Articulo Mcroorganismos UCI 2019
Articulo Mcroorganismos UCI 2019
Articulo Mcroorganismos UCI 2019
2302
Key words: Healthcare associated infections, intensive care unit, active surveillance,
environmental surveillance, behavioral surveillance, pathogen genotyping
Parole chiave: Infezioni correlate all’assistenza, terapia intensiva, sorveglianza attiva,
sorveglianza ambientale, sorveglianza comportamentale, genotipizzazione dei
patogeni
Abstract
Background. Healthcare-associated infections (HAIs), or nosocomial infections, represent a significant
burden in terms of mortality, morbidity, length of stay and costs for patients hospitalized in intensive care
units (ICUs). Surveillance systems are recommended by national and international institutions to gather
data on HAIs in order to develop and evaluate interventions that reduce the risk of HAIs.
Study Design. Here we describe the methodology and the results of the surveillance system implemented in the
ICU of the Policlinico Umberto I, a large teaching hospital in Rome, from April 2016 to October 2018.
Methods. The multimodal infection surveillance system integrates four different approaches: i) active sur-
veillance of inpatients; ii) environmental microbiological surveillance; iii) surveillance of isolated microor-
ganisms; and iv) behavioral surveillance of healthcare personnel. Data were collected on catheter-related
bloodstream infections, ventilation-associated pneumonia, catheter-associated urinary tract infections and
primary bloodstream infections that developed in patients after 48 h in the ICU. For environmental surveil-
lance 14 points were selected for sampling (i.e. bed edges, medication carts, PC keyboards, sink faucets).
The system of active surveillance of HAIs also included surveillance of microorganisms, consisting of the
molecular genotyping of bacterial isolates by pulsed-field gel electrophoresis (PFGE). From 1 November
2016, monitoring of compliance with guidelines for hand hygiene (HH) and proper glove or gown use by
healthcare personnel was included in the surveillance system. After the first six months (baseline phase), a
multimodal intervention to improve adherence to guidelines by healthcare personnel was conducted with
the ICU staff.
Results. Overall, 773 patients were included in the active surveillance. The overall incidence rate of
device-related HAIs was 14.1 (95% CI: 12.2-16.3) per 1000 patient-days. The monthly device-related
HAI incident rate showed a decreasing trend over time, with peaks of incidence becoming progressively
1
Department of Public Health and Infectious Diseases, Sapienza University of Rome, Rome, Italy
2
Department of Anesthesiology and Critical Care, Policlinico Umberto I, Sapienza University of Rome, Rome, Italy
3
Anesthesia and Intensive Care Medicine, Policlinico di Sant’Orsola, Alma Mater Studiorum University of Bologna, Bo-
logna, Italy
400 G. Migliara et al.
lower. The most common bacterial isolates were Klebsiella pneumoniae (20.7%), Acinetobacter baumannii
(17.2%), Pseudomonas aeruginosa (13.4%) and Staphylococcus aureus (5.4%). Acinetobacter baumannii
and Klebsiella pneumoniae showed the highest proportion of isolates with a multidrug-resistant profile. A
total of 819 environmental samples were collected, from which 305 bacterial isolates were retrieved. The
most frequent bacterial isolates were Acinetobacter baumannii (27.2%), Staphylococcus aureus (12.1%),
Enterococcus faecalis (11.1%), Klebsiella pneumoniae (5.2%) and Pseudomonas aeruginosa (4.7%). All
Acinetobacter baumannii, Pseudomonas aeruginosa and Klebsiella pneumoniae environmental isolates
were at least multidrug-resistant. Genotyping showed a limited number of major PFGE patterns for both
clinical and environmental isolates of Klebsiella pneumoniae and Acinetobacter baumannii. Behavioral
compliance rates significantly improved from baseline to post-intervention phase.
Conclusions. By integrating information gathered from active surveillance, environmental microbiological
surveillance, surveillance of bacterial isolates and behavioral surveillance of healthcare personnel, the
multimodal infection surveillance system returned a precise and detailed view of the infectious risk and
microbial ecology of the ICU.
Table 1 - Formulas used to calculate the risk factors for healthcare associated infections (HAIs) and the incidence of
HAIs.
was carried out during the usual activities according to the 2009 WHO Hand Hygiene
of the unit twice a month using sterile Technical Reference Manual (22). The
swabs, after the sanitization interventions, tool investigated four possible types of
in compliance with ISO 18593: 2004 (16). interaction between healthcare personnel
All samples were analyzed according and patients (i.e. touching a patient, device
to standardized culture methods for the manipulation, touching patient surroundings,
determination of alert microorganisms. and invasive procedure or body fluid
Monthly reports were produced for the exposure), all of which had HH indications
Hospital Health Directorate containing both before and afterwards. Moreover, the
the following elements: description of the observers recorded glove use during each
main characteristics of the microorganisms; interaction and, for invasive procedure or
their antibiotic-resistance profile; the exact body fluid exposure, also gown use. As a
localization of the sampling site. These result, a total of thirteen recommendations
reports were also sent to the ICU and were were investigated; eight concerned HH
discussed with the ICU personnel in monthly indications, four concerned glove use and
meetings. one concerned gown use. Compliance with
HH was calculated as the proportion of the
Surveillance focused on bacterial isolates number of performed actions to the number
The system of active surveillance of HAIs of opportunities. Glove use was deemed
also included microorganism surveillance, appropriate during device manipulation and
where molecular typing of clinical and invasive procedure or body fluid exposure,
environmental bacterial isolates was while for touching patient surroundings
performed by pulsed-field gel electrophoresis and touching a patient, glove non-use was
(PFGE). The preparation of chromosomal considered appropriate. Gown use during
DNA, restriction digestion and PFGE an invasive procedure was evaluated as
were performed as previously described appropriate. After the first six months
(17-20). Interpretation of chromosomal (baseline phase), a multimodal intervention
DNA restriction patterns was based on to improve the adherence of healthcare
the criteria of Tenover et al. (21). Briefly, personnel to the guidelines was conducted
strains showing more than three fragment with the ICU staff. It was based on education
variations were assumed to represent major and training of all healthcare personnel
PFGE patterns, while one to three fragment coupled with performance feedback, as
differences were considered to represent described elsewhere (23). For the following
PFGE pattern subtypes. 12 months (post-intervention phase), the five
observers continued to collect data to monitor
Behavioral surveillance of healthcare healthcare personnel behaviour and assess
personnel the impact over time of the intervention.
In October 2016, three nurses and two Observations were grouped into trimesters
physicians were trained to perform direct for the analysis (two at baseline, four during
observations of compliance with HH and post-intervention phase).
proper glove or gown use during their daily
care activities in the ICU. The training Statistical analysis
focused on the purposes of observation and Counts and proportions of device-
the principles of HH and glove use. From related HAI, primitive BSI, clinical and
1st November 2016 to 30th April 2018, environmental bacterial strains and their
the five observers gathered data using an resistance profiles and PFGE patterns,
anonymous observation form developed antibiotics and observation for HH compliance
404 G. Migliara et al.
and gloves and gowns use were calculated. were hospitalized for medical reasons,
Rates for device-related HAI and primary 29% following a traumatic event and 18%
BSI, as well as proportions of devices and following surgery. The median length of
antibiotics use per 100 patient-days, were stay at the ICU was 10 days (interquartile
calculated as reported in table 1. range 5-22).
Overall, 379 HAIs occurred during the
study period, of which 166 were primary
Results BSIs (43.8%) and 213 were device-related
(56.2%). Regarding the latter, there were
Active surveillance focused on inpatients 73 VAPs (19.3%), 85 CAUTIs (22.4%)
Overall, 773 patients hospitalized in the and 55 CRBSIs (14.5%). Concerning the
ICU were included in the active surveillance exposure to risk factors, the proportion of
regime. The mean age was 58.3±18.7 years device-days to patient-days was 66% for
and 66.4% of the patients were male. A invasive ventilation, 99.9% for urinary
total of 388 patients (50.2%) accessed the catheterization and 95.2% for central venous
ICU through the Emergency Department, catheterization.
258 (33.4%) were transferred from other The monthly device-related HAI incident
wards of the same hospital, 73 (9.4%) from rate showed a decreasing trend over time, with
other hospitals and 47 (6.1%) were admitted peaks of incidence becoming progressively
directly to the ICU from the community. lower, ranging from 26.9 device-related
Fifty-two percent of the ICU patients HAIs per 1000 days in October 2016 to 4.9
Figure 1 - Device-related healthcare-associated infection (HAI) rates per 1000 patient-days in the Intensive Care Unit
of Umberto I Teaching Hospital of Sapienza University of Rome.
Multimodal surveillance of HAIs in ICU 405
in September 2018 (Figure 1). Overall, in without CRBSI (Figure 2B). The overall
the period of interest the incidence rate of CRBSI incidence rate was 4.3 (95% CI: 3.3-
device-related HAIs was 16.1 (95% CI: 14.0- 5.6) per 1000 central venous catheterization-
18.4) per 1000 patient-days. In more detail, days. CAUTIs showed a reduction in the
the monthly incidence rate of VAPs showed a last seven months of surveillance (Figure
slight decrease after a peak of 21.1 per 1000 2C). The overall CAUTI incidence rate
ventilation-days reached in March 2017 was 6.7 (95%CI: 5.4-8.3) per 1000 urinary
(Figure 2A). The overall VAP incidence catheterization-days. Primary BSIs showed
rate was 8.3 (95% CI: 6.5-10.5) per 1000 a more stable trend over time with few
ventilation-days. The CRBSI rate did not peaks (Figure 2D). The overall primary BSI
showed a recognizable monthly trend, with incidence rate was 12.5 (95% CI: 10.9-14.2)
incident peaks alternating with months per 1000 patient-days (Figure 2D).
Figure 2 - Specific device-related healthcare-associated infection (HAI) rates and primary bloodstream infection rates
in the Intensive Care Unit of Umberto I Teaching Hospital of Sapienza University of Rome: A) Ventilation-associated
pneumonia (VAP) rate per 1000 ventilation-days; B) Catheter-related bloodstream infections (CRBSI) rate per 1000
central venous catheterization-days; C) Catheter-associated urinary tract infection (CAUTI) rate per 1000 urinary
catheterization-days; D) Primary bloodstream infection rate per 1000 patient-days.
406 G. Migliara et al.
Figure 3 - Days of use of antibiotic classes over 100 patient-days, expressed as a percentage, in the Intensive Care
Unit of Umberto I Teaching Hospital of Sapienza University of Rome.
Figure 4 - Resistance profiles of clinical and environmental isolates for Acinetobacter baumannii, Pseudomonas
aeruginosa, Klebsiella pneumoniae and Staphylococcus aureus in the Intensive Care Unit of Umberto I Teaching
Hospital of Sapienza University of Rome.
Legend: NA, non-assessable; N-MDR, non-multidrug resistant; MDR, multidrug resistant; MR, methicillin-resistant;
XDR, extensively drug resistant; PDR, pandrug resistant. * clinical isolates; § environmental isolates.
Multimodal surveillance of HAIs in ICU 407
The most frequently prescribed classes XDR, and 13.1% PDR). All Acinetobacter
of antibiotics were polymyxins (36.0% baumannii, Pseudomonas aeruginosa and
of patient-days), carbapenems (31.0% Klebsiella pneumoniae environmental
of patient-days), penicillins (28.0%), isolates were at least MDR (Figure 4),
antifungals (22.0%), extended-spectrum whereas 59.4% of Staphylococcus aureus
cephalosporins (15.0%), glycopeptides isolates were methicillin-resistant and 26.5%
(13.0%), glycylcyclines (12.0%) and of E. faecalis isolates where glycopeptide-
aminoglycosides (10.0%) (Figure 3). resistant.
Overall, 477 pathogens were responsible The sampling points in the ward most
for 380 HAIs that occurred during the likely to yield bacterial isolates were bed
study period. The most common bacterial edges (91 positive samples), medication
pathogens were Klebsiella pneumoniae carts (62 positive samples) and mechanical
(20.7%), Acinetobacter baumannii (17.2%), ventilation system touchscreens (59 positive
Pseudomonas aeruginosa (13.4%) and samples). Fewer positive samples were
Staphylococcus aureus (5.4%) (Figure found on the remaining surfaces sampled:
4). Concerning the resistance profile, PC keyboard and mouse (43 positive
Acinetobacter baumannii and Klebsiella samples); sink faucets (30 positive samples);
pneumoniae showed the highest proportion blood gas analyser touchscreen (20 positive
of isolates with a MDR or more severe samples).
profile (100% of Acinetobacter baumannii
and 94.0% of Klebsiella pneumoniae Surveillance of Bacterial Isolates
isolates), whereas Pseudomonas aeruginosa A total of 218 clinical and 67
showed a more mixed profile, with 52.9% environmental isolates of Acinetobacter
of the isolates not MDR. More than 50% baumannii and Klebsiella pneumoniae from
of Staphylococcus aureus isolates were the ICU were typed by macrorestriction
methycillin-resistant (MRSA) (Figure analysis of chromosomal DNA and PFGE.
4). Overall, 230 out of the 477 pathogens Genotyping of the 159 clinical isolates
responsible for HAIs (48.2%) were at least of Acinetobacter baumannii showed six
MDR (specifically, 15.1% MDR, 25.6% major PFGE patterns: PFGE pattern B was
XDR and 7.5% PDR). found in 107 isolates (67.3%), followed
by PFGE pattern A (21 isolates, 13.2%),
Environmental microbiological PFGE pattern C (20 isolates, 12.6%),
surveillance PFGE pattern E (five isolates, 3.1%), PFGE
During the study period, a total of 60 pattern F (four isolates, 2.5%) and PFGE
environmental microbiological monitoring pattern D (two isolates, 1.2%). For the
campaigns were performed and 819 samples environmental isolates, three major PFGE
were collected, which yielded 305 bacterial patterns were identified: PFGE pattern
isolates. Acinetobacter baumannii was the B (17 isolates, 47.2%), PFGE pattern A
most frequently isolated bacterial species (14 isolates, 38.9%) and PFGE pattern
(27.2%), followed by Staphylococcus C (five isolates, 13.9%). PFGE patterns
aureus (12.1%), Enterococcus faecalis D, E and F were found in clinical but not
(11.1%), Klebsiella pneumoniae (5.2%) and in environmental isolates. Genotyping
Pseudomonas aeruginosa (4.7%) (Figure of the 56 clinical isolates of Klebsiella
4). Environmental isolates showed a more pneumoniae revealed 14 major PFGE
resistant profile than clinical isolates, since patterns: PFGE pattern A was retrieved in 37
213 out of 305 isolates (69.8%) were at least isolates (66.1%), followed by PFGE pattern
MDR (specifically, 38.3% MDR, 18.4% B (four isolates, 7.1%), and PFGE patterns
408 G. Migliara et al.
nosocomial infection and of the microbial iii) sorveglianza focalizzata sui microrganismi isolati e,
ecology in the ICU at the Policlinico iv) sorveglianza comportamentale del personale sanitario.
Sono state considerate ICA le batteriemie correlate a
Umberto I Teaching Hospital. However, catetere (CRBSI), le polmoniti associata a ventilazione
the results obtained in terms of reduction (VAP), le infezioni del tratto urinario associate a catetere
of HAIs suggest that greater efforts should (CAUTI) e le batteriemie primitive che si sono verificate
be made in the implementation of targeted dopo 48 ore dall’ammissione. Per la sorveglianza ambien-
interventions, such as the application of tale sono stati selezionati 14 punti per il campionamento
bundles for the reduction of the risk infection (bordi del letto, carrelli per farmaci, tastiere per PC,
rubinetti dei lavandini). Il sistema di sorveglianza attiva
due to the use of invasive devices, together
delle ICA ha incluso inoltre una sorveglianza focalizzata
with ongoing educational interventions sui microrganismi, basata sulla genotipizzazione moleco-
for healthcare personnel, in parallel with lare degli isolati batterici attraverso l’elettroforesi su gel
continuous surveillance. a campo pulsato (PFGE). Dal 1° novembre 2016 è stato
integrato nel sistema di sorveglianza il monitoraggio del
rispetto delle linee guida sull’igiene delle mani (HH) e
Declarations dell’uso corretto di guanti e camici da parte del personale
sanitario. Dopo i primi sei mesi, è stato condotto con il
Competing interests. The authors declare that they have personale dell’UTI un intervento multimodale volto a
no competing interests. migliorare l’aderenza alle linee guida.
Funding. No funding was received for this study. Risultati. Complessivamente, 773 pazienti sono stati
inclusi nella sorveglianza attiva. Il tasso di incidenza
Acknowledgments. We wish to thank all those resident totale delle ICA correlate a dispositivi è stato di 14,1 (IC
physicians in Public Health of the Sapienza University 95%: 12,2-16,3) per 1000 giorni di degenza. L’incidenza
of Rome whose daily work makes it possible to carry out mensile delle ICA correlate a dispositivi ha mostrato
active surveillance of HAI: Aurora Angelozzi; Fulvio Ca- un andamento decrescente nel tempo, con picchi di in-
stellani; Sara Cianfanelli; Valeria D’Egidio; Pasquale de cidenza progressivamente inferiori a quelli precedenti.
Soccio; Claudia Isonne; Lorenza Lia; Annamaria Mele; Gli isolati batterici più comuni sono stati Klebsiella
Grazia Pia Prencipe; Livia Maria Salvatori. pneumoniae (20,7%), Acinetobacter baumannii (17,2%),
Pseudomonas aeruginosa (13,4%) e Staphiylococcus
aureus (5,4%). Acinetobacter baumannii e Klebsiella
Riassunto pneumoniae hanno mostrato la più alta percentuale di
isolati con un profilo multiresistente. Sono stati raccolti
Sorveglianza Multimodale delle Infezioni Correlate un totale di 819 campioni ambientali, con il recupero di
all’Assistenza in una Unità di Terapia Intensiva di 305 isolati batterici. Gli isolati batterici più frequenti
un Grande Policlinico sono stati Acinetobacter baumannii (27,2%), Staphiylo-
coccus aureus (12,1%), Enterococcus faecalis (11,1%),
Introduzione. Le infezioni correlate all’assistenza Klebsiella pneumoniae (5,2%) e Pseudomonas aerugi-
sanitaria (ICA) rappresentano una problematica signi- nosa (4,7%). Tutti gli isolati ambientali di Acinetobac-
ficativa in termini di mortalità, morbilità, durata del ter baumannii, Pseudomonas aeruginosa e Klebsiella
soggiorno e costi per i pazienti ospedalizzati nelle unità pneumoniae erano multiresistenti. La genotipizzazione
di terapia intensiva (UTI). I sistemi di sorveglianza sono ha mostrato un numero limitato di pattern PGFE per
raccomandati da istituzioni nazionali e internazionali al Klebsiella pneumoniae e Acinetobacter baumannii sia
fine di raccogliere dati sulle ICA che possano permettere negli isolati clinici che in quelli ambientali. Il tasso di
di elaborare e valutare interventi volti alla riduzione del aderenza alle linee guida sul lavaggio delle mani e l’uti-
rischio di ICA. lizzo di guanti e camici è migliorato significativamente
Disegno dello studio. In questo articolo descriviamo tra pre- e post-intervento.
la metodologia e i risultati del sistema di sorveglianza Conclusioni. Attraverso l’integrazione delle infor-
implementato nella UTI del Policlinico Umberto I, un mazioni raccolte dalla sorveglianza attiva, dalla sorve-
grande ospedale universitario di Roma, da aprile 2016 glianza microbiologica ambientale, dalla sorveglianza
a ottobre 2018. focalizzata sugli isolati batterici e dalla sorveglianza
Metodi. Il sistema multimodale di sorveglianza delle comportamentale del personale sanitario, l’applicazione
infezioni è consistito nell’integrazione di quattro diversi di questo modello restituisce una visione precisa e det-
approcci: i) sorveglianza attiva incentrata sui pazienti tagliata del rischio infettivo e dell’ecologia microbica
ricoverati; ii) sorveglianza microbiologica ambientale; all’interno dell’UTI.
Multimodal surveillance of HAIs in ICU 411
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Corresponding author: Giuseppe Migliara, MD, Department of Public Health and Infectious Diseases, Sapienza
University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy
e-mail: giuseppe.migliara@uniroma1.it