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Associations of influenza vaccination with severity of immune-related adverse events in patients with advanced thoracic cancers on immune checkpoint inhibitors

Emily Pei-Ying Lin, Li-Ching Huang, Jennifer Whisenant, Sally York, Travis Osterman, Jennifer Lewis, Wade Iams, Emily Skotte, Amanda Cass, Chih-Yuan Hsu, Yu Shyr, Leora Horn
ERJ Open Research 2022 8: 00684-2021; DOI: 10.1183/23120541.00684-2021
Emily Pei-Ying Lin
1Dept of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA
2Center for Quantitative Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
3Dept of Medical Research, Taipei Medical University Hospital, Taipei, Taiwan
4Division of Pulmonary Medicine, Dept of Internal Medicine, Taipei Medical University Hospital, Taipei, Taiwan
5Dept of Internal Medicine, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan
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  • For correspondence: emilypylin@tmu.edu.tw
Li-Ching Huang
1Dept of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA
2Center for Quantitative Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
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Jennifer Whisenant
6Division of Hemato-oncology, Dept of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
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Sally York
6Division of Hemato-oncology, Dept of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
7Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN, USA
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Travis Osterman
6Division of Hemato-oncology, Dept of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
7Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN, USA
8Dept of Biomedical Informatics, Vanderbilt University Medical Center, Nashville, TN, USA
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Jennifer Lewis
6Division of Hemato-oncology, Dept of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
7Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN, USA
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Wade Iams
6Division of Hemato-oncology, Dept of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
7Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN, USA
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Emily Skotte
6Division of Hemato-oncology, Dept of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
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Amanda Cass
6Division of Hemato-oncology, Dept of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
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  • ORCID record for Amanda Cass
Chih-Yuan Hsu
1Dept of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA
2Center for Quantitative Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
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Yu Shyr
1Dept of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA
2Center for Quantitative Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
7Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN, USA
9These authors contributed equally
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Leora Horn
6Division of Hemato-oncology, Dept of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
7Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN, USA
9These authors contributed equally
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Tables

  • Supplementary Materials
  • TABLE 1

    Demographic features of the study cohorts

    Before propensity score matchingAfter propensity score matching#
    nFV-positive (n=142)FV-negative (n=105)Combined (n=247)p-valuenFV-positive (n=105)FV-negative (n=105)Combined (n=210)p-value
    Race2470.9212100.448
     White129 (91)95 (90)224 (91)98 (93)95 (90)193 (92)
     Non-White13 (9)10 (10)23 (9)7 (7)10 (10)17 (8)
    Gender2470.3932100.889
     Male72 (51)59 (56)131 (53)60 (57)59 (56)119 (57)
     Female70 (49)46 (44)116 (47)45 (43)46 (44)91 (43)
    Age, years2470.5502100.537
     <6047 (33)31 (30)78 (32)27 (26)31 (30)58 (28)
     ≥6095 (67)74 (70)169 (68)78 (74)74 (70)152 (72)
    Smoking status2470.2192101
     Ever-smoker126 (89)98 (93)224 (91)98 (93)98 (93)196 (93)
     Never-smoker16 (11)7 (7)23 (9)7 (7)7 (7)14 (7)
    Cancer type2470.1262100.260
     NSCLC124 (87)86 (82)210 (85)89 (85)86 (82)175 (83)
     SCLC10 (7)16 (15)26 (11)9 (9)16 (15)25 (12)
     Mixed NSCLC/  SCLC3 (2)2 (2)5 (2)3 (3)2 (2)5 (2)
     Others5 (4)1 (1)6 (2)4 (4)1 (1)5 (2)
      Malignant mesothelioma4 (3)0 (0)4 (2)4 (4)0 (0)4 (2)
      Thymic cancer1 (1)1 (1)2 (1)0 (0)1 (1)1 (0)
    Stage2470.4792101
     III13 (9)7 (7)20 (8)7 (7)7 (7)14 (7)
     IV129 (91)98 (93)227 (92)98 (93)98 (93)196 (93)
    Trial patient2470.3262100.471
     Yes56 (39)35 (33)91 (37)40 (38)35 (33)75 (36)
     No86 (61)70 (67)156 (63)65 (62)70 (67)135 (64)
    ICI received¶2470.1632100.284
     PD-1 inhibitor111 (78)81 (77)192 (78)83 (79)81 (77)164 (78)
     PD-L1 inhibitor19 (13)11 (10)30 (12)10 (10)11 (10)21 (10)
     CTLA-4 inhibitor3 (2)0 (0)3 (1)3 (3)0 (0)3 (1)
     CTLA-4 combination9 (6)13 (12)22 (9)9 (9)13 (12)22 (10)
    Best ICI response2470.3962100.474
     PD48 (34)41 (39)89 (36)36 (34)41 (39)77 (37)
     Responses other than PD94 (66)64 (61)158 (64)69 (66)64 (61)133 (63)
    Comorbidities, n2340.9052100.719
     02 (2)1 (1)3 (1)3 (3)1 (1)4 (2)
     139 (30)29 (28)68 (29)33 (31)30 (29)63 (30)
     233 (25)30 (29)63 (27)28 (27)31 (30)59 (28)
     ≥357 (44)43 (42)100 (43)41 (39)43 (41)84 (40)
    Comorbidity
     Cardiovascular23485 (65)68 (66)153 (65)0.85621068 (65)69 (66)137 (65)0.885
     Pulmonary23453 (40)50 (49)103 (44)0.21621050 (48)50 (48)100 (48)1
     Metabolic23453 (40)47 (46)100 (43)0.42721043 (41)47 (45)90 (43)0.577
     Second primary cancers23434 (26)17 (17)51 (22)0.08221018 (17)17 (16)35 (17)0.853
     Autoimmune23425 (19)27 (26)52 (22)0.19321023 (22)28 (27)51 (24)0.421
     Nephrology/  urology23416 (12)15 (15)31 (13)0.59920411 (11)15 (15)26 (13)0.432
     Cerebrovascular23413 (10)11 (11)24 (10)0.8502048 (8)11 (11)19 (9)0.498
     Neurological2346 (5)8 (8)14 (6)0.3082044 (4)8 (8)12 (6)0.248
    Influenza prodromes2470.8302100.313
     Yes2 (1)3 (3)5 (2)1 (1)3 (3)4 (2)
     No140 (99)102 (97)242 (98)104 (99)102 (97)206 (98)
    Influenza-related hospitalisation2470.4192100.316
     Yes1 (1)1 (1)2 (1)0 (0)1 (1)1 (0)
     No141 (99)104 (99)245 (99)105 (100)104 (99)209 (100)

    Data are presented as n (%), unless otherwise stated. FV: influenza vaccination; NSCLC: nonsmall cell lung cancer; SCLC: small cell lung cancer; ICI: immune checkpoint inhibitor; PD-1: programmed cell death 1; PD-L1: PD-1 ligand 1; CTLA-4: cytotoxic T-lymphocyte antigen 4; PD: progressive disease. #: one of the five propensity score matching model runs after multiple imputations (numbers change very slightly among five runs); ¶: PD-1 inhibitors include nivolumab and pembrolizumab; PD-L1 inhibitors include atezolizumab and durvalumab; CTLA-4 inhibitor here indicates ipilimumab; CTLA-4 combinations include ipilimumab plus nivolumab and tremelimumab plus durvalumab.

    • TABLE 2

      Immune-related adverse events (IRAEs) in the study cohorts

      Before propensity score matchingAfter propensity score matching#
      nFV-positive (n=142)FV-negative (n=105)Combined (n=247)p-valuenFV-positive (n=105)FV-negative (n=105)Combined (n=210)p-value
      IRAEs2470.4192100.49
       Yes67 (47)55 (52)122 (49)50 (48)55 (52)105 (50)
       No75 (53)50 (48)125 (51)55 (52)50 (48)105 (50)
      IRAE severity grading2470.004*2100.004*
       Grade 51 (1)0 (0)1 (0)1 (1)0 (0)1 (0)
       Grade 42 (1)1 (1)3 (1)1 (1)1 (1)2 (1)
       Grade 326 (18)38 (36)64 (26)18 (17)38 (36)56 (27)
       Grade 227 (19)16 (15)43 (17)22 (21)16 (15)38 (18)
       Grade 111 (8)0 (0)11 (4)8 (8)0 (0)8 (4)
       No IRAEs75 (53)50 (48)125 (51)55 (52)50 (48)105 (50)
      IRAE severity group2470.006*2100.005*
       Grade 3–529 (20)39 (37)68 (28)20 (19)39 (37)59 (28)
       Grade 1–238 (27)16 (15)54 (22)30 (29)16 (15)46 (22)
       No IRAEs75 (53)50 (48)125 (50)55 (52)50 (48)105 (50)
      IRAE type
       Endocrinopathy24727¶ (19)16+ (15)43 (17)0.44021022§ (21)16ƒ (15)38 (18)0.282
        Hypothyroidism21 (15)12 (11)33 (13)17 (16)12 (11)29 (28)
        Adrenal insufficiency8 (6)4 (4)12 (5)6 (6)4 (4)10 (10)
        Hypophysitis1 (1)1 (1)2 (1)1 (1)1 (1)2 (2)
       Pneumonitis24717 (12)18 (17)35 (14)0.25021012 (11)18 (17)30 (14)0.237
       Dermatological24717 (12)7 (7)24 (10)0.16021014 (13)7 (7)21 (10)0.107
       Hepatitis/colitis24716 (11)8 (8)24 (10)0.3402108 (8)8 (8)16 (8)1
        Hepatitis9 (6)6 (6)15 (6)5 (5)6 (6)11 (5)
        Colitis7 (5)2 (2)9 (4)3 (3)2 (2)5 (2)
       Neuromuscular2475 (3)10 (10)15 (6)0.0512104 (4)10 (10)14 (7)0.097
       Severe fatigue2474 (3)4 (4)8 (3)0.6602103 (3)4 (4)7 (3)0.701
       Myocarditis2471 (1)4 (4)5 (2)0.0872101 (1)4 (4)5 (2)0.174
       Haematological2470 (0)2 (2)2 (2)12100 (0)2 (2)2 (1)0.155
       Nephritis2471 (1)0 (0)1 (0)0.3902101 (1)0 (0)1 (0)0.316
      Immunosuppressive agents for IRAEs2470.005*2100.004*
       Yes32 (23)41 (39)73 (30)22 (21)41 (39)63 (30)
       No110 (77)64 (61)174 (70)83 (79)64 (61)147 (70)
      ICI discontinuation due to IRAEs2470.018*2100.014*
       Yes25 (18)32 (30)57 (23)17 (16)32 (30)49 (23)
       No117 (82)73 (70)190 (77)88 (84)73 (70)161 (77)
      Grade 3–5 IRAEs##2470.004*2100.004*
       Yes29 (20)39 (37)68 (28)20 (19)39 (37)59 (28)
       No113 (80)66 (63)179 (72)85 (81)66 (63)151 (72)

      Data are presented as n (%), unless otherwise stated. FV: influenza vaccination; ICI: immune checkpoint inhibitor. #: one of the five propensity score matching models run after multiple imputations (the numbers varied very slightly among the five runs); ¶: three patients had both hypothyroidism and adrenal insufficiency; +: one patient had both hypothyroidism and adrenal insufficiency; §: two patients had both hypothyroidism and adrenal insufficiency; ƒ: one patient had both hypothyroidism and adrenal insufficiency; ##: denominator: cases with positive IRAE (annotated as IRAE=Yes in the table). *: p<0.05.

      • TABLE 3

        Seasonal distribution of immune-related adverse event (IRAE) occurrence

        Before propensity score matchingAfter propensity score matching#
        nFV-positive (n=67)FV-negative (n=55)Combined (n=122)p-valuenFV-positive (n=50)FV-negative (n=55)Combined (n=105)p-value
        Season of IRAEs1220.6201050.464
         Spring15 (22)9 (16)24 (20)12 (24)9 (16)21 (20)
         Summer17 (25)16 (29)33 (27)15 (30)16 (29)31 (30)
         Fall12 (18)14 (25)26 (21)7 (14)14 (25)21 (20)
         Winter23 (35)16 (30)39 (32)16 (32)16 (30)32 (30)
        Influenza season of IRAEs1220.7991050.382
         Fall/winter35 (52)30 (55)65 (53)23 (46)30 (55)53 (50)
         Spring/  summer32 (48)25 (45)57 (47)27 (54)25 (45)52 (50)

        Data are presented as n (%), unless otherwise stated. FV: influenza vaccination. #: one of the five propensity score matching models run after multiple imputations (the numbers varied very slightly among the five runs).

        • TABLE 4

          Associations between clinical features and immune-related adverse events (IRAEs) using ordinal logistic regression analysis: grade 3–5 IRAEs versus grade 1–2 IRAEs versus no IRAEs

          OR (90% CI)p-value
          FV: positive versus negative (reference)0.63 (0.40–0.99)0.046*
          Race: White versus non-White (reference)3.27 (1.13–9.47)0.034*
          Gender: male versus female (reference)0.93 (0.57–1.53)0.406
          Smoking status: ever versus never (reference)2.86 (0.97–8.42)0.055
          Age: <60 versus ≥60 years (reference)0.86 (0.49–1.52)0.335
          Trial: yes versus no (reference)1.23 (0.73–2.07)0.254
          ICI received:
           PD-L1 versus PD-1 (reference)2.36 (0.94–5.90)0.062
           CTLA-4/CTLA-4 combinations versus PD-1 (reference)2.06 (0.97–4.38)0.057

          FV: influenza vaccination; ICI: immune checkpoint inhibitor; PD-L1: PD-1 ligand 1; PD-1: programmed cell death 1; CTLA-4: cytotoxic T-lymphocyte antigen 4. Harrell's C-statistic=0.642. *: p<0.05.

          • TABLE 5

            Associations between clinical features and severe immune-related adverse events (IRAEs) using logistic regression analysis: grade 3–5 IRAEs versus grade 1–2 IRAEs plus no IRAEs#

            OR (90% CI)p-value
            FV: positive versus negative (reference)¶0.42 (0.24–0.73)0.005*
            Race: White versus non-White (reference)1.94 (0.60–6.25)0.175
            Gender: male versus female (reference)0.90 (0.51–1.58)0.378
            Smoking status: ever versus never (reference)4.34 (0.73–25.76)0.088
            Age: <60 versus ≥60 years (reference)0.99 (0.53–1.85)0.489
            Trial: yes versus no (reference)0.78 (0.41–1.46)0.257
            ICI received:
             PD-L1 versus PD-1 (reference)2.24 (0.87–5.79)0.081
             CTLA-4/CTLA-4 combinations versus PD-1 (reference)2.89 (1.22–6.87)0.022*

            FV: influenza vaccination; ICI: immune checkpoint inhibitor; PD-L1: PD-1 ligand 1; PD-1: programmed cell death 1; CTLA-4: cytotoxic T-lymphocyte antigen 4. #: comparisons made between patients with grade 3–5 IRAEs and patients with no IRAEs plus patients with grade 1–2 IRAEs; ¶: OR 0.45 by elastic-net logistic regression with α=0.5 and OR 0.61 by Bayesian logistic regression with horseshoe prior. Harrell's C-statistic=0.695. *: p<0.05.

            • TABLE 6

              Subset analysis for the associations between clinical features and immune-related adverse events (IRAEs): grade 3–5 IRAEs versus no IRAEs

              OR (90% CI)p-value
              FV: positive versus negative (reference)0.46 (0.26–0.84)0.016*
              Race: White versus non-White (reference)2.70 (0.79–9.25)0.092
              Gender: male versus female (reference)0.89 (0.48–1.67)0.382
              Smoking status: ever versus never (reference)4.97 (0.82–30.18)0.072
              Age: <60 versus ≥60 years (reference)0.86 (0.43–1.72)0.357
              Trial: yes versus no (reference)0.94 (0.48–1.85)0.439
              ICI received:
               PD-L1 versus PD-1 (reference)2.80 (0.91–8.61)0.065
               CTLA-4/CTLA-4 combinations versus PD-1 (reference)2.95 (1.13–7.72)0.032*

              FV: influenza vaccination; ICI: immune checkpoint inhibitor; PD-L1: PD-1 ligand 1; PD-1: programmed cell death 1; CTLA-4: cytotoxic T-lymphocyte antigen 4. Harrell's C-statistic=0.691. *: p<0.05.

              • TABLE 7

                Associations between clinical features and survival (progression-free survival (PFS) and overall survival (OS))

                PFSOS
                HR (90% CI)p-valueHR (90% CI)p-value
                FV: positive versus negative (reference)0.96 (0.73–1.26)0.3951.06 (0.79–1.43)0.371
                Race: White versus non-White (reference)0.70 (0.45–1.11)0.1001.03 (0.59–1.80)0.465
                Gender: male versus female (reference)0.81 (0.62–1.05)0.0910.97 (0.72–1.30)0.427
                Smoking status: ever versus never (reference)0.80 (0.48–1.33)0.2351.14 (0.61–2.15)0.363
                Age: <60 versus ≥60 years (reference)1.19 (0.88–1.60)0.1760.96 (0.68–1.37)0.428
                Trial: yes versus no (reference)0.71 (0.53–0.95)0.026*0.60 (0.43–0.83)0.005*
                ICI received:
                 PD-L1 versus PD-1 (reference)0.60 (0.34–1.07)0.0740.56 (0.28–1.12)0.083
                 CTLA-4/CTLA-4 combinations versus PD-1 (reference)1.17 (0.77–1.78)0.2641.26 (0.80–1.99)0.202

                FV: influenza vaccination; ICI: immune checkpoint inhibitor; PD-L1: PD-1 ligand 1; PD-1: programmed cell death 1; CTLA-4: cytotoxic T-lymphocyte antigen 4. Harrell's C-statistic for PFS=0.541 and for OS=0.542.

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                Associations of influenza vaccination with severity of immune-related adverse events in patients with advanced thoracic cancers on immune checkpoint inhibitors
                Emily Pei-Ying Lin, Li-Ching Huang, Jennifer Whisenant, Sally York, Travis Osterman, Jennifer Lewis, Wade Iams, Emily Skotte, Amanda Cass, Chih-Yuan Hsu, Yu Shyr, Leora Horn
                ERJ Open Research Oct 2022, 8 (4) 00684-2021; DOI: 10.1183/23120541.00684-2021

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                Associations of influenza vaccination with severity of immune-related adverse events in patients with advanced thoracic cancers on immune checkpoint inhibitors
                Emily Pei-Ying Lin, Li-Ching Huang, Jennifer Whisenant, Sally York, Travis Osterman, Jennifer Lewis, Wade Iams, Emily Skotte, Amanda Cass, Chih-Yuan Hsu, Yu Shyr, Leora Horn
                ERJ Open Research Oct 2022, 8 (4) 00684-2021; DOI: 10.1183/23120541.00684-2021
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