Scientific Letter
Health care-associated infections in patients with COVID-19 pneumonia in COVID critical care areas
Infecciones relacionadas con la asistencia sanitaria en pacientes con neumonía COVID-19 en áreas de cuidados intensivos COVID
J. Marin-Corrala,b,c,1,
, S. Pascual-Guardiac,d,e,1, R. Muñoz-Bermúdeza,b, A. Salazar-Degraciaa,b, C. Climenta,b, C. Vilà-Vilardella,b, M. Acera,b, M. Picornella,b, M.I. Restrepoc,f, J.R. Masclansa,b,g,2, F. Álvarez-Lermaa,b,g,2
Autor para correspondencia
a Critical Care Department, Hospital del Mar, Barcelona, Spain
b Critical Illness Research Group (GREPAC), Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), Barcelona, Spain
c Division of Pulmonary Diseases & Critical Care Medicine, University of Texas Health San Antonio, San Antonio, TX, USA
d Respiratory Department, Hospital del Mar, IMIM, Barcelona, Spain
e Centro de Investigación Biomédica en Red de Enfermedades Respiratorias (CIBERES), Spain
f Section of Pulmonary & Critical Care Medicine, South Texas Veterans Health Care System, San Antonio, TX, USA
g Department of Medicine, Universitat Autònoma de Barcelona (UAB), Barcelona, Spain
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Marin-Corral, S. Pascual-Guardia, R. Muñoz-Bermúdez, A. Salazar-Degracia, C. Climent, C. Vilà-Vilardell, M. Acer, M. Picornell, M.I. Restrepo, J.R. Masclans, F. Álvarez-Lerma" "autores" => array:11 [ 0 => array:4 [ "nombre" => "J." "apellidos" => "Marin-Corral" "email" => array:1 [ 0 => "jmarincorral@gmail.com" ] "referencia" => array:5 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] 3 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">1</span>" "identificador" => "fn0005" ] 4 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "S." 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"apellidos" => "Masclans" "referencia" => array:4 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">g</span>" "identificador" => "aff0035" ] 3 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">2</span>" "identificador" => "fn0010" ] ] ] 10 => array:3 [ "nombre" => "F." "apellidos" => "Álvarez-Lerma" "referencia" => array:4 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">g</span>" "identificador" => "aff0035" ] 3 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">2</span>" "identificador" => "fn0010" ] ] ] ] "afiliaciones" => array:7 [ 0 => array:3 [ "entidad" => "Critical Care Department, Hospital del Mar, Barcelona, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Critical Illness Research Group (GREPAC), Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), Barcelona, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Division of Pulmonary Diseases & Critical Care Medicine, University of Texas Health San Antonio, San Antonio, TX, USA" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Respiratory Department, Hospital del Mar, IMIM, Barcelona, Spain" "etiqueta" => "d" "identificador" => "aff0020" ] 4 => array:3 [ "entidad" => "Centro de Investigación Biomédica en Red de Enfermedades Respiratorias (CIBERES), Spain" "etiqueta" => "e" "identificador" => "aff0025" ] 5 => array:3 [ "entidad" => "Section of Pulmonary & Critical Care Medicine, South Texas Veterans Health Care System, San Antonio, TX, USA" "etiqueta" => "f" "identificador" => "aff0030" ] 6 => array:3 [ "entidad" => "Department of Medicine, Universitat Autònoma de Barcelona (UAB), Barcelona, Spain" "etiqueta" => "g" "identificador" => "aff0035" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Infecciones relacionadas con la asistencia sanitaria en pacientes con neumonía COVID-19 en áreas de cuidados intensivos COVID" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1466 "Ancho" => 2508 "Tamanyo" => 242274 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Prevalence (A) and rates (B) of the different types of HAI in patients with pneumonia secondary to COVID-19 admitted to the COVID-19 critical care area.</p> <p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">HAI: health-care associated infection; BACT: bacteraemia; CRBSI: catheter-related bloodstream infection; BUO: bacteraemia of unknown origin; SB: secondary bacteraemia; UTI: urinary tract infection; VLRTI: ventilator-associated lower respiratory tract infection; VAT: ventilator-associated tracheobronchitis; VAP: ventilator-associated pneumonia; IPU: infected pressure ulcer; TSI: tracheostomy site infection.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">The first wave of the COVID-19 pandemic challenged health systems worldwide. Its high capacity to generate critical patients required rapid expansion of beds beyond the classical intensive care unit (ICU) to other spaces termed “expanded ICU (eICU)”, as well as repurposing and redistribution of resources, personnel from other areas and specialised personnel. This new situation made it more difficult to comply with the recommendations for prevention of health care-associated infections (HAIs) what added to the higher exposition of patients to immunosuppressive treatments or requiring long ICU stays, made them more susceptible to HAIs. Several studies have shown higher rates of HAIs in COVID-19, but none of them as a principal factor in critically ill patients.<a class="elsevierStyleCrossRefs" href="#bib0065"><span class="elsevierStyleSup">1–8</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Our aims were to determine the rates, aetiology, risk factors and impact of HAIs diagnosed in critically ill patients with COVID-19 pneumonia admitted to the different COVID-19 ICUs. It is a retrospective, observational, single-centre study. We evaluated all nosocomial bacteraemias (bloodstream infections or BSI), urinary tract (UTI), respiratory (VLRTI), pressure ulcer (IPU) and tracheostomy site infections (TSI) in patients with COVID-19 pneumonia admitted to one COVID-19 ICU (principal ICU or one of our 3 eICUs). The HAI incidence rates (IR) were analysed according to the patients’ location. Risk factors for HAI were identified from multivariate analysis. ICU length of stay (LOS) and mortality were analysed according to the number of HAIs (0, 1, 2, or ≥3). More details are shown in the <a class="elsevierStyleCrossRef" href="#sec0010">online supplemental material</a>.</p><p id="par0015" class="elsevierStylePara elsevierViewall">A total of 158 patients were admitted to the ICUs and 132 (83.5%) were included (<a class="elsevierStyleCrossRef" href="#sec0010">Figure 1e</a>). Transfer between the different ICUs are shown in <a class="elsevierStyleCrossRef" href="#sec0010">Figure 2e</a>. Eighty-nine HAIs (IR 42.0<span class="elsevierStyleHsp" style=""></span>episodes/1000d) were identified in 39 patients (29.5%). The most common HAIs were BSI (IR 16.5), UTI (IR 12.7) and VLRTI (IR 11.6) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). The original ICU had the lowest rates of HAI (<a class="elsevierStyleCrossRef" href="#sec0010">Figure 3e</a>). The distribution of different HAIs over time and in the different ICUs is shown in <a class="elsevierStyleCrossRef" href="#sec0010">Figure 4Ae and 4Be</a>. Characteristics of patients according to HAIs are shown in <a class="elsevierStyleCrossRef" href="#sec0010">Table 1e</a>. Only renal replacement therapy (RRT, OR 8.74 [1.40–54.49]) and length of ICU stay (OR 1.11 [1.03–1.21]) were independently associated with HAI. One-hundred and fourteen microorganisms were identified, the most common being <span class="elsevierStyleItalic">P. aeruginosa</span> (18.4%), enterococci (17.5%) and <span class="elsevierStyleItalic">Candida</span> spp (25.0%) (<a class="elsevierStyleCrossRef" href="#sec0010">Figure 5e and Table 2e</a>). Of all the causative organisms isolated, 18.4% were MDR (<a class="elsevierStyleCrossRef" href="#sec0010">Table 3e</a>). The distribution of the microorganisms over time for each of the HAIs in each unit is shown in <a class="elsevierStyleCrossRef" href="#sec0010">Figure 4Ce</a>. Among patients with HAI while in the ICU, 69.2% had more than one (<a class="elsevierStyleCrossRef" href="#sec0010">Figure 6e</a>) and the ICU LOS and mortality showed statistically significant differences according to the number of HAIs present (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">There are multiple reasons that could explain the increase in HAIs in the population with COVID-19 admitted to ICUs. Structural reasons (opening of new ICU beds in other spaces in the hospital or eICU), organisational reasons (incorporation of new teams of doctors and nurses not previously trained in critical care) and functional reasons (changes in the standards of patient care, use of PPI during long shifts) may all play a role and make it difficult to adhere to the recommendations proposed by different scientific societies for HAI prevention.<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">9</span></a> These aspects of care and organisation varied in the different units of the COVID ICUs and would explain the differences between them in the rates and time until onset of HAI. In addition, the need for an eICU itself meant increased transfer of patients between ICUs, which could have predisposed the development of HAI. Finally, individual patient susceptibility to infection could also have played a role in those patients with more than one HAI.</p><p id="par0025" class="elsevierStylePara elsevierViewall">Characteristics of patients with COVID-19 who developed HAI, were similar to those published in other series of patients requiring ICU admission.<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">10–12</span></a> Their profile was that of older age, with increased illness severity, a history of stroke and/or diabetes, need for invasive devices or proning and RRT. On tests from the first 24<span class="elsevierStyleHsp" style=""></span>h in ICU, no differences were observed in markers of immune response, inflammation or altered clotting, which indicates that in the onset of HAI, exposure to external risk factors are more relevant. RRT was identified as an individual risk factor for HAI. This could be related to the need for more than one venous catheter and the manipulations involved in placing and managing them. Among 16 patients who required RRT, 10 patients (62.5%) had at least one episode of catheter related BSI (CRBSI) or bacteriemia of unknown origin (12 episodes in total). BSI post vascular catheter placement in patients that require RRT may indicate an area of quality improvement at the time of catheter insertion and subsequent care.</p><p id="par0030" class="elsevierStylePara elsevierViewall">Among the microorganisms identified as causing HAIs, many were part of the primary and secondary endogenous microflora (species of <span class="elsevierStyleItalic">Candida</span>, <span class="elsevierStyleItalic">Enterococcus</span> and enterobacterales, in particular <span class="elsevierStyleItalic">K. pneumoniae)</span> while those associated with cross transmission or reservoirs were less common. Endogenous flora was particularly common in UTIs and primary bacteraemias, suggesting spread from the gut flora. In contrast, <span class="elsevierStyleItalic">P. aeruginosa</span>, the most prevalent pathogen in our hospital for colonisation or nosocomial infection was associated with cross transmission particularly in patients who developed VLRTIs. Surprisingly, the presence of MDR pathogens was low and heterogeneous, and there were no identified outbreaks.</p><p id="par0035" class="elsevierStylePara elsevierViewall">Total ICU LOS conditioned the development of HAIs. Patients who developed one or more HAIs had longer total ICU LOS, although in most cases ICU LOS prior to HAI and total ICU LOS in patients without HAI were similar. Presence of HAI and total number of HAIs per patient were associated with higher ICU mortality. Unfortunately, 20% of patients who died in the ICU had a diagnosis of HAI within 72<span class="elsevierStyleHsp" style=""></span>h of death.</p><p id="par0040" class="elsevierStylePara elsevierViewall">In conclusion, the high rates of HAI, the differences observed between the main ICU and the three expanded units, the movement of patients between ICUs and the significant clinical impact and use of resources indicate that we must plan specific interventions to minimise such patterns in future pandemics and epidemics.</p></span>" "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:2 [ 0 => array:3 [ "etiqueta" => "1" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">These authors contributed equally to the study.</p>" "identificador" => "fn0005" ] 1 => array:3 [ "etiqueta" => "2" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">These authors contributed equally to the study.</p>" "identificador" => "fn0010" ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "<p id="par0050" class="elsevierStylePara elsevierViewall">The following are the supplementary data to this article:<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>" "etiqueta" => "Appendix A" "titulo" => "Supplementary data" "identificador" => "sec0010" ] ] ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1466 "Ancho" => 2508 "Tamanyo" => 242274 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Prevalence (A) and rates (B) of the different types of HAI in patients with pneumonia secondary to COVID-19 admitted to the COVID-19 critical care area.</p> <p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">HAI: health-care associated infection; BACT: bacteraemia; CRBSI: catheter-related bloodstream infection; BUO: bacteraemia of unknown origin; SB: secondary bacteraemia; UTI: urinary tract infection; VLRTI: ventilator-associated lower respiratory tract infection; VAT: ventilator-associated tracheobronchitis; VAP: ventilator-associated pneumonia; IPU: infected pressure ulcer; TSI: tracheostomy site infection.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2420 "Ancho" => 2508 "Tamanyo" => 276534 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Outcomes: length of ICU stay and mortality in patients with COVID-19 pneumonia admitted to the COVID-19 intensive care units.</p> <p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">***<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.001 vs No HAI; **<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>≤<span class="elsevierStyleHsp" style=""></span>0.05 vs No HAI; <span class="elsevierStyleSup">#</span><span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.05 vs 2 HAIs.</p>" ] ] 2 => array:5 [ "identificador" => "upi0005" "tipo" => "MULTIMEDIAECOMPONENTE" "mostrarFloat" => false "mostrarDisplay" => true "Ecomponente" => array:2 [ "fichero" => "mmc1.pdf" "ficheroTamanyo" => 908792 ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:12 [ 0 => array:3 [ "identificador" => "bib0065" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Patient characteristics, clinical course and factors associated to ICU mortality in critically ill patients infected with SARS-CoV-2 in Spain: a prospective, cohort, multicentre study" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "C. 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