Eur J Cardiothorac Surg 2008;33:666-672. doi:10.1016/j.ejcts.2007.12.046
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
Microbiologically documented nosocomial infections after cardiac surgery: an 18-month prospective tertiary care centre report
Luca Salvatore De Santoa,*,
Ciro Banconeb,
Giuseppe Santarpinob,
Gianpaolo Romanoc,
Marisa De Feob,
Michelangelo Scardonec,
Nicola Galdieric,
Maurizio Cotrufob
a Chair of Cardiac Surgery, University of Foggia, Foggia, Italy
b Department of Cardiothoracic Sciences, Second University of Naples, Naples, Italy
c Department of Cardiovascular Surgery and Transplants, Monaldi Hospital, Naples, Italy
Received 3 September 2007;
received in revised form 27 December 2007;
accepted 27 December 2007.
* Corresponding author. Address: Viale Colli Aminei 491, 80131 Naples, Italy. Tel.: +39 081 5922118; fax: +39 081 5464594. (Email: luca.desanto{at}ospedalemonaldi.it; l.desanto{at}unifg.it).
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Abstract
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Objective: The aim of this study was to prospectively evaluate frequency, characteristics, and predictors of nosocomial infections (NI) in a tertiary care centre. Methods: Study population included 925 patients (mean age 62.3 ± 12.5, 32.3% females, 22.9% diabetics, 6.8% with previous cardiac procedures) operated on between June 2005 and December 2006 (CABG 48.72%, valvular procedures 30.05%, thoracic aortic 10.9%, heart transplantations 3.78% and miscellanea 6.55%, procedure status: elective 72.9%, urgent 15.9% and emergent 11.2%). The study population was divided in two groups according to development of NI. Primary endpoints were multiorgan failure (MOF) and hospital mortality in the two groups. Secondary endpoints were length of intubation, intensive care unit (ICU) stay and overall hospitalisation. Univariate and multivariate analysis of NI predictors was conducted between 115 perioperative variables. Results: Eighty-three patients (9%) developed a NI. Infections affected respiratory tract in 51.8%, blood stream in 20.5 and wound infection in 27.7 (13.3% deep wound). Staphylococcal species (60.6%) predominated in blood stream and surgical wound infections while Gram-negative species predominated in respiratory infections. Patients affected by NI experienced significantly higher incidence of MOF (12% vs 0.8%) and hospital mortality (24.1 vs 6.9%). Development of NI significantly lengthened all the steps of postoperative process of care (length of intubation: 49.9 ± 73 h vs 19.1 ± 35.2; ICU stay: 10.4 ± 12.8 days vs 3.4 ± 4.6 and hospitalisation 20.7 ± 15.3 vs 10.6 ± 7). Independent predictors of NI were immunosuppressive therapy [OR 12.9 (CI 5.07–31.2)], reintubation [OR 10.3 (CI 4.6–2.3)], stroke [OR 9.5 (CI 1.8–49)], resternotomy for bleeding [OR 6.7 (CI 1.9–23.6)], emergent/urgent status [OR 3.6 (CI 1.5–8.4)], CVVH [OR 3.2 (CI 1.4–7.5)] and length of intubation [OR 1.03 (CI 1.01–1.1)]. Conclusions: NI still represents a serious complication. Presence of identified determinants of NI should prompt modification of management algorithms.
Key Words: Cardiac surgery • Postoperative complications • Nosocomial infections • Outcomes • Risk factors
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1. Introduction
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According to recent reports, nosocomial infections (NI) represent the main non-cardiac complication after heart surgery [1]. They imply a substantial morbidity, prolonged hospitalisation, higher mortality and economic burden [2–4]. Patterns of patient referral, length and extent of surgical procedures, perioperative utilisation of invasive devices, along with high dependency on hospital staff act as powerful predisposing factors in this patient subset [4,5]. Few studies have addressed the incidence of postoperative infections specifically in patients undergoing cardiac procedures. As part of our hospital's ongoing continuous quality improvement program, supported by a grant of the Italian Ministry of University and Research, we performed a prospective cohort study designed to determine the frequency rate, identify risk factors and examine the implications of nosocomial infections in a tertiary care in a university affiliated cardiac surgery centre.
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2. Materials and methods
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2.1 Study setting and population
The study was conducted at the Department of Cardiothoracic and Respiratory Sciences of the Second University of Naples located in an affiliated teaching hospital (V. Monaldi Hospital). At our institution, nearly 700 patients have cardiac surgery annually and are admitted to a dedicated 12-bed intensive care unit (ICU). Information from these patients is collected on a daily basis and maintained in the cardiac anesthesia database. The department of infectious disease stores microbiology data in a routinely recorded independent electronic database, blinded to patient's characteristics and survival data. During an 18-month period (June 2005 to December 2006), all patients undergoing cardiac surgery, with the only exclusion of those affected by active infective endocarditis, were selected for this investigation. Inclusion of heart transplant recipients, who are known to be extremely prone to nosocomial infection, was aimed to detect the real incidence of target events in the daily practice of a tertiary care centre. All cardiac procedures were performed by the same staff members throughout the entire study period. All patients received the same standard care. The surgical and anesthetic techniques, the type of cardiopulmonary bypass, and the treatment received in the ICU did not differ from ordinary procedures. After admission to the ICU, all patients were ventilated mechanically and monitored by continuous electrocardiographic recording. All patients had at least one central venous catheter and the arterial blood pressure was monitored by a catheter introduced in the radial artery, while invasive haemodynamic monitoring was employed only in high-risk patients. After verifying haemodynamic stability, the patients were always placed at a position of 45°. Principles of postoperative care were previously reported and comply with published guidelines [6,7]. Antibiotic prophylaxis was based on a single β-lactam antibiotic and routine mupirocin administration. When the patients were clinically stable, they were transferred from the ICU to a surgical ward, without any intermediate stay at a subacute unit. Body temperature was recorded every 6 h in the ICU, and twice daily thereafter. Haematologic and biochemical tests and chest radiographs were performed preoperatively and every day during ICU stay and before discharge. In addition, laboratory tests and radiographs were performed as clinically indicated. All patients were evaluated daily to detect any nosocomial infection. Bacteriologic examinations of blood, tracheal secretions, urine, central venous catheter tips, and wound swabs were performed as clinically indicated. Research protocol was approved by the local ethics and research committee, which waived the need for informed consent.
2.2 Study design and aims
A prospective observational cohort design was employed segregating study patients according to the presence or absence of an acquired nosocomial infection. Development of multiorgan failure and hospital mortality were the main outcome compared between the two study groups. We also assessed, as secondary outcomes, the durations of intubation, intensive care unit stay and overall hospitalisation.
2.3 Definitions
All definitions were selected prospectively as part of the original study design. Nosocomial infections (urinary tract, bloodstream, wound infection) were defined according to criteria established by the Centers for Disease Control and Prevention [8,9]. The diagnostic criteria for ventilator-associated pneumonia (VAP) were those established by the American College of Chest Physicians [10].
The definition used for multiple organ failure (MOF) was that proposed by the American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference [11].
Antibiotic-resistant bacteria were defined as Gram-negative bacteria resistant to aminoglycosides, third-generation cephalosporins, extended-spectrum penicillins, quinolones, or imipenem, and Gram-positive bacteria resistant to oxacillin or vancomycin.
2.4 Data analysis
Data are expressed as mean ± SD for continuous variables and as percentages for categorical variables. For comparison of continuous variables, Student's t-test or the Mann–Whitney test for normally and non-normally distributed variables was used. Categoric variables were compared by 
2 or Fisher's exact test. Variables associated with the development of microbiologically documented nosocomial infection, hospital mortality and multiple organ failure after the univariate analysis (p
< 0.05) were included in a forward conditional multivariable logistic regression model. All statistical analyses were performed with SPSS 10.0 (SPSS Inc., Chicago, Ill). Statistical significance was defined as p
0.05.
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3. Results
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3.1 Patients
Study population included 925 patients (mean age 62.3 ± 12.5, 32.3% females) operated on between June 2005 and December 2006. Surgical case mix comprised: CABG 48.8%, valvular procedures 30.1%, thoracic aortic 11%, others 10.1% (heart transplantations 3.8%). The distribution according to surgical priority was as follows: elective 72.9%, urgent 15.9% and emergent 11.2%. A redo procedure was performed in 6.8% of the cases.
3.2 Incidence and risk factors for nosocomial infection
Eighty-three patients (9%) acquired 120 microbiologically documented nosocomial infections (mean 1.4 per patient) during their hospital stay. Sixty-one patients (73.5%) developed a single infection and 22 patients (26.5%) experienced multiple nosocomial infections (2.4% of overall population). Fig. 1
presents the sites of NI. Ventilator-associated pneumonia was the most common infection (incidence: 4.6% of study population) followed by surgical site (incidence: 3.4% [2.2% superficial wound infections, 1.2% mediastinitis]), bloodstream (incidence: 2.5%), miscellanea (incidence: 1.8% [mainly intravascular catheter colonisations and catheter exit site infections]) and urinary tract (incidence: 0.4%).
Table 1
reports microbiological data single NI. The most common isolated pathogens associated with a nosocomial infection were Gram-positive bacteria (60.4%) followed by Gram-negative bacteria (39.1%). Among these isolated pathogens, of 24.6% the Gram-positive bacteria and 61.7 % of the Gram-negative bacteria were classified as antibiotic resistant.
Table 2
summarises baseline and operative characteristics stratifying patients according to infection development. Those experiencing an infectious complication proved a more complex case mix. Table 3
reports on details of perioperative process of care. As shown, NI group experienced a more demanding postoperative course with significant resource utilisation. Determinants of NI at multivariate analysis were as follows: immunosuppressive therapy [OR 12.9 (CI 5.07–31.2)], emergent/urgent status [OR 3.6 (CI 1.5–8.4)], resternotomy for bleeding [OR 6.7 (CI 1.9–23.6)], stroke [OR 9.5 (CI 1.8–49)], CVVH [OR 3.2 (CI 1.4–7.5)], length of intubation [OR 1.0 (CI 1.01–1.1)] and reintubation [OR 10.3 (CI 4.6–2.3)]. Determinants of the acquisition of the three, more severe, individual nosocomial infections examined are summarised in Table 4
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3.3 Study endpoints: hospital mortality, multiple organ failure and lengths of stay
Hospital mortality for the whole cohort of cardiac surgery patients during the study period was (8.4%). The all-cause mortality rate of patients developing a nosocomial infection (24.9%) was significantly greater than that of patients without a nosocomial infection (6.9%) (RR 3.6; p
< 0.001). Mortality associated to individual NI is reported in Fig. 1. Urinary tract, bloodstream infections and ventilator-associated pneumonia implied a worse outcome. Multiple infections implied more a severe outcome (40.9%) and association of bloodstream infection with pneumonia was the worst (6/11 pts, 54.5%). Results of multivariate analysis on determinants of hospital mortality are reported in Table 5
. Seventeen patients (1.8%) out of the whole cohort developed multiorgan failure. Patients acquiring a nosocomial infection were significantly more likely to develop multiple organ failure compared to non-infected patients (12% vs 0.8%; p
< 0.0001). Multivariate analysis demonstrated that emergent surgery [OR 3.65 (CI 1.2–5.73)], reintubation [OR 2.25 (CI 1.33–3.8)] and LVEF [OR 0.97 (CI 0.93–0.99)] were independent risk factors for the development of multiple organ failure. As to secondary endpoints, development of NI significantly lengthened hospital care. Intubation, ICU stay and hospitalisation were: 49.9 ± 73 h versus 16 ± 26 (p
< 0.0001), 10.4 ± 12.8 days versus 3.4 ± 4.6 (p
< 0.0001) and 20.7 ± 15.3 versus 10.6 ± 7 (p
< 0.0001), respectively.
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4. Discussion
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Epidemiologic features of microbiologically documented nosocomial infection in this prospective cohort of cardiac surgery patients proved homogeneous to those recently reported [1,2]. The 9% incidence observed favourably compares with the overall 9.9% rate registered by the ESGNI (European Study Group of Nosocomial Infection) 007 Study and, in particular with the 12.3% rate disclosed in teaching institutions [3]. VAP was the main cause of postoperative infection in this patient subset followed by surgical site and bloodstream infections. This figure together with the type of pathogens isolated, the pattern of multidrug resistance and mortality rates associated with individual NI and to multiple site infections mirror data from major series [3–5,12–14]. It is noteworthy to underscore that mortality rates in patients suffering from mediastinitis are remarkably low due to an aggressive strategy of early debridement surgery combined with vacuum-assisted closure and final pectoralis muscle flap closure. Such results favourably compare with those forwarded by highly experienced centres [12]. The relevant mortality rates observed in patients affected by urinary tract infections are the result of a really small sample size and of the peculiar case mix with the coexistence of other more severe NI and relevant postoperative non-infectious complications.
In the present experience, multivariate analysis disclosed the following as determinants of NI: immunosuppressive therapy, emergent/urgent status, resternotomy for bleeding, stroke, CVVH, length of intubation and reintubation.
As far as immunosuppressive regimen is concerned a risk factor analysis from a recent prospective Greek study reported a similar finding. On the other side NI have been long recognised as relevant factors for post-transplant morbidity and mortality in thoracic transplant recipients [5,15,16]. Still only a few reports on NI in critically ill thoracic transplant recipients exist in the literature, limited by small sample sizes, the retrospective nature of the analyses, and the lack of standardised diagnostic definitions. Thirty-five heart transplant recipient were included in the present series (3.8% of the study cohort), 22.8% presenting with UNOS status I, 31.4% with high pretransplant pulmonary vascular resistance and 31.4% with a previous cardiac surgical procedure. Incidence of NI was 22.9% in the transplanted subset and observed hospital mortality was as low as 12.5%. This figure deserves at least two considerations. First, the disclosed incidence is lower by far than that currently reported (38–173%) [16]. This could be partly explained by the publication biases mentioned before and partly by the effectiveness of our current practice of active infection surveillance and prophylaxis that has been previously described [17]. Second, hospital mortality rate in the transplanted infected cohort, which also proved lower than those usually reported, was lower than that observed in the rest of the infected subgroup of present study. Such favourable results are maybe due to a closer surveillance and a more aggressive management induced by the immunosuppressive regimen.
High surgical priority, reflecting either critical illness, limited preoperative evaluation of co-morbid conditions and higher tendency to bleeding, proved a risk factor for NI in the present series, which, reporting a tertiary care centre experience, included 27.1% of the patients operated on a urgent /emergent basis. Such finding is in good keeping with the results of the study by Rebollo et al. [18].
The role of resternotomy for bleeding (2.2% in the whole cohort, 6% in infected group) in the pathogenesis of NI, which reflects prolonged operative manipulation, delayed sternal closure and enhanced usage of blood transfusions has also been pointed out in authoritative studies [4,12,18,19].
The incidence of stroke in present series was 1% of the whole study population with a significantly higher percentage in the infected subgroup (6% vs 0.5%, p
< 0.001). Relevance of stroke as a predisposing factor for NI is well documented since it enhances the already high dependency on hospital staff and the need and length of utilisation of invasive devices, especially mechanical ventilation [20,21]. On the other side extent and length of usage of invasive devices are well-established determinants of hospital mortality and morbidity [1,5,7]. Hospital mortality and multiple organ failure were primary endpoints of the present study. Patients suffering from NI experienced significantly worse outcomes. Nevertheless, when performing the multivariate analysis, infection proved a determinant neither of hospital mortality nor of MOF. Actually apart from female sex, age and emergent surgery, redo surgery and usage of invasive devices (reintubation, IABP, and CVVH [continuous veno-venous haemofiltration]) were independently associated with increased mortality. Notably, LVEF and NIV (non-invasive ventilation) utilisation proved protective. This is in good keeping with a growing body of evidence that shows that avoidance of reintubation, through the usage of less invasive ventilatory modalities, reduces the incidence of VAP while effectively treating respiratory insufficiency in critically ill patients [22]. Such evidence has been rapidly incorporated in our clinical practice as demonstrated by a NIV usage in as high as 10.7% of whole study cohort. When determining independent predictors of the development of multiple organ failure, beside emergent surgery and LVEF, again, reintubation emerged as an independent predictor. Similarly, multivariate analysis of predictors of the three single most dreaded NI underscored the independent role of intubation and CVVH. However, the link between hospital outcomes, organ dysfunction/failure, intensive care invasiveness and nosocomial infection may be more complex than described and often follows a vicious circle. Such complication cascade pathway has been elegantly presented in a complex study by Hein et al. [23] who examined the 3-year survival after four major post-cardiac operative complications and is the clinical bottom line of the authoritative report by Welsby et al. from the Duke University [1] on the effects of the association of postoperative complication. Indeed, in the present series invasive monitoring was instituted in 77.1% of the infected subgroup. As high as 15.8% of these patients needed an IABP, 27.7% renal replacement therapy with CVVH, 27.7% were reintubated and 22% underwent a tracheostomy. Multiple organ failure developed in 12% and a multiple site infection in 26.5%. Death rate for MOF and multiple site infection were 30% and 40.9%, respectively. Such figures are homogeneous with most recently published data [24,25].
Major strengths of this study are the large cohort prospective design, the single centre setting and the adherence to standardised definition of index events and complications. In particular, confinement of this study to a single centre with a standardised perioperative care pathway significantly limited the variability due to the influence of individual and institutional practice on hospital and ICU length of stay and pattern of resource utilisation which are invaluable tools of outcomes measures in morbidity studies. The present study suffers as well from several limitations. First, there could have been an underestimation of real nosocomial infection incidence since only those microbiologically documented were evaluated for study design. Second, despite a large prospective cohort of patients enrolled, the study may still be statistically underpowered due to the relatively small number of index cases with a definite probability of type II error. Thirdly, the database was prepared taking into account that only a minority of patients in our institution undergo heart-beating surgery. Thus, we are unable to express any conclusion on the role of evolving technologies. Similarly, since data were obtained in a single cardiac centre, the influence of specific standards of clinical practice and a unique patient population may have led to one-sided results not readily transferable to other patient populations.
In conclusion, this study reported that microbiologically documented nosocomial infections still represent a frequent postoperative complication associated with significant morbidity and mortality. Several determinants of NI were identified. Some of them are closely related to patients’ characteristics and to the referral pattern of a tertiary care university affiliated teaching centre. Others, and primarily the invasiveness of critical care, appear to be amenable to prospective interventions. Recognition of such risk factors may help to improve the outcomes by developing new management algorithms and enhancing active surveillance and secondary prevention.
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Appendix A
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Conference discussion
Dr P. Ruchat (Lausanne, Switzerland): There are very few papers who are dealing with that problem, so it's always interesting to look at what you are doing in the clinical situation.
Congratulations because you have very low nosocomial infection in your collective, so the patient is quite young. The mean age is 62 years old.
What is interesting, you also put your collective of transplant patients. I think this is probably a way of having a bias in your collective because this is a special population, and you should probably take them out.
I have a few questions about the diabetic patient because we know that diabetes is also a risk factor for nosocomial infection. So probably you don’t have this criteria that was found by your multivariate analysis because your study is a little bit underpowered. And this is probably a Type II error in your collective because you have only 83 nosocomial infections among about 1000 patients.
So I’d like to have some comment about the transplant patient you put in your collective, and what about the diabetes patient?
Dr De Santo: The inclusion of transplanted patients was aimed to understand the real nosocomial infection rate during the study frame when performing all types of procedures. Interestingly, it gives us also the chance to note that patients on immunosuppressive regimen, as far as mortality associated to infections is concerned, have better results than the other patients.
Actually, we tried to exclude infectious episodes in the transplanted cohort which were not related to a nosocomial acquired infection, but were related to the relapse of previous infections.
Like others, for example, we have taken out all the data from CMV infection which are closely related to the immunosuppressive status.
As to the fact that it is possible to have a statistical error Type II, this is true. We are fortunate enough to have just 83 infected patients, so it is intrinsic there may be an under power for certain risk factors including diabetes.
But maybe this forces us to continue this survey to have a larger study population.
Dr Ruchat: Just a last comment. For example, your heart transplant patient, is diabetes a contraindication for transplantation in your group? Because this is a main bias if you have about, I don’t know, maybe 35 or 40 patients transplant, if they have no diabetes, there could be a bias in the analysis.
Dr DeSanto: No. We usually include diabetic patients unless they are in an end stage, with end organ damage, such as renal failure needing dialysis, or severe peripheral vascular disease. These are our exclusion criteria.
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Acknowledgments
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Authors are deeply grateful to Maria Gabriella Grassia; Associate Professor of Social Statistics at Federico II University, Naples Italy, for the invaluable help for statistical analysis and data interpretation.
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Footnotes
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Presented at the 21st Annual Meeting of the European Association for Cardio-thoracic Surgery, Geneva, Switzerland, September 16–19, 2007.
This study was supported by a MiUR (Italian Ministry of University and Research) grant (PRIN 2004062188).
Research was carried out at the Department of Cardiothoracic Sciences, Second University of Naples, Naples, Italy.
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Abstract
1. Introduction
