| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Review |
1 Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos Street, 151 23 Marousi, Athens, Greece
2 Department of Medicine, Tufts University School of Medicine, Boston, Massachusetts, USA
Correspondence
Matthew E. Falagas
matthew.falagas{at}tufts.edu
Background
The medical community has been witnessing a growing epidemic of infections due to Gram-negative bacteria resistant to many classes of antibiotics in most countries of the world (Sharma et al., 2005; Canton et al., 2003; Hsueh et al., 2002; Landman et al., 2002). Several investigators have studied the various aspects of these infections including mechanisms and risk factors of development of resistance as well as the effectiveness and toxicity of various therapeutic options (Harbarth & Samore, 2005; Epstein et al., 2004). In addition, the prevalence and epidemiology of bacteria resistant to antimicrobial agents have become the focus of numerous single-centre and multi-centre surveillance studies (Tambic et al., 2002; Jones, 2003).
We observed that different definitions regarding antimicrobial resistance are used in publications dealing with infections caused by Acinetobacter baumannii or Pseudomonas aeruginosa. In particular the terms ‘multidrug-resistant (MDR)’ and ‘pandrug-resistant (PDR)’ have been used to characterize isolates of A. baumannii or P. aeruginosa with a variety of genotypic and phenotypic characteristics. This is a noteworthy fact that causes considerable confusion among researchers and clinicians. Thus we sought to systematically examine the various definitions of MDR and PDR A. baumannii and P. aeruginosa used in the biomedical literature during recent years.
Literature search
We searched for relevant studies indexed in the PubMed database and published in the period 01/2000–09/2005. We searched for articles that had the words ‘multidrug’, ‘multi-drug’, ‘MDR’, ‘multiresistance’, ‘multi-resistance’, ‘multiresistant’, ‘multi-resistant’, ‘pandrug’, ‘pan-drug’ or ‘PDR’ and ‘Acinetobacter baumannii’ or ‘Pseudomonas aeruginosa’ in their title.
Our search was limited to studies that were performed in humans, were written in English, and had available abstracts in PubMed, by making use of the respective ‘Limits' functions of the PubMed search engine. The title and the abstract of studies that were retrieved from the initial search were examined for relevance. Then, the full-published papers of the relevant studies were reviewed to extract the definitions of MDR or PDR A. baumannii or P. aeruginosa used in the papers. We excluded from further analysis studies that were written by the same first author when the same definition for MDR or PDR was used.
Reviewed publications
We reviewed the title and the abstract of 107 initially retrieved studies, out of which 53 studies reported results for A. baumannii and 54 for P. aeruginosa isolates. Based on our inclusion criteria we identified 50 (Abbo et al., 2005; Alarcon et al., 2001; Appleman et al., 2000; Blahova et al., 2001; Bou et al., 2000; Cawley et al., 2002; Corbella et al., 2000; El Shafie et al., 2004; Gales et al., 2001; Garnacho-Montero et al., 2003; Giacometti et al., 2000; Giamarellos-Bourboulis et al., 2001; Gorman et al., 2003; Higgins et al., 2004; Hsueh et al., 2002; Huys et al., 2005; Jain & Danziger, 2004; Jiménez-Mejías et al., 2002; Jones et al., 2004; Joshi et al., 2003; Kuo et al., 2003, 2004; Landman et al., 2002; Lee et al., 2005; Levin et al., 2001; Ling et al., 2001; Maniatis et al., 2003; Maragakis et al., 2004; Maslow et al., 2005; Michalopoulos et al., 2005a; Mussi et al., 2005; Oh et al., 2002; Paavilainen et al., 2001; Pimentel et al., 2005; Podnos et al., 2001; Roberts et al., 2001; Ruiz et al., 2003; Saugar et al., 2002; Simor et al., 2002; Smolyakov et al., 2003; Tognim et al., 2004; Turton et al., 2004; Urban et al., 2003; van Dessel et al., 2004; Wang et al., 2003; Wilson et al., 2004; Wood et al., 2003; Wu et al., 2004; Yoon et al., 2004; Zeana et al., 2003) and 42 (Ahmed et al., 2002; Belet et al., 2004; Bratu et al., 2005; Brito et al., 2003; Bukholm et al., 2002; Cao et al., 2004; Davies et al., 2003; Defez et al., 2004; Domenig et al., 2001; Douglas et al., 2001; Dubois et al., 2001; Erdem et al., 2003; Fraser et al., 2004; Giamarellos-Bourboulis et al., 2000, 2005; Goossens, 2003; Hamer, 2000; Hsueh et al., 2005; Jones et al., 2001; Jones et al., 2004; Jung et al., 2004; Kocazeybek et al., 2002; Landman et al., 2002; Lang et al., 2000; Lin et al., 2003; Luzzaro et al., 2001; Mirakhur et al., 2003; Miranda et al., 2001; Ohmagari et al., 2005; Oie et al., 2003; Ortega et al., 2004; Pagani et al., 2005; Paramythiotou et al., 2004; Pellegrino et al., 2002; Pirnay et al., 2003; Pitten et al., 2001; Rossolini & Mantengoli, 2005; Schelenz & French, 2000; Shahid et al., 2003; Takeyama et al., 2002; Tascini et al., 2004; Thong et al., 2004) studies that reported on MDR or PDR A. baumannii and P. aeruginosa isolates, respectively. Three studies that reported on MDR Acinetobacter were excluded because they referred to species other than A. baumannii (two studies) or had the same first author who used the same definition of MDR in another paper included in our systematic review (one study). Twelve studies that reported on MDR Pseudomonas were excluded because they described cellular mechanisms for multidrug resistance (five studies), had the same first author and used the same definition of MDR P. aeruginosa as another paper included in our review (four studies), referred to species other than P. aeruginosa (two studies), or reported on MDR cancer cells and not P. aeruginosa (one study).
MDR and PDR A. baumannii
In Table 1
we present the characteristics of the 50 studies that reported on MDR or PDR A. baumannii isolates. As shown, substantially different definitions were used in the identified studies. Four studies reported on PDR isolates (Kuo et al., 2003, 2004; Lee et al., 2005; Wang et al., 2003). The term PDR was used inappropriately in all of these studies. Specifically, the term PDR was used despite the fact that the isolates were not tested for in vitro susceptibility to sulbactam in two studies (Lee et al., 2005; Kuo et al., 2003) and to polymyxins in three studies (Kuo et al., 2003, 2004; Lee et al., 2005). In one study the isolates were defined as PDR although they were tested and found to be sensitive to colistin (Wang et al., 2003).
|
All parts of a broad spectrum of the antimicrobial resistance profiles were used to define the term MDR A. baumannii in the reviewed studies. On one side of the spectrum, the minimum resistance that was required for an isolate to be described as MDR, which is resistance to representative antibiotics of at least two classes of antimicrobial agents, was used in one study (Huys et al., 2005). The middle of the spectrum of the antimicrobial resistance profiles regarding the definition of the term MDR A. baumannii was used in a considerable proportion of papers (24 studies). Specifically, in these studies, A. baumannii isolates were defined as MDR if they were resistant to representative antibiotics of at least three different classes of antimicrobial agents. The most common antibiotic categories tested against A. baumannii in these studies were aminoglycosides, antipseudomonal penicillins, carbapenems, cephalosporins and quinolones; in addition, colistin, ampicillin/sulbactam and/or tetracyclines (doxycycline or minocycline) were agents that were tested occasionally. On the other side of the spectrum of the various definitions of MDR A. baumannii, there was a group of eight studies in which the term MDR described isolates that exhibited resistance to all but one of the tested agents, most commonly polymyxins [colistin in three studies (Garnacho-Montero et al., 2003; Jiménez-Mejías et al., 2002; Levin et al., 2001) and polymyxin B in one (Podnos et al., 2001)], doxycycline or minocycline (one study) (Wood et al., 2003), imipenem (one study) (Gorman et al., 2003), amikacin (one study) (El Shafie et al., 2004), or any one of the tested antibiotic categories (one study) (Maragakis et al., 2004).
MDR and PDR P. aeruginosa
In Table 2, we present the 42 identified studies that reported on MDR or PDR P. aeruginosa isolates. As shown in Table 2, the terms PDR and MDR are defined and used in various ways when referring to P. aeruginosa isolates also. The term PDR was used in one study and was also defined inappropriately despite the sensitivity of P. aeruginosa to colistin (Hsueh et al., 2005).
|
The term MDR P. aeruginosa was used in the remaining 32 studies for isolates that had a diversity of antimicrobial susceptibility profiles, similarly to most of the studies that reported on MDR A. baumannii. Specifically, on one side of the spectrum of the antimicrobial resistance profiles the term MDR was used for isolates with the least resistant profile that can be appropriately characterized as MDR, which is resistance to at least two specific representatives of at least two classes of antibiotics (four studies) (Erdem et al., 2003; Ortega et al., 2004; Schelenz & French, 2000; Tascini et al., 2004). In the great majority of the rest of the analysed articles (25 studies), the term MDR P. aeruginosa was used to report on isolates resistant to at least three drugs from a variety of antibiotic categories, mainly aminoglycosides, antipseudomonal penicillins, carbapenems, cephalosporins and quinolones. Finally, on the other extreme of the spectrum of the antimicrobial resistance profiles for the definition of MDR, isolates were described as MDR if they were resistant to all tested antibiotics (one study) (Giamarellos-Bourboulis et al., 2000) or to all tested antibiotics except for colistin (two studies) (Dubois et al., 2001; Thong et al., 2004).
Evaluation of the reviewed data
The main finding of our systematic review is that the terms MDR and PDR for A. baumannii and P. aeruginosa are defined and/or used by researchers around the world in a variety of ways. This variability may cause confusion, since there are considerable differences in the antibiotics tested in vitro in each of the presented studies. Specifically, the data presented in this systematic review show that investigators use different resistance profiles to various antimicrobial agents to define the term MDR or PDR A. baumannii or P. aeruginosa.
Although there have been a few attempts from some committees to establish rational and evidence-based definitions for MDR, it seems that these definitions were not widely accepted and used. Concerns may be raised about the validity and usefulness of some of the proposed definitions. For example, the definition by the French National Committee for Nosocomial Infections, which was used in the study by Defez et al. (2004), could be easily criticized since the finding of resistance to just one of three selected antibiotics (ticarcillin, ceftazidime and imipenem) sufficed to define an isolate as MDR. This definition contrasts with the meaning of the prefix multi (that in Latin means ‘many’) because the definition takes into account only resistance to ß-lactam antibiotics. On the other hand, the definition by the American Cystic Fibrosis Foundation that was used in the study by Davies et al. (2003) regarding MDR P. aeruginosa isolates from cystic fibrosis patients was more inclusive and the term MDR was used in agreement with this definition in some relevant studies (Mirakhur et al., 2003; Jones et al., 2001; Lang et al., 2000).
The confusion regarding the use of the term PDR is more profound than for the term MDR. This is because the prefix pan (that in Greek means ‘every’ or ‘to all’) should not be interpreted in more than one way. Thus it is rather confusing that some investigators use this term to describe isolates that are susceptible only to polymyxins (Wang et al., 2003). Although such isolates exhibit resistance to many antibiotics, the existence of even one antibiotic with good activity against the microbes automatically excludes the isolates from being called PDR. In addition, an isolate should have a documented resistance to representative antibiotics of specific classes of antimicrobial agents to be characterized as PDR. Thus a P. aeruginosa isolate should be defined as PDR only if it is resistant to agents from all seven available antipseudomonal classes of antimicrobial agents, i.e. antipseudomonal penicillins, cephalosporins, carbapenems, monobactams, quinolones, aminoglycosides and polymyxins (Falagas et al., 2005). Similarly, with the current knowledge regarding antimicrobial resistance patterns worldwide, A. baumannii isolates should be called PDR if they are resistant to representative antibiotics from all of the above categories plus to sulbactam, to one tetracycline (minocycline or doxycycline) and tigecycline. Departure from these definitions of PDR A. baumannii and P. aeruginosa may cause confusion to clinicians because it suggests the lack of antimicrobial agents for the management of infections caused by these bacteria, while a potential salvage therapeutic option is available (Michalopoulos et al., 2005b).
Limitations in the evaluation of the reviewed data
Our review is not without limitations. We restricted our search to papers published in English. However, the search and analysis of articles published in other languages would have probably revealed more confusion regarding the definition of the terms MDR and PDR A. baumannii and P. aeruginosa. Also, we limited our search to a recent period (01/2000–09/2005) because we appreciate that the definition of MDR may be evolving over time due to changes in the antimicrobial resistance patterns of bacteria. In addition, we did not extract data regarding the cut-off points used for the in vitro antimicrobial susceptibility testing, although such an effort would probably reveal more problems in the use of the various definitions of the terms MDR and PDR A. baumannii and P. aeruginosa. Furthermore, there is a need to mention that our review deals with resistance as measured in vitro. The clinical response of a patient after the administration of an antimicrobial agent(s) does not always correlate with the laboratory findings. Finally, it should be mentioned that definitions related to antimicrobial resistance patterns of pathogens need continuous update; for example, the in vitro susceptibility of Acinetobacter isolates to tigecycline should or will need to be tested also.
Conclusion
Our review reveals that various definitions have been used for the term MDR and even more importantly for the term PDR A. baumannii or P. aeruginosa isolates in the relevant publications during recent years. We believe that the relevant professional societies and authorities responsible for the surveillance and prevention of bacterial resistance to antimicrobial agents should try to formulate definitions for both terms, in order to enhance the communication between researchers and clinicians around the world. We acknowledge that it is probably difficult to establish a definition for MDR A. baumannii and P. aeruginosa that would be widely accepted by investigators and clinicians worldwide. However, we believe that a widely accepted definition for PDR A. baumannii and P. aeruginosa should be uniformly used.
REFERENCES
Abbo, A., Navon-Venezia, S., Hammer-Muntz, O., Krichali, T., Siegman-Igra, Y. & Carmeli, Y. (2005). Multidrug-resistant Acinetobacter baumannii. Emerg Infect Dis 11, 22–29.[Medline]
Ahmed, N., Bal, A., Khan, A. A. & 9 other authors (2002). Whole genome fingerprinting and genotyping of multiple drug resistant (MDR) isolates of Pseudomonas aeruginosa from endophthalmitis patients in India. Infect Genet Evol 1, 237–242.[CrossRef][Medline]
Alarcon, T., Lopez-Hernandez, S., Andreu, D., Saugar, J. M., Rivas, L. & Lopez-Brea, M. (2001). In vitro activity of CA(1-8)M(1-18), a synthetic cecropin A-melittin hybrid peptide, against multiresistant Acinetobacter baumannii strains. Rev Esp Quimioter 14, 184–190.[Medline]
Appleman, M. D., Belzberg, H., Citron, D. M., Heseltine, P. N., Yellin, A. E., Murray, J. & Berne, T. V. (2000). In vitro activities of nontraditional antimicrobials against multiresistant Acinetobacter baumannii strains isolated in an intensive care unit outbreak. Antimicrob Agents Chemother 44, 1035–1040.
Belet, N., Haciomeroglu, P. & Kucukoduk, S. (2004). Ciprofloxacin treatment in newborns with multi-drug-resistant nosocomial Pseudomonas infections. Biol Neonate 85, 263–268.[CrossRef][Medline]
Blahova, J., Kralikova, K., Krcmery, V., Sr, Kubonova, K., Vaculikova, A., Mikovicova, A., Klokocnikova, L., Hanzen, J. & Jezek, P. (2001). Transferable antibiotic resistance in multiresistant nosocomial Acinetobacter baumannii strains from seven clinics in the Slovak and Czech Republics. J Chemother 13, 143–147.[Medline]
Bou, G., Cervero, G., Dominguez, M. A., Quereda, C. & Martinez-Beltran, J. (2000). Characterization of a nosocomial outbreak caused by a multiresistant Acinetobacter baumannii strain with a carbapenem-hydrolyzing enzyme: high-level carbapenem resistance in A. baumannii is not due solely to the presence of beta-lactamases. J Clin Microbiol 38, 3299–3305.
Bratu, S., Quale, J., Cebular, S., Heddurshetti, R. & Landman, D. (2005). Multidrug-resistant Pseudomonas aeruginosa in Brooklyn, New York: molecular epidemiology and in vitro activity of polymyxin B. Eur J Clin Microbiol Infect Dis 24, 196–201.[CrossRef][Medline]
Brito, D. V., Oliveira, E. J., Matos, C., Abdallah, V. O. & Gontijo Filho, P. P. (2003). An outbreak of conjunctivitis caused by multiresistant Pseudomonas aeruginosa in a Brazilian newborn intensive care unit. Braz J Infect Dis 7, 234–235.[Medline]
Bukholm, G., Tannaes, T., Kjelsberg, A. B. & Smith-Erichsen, N. (2002). An outbreak of multidrug-resistant Pseudomonas aeruginosa associated with increased risk of patient death in an intensive care unit. Infect Control Hosp Epidemiol 23, 441–446.[CrossRef][Medline]
Canton, R., Coque, T. M. & Baquero, F. (2003). Multi-resistant Gram-negative bacilli: from epidemics to endemics. Curr Opin Infect Dis 16, 315–325.[Medline]
Cao, B., Wang, H., Sun, H., Zhu, Y. & Chen, M. (2004). Risk factors and clinical outcomes of nosocomial multi-drug resistant Pseudomonas aeruginosa infections. J Hosp Infect 57, 112–118.[CrossRef][Medline]
Cawley, M. J., Suh, C., Lee, S. & Ackerman, B. H. (2002). Nontraditional dosing of ampicillin-sulbactam for multidrug-resistant Acinetobacter baumannii meningitis. Pharmacotherapy 22, 527–532.[CrossRef][Medline]
Corbella, X., Montero, A., Pujol, M., Dominguez, M. A., Ayats, J., Argerich, M. J., Garrigosa, F., Ariza, J. & Gudiol, F. (2000). Emergence and rapid spread of carbapenem resistance during a large and sustained hospital outbreak of multiresistant Acinetobacter baumannii. J Clin Microbiol 38, 4086–4095.
Davies, G., McShane, D., Davies, J. C. & Bush, A. (2003). Multiresistant Pseudomonas aeruginosa in a pediatric cystic fibrosis center: natural history and implications for segregation. Pediatr Pulmonol 35, 253–256.[CrossRef][Medline]
Defez, C., Fabbro-Peray, P., Bouziges, N., Gouby, A., Mahamat, A., Daures, J. P. & Sotto, A. (2004). Risk factors for multidrug-resistant Pseudomonas aeruginosa nosocomial infection. J Hosp Infect 57, 209–216.[CrossRef][Medline]
Domenig, C., Traunmuller, F., Kozek, S., Wisser, W., Klepetko, W., Steininger, R., Spiss, C. & Thalhammer, F. (2001). Continuous beta-lactam antibiotic therapy in a double-lung transplanted patient with a multidrug-resistant Pseudomonas aeruginosa infection. Transplantation 71, 744–745.[CrossRef][Medline]
Douglas, M. W., Mulholland, K., Denyer, V. & Gottlieb, T. (2001). Multi-drug resistant Pseudomonas aeruginosa outbreak in a burns unit – an infection control study. Burns 27, 131–135.[CrossRef][Medline]
Dubois, V., Arpin, C., Melon, M., Melon, B., Andre, C., Frigo, C. & Quentin, C. (2001). Nosocomial outbreak due to a multiresistant strain of Pseudomonas aeruginosa P12: efficacy of cefepime-amikacin therapy and analysis of beta-lactam resistance. J Clin Microbiol 39, 2072–2078.
El Shafie, S. S., Alishaq, M. & Leni, G. M. (2004). Investigation of an outbreak of multidrug-resistant Acinetobacter baumannii in trauma intensive care unit. J Hosp Infect 56, 101–105.[CrossRef][Medline]
Epstein, B. J., Gums, J. G. & Drlica, K. (2004). The changing face of antibiotic prescribing: the mutant selection window. Ann Pharmacother 38, 1675–1682.
Erdem, I., Kucukercan, M. & Ceran, N. (2003). In vitro activity of combination therapy with cefepime, piperacillin-tazobactam, or meropenem with ciprofloxacin against multidrug-resistant Pseudomonas aeruginosa strains. Chemotherapy 49, 294–297.[CrossRef][Medline]
Falagas, M. E., Bliziotis, I. A., Kasiakou, S. K., Samonis, G., Athanassopoulou, P. & Michalopoulos, A. (2005). Outcome of infections due to pandrug-resistant (PDR) Gram-negative bacteria. BMC Infect Dis 5, 24.[CrossRef][Medline]
Fraser, T. G., Reiner, S., Malczynski, M., Yarnold, P. R., Warren, J. & Noskin, G. A. (2004). Multidrug-resistant Pseudomonas aeruginosa cholangitis after endoscopic retrograde cholangiopancreatography: failure of routine endoscope cultures to prevent an outbreak. Infect Control Hosp Epidemiol 25, 856–859.[CrossRef][Medline]
Gales, A. C., Jones, R. N., Forward, K. R., Linares, J., Sader, H. S. & Verhoef, J. (2001). Emerging importance of multidrug-resistant Acinetobacter species and Stenotrophomonas maltophilia as pathogens in seriously ill patients: geographic patterns, epidemiological features, and trends in the SENTRY Antimicrobial Surveillance Program (1997–1999). Clin Infect Dis 32, S104–S113.
Garnacho-Montero, J., Ortiz-Leyba, C., Jimenez-Jimenez, F. J., Barrero-Almodovar, A. E., Garcia-Garmendia, J. L., Bernabeu-Wittell, M., Gallego-Lara, S. L. & Madrazo-Osuna, J. (2003). Treatment of multidrug-resistant Acinetobacter baumannii ventilator-associated pneumonia (VAP) with intravenous colistin: a comparison with imipenem-susceptible VAP. Clin Infect Dis 36, 1111–1118.[CrossRef][Medline]
Giacometti, A., Cirioni, O., Del Prete, M. S., Barchiesi, F., Paggi, A. M., Petrelli, E. & Scalise, G. (2000). Comparative activities of polycationic peptides and clinically used antimicrobial agents against multidrug-resistant nosocomial isolates of Acinetobacter baumannii. J Antimicrob Chemother 46, 807–810.
Giamarellos-Bourboulis, E. J., Grecka, P., Dionyssiou-Asteriou, A. & Giamarellou, H. (2000). Impact of n-6 polyunsaturated fatty acids on growth of multidrug-resistant Pseudomonas aeruginosa: interactions with amikacin and ceftazidime. Antimicrob Agents Chemother 44, 2187–2189.
Giamarellos-Bourboulis, E. J., Xirouchaki, E. & Giamarellou, H. (2001). Interactions of colistin and rifampin on multidrug-resistant Acinetobacter baumannii. Diagn Microbiol Infect Dis 40, 117–120.[CrossRef][Medline]
Giamarellos-Bourboulis, E. J., Kentepozidis, N., Antonopoulou, A., Plachouras, D., Tsaganos, T. & Giamarellou, H. (2005). Postantibiotic effect of antimicrobial combinations on multidrug-resistant Pseudomonas aeruginosa. Diagn Microbiol Infect Dis 51, 113–117.[CrossRef][Medline]
Goossens, H. (2003). Susceptibility of multi-drug-resistant Pseudomonas aeruginosa in intensive care units: results from the European MYSTIC study group. Clin Microbiol Infect 9, 980–983.[CrossRef][Medline]
Gorman, S. K., Zed, P. J., Dhingra, V. K. & Ronco, J. J. (2003). Rapid imipenem/cilastatin desensitization for multidrug-resistant Acinetobacter pneumonia. Ann Pharmacother 37, 513–516.
Hamer, D. H. (2000). Treatment of nosocomial pneumonia and tracheobronchitis caused by multidrug-resistant Pseudomonas aeruginosa with aerosolized colistin. Am J Respir Crit Care Med 162, 328–330.
Harbarth, S. & Samore, M. H. (2005). Antimicrobial resistance determinants and future control. Emerg Infect Dis 11, 794–801.[Medline]
Higgins, P. G., Wisplinghoff, H., Stefanik, D. & Seifert, H. (2004). In vitro activities of the beta-lactamase inhibitors clavulanic acid, sulbactam, and tazobactam alone or in combination with beta-lactams against epidemiologically characterized multidrug-resistant Acinetobacter baumannii strains. Antimicrob Agents Chemother 48, 1586–1592.
Hsueh, P. R., Liu, C. Y. & Luh, K. T. (2002). Current status of antimicrobial resistance in Taiwan. Emerg Infect Dis 8, 132–137.[Medline]
Hsueh, P. R., Tseng, S. P., Teng, L. J. & Ho, S. W. (2005). Pan-drug-resistant Pseudomonas aeruginosa causing nosocomial infection at a university hospital in Taiwan. Clin Microbiol Infect 11, 670–673.[CrossRef][Medline]
Huys, G., Cnockaert, M., Vaneechoutte, M., Woodford, N., Nemec, A., Dijkshoorn, L. & Swings, J. (2005). Distribution of tetracycline resistance genes in genotypically related and unrelated multiresistant Acinetobacter baumannii strains from different European hospitals. Res Microbiol 156, 348–355.[Medline]
Jain, R. & Danziger, L. H. (2004). Multidrug-resistant Acinetobacter infections: an emerging challenge to clinicians. Ann Pharmacother 38, 1449–1459.
Jiménez-Mejías, M. E., Pichardo-Guerrero, C., Márquez-Rivas, F. J., Martín-Lozano, D., Prados, T. & Pachón, J. (2002). Cerebrospinal fluid penetration and pharmacokinetic/pharmacodynamic parameters of intravenously administered colistin in a case of multidrug-resistant Acinetobacter baumannii meningitis. Eur J Clin Microbiol Infect Dis 21, 212–214.[CrossRef][Medline]
Jones, A. M., Govan, J. R., Doherty, C. J., Dodd, M. E., Isalska, B. J., Stanbridge, T. N. & Webb, A. K. (2001). Spread of a multiresistant strain of Pseudomonas aeruginosa in an adult cystic fibrosis clinic. Lancet 358, 557–558.[CrossRef][Medline]
Jones, R. N. (2003). Global epidemiology of antimicrobial resistance among community-acquired and nosocomial pathogens: a five-year summary from the SENTRY Antimicrobial Surveillance Program (1997–2001). Semin Respir Crit Care Med 24, 121–134.[CrossRef][Medline]
Jones, R. N., Deshpande, L., Fritsche, T. R. & Sader, H. S. (2004). Determination of epidemic clonality among multidrug-resistant strains of Acinetobacter spp. and Pseudomonas aeruginosa in the MYSTIC Programme (USA, 1999–2003). Diagn Microbiol Infect Dis 49, 211–216.[CrossRef][Medline]
Joshi, S. G., Litake, G. M., Niphadkar, K. B. & Ghole, V. S. (2003). Multidrug resistant Acinetobacter baumannii isolates from a teaching hospital. J Infect Chemother 9, 187–190.[Medline]
Jung, R., Fish, D. N., Obritsch, M. D. & MacLaren, R. (2004). Surveillance of multi-drug resistant Pseudomonas aeruginosa in an urban tertiary-care teaching hospital. J Hosp Infect 57, 105–111.[CrossRef][Medline]
Kocazeybek, B., Arabaci, U., Erenturk, S. & Akdur, H. (2002). Investigation of various antibiotic combinations using the E-Test method in multiresistant Pseudomonas aeruginosa strains. Chemotherapy 48, 31–35.[CrossRef][Medline]
Kuo, L. C., Yu, C. J., Lee, L. N., Wang, J. L., Wang, H. C., Hsueh, P. R. & Yang, P. C. (2003). Clinical features of pandrug-resistant Acinetobacter baumannii bacteremia at a university hospital in Taiwan. J Formos Med Assoc 102, 601–606.[Medline]
Kuo, L. C., Teng, L. J., Yu, C. J., Ho, S. W. & Hsueh, P. R. (2004). Dissemination of a clone of unusual phenotype of pandrug-resistant Acinetobacter baumannii at a university hospital in Taiwan. J Clin Microbiol 42, 1759–1763.
Landman, D., Quale, J. M., Mayorga, D., Adedeji, A., Vangala, K., Ravishankar, J., Flores, C. & Brooks, S. (2002). Citywide clonal outbreak of multiresistant Acinetobacter baumannii and Pseudomonas aeruginosa in Brooklyn, NY: the preantibiotic era has returned. Arch Intern Med 162, 1515–1520.
Lang, B. J., Aaron, S. D., Ferris, W., Hebert, P. C. & MacDonald, N. E. (2000). Multiple combination bactericidal antibiotic testing for patients with cystic fibrosis infected with multiresistant strains of Pseudomonas aeruginosa. Am J Respir Crit Care Med 162, 2241–2245.
Lee, C. M., Lim, H. K., Liu, C. P. & Tseng, H. K. (2005). Treatment of pan-drug resistant Acinetobacter baumannii. Scand J Infect Dis 37, 195–199.[CrossRef][Medline]
Levin, A. S., Gobara, S., Mendes, C. M., Cursino, M. R. & Sinto, S. (2001). Environmental contamination by multidrug-resistant Acinetobacter baumannii in an intensive care unit. Infect Control Hosp Epidemiol 22, 717–720.[CrossRef][Medline]
Lin, Y. W., Adachi, S., Watanabe, K., Umeda, K. & Nakahata, T. (2003). Serial granulocyte transfusions as a treatment for sepsis due to multidrug-resistant Pseudomonas aeruginosa in a neutropenic patient. J Clin Microbiol 41, 4892–4893.
Ling, M. L., Ang, A., Wee, M. & Wang, G. C. (2001). A nosocomial outbreak of multiresistant Acinetobacter baumannii originating from an intensive care unit. Infect Control Hosp Epidemiol 22, 48–49.[CrossRef][Medline]
Luzzaro, F., Mantengoli, E., Perilli, M., Lombardi, G., Orlandi, V., Orsatti, A., Amicosante, G., Rossolini, G. M. & Toniolo, A. (2001). Dynamics of a nosocomial outbreak of multidrug-resistant Pseudomonas aeruginosa producing the PER-1 extended-spectrum beta-lactamase. J Clin Microbiol 39, 1865–1870.
Maniatis, A. N., Pournaras, S., Orkopoulou, S., Tassios, P. T. & Legakis, N. J. (2003). Multiresistant Acinetobacter baumannii isolates in intensive care units in Greece. Clin Microbiol Infect 9, 547–553.[CrossRef][Medline]
Maragakis, L. L., Cosgrove, S. E., Song, X. & 7 other authors (2004). An outbreak of multidrug-resistant Acinetobacter baumannii associated with pulsatile lavage wound treatment. JAMA 292, 3006–3011.
Maslow, J. N., Glaze, T., Adams, P. & Lataillade, M. (2005). Concurrent outbreak of multidrug-resistant and susceptible subclones of Acinetobacter baumannii affecting different wards of a single hospital. Infect Control Hosp Epidemiol 26, 69–75.[CrossRef][Medline]
Michalopoulos, A., Kasiakou, S. K., Rosmarakis, E. S. & Falagas, M. E. (2005a). Cure of multidrug-resistant Acinetobacter baumannii bacteraemia with continuous intravenous infusion of colistin. Scand J Infect Dis 37, 142–145.[CrossRef][Medline]
Michalopoulos, A. S., Tsiodras, S., Rellos, K., Mentzelopoulos, S. & Falagas, M. E. (2005b). Colistin treatment in patients with ICU-acquired infections caused by multiresistant Gram-negative bacteria: the renaissance of an old antibiotic. Clin Microbiol Infect 11, 115–121.[CrossRef][Medline]
Mirakhur, A., Gallagher, M. J., Ledson, M. J., Hart, C. A. & Walshaw, M. J. (2003). Fosfomycin therapy for multiresistant Pseudomonas aeruginosa in cystic fibrosis. J Cyst Fibros 2, 19–24.[CrossRef][Medline]
Miranda, G., Leanos, B., Marquez, L., Valenzuela, A., Silva, J., Carrillo, B., Munoz, O. & Solorzano, F. (2001). Molecular epidemiology of a multiresistant Pseudomonas aeruginosa outbreak in a paediatric intensive care unit. Scand J Infect Dis 33, 738–743.[CrossRef][Medline]
Mussi, M. A., Limansky, A. S. & Viale, A. M. (2005). Acquisition of resistance to carbapenems in multidrug-resistant clinical strains of Acinetobacter baumannii: natural insertional inactivation of a gene encoding a member of a novel family of beta-barrel outer membrane proteins. Antimicrob Agents Chemother 49, 1432–1440.
Oh, J. Y., Kim, K. S., Jeong, Y. W., Cho, J. W., Park, J. C. & Lee, J. C. (2002). Epidemiological typing and prevalence of integrons in multiresistant Acinetobacter strains. APMIS 110, 247–252.[CrossRef][Medline]
Ohmagari, N., Hanna, H., Graviss, L. & 8 other authors (2005). Risk factors for infections with multidrug-resistant Pseudomonas aeruginosa in patients with cancer. Cancer 104, 205–212.[CrossRef][Medline]
Oie, S., Uematsu, T., Sawa, A., Mizuno, H., Tomita, M., Ishida, S., Okano, Y. & Kamiya, A. (2003). In vitro effects of combinations of antipseudomonal agents against seven strains of multidrug-resistant Pseudomonas aeruginosa. J Antimicrob Chemother 52, 911–914.
Ortega, B., Groeneveld, A. B. & Schultsz, C. (2004). Endemic multidrug-resistant Pseudomonas aeruginosa in critically ill patients. Infect Control Hosp Epidemiol 25, 825–831.[CrossRef][Medline]
Paavilainen, T., Alanen, M., Makela, M., Routamaa, M., Jarvinen, H., Huovinen, P. & Kotilainen, P. (2001). Infrequent isolation of multiresistant Acinetobacter baumannii from the staff tending a colonized patient with severe burns. Infect Control Hosp Epidemiol 22, 388–391.[CrossRef][Medline]
Pagani, L., Colinon, C., Migliavacca, R., Labonia, M., Docquier, J. D., Nucleo, E., Spalla, M., Li Bergoli, M. & Rossolini, G. M. (2005). Nosocomial outbreak caused by multidrug-resistant Pseudomonas aeruginosa producing IMP-13 metallo-beta-lactamase. J Clin Microbiol 43, 3824–3828.
Paramythiotou, E., Lucet, J. C., Timsit, J. F. & 7 other authors (2004). Acquisition of multidrug-resistant Pseudomonas aeruginosa in patients in intensive care units: role of antibiotics with antipseudomonal activity. Clin Infect Dis 38, 670–677.[CrossRef][Medline]
Pellegrino, F. L., Teixeira, L. M., Carvalho, Md. Mda. G. & 8 other authors (2002). Occurrence of a multidrug-resistant Pseudomonas aeruginosa clone in different hospitals in Rio de Janeiro, Brazil. J Clin Microbiol 40, 2420–2424.
Pimentel, J. D., Low, J., Styles, K., Harris, O. C., Hughes, A. & Athan, E. (2005). Control of an outbreak of multi-drug-resistant Acinetobacter baumannii in an intensive care unit and a surgical ward. J Hosp Infect 59, 249–253.[CrossRef][Medline]
Pirnay, J. P., De Vos, D., Cochez, C. & 7 other authors (2003). Molecular epidemiology of Pseudomonas aeruginosa colonization in a burn unit: persistence of a multidrug-resistant clone and a silver sulfadiazine-resistant clone. J Clin Microbiol 41, 1192–1202.
Pitten, F. A., Panzig, B., Schroder, G., Tietze, K. & Kramer, A. (2001). Transmission of a multiresistant Pseudomonas aeruginosa strain at a German University Hospital. J Hosp Infect 47, 125–130.[CrossRef][Medline]
Podnos, Y. D., Cinat, M. E., Wilson, S. E., Cooke, J., Gornick, W. & Thrupp, L. D. (2001). Eradication of multi-drug resistant Acinetobacter from an intensive care unit. Surg Infect (Larchmt) 2, 297–301.
Roberts, S. A., Findlay, R. & Lang, S. D. (2001). Investigation of an outbreak of multi-drug resistant Acinetobacter baumannii in an intensive care burns unit. J Hosp Infect 48, 228–232.[CrossRef][Medline]
Rossolini, G. M. & Mantengoli, E. (2005). Treatment and control of severe infections caused by multiresistant Pseudomonas aeruginosa. Clin Microbiol Infect 11, 17–32.
Ruiz, J., Navia, M. M., Casals, C., Sierra, J. M., Jimenez De Anta, M. T. & Vila, J. (2003). Integron-mediated antibiotic multiresistance in Acinetobacter baumannii clinical isolates from Spain. Clin Microbiol Infect 9, 907–911.[CrossRef][Medline]
Saugar, J. M., Alarcon, T., Lopez-Hernandez, S., Lopez-Brea, M., Andreu, D. & Rivas, L. (2002). Activities of polymyxin B and cecropin A-,melittin peptide CA(1-8)M(1-18) against a multiresistant strain of Acinetobacter baumannii. Antimicrob Agents Chemother 46, 875–878.
Schelenz, S. & French, G. (2000). An outbreak of multidrug-resistant Pseudomonas aeruginosa infection associated with contamination of bronchoscopes and an endoscope washer-disinfector. J Hosp Infect 46, 23–30.[CrossRef][Medline]
Shahid, M., Malik, A. & Sheeba (2003). Multidrug-resistant Pseudomonas aeruginosa strains harbouring R-plasmids and AmpC beta-lactamases isolated from hospitalised burn patients in a tertiary care hospital of North India. FEMS Microbiol Lett 228, 181–186.[CrossRef][Medline]
Sharma, R., Sharma, C. L. & Kapoor, B. (2005). Antibacterial resistance: current problems and possible solutions. Indian J Med Sci 59, 120–129.[Medline]
Simor, A. E., Lee, M., Vearncombe, M. & 7 other authors (2002). An outbreak due to multiresistant Acinetobacter baumannii in a burn unit: risk factors for acquisition and management. Infect Control Hosp Epidemiol 23, 261–267.[CrossRef][Medline]
Smolyakov, R., Borer, A., Riesenberg, K., Schlaeffer, F., Alkan, M., Porath, A., Rimar, D., Almog, Y. & Gilad, J. (2003). Nosocomial multi-drug resistant Acinetobacter baumannii bloodstream infection: risk factors and outcome with ampicillin-sulbactam treatment. J Hosp Infect 54, 32–38.[CrossRef][Medline]
Takeyama, K., Kunishima, Y., Matsukawa, M., Takahashi, S., Hirose, T., Kobayashi, N., Kobayashi, I. & Tsukamoto, T. (2002). Multidrug-resistant Pseudomonas aeruginosa isolated from the urine of patients with urinary tract infection. J Infect Chemother 8, 59–63.[Medline]
Tambic, A. A., Tambic, T., Kalenic, S. & Jankovic, V. (2002). Surveillance for antimicrobial resistance in Croatia. Emerg Infect Dis 8, 14–18.[Medline]
Tascini, C., Gemignani, G., Ferranti, S., Tagliaferri, E., Leonildi, A., Lucarini, A. & Menichetti, F. (2004). Microbiological activity and clinical efficacy of a colistin and rifampin combination in multidrug-resistant Pseudomonas aeruginosa infections. J Chemother 16, 282–287.[Medline]
Thong, K. L., Lai, K. S., Ganeswrie, R. & Puthucheary, S. D. (2004). Pulsed-field gel electrophoresis of multidrug-resistant and -sensitive strains of Pseudomonas aeruginosa from a Malaysian hospital. Jpn J Infect Dis 57, 206–209.[Medline]
Tognim, M. C., Andrade, S. S., Silbert, S., Gales, A. C., Jones, R. N. & Sader, H. S. (2004). 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. Int J Infect Dis 8, 284–291.[CrossRef][Medline]
Turton, J. F., Kaufmann, M. E., Warner, M., Coelho, J., Dijkshoorn, L., van der Reijden, T. & Pitt, T. L. (2004). A prevalent, multiresistant clone of Acinetobacter baumannii in Southeast England. J Hosp Infect 58, 170–179.[CrossRef][Medline]
Urban, C., Segal-Maurer, S. & Rahal, J. J. (2003). Considerations in control and treatment of nosocomial infections due to multidrug-resistant Acinetobacter baumannii. Clin Infect Dis 36, 1268–1274.[CrossRef][Medline]
van Dessel, H., Dijkshoorn, L., van der Reijden, T., Bakker, N., Paauw, A., van den Broek, P., Verhoef, J. & Brisse, S. (2004). Identification of a new geographically widespread multiresistant Acinetobacter baumannii clone from European hospitals. Res Microbiol 155, 105–112.[Medline]
Wang, S. H., Sheng, W. H., Chang, Y. Y. & 7 other authors (2003). Healthcare-associated outbreak due to pan-drug resistant Acinetobacter baumannii in a surgical intensive care unit. J Hosp Infect 53, 97–102.[CrossRef][Medline]
Wilson, S. J., Knipe, C. J., Zieger, M. J., Gabehart, K. M., Goodman, J. E., Volk, H. M. & Sood, R. (2004). Direct costs of multidrug-resistant Acinetobacter baumannii in the burn unit of a public teaching hospital. Am J Infect Control 32, 342–344.[CrossRef][Medline]
Wood, G. C., Hanes, S. D., Boucher, B. A., Croce, M. A. & Fabian, T. C. (2003). Tetracyclines for treating multidrug-resistant Acinetobacter baumannii ventilator-associated pneumonia. Intensive Care Med 29, 2072–2076.[CrossRef][Medline]
Wu, T. L., Ma, L., Chang, J. C., Su, L. H., Chu, C., Leu, H. S. & Siu, L. K. (2004). Variable resistance patterns of integron-associated multidrug-resistant Acinetobacter baumannii isolates in a surgical intensive care unit. Microb Drug Resist 10, 292–299.[CrossRef][Medline]
Yoon, J., Urban, C., Terzian, C., Mariano, N. & Rahal, J. J. (2004). In vitro double and triple synergistic activities of Polymyxin B, imipenem, and rifampin against multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother 48, 753–757.
Zeana, C., Larson, E., Sahni, J., Bayuga, S. J., Wu, F. & Della-Latta, P. (2003). The epidemiology of multidrug-resistant Acinetobacter baumannii: does the community represent a reservoir? Infect Control Hosp Epidemiol 24, 275–279.[CrossRef][Medline]
This article has been cited by other articles:
|
|
 |
|
  E. O'Fallon, A. Pop-Vicas, and E. D'Agata The Emerging Threat of Multidrug-Resistant Gram-Negative Organisms in Long-Term Care Facilities J Gerontol A Biol Sci Med Sci, January 27, 2009; (2009) gln020v2. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Kelesidis, D. E. Karageorgopoulos, I. Kelesidis, and M. E. Falagas Tigecycline for the treatment of multidrug-resistant Enterobacteriaceae: a systematic review of the evidence from microbiological and clinical studies J. Antimicrob. Chemother., November 1, 2008; 62(5): 895 - 904. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. G. Giske, D. L. Monnet, O. Cars, Y. Carmeli, and on behalf of ReAct-Action on Antibiotic Resistance Clinical and Economic Impact of Common Multidrug-Resistant Gram-Negative Bacilli Antimicrob. Agents Chemother., March 1, 2008; 52(3): 813 - 821. [Full Text] [PDF]
|
|
|
|
|
|
G. A. Pankuch, G. Lin, H. Seifert, and P. C. Appelbaum Activity of Meropenem with and without Ciprofloxacin and Colistin against Pseudomonas aeruginosa and Acinetobacter baumannii Antimicrob. Agents Chemother., January 1, 2008; 52(1): 333 - 336. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. R. W. Govan Multidrug-resistant pulmonary infection in cystic fibrosis - what does 'resistant' mean? J. Med. Microbiol., December 1, 2006; 55(Pt 12): 1615 - 1617. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| INT J SYST EVOL MICROBIOL | J MED MICROBIOL | MICROBIOLOGY | J GEN VIROL | ALL SGM JOURNALS |
