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Vol. 59. Issue 11.
Pages 772-778 (November 2023)
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Visits
10419
Vol. 59. Issue 11.
Pages 772-778 (November 2023)
Scientific Letter
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Clinical Outcomes of Critical COVID-19 in HIV-Infected Adults: A Propensity Score Matched Analysis
Visits
10419
Catia Cilloniza,b,c,d,
Corresponding author
cilloniz@recerca.clinic.cat

Corresponding authors.
, Anna Motosa,b,c, Joan Cansecoa,b, Yhivian Peñascoe, Pilar Ricartf, Elena Abrilg, José Manuel Gómez Garcíah, Aaron Blandino Ortizi,j, Nadia García Mateok, Ángel Sánchez-Mirallesl, Nieves Francom, Jordi Rieran, Ricard Ferrern, Elena Bustamante-Munguirao, Jesús Caballerop, Amalia Martínez de la Gándaraq, Susana Sanchor, Joan-Ramon Masclanss,t, Luis Urrelo-Cerrónu, Nieves Carbonellv..., Lorenzo Socíasw, Carme Barberàx, José A. Lorentea,y, Óscar Peñuelas Rodrígueza,y, Rosario Menéndeza,z, David de Gonzalo-Calvoa,x, Adrian Ceccatoa,aa,ag, Laia Fernandez-Barata,b,c, Dario Garcia-Gasullaab, Albert Gabarrusa,b, Carolina Garcia-Vidalac, Asunción Morenoac, Ferran Barbéa,ad, José M. Miroac,ae,1,
Corresponding author
jmmiro@ub.edu

Corresponding authors.
, Antoni Torresa,b,c,af,1,
on behalf of CIBERESUCICOVID Project (COV20/00110, ISCIII) Ver más
a CIBER of Respiratory Diseases (CIBERES), Madrid, Spain
b August Pi i Sunyer Biomedical Research Institute (IDIBAPS), Spain
c University of Barcelona, Spain
d Faculty of Health Sciences, Continental University, Huancayo, Peru
e Intensive Medicine Department, Hospital Universitario Marqués of Valdecilla, Santander, Spain
f Intensive Medicine Department, Hospital Universitari Germans Trias, Badalona, Spain
g Hospital Universitario Torrejón, Madrid, Spain
h Hospital General Universitario Gregorio Marañón, Madrid, Spain
i Intensive Care Department, Hospital Universitario Ramón y Cajal, Madrid, Spain
j Universidad de Alcalá, Madrid, Spain
k Group for Biomedical Research in Sepsis (BioSepsis), Instituto de Investigación Biomédica de Salamanca (IBSAL), Paseo de San Vicente, Salamanca, Spain
l Hospital de Sant Joan d’Alacant, Alacant, Spain
m Hospital Universitario de Móstoles, Madrid, Spain
n Intensive Care Department, Vall d’Hebron Hospital Universitari, SODIR Research Group, Vall d’Hebron Institut de Recerca (VHIR), Barcelona, Spain
o Department of Intensive Care Medicine, Hospital Clínico Universitario Valladolid, Valladolid, Spain
p Critical Care Department, Hospital Universitari Arnau de Vilanova, IRBLleida, Lleida, Spain
q Hospital Universitario Infanta Leonor, Madrid, Spain
r Critical Care Department, Hospital Universitario y Politecnico de La Fe, Valencia, Spain
s Critical Care Department, Hospital del Mar, Critical Illness Research Group (GREPAC), Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), Barcelona, Spain
t Department of Medicine and Life Sciences (MELIS), Universitat Pompeu Fabra (UPF), Barcelona, Spain
u Hospital de Tortosa Verge de la Cinta, Tarragona, Spain
v Intensive Care Unit, Hospital Clinico Universitario de Valencia, Spain
w Intensive Care Unit, Hospital Son Llàtzer, Palma de Mallorca, Illes Balears, Spain
x Hospital Santa Maria, IRBLleida, Lleida, Spain
y Hospital Universitario de Getafe, Madrid, Spain
z Pulmonology Service, University and Polytechnic Hospital La Fe, Valencia, Spain
aa Critical Care Center, ParcTaulí Hospital Universitari, Institut d’Investigació i Innovació Parc Taulí I3PT, Sabadell, Spain
ab Barcelona Supercomputing Center, Spain
ac Department of Infectious Diseases, Hospital Clinic-IDIBAPS, University of Barcelona, Barcelona, Spain
ad Pulmonary Department, Translational Research in Respiratory Medicine, University Hospital Arnau de Vilanova and Santa Maria, IRBLleida, Spain
ae CIBER de Enfermedades Infecciosas (CIBERINFEC), Madrid, Spain
af Pulmonology Department, Hospital Clinic of Barcelona, Spain
ag Intensive Care Unit, Hospital Universitari Sagrat Cor, Grupo Quironsalud, Barcelona, Spain
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Table 1. Demographics and clinical characteristics at admission, and complications and outcomes during ICU admission.
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To the Director,

There is conflicting information regarding the severity and outcomes of COVID-19 in people living with human immunodeficiency virus (PLHIV). Data from previously published matched case–control studies showed no differences in severity or outcome between HIV-infected and HIV-negative patients.1–3 Also, a cohort study of 2988 HIV-infected patients evaluating the association between HIV and COVID-19 diagnoses, hospitalisation, and in-hospital death in New York State reported poor outcomes in HIV-infected patients compared with HIV-negative patients.4 There are no specific studies investigating the severity and outcomes of critically ill patients with COVID-19 and HIV-infection. We aim to investigate whether the clinical presentation, severity and outcomes of COVID-19 in critically ill HIV-infected patients were comparable to those seen in non-HIV-infected patients.

The CIBERESUCICOVID is a multicentre, observational, prospective/retrospective cohort study (NCT04457505) of 6512 consecutive patients with SARS-CoV-2 infection who were admitted to 69 ICUs in Spain between February 2020 and July 2022. Approved by the ethical committee – HCB/2020/0370. Data was collected as previously described.5 The primary outcome was all-cause 90-day mortality. Secondary outcomes included all-cause in-hospital, 15-day, 30-day and 1-year mortality, length of ICU and hospital stay, and ventilator and ICU-free days. Propensity score matching (PSM) method6,7 was used to obtain the balance among baseline variables between patients with and without HIV. We used a 1:2 nearest-neighbour matching with age, sex, number of comorbidities and SOFA as covariates and an exact matching constraint on wave of COVID-19 and centre, without replacement and within a calliper width of 0.6. We estimated the 15-, 30- and 90-day, and 1-year mortality with 95% confidence intervals (CI).8 We analysed the association between HIV infection and mortality by means of Cox regression analyses. Survival curves of patients with and without HIV were obtained using the Kaplan–Meier method and compared using the Gehan–Breslow–Wilcoxon test.9

Fig. 1 depicts patients flow-chart and Table 1 describes the full cohort (N=6406: 6372 HIV-negative and 34 PLHIV) and the propensity score matching (N=93, 62 HIV-negative and 31 PLHIV) cohort. In the full cohort, patients with HIV infection were younger, presented higher numbers of comorbidities, were more frequently current smokers, alcohol abusers, had higher APACHE II scores at ICU admission than patients without HIV infection. After PSM, no significant differences were found in age, number of comorbidities, proportion of smokers or alcohol abusers. However, the APACHE II score was higher in PLHIV (Table 1). Sex and SOFA did not differ between groups before and after PSM. In the full cohort, cardiac ischaemia was the only complication that differed between groups, showing a higher rate in the HIV infection group compared to non-HIV infection group. After PSM, no significant differences were found in any complication. Finally, all outcomes did not differ between groups before and after PSM. In the full cohort, the 15-, 30-, 90-day, and 1-year mortality rates were 12% (95% CI, 12–13%), 25% (95% CI, 23–26%), 34% (95% CI, 33–35%) and 39% (95% CI, 38–40%) in the non-HIV infection group, compared with 16% (95% CI, 3–28%), 22% (95% CI, 8–36%), 22% (95% CI, 8–36%) and 27% (95% CI, 11–42%) in the HIV infection group, respectively. After PSM, the 15-, 30-, 90-day, and 1-year mortality rates were 10% (95% CI, 2–17%), 21% (95% CI, 11–31%), 26% (95% CI, 15–37%) and 30% (95% CI, 18–42%) in the non-HIV infection group, compared with 14% (95% CI, 1–26%), 21% (95% CI, 6–35%), 21% (95% CI, 6–35%) and 26% (95% CI, 9–42%) in the HIV infection group, respectively. In the full cohort, Cox regression analyses for 15-, 30-, 90-day, and 1-year mortality did not find significant differences between groups, giving HRs of 1.24 (95% CI, 0.52–2.99), 0.92 (95% CI, 0.44–1.94), 0.66 (95% CI, 0.32–1.40) and 0.73 (95% CI, 0.36–1.46), respectively. After PSM, Cox regression analyses for 15-, 30-, 90-day, and 1-year mortality did not find significant differences between groups, giving HRs of 1.40 (95% CI, 0.39–4.95), 1.01 (95% CI, 0.38–2.65), 0.81 (95% CI, 0.32–2.07) and 0.89 (95% CI, 0.37–2.15), respectively.

Fig. 1.

Flow chart of the study population.

(0.42MB).
Table 1.

Demographics and clinical characteristics at admission, and complications and outcomes during ICU admission.

Variables  Full cohort (N=6406)Propensity score matching (N=93)
  No  Non-HIV infection (N=6372)  HIV infection (N=34)  P-value  No  Non-HIV infection (N=62)  HIV infection (N=31)  P-value 
Waves of COVID-19  6406      0.729  93      >0.999 
First: 8/1/2020 to 9/5/2020    3048 (48)  18 (53)  –    32 (52)  16 (52)  – 
Second: 10/5/2020 to 7/12/2020    1839 (29)  11 (32)  –    22 (35)  11 (35)  – 
Third: 8/12/2020 to 9/3/2021    873 (14)  5 (15)  –    8 (13)  4 (13)  – 
Fourth: 10/3/2021 to 15/6/2021    187 (3)  0 (0)  –    0 (0)  0 (0)  – 
Fifth: 16/6/2021 to 13/10/2021    245 (4)  0 (0)  –    0 (0)  0 (0)  – 
Sixth: 14/10/2021 to 27/3/2022    163 (3)  0 (0)  –    0 (0)  0 (0)  – 
Seventh or higher: 28/3/2022 to 6/7/2022    16 (0.3)  0 (0)  –    0 (0)  0 (0)  – 
Age, median (Q1;Q3), years  6406  63 (54; 71)  51 (47; 65)  <0.001  93  57.5 (46; 64)  51 (48; 65)  0.619 
Male sex,n(%)  6406  4484 (70)  26 (76)  0.437  93  46 (74)  23 (74)  >0.999 
BMI, median (Q1;Q3), kg/m2  5631  28.9 (26; 32.3)  26.9 (23.6; 33.1)  0.174  77  29.4 (26.5; 31.9)  26.9 (23.9; 34.6)  0.277 
Number of comorbidities, median (Q1;Q3)  5745  2 (1; 3)  2.5 (2; 4)  <0.001  84  3 (1; 4)  2 (2; 4)  0.931 
Comorbidities,n(%)
Diabetes mellitus  6406  1577 (25)  11 (32)  0.306  93  24 (39)  8 (26)  0.217 
Hypertension  6405  3208 (50)  18 (53)  0.763  93  41 (66)  15 (48)  0.099 
Metabolic disease  6396  1955 (31)  8 (24)  0.364  93  35 (56)  7 (23)  0.002 
Chronic liver disease  6405  225 (4)  4 (12)  0.032  93  3 (5)  3 (10)  0.397 
Chronic heart disease  6405  819 (13)  3 (9)  0.614  93  21 (34)  3 (10)  0.012 
Chronic lung disease  6406  985 (15)  4 (12)  0.811  93  16 (26)  3 (10)  0.069 
Chronic renal failure  6405  455 (7)  3 (9)  0.732  93  8 (13)  2 (6)  0.487 
Immunosuppressiona  6403  237 (4)  34 (100)  <0.001  93  5 (8)  31 (100)  <0.001 
Solid transplantation    109 (2)  2 (6)  0.117    3 (5)  2 (6)  >0.999 
Bone transplantation    6 (0.1)  0 (0)  >0.999    0 (0)  0 (0)  – 
AIDS or HIV infection    0 (0)  34 (100)  –    0 (0)  31 (100)  – 
Other    147 (2)  1 (3)  0.549    2 (3)  1 (3)  >0.999 
Smoking habit  5915      0.007  88      0.396 
No smoke    3706 (63)  17 (55)  0.349    31 (53)  16 (55)  – 
Current smoke    347 (6)  6 (19)  0.009    7 (12)  6 (21)  – 
Former smoke    1831 (31)  8 (26)  0.524    21 (36)  7 (24)  – 
Alcohol abuse (current or former)  5847  317 (5)  7 (23)  <0.001  85  4 (7)  5 (18)  0.148 
Nursing-home,n(%)  6252  103 (2)  1 (3)  0.416  91  0 (0)  1 (3)  0.319 
Previous 30 days admission,n(%)  6404  229 (4)  3 (9)  0.124  93  5 (8)  2 (6)  >0.999 
Days since initial symptoms to ICU admission, median (Q1;Q3)  6365  9 (7; 12)  7 (5; 10)  0.013  93  8.5 (6; 12)  9 (5; 10)  0.508 
Treatment before admission,n(%)                 
Angiotensin-converting enzyme inhibitor  3175  1225 (39)  5 (29)  0.429  55  21 (51)  2 (14)  0.016 
Statin  6366  1983 (31)  12 (35)  0.618  91  26 (42)  10 (32)  0.366 
Non-steroidal anti-inflammatory drug  6280  755 (12)  2 (6)  0.422  90  13 (21)  2 (7)  0.131 
Corticosteroids  6363  521 (8)  3 (9)  0.750  90  9 (15)  3 (10)  0.744 
Antibiotics  6358  860 (14)  5 (15)  0.802  93  11 (18)  4 (13)  0.550 
SARS-CoV-2 vaccine  3561  269 (8)  0 (0)  0.622  43  0 (0)  0 (0)  – 
Two doses of SARS-CoV-2 vaccine  216  151 (70)  0 (0)  <0.001  0 (0)  0 (0)  – 
Characteristics at ICU admission                 
Glasgow Coma Scale, median (Q1; Q3)  5196  15 (15; 15)  15 (15; 15)  0.664  74  15 (15; 15)  15 (15; 15)  0.652 
APACHE-II score, median (Q1; Q3)  3708  12 (9; 15)  16.5 (14; 20)  <0.001  51  10 (6; 13)  16.5 (14; 18)  <0.001 
SOFA score, median (Q1; Q3)  4416  5 (3; 7)  5.5 (4; 8)  0.288  61  4 (3; 7)  5.5 (4; 8)  0.297 
SOFA haemodynamic component, median (Q1; Q3)  6165  0 (0; 4)  0 (0; 4)  0.890  87  0 (0; 4)  0 (0; 4)  0.779 
SOFA renal component, median (Q1; Q3)  6305  0 (0; 0)  0 (0; 1)  0.052  93  0 (0; 1)  0 (0; 1)  0.614 
Temperature, median (Q1; Q3), °C  5982  36.7 (36; 37.5)  36.8 (35.8; 37.8)  0.693  88  36.8 (36; 37.7)  37 (35.9; 38)  0.572 
Respiratory rate, median (Q1; Q3), bpm  5719  25 (21; 30)  26 (23; 35)  0.153  81  24.5 (22; 30)  25 (23; 35)  0.379 
Arterial blood gases at ICU admission
PaO2/FiO2ratio, median (Q1; Q3)  5351  112 (80; 164)  94 (79; 151)  0.343  77  112 (79; 176)  92.5 (79; 151)  0.176 
PaO2/FiO2ratio in ventilated patients, median (Q1; Q3)  5063  111 (80; 162)  94 (79; 148)  0.367  70  107 (79; 174)  89 (76; 130)  0.145 
PaO2/FiO2ratio categories in ventilated patients, n (%)  5063      0.055  70      0.222 
Severe (<100)    2126 (42)  15 (60)  –    22 (47)  15 (65)  – 
Moderate (≥100 to <200)    2160 (43)  4 (16)  –    15 (32)  3 (13)  – 
Mild (≥200 to <300)    546 (11)  4 (16)  –    3 (6)  3 (13)  – 
No ARDS (≥300)    206 (4)  2 (8)  –    7 (15)  2 (9)  – 
pH, median (Q1; Q3)  5787  7.41 (7.34; 7.46)  7.38 (7.3; 7.42)  0.094  86  7.42 (7.36; 7.46)  7.38 (7.31; 7.43)  0.142 
PaCO2, median (Q1; Q3), mmHg  5628  39 (34; 46.8)  38.5 (31; 59.2)  0.869  81  38 (34.1; 43)  39.8 (31; 60)  0.504 
PaCO2in ventilated patients, median (Q1; Q3), mmHg  5265  39.3 (34; 47)  38.5 (31; 59.2)  0.811  71  38 (34.2; 45.5)  41 (31; 60)  0.535 
Laboratory findings at ICU admission
Haemoglobin, median (Q1; Q3), g/dL  6144  13.2 (12; 14.4)  12.4 (11; 14)  0.037  92  12.3 (11.5; 14.8)  12.5 (11; 14.1)  0.661 
Leucocyte count, median (Q1; Q3), 109/L  6293  8.9 (6.4; 12.5)  8.9 (7.1; 14)  0.516  93  8.1 (6.1; 12.1)  8.7 (7.1; 14)  0.401 
Lymphocyte count, median (Q1; Q3), 109/L  6202  0.69 (0.47; 0.98)  0.79 (0.6; 1.4)  0.032  93  0.73 (0.4; 1.2)  0.73 (0.53; 1.4)  0.498 
Neutrophil count, median (Q1; Q3), 109/L  6171  7.7 (5.2; 11.1)  7.4 (5.7; 12.5)  0.696  93  7.1 (4.7; 11.3)  7.3 (5.7; 12.9)  0.436 
Monocyte count, median (Q1; Q3), 109/L  5988  0.36 (0.2; 0.53)  0.35 (0.28; 0.5)  0.569  92  0.4 (0.2; 0.54)  0.33 (0.25; 0.5)  0.822 
Platelet count, median (Q1; Q3), 109/L  6291  232 (177; 303)  222 (144; 299)  0.210  93  212 (156; 272)  230 (160; 316)  0.483 
D-dimer, median (Q1; Q3), ng/mL  5376  980 (500; 2300)  949 (522; 1855)  0.737  82  647 (356; 2250)  1100 (544; 1970)  0.200 
C-reactive protein, median (Q1; Q3), mg/L  5977  127 (61; 219)  167 (82; 245)  0.240  91  111 (69; 194)  172 (91; 221)  0.065 
Serum creatinine, median (Q1; Q3), mg/dL  6303  0.83 (0.67; 1.08)  0.99 (0.78; 1.51)  0.037  93  0.89 (0.74; 1.5)  0.99 (0.72; 1.51)  0.741 
LDH, median (Q1; Q3), U/L  5203  477 (362; 654)  465 (351; 529)  0.194  81  439 (303; 591)  472 (357; 589)  0.347 
Ferritin, median (Q1; Q3), ng/mL  3341  1151 (609; 1915)  921 (339; 1756)  0.520  48  800 (473; 1365)  921 (339; 1756)  0.556 
Respiratory support at ICU admissionb  6391      0.376  93      0.531 
Conventional oxygen therapy    442 (7)  4 (12)  –    8 (13)  3 (10)  – 
High-flow nasal cannula    1760 (28)  12 (35)  –    27 (44)  11 (35)  – 
Non-invasive mechanical ventilation    750 (12)  2 (6)  –    1 (2)  2 (6)  – 
Invasive mechanical ventilation    3405 (54)  16 (47)  –    26 (42)  15 (48)  – 
Septic shock at ICU admissionc  5864  428 (7)  3 (10)  0.494  87  4 (7)  1 (4)  >0.999 
Complications during ICU admission,n(%)                 
Bacterial pneumoniad  6366  1748 (28)  11 (33)  0.463  92  21 (34)  10 (33)  0.959 
Pneumothorax  6394  511 (8)  2 (6)  >0.999  93  2 (3)  2 (6)  0.598 
Pleural effusion  6389  658 (10)  6 (18)  0.159  93  5 (8)  5 (16)  0.292 
Organising pneumonia  6307  291 (5)  3 (9)  0.186  91  3 (5)  3 (10)  0.379 
Tracheobronchitis  6358  55 (1)  0 (0)  >0.999  91  2 (3)  0 (0)  >0.999 
Pulmonary embolism  6245  594 (10)  2 (6)  0.765  91  8 (13)  2 (7)  0.488 
Endocarditis  6391  20 (0.3)  0 (0)  >0.999  92  0 (0)  0 (0)  – 
Myocarditis/pericarditis  6396  107 (2)  0 (0)  >0.999  92  0 (0)  0 (0)  – 
Cardiomyopathy  6394  118 (2)  0 (0)  >0.999  92  0 (0)  0 (0)  – 
Heart failure  6395  146 (2)  0 (0)  >0.999  93  0 (0)  0 (0)  – 
Cardiac ischaemia  6393  114 (2)  3 (9)  0.024  93  1 (2)  3 (10)  0.106 
Bacteraemia  6386  1645 (26)  5 (15)  0.160  92  16 (26)  5 (17)  0.328 
Stroke  6392  111 (2)  0 (0)  >0.999  93  0 (0)  0 (0)  – 
Delirium  6380  1198 (19)  8 (24)  0.490  93  11 (18)  8 (26)  0.363 
Coagulation disordere  6384  1975 (31)  8 (24)  0.396  92  19 (31)  7 (23)  0.465 
Disseminated intravascular coagulationf  1944  806 (42)  3 (38)  >0.999  26  9 (47)  2 (29)  0.658 
Anaemiag  6398  3939 (62)  22 (65)  0.736  93  40 (65)  20 (65)  >0.999 
Rhabdomyolysis  6374  225 (4)  1 (3)  >0.999  93  1 (2)  1 (3)  >0.999 
Acute renal failureh  6397  2081 (33)  11 (32)  0.965  93  25 (40)  10 (32)  0.449 
Pancreatitis  6384  57 (1)  0 (0)  >0.999  93  1 (2)  0 (0)  >0.999 
Liver dysfunction  6396  2036 (32)  7 (21)  0.155  93  17 (27)  7 (23)  0.615 
Hyperglycaemia  6394  4687 (74)  24 (71)  0.682  93  46 (74)  23 (74)  >0.999 
Haemorrhage  6395  481 (8)  1 (3)  0.514  93  6 (10)  1 (3)  0.418 
Outcomes
In-hospital mortality, n (%)  6406  1950 (31)  8 (24)  0.372  93  16 (26)  7 (23)  0.734 
15-Day mortality, n (%)i  6191  769 (12)  5 (16)  0.589  91  6 (10)  4 (14)  0.720 
30-Day mortality, n (%)j  5998  1463 (25)  7 (22)  0.728  91  13 (21)  6 (21)  0.976 
90-Day mortality, n (%)k  5804  1952 (34)  7 (22)  0.154  90  16 (26)  6 (21)  0.568 
1-Year mortality, n (%)l  5191  2015 (39)  8 (27)  0.166  83  17 (30)  7 (26)  0.677 
Length of ICU stay, median (Q1; Q3), days
All patients  6402  14 (7; 27)  11.5 (7; 20)  0.404  94  17 (8; 29)  12 (7; 23)  0.392 
Surviving patients  4445  13 (7; 27)  11.5 (7; 23)  0.659  70  17 (7; 29)  12 (7.5; 25.5)  0.642 
Length of hospital stay, median (Q1; Q3), days
All patients  6400  23 (14; 39)  18 (12; 40)  0.477  93  25 (15; 43)  22 (12; 42)  0.729 
Surviving patients  4446  26 (16; 44)  25.5 (15; 42)  0.699  70  26.5 (15; 45)  27.5 (15; 42.5)  0.995 
Ventilator-free days, median (Q1; Q3)  4900  0 (0; 16)  9 (0; 18)  0.306  66  0 (0; 14)  9 (0; 18)  0.399 
Invasive mechanical ventilation length, median (Q1; Q3), daysm
All patients  4714  15 (8; 27)  13 (8; 19)  0.348  62  17.5 (9; 25.5)  13 (9; 19)  0.205 
Surviving patients  2939  14 (8; 27)  13 (9; 19)  0.582  43  20 (9; 26)  13.5 (9; 23)  0.399 
ICU-free days, median (Q1; Q3)  6403  3 (0; 19)  12 (0; 20)  0.339  93  2.5 (0; 19)  12 (0; 19)  0.567 
Readmission, n (%)n  3254  417 (13)  5 (21)  0.227  62  4 (10)  4 (18)  0.438 
Chest X-ray, n (%)o
Abnormal  3171  2845 (90)  23 (96)  0.723  62  35 (88)  21 (95)  0.409 
Persistent infiltrates  3171  71 (2)  0 (0)  >0.999  62  2 (5)  0 (0)  0.535 
Diffuse interstitial lung disease  3171  12 (0.4)  0 (0)  >0.999  62  0 (0)  0 (0)  – 
Fibrotic tract  3171  69 (2)  0 (9)  >0.999  62  2 (5)  0 (0)  0.535 
Emphysema  3171  5 (0.2)  0 (0)  >0.999  62  1 (3)  0 (0)  >0.999 
Others  3171  50 (2)  1 (4)  0.323  62  1 (3)  1 (5)  >0.999 
CT scan, n (%)o
Abnormal  3172  3020 (96)  24 (100)  0.623  62  39 (98)  22 (100)  >0.999 
Persistent infiltrates  3172  202 (6)  1 (4)  >0.999  62  5 (13)  1 (5)  0.409 
Diffuse interstitial lung disease  3172  35 (1)  0 (0)  >0.999  62  1 (3)  0 (0)  >0.999 
Fibrotic tract  3172  183 (6)  0 (0)  0.397  62  2 (5)  0 (0)  0.535 
Emphysema  3172  58 (2)  0 (0)  >0.999  62  0 (0)  0 (0)  – 
Pulmonary embolism  3172  7 (0.2)  0 (0)  >0.999  62  0 (0)  0 (0)  – 
Others  3172  258 (8)  2 (8)  >0.999  62  4 (10)  2 (9)  >0.999 

Abbreviations: HIV indicates human immunodeficiency virus; Q1, first quartile; Q3, third quartile; BMI, body mass index; AIDS, acquired immunodeficiency syndrome; ICU, intensive care unit; APACHE, acute physiology and chronic health evaluation; SOFA, sequential organ failure assessment; PaO2, partial pressure of arterial oxygen; FiO2, fraction of inspired oxygen; LDH, lactate dehydrogenase. Percentages calculated on non-missing data. P-values marked in bold indicate numbers that are statistically significant at the 95% confidence limit.

a

Possibly>1 cause of immunosuppression.

b

Patients who received high-flow nasal cannula but needed non-invasive mechanical ventilation were included in the non-invasive mechanical ventilation group. Patients who received high-flow nasal cannula and/or non-invasive ventilation but needed intubation were included in the invasive mechanical ventilation group.

c

Criteria for the Sepsis-3 definition of septic shock include vasopressor treatment and a lactate concentration>2mmol/L at ICU admission.

d

Clinically or radiologically diagnosed bacterial pneumonia managed with antimicrobials. Bacteriologic confirmation was not required.

e

Abnormal coagulation was identified by abnormal prothrombin time or activated partial thromboplastin time.

f

Disseminated intravascular coagulation was defined by thrombocytopenia, prolonged prothrombin time, low fibrinogen, elevated D-dimer and thrombotic microangiopathy.

g

Haemoglobin consistently below 120g/L for non-pregnant women and 130g/L for men.

h

Acute renal injury was defined as either an increase in serum creatinine by ≥0.3mg/dL within 48h or an increase in serum creatinine to ≥1.5 times that at baseline.

i

Calculated only for patients with 15-day follow-up in the full cohort (6159 in the non-HIV infection group and 32 in the HIV infection group) and in the propensity score matching (62 in the non-HIV infection group and 29 in the HIV infection group).

j

Calculated only for patients with 30-day follow-up in the full cohort (5966 in the non-HIV infection group and 32 in the HIV infection group) and in the propensity score matching (62 in the non-HIV infection group and 29 in the HIV infection group).

k

Calculated only for patients with 90-day follow-up in the full cohort (5772 in the non-HIV infection group and 32 in the HIV infection group) and in the propensity score matching (61 in the non-HIV infection group and 29 in the HIV infection group).

l

Calculated only for patients with 1-year follow-up in the full cohort (5161 in the non-HIV infection group and 30 in the HIV infection group) and in the propensity score matching (56 in the non-HIV infection group and 27 in the HIV infection group).

m

Duration of invasive mechanical ventilation was measured from initiation of ventilation until either successful extubation, successful permanent disconnection or death.

n

Within 1 year of hospital discharge.

o

At 1 year of hospital discharge.

Of the 34 PLHIV included in the study, 26 (76%) were males, with a median (IQR) age of 51 (47; 65) years. Data on the probable route of exposure were available in 47% of cases. HIV infection was acquired by men who have sex with men and intravenous drug use in 7 (44%) and 5 (31%) cases, respectively. Data on available ART therapy was available in 29 cases (85%). Twenty-five out of 29 cases (86%) were on antiretroviral therapy (ART) at the time of hospital admission. ART regimens were based on integrase inhibitors, non-nucleoside reverse transcriptase inhibitors, protease inhibitors, and other regimens in 11 (44%), 9 (36%), 3 (12%), and 2 (8%) cases, respectively. Data on HIV-RNA viral load in plasma was available in 27 patients (79%). Twenty-one out of 27 patients (84%) had an undetectable HIV-RNA viral load in plasma (<50copies/mL). Data on CD4+ T cell count was available in 21 patients (62%). The median (IQR) last CD4+ T cell count was 518 (421; 823)/mm3. The percentage of PLHIV with less than 200 CD4cells/mm3 was 4.7%. Three patients (10%) presented co-infection with HCV, and three patients (10%) had HBV co-infection. There were also no differences regarding outcomes between HIV-infected patients with undetectable and detectable HIV viral load.

This is the first national multicentre study that describes the clinical characteristics and outcomes of critical COVID-19 in PLHIV admitted to the ICU and compares them with the HIV-negative general population, concluding that the short- and medium-term prognosis is similar in PLHIV who are virological suppressed on ART and are not immunosuppressed (CD4200cells/mm3). In our study PLHIV accounted for approximately 0.5% of total hospitalised, critically ill COVID-19 cases in the ICU. This data is in line with previous studies.2–4 Despite PLHIV presenting higher APACHE-II scores at ICU admission, outcomes did not differ between groups before and after PSM (in-hospital, 30-, 90-day and 1-year mortality). Similar results were reported by previous studies in hospitalised patients.10–12 Data from a recent systemic review and meta-analysis that included data from 28 studies found no difference in the risk of death between HIV-infected patients and HIV-negative (OR, 1.09; 95% CI, 0.93–1.26; P>0.001).12

The major strengths of this study include its multicentre nature, the consecutive inclusion of all patients from each unit, thorough checking of data quality, and the high number of patients analysed and long-term follow-up. On the other hand, despite exhaustive propensity score analysis for underlying conditions, a possible limitation of the propensity score methods is their inability to control for unmeasured confounding. A main limitation is the small number of cases, precluding any robust conclusions. In particular, the analysis of outcomes using this size sample may have led to a large type-II error that prevents us from generalising our results. However, there are no similar studies investigating the severity and outcomes of critically ill patients with COVID-19 and HIV-infection, so this information is of value. Also, these results do not apply to PLHIV who are off ART and/or are immunosuppressed, because they are underrepresented in our study. Finally, as we examined real-world data, limitations associated to their observational nature and missing data should be considered.

Although limited by the small sample size, our main conclusion is that critically ill COVID-19 in non-immunosuppressed and virologically suppressed HIV-infected individuals seems to present neither a more severe disease nor a worse clinical outcome than HIV-negative patients. Further research in large cohorts should be encouraged to improve our knowledge on the impact of SARS-CoV-2 in critically ill HIV-infected patients.

Authors’ contributions

All the authors contributed to the conception and design, acquisition of data, drafting of the article, critical revision, and final approval of the manuscript.

Funding

Financial support was provided by Instituto de Salud Carlos III de Madrid (COV20/00110, ISCIII); Fondo Europeo de Desarrollo Regional (FEDER); “Una manera de hacer Europa”; Centro de Investigación Biomedica En Red–Enfermedades Respiratorias (CIBERES); and Donation program “estar preparados” UNESPA, Madrid, Spain. JMM received a personal 80:20 research grant from Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain, during 2017–23. CC received a grant from the Fondo de Investigación Sanitaria (PI19/00207), Instituto de Salud Carlos III, co-funded by the European Union.

Conflict of interests

JMM has received consulting honoraria and/or research grants from AbbVie, Angelini, Contrafect, Cubist, Genentech, Gilead Sciences, Jansen, Lysovant, Medtronic, MSD, Novartis, Pfizer, and ViiV Healthcare, outside the submitted work. All other authors have no conflicts.

Acknowledgments

We want to express our appreciation to all CIBERESUCICOVID members for their contribution to this work and their precious task and effort in clinical care and daily practice with all our patients.

Appendix A
CIBERESUCICOVID Project Investigators

Víctor D. Gumucio-Sanguino, Rafael Mañez: Hospital Universitario de Bellvitge, Barcelona. Jordi Solé-Violan, Felipe Rodríguez de Castro: Hospital Dr. Negrín, Las Palmas. Fernando Suarez-Sipmann: Hospital Universitario La Princesa, Madrid. Ruth Noemí Jorge García, María Mora Aznar: Hospital Nuestra Señora de Gracia, Zaragoza. Mateu Torres, María Martínez, Cynthia Alegre, Sofía Contreras: Hospital Universitari Vall d’Hebron, Barcelona, Javier Trujillano, Montse Vallverdú, Miguel León, Mariona Badía, Begoña Balsera, Lluís Servià, Judit Vilanova, Silvia Rodríguez, Neus Montserrat, Silvia Iglesias, Javier Prados, Sula Carvalho, Mar Miralbés, Josman Monclou, Gabriel Jiménez, Jordi Codina, Estela Val, Pablo Pagliarani, Jorge Rubio, Dulce Morales, Andrés Pujol, Àngels Furro, Beatriz García, Gerard Torres, José Javier Vengoechea, David de Gonzalo Calvo, Jessica González, Silvia Gómez: Hospital Universitari Arnau de Vilanova, Lleida. José M. Gómez: Hospital General Universitario Gregorio Marañón, Madrid. José Barberán: Hospital Universitario HM Montepríncipe. Guillermo M. Albaiceta, Lorena Forcelledo Espina, Emilio García Prieto, Paula Martín Vicente, Cecilia del Busto Martínez: Hospital Universitario Central de Asturias, Oviedo. Pablo Vidal: Complexo Hospitalario Universitario de Ourense, Ourense. José Luis García Garmendia, María Aguilar Cabello, Carmen Eulalia Martínez Fernández: Hospital San Juan de Dios del Aljarafe, Sevilla. Nieves Carbonell, María Luisa Blasco Cortés, Ainhoa Serrano Lázaro, Mar Juan Díaz: Hospital Clínic Universitari de València, Valencia. Luis Jorge Valdivia: Hospital Universitario de León, León. María Victoria Boado, David Iglesias: Hospital Universitario de Cruces, Barakaldo. Maria del Carmen de la Torre: Hospital de Mataró. Ignacio Martínez Varela, María Teresa Bouza Vieiro, Inés Esmorís Arijón: Hospital Universitario Lucus Augusti, Lugo. David Campi Hermoso, Rafaela Nogueras Salinas, Teresa Farre Monjo, Ramon Nogue Bou, Gregorio Marco Naya, Núria Ramon Coll: Hospital Universitari de Santa Maria, Lleida. Mercedes Catalán-González, Juan Carlos Montejo-González: Hospital Universitario 12 de Octubre, Madrid. Gloria Renedo Sanchez-Giron, Juan Bustamante-Munguira, Ramon Cicuendez Avila, Nuria Mamolar Herrera: Hospital Clínico Universitario, Valladolid. Raquel Almansa: Instituto de Investigación Biomédica de Salamanca (IBSAL). Víctor Sagredo: Hospital Universitario de Salamanca, Salamanca. Jose M. Añón, Alexander Agrifoglio, Lucia Cachafeiro, Emilio Maseda: Hospital Universitario La Paz-Carlos III, Madrid. Mariana Andrea Novo, Albert Figueras, Maria Teresa Janer, Laura Soliva, Marta Ocón, Luisa Clar, J Ignacio Ayestarán: Hospital Universitario Son Espases, Palma de Mallorca. Sandra Campos Fernández: Hospital Universitario Marqués de Valdecilla, Santander. Mireia Serra-Fortuny, Eva Forcadell-Ferreres, Inmaculada Salvador-Adell, Neus Bofill, Berta Adell-Serrano, María José Centelles-Serrano, Núria Casacuberta-Barberà, Luis Urrelo-Cerrón, Diego Franch-Llasat, Ferran Roche-Campo: Hospital Verge de la Cinta de Tortosa, Tarragona. Pablo Ryan Murúa, Covadonga Rodríguez Ruíz, Laura Carrión García, Juan I. Lazo Álvarez: Hospital Universitario Infanta Leonor, Madrid. Ana Loza-Vázquez, Desire Macias Guerrero: Hospital Universitario Virgen de Valme, Sevilla. Arturo Huerta, Daniel Tognetti: Clínica Sagrada Familia, Barcelona. Carlos García Redruello, David Mosquera Rodríguez, Eva María Menor Fernández, Sabela Vara Adrio, Vanesa Gómez Casal, Marta Segura Pensado, María Digna Rivas Vilas, Amaia García Sagastume: Hospital de Vigo, Vigo. Raul de Pablo Sánchez, David Pestaña Laguna, Tommaso Bardi: Hospital Universitario Ramón y Cajal, Madrid. Rosario Amaya Villar, Carmen Gómez González, Maria Luisa Gascón Castillo: Hospital Universitario Virgen del Rocío, Sevilla. José Garnacho-Montero, María Luisa Cantón-Bulnes: Hospital Universitario Virgen Macarena, Sevilla. Judith Marin-Corral, Cristina Carbajales Pérez: Hospital Álvaro Cunqueiro, Vigo. Ana Salazar Degracia, Judit Bigas, Rosana Muñoz-Bermúdez, Clara Vilà-Vilardel, Francisco Parrilla, Irene Dot, Ana Zapatero, Yolanda Díaz, María Pilar Gracia, Purificación Pérez, Andrea Castellví, Cristina Climent: Hospital del Mar, Barcelona. Lidia Serra, Laura Barbena, Iosune Cano: Consorci Sanitari del Maresme, Barcelona. Alba Herraiz, Pilar Marcos, Laura Rodríguez, Maria Teresa Sariñena, Ana Sánchez: Hospital Universitari Germans Trias i Pujol, Badalona. Alejandro Úbeda: Hospital Punta de Europa, Algeciras. María Cruz Martin Delgado: Hospital Universitario Torrejón-Universidad Francisco de Vitoria, Madrid. Elena Gallego, Juan Fernando Masa Jiménez: Hospital Universitario San Pedro de Alcántara, Cáceres. Gemma Gomà, Emili Díaz: Hospital Parc Taulí, Sabadell. Mercedes Ibarz, Diego De Mendoza: Hospital Universitari Sagrat Cor, Bacelona. Enric Barbeta, Victoria Alcaraz-Serrano, Joan Ramon Badia, Manuel Castella, Leticia Bueno, Andrea Palomeque, Pamela Conde, Javier Fernández, Karsa Kiarostami, Alexandre López-Gavín, Cecilia L. Mantellini, Carla Speziale, Nil Vázquez, Hua Yang, Minlan Yang, Carlos Ferrando, Pedro Castro, Marta Arrieta, Jose Maria Nicolas, Rut Andrea: Hospital Clinic, Barcelona. Marta Barroso, Raquel Pérez, Sergio Álvarez, Adrián Tormos: Barcelona Supercomputing Center, Barcelona. Luis Tamayo Lomas, Cesar Aldecoa, Rubén Herrán-Monge, José Ángel Berezo García, Pedro Enríquez Giraudo: Hospital Rio Hortega, Valladolid. Pablo Cardinal Fernández, Alberto Rubio López, Orville Báez Pravia: Hospitales HM, Madrid. Juan López Messa, Leire Pérez Bastida, Antonjo Alvarez Ruiz: Complejo Asistencial Universitario de Palencia, Palencia. José Trenado, Anna Parera Pous: Hospital Universitari MutuaTerrassa, Terrassa. Cristóbal Galbán, Ana López Lago, Eva Saborido Paz, Patricia Barral Segade: Hospital de Santiago de Compostela, Santiago. Ana Balan Mariño, Manuel Valledor Mendez: Hospital San Agustin, Avilés. Raúl de Frutos, Luciano Aguilera: Hospital Basurto, Basurto. Felipe Pérez-García, Esther López-Ramos, Ángela Leonor Ruiz-García, Belén Beteré: Hospital Universitario Principe Asturias, Alcala de Henares. Rafael Blancas: Hospital Universitario del Tajo, Aranjuez. Cristina Dólera, Gloria Perez Planelles, Enrique Marmol Peis, Maria Dolores Martínez Juan, Miriam Ruiz Miralles, Eva Perez Rubio, Maria Van der Hofstadt Martin-Montalvo, Tatiana Villada Warrington: Hospital Universitario Sant Joan d’Alacant, Alicante. Juan Carlos Pozo-Laderas: Hospital Universitario Reina Sofia. Ángel Estella, Sara Guadalupe Moreno Cano: Hospital de Jerez, Jerez. Federico Gordo: Hospital Universitario del Henares, Coslada. Basilisa Martínez Palacios: Hospital Universitario Infanta Cristina, Parla. Maite Nieto, Maria Teresa Nieto: Hospital de Segovia, Segovia. Sergio Ossa: Hospital de Burgos, Burgos. Ana Ortega: Hospital Montecelo, Pontevedra. Miguel Sánchez: Hospital Clínico, Madrid. Bitor Santacoloma: Hospital Galdakao, Galdakao.

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Equivalent merits as senior authors.

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