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Acinetobacter infections: a growing threat for critically ill patients

Published online by Cambridge University Press:  25 September 2007

M. E. FALAGAS ,
E. A. KARVELI ,
I. I. SIEMPOS  and
K. Z. VARDAKAS
M. E. FALAGAS*
Affiliation:
Alfa Institute of Biomedical Sciences (AIBS), Athens, Greece Department of Medicine, Tufts University School of Medicine, Boston, MA, USA
E. A. KARVELI
Affiliation:
Alfa Institute of Biomedical Sciences (AIBS), Athens, Greece
I. I. SIEMPOS
Affiliation:
Alfa Institute of Biomedical Sciences (AIBS), Athens, Greece
K. Z. VARDAKAS
Affiliation:
Alfa Institute of Biomedical Sciences (AIBS), Athens, Greece
*
*Author for correspondence: M. E. Falagas, M.D., M.Sc., D.Sc., Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos Street, 151 23 Marousi, Greece. (Email: m.falagas@aibs.gr)
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Summary

There has been increasing concern regarding the rise of Acinetobacter infections in critically ill patients. We extracted information regarding the relative frequency of Acinetobacter pneumonia and bacteraemia in intensive-care-unit (ICU) patients and the antimicrobial resistance of Acinetobacter isolates from studies identified in electronic databases. Acinetobacter infections most frequently involve the respiratory tract of intubated patients and Acinetobacter pneumonia has been more common in critically ill patients in Asian (range 4–44%) and European (0–35%) hospitals than in United States hospitals (6–11%). There is also a gradient in Europe regarding the proportion of ICU-acquired pneumonias caused by Acinetobacter with low numbers in Scandinavia, and gradually rising in Central and Southern Europe. A higher proportion of Acinetobacter isolates were resistant to aminoglycosides and piperacillin/tazobactam in Asian and European countries than in the United States. The data suggest that Acinetobacter infections are a growing threat affecting a considerable proportion of critically ill patients, especially in Asia and Europe.

Type
Review Article
Information
Epidemiology & Infection , Volume 136 , Issue 8 , August 2008 , pp. 1009 - 1019
Copyright
Copyright © 2007 Cambridge University Press

INTRODUCTION

A considerable proportion of critically ill patients acquire an infection during their stay in an intensive care unit (ICU) and the frequency of these infections varies considerably in different populations and clinical settings [Reference Alberti1–Reference Fournier and Richet3]. The development of ICU-acquired infections is strongly related to prolonged ICU stay and is associated with worse outcomes including increased morbidity and mortality [Reference Fagon4, Reference Falagas, Bliziotis and Siempos5].

During the last two decades clinicians in various countries have witnessed a growing number of critically ill patients who suffer from infections due to microorganisms that belong to the Acinetobacter genus, mainly strains of the species Acinetobacter baumannii. Acinetobacter are a group of non-fermentative Gram-negative bacteria that have minimal nutritional requirements and can survive on a variety of surfaces and aqueous environments [Reference Fournier and Richet3, Reference Warskow and Juni6]. Apart from ICU patients it has been shown to be a cause of community-acquired respiratory tract infections, including pneumonia, in immunocompetent people living in the tropics [Reference Anstey7]. In addition, Acinetobacter has been identified as one of the most common causes of infection in soldiers who sustained trauma during the Vietnam, Afghanistan, and Iraq wars [Reference Zapor and Moran8]. However, despite these important associations, they cannot be compared with the magnitude of the growing global epidemic of Acinetobacter ICU-acquired infections in critically ill patients. In this article, we undertook a review of surveillance and other prospective and retrospective studies of ICU-acquired infections to estimate the frequency and antimicrobial resistance patterns of Acinetobacter in critically ill patients in various areas of the world.

METHODS

Search strategy and study selection

We initially screened 565 studies that were retrieved by searches of the PubMed, Cochrane, and Current Contents databases (papers archived by April 2006) by using the key terms ‘Acinetobacter’ and ‘(intensive care or ICU or critically ill)’. Then, we focused on surveillance and other prospective and retrospective studies of ICU-acquired infections excluding randomized controlled trials and case-control studies. We further reviewed studies that reported the number of Acinetobacter isolates as well as the total number of bacterial isolates from specimens collected from ICU patients with pneumonia and/or bacteraemia. In addition, we included studies that provided data regarding the antimicrobial resistance of Acinetobacter isolates from critically ill patients receiving care in the ICU setting. We excluded studies that focused on paediatric patients, evaluated ICU infection outbreaks, or studied less than 11 patients or Acinetobacter isolates. Moreover, a study was not eligible for inclusion in our review if it evaluated isolates collected from the hospital environment (not clinical isolates). Data were collected from studies written in English, French, German or Italian.

Data extraction

We extracted data from the reviewed studies regarding the relative frequency of various pathogens causing ICU-acquired infections and the antimicrobial resistance of Acinetobacter from in vitro susceptibility tests. In order to present data regarding ICU-acquired Acinetobacter infections in hospitals in various countries through the years, studies were divided in subcategories, by the geographic area where the hospital-ICU was located (Europe, North America, South America, Asia, Africa, and Oceania).

Definitions

An infection was defined as ICU-acquired if the onset occurred at least 48 h after admission of the patient to the ICU. In studies that focused exclusively on patients with ICU-acquired pneumonia, isolates from cultures of sputum, tracheo-bronchial aspirates, bronchoalveolar lavage, protected brush specimens, and/or blood were included in our analysis. In three of the reviewed studies isolates from polymicrobial infections were excluded from the analysis [Reference Crowe9–Reference Wisplinghoff11].

RESULTS

ICU-acquired pneumonia and bacteraemia

Forty-one studies were identified that fulfilled the inclusion criteria for review and reported data on the relative frequency of isolation of Acinetobacter from infected adult patients with ICU-acquired pneumonia or bacteraemia [Reference Crowe9–Reference Meric49]. Most of the Acinetobacter isolates were classified as Acinetobacter baumannii. Table 1 shows that 25 of the 41 studies were prospective; eight additional studies were characterized as surveillance studies, and so were considered to be prospective in design. The remaining eight studies were retrospective.

Table 1. Acinetobacter intensive care unit-acquired infections (mainly pneumonia and/or bacteraemia) in patients reported in the reviewed studies

ICU, Intensive care unit; VAP, ventilator-associated pneumonia; RTI, respiratory tract infections; UTI, urinary tract infections; CVC, central venous catheter; BSI, bloodstream infections; MV, mechanically ventilated; n.a., not applicable, UK, United Kingdom; USA, United States of America.

* Chronological presentation of studies by the mean time of examined period.

† Studies describing outbreaks of Acinetobacter infection were excluded from this review.

‡ Percentage of infected patients out of the total number of patients admitted to the ICU.

§ Percentage of infected patients out of those that stayed >48 h in the ICU.

It is evident that the frequency of Acinetobacter infections among patients with ICU-acquired pneumonia and/or bacteraemia varies considerably between different countries, and even between different regions of the same country. However, Acinetobacter was a more common cause of ICU-acquired pneumonia in studies originating from Asian (range 4–44%) and European countries (0–35%) than in those originating from the United States (6–11%). A gradient in the proportion of ICU-acquired pneumonias caused by Acinetobacter in various European countries was apparent. Specifically, rates were very low in Scandinavia and became gradually higher in Germany and the United Kingdom, and highest rates were reported for France, Spain, Italy, and finally Greece and Turkey.

The available data from South America countries were limited and we did not identify a study originating from Africa or Oceania that fulfilled the criteria for inclusion in the review. Overall, the available data from the reviewed studies do not permit firm conclusions to be made regarding the secular trends of the relative frequency of Acinetobacter infections among patients with ICU-acquired pneumonia and/or bacteraemia during the last three decades.

Antimicrobial resistance of Acinetobacter clinical isolates

We identified 32 studies that fulfilled the criteria for inclusion in this part of the review [Reference Crowe9, Reference Barsic16, Reference Gruson21, Reference Sofianou26, Reference Santucci34, Reference Kanafani44, Reference Agarwal48, Reference Mulin50–Reference Hammond and Potgieter74]. These studies reported data on the in vitro susceptibility testing of Acinetobacter isolates from patients with ICU-acquired infections; seven also reported data on the relative frequency of Acinetobacter infection among patients with ICU-acquired pneumonia and/or bacteraemia [Reference Crowe9, Reference Barsic16, Reference Gruson21, Reference Sofianou26, Reference Santucci34, Reference Kanafani44, Reference Agarwal48]. The data on the antimicrobial resistance of Acinetobacter isolates are summarized in Table 2. Some studies included not only Acinetobacter isolates that were thought to be the cause of infection but also isolates thought to represent colonization.

Table 2. Antimicrobial resistance of Acinetobacter isolates from patients in the intensive care unit setting in various countries

n.a., Not applicable; USA, United States of America; UK, United Kingdom.

Most studies gave information on the in vitro susceptibility of Acinetobacter isolates to piperacillin/tazobactam, aminoglycosides, third-generation cephalosporins, quinolones, and imipenem. In contrast, only a few studies reported the susceptibility of isolates to sulbactam, meropenem, and polymyxins. Two studies, one from Brazil and the other from seven countries in South America found that 0/19 and 6/166 (4%) of Acinetobacter isolates were resistant to polymyxin B [Reference Santucci34, Reference Tognim63].

A careful review of the data presented in Table 2 suggests that the proportions of Acinetobacter isolates that were resistant to various antimicrobial agents were higher in the studies originating from Asian and European countries than the United States. It is evident that most Acinetobacter isolates were susceptible to imipenem (as well as meropenem in the few studies that included testing for this antibiotic). Further, the majority of Acinetobacter clinical isolates from critically ill patients originating from the developed world were susceptible to piperacillin/tazobactam, but again it appears that a higher proportion of isolates from the United States than from European countries were susceptible to this agent.

It is noteworthy that several studies reported approximately 90% of Acinetobacter isolates from critically ill patients were resistant to aminoglycosides in European countries, while less than 50% of such isolates were resistant to aminoglycosides in all but one study from the United States. A broad range of the proportion of clinical isolates with resistance to third-generation cephalosporins (6–95%) was observed. Finally, about 50% of Acinetobacter isolates were resistant to ciprofloxacin, even in the United States.

DISCUSSION

Limitations

We must acknowledge several limitations of our review. First, we elected to review only a subset of the available studies on ICU-acquired infections that may have included data on Acinetobacter infections. However, studies using another design including randomized controlled trials, case-control studies, and case reports would not be helpful in our attempt to summarize the available data regarding the relative frequency of isolation of Acinetobacter from infected adult patients with ICU-acquired pneumonia or bacteraemia.

Second, we excluded studies focusing on outbreaks of Acinetobacter nosocomial infections. It should be emphasized that outbreaks of such infections have become relatively common in hospitals in several parts of the world, especially in the ICU setting, contributing significantly to the overall morbidity and mortality attributable to this pathogen [Reference Fournier and Richet3]. Moreover, the distinction between endemic Acinetobacter infections in an ICU or hospital and an outbreak of such infections is usually not obvious. Thus, it is likely that a proportion of Acinetobacter infections that occurred in critically ill patients in the reviewed studies were part of an unrecognized outbreak. The differences that are noted between studies in the same country (e.g. the United States) or areas of a specific continent (e.g. Central Europe) may reflect the presence of such outbreaks.

Third, different methods were used among the studies for determination of antimicrobial resistance and thus observed differences in susceptibility may be a consequence of methodology. In addition, results from poorly standardized methods such as agar diffusion tests may have lead to false interpretations. Another limitation of our literature search for relevant studies on Acinetobacter infections is related to the changes in taxonomic classification of Acinetobacter spp. The majority of studies used methods that were not able to unambiguously identify A. baumannii and therefore it can not be excluded that Acinetobacter genomic species 3 or 13 or even Acinetobacter spp. outside the A. calcoaceticus–A. baumannii complex were misidentified.

We did not adopt a mathematical approach to the synthesis of extracted data on the secular trends of the relative frequency of Acinetobacter infections among patients with ICU-acquired pneumonia and/or bacteraemia. This was done for several reasons. Among them, the most important was that the studies were conducted in hospitals in several different cities/areas of different countries. No single centre provided a second report with relevant data from different (non-consecutive) time periods. However, several of the studies were conducted over a long period of time permitting a limited evaluation of the trends of Acinetobacter infections in critically ill patients within a specific setting.

Critical evaluation of the reviewed studies

The data suggest that Acinetobacter is indeed a growing public health threat affecting a considerable proportion of critically ill patients in several parts of the world. The increasing number of published studies regarding Acinetobacter ICU-acquired infections during the last decade represents a growing concern among clinicians and researchers for this emerging pathogen. These infections most frequently involve the respiratory tract of intubated patients. However, Acinetobacter is also a common cause of urinary tract and wound infections in ICU patients and on occasion local infections can progress to bacteraemia [Reference Karlowsky62]. The data also support the view that infections caused by Acinetobacter are more common in critically ill patients receiving care in the ICU setting in hospitals in Asian and European countries and are considerably lower in the United States. Furthermore, the proportions of Acinetobacter isolates that were resistant to various antimicrobial agents in the studies from Asia and Europe were also higher than their counterparts from the United States. A notable exception was the low incidence of resistance from The Netherlands and Scandinavia [Reference Hanberger27] which is in keeping with the relatively few problems of resistance of other pathogens such as Staphylococcus aureus, Enterococcus spp. Pseudomonas aeruginosa, and Enterobacteriaceae found in these countries compared to other parts of the world.

The data also suggest that there are several noteworthy differences in the antimicrobial resistance patterns between Acinetobacter isolates from critically ill patients in European and United States hospitals, chief of the higher rates of resistance in Europe for piperacillin/tazobactam and aminoglycosides. These differences probably mirror the relative frequency of ICU-acquired infections due to Acinetobacter in patients in these two geographical areas. Although several assumptions can be made, including differences in antibiotic prescribing policies and infection control practices between countries, no firm conclusions can be made regarding the reasons for the observed differences.

Finally, it should be emphasized that data for the in vitro susceptibility testing of Acinetobacter clinical isolates were not available in most of the studies included in our review for three important antibiotics with proven activity against this organism. Indeed, only a few studies reported results of isolates to meropenem [Reference Krause54, Reference Jones56, Reference Karlowsky62, Reference Tognim63, Reference Wang and Chen68, Reference Hsueh69, Reference Yildirim71], sulbactam [Reference Agodi58, Reference Friedland60, Reference Hsueh69], and polymyxins B and E. In addition, the data confirm that Acinetobacter spp. are frequently resistant to aminoglycosides and third-generation cephalosporins, which means that these antibiotics should be avoided for the treatment of these infections.

DECLARATION OF INTEREST

None.

References

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Figure 0

Table 1. Acinetobacter intensive care unit-acquired infections (mainly pneumonia and/or bacteraemia) in patients reported in the reviewed studies

Figure 1

Table 2. Antimicrobial resistance of Acinetobacter isolates from patients in the intensive care unit setting in various countries