpoint antibodies. Annals of Oncology, 26(12), 2375–2391. https://doi.org/10.1093/annonc/mdv383CrossRefPubMedPubMedCentral

59.

Conroy, M., & Naidoo, J. (2022). Immune-related adverse events and the balancing act of immunotherapy. Nature Communications, 13(1), 392. https://doi.org/10.1038/s41467-022-27960-2CrossRefPubMedPubMedCentral

60.

Iwama, S., De Remigis, A., Callahan, M. K., Slovin, S. F., Wolchok, J. D., & Caturegli, P. (2014). Pituitary expression of CTLA-4 mediates hypophysitis secondary to administration of CTLA-4 blocking antibody. Science Translational Medicine, 6(230), 230ra245. https://doi.org/10.1126/scitranslmed.3008002CrossRef

61.

Caturegli, P., Di Dalmazi, G., Lombardi, M., Grosso, F., Larman, H. B., Larman, T., Taverna, G., Cosottini, M., & Lupi, I. (2016). Hypophysitis secondary to cytotoxic T-lymphocyte-associated protein 4 blockade: Insights into pathogenesis from an autopsy series. The American journal of pathology, 186(12), 3225–3235. https://doi.org/10.1016/j.ajpath.2016.08.020CrossRefPubMedPubMedCentral

62.

Risbjerg, R. S., Hansen, M. V., Sørensen, A. S., & Kragstrup, T. W. (2020). The effects of B cell depletion on immune related adverse events associated with immune checkpoint inhibition. Experimental Hematology & Oncology, 9(1), 9. https://doi.org/10.1186/s40164-020-00167-1CrossRef

63.

Tarhini, A. A., Zahoor, H., Lin, Y., Malhotra, U., Sander, C., Butterfield, L. H., & Kirkwood, J. M. (2015). Baseline circulating IL-17 predicts toxicity while TGF-beta1 and IL-10 are prognostic of relapse in ipilimumab neoadjuvant therapy of melanoma. Journal for Immunotherapy of Cancer, 3, 39. https://doi.org/10.1186/s40425-015-0081-1CrossRefPubMedPubMedCentral

64.

Berman, D., Parker, S. M., Siegel, J., Chasalow, S. D., Weber, J., Galbraith, S., Targan, S. R., & Wang, H. L. (2010). Blockade of cytotoxic T-lymphocyte antigen-4 by ipilimumab results in dysregulation of gastrointestinal immunity in patients with advanced melanoma. Cancer immunity, 10, 11–11. https://pubmed.ncbi.nlm.nih.gov/21090563; https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2999944/

65.

Cascone, T., William, W. N., Jr., Weissferdt, A., Leung, C. H., Lin, H. Y., Pataer, A., Godoy, M. C. B., Carter, B. W., Federico, L., Reuben, A., Khan, M. A. W., Dejima, H., Francisco-Cruz, A., Parra, E. R., Solis, L. M., Fujimoto, J., Tran, H. T., Kalhor, N., Fossella, F. V., Mott, F. E., et al. (2021). Neoadjuvant nivolumab or nivolumab plus ipilimumab in operable non-small cell lung cancer: The phase 2 randomized NEOSTAR trial. Nature Medicine, 27(3), 504–514. https://doi.org/10.1038/s41591-020-01224-2CrossRefPubMedPubMedCentral

66.

Hodi, F. S., O’Day, S. J., McDermott, D. F., Weber, R. W., Sosman, J. A., Haanen, J. B., Gonzalez, R., Robert, C., Schadendorf, D., Hassel, J. C., Akerley, W., van den Eertwegh, A. J., Lutzky, J., Lorigan, P., Vaubel, J. M., Linette, G. P., Hogg, D., Ottensmeier, C. H., Lebbe, C., Peschel, C., et al. (2010). Improved survival with ipilimumab in patients with metastatic melanoma. New England Journal of Medicine, 363(8), 711–723. https://doi.org/10.1056/NEJMoa1003466CrossRefPubMed

67.

Tomasini, P., Khobta, N., Greillier, L., & Barlesi, F. (2012). Ipilimumab: Its potential in non-small cell lung cancer. Therapeutic Advances in Medical Oncology, 4(2), 43–50. https://doi.org/10.1177/1758834011431718CrossRefPubMedPubMedCentral

68.

Horn, L., Spigel, D. R., Vokes, E. E., Holgado, E., Ready, N., Steins, M., Poddubskaya, E., Borghaei, H., Felip, E., Paz-Ares, L., Pluzanski, A., Reckamp, K. L., Burgio, M. A., Kohlhäeufl, M., Waterhouse, D., Barlesi, F., Antonia, S., Arrieta, O., Fayette, J., Crinò, L., et al. (2017). Nivolumab versus docetaxel in previously treated patients with advanced non-small-cell lung cancer: Two-year outcomes from two randomized, open-label, phase III trials (CheckMate 017 and CheckMate 057). Journal of Clinical Oncology, 35(35), 3924–3933. https://doi.org/10.1200/jco.2017.74.3062CrossRefPubMedPubMedCentral

69.

Komiya, K., Nakamura, T., Abe, T., Ogusu, S., Nakashima, C., Takahashi, K., Kimura, S., & Sueoka-Aragane, N. (2019). Discontinuation due to immune-related adverse events is a possible predictive factor for immune checkpoint inhibitors in patients with non-small cell lung cancer. Thorac Cancer, 10(9), 1798–1804. https://doi.org/10.1111/1759-7714.13149CrossRefPubMedPubMedCentral

70.

Cortellini, A., Friedlaender, A., Banna, G. L., Porzio, G., Bersanelli, M., Cappuzzo, F., Aerts, J. G. J. V., Giusti, R., Bria, E., Cortinovis, D., Grossi, F., Migliorino, M. R., Galetta, D., Passiglia, F., Berardi, R., Mazzoni, F., Di Noia, V., Signorelli, D., Tuzi, A., Gelibter, A., et al. (2020). Immune-related adverse events of pembrolizumab in a large real-world cohort of patients with NSCLC with a PD-L1 expression ≥ 50% and their relationship with clinical outcomes. Clinical Lung Cancer, 21(6), 498-508.e492. https://doi.org/10.1016/j.cllc.2020.06.010CrossRefPubMed

71.

Teraoka, S., Fujimoto, D., Morimoto, T., Kawachi, H., Ito, M., Sato, Y., Nagata, K., Nakagawa, A., Otsuka, K., Uehara, K., Imai, Y., Ishida, K., Fukuoka, J., & Tomii, K. (2017). Early immune-related adverse events and association with outcome in advanced non-small cell lung cancer patients treated with nivolumab: A prospective cohort study. Journal of Thoracic Oncology, 12(12), 1798–1805. https://doi.org/10.1016/j.jtho.2017.08.022CrossRefPubMed

72.

Sato, K., Akamatsu, H., Murakami, E., Sasaki, S., Kanai, K., Hayata, A., Tokudome, N., Akamatsu, K., Koh, Y., Ueda, H., Nakanishi, M., & Yamamoto, N. (2018). Correlation between immune-related adverse events and efficacy in non-small cell lung cancer treated with nivolumab. Lung Cancer, 115, 71–74. https://doi.org/10.1016/j.lungcan.2017.11.019CrossRefPubMed

73.

Toi, Y., Sugawara, S., Kawashima, Y., Aiba, T., Kawana, S., Saito, R., Tsurumi, K., Suzuki, K., Shimizu, H., Sugisaka, J., Ono, H., Domeki, Y., Terayama, K., Nakamura, A., Yamanda, S., Kimura, Y., & Honda, Y. (2018). Association of immune-related adverse events with clinical benefit in patients with advanced non-small-cell lung cancer treated with nivolumab. The Oncologist, 23(11), 1358–1365. https://doi.org/10.1634/theoncologist.2017-0384CrossRefPubMedPubMedCentral

74.

Dall’Olio, F. G., Nunno, V. D., & Massari, F. (2020). Immortal time bias question in the association between toxicity and outcome of immune checkpoint inhibitors. Journal of Clinical Oncology, 38(1), 105-106. https://doi.org/10.1200/jco.19.01728

75.

Forde, P. M., Chaft, J. E., Smith, K. N., Anagnostou, V., Cottrell, T. R., Hellmann, M. D., Zahurak, M., Yang, S. C., Jones, D. R., Broderick, S., Battafarano, R. J., Velez, M. J., Rekhtman, N., Olah, Z., Naidoo, J., Marrone, K. A., Verde, F., Guo, H., Zhang, J., Caushi, J. X., et al. (2018). Neoadjuvant PD-1 blockade in resectable lung cancer. New England Journal of Medicine, 378(21), 1976–1986. https://doi.org/10.1056/NEJMoa1716078CrossRefPubMed

76.

Gao, S., Li, N., Gao, S., Xue, Q., Ying, J., Wang, S., Tao, X., Zhao, J., Mao, Y., Wang, B., Shao, K., Lei, W., Wang, D., Lv, F., Zhao, L., Zhang, F., Zhao, Z., Su, K., Tan, F., Gao, Y., et al. (2020). Neoadjuvant PD-1 inhibitor (Sintilimab) in NSCLC. Journal of Thoracic Oncology, 15(5), 816–826. https://doi.org/10.1016/j.jtho.2020.01.017CrossRefPubMed

77.

Provencio, M., Nadal, E., Insa, A., García-Campelo, M. R., Casal-Rubio, J., Dómine, M., Majem, M., Rodríguez-Abreu, D., Martínez-Martí, A., De Castro Carpeño, J., Cobo, M., López Vivanco, G., Del Barco, E., Bernabé Caro, R., Viñolas, N., Barneto Aranda, I., Viteri, S., Pereira, E., Royuela, A., Casarrubios, M., et al. (2020). Neoadjuvant chemotherapy and nivolumab in resectable non-small-cell lung cancer (NADIM): An open-label, multicentre, single-arm, phase 2 trial. The lancet Oncology, 21(11), 1413–1422. https://doi.org/10.1016/s1470-2045(20)30453-8CrossRefPubMed

78.

Routy, B., Le Chatelier, E., Derosa, L., Duong, C. P. M., Alou, M. T., Daillère, R., Fluckiger, A., Messaoudene, M., Rauber, C., Roberti, M. P., Fidelle, M., Flament, C., Poirier-Colame, V., Opolon, P., Klein, C., Iribarren, K., Mondragón, L., Jacquelot, N., Qu, B., Ferrere, G., et al. (2018). Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science, 359(6371), 91–97. https://doi.org/10.1126/science.aan3706CrossRefPubMed

79.

Iida, N., Dzutsev, A., Stewart, C. A., Smith, L., Bouladoux, N., Weingarten, R. A., Molina, D. A., Salcedo, R., Back, T., Cramer, S., Dai, R.-M., Kiu, H., Cardone, M., Naik, S., Patri, A. K., Wang, E., Marincola, F. M., Frank, K. M., Belkaid, Y., Trinchieri, G., et al. (2013). Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science, 342(6161), 967–970. https://doi.org/10.1126/science.1240527CrossRefPubMedPubMedCentral

80.

Vétizou, M., Pitt, J. M., Daillère, R., Lepage, P., Waldschmitt, N., Flament, C., Rusakiewicz, S., Routy, B., Roberti, M. P., Duong, C. P. M., Poirier-Colame, V., Roux, A., Becharef, S., Formenti, S., Golden, E., Cording, S., Eberl, G., Schlitzer, A., Ginhoux, F., Mani, S., et al. (2015). Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science, 350(6264), 1079–1084. https://doi.org/10.1126/science.aad1329CrossRefPubMedPubMedCentral

81.

Coutzac, C., Jouniaux, J.-M., Paci, A., Schmidt, J., Mallardo, D., Seck, A., Asvatourian, V., Cassard, L., Saulnier, P., Lacroix, L., Woerther, P.-L., Vozy, A., Naigeon, M., Nebot-Bral, L., Desbois, M., Simeone, E., Mateus, C., Boselli, L., Grivel, J., Soularue, E., et al. (2020). Systemic short chain fatty acids limit antitumor effect of CTLA-4 blockade in hosts with cancer. Nature Communications, 11(1), 2168. https://doi.org/10.1038/s41467-020-16079-xCrossRefPubMedPubMedCentral

82.

Frankel, A. E., Coughlin, L. A., Kim, J., Froehlich, T. W., Xie, Y., Frenkel, E. P., & Koh, A. Y. (2017). Metagenomic shotgun sequencing and unbiased metabolomic profiling identify specific human gut microbiota and metabolites associated with immune checkpoint therapy efficacy in melanoma patients. Neoplasia, 19(10), 848–855. https://doi.org/10.1016/j.neo.2017.08.004CrossRefPubMedPubMedCentral

83.

Lurienne, L., Cervesi, J., Duhalde, L., de Gunzburg, J., Andremont, A., Zalcman, G., Buffet, R., & Bandinelli, P. A. (2020). NSCLC immunotherapy efficacy and antibiotic use: A systematic review and meta-analysis. Journal of Thoracic Oncology, 15(7), 1147–1159. https://doi.org/10.1016/j.jtho.2020.03.002CrossRefPubMed

84.

Wilson, B. E., Routy, B., Nagrial, A., & Chin, V. T. (2020). The effect of antibiotics on clinical outcomes in immune-checkpoint blockade: A systematic review and meta-analysis of observational studies. Cancer Immunology, Immunotherapy, 69(3), 343–354. https://doi.org/10.1007/s00262-019-02453-2CrossRefPubMed

85.

Derosa, L., Routy, B., Thomas, A. M., Iebba, V., Zalcman, G., Friard, S., Mazieres, J., Audigier-Valette, C., Moro-Sibilot, D., Goldwasser, F., Silva, C. A. C., Terrisse, S., Bonvalet, M., Scherpereel, A., Pegliasco, H., Richard, C., Ghiringhelli, F., Elkrief, A., Desilets, A., Blanc-Durand, F., et al. (2022). Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer. Nature Medicine. https://doi.org/10.1038/s41591-021-01655-5

86.

Verschueren, M. V., van der Welle, C. M. C., Tonn, M., Schramel, F., Peters, B. J. M., & van de Garde, E. M. W. (2021). The association between gut microbiome affecting concomitant medication and the effectiveness of immunotherapy in patients with stage IV NSCLC. Science and Reports, 11(1), 23331. https://doi.org/10.1038/s41598-021-02598-0CrossRef

87.

Ochi, N., Ichihara, E., Takigawa, N., Harada, D., Inoue, K., Shibayama, T., Hosokawa, S., Kishino, D., Harita, S., Oda, N., Hara, N., Hotta, K., Maeda, Y., & Kiura, K. (2021). The effects of antibiotics on the efficacy of immune checkpoint inhibitors in patients with non-small-cell lung cancer differ based on PD-L1 expression. European Journal of Cancer, 149, 73–81. https://doi.org/10.1016/j.ejca.2021.02.040CrossRefPubMed

88.

Giordan, Q., Salleron, J., Vallance, C., Moriana, C., & Clement-Duchene, C. (2021). Impact of antibiotics and proton pump inhibitors on efficacy and tolerance of anti-PD-1 immune checkpoint inhibitors. Frontiers in Immunology, 12, 716317. https://doi.org/10.3389/fimmu.2021.716317CrossRefPubMedPubMedCentral

89.

Geum, M. J., Kim, C., Kang, J. E., Choi, J. H., Kim, J. S., Son, E. S., Lim, S. M., & Rhie, S. J. (2021). Broad-spectrum antibiotic regimen affects survival in patients receiving nivolumab for non-small cell lung cancer. Pharmaceuticals (Basel), 14(5). https://doi.org/10.3390/ph14050445

90.

Cortellini, A., Ricciuti, B., Facchinetti, F., Alessi, J. V. M., Venkatraman, D., Dall’Olio, F. G., Cravero, P., Vaz, V. R., Ottaviani, D., Majem, M., Piedra, A., Sullivan, I., Lee, K. A., Lamberti, G., Hussain, N., Clark, J., Bolina, A., Barba, A., Benitez, J. C., Gorría, T., et al. (2021). Antibiotic-exposed patients with non-small-cell lung cancer preserve efficacy outcomes following first-line chemo-immunotherapy. Annals of Oncology, 32(11), 1391-1399. https://doi.org/10.1016/j.annonc.2021.08.1744

91.

Cortellini, A., Di Maio, M., Nigro, O., Leonetti, A., Cortinovis, D. L., Aerts, J. G. J. V., Guaitoli, G., Barbieri, F., Giusti, R., Ferrara, M. G., Bria, E., Argento, E., Grossi, F., Rijavec, E., Guida, A., Berardi, R., Torniai, M., Sforza, V., Genova, C., Mazzoni, F., et al. (2021). Differential influence of antibiotic therapy and other medications on oncological outcomes of patients with non-small cell lung cancer treated with first-line pembrolizumab versus cytotoxic chemotherapy. Journal for ImmunoTherapy of Cancer, 9(4), e002421. https://doi.org/10.1136/jitc-2021-002421CrossRefPubMedPubMedCentral

92.

Castello, A., Rossi, S., Toschi, L., & Lopci, E. (2021). Impact of antibiotic therapy and metabolic parameters in non-small cell lung cancer patients receiving checkpoint inhibitors. J Clin Med, 10(6), 1251. https://doi.org/10.3390/jcm10061251

93.

Chalabi, M., Cardona, A., Nagarkar, D. R., Dhawahir Scala, A., Gandara, D. R., Rittmeyer, A., Albert, M. L., Powles, T., Kok, M., & Herrera, F. G. (2020). Efficacy of chemotherapy and atezolizumab in patients with non-small-cell lung cancer receiving antibiotics and proton pump inhibitors: Pooled post hoc analyses of the OAK and POPLAR trials. Annals of Oncology, 31(4), 525–531. https://doi.org/10.1016/j.annonc.2020.01.006CrossRefPubMed

94.

Zhao, S., Gao, G., Li, W., Li, X., Zhao, C., Jiang, T., Jia, Y., He, Y., Li, A., Su, C., Ren, S., Chen, X., & Zhou, C. (2019). Antibiotics are associated with attenuated efficacy of anti-PD-1/PD-L1 therapies in Chinese patients with advanced non-small cell lung cancer. Lung Cancer, 130, 10–17. https://doi.org/10.1016/j.lungcan.2019.01.017CrossRefPubMed

95.

Pinato, D. J., Howlett, S., Ottaviani, D., Urus, H., Patel, A., Mineo, T., Brock, C., Power, D., Hatcher, O., Falconer, A., Ingle, M., Brown, A., Gujral, D., Partridge, S., Sarwar, N., Gonzalez, M., Bendle, M., Lewanski, C., Newsom-Davis, T., Allara, E., et al. (2019). Association of prior antibiotic treatment with survival and response to immune checkpoint inhibitor therapy in patients with cancer. JAMA Oncology, 5(12), 1774–1778. https://doi.org/10.1001/jamaoncol.2019.2785CrossRefPubMedPubMedCentral

96.

Ouaknine Krief, J., Helly de Tauriers, P., Dumenil, C., Neveux, N., Dumoulin, J., Giraud, V., Labrune, S., Tisserand, J., Julie, C., Emile, J.-F., Chinet, T., & Giroux Leprieur, E. (2019). Role of antibiotic use, plasma citrulline and blood microbiome in advanced non-small cell lung cancer patients treated with nivolumab. Journal for ImmunoTherapy of Cancer, 7(1), 176. https://doi.org/10.1186/s40425-019-0658-1CrossRefPubMedPubMedCentral

97.

Huemer, F., Lang, D., Westphal, T., Gampenrieder, S. P., Hutarew, G., Weiss, L., Hackl, H., Lamprecht, B., Rinnerthaler, G., & Greil, R. (2019). Baseline absolute lymphocyte count and ECOG performance score are associated with survival in advanced non-small cell lung cancer undergoing PD-1/PD-L1 blockade. J Clin Med, 8(7). https://doi.org/10.3390/jcm8071014

98.

Hakozaki, T., Okuma, Y., Omori, M., & Hosomi, Y. (2019). Impact of prior antibiotic use on the efficacy of nivolumab for non-small cell lung cancer. Oncology Letters, 17(3), 2946–2952. https://doi.org/10.3892/ol.2019.9899CrossRefPubMedPubMedCentral

99.

Galli, G., Triulzi, T., Proto, C., Signorelli, D., Imbimbo, M., Poggi, M., Fucà, G., Ganzinelli, M., Vitali, M., Palmieri, D., Tessari, A., de Braud, F., Garassino, M. C., Colombo, M. P., & Lo Russo, G. (2019). Association between antibiotic-immunotherapy exposure ratio and outcome in metastatic non small cell lung cancer. Lung Cancer, 132, 72–78. https://doi.org/10.1016/j.lungcan.2019.04.008CrossRefPubMed

100.

Derosa, L., Hellmann, M. D., Spaziano, M., Halpenny, D., Fidelle, M., Rizvi, H., Long, N., Plodkowski, A. J., Arbour, K. C., Chaft, J. E., Rouche, J. A., Zitvogel, L., Zalcman, G., Albiges, L., Escudier, B., & Routy, B. (2018). Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non-small-cell lung cancer. Annals of Oncology, 29(6), 1437–1444. https://doi.org/10.1093/annonc/mdy103CrossRefPubMedPubMedCentral

101.

Stokes, W. A., Behera, M., Jiang, R., Gutman, D., Giuste, F., Burns, A., Sebastian, N., Ramalingam, S., Sukhatme, V., Lowe, M. C., Ramalingam, S. S., Sukhatme, V., & Moghanaki, D. (2021). Effect of antibiotic therapy on immunotherapy outcomes for non-small cell lung cancer: Analysis from the Veterans Health Administration Database. Journal of Clinical Oncology, 39(15_suppl), 9017–9017. https://doi.org/10.1200/JCO.2021.39.15_suppl.9017

102.

Mohiuddin, J. J., Chu, B., Facciabene, A., Poirier, K., Wang, X., Doucette, A., Zheng, C., Xu, W., Anstadt, E. J., Amaravadi, R. K., Karakousis, G. C., Mitchell, T. C., Huang, A. C., Shabason, J. E., Lin, A., Swisher-McClure, S., Maity, A., Schuchter, L. M., & Lukens, J. N. (2021). Association of antibiotic exposure with survival and toxicity in patients with melanoma receiving immunotherapy. Journal of the National Cancer Institute, 113(2), 162–170. https://doi.org/10.1093/jnci/djaa057CrossRefPubMed

103.

Weber, J., Mandala, M., Del Vecchio, M., Gogas, H. J., Arance, A. M., Cowey, C. L., Dalle, S., Schenker, M., Chiarion-Sileni, V., Marquez-Rodas, I., Grob, J. J., Butler, M. O., Middleton, M. R., Maio, M., Atkinson, V., Queirolo, P., Gonzalez, R., Kudchadkar, R. R., Smylie, M., Meyer, N., et al. (2017). Adjuvant nivolumab versus ipilimumab in resected stage III or IV melanoma. New England Journal of Medicine, 377(19), 1824–1835. https://doi.org/10.1056/NEJMoa1709030CrossRefPubMed

104.

Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J. J., Rutkowski, P., Lao, C. D., Cowey, C. L., Schadendorf, D., Wagstaff, J., Dummer, R., Ferrucci, P. F., Smylie, M., Hogg, D., Hill, A., Marquez-Rodas, I., Haanen, J., Guidoboni, M., Maio, M., Schoffski, P., Carlino, M. S., et al. (2019). Five-year survival with combined nivolumab and ipilimumab in advanced melanoma. New England Journal of Medicine, 381(16), 1535–1546. https://doi.org/10.1056/NEJMoa1910836CrossRefPubMed

105.

Sivan, A., Corrales, L., Hubert, N., Williams, J. B., Aquino-Michaels, K., Earley, Z. M., Benyamin, F. W., Lei, Y. M., Jabri, B., Alegre, M. L., Chang, E. B., & Gajewski, T. F. (2015). Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science, 350(6264), 1084–1089. https://doi.org/10.1126/science.aac4255CrossRefPubMedPubMedCentral

106.

Matson, V., Fessler, J., Bao, R., Chongsuwat, T., Zha, Y., Alegre, M. L., Luke, J. J., & Gajewski, T. F. (2018). The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science, 359(6371), 104–108. https://doi.org/10.1126/science.aao3290CrossRefPubMedPubMedCentral

107.

Gopalakrishnan, V., Spencer, C. N., Nezi, L., Reuben, A., Andrews, M. C., Karpinets, T. V., Prieto, P. A., Vicente, D., Hoffman, K., Wei, S. C., Cogdill, A. P., Zhao, L., Hudgens, C. W., Hutchinson, D. S., Manzo, T., Macedo, M. P., d., Cotechini, T., Kumar, T., Chen, W. S., Reddy, S. M., et al. (2018). Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science, 359(6371), 97–103. https://doi.org/10.1126/science.aan4236CrossRefPubMed

108.

Robinson, M., Vervier, K., Popple, A., Harris, S., Hudson, R., Adams, D., Rabbie, R., Milne, D., Booth, C., Welsh, S. J., Bruce, D., Corrie, P. G., & Lawley, T. (2021). Using precision microbiome profiling to develop a biomarker for immune checkpoint inhibitor response and a novel therapeutic. Journal of Clinical Oncology, 39(15_suppl), e21546-e21546. https://doi.org/10.1200/JCO.2021.39.15_suppl.e21546

109.

Robinson, M., Vervier, K., Harris, S., Adams, D., Milne, D., Booth, C., Barker, E., Parkinson, C., Bruce, D., Welesh, S., Corrie, P., & Lawley, T. (2020). 673 Precision microbiome mapping identifies a microbiome signature predictive of Immune checkpoint inhibitor response across multiple research study cohorts. Journal for ImmunoTherapy of Cancer, 8(Suppl 3), A404–A404. https://doi.org/10.1136/jitc-2020-SITC2020.0673CrossRef

110.

Dubin, K., Callahan, M. K., Ren, B., Khanin, R., Viale, A., Ling, L., No, D., Gobourne, A., Littmann, E., Huttenhower, C., Pamer, E. G., & Wolchok, J. D. (2016). Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nature Communications, 7(1), 10391. https://doi.org/10.1038/ncomms10391CrossRefPubMedPubMedCentral

111.

Chaput, N., Lepage, P., Coutzac, C., Soularue, E., Le Roux, K., Monot, C., Boselli, L., Routier, E., Cassard, L., Collins, M., Vaysse, T., Marthey, L., Eggermont, A., Asvatourian, V., Lanoy, E., Mateus, C., Robert, C., & Carbonnel, F. (2017). Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Annals of Oncology, 28(6), 1368–1379. https://doi.org/10.1093/annonc/mdx108CrossRefPubMed

112.

Motzer, R. J., Tannir, N. M., McDermott, D. F., Aren Frontera, O., Melichar, B., Choueiri, T. K., Plimack, E. R., Barthelemy, P., Porta, C., George, S., Powles, T., Donskov, F., Neiman, V., Kollmannsberger, C. K., Salman, P., Gurney, H., Hawkins, R., Ravaud, A., Grimm, M. O., Bracarda, S., et al. (2018). Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. New England Journal of Medicine, 378(14), 1277–1290. https://doi.org/10.1056/NEJMoa1712126CrossRefPubMed

113.

Derosa, L., Routy, B., Fidelle, M., Iebba, V., Alla, L., Pasolli, E., Segata, N., Desnoyer, A., Pietrantonio, F., Ferrere, G., Fahrner, J. E., Le Chatellier, E., Pons, N., Galleron, N., Roume, H., Duong, C. P. M., Mondragón, L., Iribarren, K., Bonvalet, M., Terrisse, S., et al. (2020). Gut bacteria composition drives primary resistance to cancer immunotherapy in renal cell carcinoma patients. European Urology, 78(2), 195–206. https://doi.org/10.1016/j.eururo.2020.04.044CrossRefPubMed

114.

Guven, D. C., Acar, R., Yekeduz, E., Bilgetekin, I., Baytemur, N. K., Erol, C., Ceylan, F., Sendur, M. A., Demirci, U., Urun, Y., Karadurmus, N., Erman, M., & Kilickap, S. (2021). The association between antibiotic use and survival in renal cell carcinoma patients treated with immunotherapy: A multi-center study. Current Problems Cancer, 100760. https://doi.org/10.1016/j.currproblcancer.2021.100760

115.

Salgia, N. J., Bergerot, P. G., Maia, M. C., Dizman, N., Hsu, J., Gillece, J. D., Folkerts, M., Reining, L., Trent, J., Highlander, S. K., & Pal, S. K. (2020). Stool microbiome profiling of patients with metastatic renal cell carcinoma receiving anti-PD-1 immune checkpoint inhibitors. European Urology, 78(4), 498–502. https://doi.org/10.1016/j.eururo.2020.07.011CrossRefPubMed

116.

Eisenhauer, E. A., Therasse, P., Bogaerts, J., Schwartz, L. H., Sargent, D., Ford, R., Dancey, J., Arbuck, S., Gwyther, S., Mooney, M., Rubinstein, L., Shankar, L., Dodd, L., Kaplan, R., Lacombe, D., & Verweij, J. (2009). New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1.1). Eur J Cancer, 45(2), 228–247. https://doi.org/10.1016/j.ejca.2008.10.026CrossRefPubMed

117.

Schwartz, L. H., Litière, S., de Vries, E., Ford, R., Gwyther, S., Mandrekar, S., Shankar, L., Bogaerts, J., Chen, A., Dancey, J., Hayes, W., Hodi, F. S., Hoekstra, O. S., Huang, E. P., Lin, N., Liu, Y., Therasse, P., Wolchok, J. D., & Seymour, L. (2016). RECIST 1.1-Update and clarification: From the RECIST committee. European Journal of Cancer, 62, 132–137. https://doi.org/10.1016/j.ejca.2016.03.081CrossRefPubMedPubMedCentral

118.

Jin, Y., Dong, H., Xia, L., Yang, Y., Zhu, Y., Shen, Y., Zheng, H., Yao, C., Wang, Y., & Lu, S. (2019). The diversity of gut microbiome is associated with favorable responses to anti-programmed death 1 immunotherapy in Chinese patients with NSCLC. Journal of Thoracic Oncology, 14(8), 1378–1389. https://doi.org/10.1016/j.jtho.2019.04.007CrossRefPubMed

119.

Hakozaki, T., Richard, C., Elkrief, A., Hosomi, Y., Benlaïfaoui, M., Mimpen, I., Terrisse, S., Derosa, L., Zitvogel, L., Routy, B., & Okuma, Y. (2020). The gut microbiome associates with immune checkpoint inhibition outcomes in patients with advanced non-small cell lung cancer. Cancer Immunology Research, 8(10), 1243–1250. https://doi.org/10.1158/2326-6066.Cir-20-0196CrossRefPubMed

120.

Liu, T., Xiong, Q., Li, L., & Hu, Y. (2019). Intestinal microbiota predicts lung cancer patients at risk of immune-related diarrhea. Immunotherapy, 11(5), 385–396. https://doi.org/10.2217/imt-2018-0144CrossRefPubMed

121.

Chau, J., Yadav, M., Liu, B., Furqan, M., Dai, Q., Shahi, S., Gupta, A., Mercer, K. N., Eastman, E., Hejleh, T. A., Chan, C., Weiner, G. J., Cherwin, C., Lee, S. T. M., Zhong, C., Mangalam, A., & Zhang, J. (2021). Prospective correlation between the patient microbiome with response to and development of immune-mediated adverse effects to immunotherapy in lung cancer. BMC Cancer, 21(1), 808. https://doi.org/10.1186/s12885-021-08530-zCrossRefPubMedPubMedCentral

122.

Baruch, E. N., Youngster, I., Ben-Betzalel, G., Ortenberg, R., Lahat, A., Katz, L., Adler, K., Dick-Necula, D., Raskin, S., Bloch, N., Rotin, D., Anafi, L., Avivi, C., Melnichenko, J., Steinberg-Silman, Y., Mamtani, R., Harati, H., Asher, N., Shapira-Frommer, R., Brosh-Nissimov, T., et al. (2021). Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients. Science, 371(6529), 602–609. https://doi.org/10.1126/science.abb5920CrossRefPubMed

123.

Davar, D., Dzutsev, A. K., McCulloch, J. A., Rodrigues, R. R., Chauvin, J.-M., Morrison, R. M., Deblasio, R. N., Menna, C., Ding, Q., Pagliano, O., Zidi, B., Zhang, S., Badger, J. H., Vetizou, M., Cole, A. M., Fernandes, M. R., Prescott, S., Costa, R. G. F., Balaji, A. K., Morgun, A., et al. (2021). Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science, 371(6529), 595–602. https://doi.org/10.1126/science.abf3363CrossRefPubMedPubMedCentral

124.

Dizman, N., Meza, L., Bergerot, P., Alcantara, M., Dorff, T., Lyou, Y., Frankel, P., Cui, Y., Mira, V., Llamas, M., Hsu, J., Zengin, Z., Salgia, N., Salgia, S., Malhotra, J., Chawla, N., Chehrazi-Raffle, A., Muddasani, R., Gillece, J., Reining, L., et al. (2022). Nivolumab plus ipilimumab with or without live bacterial supplementation in metastatic renal cell carcinoma: a randomized phase 1 trial. Nature Medicine. https://doi.org/10.1038/s41591-022-01694-6

125.

van Nood, E., Vrieze, A., Nieuwdorp, M., Fuentes, S., Zoetendal, E. G., de Vos, W. M., Visser, C. E., Kuijper, E. J., Bartelsman, J. F., Tijssen, J. G., Speelman, P., Dijkgraaf, M. G., & Keller, J. J. (2013). Duodenal infusion of donor feces for recurrent Clostridium difficile. New England Journal of Medicine, 368(5), 407–415. https://doi.org/10.1056/NEJMoa1205037CrossRefPubMed

126.

Wang, Y., Wiesnoski, D. H., Helmink, B. A., Gopalakrishnan, V., Choi, K., DuPont, H. L., Jiang, Z. D., Abu-Sbeih, H., Sanchez, C. A., Chang, C. C., Parra, E. R., Francisco-Cruz, A., Raju, G. S., Stroehlein, J. R., Campbell, M. T., Gao, J., Subudhi, S. K., Maru, D. M., Blando, J. M., Lazar, A. J., et al. (2018). Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis. Nature Medicine, 24(12), 1804–1808. https://doi.org/10.1038/s41591-018-0238-9CrossRefPubMedPubMedCentral

127.

Smibert, O. C., Guo, C. W., Khoo, C., Thursky, K. A., Sandhu, S., & Slavin, M. A. (2019). Microbiome transplantation and modulation of immune related adverse events. EClinicalMedicine, 8, 10–11. https://doi.org/10.1016/j.eclinm.2019.03.003CrossRefPubMedPubMedCentral

128.

Shaikh, F. Y., White, J. R., Gills, J. J., Hakozaki, T., Richard, C., Routy, B., Okuma, Y., Usyk, M., Pandey, A., Weber, J. S., Ahn, J., Lipson, E. J., Naidoo, J., Pardoll, D. M., & Sears, C. L. (2021). A uniform computational approach improved on existing pipelines to reveal microbiome biomarkers of nonresponse to immune checkpoint inhibitors. Clinical Cancer Research, 27(9), 2571–2583. https://doi.org/10.1158/1078-0432.Ccr-20-4834CrossRefPubMedPubMedCentral

129.

Betof Warner, A., Palmer, J. S., Shoushtari, A. N., Goldman, D. A., Panageas, K. S., Hayes, S. A., Bajwa, R., Momtaz, P., Callahan, M. K., Wolchok, J. D., Postow, M. A., & Chapman, P. B. (2020). Long-term outcomes and responses to retreatment in patients with melanoma treated with PD-1 blockade. Journal of Clinical Oncology, 38(15), 1655–1663. https://doi.org/10.1200/jco.19.01464CrossRefPubMedPubMedCentral

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The gut microbiome, immune check point inhibition and immune-related adverse events in non-small cell lung cancer

Abstract

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2022

Mechanistic insights into the interplays between neutrophils and other immune cells in cancer development and progression

Treatment against glucose-dependent cancers through metabolic PFKFB3 targeting of glycolytic flux

Inflammatory bowel disease and carcinogenesis

Connecting the Human Microbiome and Pancreatic Cancer

Nanotechnology-aided advancement in the combating of cancer metastasis

The paradoxical role of inositol in cancer: a consequence of the metabolic state of a tumor

Keynote webinar | Spotlight on antibody–drug conjugates in cancer