1. Epidemiology and Global Health

Clinical characteristics, racial inequities, and outcomes in patients with breast cancer and COVID-19: A COVID-19 and cancer consortium (CCC19) cohort study

  1. Gayathri Nagaraj  Is a corresponding author
  2. Shaveta Vinayak
  3. Ali Raza Khaki
  4. Tianyi Sun
  5. Nicole M Kuderer
  6. David M Aboulafia
  7. Jared D Acoba
  8. Joy Awosika
  9. Ziad Bakouny
  10. Nicole B Balmaceda
  11. Ting Bao
  12. Babar Bashir
  13. Stephanie Berg
  14. Mehmet A Bilen
  15. Poorva Bindal
  16. Sibel Blau
  17. Brianne E Bodin
  18. Hala T Borno
  19. Cecilia Castellano
  20. Horyun Choi
  21. John Deeken
  22. Aakash Desai
  23. Natasha Edwin
  24. Lawrence E Feldman
  25. Daniel B Flora
  26. Christopher R Friese
  27. Matthew D Galsky
  28. Cyndi J Gonzalez
  29. Petros Grivas
  30. Shilpa Gupta
  31. Marcy Haynam
  32. Hannah Heilman
  33. Dawn L Hershman
  34. Clara Hwang
  35. Chinmay Jani
  36. Sachin R Jhawar
  37. Monika Joshi
  38. Virginia Kaklamani
  39. Elizabeth J Klein
  40. Natalie Knox
  41. Vadim S Koshkin
  42. Amit A Kulkarni
  43. Daniel H Kwon
  44. Chris Labaki
  45. Philip E Lammers
  46. Kate I Lathrop
  47. Mark A Lewis
  48. Xuanyi Li
  49. Gilbert de Lima Lopes
  50. Gary H Lyman
  51. Della F Makower
  52. Abdul-Hai Mansoor
  53. Merry-Jennifer Markham
  54. Sandeep H Mashru
  55. Rana R McKay
  56. Ian Messing
  57. Vasil Mico
  58. Rajani Nadkarni
  59. Swathi Namburi
  60. Ryan H Nguyen
  61. Taylor Kristian Nonato
  62. Tracey Lynn O'Connor
  63. Orestis A Panagiotou
  64. Kyu Park
  65. Jaymin M Patel
  66. Kanishka GopikaBimal Patel
  67. Jeffrey Peppercorn
  68. Hyma Polimera
  69. Matthew Puc
  70. Yuan James Rao
  71. Pedram Razavi
  72. Sonya A Reid
  73. Jonathan W Riess
  74. Donna R Rivera
  75. Mark Robson
  76. Suzanne J Rose
  77. Atlantis D Russ
  78. Lidia Schapira
  79. Pankil K Shah
  80. M Kelly Shanahan
  81. Lauren C Shapiro
  82. Melissa Smits
  83. Daniel G Stover
  84. Mitrianna Streckfuss
  85. Lisa Tachiki
  86. Michael A Thompson
  87. Sara M Tolaney
  88. Lisa B Weissmann
  89. Grace Wilson
  90. Michael T Wotman
  91. Elizabeth M Wulff-Burchfield
  92. Sanjay Mishra
  93. Benjamin French
  94. Jeremy L Warner
  95. Maryam B Lustberg
  96. Melissa K Accordino
  97. Dimpy P Shah  Is a corresponding author
  98. On behalf of the COVID-19 and Cancer Consortium
  1. Loma Linda University Cancer Center, United States
  2. Fred Hutchinson Cancer Research Center, United States
  3. University of Washington, United States
  4. Seattle Cancer Care Alliance, United States
  5. Stanford University, United States
  6. Vanderbilt University Medical Center, United States
  7. Advanced Cancer Research Group, United States
  8. Virginia Mason Cancer Institute, United States
  9. University of Hawaii Cancer Center, United States
  10. University of Cincinnati Cancer Center, United States
  11. Dana-Farber Cancer Institute, United States
  12. The University of Kansas Cancer Center, United States
  13. Memorial Sloan Kettering Cancer Center, United States
  14. Sidney Kimmel Comprehensive Cancer Center, Thomas Jefferson University, United States
  15. Loyola University Medical Center, United States
  16. Winship Cancer Institute, Emory University, United States
  17. Beth Israel Deaconess Medical Center, United States
  18. Northwest Medical Specialties, United States
  19. Herbert Irving Comprehensive Cancer Center, Columbia University, United States
  20. Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, United States
  21. Inova Schar Cancer Institute, United States
  22. Mayo Clinic, United States
  23. ThedaCare Cancer Care, United States
  24. University of Illinois Hospital & Health Sciences System, United States
  25. St. Elizabeth Healthcare, United States
  26. Rogel Cancer Center, University of Michigan-Ann Arbor, United States
  27. Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, United States
  28. Cleveland Clinic, United States
  29. The Ohio State University Comprehensive Cancer Center, United States
  30. Henry Ford Cancer Institute, Henry Ford Hospital, United States
  31. Mount Auburn Hospital, United States
  32. Penn State Health St Joseph Cancer Center, United States
  33. Mays Cancer Center, The University of Texas Health San Antonio MD Anderson Cancer Center, United States
  34. Lifespan Cancer Institute, Brown University, United States
  35. Stritch School of Medicine, Loyola University, United States
  36. Masonic Cancer Center, University of Minnesota, United States
  37. Baptist Cancer Center, United States
  38. Intermountain Healthcare, United States
  39. Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, United States
  40. Montefiore Medical Center, Albert Einstein College of Medicine, United States
  41. Kaiser Permanente Northwest, United States
  42. Division of Hematology and Oncology, University of Florida Health Cancer Center, United States
  43. Moores Cancer Center, University of California, San Diego, United States
  44. Division of Radiation Oncology, George Washington University, United States
  45. Hartford HealthCare Cancer Institute, United States
  46. Roswell Park Comprehensive Cancer Center, United States
  47. UC Davis Comprehensive Cancer Center, University of California, Davis, United States
  48. Massachusetts General Hospital, United States
  49. Virtua Health, United States
  50. Division of Cancer Control and Population Sciences, National Cancer Institute, United States
  51. Carl & Dorothy Bennett Cancer Center, Stamford Hospital, United States
  52. METAvivor, United States
  53. Aurora Cancer Care, Advocate Aurora Health, United States
  54. Yale Cancer Center, Yale University School of Medicine, United States
https://doi.org/10.7554/eLife.82618
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Cite this article
  1. Gayathri Nagaraj
  2. Shaveta Vinayak
  3. Ali Raza Khaki
  4. Tianyi Sun
  5. Nicole M Kuderer
  6. David M Aboulafia
  7. Jared D Acoba
  8. Joy Awosika
  9. Ziad Bakouny
  10. Nicole B Balmaceda
  11. Ting Bao
  12. Babar Bashir
  13. Stephanie Berg
  14. Mehmet A Bilen
  15. Poorva Bindal
  16. Sibel Blau
  17. Brianne E Bodin
  18. Hala T Borno
  19. Cecilia Castellano
  20. Horyun Choi
  21. John Deeken
  22. Aakash Desai
  23. Natasha Edwin
  24. Lawrence E Feldman
  25. Daniel B Flora
  26. Christopher R Friese
  27. Matthew D Galsky
  28. Cyndi J Gonzalez
  29. Petros Grivas
  30. Shilpa Gupta
  31. Marcy Haynam
  32. Hannah Heilman
  33. Dawn L Hershman
  34. Clara Hwang
  35. Chinmay Jani
  36. Sachin R Jhawar
  37. Monika Joshi
  38. Virginia Kaklamani
  39. Elizabeth J Klein
  40. Natalie Knox
  41. Vadim S Koshkin
  42. Amit A Kulkarni
  43. Daniel H Kwon
  44. Chris Labaki
  45. Philip E Lammers
  46. Kate I Lathrop
  47. Mark A Lewis
  48. Xuanyi Li
  49. Gilbert de Lima Lopes
  50. Gary H Lyman
  51. Della F Makower
  52. Abdul-Hai Mansoor
  53. Merry-Jennifer Markham
  54. Sandeep H Mashru
  55. Rana R McKay
  56. Ian Messing
  57. Vasil Mico
  58. Rajani Nadkarni
  59. Swathi Namburi
  60. Ryan H Nguyen
  61. Taylor Kristian Nonato
  62. Tracey Lynn O'Connor
  63. Orestis A Panagiotou
  64. Kyu Park
  65. Jaymin M Patel
  66. Kanishka GopikaBimal Patel
  67. Jeffrey Peppercorn
  68. Hyma Polimera
  69. Matthew Puc
  70. Yuan James Rao
  71. Pedram Razavi
  72. Sonya A Reid
  73. Jonathan W Riess
  74. Donna R Rivera
  75. Mark Robson
  76. Suzanne J Rose
  77. Atlantis D Russ
  78. Lidia Schapira
  79. Pankil K Shah
  80. M Kelly Shanahan
  81. Lauren C Shapiro
  82. Melissa Smits
  83. Daniel G Stover
  84. Mitrianna Streckfuss
  85. Lisa Tachiki
  86. Michael A Thompson
  87. Sara M Tolaney
  88. Lisa B Weissmann
  89. Grace Wilson
  90. Michael T Wotman
  91. Elizabeth M Wulff-Burchfield
  92. Sanjay Mishra
  93. Benjamin French
  94. Jeremy L Warner
  95. Maryam B Lustberg
  96. Melissa K Accordino
  97. Dimpy P Shah
  98. On behalf of the COVID-19 and Cancer Consortium
(2023)
Clinical characteristics, racial inequities, and outcomes in patients with breast cancer and COVID-19: A COVID-19 and cancer consortium (CCC19) cohort study
eLife 12:e82618.
https://doi.org/10.7554/eLife.82618
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  3. Download .RIS
2 figures, 15 tables and 1 additional file

Figures

Figure 1
Download asset Open asset
Consort flow diagram.

Descriptive flow chart of patients included in the study.

Appendix 4—figure 1
Download asset Open asset
Represents graphical methods used to verify the proportional odds assumptions.

Tables

Table 1
Baseline characteristics by race/ethnicity.






NHWBlackHispanicAAPIOthersAll
(n=736, 53%)(n=289, 21%)(n=235, 17%)(n=45, 3%)(n=78, 6%)(n=1383, 100%)
Median age, years* [IQR]64 (54–76)61 (52–69)53 (46–62)54 (43–73)62 (53–71)61 (51–72)
Median follow-up, days [IQR]90 (30–135)90 (30–180)90 (30–135)42 (21–90)70 (30–180)90 (30–135)
Smoking status
Never460 (62%)186 (64%)180 (77%)35 (78%)50 (64%)911 (66%)
Current or former261 (35%)95 (33%)53 (23%)8 (18%)25 (32%)442 (32%)
Missing/unknown15 (2%)8 (3%)2 (1%)2 (4%)3 (4%)30 (2%)
Obesity
No421 (57%)133 (46%)116 (49%)32 (71%)45 (58%)747 (54%)
Yes308 (42%)156 (54%)116 (49%)13 (29%)33 (42%)626 (45%)
Missing/unknown7 (1%)0 (0%)3 (1%)0 (0%)0 (0%)10 (1%)
Comorbidities†
Cardiovascular179 (24%)60 (21%)14 (6%)7 (16%)11 (14%)271 (20%)
Pulmonary125 (17%)65 (22%)33 (14%)<5 (<11%)7 (9%)234 (17%)
Renal disease66 (9%)31 (11%)13 (6%)<5 (<11%)<5 (<6%)115 (8%)
Diabetes mellitus127 (17%)98 (34%)51 (22%)10 (22%)20 (26%)306 (22%)
Missing/unknown9 (1%)1 (<1%)5 (2%)0 (0%)0 (0%)15 (1%)
ECOG performance status
0314 (43%)130 (45%)123 (52%)18 (40%)32 (41%)617 (45%)
1135 (18%)72 (25%)48 (20%)10 (22%)16 (21%)281 (20%)
2+69 (9%)33 (11%)15 (6%)5 (11%)5 (6%)127 (9%)
Unknown218 (30%)53 (18%)49 (21%)12 (27%)25 (32%)357 (26%)
Missing0 (0%)1 (<1%)0 (0%)0 (0%)0 (0%)1 (<1%)
Region
Northeast247 (34%)101 (35%)106 (45%)12 (27%)26 (33%)492 (36%)
Midwest239 (32%)110 (38%)23 (10%)8 (18%)12 (15%)392 (28%)
South116 (16%)58 (20%)27 (11%)X*14 (18%)218 (16%)
West128 (17%)16 (6%)77 (33%)22 (49%)24 (31%)267 (19%)
Undesignated6 (1%)4 (1%)2 (1%)3 (7%)*2 (3%)14 (1%)
Month/year of COVID-19 diagnosis
Jan-Apr 2020140 (19%)74 (26%)41 (17%)8 (18%)20 (26%)283 (20%)
May-Aug 2020279 (38%)141 (49%)101 (43%)24 (53%)30 (38%)575 (42%)
Sept-Dec 2020197 (27%)42 (15%)50 (21%)5 (11%)16 (21%)310 (22%)
Jan-Jun 2021118 (16%)32 (11%)41 (17%)7 (16%)12 (15%)210 (15%)
Missing/unknown2 (<1%)0 (0%)2 (1%)1 (2%)0 (0%)5 (<1%)
Area of patient residence
Urban193 (26%)136 (47%)124 (53%)13 (29%)30 (38%)496 (36%)
Suburban315 (43%)77 (27%)65 (28%)17 (38%)31 (40%)505 (37%)
Rural81 (11%)7 (2%)9 (4%)X*0 (0%)98 (7%)
Missing/unknown147 (20%)69 (24%)37 (16%)15 (33%)*17 (22%)284 (21%)
Treatment center characteristics
Academic medical center123 (17%)102 (35%)43 (18%)7 (16%)11 (14%)286 (21%)
Community practice238 (32%)51 (18%)44 (19%)X*23 (29%)359 (26%)
Tertiary care center375 (51%)136 (47%)147 (63%)35 (78%)44 (56%)737 (53%)
Missing/unknown0 (0%)0 (0%)1 (<1%)3 (7%)*0 (0%)1 (<1%)
Receptor status
HR+/HER2-419 (57%)135 (47%)102 (43%)22 (49%)43 (55%)721 (52%)
HR+/HER2+102 (14%)35 (12%)43 (18%)7 (16%)9 (12%)196 (14%)
HR-/HER2+46 (6%)28 (10%)32 (14%)X*X*111 (8%)
Triple negative57 (8%)54 (19%)35 (15%)5 (11%)7 (9%)158 (11%)
Missing/unknown112 (15%)37 (13%)23 (10%)11 (24%)19 (24%)*197 (14%)
Cancer status
Remission/NED, >5 years247 (34%)76 (26%)23 (10%)9 (20%)20 (26%)375 (27%)
Remission/NED, <5 years234 (32%)100 (35%)77 (33%)11 (24%)26 (33%)448 (32%)
Active and responding68 (9%)35 (12%)56 (24%)X*11 (14%)173 (13%)
Active and stable91 (12%)28 (10%)35 (15%)10 (22%)5 (6%)169 (12%)
Active and progressing41 (6%)27 (9%)20 (9%)6 (13%)X*97 (7%)
Unknown48 (7%)19 (7%)22 (9%)6 (13%)*15 (19%)*104 (8%)
Missing7 (1%)4 (1%)2 (1%)3 (7%)1 (1%)17 (1%)
Timing of anti-cancer therapy
Never/after COVID-1924 (3%)10 (3%)7 (3%)X*7 (9%)50 (4%)
0–4 weeks364 (49%)135 (47%)158 (67%)25 (56%)39 (50%)721 (52%)
1–3 months26 (4%)20 (7%)19 (8%)0 (0%)X*69 (5%)
>3 months303 (41%)118 (41%)45 (19%)18 (40%)24 (31%)508 (37%)
Missing/unknown19 (3%)6 (2%)6 (3%)2 (4%)*8 (10%)*35 (3%)
Modality of active anti-cancer therapy‡, §
None333 (45%)127 (44%)53 (23%)20 (44%)30 (38%)563 (41%)
Chemotherapy117 (16%)68 (24%)88 (37%)11 (24%)14 (18%)298 (22%)
Targeted therapy112 (15%)38 (13%)59 (25%)8 (18%)11 (14%)228 (16%)
Anti-HER2 therapy60 (8%)17 (6%)36 (15%)<5 (<11%)<5 (<6%)123 (9%)
CDK4/6 inhibitor33 (4%)12 (4%)14 (6%)<5 (<11%)<5 (<6%)65 (5%)
Other14 (2%)5 (2%)<5 (<2%)<5 (<11%)0 (0%)24 (2%)
Endocrine therapy283 (38%)86 (30%)91 (39%)15 (33%)26 (33%)501 (36%)
Immunotherapy12 (2%)8 (3%)<5 (<2%)<5 (<11%)<5 (<6%)28 (2%)
Local (surgery/radiation)80 (11%)37 (13%)41 (17%)<5 (<11%)9 (12%)172 (12%)
Other13 (2%)3 (1%)2 (1%)0 (0%)0 (0%)18 (1%)
Missing/unknown12 (2%)7 (2%)5 (2%)0 (0%)5 (6%)29 (2%)
Severity of COVID-19
Mild535 (73%)177 (61%)173 (74%)28 (62%)50 (64%)963 (70%)
Moderate174 (24%)97 (34%)56 (24%)14 (31%)21 (27%)362 (26%)
Severe25 (3%)15 (5%)6 (3%)X*7 (9%)56 (4%)
Missing/unknown2 (<1%)0 (0%)0 (0%)3 (7%)*0 (0%)2 (<1%)

  1. Variable categories with one to five cases are masked by replacing with N < 5 according to CCC19 policy.

  2. *

    Cells combined to mask N<5 according to CCC19 low count policy.

  3. †

    Age was truncated at 90.

  4. ‡

    Percentages could sum to >100% because categories are not mutually exclusive.

  5. §

    Within 3 months of COVID-19 diagnosis.

  6. Therapies other than anti-Her2 therapy or CDK4/6 inhibitor.

Table 2
Outcomes, clinical complications, and COVID-19 interventions.
NHWBlackHispanicAAPIOtherAll
n** (%)n** (%)n** (%)n** (%)n** (%)n** (%)
Outcomes
Total all-cause mortality*60 (8)38 (13)12 (5)<5(<11)9 (12)123 (9)
30-day all-cause mortality†40 (5)29 (10)8 (3)<5 (<11)8 (10)89 (6)
Received mechanical ventilation*24 (3)26 (9)11 (5)<5 (<11)<5 (<6)69 (5)
Admitted to an intensive care unit*45 (6)31 (11)18 (8)7 (16)10 (13)111 (8)
Admitted to the hospital*245 (33)137 (47)77 (33)20 (44)33 (42)512 (37)
Clinical complications
Any cardiovascular complication‡82 (11)50 (17)30 (13)6 (13)18 (23)186 (14)
Any pulmonary complication§170 (23)88 (31)43 (18)12 (27)23 (30)336 (24)
Any gastrointestinal complication12 (2)7 (2)<5 (<2)<5 (<11)<5 (<7)26 (2)
Acute kidney injury41 (6)46 (16)11 (5)5 (11)10 (13)113 (8)
Multisystem organ failure10 (1)12 (4)<5 (<2)<5 (<11)<5 (<7)29 (2)
Superimposed infection62 (9)42 (15)14 (6)7 (16)<5 (<7)129 (10)
Sepsis43 (6)24 (8)15 (6)7 (16)12 (16)101 (7)
Any bleeding15 (2)7 (2)<5 (<2)<5 (<11)<5 (<7)29 (2)
Interventions
Remdesivir68 (10)20 (7)15 (7)8 (18)5 (7)116 (9)
Hydroxychloroquine60 (9)41 (15)14 (6)<5 (<11)11 (15)129 (10)
Systemic corticosteroids107 (15)50 (18)31 (14)8 (18)13 (18)209 (16)
Other112 (16)53 (19)36 (16)11 (25)12 (17)224 (17)
Supplemental oxygen173 (24)87 (31)43 (19)14 (31)24 (31)341 (25)

  1. Variable categories with one to five cases are masked by replacing with N<5 according to CCC19 policy.

  2. *

    Included in primary outcome.

  3. †

    Secondary outcome.

  4. ‡

    Cardiovascular complication includes hypotension, myocardial infarction, other cardiac ischemia, atrial fibrillation, ventricular fibrillation, other cardiac arrhythmia, cardiomyopathy, congestive heart failure, pulmonary embolism (PE), deep vein thrombosis (DVT), stroke, thrombosis NOS complication.

  5. §

    Pulmonary complication includes respiratory failure, pneumonitis, pneumonia, acute respiratory distress syndrome (ARDS), PE, pleural effusion, empyema.

  6. Gastrointestinal complication includes acute hepatic injury, ascites, bowel obstruction, bowel perforation, ileus, peritonitis.

  7. **

    N based on number of patients with non-missing data.

Table 3
Systemic treatments received within 3 months prior to COVID-19 diagnosis.
N (%)
Total679 (100%)
Endocrine therapy alone336 (49.5)
CDK4/6 inhibitor ± endocrine therapy63 (9)
Other targeted therapy ± endocrine therapy10 (1.5)
Anti-HER2 therapy ± endocrine therapy78 (11.5)
Anti-HER2 therapy + chemotherapy48 (7)
Single agent chemotherapy ± endocrine therapy55 (8)
Combination chemotherapy ± endocrine therapy60 (9)
Immunotherapy ± chemotherapy19 (3)
Other combination therapies10 (1.5)
Table 4
Adjusted associations of baseline characteristics with COVID-19 severity outcome.
COVID-19 severity
OR (95% CI)
Age (per decade)1.48 (1.32–1.67)
Race (Ref: non-Hispanic White)*
Non-Hispanic Black1.74 (1.24–2.45)
Hispanic1.38 (0.93–2.05)
Non-Hispanic AAPI3.40 (1.70–6.79)
Other2.97 (1.71–5.17)
Obesity (Ref: No)1.20 (0.92–1.57)
Cardiovascular comorbidity (Ref: No)2.26 (1.63–3.15)
Pulmonary comorbidity (Ref: No)1.65 (1.20–2.29)
Renal disease (Ref: No)1.34 (0.86–2.07)
Diabetes mellitus (Ref: No)2.25 (1.66–3.04)
ECOG performance status (Ref: 0)
11.74 (1.22–2.48)
2+7.78 (4.83–12.5)
Unknown2.26 (1.61–3.19)
Cancer status (Ref: Remission/NED, >5 years)
Remission or NED, <5 years0.91 (0.63–1.33)
Active and responding1.07 (0.63–1.83)
Active and stable1.37 (0.82–2.28)
Active and progressing12.5 (6.89–22.6)
Unknown1.79 (0.96–3.34)
Chemotherapy (Ref: No)1.37 (0.91–2.06)
Anti-HER2 therapy (Ref: No)1.13 (0.67–1.92)
CDK 4/6 inhibitor (Ref: No)1.21 (0.60–2.42)
Other targeted therapies† (Ref: No)1.78 (0.69–4.59)
Endocrine therapy (Ref: No)1.00 (0.73–1.37)
Locoregional therapy (Ref: No)1.36 (0.88–2.10)
Never received cancer treatment (Ref: >3 month)0.65 (0.28–1.49)
Month/year of COVID-19 diagnosis (Ref: Jan-Apr 2020)
May-Aug 20200.57 (0.41–0.81)
Sept-Dec 20200.45 (0.30–0.68)
Jan-Jun 20210.57 (0.36–0.89)
Region (Ref: Northeast)
Midwest0.76 (0.54–1.05)
South0.76 (0.51–1.13)
West0.43 (0.29–0.65)
  1. *

    Odds ratios greater than 1 indicate higher odds of composite outcome. The p value for evaluating the null hypothesis of equality in odds ratios across race (4 degrees of freedom) was <0.001.

  2. †

    Therapies other than CDK4/6 inhibitor or anti-HER2 therapy. All variance inflation factors are <1.8 for the model.

Appendix 3—table 1
Primary outcome.
Outcome descriptionOutcome variable nameOutcome values
Custom ordinal outcome with death at any timeder_ordinal_v1a0=not hospitalized; 1=hospitalized; 2=ICU; 3=mechanical ventilation; 4=death at any time
Follow-up in days, with some estimation for intervalsder_days_fuInteger (days)
Appendix 3—table 2
Secondary outcome.
Outcome descriptionOutcome variable nameOutcome valuesAdditional Details
Derived dead/alive variableder_deadbinary0=No; 1=Yes; 99=Unknown
Derived variable indicating whether patient has died within 30 days of COVID-19 diagnosis (default = No)der_dead300=No; 1=Yes; 99=Unknown
Derived variable indicating whether patients required mechanical ventilationder_mv0=No; 1=Yes; 99=Unknown
Derived variable indicating time in ICUder_ICU0=No; 1=Yes; 99=Unknown
Derived hospitalized/not hospitalized variableder_hosp0=No; 1=Yes; 99=Unknown
Derived cardiovascular complication variable (see additional details)der_CV_event_v2 (der_any_CV is the variable name in R script)0=No; 1=Yes; 99=UnknownDerived with the following derived variables: der_hotn_comp, der_MI_comp, der_card_isch_comp, der_AFib_comp, der_VF_comp, der_arry_oth_comp, der_CMY_comp, der_CHF_comp, der_PE_comp, der_DVT_comp, der_stroke_comp, der_thrombosis_NOS_comp
Coded as 1 if any of these variables is 1; coded as 0 if all these variables are 0; coded as 99 if any of variables is 99 and der_CV_event_v2 is missing; otherwise, NA
For all listed variable here:
0=No, 1=Yes, 99=Unknown
Derived pulmonary complication variable (see additional details)der_pulm_event (der_any_Pulm is the variable name in R script)0=No; 1=Yes; 99=UnknownDerived with the following derived variables: der_resp_failure_comp, der_pneumonitis_comp, der_pneumonia_comp, der_ARDS_comp, der_PE_comp, der_pleural_eff_comp, der_empyema_comp
Coded as 1 if any of these variables is 1; coded as 0 if all these variables are 0; coded as 99 if any of variables is 99 and der_pulm_event is missing; otherwise, NA
For all listed variable here:
0=No, 1=Yes, 99=Unknown
Derived gastrointestinal complication variable (see additional details)der_GI_event
(der_any_Gast is the variable name in R script)		0=No; 1=Yes; 99=UnknownDerived with the following derived variables: der_AHI_comp, der_ascites_comp, der_BO_comp, der_bowelPerf_comp, der_ileus_comp, der_peritonitis_comp
Coded as 1 if any of these variables is 1; coded as 0 if all these variables are 0; coded as 99 if any of variables is 99 and der_GI_event is missing; otherwise, NA
For all listed variable here:
0=No, 1=Yes, 99=Unknown
Acute kidney injury (checkbox only)der_AKI_comp0=No; 1=Yes; 99=Unknown
Multisystem organ failureder_MOF_comp0=No; 1=Yes; 99=Unknown
Any co-infection within ±2 weeks of COVID-19 dxder_coinfection_any0=No; 1=Yes; 99=Unknown
Sepsisder_sepsis_comp0=No; 1=Yes; 99=Unknown
Bleedingder_bleeding_comp0=No; 1=Yes; 99=Unknown
DIC (without modifier of definite/probable/possible)der_DIC_comp0=No; 1=Yes; 99=Unknown
Remdesivir as treatment for COVID-19 everder_rem0=No; 1=Yes; 99=Unknown
Hydroxychloroquine as COVID-19 treatment everder_hcq0=No; 1=Yes; 99=Unknown
Steroids as COVID-19 treatment everder_steroids_c190=No; 1=Yes; 99=Unknown
COVID-19 treatments other than HCQ, steroids, remdesivirder_other_tx_c19_v20=No; 1=Yes; 99=Unknown
Indicates whether patient has ever had supplemental o2der_o2_ever0=No; 1=Yes; 99=Unknown
Appendix 3—table 3
Covariate description.
Covariate descriptionVariable nameCovariate valuesAdditional details
Race/ethnicity including Asiander_race_v2Hispanic; Non-Hispanic AAPI; Non-Hispanic Black; Non-Hispanic White; Other
Age with imputation for categoricalsder_age_truncYears (continuous 18–89; patients noted to be greater than 89 are set to be age = 90)
Insurance typeder_insuranceMedicaid alone; Medicare alone; Medicare/Medicaid ± other; Other government ± other; Private ± other; Uninsured; Unknown
Derived variable for smoking status collapsing the current/former smoker variablesder_smoking2Never; Current or Former; Unknown
Binary obesity (BMI ≥ 30 or checkbox checked) indicatorder_obesity0=No; 1=Yes; 99=Unknown
Cardiovascular comorbidity (CAD, CHF, Afib, arrhythmia NOS, PVD, CVA, cardiac disease NOS)der_card0=No; 1=Yes; 99=Unknown
Derived variable indicating whether patient has pulmonary comorbiditiesder_pulm0=No; 1=Yes; 99=Unknown
Renal comorbiditiesder_renal0=No; 1=Yes; 99=Unknown
Derived variable indicating whether patient has diabetes mellitusder_dm20=No; 1=Yes; 99=Unknown
Performance statusder_ecogcat2ECOG 0, 1, or 2+
Breast biomarkers combined variableder_breast_biomarkers1=ER + ; 2=ER + /HER2+; 3=HER2+; 4=triple negative; 99=Unknown
Derived variable indicating cancer status
(splits remission/NED by cancer timing)		der_cancer_status_v40 - Remission/NED, remote; 1 - Remission/NED, recent; 2 - Active, responding; 3 - Active, stable; 4 - Active, progressing; 99 - Unknown
Timing of cancer treatment relative to COVID-19, collapsedder_cancer_tx_timing_v20=more than 3 months; 1=0–4 weeks; 2=1–3 months (*); 88=never or after COVID-19 diagnosis; 99=unknown
No cancer treatment in the 3 months prior to COVID-19der_cancertr_none0=No; 1=Yes; 99=UnknownDerived with the following covariates: der_any_cyto, der_any_targeted, der_any_endo, der_any_immuno, der_any_local, der_any_other
Coded as 1 if all these variables are 0; coded as 0 if any of these variables is 1; coded as 99 if any of these variables is 99; otherwise, NA
Any cytotoxic cancer treatment in the 3 months prior to COVID-19der_any_cyto0=No; 1=Yes; 99=Unknown
Any targeted therapy in the 3 months prior to COVID-19der_any_targeted0=No; 1=Yes; 99=Unknown
Any targeted therapy includes an anti-HER2 therapy in the 3 months prior to COVID-19der_her2_3 m0=No; 1=YesDerived with der_her2, der_any_targeted.
Coded as 1 if der_any_targeted is 1 and der_her2 is 1
Coded as 0 if: a. der_any_targeted is 1 and der_her2 is 0
der_any_targeted is 1
Otherwise, NA der_her2:
0=No; 1=Yes
Any targeted therapy includes a CDK4/6 inhibitor therapy in the 3 months prior to COVID-19der_cdk46i_3 m0=No; 1=YesDerived with der_cdk46i, der_any_targeted.
Coded as 1 if der_any_targeted is 1 and der_cdk46i is 1
Coded as 0 if: a. der_any_targeted is 1 and der_cdk46i is 0
der_any_targeted is 1
Otherwise, NA der_cdk46i:
0=No; 1=Yes
Any other targeted therapy (not anti-HER2/CDK4/6 inhibitor) in the 3 months prior to COVID-19der_other_3 m0=No; 1=YesDerived with der_targeted_not_her2_cdk46i, der_any_targeted.
Coded as 1 if der_any_targeted is 1 and der_targeted_not_her2_cdk46i is 1
Coded as 0 if: a. der_any_targeted is 1 and der_targeted_not_her2_cdk46i is 0
der_any_targeted is 1
Otherwise, NA der_targeted_not_her2_cdk46i:
0=No; 1=Yes
Any endocrine therapy in the 3 months prior to COVID-19der_any_endo0=No; 1=Yes; 99=Unknown
Any immunotherapy in the 3 months prior to COVID-19der_any_immuno0=No; 1=Yes; 99=Unknown
Any local therapy (surgery or RT) within 3 monthsder_any_local0=No; 1=Yes; 99=Unknown
Any other cancer therapy in the 3 months prior to COVID-19der_any_other0=No; 1=Yes; 99=Unknown
Region of patient residence with ex-US collapsedder_region_v2Non-US; Other; Undesignated US; US Midwest; US Northeast; US South; US West
Trimester and year of diagnosis, using the most recent side of the interval as anchorder_tri_rt_dxT1 2020; T2 2020; T3 2020; T1 2021
What type of area does the patient primarily reside in?urban_rural11, Urban (city) | 2, Suburban (town, suburbs) | 3, Rural (country) | 88, Other | 99, Unknown
The type of health care center providing the patient’s datader_site_typeAMC = academic medical center; CP = community practice; TCC = tertiary care center
Initial severity and course of illnessseverity_of_covid_19_v211, Mild (no hospitalization required) | 2, Moderate (hospitalization indicated) | 3, Severe (ICU admission indicated) | 99, Unknown
Derived treatment intentder_tr_intentUnknown Treatment; Not on Treatment; Palliative; Curative; Missing
Unknown Treatment and Missing were collapsed for analysis		Derived with der_anytx and treatment_intent:
Coded as ‘Unknown Treatment’ if der_anytx is NA or 99;
Coded as ‘Not on Treatment’ if der_anytx is 0
Coded as ‘Palliative’ if der_anytx is 1 and treatment_intent is 2
Coded as ‘Curative’ if der_anytx is 1 and treatment_intent is 1
Otherwise, Missing der_anytx:
0=No; 1=Yes; 99=Unknown
Treatment_intent: 1, Curative | 2, Palliative | 99, Unclear or unknown
Most recent line of cancer treatment, including systemic and non-systemic therapiesder_txlineUntreated in last 12 months; Curative NOS; First line; Non-curative NOS; Other; Second line or greater; Unknown
Hematologic malignancy indicatorder_heme0=No; 1=Yes
Appendix 3—table 4
Other covariates used for analysis.
Other covariate related to cohort selection for analysisVariable nameCovariate valuesCovariate description
Sex
(recode other/prefer not to say gender -->missing)		der_sexMale, Female
Breast cancerder_Breast0=No; 1=Yes
Cancer type of second malignancy.
If the patient has more than two malignancies, please select the second-most recently diagnosed cancer type. If unknown or unclear, please specify in the free text box below		cancer_type_21‘’ indicates no second malignancy
Region of patient residence with US and ex-US collapsedder_region_v3Non-US; Other; US
Appendix 3—table 5
New covariates added (2-5-22).
New covariateVariable nameCovariate valuesCovariate description
MBC vs non-MBCder_metastatic0=No; 1=Yes; 99=UnknownMetastatic cancer status (only applicable to solid tumors/lymphoma)
MBC site of metastasisder_met_bone0=No; 1=Yes; 99=UnknownMetastatic to bone
MBC site of metastasisder_met_liver0=No; 1=Yes; 99=UnknownMetastatic to liver
MBC site of metastasisder_met_lung_v20=No; 1=Yes; 99=UnknownMetastatic to lung
Appendix 5—table 1
Unadjusted rates of outcomes after COVID-19 diagnosis by cancer status.
NED >5yearsNED <5yearsActive and respondingActive andstableActive and progressingMissing/ unknownTotal
n* (%)n* (%)n* (%)n* (%)n* (%)n* (%)n* (%)
Outcomes
Total all-cause mortality†40 (11)12 (3)12 (7)11 (7)37 (38)11 (9)123 (9)
30-day all-cause mortality ‡29 (8)10 (2)10 (6)4 (2)27 (28)9 (7)89 (6)
Received mechanical ventilation†20 (5)13 (3)9 (5)7 (4)12 (12)8 (7)69 (5)
Admitted to an intensive care unit†35 (10)25 (6)13 (8)8 (5)18 (19)12 (10)111 (8)
Admitted to the hospital†163 (43)129 (29)54 (31)57 (34)70 (72)39 (32)512 (37)
  1. *

    N is based on non-missing data.

  2. †

    Included in primary ordinal COVID-19 severity outcome.

  3. ‡

    Secondary outcome.

Appendix 6—table 1
Baseline characteristics of female patients with MBC and COVID-19.
MBC
(N=233)
Age, years†
Median [IQR]58.0 [49.8, 68.3]
Race/ethnicity
Non-Hispanic White107 (46%)
Non-Hispanic Black56 (24%)
Hispanic50 (21%)
Non-Hispanic AAPI10 (4%)
Other10 (4%)
Smoking status
Never162 (70%)
Current or former66 (28%)
Missing/unknown5 (2%)
Obesity
No139 (60%)
Yes93 (40%)
Comorbidities‡
Cardiovascular42 (18%)
Pulmonary37 (16%)
Renal disease16 (7%)
Diabetes mellitus52 (22%)
Missing/unknown3 (1%)
ECOG performance status
063 (27%)
184 (36%)
2+42 (18%)
Unknown44 (19%)
Missing0 (0%)
Receptor status
HR+/HER2-98 (42%)
HR+/HER2+53 (23%)
HR-/HER2+26 (11%)
Triple negative33 (14%)
Missing/unknown23 (10%)
Cancer status
Active and responding55 (24%)
Active and stable78 (33%)
Active and progressing74 (32%)
Unknown25 (11%)
Missing0 (0%)
Metastatic sites (MBC)
Lung65 (28%)
Bone135 (58%)
Liver61 (26%)
Missing/unknown19 (8%)
Timing of anti-cancer therapy
Never/after COVID-19X*
0–4 weeks189 (81%)
1–3 months14 (6%)
>3 months19 (8%)
Missing/unknown11 (5%)*
Modality of active anti-cancer therapy‡, §
None24 (10%)
Cytotoxic chemotherapy114 (49%)
Targeted therapy115 (49%)
Endocrine therapy98 (42%)
Immunotherapy17 (7%)
Local (surgery/radiation)27 (12%)
Other6 (3%)
Missing/unknown6 (3%)
Region
Northeast97 (42%)
Midwest44 (19%)
South34 (15%)
West56 (24%)
Undesignated2 (1%)
Period of COVID-19 diagnosis
Jan-Apr 202033 (14%)
May-Aug 2020101 (43%)
Sept-Dec 202052 (22%)
Jan-Aug 202145 (19%)
Missing/unknown2 (1%)
Area of patient residence
Urban103 (44%)
Suburban80 (34%)
Rural12 (5%)
Missing/unknown38 (16%)
Treatment center characteristics
Academic medical center43 (18%)
Community practice63 (27%)
Tertiary care center127 (55%)
Missing/unknown0 (0%)
Severity of COVID-19
Mild126 (54%)
Moderate93 (40%)
Severe13 (6%)
Missing/unknown1 (<1%)
  1. *

    Cells combined to mask N<5 according to CCC19 low count policy.

  2. †

    Age was truncated at 90 years.

  3. ‡

    Percentages could sum to >100% because categories are not mutually exclusive.

  4. §

    Within 3 months of COVID-19 diagnosis.

Appendix 6—table 2
Unadjusted rates of outcomes after COVID-19 diagnosis in female patients with MBC.
n** (%)
Outcomes
Total all-cause mortality*45 (19)
30-day all-cause mortality†28 (12)
Received mechanical ventilation*20 (9)
Admitted to an intensive care unit*29 (12)
Admitted to the hospital*124 (53)
Clinical complications
Any cardiovascular complication‡48 (21)
Any pulmonary complication§86 (37)
Any gastrointestinal complication13 (6)
Acute kidney injury32 (14)
Multisystem organ failure12 (5)
Superimposed infection32 (14)
Sepsis28 (12)
Any bleeding8 (3)
Interventions
Remdesivir35 (15)
Hydroxychloroquine25 (11)
Corticosteroids65 (29)
Covid Other45 (20)
Supplemental oxygen84 (37)
  1. *

    Included in primary ordinal COVID-19 severity outcome.

  2. †

    Secondary outcome.

  3. ‡

    Cardiovascular complication includes hypotension, myocardial infarction, other cardiac ischemia, atrial fibrillation, ventricular fibrillation, other cardiac arrhythmia, cardiomyopathy, congestive heart failure, pulmonary embolism (PE), deep vein thrombosis (DVT), stroke, thrombosis NOS complication.

  4. §

    Pulmonary complication includes respiratory failure, pneumonitis, pneumonia, acute respiratory distress syndrome (ARDS), PE, pleural effusion, empyema.

  5. Gastrointestinal complication includes acute hepatic injury, ascites, bowel obstruction, bowel perforation, ileus, peritonitis.

  6. **

    N is based on non-missing data.

Appendix 7—table 1
Adjusted associations of race factors with COVID-19 severity outcome.
COVID-19 severity
OR (95% CI)Point value e estimates*Lower bound e values*
Race (Ref: NHW)
Black1.74 (1.24–2.45)1.971.47
Hispanic1.38 (0.93–2.05)1.631.00
AAPI3.40 (1.70–6.79)3.091.93
Other2.97 (1.71–5.17)2.841.94
  1. *

    These values were calculated based on the formula for logistic regression

Appendix 8—table 1
Baseline characteristics of male patients with breast cancer and COVID-19.
Total25 (100%)
Age, years†
Median [IQR]67.0 [60–75]
Race/ethnicity
NHW13 (52%)
Black8 (32%)
Hispanic<5 (<20%)
AAPI0 (0%)
Other<5 (<20%)
Smoking status
Never18 (72%)
Current or former7 (28%)
Obesity
No12 (48%)
Yes13 (52%)
Comorbidities ‡
Cardiovascular6 (24%)
Pulmonary5 (20%)
Renal disease<5 (<20%)
Diabetes mellitus11 (44%)
ECOG performance status
05 (20%)
110 (40%)
2+X*
Unknown10 (40%)*
Receptor status
HR+/HER2-18 (72%)
HR+/HER2+5 (20%)
HR+/HER2+X*
Triple negative0 (0%)
Missing/unknown2 (8%)*
Cancer status
Remission or NED, >5 years<5 (<20%)
Remission or NED, <5 years6 (24%)
Active and responding<5 (<20%)
Active and stable<5 (<20%)
Active and progressing5 (20%)
Unknown3 (12%)
Timing of anti-cancer therapy
Never/after COVID-19<5 (<20%)
0–4 weeks17 (68%)
1–3 months0 (0%)
>3 months<5 (<20%)
Missing/unknown1 (4%)
Modality of active anti-cancer therapy‡, §
None7 (28%)
Chemotherapy6 (24%)
Targeted therapy6 (24%)
Endocrine therapy10 (40%)
Immunotherapy0 (0%)
Local (surgery/radiation)<5 (<20%)
Other0 (0%)
Missing/unknown1 (4%)
Region
Northeast11 (44%)
Midwest<5 (<20%)
South<5 (<20%)
West7 (28%)
Undesignated0 (0%)
Period of COVID-19 diagnosis
Jan-Apr 202010 (40%)
May-Aug 20209 (36%)
Sept-Dec 20205 (20%)
Area of patient residence
Urban9 (36%)
Suburban8 (32%)
Rural0 (0%)
Missing/unknown8 (32%)
Severity of COVID19
Mild11 (44%)
Moderate/severe14 (56%)

  1. Variable categories with one to five cases are masked by replacing with N<5 according to CCC19 policy.

  2. *

    Cells combined to mask N<5 according to CCC19 low count policy.

  3. †

    Age was truncated at 90 years.

  4. ‡

    Percentages could sum to >100% because categories are not mutually exclusive.

  5. §

    Within 3 months of COVID-19 diagnosis.

Appendix 8—table 2
Unadjusted rates of outcomes after COVID-19 diagnosis among male patients with BC.
Outcomes
Total all-cause mortality5 (20)
30-day all-cause mortality5 (20)
Received mechanical ventilation<5 (<20%)
Admitted to an intensive care unit<5 (<20%)
Admitted to the hospital15 (60)
Clinical complications
Any cardiovascular complication*<5 (<20%)
Any pulmonary complication†12 (48)
Any gastrointestinal complication‡0 (0%)
Acute kidney injury<5 (<20%)
Multisystem organ failure<5 (<20%)
Superimposed infection<5 (<20%)
Sepsis<5 (<20%)
Any bleeding<5 (<20%)
Interventions
Remdesivir<5 (<20%)
Hydroxychloroquine7 (28)
Corticosteroids<5 (<20%)
Other9 (36)
Supplemental oxygen12 (48)

  1. Variable categories with one to five cases are masked by replacing with N<5 according to CCC19 policy

  2. *

    Cardiovascular complication includes hypotension, myocardial infarction, other cardiac ischemia, atrial fibrillation, ventricular fibrillation, other cardiac arrhythmia, cardiomyopathy, congestive heart failure, pulmonary embolism (PE), deep vein thrombosis (DVT), stroke, thrombosis NOS complication.

  3. †

    Pulmonary complication includes respiratory failure, pneumonitis, pneumonia, acute respiratory distress syndrome (ARDS), PE, pleural effusion, empyema.

  4. ‡

    Gastrointestinal complication includes acute hepatic injury, ascites, bowel obstruction, bowel perforation, ileus, peritonitis.

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  1. Gayathri Nagaraj
  2. Shaveta Vinayak
  3. Ali Raza Khaki
  4. Tianyi Sun
  5. Nicole M Kuderer
  6. David M Aboulafia
  7. Jared D Acoba
  8. Joy Awosika
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  10. Nicole B Balmaceda
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  21. John Deeken
  22. Aakash Desai
  23. Natasha Edwin
  24. Lawrence E Feldman
  25. Daniel B Flora
  26. Christopher R Friese
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  28. Cyndi J Gonzalez
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  30. Shilpa Gupta
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  37. Monika Joshi
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  41. Vadim S Koshkin
  42. Amit A Kulkarni
  43. Daniel H Kwon
  44. Chris Labaki
  45. Philip E Lammers
  46. Kate I Lathrop
  47. Mark A Lewis
  48. Xuanyi Li
  49. Gilbert de Lima Lopes
  50. Gary H Lyman
  51. Della F Makower
  52. Abdul-Hai Mansoor
  53. Merry-Jennifer Markham
  54. Sandeep H Mashru
  55. Rana R McKay
  56. Ian Messing
  57. Vasil Mico
  58. Rajani Nadkarni
  59. Swathi Namburi
  60. Ryan H Nguyen
  61. Taylor Kristian Nonato
  62. Tracey Lynn O'Connor
  63. Orestis A Panagiotou
  64. Kyu Park
  65. Jaymin M Patel
  66. Kanishka GopikaBimal Patel
  67. Jeffrey Peppercorn
  68. Hyma Polimera
  69. Matthew Puc
  70. Yuan James Rao
  71. Pedram Razavi
  72. Sonya A Reid
  73. Jonathan W Riess
  74. Donna R Rivera
  75. Mark Robson
  76. Suzanne J Rose
  77. Atlantis D Russ
  78. Lidia Schapira
  79. Pankil K Shah
  80. M Kelly Shanahan
  81. Lauren C Shapiro
  82. Melissa Smits
  83. Daniel G Stover
  84. Mitrianna Streckfuss
  85. Lisa Tachiki
  86. Michael A Thompson
  87. Sara M Tolaney
  88. Lisa B Weissmann
  89. Grace Wilson
  90. Michael T Wotman
  91. Elizabeth M Wulff-Burchfield
  92. Sanjay Mishra
  93. Benjamin French
  94. Jeremy L Warner
  95. Maryam B Lustberg
  96. Melissa K Accordino
  97. Dimpy P Shah
  98. On behalf of the COVID-19 and Cancer Consortium
(2023)
Clinical characteristics, racial inequities, and outcomes in patients with breast cancer and COVID-19: A COVID-19 and cancer consortium (CCC19) cohort study
eLife 12:e82618.
https://doi.org/10.7554/eLife.82618