Scholarly article on topic 'The impact of hospital-acquired infections with multidrug-resistant bacteria in an oncology intensive care unit'

The impact of hospital-acquired infections with multidrug-resistant bacteria in an oncology intensive care unit Academic research paper on "Health sciences"

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{Cancer / Surveillance / "Intensive care unit" / "Hospital-acquired infection" / "Multidrug-resistant bacteria" / Mortality}

Abstract of research paper on Health sciences, author of scientific article — P. Cornejo-Juárez, D. Vilar-Compte, C. Pérez-Jiménez, S.A. Ñamendys-Silva, S. Sandoval-Hernández, et al.

Summary Objective To describe overall site-specific hospital-acquired infection (HAI) rates and to describe the microbiological and antibiotic resistance profiles of infecting pathogens, together with their impact on multidrug-resistant (MDR) bacteria-associated mortality. Methods We conducted a 5-year retrospective descriptive study of HAI in patients in the intensive care unit (ICU) of a cancer center in Mexico from January 2007 to December 2011. The following information was collected: patient characteristics and comorbidities, data related to the neoplasm and its treatment, microbiology, and the resistance pattern of all isolates. Results During the study period, 1418 patients were admitted to the ICU; 134 of them developed 159 infections, with an incidence of 11.2/100 hospitalized patients and 32.2/per 1000 patient-days. Two hundred sixty-six microorganisms were isolated. The overall prevalence of MDR-HAI was 39.5%. The most frequent organisms were as follows: 54 (20%) Escherichia coli (94.4% of these were extended-spectrum beta-lactamase producers), 32 (12%) Staphylococcus aureus (90.6% of these were methicillin-resistant), 32 (12%) Enterococcus faecium (18.7% of these were vancomycin-resistant), and 20 (6%) Acinetobacter baumannii (all were MDR). Among patients admitted to the ICU, 252 (17.8%) died. Death was related to the HAI in 58 (23%) of these patients (p <0.001) and 51 (88%) had a MDR organism isolated (p =0.05). Conclusions The emergence of MDR bacteria poses a difficult task for physicians, who have limited therapeutic options. Critically ill cancer patients admitted to the ICU are at major risk of a bacterial MDR-HAI that will impact adversely on mortality.

Academic research paper on topic "The impact of hospital-acquired infections with multidrug-resistant bacteria in an oncology intensive care unit"

Accepted Manuscript

Title: The impact of hospital acquired infections with multidrug-resistant bacterial at an oncological intensive care unit

Author: P Cornejo-Juarez D Vilar-Compte C Perez-Jimenez SA Namendys-Silva S Sandoval-Hernandez P Volkow-Fernandez

PII: DOI:

Reference:

S1201-9712(14)01740-8 http://dx.doi.Org/doi:10.1016/j.ijid.2014.12.022 IJID 2211

To appear in:

International Journal of Infectious Diseases

Received date: Revised date: Accepted date:

8-8-2014

8-11-2014

15-12-2014

Please cite this article as: Cornejo-Juarez P, Vilar-Compte D, Perez-Jimenez C, Namendys-Silva SA, Sandoval-Hernandez S, Volkow-Fernandez P, The impact of hospital acquired infections with multidrug-resistant bacterial at an oncological intensive care unit, International Journal of Infectious Diseases (2014), http://dx.doi.org/10.1016Zj.ijid.2014.12.022

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Highlights

• Multidrug resistant bacteria (MDR) are an increasing health concern worldwide.

• Hospital-acquired infections (HAI) are a major problem in critical care patients.

• Patients with cancer have an increased risk of HAI and higher associated mortality.

• MDR pathogens are frequently involved in this setting.

• Antimicrobial stewardship is a key factor for prevention of HAI in the ICU. Infections related with MDR bacteria increase mortality.

The impact of hospital acquired infections with multidrug-resistant bacterial

at an oncological intensive care unit

Cornejo-Juárez P1*, Vilar-Compte D1, Pérez-Jiménez C1, Ñamendys-Silva SA2, Sandoval-Hernández S1 and Volkow-Fernández P1

department of Infectious Disease, 2Department of Critical Care Medicine, Instituto Nacional de Cancerología, Mexico City, Mexico

Corresponding author: Instituto Nacional de Cancerología. Av. San Fernando No. 22, Col. Sección XVI, Tlalpan, 14080 México, D.F., México. E-mail: patcornejo@yahoo.com

Abstract

Purpose: To describe overall site-specific Hospital acquired infections (HAI) rates, and to describe the microbiological and antibiotic resistance profiles of infecting pathogens, together with their impact on multidrug-resistant bacteria-associated mortality.

Methods: We conducted a 5-year retrospective descriptive study of HAI in patients at the ICU from January 2007 to December 2011 at a cancer center in Mexico. Patients' characteristics and comorbidities, data related with the neoplasia and its treatment, microbiology, and the resistant pattern for all isolates were collected. Results: During the study period, 1,418 patients were admitted to the ICU; 134 of them developed 159 infections, with an incidence of 11.2/100 hospitalized patients and 32.2/per 1,000 patient-days. Two hundred sixty six microorganisms were isolated. Overall prevalence of MDR-HAI was 39.5%; the most frequent organisms were as follows: 54 (20%) Escherichia coli, 94.4% of these were extended-spectrum beta-lactamases producers; 32 (12%) Staphylococcus aureus, 90.6% of these methicillin-resistant; 32 (12%) Enterococcus faecium, 18.7% of these vancomycin-resistant; and 20 (6%) Acinetobacter baumannii, all of these were MDR. Among patients admitted to the ICU, 252 (17.8%) died, 58 (23%) of these related to HAI (p <0.001) and 51 (88%) with an MDRB isolated (p=0.05). Conclusions: The emergence of MDRB poses a difficult task for physicians, who have limited therapeutic options. Critically ill cancer patients admitted to the ICU are at major risk of HAI-MDRB infection that will impact adversely on mortality.

Key words: Cancer; Surveillance; Cancer; Intensive care unit; Hospital acquired

infection; Multidrug resistant bacteria; Mortality.

Introduction

Hospital acquired infections (HAI) have been recognized for over a century as a critical problem affecting the quality of health care and a major source of adverse health care outcomes [1,2]. The emergence of multidrug-resistant bacteria (MDRB) has become a public health problem, creating a new burden on medical care in hospitals, particularly for patients admitted to intensive care units (ICU) [1]. In critical care units, there is extensive antimicrobial use imposing a selective pressure and promoting the emergence of MDRB [1]. In addition to this, ICU patients have an increased risk of infections due to their underlying diseases or conditions, impaired immunity, and exposure to multiple invasive devices (mechanical ventilation, central venous catheters [CVC], and urinary tract catheters) [1,3,4]. The incidence of ICU-HAI is 5-10 times higher than HAI rates from general ward patients [5]. HAI in the ICU have been associated with increased morbidity, mortality, and costs [1,6,7].

The aim of this study was to describe the incidence of HAI at an oncological ICU and to describe the microbiological and antibiotic resistance profiles of infecting pathogens, together with their impact on MDRB-associated mortality.

Methods

The National Cancer Institute of Mexico (INCan) is a 135-bed referral, teaching hospital located in Mexico City for adult patients with cancer, with an average of 170,000 medical visits per year; there are 7,500 hospital discharges, 1,400 long-

indwelling CVC placements, 34,000 chemotherapy-infusion sessions, and >3,500 major surgery procedures performed each year. Efforts have been carried out to improve the outcome of cancer patients admitted to the six-bed medical and surgical ICU [8], including better selection of patients and standardized care; nonetheless, mortality trends have increased over the past years in parallel with the increase of MDRB-HAI (Table 1).

We conducted a 5-year retrospective descriptive study of HAI in patients at the ICU from January 2007 to December 2011. Data was obtained from ICU daily reports, infection control surveillance forms, microbiology laboratory reports, and patients' medical charts. Patients' characteristics and comorbidities, data related with the neoplasia and its treatment, microbiology, and the resistant pattern for all isolates were collected. The Sequential Organ Failure Assessment (SOFA) score [9] at ICU admission and at infection detection, length of ICU stay, number of ventilator-days, days of CVC stay, and urinary tract catheter-days were also reviewed. HAI were defined using Centers for Disease Control and Prevention criteria (CDC, 2008) [10].

Cultures from blood, urine, tracheobronchial secretions, and from any other site with clinical suspicion of infection were obtained. Bacteria were cultured using standard microbiological methods. Antimicrobial susceptibility testing was performed by the automated BD Phoenix™ (USA) and the Kirby-Bauer disk diffusion technique (Clinical Laboratory Standards Institute, CLSI) [11]. Antimicrobial treatment was considered appropriate when the patient received an

antibiotic for which the isolated bacteria was susceptible, during the first 24 h of clinical infection and if the patient had received this for >72 h [12].

Infections occurring at more than one site in the same patient were reported as separate infection events, unless the same bacterium was isolated at the same time. Clinical outcome was considered until hospital discharge or death. For the purposes of this investigation, death was classified as HAI-attributable and non-HAI-infection-related according to medical staff that certified the death, along with a clinical chart review by at least two of the authors of the current manuscript.

MDRB included: Methicillin-resistant Staphylococcus aureus (MRSA); Vancomycin-resistant Enterococcus faecium (VRE); Extended-spectrum beta-lactamases (ESBL) Escherichia coli and Klebsiella spp.; Pseudomonas aeruginosa, Acinetobacter spp. and other Gram-negative bacteria were considered multidrug-resistant (MDR) if showed resistance to fluoroquinolones, cephalosporins, and carbapenems.

Statistical analysis

Categorical variables were compared using the chi-square or the Fisher exact test as appropriate. Continuous data were compared by means of the Mann-Whitney U test or by the Student t test according to the data distribution. Odds ratios (OR) with 95% Confidence intervals (95% CI) were calculated. P values <0.05 were considered statistically significant. Device utilization ratios, site-specific incidence rates per 100 patients, and site-specific incidence densities per 1,000 days at risk or per 1,000 patient-days were calculated. Data was analyzed using Epi-Info (ver.

7) and STATA (ver. 12) statistical software.

Results

During the study period there were 1,418 admissions to the ICU. There were 159 HAI in 134 patients (110 with one, 23 with two, and 1 with three HAI episodes, respectively). The overall incidence of HAI at the ICU was 11.2 per 100 patients, and 32.2/1,000 patient-days (Table 1).

Median age was 50 years, 65 patients (48.4%) were male. Most frequent causes for ICU admission were septic shock (43%), hypovolemic shock (25%), respiratory failure (15%), and postoperative care (10%). Other demographic and clinical characteristics are shown in Table 2.

There were 72 patients (45.3%) with Ventilator-associated pneumonia (VAP), 41 (25.8%) with Catheter-associated Urinary tract infection (CA-UTI), 21 (13.2%) with Surgical site infection (SSI), 20 (12.6%) cases of abdominal sepsis, and 5 (3.1%) with Central-line-associated bloodstream infection (CLABSI). The CA-UTI rate was 17.1/1,000 catheter/days. Mean VAP rate was 8.2/1,000 ventilator/days. Mean days of mechanical ventilation in those patients who developed VAP were 14.4 ± 10.2 days.

Of all nosocomial infections, 145 (91.2%) were culture- confirmed and 14 (8.8%) were clinically defined as culture-negative infections. There were 266 microorganisms isolated, 105 were considered MDR; the overall prevalence was 39.5%. These bacteria were distributed as follows: 148 Gram-negative (55.6%); 86 Gram-positive (32.3%), and 32 yeasts (12.1%). The most frequent organisms were: E. coli (n = 54; 20%), 94.4% of these were ESBL producers; S. aureus (n = 32; 12%), 90.6% of these were Methicillin-resistant (MRSA); E. faecium (n = 32;

12%); 18.7% were Vancomycin-resistant (VRE); P. aeruginosa (n= 29; 11%), 14% were MDR and Acinetobacter baumannii (n = 15; 6%), all of these were MDR (Table 3).

Mean days of ICU hospitalization were longer in patients who developed MDRB-HAI compared to that of patients with HAI with susceptible bacteria (16 ± 10 days vs. 12 ± 6, p = 0.02). MDRB were more frequently isolated in patients who developed VAP (p = 0.03) and bacteremia (p = 0.003). Appropriate empirical antimicrobial treatment was initiated in 75 patients (56%), although it did not influence mortality (p= 0.9) even in the presence of MDRB (p = 0.8). The SOFA score at ICU admission was 8.4 ± 3.3 and at HAI diagnosis was 7.4 ± 4.1 (p = 0.03J with no statistical difference between patients who developed or not MDRB-HAI (7.1 ± 3.5 vs. 7.4 ± 4.1, respectively p = 0.5).

Mortality rate of patients with hematological malignancies did not differ from that of patients with solid tumors, even in those with MDRB (p = 0.7). Among patients admitted to the UCI (N=1418) during the study period, 252 died (17.8%). Fifty eight patients (23%) had a HAI; and 51 (88%) had a MDRB isolated. Mortality related with MDRB-HAI was significantly higher than those with non-MDRB-HAI (p=0.05).

In 2011, the ICU experienced a 5-month outbreak of MDR-A. baumannii from bronchial secretions in 13 patients (also isolated from blood in one patient, urine and surgical site infection in one patient each); in two patients it was isolated only in blood cultures. Eleven patients died (73%) increasing HAI mortality to 53%.

Discussion

Cancer is a leading cause of death worldwide, accounting for 13% of all deaths in the year 2008 [13]. Along with its higher incidence, more cancer patients receive multimodal treatment, with chemotherapy, radiation, surgery, and/or molecular targeted therapies, with increased rates of remission and cure. Within in-hospital medical care, patients with cancer admitted to the ICU are becoming more common [14-17].

ICU-HAI rates are higher than in general hospital wards due to the complex interactions between, the patient's underlying diseases, comorbidities, severity of illness, type of ICU, length of stay, and use of multiple invasive devices [2,18]. A study conducted in patients with hematological malignancies admitted to the ICU showed that mechanical ventilation and >2 organ failures were independently associated with in-hospital mortality. Mortality reported in ICU, in-hospital, and at 6 months were 34%, 46%, and 59%, respectively [15]. Another study reported that mortality in cancer patients was negatively influenced by respiratory failure and septic shock development during the ICU stay [16].

A previous report at our Institution showed an overall mortality during a 6-year surveillance period of 18% (302 deaths/1,670 patients), but there was not data about the infections related [8]. In this study, mortality was reported in 18%; 23% of all the cases were associated with a HAI.

Analyzing the infection rate by site, there was a clearly increase in VAP in 2011, related with the Acinetobacter outbreak described. The prevalence of MDR-HAI pathogens was significantly higher in the same year. Analyzing the rest of the period studied (2007-2010) there was not a significant variation in the infection

rate. What is noteworthy is the CLABSI rate is less than 1, which is in relation to strict management of vascular central lines in our hospital. Risk of infection with MDRB has been related to a number of risk factors, including previous antimicrobial therapy, cross-transmission and length of hospital stay [3,19]. Critically ill cancer patients admitted to the ICU have a major risk of HAI-MDRB infection that will impact negatively on mortality [2, 20], rendering the enormous efforts to cure and control the cancer wasteful and inefficient. Eighty eight percent of our patients who develop an HAI and died, had a MDRB isolated, reflecting the relationship between these multi-resistant bacteria and the high risk of mortality.

As previously reported, the increase in mortality among patients with a HAI-MDRB, even with appropriate therapy, is higher compared to increases in other series of non-cancer patients [20]. As described in other studies, we found a higher mortality in patients with MDRB-HAI, regardless of whether or not they had received appropriate antimicrobial therapy. These findings could be explained because morbidity and organ failure present in ICU patients act as independent factors related with mortality. In a previous report from our Institution in patients with hematologic malignancies and bacteremia due to E. coli-ESBL, mortality was twice as big of patients with isolations of non-ESBL E. coli [12]. The percentage observed of isolates with antimicrobial resistance in our ICU reflects the common and increasing problem of emerging resistance patterns in all types of hospital wards [21].

In 2011, related with an MDR-Acinetobacter spp. outbreak HAI-rate and HAI-mortality were increased. This bacterium has become an emerging nosocomial

pathogen, particularly in ICU, and is frequently associated with outbreaks, most commonly of VAP [22-24]. It has often been attributed to contaminated medical equipment and materials in contact with water, as well as environmental surfaces [19,25]. When other resistant microorganisms were evaluated, none was associated to a high mortality or lengthy hospitalization, although estimates are imprecise given the low number of the latter isolates. Our institutional program enhances antimicrobial stewardship and monitor antimicrobial resistance. These measures have been reinforced since 2011, including ICU antimicrobial restriction and consultation with an infectious diseases specialist, de-escalation of therapy and antimicrobial dose optimization. The emergence of MDRB poses a difficult task for physicians, who are aggravated by reduced or non-existent therapeutic options. Critically ill cancer patients admitted to the ICU are at major risk of HAI-MDRB infection that will impact adversely on mortality, despite enormous efforts and expenses.

Conflict of interest

All authors declare not to have conflict of interests. The study authors conducted data collection and analysis. There was any funding source for the research study. We agree to allow the journal to review data if requested.

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Table 1. Hospital acquired infections (HAI), overall mortality, and infection-related mortality at an Intensive care unit (ICU).

Year 2007 2008 2009 2010 2011

Rate of HAI 8.6 8.9 11.5 9.5 17.4

Patients admitted to ICU (n) 341 296 277 273 252

ICU overall mortality (%) 19 18 17 18 18

HAI- mortality (%) 19 31 29 25 53

Median days ICU stay - 4 2 2 3 4

(interquartile range) (2-4) (1-4) (1-6) (1-6) (2-5)

Infection rate by site*

VAP 3.8 4.7 4.3 3.7 9.5

VAP/1000 ventilator-days 11.7 15.8 14.4 12.2 31.7

CA-UTI 2 3 3.9 3.7 2.6

CA-UTI/1000 catheter-day 3.4 5 6.6 6.1 3.6

CLABSI 0.8 0 0.4 0 0.8

SSI 0.3 1.3 1.8 1 2.1

Abdominal sepsis 0.6 1 1.1 2.2 2

Prevalence (%) MDR-HAI pathogens& 37.5 33.3 29.4 33.3 65.1

* VAP: Ventilator associated pneumonia; CA-UTI: catheter-associated urinary tract infection; CLABSI: Central line associated bloodstream infection; SSI: Surgical site infection. &MDR: Multidrug resistant bacteria (ESBL- E. coli; MDR/XDR- P.

aeruginosa; MDR- A. baumannii; Methicillin-resistant S. aureus, Vancomycin-resistant enterococcus)

Table 2.Demographic and clinical characteristics in Intensive care unit (ICU) patients with Hospital acquired infections (HAI) (2007-2011).

Characteristic - N (%) Patients (n = 134)

Median age (years) 50 (range, 16-93)

Male 65 (48.5%)

Underlying oncologic disease

Genitourinary 32 (23.9)

Lymphoma 16 (11.9)

Acute leukemia 14 (10.4)

Esophagus and stomach 10 (7.5)

Colon and rectum 9 (6.7)

Breast 6 (4.5)

Status of cancer at ICU admission

Recent diagnosis 83 (64)

Progression 11 (8.5)

Complete remission 16 (12.3)

Recurrence 12 (9.2)

Non-response 8 (6.1)

ICU admission diagnosis

Septic shock 58 (43)

Hypovolemic shock 33 (25)

Respiratory failure 20 (14.9)

Postoperative surgical care 14 (10.4)

Other reasons 6 (4.4)

Chemotherapy within 2 months 26 (19.4)

Mechanical ventilation 131 (97.8)

Comorbidities: 97 (72.4)

No comorbidities 17 (12.7)

Hypertensiona 14 (10.4)

Diabetes mellitus 6 (4.5)

Chronic renal failure 7 (5.2)

Otherb

a6 patients had two co-morbidities. b4 patients with systemic lupus erythematosus, 1 with fever and neutropenia, 1 with HIV, and 1 with deep venous thrombosis.

Table 3. Most frequent microorganisms isolated in Intensive care unit (ICU)

patients with Hospital acquired infections (HAI) (2007-2011)

Microorganisms Pneumonia Urinary Surgical site Blood- Abdominal Total

tract infection stream sepsis

infection infection

Escherichia colia

ESBL 10 7 10 11 4 42

Non-ESBL 4 4 0 3 1 12

Staphylococcus aureusb

MRSA 13 0 7 9 0 29

MSSA 1 0 0 1 1 3

Enterococcus faeciumc

VRE 0 1 2 3 0 6

Vancomycin-S 3 9 4 9 1 26

Other Gram- negatived 16 5 11 3 1 31

Pseudomonas aeruginosae

MDR 2 0 0 2 0 4

XDR 3 0 0 1 0 4

Non-resistant 15 5 3 5 1 29

Acinetobacter baumanniif

MDR 12 1 2 5 0 20

E. faecalisg 3 6 8 3 0 20

Klebsiella sppg 8 2 0 1 0 11

MDR 40 9 21 31 4 105

Non-MDR 50 31 26 25 5 137

aESBL: Extended spectrum beta-lactamases. bMRSA: Methicillin resistant S. aureus. MSSA: Methicillin susceptible S. aureus. cVancomycin-S: Vancomycin-susceptible. VRE: Vancomycin resistant enterococcus. dOther Gram negative: Enterobacter cloacae, E. aerogenes, Morganella morganii, Serratia marscecens, K. Oxytoca, Citrobacter freundii, Proteus mirabilis, Stenotrophomonas maltophilia, A. lwoffii. eMDR: Multidrug resistant (resistant to fluoroquinolones and cephalosporins); XDR: Extremely drug-resistant (also resistant to carbapenems). fAll A. baumannii strains were MDR (except for tigecycline and colistin). All were isolated in 2011 corresponding to an ICU outbreak. gThese bacteria were not MDR.