Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-14T04:28:52.725Z Has data issue: false hasContentIssue false
  • English
  • Français

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)
Rights & Permissions [Opens in a new window]

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

REFERENCES

1. Alberti, C, et al. Epidemiology of sepsis and infection in ICU patients from an international multicenter cohort study. Intensive Care Medicine 2002; 28: 108–121.CrossRefGoogle Scholar
2. Trilla, A. Epidemiology of nosocomial infections in adult intensive care units. Intensive Care Medicine 1994; 20 (Suppl. 3): 1–4.CrossRefGoogle ScholarPubMed
3. Fournier, PE, Richet, H. The epidemiology and control of Acinetobacter baumannii in health care facilities. Clinical Infectious Diseases 2006; 42: 692–699.CrossRefGoogle ScholarPubMed
4. Fagon, JY, et al. Mortality attributable to nosocomial infections in the ICU. Infection Control and Hospital Epidemiology 1994; 15: 428–434.CrossRefGoogle ScholarPubMed
5. Falagas, ME, Bliziotis, IA, Siempos, II. Attributable mortality of Acinetobacter baumannii infections in critically ill patients: a systematic review of matched cohort and case-control studies. Critical Care 2006; 10: R48.CrossRefGoogle ScholarPubMed
6. Warskow, AL, Juni, E. Nutritional requirements of Acinetobacter strains isolated from soil, water, and sewage. Journal of Bacteriology 1972; 112: 1014–1016.CrossRefGoogle ScholarPubMed
7. Anstey, NM, et al. Community-acquired bacteremic Acinetobacter pneumonia in tropical Australia is caused by diverse strains of Acinetobacter baumannii, with carriage in the throat in at-risk groups. Journal of Clinical Microbiology 2002; 40: 685–686.CrossRefGoogle ScholarPubMed
8. Zapor, MJ, Moran, KA. Infectious diseases during wartime. Current Opinion in Infectious Diseases 2005; 18: 395–399.CrossRefGoogle ScholarPubMed
9. Crowe, M, et al. Bacteraemia in the adult intensive care unit of a teaching hospital in Nottingham, UK, 1985–1996. European Journal of Clinical Microbiology and Infectious Diseases 1998; 17: 377–384.Google ScholarPubMed
10. Bang, RL, et al. Burn septicaemia: an analysis of 79 patients. Burns 1998; 24: 354–361.CrossRefGoogle ScholarPubMed
11. Wisplinghoff, H, et al. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clinical Infectious Diseases 2004; 39: 309–317.CrossRefGoogle Scholar
12. Costantini, M, et al. Hospital acquired infections surveillance and control in intensive care services. Results of an incidence study. European Journal of Epidemiology 1987; 3: 347–355.CrossRefGoogle ScholarPubMed
13. Jimenez, P, et al. Incidence and etiology of pneumonia acquired during mechanical ventilation. Critical Care Medicine 1989; 17: 882–885.CrossRefGoogle ScholarPubMed
14. Fussle, R, et al. Microbiological care of ventilated intensive care patients. Feasibility of diagnosis and therapy of pulmonary infection. Anaesthetist 1991; 40: 491–496.Google ScholarPubMed
15. Garrouste-Orgeas, M, et al. Oropharyngeal or gastric colonization and nosocomial pneumonia in adult intensive care unit patients. A prospective study based on genomic DNA analysis. American Journal of Respiratory and Critical Care Medicine 1997; 156: 1647–1655.CrossRefGoogle ScholarPubMed
16. Barsic, B, et al. Antibiotic resistance among gram-negative nosocomial pathogens in the intensive care unit: results of 6-year body-site monitoring. Clinical Therapeutics 1997; 19: 691–700.CrossRefGoogle ScholarPubMed
17. Trouillet, JL, et al. Ventilator-associated pneumonia caused by potentially drug-resistant bacteria. American Journal of Respiratory and Critical Care Medicine 1998; 157: 531–539.CrossRefGoogle ScholarPubMed
18. Garcia-Garmendia, JL, et al. Risk factors for Acinetobacter baumannii nosocomial bacteremia in critically ill patients: a cohort study. Clinical Infectious Diseases 2001; 33: 939–946.CrossRefGoogle ScholarPubMed
19. Artigas, AT, et al. Risk factors for nosocomial pneumonia in critically ill trauma patients. Critical Care Medicine 2001; 29: 304–309.CrossRefGoogle Scholar
20. Akca, O, et al. Risk factors for early-onset, ventilator-associated pneumonia in critical care patients: selected multiresistant versus nonresistant bacteria. Anesthesiology 2000; 93: 638–645.CrossRefGoogle ScholarPubMed
21. Gruson, D, et al. Rotation and restricted use of antibiotics in a medical intensive care unit. Impact on the incidence of ventilator-associated pneumonia caused by antibiotic-resistant gram-negative bacteria. American Journal of Respiratory and Critical Care Medicine 2000; 162: 837–843.CrossRefGoogle Scholar
22. Cendrero, JAC, et al. Role of different routes of tracheal colonization in the development of pneumonia in patients receiving mechanical ventilation. Chest 1999; 116: 462–470.CrossRefGoogle Scholar
23. Heckmann, JG, et al. Nosocomial pneumonias in a neurology intensive care unit. Deutsche Medizinische Wochenschrift 1999; 124: 919–924.CrossRefGoogle Scholar
24. Weist, K, et al. How many nosocomial infections are associated with cross-transmission? A prospective cohort study in a surgical intensive care unit. Infection Control and Hospital Epidemiology 2002; 23: 127–132.CrossRefGoogle Scholar
25. Vosylius, S, Sipylaite, J, Ivaskevicius, J. Intensive care unit acquired infection: prevalence and impact on morbidity and mortality. Acta Anaesthesiologica Scandinavica 2003; 47: 1132–1137.CrossRefGoogle ScholarPubMed
26. Sofianou, DC, et al. Analysis of risk factors for ventilator-associated pneumonia in a multidisciplinary intensive care unit. European Journal of Clinical Microbiology and Infectious Diseases 2000; 19: 460–463.CrossRefGoogle Scholar
27. Hanberger, H, et al. High antibiotic susceptibility among bacterial pathogens in Swedish ICUs. Report from a nation-wide surveillance program using TA90 as a novel index of susceptibility. Scandinavian Journal of Infectious Diseases 2004; 36: 24–30.CrossRefGoogle ScholarPubMed
28. Ertugrul, BM, et al. Ventilator-associated pneumonia in surgical emergency intensive care unit. Saudi Medical Journal 2006; 27: 52–57.Google ScholarPubMed
29. Piazza, O, et al. Incidence of antimicrobial-resistant ventilator associated pneumonia: an eighteen-month survey. Panminerva Medizine 2005; 47: 265–267.Google ScholarPubMed
30. Richards, MJ, et al. Nosocomial infections in medical intensive care units in the United States. Critical Care Medicine 1999; 27: 887–892.CrossRefGoogle ScholarPubMed
31. Kollef, MH, et al. The effect of late-onset ventilator-associated pneumonia in determining patient mortality. Chest 1995; 108: 1655–1662.CrossRefGoogle ScholarPubMed
32. Wood, GC, et al. Evaluation of a clinical pathway for ventilator-associated pneumonia: changes in bacterial flora and the adequacy of empiric antibiotics over a three-year period. Surgical Infections 2005; 6: 203–213.CrossRefGoogle Scholar
33. Gaynes, R, Edwards, JR. Overview of nosocomial infections caused by gram-negative bacilli. Clinical Infectious Diseases 2005; 41: 848–854.Google ScholarPubMed
34. Santucci, SG, et al. Infections in a burn intensive care unit: experience of seven years. Journal of Hospital Infections 2003; 53: 6–13.CrossRefGoogle Scholar
35. Bilevicius, E, et al. Multiple organ failure in septic patients. Brazilian Journal of Infectious Diseases 2001; 5: 103–110.Google ScholarPubMed
36. Chung, KI, et al. Nosocomial pneumonia in medico-surgical intensive care unit. Journal of Korean Medical Science 1992; 7: 241–251.CrossRefGoogle ScholarPubMed
37. Singh, AK, et al. Antibiotic sensitivity pattern of the bacteria isolated from nosocomial infections in ICU. Journal of Communicable Diseases 2002; 34: 257–263.Google ScholarPubMed
38. Sun, T, et al. Retrospective study on clinical features and risk factors of ventilator-associated pneumonia. Zhonghua Nei Ke Za Zhi 2002; 41: 468–471.Google ScholarPubMed
39. Mahmood, A. Blood stream infections in a medical intensive care unit: spectrum and antibiotic susceptibility pattern. Journal of Pakistan Medical Association 2001; 51: 213–215.Google Scholar
40. Wu, CL, et al. Quantitative culture of endotracheal aspirates in the diagnosis of ventilator-associated pneumonia in patients with treatment failure. Chest 2002; 122: 662–668.CrossRefGoogle ScholarPubMed
41. Rozaidi, SW, Sukro, J, Dan, A. The incidence of nosocomial infection in the Intensive Care Unit, Hospital Universiti Kebangsaan Malaysia: ICU-acquired nosocomial infection surveillance program 1998–1999. Medical Journal of Malaysia 2001; 56: 207–222.Google ScholarPubMed
42. Hira, HS, Zachariah, S, Kumar, R. Evaluation of ventilator-associated lower respiratory tract infection and tracheobronchial aspiration of gastrointestinal contents. Journal of the Association of Physicians of India 2002; 50: 1381–1385.Google ScholarPubMed
43. Erbay, H, et al. Nosocomial infections in intensive care unit in a Turkish university hospital: a 2-year survey. Intensive Care Medicine 2003; 29: 1482–1488.CrossRefGoogle Scholar
44. Kanafani, ZA, et al. Ventilator-associated pneumonia at a tertiary-care center in a developing country: incidence, microbiology, and susceptibility patterns of isolated microorganisms. Infection Control and Hospital Epidemiology 2003; 24: 864–869.CrossRefGoogle Scholar
45. Pawar, M, et al. Ventilator-associated pneumonia: Incidence, risk factors, outcome, and microbiology. Journal of Cardiothoracic and Vascular Anesthesia 2003; 17: 22–28.CrossRefGoogle ScholarPubMed
46. Pawar, M, et al. Central venous catheter-related blood stream infections: incidence, risk factors, outcome, and associated pathogens. Journal of Cardiothoracic and Vascular Anesthesia 2004; 18: 304–308.CrossRefGoogle ScholarPubMed
47. Namiduru, M, et al. Antibiotic resistance of bacterial ventilator-associated pneumonia in surgical intensive care units. Journal of Internal Medicine Research 2004; 32: 78–83.Google ScholarPubMed
48. Agarwal, R, et al. Epidemiology, risk factors and outcome of nosocomial infections in a Respiratory Intensive Care Unit in North India. Journal of Infection 2005; 53: 98–105.CrossRefGoogle Scholar
49. Meric, M, et al. Intensive care unit-acquired infections: incidence, risk factors and associated mortality in a Turkish university hospital. Japanese Journal of Infectious Diseases 2005; 58: 297–302.CrossRefGoogle Scholar
50. Mulin, B, et al. Risk factors for nosocomial colonization with multiresistant Acinetobacter baumannii. European Journal of Clinical Microbiology and Infectious Diseases 1995; 14: 569–576.CrossRefGoogle ScholarPubMed
51. Hanberger, H, et al. Antibiotic susceptibility among aerobic gram-negative bacilli in intensive care units in 5 European countries. French and Portuguese ICU Study Groups. Journal of the American Medical Association 1999; 281: 67–71.CrossRefGoogle ScholarPubMed
52. Siegrist, HH, Nepa, MC, Jacquet, A. Susceptibility to levofloxacin of clinical isolates of bacteria from intensive care and haematology/oncology patients in Switzerland: a multicentre study. Journal of Antimicrobial Chemotherapy 1999; 43: 51–54.CrossRefGoogle ScholarPubMed
53. Barsic, B, et al. Antibiotic resistance among nosocomial isolates in a Croatian intensive care unit–results of a twelve-year focal surveillance of nosocomial infections. Journal of Chemotherapy 2004; 16: 273–281.CrossRefGoogle Scholar
54. Krause, R, et al. In vitro activity of newer broad spectrum beta-lactam antibiotics against enterobacteriaceae and non-fermenters: a report from Austrian intensive care units. Austrian Carbapenem Susceptibility Surveillance Group. Wiener Klinische Wochenschrift 1999; 111: 549–554.Google ScholarPubMed
55. Villari, P, et al. Unusual genetic heterogeneity of Acinetobacter baumannii isolates in a university hospital in Italy. American Journal of Infection Control 1999; 27: 247–253.CrossRefGoogle Scholar
56. Jones, ME, et al. Emerging resistance among bacterial pathogens in the intensive care unit – a European and North American Surveillance study (2000–2002). Annals of Clinical Microbiology and Antimicrobials 2004; 3: 14–24.CrossRefGoogle ScholarPubMed
57. Garnacho-Montero, J, et al. Acinetobacter baumannii ventilator-associated pneumonia: epidemiological and clinical findings. Intensive Care Medicine 2005; 31: 649–655.CrossRefGoogle ScholarPubMed
58. Agodi, A, et al. Alert surveillance of intensive care unit-acquired Acinetobacter infections in a Sicilian hospital. Clinical Microbiology and Infection 2006; 12: 241–247.CrossRefGoogle Scholar
59. Wisplinghoff, H, et al. Nosocomial bloodstream infections caused by Acinetobacter species in United States hospitals: clinical features, molecular epidemiology, and antimicrobial susceptibility. Clinical Infectious Diseases 2000; 31: 690–697.CrossRefGoogle ScholarPubMed
60. Friedland, I, et al. Phenotypic antimicrobial resistance patterns in Pseudomonas aeruginosa and Acinetobacter: results of a Multicenter Intensive Care Unit Surveillance Study, 1995–2000. Diagnostic Microbiology and Infectious Disease 2003; 45: 245–250.CrossRefGoogle ScholarPubMed
61. Namias, N, et al. Incidence and susceptibility of pathogenic bacteria vary between intensive care units within a single hospital: implications for empiric antibiotic strategies. Journal of Trauma 2000; 49: 638–645.CrossRefGoogle ScholarPubMed
62. Karlowsky, JA, et al. Surveillance for antimicrobial susceptibility among clinical isolates of Pseudomonas aeruginosa and Acinetobacter baumannii from hospitalized patients in the United States, 1998 to 2001. Antimicrobial Agents and Chemotherapy 2003; 47: 1681–1688.CrossRefGoogle ScholarPubMed
63. Tognim, MC, et al. Resistance trends of Acinetobacter spp. in Latin America and characterization of international dissemination of multi-drug resistant strains: five-year report of the SENTRY Antimicrobial Surveillance Program. International Journal of Infectious Diseases 2004; 8: 284–291.CrossRefGoogle ScholarPubMed
64. Gulati, S, et al. Nosocomial infections due to Acinetobacter baumannii in a neurosurgery ICU. Neurology India 2001; 49: 134–137.Google Scholar
65. Gunseren, F, et al. A surveillance study of antimicrobial resistance of gram-negative bacteria isolated from intensive care units in eight hospitals in Turkey. Journal of Antimicrobial Chemotherapy 1999; 43: 373–378.CrossRefGoogle ScholarPubMed
66. Jang, TN, et al. Nosocomial gram-negative bacteremia in critically ill patients: epidemiologic characteristics and prognostic factors in 147 episodes. Journal of the Formosan Medical Association 1999; 98: 465–473.Google ScholarPubMed
67. Yucesoy, M, et al. Antimicrobial resistance of gram-negative isolates from intensive care units in Turkey: comparison to previous three years. Journal of Chemotherapy 2000; 12: 294–298.CrossRefGoogle ScholarPubMed
68. Wang, H, Chen, M. Surveillance for antimicrobial resistance among clinical isolates of gram-negative bacteria from intensive care unit patients in China, 1996 to 2002. Diagnostic Microbiology and Infectious Disease 2005; 51: 201–208.CrossRefGoogle Scholar
69. Hsueh, PR, et al. Multicenter surveillance of antimicrobial resistance of major bacterial pathogens in intensive care units in 2000 in Taiwan. Microbial Drug Resistance 2001; 7: 373–382.CrossRefGoogle ScholarPubMed
70. Thongpiyapoom, S, et al. Device-associated infections and patterns of antimicrobial resistance in a medical-surgical intensive care unit in a university hospital in Thailand. Journal of the Medical Association of Thailand 2004; 87: 819–824.Google Scholar
71. Yildirim, S, et al. Bacteriological profile and antibiotic resistance: comparison of findings in a burn intensive care unit, other intensive care units, and the hospital services unit of a single center. Journal of Burn Care and Rehabilitation 2005; 26: 488–492.CrossRefGoogle Scholar
72. Akcam, FZ, et al. Microbiological surveillance in the intensive care unit: a tertiary hospital experience. Medical Science Monitor 2006; 12: CR81–85.Google ScholarPubMed
73. Potgieter, PD, et al. Nosocomial infections in a respiratory intensive care unit. Critical Care Medicine 1987; 15: 495–498.CrossRefGoogle Scholar
74. Hammond, JM, Potgieter, PD. Long-term effects of selective decontamination on antimicrobial resistance. Critical Care Medicine 1995; 23: 637–645.CrossRefGoogle ScholarPubMed
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